Advances in Parasit Ology

8/19/2019 Advances in Parasit Ology

http://slidepdf.com/reader/full/advances-in-parasit-ology 1/321



Editor ia l oard

M. Colu zzi, Director, Istituto de P arassitologia, Universit~t Degli Studi di

Ro m a La S apienza , P. le A. Moro 5, 00185 Ro ma, Italy

C. C om be s, Laboratoire de Biologie Anim ale, Universit6 de Perpignan , Centre

d~ Biologie et d Eco log ie Tropicale et M 6diterran6enne, Avenue de

Villeneuve, 66860 P erpignan Cedex, France

D.D. Despommier, Divis ion of Tropical Medicine and Environmental

Sciences, D epartmen t of Microbiology, Columb ia University, 630 W est

168th Street, N ew York, NY 10032, US A

J.J. Shaw , Instituto de Ci~ncias Biom6dicas, Universidade de S~o Paulo,

av. Pro f Lineu Prestes 1374, 05508-900, Cidade U niversit~ ia, S ao Paulo,

SP, Brazil

K. Tan abe , Laboratory of Biology, Osaka Institute of Technology, 5-16-1

Oh miy a Asahi-Ku, Osaka, 535, Japan

P. W enk , Falkenweg 69, D-72076 Ttibingen, Germany



CONTRIBUTORS TO VOLUM E 5

C. M. ADEMA Department o f Biology, University of New Mexico , 167A

Castetter Hall, Albuquerque, NM 87131-1091, USA

D. W. DUNr rE Department o f Pathology, University o f Cambridge, Tennis

Court Road, Cambridge CB2 1QP, UK

K. E

HOFFMANN

Department of Pathology, University of Cambridge,

Tennis Court Road, Cambridge CB2 1QP, UK

E HORAK Department o f Parasitology, Charles University, Vini(nd 7, CZ-

12844 Prague 2, Czech Republic

L. KOLA~OVA Department o f Tropical Medicine, 3rd Clinic o f lnfectious

and Tropical Diseases, Faculty Hospital Bulovka, Charles University,

CZ-12800 Prague 2 and Institute fo r Postgraduate Medical Education,

Rusk6 85, CZ-IO005 Prague 10, Czech Republic

K. MARSH Centre fo r Tropical Medicine, University o f Oxford, John

Radcliffe Hospital, Headington, Oxford OX3 9DU, UK and Centre fo r

Geographic Medicine, Kenya M edical Research Institute, PO Box 230,

Kilifi, Kenya

R. W. SNOW Cen tre fo r Tropical Medicine, University o f Oxford, John

Radcliffe Hospital, Headington, Oxford OX3 9DU, UK and the Wellcome

Trust~Kenya Medical Research Institute Collaborative Programme, P. 0.

Box 43640, Nairobi, Kenya

J. D. THOMASSchool o f Biological Sciences, University o f Sussex, Falmer,

Brighton, Eas t Sussex BN1 9Q G, UK

T. A. WYNN Laboratory of Parasitic Diseases, Immunobiology Section,

Schistosomiasis Immunology and Pathology Unit, 50 Sou th Drive,

Room 6154, MSC 8003, Bethesda, MD 20892, USA



PREF CE

It is rare for one parasitologist to have the opportunity to continue investiga-

t ions over half a century. Don Thom as Universi ty of Sussex, UK ) has had the

insight to realize how im portant this kind o f observation can be and has con-

tributed a fascinating cha pter concerning the eco log y of helminth parasites and

their fish hosts. H e first carried out eco logica l studies involving salmo nid fish

in Welsh rivers in the early nineteen fifties, his interest being their feeding

behaviour, helminth parasites and intermediate hosts. An opportunity to follow

up these studies in 1998 made i t possible to ascertain how changing environ-

menta l condi t ions might have impacted on the sa lmonid hosts and thei r

parasites. Do n uses this study as a back drop to delve into many im portant ques-

t ions concerning interactions betw een populations o f helminth parasites, their

hosts and their environment. There is much to st imulate the reader here

together with ideas for future research.

Almost twenty years have passed since the last detailed review on avian

schistosom es within the genus

richobilharzia

by Blair and Islam 1983). So

what has been happening in the interim? In a comprehensive chapter Petr

Hor~ik, Libuge Kol~i~ov~ Charles Universi ty, Czech Republic) and Coen

Ade ma Universi ty of New M exico, US A) br ing together a weal th of new

informat ion concerning recognized

richobilharzia

species, their biology,

interactions with their hosts and the pathology associated with infection.

Part icular at tention is given to problems concerning the systematics of the

genus and to morphological and m olecular methods available for species char-

acterization. Due to the non-specific penetration of the cercariae through the

skin, contact with water bodies containing infected snails and cercariae can

lead to cercarial dermatitis in m an. C ercarial derm atitis is a com m on condition,

which with few exceptions occurs globally. O f perhaps greater concern is that

developing schistosomula have now been reported from various organs and

nervous t issue of mammals, which may lead to further complications. The

chapter ends by con sidering the epidem iolog y of cercarial dermatitis including

the identification of potential transmission sites and possib le control measures.

In the third chapter, B ob Sn ow and K evin Marsh, from the K enya Medical

Research Insti tute, discuss the com plicated relationships be twe en intensity of

malarial transmission, which can range from fewer than one infective mos-

quito bite per year to several thousand such bites, and the burden o f mortali ty

and morbidity. At the lower end of the range, al l age groups are at r isk of



v i i i P R E F C E

developing severe malaria w ith, mainly, cerebral involvement, wh ereas at the

higher end i t is predominantly infants w ho are at r isk of severe disease, and

malarial anaemia rather than cerebral malaria dominates the clinical picture.

This of course reflects the increasingly rapid development of immunity as

transmission intensity increases. The authors conclude that it is in areas of

mo derate to high transmission that interventions such as the use o f insecticide-

treated bed nets ITNs) w ill have the greatest effect in reducing disease and

mortality. In areas o f high transm ission intensity, the data sug gest that malar-

ial and all-cause mortality appear to saturate, although the authors agree that

this is contentious. If this is so, initial reductio ns in m ortality m ay be difficult

to sustain as even the reduced mortali ty rate may l ie within the saturated

region of the curve. Ho wever, the overall benefi ts of using ITN s in reducing

the disease burden regardless of transmission intensity and in producing even

limited reduction o f infant mortali ty rates em phasize that their use sho uld be

encourag ed in al l areas of Africa w here m alaria is endemic.

Most helminth infections induce immune responses characterized by pro-

duction o f Th-associated cytokin es and antibodies. These h ave usually taken to

be host-protective, with a highly regulated and controlled host inflamm atory

response directed against parasite antigens and leading to a chronic infection

with mild symptoms. The f inal review by Kar l Hoffmann and D avid Dunne o f

the Department o f Pathology of the Universi ty of Cambridge U K, and Thomas

Wynne of the Immunology Section, The National Insti tutes of Health USA,

using schis tosomiasis as a model demonstra tes tha t , whi le most chronic

induced type-2 associated med iated responses are held in check b y regulated

control mechanisms, prolonged cytokine biases can be not only undesirable

but, in fact, lethal. Uncontrolled polarized type-1 immune responses can also

lead to a serious increase in host imm uno-pathology.

John Baker

Ralph M uller

David Roll inson



The Ecology of Fish Parasites wit h Particular

Reference to Helminth Parasites and their

Salmonid Fish Hosts in Welsh Rivers:

A Review of Some of the Central Questions

J . D . T h o m a s

School of Biological Sciences University o f Sussex Falmer

Brighton East Sussex BN1 9Q G UK

A b s tr a ct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

1. I n t r o d u c ti o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

2. E c o lo g ic a l B a c k g r o u n d . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

2.1. T o p o g r a p h y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

2 .2 . P h y s i c o c h e m i c a l c h a r a c t e ri s t ic s o f s t u d y s i te s . . . . . . . . . . . . . . . . . . . . . . . 8

2 .3 . M e t h o d s u s e d f o r in v e s t i g a t i n g t h e h e l m i n t h p a r a s i t e s a n d th e i r

f is h h o s ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

2 .4 . M e t h o d s u s e d f o r in v e s t i g a t i n g t h e i n v e r t e b r a t e f a u n a i n c l u d i n g

i n t e r m e d ia t e h o s t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

2.5 . S p e c ie s o f h e l m i n t h p a r as i te s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

2 .6 . T h e l if e h i s t o r y s t r a t e g i e s o f t h e p a r a s i t e s . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 2

3 . D i s p e r s i o n P a t t er n s o f t h e H e l m i n t h P a r a s it e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 9

4. S p a t i o t e m p o r a l A s p e c t s o f t h e P a ra s it ic F a u na . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2

4 .1 . Q u a n t i t a t iv e d a ta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2

4 .2 . P h y s i c o c h e m i c a l f a c t o r s t h a t m a y i n f l u e n c e t h e d i s t r ib u t i o n a n d

a b u n d a n c e o f t h e p a r as i te s a n d t h e i r f is h h o s t s . . . . . . . . . . . . . . . . . . . . . . 3 2

4.2.1 W a t e r f l o w s a n d w a t e r t y p e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2

4 .2 .2 . W a t e r t e m p e r a t u r e a n d p h o t o p e r i o d . . . . . . . . . . . . . . . . . . . . . . . . . . 3 5

4 .2 .3 . W a t e r c h e m i s t r y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3

5 . T h e R e l a t i o n s h i p s b e t w e e n P a r a s it e A b u n d a n c e a n d t h e A g e a n d S iz e o f

t h e F is h H o s ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 5

5 .1 . Q u a n t i ta t i v e d a ta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 5

5 .2. C a u s a t iv e m e c h a n i s m s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 0

5 .3 . E c o lo g ic a l r e l e va n c e a n d d e n s i t y d e p e n d e n c e . . . . . . . . . . . . . . . . . . . . . . . 5 4

6 . R e l a t i o n s h i p s b e t w e e n P a r a si t e A b u n d a n c e a n d t h e W e l l b e i n g o f t h e

F is h H o s ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 9

6 .1 . I n t r o d u c ti o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 9

6 .2 . P a t h o l o g y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 9

A D V A N C E S I N P A R A S I T O L O G Y V O L 5 2 Copyright © 2002 Elsevier Science Ltd

0 0 6 5 - 3 0 8 X

ll rights of reproduction in any form reserved



2 J . D . T H O M A S

6 4

6.5.

6.6.

7 . Sex

7.1.

7.2.

6 .3 . S ta t i s t ica l a n a l ys e s o f t h e re l a t i o n sh i p s b e tw e e n p a ra s i te

a b u n d a n c e a n d t h e c o n d i t io n f a c t o r a n d a d i p o s e i n d e x . . . . . . . . . . . . . . 61

R e a s o n s f o r t h e a b s e n c e o f h a r m f u l e f f e c ts d u e t o p a r a s i t e s . . . . . . . . . . 7 0

R e a s o n s f o r s o m e p a r a si t es c a u s in g d e t r im e n t a l e f fe c t s . . . . . . . . . . . . . . 7 0

C o n c lu s io n s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 3

B ia s in P a r as i ti s m a n d C a u s a t iv e M e c h a n i s m s . . . . . . . . . . . . . . . . . . . . . . . 7 4

I n tr o du c t io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 4

A n e v a l u a t i o n o f t h e H a m i l t o n - Z u k a n d i m m u n o c o m p e t e n c e

h y p o th e s e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 5

7 .3 . C o n c l u s i on s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 9

8 . T h e H e l m i n t h F a u n a o f T r o u t a n d S a l m o n P a rr : C o m p a r a t i v e

A s p ec t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 2

9 . C h a n g e s in th e H e l m i n th Fa u n a a n d th e i r H o s ts b e tw e e n 1 9 50 a n d 1 9 98 :

C a u s a t iv e M e c h a n i s m s a n d P o l lu t i on B i o i n di c a t o rs . . . . . . . . . . . . . . . . . . . . . . 9 6

9 .1 . C o m p a r i s o n o f p r e v a l e n c e a b u n d a n c e a n d d i v e r s i t y o f h e l m i n t h

p a r a si te s in 1 95 0 a n d 1 99 8 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 6

9 .2 . R e a so n s fo r t h e d e c l i n e i n p a ra s i t i c f a u n a b e tw e e n 1 9 50 a n d 19 9 8 . . . . . 9 7

9 .3 . E l u c i d a t io n o f e n v i r o n m e n t a l fa c t o r s t h a t m a y h a v e ca u s e d t h e

d e c li n e in t h e i n t e r m e d ia t e h o s ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 03

9 .4 . H e l m i n t h p a r a s i t e s a n d o t h e r a q u a ti c o r g a n i s m s a s p o l l u t i o n

b i o in d i c a t o rs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 13

9 .5 . F is h p a r a s i t e s a s s o u r c e s o f i n f o r m a t i o n o n p o l l u t i o n . . . . . . . . . . . . . . . . 1 17

1 0. I n t e r a c t io n s b e t w e e n S p e c i e s o f H e l m i n t h P a r a s it e s i n F is h . . . . . . . . . . . . . . . . 1 18

1 0.1 . I n t r od u c t i on . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 18

1 0.2 . E v i d e n c e o f i n t e r s p e c ie s c o m p e t i t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 19

1 0.3 . M e c h a n i s m s o f c o m p e t i t i v e i n t er a c t io n s . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 29

1 0.4 . M e c h a n i s m s w h i c h r e d u c e t h e s e v e r i t y o f e x p l o i t a t i v e c o m p e t i t i o n . . . . 1 30

1 0.5 . E v o l u t i o n a r y a s p e c t s o f i n t e r s p e c i e s c o m p e t i t i o n . . . . . . . . . . . . . . . . . . . 1 32

A c k n o w l e d g e m e n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 34

R e fe r en c es . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 34

BSTR CT

Ecological studies carried out in Welsh r ivers on the feeding behaviour of

salm onid fish their helminth p arasites and intermediate hos ts in the early 1950s

and in 1998 have been us ed as a basis to review the literature dealing with the fol-

lowing questions. First how are the helminth popu lations dispersed in

spac e-tim e? Seco nd to what extent are the distributional patterns and the life

history strategies o f the parasites influenced b y physico chem ical factors? Third

to w hat extent are populations o f helmith parasites in salmon id fish influenced by

host characteristics including the genom e sex age size social position and

feeding behaviou r? Fourth are the populations o f parasites regulated in a density-

depende nt manner? Fifth do the parasites influence the survival and wellbeing

of their salmonid hosts and the evolution of sex? Sixth to what extent is the par-

asite community influenced by environmental changes including those of an

anthropogenic nature and can the parasites be us ed as bioindica tors o f pollu tion?



ECOLOGY OF FISH PARASITES

As with most parasites the helminth species found were highly overdis-

persed thus making i t necessary to undertake a log10 (1 + x) conversion for

statistical analyses. Statistical analyses confirm that the genome, age and sex

of salm onid fish hosts, the station and seaso nal change in radiation levels we re

significant factors in predicting the number of parasites. The evidence given

supports the hypothesis that the feeding behaviour and habitat selection by the

host fish, their position in the social hierarchy and the overdispe rsed nature of

the transmission sites are the key factors in causing differences in the parasitic

fauna related to host species, age, size and sex. Differences in the helminth par-

asite com mu nity related to station can be explained on the basis of differences

in water types, sediments and chem istry. Altho ugh the evidence presented is in

accord with the consensus view that temperature is correlated with seasonal

changes in the abundance of many species of helminth parasites, i t is argued

that it m ay no t be the direct causative m echanism . It is postulated that the life

history strategy that results in a decline in abundance of the more vulnerable

adult parasites in the gut of the salmonid hosts during the sum me r has arisen

as a result of evolutionary pressures. At this time, the gut environment is par-

t icularly inhospitable be cause o f the temperature-related enh ancem ent of the

host s im mu ne mechan ism and the increased gut turnover rate. In contrast, the

larval stages in the imm unologically and m etabolically more benign interme-

diate host would be under less intensive selective pressures. I t is postulated

therefore that evolutionary pressures have caused the parasites to leave the

definitive host and concentrate their reproductive efforts in the intermediate

hosts during the wa rmer m onths.

Eviden ce is given in support o f the hypothesis that the parasite po pulations

are regulated in a density-dependent manner and that the regulatory mecha-

nisms ma y involve the host s im mu ne mech anisms and in t raspecies

competi t ion and interspecies competi t ion of an exploitat ive or interference

nature. Quantitative studies using K factor analysis and bioch em ical research

to elucidate the nature o f the interference m echanisms are required to test this

hypothesis. The absence of age-related resistance indicates an old and stable

relationship in which the immunosuppressive and immunoavoidance mecha-

nism s o f the parasites and h osts, respectively, are in balance. T his indicates that

the introduction of novel parasites or new genetic strains of host f ish could

result in harmful epidemics.

Despite causing t issue damage, there was no evidence o f parasite-induced

mortality among the salmonids in the Teifi.This finding is in accord with the

generally accepted view that most freshwaters are not troubled by parasite

problems, although parasites are present in abundance. In fact, parasite abun-

dance in the sa lmonid f ish in theTeif i was posi t ive ly corre la ted wi th the

condition factor and the adipose index. Two testable hypo theses wer e advanced

to explain these observations. First , the m ore dom inant well-condit ioned fish

in the hierarchy are more l ikely to acquire parasites bec ause they ingest mo re



4 J D THOMAS

food i tems and spend more t ime in sheltered habitats with deposit ing sedi-

ments where transmission mainly occurs. Second, the parasites may release

factors that st imulate the host s imm une and endocrinological system s to pro-

duc e factors that enhan ce som atic grow th and inhibit reproduc tion o f the host.

This benign re la t ionship is considered to be indica t ive of long- term

coevolution.

The sex of the f ish had a sigif icant influence on the abundance of the para-

sites in total and also on particular species with the bias in all cases being in

favou r of the fem ale fish. This review show s that sex bias in parasitism is gen-

erally not strong and that m ale bias in parasitism is not a general rule. Taken as

a whole , the resul ts fa i l to suppor t most of the predic t ions based on the

Ha milto n-Zu k and the immun ocomp etence hypotheses. Possible hypotheses to

explain wh y parasitism tends to be higher in female than in male trout include

testosterone immunosuppression, cort icosteroid-based immune suppression

and differences between the size and behaviour of the sexes. However, the

latter two hypotheses have more credence, al though testosterone levels are

higher in female than male trout.

Betw een the early 1950s and 1998 there has been a m arked decline in the

prevalence, abundance and diversity of the helminth parasite com mun ities in

salmonid fish as well as their intermediate hosts. Possible reasons for these

declines include heavy metal pollution, increased acidity and habitat degrada-

t ion l inked to changes in land use. I t is concluded that al though helminth

parasites can provide supplem entary information on pollution, the use of biotic

indices based on the Biological monitoring working party (BMWP) or River

invertebrate prediction and classif ication system (RIVPACS) methods are

preferable. However, as these methods were designed to m easure the impact of

organic pollution they lack the sensitivity for measuring metal pollution. It is

advocated therefore that new biomonitoring methods should be developed to

measu re the impact o f heavy m etal pollution using biotic indices based on the

sampling of the susceptible invertebrate communities inhabit ing deposit ing

sedim ents in the transmission sites of helminth parasites.

1 I NTRODUCTI ON

Earlier studies of f ish parasites w ere o f necessity mainly conc erned with tax-

onom y, geogra phical distribution, host specificity and parasites life cycles.

These pioneering studies raised many questions regarding the nature of the

interactions between the parasites, the host and their environment and the

mecha nisms resp onsible for causing the observed patterns. Som e of the most

important o f these, which are sum marised in Figure 1, are as follows. First ,

how are the parasite species distr ibuted spatiotemporally. Second, to what



E CO LOG Y OF F I S H P A RA S ITE S

PHYSICO-CHEMICAL ACTO RS COM MUN ITY EVEL

FEED ORWARD

RESOURC

NUTR/EN~

HIGHLYPREDICTABLE q l ~ L ATHOGEN

DIURNAL,LUNARAND SOURCEOI

SEASONALCHANGES N

PHOTOPERIOD. --RESISTAN(

LESSPREDICTABLE -------IMMUNIT

TEMPERARURE, RESOURC

RAINFALL

N UT R I N ~

WATERCHEMISTRY

FLOWVELOCITY

CONSUMERSPECIES

PREDATOR.MACRO-PARASITESR MICRO-

PARASITES

INDIVIDUALOR POPULATION LEVEL

rlo~N cor,r R o ~ P A R A S I T E

I REPRODUCTION

t

GROWTH

Figure 1

Eco logical factors that may influen ce the distribution and abunda nce of

helminth pa rasites and their hosts.

ex ten t a re pa ras it e pop u la t ions in f luenced by phys icochem ica l f ac to r s inc lud ing

those that vary seaso nal ly in a predic table w ay ? Third , i s there any e videnc e that

the l i f e h i s to ry s t ra teg ies o f the pa ras i t e s have evo lv ed to r espond to p red ic t ive

o r f eed fo rwa rd s igna ls? Four th , to wha t ex ten t a re pa rasi t e popu la t ions in f lu -

enced by the genome, s ex , age , l eng th , we igh t , soc ia l pos i t ion and f eed ing

beh av iou r o f the hos t? F i fth , i s the re any ev idence tha t the pa ras it e pop u la t ions

a re r egu la ted in a dens i ty -dependen t man ner b y com pet i t ion fo r r e sources , p re -

da t ion , pa ras i t ism and the ho s t s d e fens ive mec han ism s? S ix th , i s the re any

ev iden ce tha t the pa ras it e s in f luence the hea l th and su rv iva l o f the hos t s, d r ive

the ir popu la t ion cyc les (F ree land , 1976 ; Ander son and M ay , 1979; D ob son and

Hud son , 1992), de te rmine hos t gene t ic s t ruc tu re (Sh yko f and Schm id t -Hempel ,

1991) and f avour the evo lu t ion o f s ex (Hami l ton , 1980 ; Hami l ton and Zuk ,

1982; Fols tad and Kar ter, 1992)? Seventh , to w hat ex tent m ay the helm inth

c o m m u n i t y b e i n f l u e n c e d b y e n v i r o n m e n t a l c h a n g e s , i n c l u d i n g t h o s e o f a n

an th ropogen ic na tu re , and a re they su i t ab le b io ind ica to r s o f po l lu t ion?

Som e o f these ques t ions w ere addres sed du r ing an ea r l i e r inves t iga t ion ca r -

r i ed ou t on the t rou t ,

Salmo trutta

L. ) and the s a lmon pa r r

Salmo salar

L.) a t

th ree s t a t ions on tw o r ive r sys tem s in Wes t W ales in the ea r ly 1950s (Thom as ,

1956 , 1957 , 1958a ,b , 1962 , 1964a ,b , c ) . Th e fo l lowing deve lo pm en ts have

m ade i t poss ib le to re-exam ine the se ques t ions . F irst ly , new, mo re pow erfu l s ta-

t i s t i c a l s o f t w a r e h a s m a d e i t p o s s i b l e t o r e a n a l y s e q u a n t i t a t i v e d a t a m o r e

r igo rous ly . Seco nd ly , re sea rch b y f i sh pa ras i to log i s t s ca r r i ed ou t subse quen t ly

h a s m a d e f u r t h e r v a l u a b l e c o n t ri b u t io n s t o o u r k n o w l e d g e a n d u n d e r s t an d i n g

thus m ak ing i t pos s ib le to r e in te rp re t the da ta . Th i rd ly , tw o o f the r ive rs s tud -

i e d , n a m e l y t h e T e i f i a n d t h e P y s g o t w r , h a v e u n d e r g o n e m a n y d e t r i m e n t a l

c h a n g e s a s a r e s u l t o f i n c r e a s e d l e v e l s o f a b s t r a c t i o n a n d a c i d d e p o s i t i o n ,

cana l i s a t ion and ch anges in l and use s ince the 1950s . An oppo r tun i ty to r ev i s i t



6 J D THOMAS

these sites in 1998 made it possible to ascertain how changing environmental

conditions might have impacted on the salmonid hosts and their parasites. In

this review, the necessary back ground will be included to m ake i t possible to

address fully the questions outl ined above.

2 ECOLOGICAL BACKGROU ND

2 1 Topog r aphy

The area studied Figure 2) is geologically very uniform, consist ing mainly of

sedimentary Silurian gri ts and shales, except where anticl inal folding and

faulting brings out Ordovician strata in the eastern region. The region as a

wh ole is traversed b y the Teifi and Towy anticlines. Weathering has resulted in

an area that is predom inantly bleak, high m oorland with a capping o f poor,

calcium-deficient soil. As a result, except in the valleys, land is poorly devel-

oped, supporting only a sparse population. Both rivers under consideration

have their sourc es at high altitudes in peat bogs o r lakes in upland mo ors char-

acterised by rough, yellow m ountain pasture in dry places and

Sphagnum

in the

wetter regions.

The Teifi has its source in Llyn Tefi, one of six upland lakes at an altitude

of 455 m OD on the southern edge of the Plynlimmon plateau in the western

region of the Cambrian Mountains. I t is approximately 117.5 km long with a

catchment of app roximately 1007 km 2. After being joined by over 70 tr ibutar-

ies it flow s into Cardigan Bay. In its first 7 km the channel falls 215 m b ut for

the next 15 km, as it passes through the Tregaron Bog Cors Goc h Glan Teifi),

the channel gradient is negligible. In this raised bog the river wanders slug-

gishly through a vast quagmire with a substratum consist ing mainly of f ine

gravel and silt. Whe n n ot in flood the wa ter flow is barely detectable and it con-

sists of a long series of deep stagnant pools connected by short s tretches of

shallow water. At the southwest end the r iver swells into broad and muddy

shallows. Along the r iver banks the vegetation forms a well-defined river ter-

race, the most abundant plants being

Juncus effusus Phalaris arundacea

Desch am pia caespitosa Carex acuta Galium palustre Ran uncu lus acris

and

Equisitum

species God win and Conw ay, 1939). Subm ersed vegetation is also

abundant.

Nuph ar lutea

grows by the edges o f deep pools whi le

Potomogeton

natans Myriophyllum Ranunculus penicillatus

Dumart) var.

penicillatus

and

Callitriche obtusangula

thrive in the shallows.

Glyceriafluitans

grows patchily

on the margins. According to Broo ker 1984) Apiu m inundatum L uronium

natans

and

Nup har lutea are

restricted to the Tregaron Bog . Stations 1 and 2

for the faunistic studies and S tation A fo r the fish collection are located on the

southern end of the bog Figure 2).



E CO LOG Y OF F I SH P A RA S ITE S

Figure 2

Map showing the river systems investigated. The grid references and site

landmarks for Stations 1-8 on the Teifi where the invertebrate samples, including interme-

diate hosts, were collected are as follows: 1) SN 6750 6186; Tregaron Bog; shallows 1.5 km

N of Pont Eynon. 2) SN 6727 6148; 200 m north of Pont Eynon. 3) SN 6638 5775;

below Tyndomen. 4) SN 6645 5717; near mouth of River Caftan. 5) SN 6528 5691; near

Pontllanio Bridge. 6) SN 6489 5685; at bend below Pontllanio Bridge. 7) SN 6468 5636;

near Old Mill, Llanio Isaf. 8) SN 6423 5440; at bend below Pontgoyan Bridge. Fish sam-

ples used to collect belminth parasites were obtained from station A in the Tregaron Bog

area which encompasses Stations 1-2 above and also from Station B located below the bog

area which encompasses Stations 3-7 above. Station D is located on the Pysgotwr, a tribu-

tary of the River Towy.

Downs tream of the bog the gradient is relatively constant falling at a rate of

about 150 m in 100 km. The river, now swollen to a width of 20-30 m by

numerous tributaries, meanders through farmland dominated by sheep and

dairy farming, forming a succession of pools, fifties, fast reaches and back-

waters. The substratum consists of cobbles, pebbles, coarse gravel and silt

depending on the water type. Submersed macrophytes consist mainly of ubiq-

uitous Ran unculus penici l latus Potomogeton natans M yriophyl lum sp.,

Callitriche hamulata and C. stagnalis on gravel beds and Fontinalis

antipyretica on stony substrate. Over the last 50 years both the submersed

macrophytes and riparian trees, such as the alder and willows, have become



8 J D THOMAS

less abundant. As a result the main river and particularly some of the tributar-

ies, which have been subjected to canalisation, have become more erosive in

character. Stations 3-8 for the faunistic studies are located in the upper region

of the Teifi between Tyndomen and Pont Goyan. Salmonid fish were collected

at Station B Stations 3-7 in faunistic study).

The Pysgotwr, one of the small headwaters of the River Towy Figure 2), is

situated at an altitude of 430 m on impermeable mudstones and shales of the

Silurian series Station D). During the 1950s its catchment, which consisted of

peat bogs and rough, virtually treeless mountain pasture, was used for sheep

farming. At that time the characteristic bankside species were

Drosera rotun-

di fo l ia Mo lin ia caerula

and

Juncus squarrosus .

Often the smaller feeder

streams were almost completely shaded by the latter species. As a result of the

steep gradient the small 1-4.5 m wide stream had many small waterfalls with

scour pools followed by fast reaches and riffles. The substrate was strongly

erosive in character, consisting mainly of small boulders, cobbles and coarse

gravel usually colonised by epilithic algae and

Fontinalis antipyretica.

Since then, however, virtually the entire catchment has been planted with

coniferous woodland.

2 2

Phys i co chem i ca l ha r ac t e ri s t ic s o f S t ud y S i te s

As the Teifi and Towy catchments are located in one of the wet areas of the

British Isles, with a mean annual rainfall of 1430 mm, the rivers exhibit spate

characteristics. Thus, the average flow, the maximum instantaneous flow and

the minimum dally mean flows for the Teifi are 28.38,448.80 and 0.73 cumecs,

respectively. Following changes in land use including land drainage, increased

erosion due to a doubling of the sheep population since 1950, and canalisation

of parts of the main river and some of the feeder streams, the river has become

more susceptible to spates and consequently more erosive in character.

As might be expected from the geology the waters from the upper reaches

of the Teifi and the Tywi have low conductivities, low base contents with Na +

> Ca2+), low alkalinities and low micronutrient content Table 1). It is of inter-

est that the Teifi retains its dystrophic, mountain stream characteristics

throughout its length. In the 1980 National Water Quality Survey most of the

river was classified as 1A except for some sections of the tributaries and the

main river upstream of Tregaron. These were placed in Grade 2 because of ele-

vated concentrations of zinc, originating in disused mine-workings in the upper

catchment Brooker, 1984). It is of interest that measurable concentrations of

zinc and lead were found in the water columns below Tregaron during the

present investigation Table 1).



E C O L O G Y O F F IS H P A R A S I T E S 9

_ =

~ g ~ ~ ~ •

~

~ ~ m o o o ~ ~ o ~ ~ o

~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ V ~ ~ ~ ~ ~ ~

~ ~ ~ ~ V ~ ~

~ ~ ~ ~ ~ 1 ~

~ o o ~ ~

• ~

~

I ~ I ~ ~ ~

~ ~ ~ ~

II

o _ ~



10 J D THOMA S

2 3

Me t h o d s U s e d o r In v e s t i g a t in g t h e H el m i n t h P a r a s i t e s a n d

t h e i r i s h H o s t s

Table 2 shows the nu mb er o f sa lmon id f ish and ee ls col lec ted a t the three s ta-

t ions for the invest iga t ion of he lminth paras i tes and feeding beh aviour as w el l

as the dates of col lec t ion . These f ish were captured by angl ing dur ing the ear-

l i e r inves t iga t ion and by e lec t ro f i sh ing in 1998 . Af te r g iv ing each f i sh a

reference number the fo l lowing information was recorded on cards: the date

and locat ion o f capture , species of f ish , weight in grams, the absolute length in

cent imetres , sex and age of the f ish ( fo l lowing sca le examinat ion a t a la ter

date) . The n umb ers o f each helminth paras i te species foun d on the skin , gi l ls ,

cardiac region of s tom ach, pylor ic region of s tomach, pylor ic caecae , pylor ic

caecae region of in tes tine , post-pylor ic region of in tes tine , rec tum and c loacal

region of each f ish were counted . The adipose index, which rang ed f rom 0 to

3 , g ives a meas ure of the am oun t of fa t deposi ted in the region o f the pylor ic

caecae and the s tomach region and was assessed v isual ly. Identi f ica t ion of par-

as i tes was carr ied out as far as poss ib le us ing l iv ing mater ia l but a l l the

individual paras i tes w ere a lso f ixed pr ior to fu ture examinat ion . In the case of

the t rematod es th is involved f ix ing a la rge representa t ive sample in G ilson s

f lu id under s l ight pressure f ro m a cove r g lass and then s ta in ing in toto prepa-

ra t ions in Coeles t ine Blue B and M ayer s paracarmine . T ransverse and sagi t ta l

ser ia l sec t ions were s ta ined in Ehrl ich s haem atoxy l in and eosin . These pro-

cedures made i t poss ib le to demons t ra te the coex is tence o f two sympa t r ic

species, Crepidostomum metoecus and C.far ion i s in the a l imentary canals of

the same f i sh spec ies (Thomas , 1957 ; 1958b) . When obse rv ing l iv ing

Crepidostomum i t was no ted tha t som e individuals , whic h turned out to be C.

metoecus were m ore e longa ted and mobi le than C. farion is. This observat ion

and the tende ncy of the two species to be segregated in the a l imenta ry canal

facili tated identification (Thom as, 1958b). Similar me thods w ere used fo r iden-

tifyin g the other Plat yhe lm inth es species (Tho ma s, 1956; 1958a; 1964a, b, c) .

Table 2

The number of fish examined and periods of investigation

Habitat No. fish examined Period of investigation

Trout Salmon parr Eels

Teifi Station A 215 15 88

Teifi Station A

Teifi Station B 685 274 155

Teifi Station B 16 2

Pysgotwr Station D 273

Mar-Jun 1951

Sep-Nov 1951

Jan-Dec 1951

Jun 1998

Jun-Aug 1951

Jan-Feb 1952




Nematodes and Acanthocephala were examined as described in Mahoney

(1966). All the helminth parasites were fixed in Gilson's fluid and stored in

formol-alcohol (Mahoney, 1966). The results are expressed in terms of per-

centage prevalence ( fish infected), mean abundance or mean intensities

(Bush

et al.

1997). The community structure of the helminth parasites was

quantified at the component and infra-population levels using the

Berger-Parker index, the Simpson diversity index, the Shannon-Wiener index

and Brillouin's index (Magurran, 1988; Bush

et al .

1997).

The weight and length was recorded for each fish, thus making it possible to

calculate the condition factor (Thomas, 1964c). The stomachs of all the host fish

were also examined for food items. These were identified at least to genera and

quantified as described by Thomas (1962, 1964c). Unfortunately, it was not pos-

sible to obtain fish from the Pysgotwr in 1998 due to their demise as a result of

acid deposition that was exacerbated by afforestation with coniferous trees.

2 4

Me t h o d s U s e d o r n v e s t i g a t in g t h e In v e r t eb r a t e a u n a

In c l u d i n g n t e rm e d i a t e H o s t s

The methods used in the earlier investigation for collecting the invertebrate

fauna, using a fine-mesh net with a semicircular opening, over as wide a range

of habitats as possible have been described (Thomas, 1962). These studies

made it possible to identify sites where Sphaerium corneum occurred in abun-

dance in backwaters and under banks. Laboratory experiments revealed that this

was the molluscan host of

Phy l lod is tomum s imi le

(Thomas, 1956, 1958a).

Sphaerium corneum

and other sphaeriid species have also been implicated as

the molluscan hosts for

Crepidostomum

species (Brown, 1927; Moravec 1982).

However, when the River Teifi was revisited in 1997

S. corneum

could not be

found in study sites where it had formerly been abundant. It was determined

therefore to undertake further work to elucidate the possible causes of its

decline. This work, which was made possible by assistance from the

Environment Agency, involved sampling at Stations 1-8 (Figure 2) using nets,

as described above, and also a cylindrical, plastic sampler to obtain quantitative

samples. The sampler measured 65 cm in length and had a diameter of 10 cm.

Penetration of depositing sediments was facilitated by having wooden handles,

held in position by a steel sleeve, 15 cm from the top of the cylinder. The pro-

vision of flexible ducting, secured to the top end of the cylinder and held above

the water surface, made it possible to extract the water column above the core

by means of a pump. This procedure greatly facilitated the extraction of the core

from the sediment. Following extraction the cores were divided into three sec-

tions, each up to 20 cm in depth. These were then washed and sieved (125 lam)

to facilitate the extraction of bivalve molluscs and other invertebrates.

The sediments were then placed in plastic bags and taken to the



12 J D THOMAS

Environment A genc y (EA) laboratory for the analysis of heavy m etals includ-

ing copper, zinc, lead and chrom ium using Auto mated Concentration Analysis

System (ACAS ) accredi ted methods.

2 5 Sp e c i e s o f He lm i n t h P a r a s i t e s

The bro wn trout at Stations A and B on the Teifi had a muc h richer fauna of

nine and eight species, respectively, com pared w ith only four species ofbrow n

trout at Station D (Table 3). The only difference betwe en the specific com po-

sition of the parasitic c omm unities o f trout from Stations A and B w as that the

plerocercoid larvae of the al logenic cestode,

Diphyllobo thrium ditremum,

only

occurred in the former station. In contrast to the trout, the salmon parr har-

bou red only fo ur and six species from Stations A and B, respectively. O f the six

species of parasites found in eels, two, nam ely Bothriocephalus claviceps and

Paraquimperia tenerrima,

we re unique to this fish species. As

Cucullanus T.)

truttae constituted more than 90 of the total num ber of individual nematodes

found in the trout the statistical data presented subsequen tly refer mainly to this

species. In contrast, C. ephemeriderum occurred m ore com monly than C. trut-

tae in the salmon parr.

2 6

Th e L i f e H i s t o r y S tr a t e g i e s o f h e Pa r a s i te s

The salmonids are an ancient group of teleost f ish and have probably co-

evolved with their helminth parasites and their intermediate hosts since before

the Cretaceous period, 70- 14 0 m illion years ago (Norman, 1963). Their geo-

graphic distribution today is circumpolar and it is likely that they colonised

freshwater ec osyste ms in Britain follow ing the retreat o f the glaciers after the

end o f the last ice age abo ut 13 000 ye ars ago (Ferguso n, 1989). O f the factors

that limit o r influence the distribution o f the parasites (Table 3) the host sp ecies

(Table 4) are clearly obligatory. Tables 3 and 5 show that

D. sagittata

is

restr icted to salmonid species (Hoffman, 1998) whereas the other species of

fish parasites fou nd are less specific with the exc eption of Paraquimperia ten-

errima

in eels. According to Moravec (1994) the lat ter is an example of a

mo noxen ous species occurring in isolated, endemic or rel ict species. The low

levels of specificity exhibited by the other helminths in the definitive hosts m ay

be part ly due to the fact that som e of the f ish harbouring the parasite species

are incidental (or postcyclic, paradefinit ive, euparatenic or metaparatenic

hosts), rather than true definitive hosts according to Moravec (1994). This

wo uld not be surprising in view o f the predatory, piscivorous and cannibalis-

t ic behav iour of ma ny species of freshwater f ish. There is som e circumstantial

evidence that the eel may have been acting as a postcyclic host rather than the




Table

3 A list o f the helminth parasites encountered, their hosts, microhabitats in the

hosts and stations where found

Taxo n Parasite species Ho sts Location Station

M o n o g e n e a

Disco cotyle sagittata Salm o trutta L.

Leuckart , 1840) Sa l m o sa l ar L .

Digenea

Crepidostomum far ion is Salm o trutta L.

Mueller, 1785)

Sa l m o sa l ar L .

Ang ui l la anguil la L .

Digenea

Crepidostomum metoecus Salm o trutta L.

Braun, 1900)

Salmo salar L

Angui l la angui l la L .

Di genea

Phyl lodis tomu m s imi le Salmo t rut ta L .

Nybelin, 1926)

Cestoda

Bothriocephalus claviceps An gu il la anguil la L.

Goeze, 1782)

Cestoda

DiphyUobothrium ditrem um Salm o trutta L.

Creplin, 1825)

Nematoda

Raph idascar is acus Salmo t rut ta L .

Bloch, 1779)

Ang ui l la anguil la L .

Nematoda

Paraquimperia tenerrima An guil la anguil la L.

Linstow, 1878)

Nematoda

Cystidicoloides Sa lmo trutta L.

ephemeriderum Salm o salar L

Linstow, 1872)

Nematoda

Cucullanus Truttaedacnitis) Sa lm o trutta L.

truttae Fabricius, 1794)

Nematoda

Capillaria

sp.

Salmo trutta L.

Acanthocephala

Neoechinorhynchus ruti l i Salm o trutta L.

Mueller,1790)

Sa l m o sa l ar L .

Angui l la angui l la L .

Gil l s A, B, D

Gi l l s A, B

Intest ine A, B, D

Intestine A, B

Intestine A, B

Int.,pyl.caecae

Int.,pyl.caecae

Intestine

Urinary A,B

bladder

Duodenum A,B

and intest ine

Mesentery, A

coelum

Intestine A , B

Intestine A , B

Intestine A , B

Stomach, int . A, B

and pylo nc caecae B

Int. and py l , caecae A ,B

Int . and pyl .caecae A, B

Int . and pyl .caecae A, B, C

Int . and pyl .caecae A, B

Duodenum,

intestine

t r u e d e f i n i t i v e h o s t f o r t h e t w o repidostomum spe c ie s i n t he Te i f i a s i t i s

k n o w n t o p r e y o n b o t h s a l m o n i d s p e c ie s . T h u s , t h e v a l u e s f o r p r e v a l e n c e a n d

a b u n d a n c e o f t h e s e p a ra s i te s i n th e e e l s w e r e f o u n d t o b e m u c h l o w e r t h a n i n

s a l m o n i d s p e c i e s T h o m a s , 1 9 6 4 c ) , d e s p i t e th e f a c t t h a t t h e d i e t a ry n i c h e s o f a ll

t h r e e s p e c i e s o v e r l a p . H o w e v e r , i t i s p o s s i b l e t h a t t h e s e d i f f e r e n c e s m a y h a v e

b e e n p a r t l y d u e t o t h e f a c t t h a t t h e e e l i s i n a c t i v e a n d c e a s e s t o f e e d i n t h e

w i n t e r m o n t h s w h e n t h e t e m p e r a t u r e i s b e l o w 1 0 ° C T h o m a s , 1 9 6 2 ) .



14 J D THOMAS

Table

4 A summary of the ecological conditions which are obligatory for the

survival of helminth parasites and also those which are favourable to them

1. Hosts

1.1.

1.2.

Parasites not requiting intermediate hosts

Parasites requiring one or more intermediate hosts as well the definitive host

Environmental conditions which are favourable to parasites and hosts

2. I. Low or zero current velocities for transmission. These are typically found in

lentic ecosystems and in lotic ecosystems in dead spaces in backwaters,

undercut banks, pools, the interstitial pore water and very close to the sediment

surface

2.2. Optimal temperature range; this is 10-16°C fo r the growth of trout. Parasites

have a wide range o f tolerance but a temperature of > 10°C is generally

necessary to stimulate reproductive activity

2.3. pH > 5.5 for both hosts and parasites. Trout and intermediate hosts, such as

Pisidium are tolerant to pH conditions o f 5.5-6.5 but as the optimal pH range

for molluscan and arthropod hosts is generally 6.5-8.3 the species richness o f

parasites tends to be higher in this range

2.4. Low levels of organic loading and high oxygen concentrations

I t i s no t un l ike ly tha t the record of

Phyllodistomum

i n the ee l by Kennedy

1974) ma y a l so have been due to pos tcyc l i c in fec t ion a s it was absen t f rom the

ee l s exam ined f rom the Te i fi Thom as , 1964c). The reco rd o f Phyllodistomum

i n the sa lm on pa r r by the sam e au tho r i s a lso unexpec ted in v iew o f i ts absence

f rom the sa lmon pa r r in the R ive r Te i f i where i t was commonly found in the

trout .

The in fo rma t ion , wh ich i s cu r r en t ly ava i l ab le r ega rd ing the pa ras i t e s and

thei r in terme dia te hosts o f the paras i tes l i s ted in Table 5 i s an essen t ia l p re-

r equ i s i t e towards an unde r s t and ing o f the i r eco logy . Cor rec t iden t i f i ca t ion

com es f ir s t. In th is connec t ion i t should be no ted tha t Kakaj i 1969) conside red

P. simile t o b e a s y n o n y m o f Phyllodistomum folium. However , th i s au tho r

fa i led to take in to account d iagnost ic fea tures , suc h as the d is t ribu t ion o f the

senso ry pap i l l ae in the adu l ts , and the d i f f e r ences be twe en the l i fe cyc le s and

l a r v a l a n a t o m y o f

P. fol ium

Gine t s in skaya , 1961 ) and

P. simile

T h o m a s ,

1958a) . I t is therefore safer a t th is s tage in our know ledg e to consider these tw o

spec ie s to be d is t inc t . Wi thou t due ca re s ib l ing spec ie s can eas i ly be co n fused

as were

C. farionis and C. metoecus

un ti l t hey were d i s t ingu i shed by Th om as

1957, 1958b).

D i g e n e t i c t r e m a t o d e s g e n e r a l l y s h o w a f a i r l y h i g h l e v e l o f s p e c i f i c i t y

towards the i r mo l lu scan hos t s . The re i s a gene ra l consensus tha t f r e shwa te r

b iva lves o f the f am i ly Sphae r i idae se rve as hos t s fo r Crepidostomum spec ie s

inc lud ing

C. cornutum C. farionis C. isostonum

and

C. metoecus

Nr l le r ,

1928; Brown, 1927; Bayl is , 1931; Hopkins , 1934; Moravec , 1982; Hoffman,



ECOLOGY OF FISH PARASITES 15

0

i

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16 J D THOM AS

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ECOLO GY OF FISH PARASITES 7

t ~

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18 J D THOMAS

1998). The c la im mad e by Aw ach ie 1968) tha t Lym naeaperegra i s a lso a hos t

o f

C. metoecus

the re fo re r equ i res ve r i f ica t ion . How ever , a s the re i s ev idence

tha t s evera l spec ies o f

Pis id ium

and

Sphaer ium

m ay be im pl ica ted as a l te rna -

t i v e i n t e r m e d i a t e h o s t s o f a n o t h e r a l l o c r e a d i i d t r e m a t o d e ,

Bunodera

luciopercae An drews and Ch ubb , 1980), th i s low leve l o f spec i f i c i ty m ay

a l so app ly in the case o f

Crepidostomum

species .

The l eve l o f spec i f i c i ty showed b y d igene t i c pa ras i t e s to the s econd in te r -

m ed ia te ho s t s i s genera l ly low er than tha t to the m ol luscan hos t . In the case o f

Crepidostomum spec ies they inc lude Gam marus pulex and Ramel logammarus

vancouverens i s

a s w e l l a s i n s e c t s b e l o n g i n g t o t h e o r d e r s P l e c o p t e r a ,

E p h e m e r o p t e r a a n d M e g a l o p t e r a T a b l e 5 ). T h e p r e se n c e o f

Crepidostomum

far ioni s

in Arc t i c Char r f rom Green land and I ce land Du e and Cur t is , 1995) ,

where amphipods and Ephemerop te ra a re absen t , ind ica tes tha t th i s pa ras i t e

has so m e f l ex ib i li ty in i ts cho ic e o f s econ d in te rmed ia te hos t.

D u r i n g 1 9 5 1 - 1 9 5 2 i t w a s s h o w n t h a t t h e f r e s h w a t e r b i v a l v e

Sphaer ium

eorneum

a c t e d a s t h e m o l l u s c a n h o s t o f

Phyl lod i s tomum s imi le

T h o m a s ,

1956 , 1958a , 1964c) . A l though i t was shown tha t the metace rca r iae in the

s p o r o c y s t s i n f e c t e d t h e t r o u t i t i s p o s s i b l e t h a t i n s e c t l a r v a e , i n c l u d i n g

an isop te ran d ragonf ly l a rvae , may a l so have been impl ica ted as an op t iona l

secon dary in te rmed ia te hos t a s is the case w i th o the r

Phyl lod i s tomum

spec ies

T h o m a s , 1 9 5 8 a ; G i n e t s i n s k a y a , 1 9 6 1 ). In c o n t r a s t, t h e s p o r o c y s t s o f

Phy l lodistom um dogieli w h i c h d e v e l o p i n Drei ssena polymo rpha l e a v e t h e

hos t a f t e r the metace rca r iae deve lop and a re p resum ab ly sw a l lowe d d i r ec t ly by

the d ef in i t ive hos ts ,

Ruti lus rut i lus

o r

Abramis brama

Ginets inskaya, 1961) .

A s Phyl lodistomum simi le was a lso found in the t rout in the Teif i in 1998, in

t h e a p p a re n t a b s e n c e o f

Sphae rium eorneum

i t w ou ld appear tha t th i s tr ema-

t o d e m i g h t a l s o u s e

Pis id ium

spec ies a s a l t e rna tive m ol luscan hos t s.

S m a l l c r u s t a c e a , n a m e l y o s t r a c o d s , s e r v e a s t h e i n t e r m e d i a t e h o s t s o f

Neoechinorhynchus

spec ies , inc lud ing

N. cristatus N. cylindricus N. sag ina-

tus

a n d

N. ruti l i

M err i t t and P ra t t, 1964 ; W alkey , 1967 ; Va l tonen , 1979 ;

Dezful i , 1996; Hoffman, 1998) . Larvae ofN. rutili in the a lder - f ly Sialis lutaria

h a v e a l s o b e e n s h o w n to b e i n f e c t i v e t o r a i n b o w t r o u t L a s s i e r e , 1 9 8 8 ;

Hof fman , 1998) bu t i t i s pos s ib le tha t these may be ac t ing on ly as pa ra ten ic

hos t s W alkey , 1967). Las s ie re and Cro m pton 1988) a l so dem ons t r a ted the

i n v o l v e m e n t o f th e s t ic k l e b a c k

Gasterosteus aculeatus

in the p os tcyc l i c t r ans -

m i s s i o n o f

N. rutili

in to r a inbow t rou t . O ther smal l c rus tacea , the copepods ,

a l so s e rve as hos t s fo r the p roce rco ids o f the tw o ces tod e spec ies , D. di tremum

and

B. claviceps.

Sm al l f i sh ac t a s ca r t i e r o r pa ra ten ic hos t s fo r

B. claviceps

w h i l e t h e p l e r o c e r c o i d s o f

D. ditremum

the on ly a l logen ic pa ras i t e in the

com m uni ty , deve lop in spec ies o f s a lmon idae Tab le 7 ).

Larger ben th ic inver teb ra tes a re imp l ica ted as hos t s o f the nem atode spec ies

Capillaria

a n d

Cystidicoloides ephemeridarum.

A c c o r d i n g t o M o r a v e c 1 9 9 4 )

o l i g o c h a e t e w o r m s m a y b e o b l i g a te i n te r m e d i a te h o s t s fo r Capi l laria sp. or




a l t e r n a t i v e l y d e v e l o p m e n t m a y b e h o m o x e n o u s o r d i r e c t i n t h e f i s h h o s t .

S e v e r a l s p e c i e s o f m a y f l i e s m a y a c t a s i n t e r m e d i a t e h o s t s o f C . e p h e m e r i -

d a r u m

( T a b l e 5 ) w h i l e s m a l l f o r a g e f i sh m a y a c t as p a r a t e n i c h o s ts . M o r a v e c

( 1 9 9 4 ) s h o w e d t h a t a m m o c o e t e l a rv a e o f l a m p r e y s a r e t h e o b l i g a t o r y i n t e r m e -

d i a t e h o s t s o f Cuc u l l anus T . t r u t t ae t he d o m i n a n t n e m a t o d e p a r a s i te o f t h e t ro u t

i n t h e T e i f i , b u t s a l m o n i d f i s h m a y a c t a s p a r a t e n i c a n d a s p o s t c y c l i c h o s t s .

D u r i n g 1 9 5 0 th e a m m o c o e t e l a rv a e w e r e f o u n d to c o e x i s t i n d e p o s it i n g s e d i -

m e n t s w i t h S p h a e r i u m c o r n e u m i n t h e R i v e r T e i f i . F i s h s p e c i e s , i n c l u d i n g

S a l m o t r u t ta a l s o s e r v e a s i n t e r m e d i a t e h o s t s f o r R . a c u s a l th o u g h a n u m b e r o f

i n v e r t e b r a t e s p e c i e s ( T a b l e 5 ) m a y a c t a s p a r a t e n i c h o s t s ( A l v a r e z P e l l i t e r o ,

1 9 7 8 ; M o r a v e c , 1 9 9 4 ) .

A c c o r d i n g t o M o r a v e c ( 1 9 9 4 ) t h e l if e c y c l e o f

P . t e n e r r i m a

r e m a i n s t o b e

e l u c id a t e d . M u c h w o r k r e m a i n s t o b e d o n e t o a c h i e v e a c o m p l e t e id e n t i fi c a ti o n

o f t h e i n t e r m e d i a t e h o s t s t h a t a r e i n v o l v e d i n t h e t r a n s m i s s i o n o f t h e h e l m i n t h

p a r a s i te s i n t h e T e i fi , P y s g o t w r a n d o t h e r r i v e r sy s t e m s . T h i s p r o b l e m i s g r e a t l y

e x a c e r b a t e d b y t h e l o w l e v e l o f s p e c i f ic i ty . P r e s u m a b l y t h is h a s a r is e n a s a

r e s u l t o f th e s t o c h a s t i c a n d u n p r e d i c t a b l e n a t u r e o f e x i s te n c e i n f r e s h w a t e r

e c o s y s t e m s . H o w e v e r , s u c h i n f o r m a t i o n i s e s s e n ti a l f o r a f u ll u n d e r s t a n d i n g o f

t h e m e c h a n i s m s t h a t ar e i n v o l v e d i n re g u l a t in g t h e i r p o p u l a t i o n d y n a m i c s .

3 D I S P E R S I O N P A T TE R N S O F T H E H E L M I N T H P A R A S I T E S

T h e f r e q u e n c y p a t t e rn s f o r t h e p a ra s i te s o f t h e t w o s a l m o n i d s p e c i es a n d t h e

v a r i a n c e / m e a n r a t i o s a n d t h e d i s p e r s i o n i n d i c e s ( T a b l e 6 ) i n d i c a t e t h a t a l l t h e

p a r a s it e p o p u l a t i o n s h a v e s t ro n g l y c l u m p e d , a g g r e g a te d , o v e r d i s p e r s e d o r c o n -

t a g i o u s d i s tr i b u ti o n s . H o w e v e r , i t i s n o t e w o r t h y t h a t t h e v a l u e s f o r t h e

Table 6 Th e varianc e/m ean ratios and the dispersio n indices (1D = 2 (n - 1)/.~) fo r

the parasites of the brown trout and salm on parr

Parasite Brow n trout Salmo n parr

S2/x 1D S2/x I o

Discocotyle sagittata 3.68 4 338.3 1.19

Crepidostomumfarionis 6.58 7 756.7 2.24

Crepidostomum metoecus

35.23 41 533.8 11.87

Phyllodistomum simile 5.72 6 747.7 -

Neoechinorhynchus rutili 17.62 20 737.7 11.16

Nem atodes 13.42 15 825.7 9.47

Total parasites 30.44 35 885.7 11.83

326.2

611.0

3 241.5

3 045.4

2 586.0

3 229.3



2 0 J D T H O M A S

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variance/mean ratios and dispersion indices are consistently higher for the

parasites of the brown trout than those of the salmon parr. In view of these dis-

persionary patterns it was necessary to normalise the data as far as possible

before undertaking parametric statistical analyses. To overcome difficulties

with zero counts the lOgl0 1 + x) transformation, where x is the number of par-

asites, was used.

In order to explain these distribution patterns it is necessary to consider the

behaviour and physiology of the host and the distribution patterns of the infec-

tive stages. If every potential host were equally exposed to a chance of being

infected by the same numbers of infective stages at a time and if the microen-

vironments inside all the hosts were identical, both physiologically and

immunologically, the frequency distribution should follow the Poisson series.

Each host will therefore have the population mean as its expected frequency.

Such random distributions have been described for some parasites, such as

s c a r i d i a g a l l i

in chickens, provided they were genetically identical, fed with

the same number of infective eggs and kept under identical conditions

Northam and Rocha, 1958). Hopkins 1959) also found this to be the case

with populations of

P r o t e o c e p h a l u s f i l i c o l l i s

in

G a s t e r o s te u s a c u l e a t u s

under

natural conditions. He postulated that this distribution was due to the random

distribution of copepods, infected with only one procercoid, and to random

feeding by the sticklebacks.

As in the present case, however, most parasite distributions exhibit overdis-

persion and conform to the negative binomial model Thomas, 1965). In the

case of bird parasites variance/mean ratios are much higher than those for

trout with most of the values in the 10-100 and 100-1000 categories while

some are higher than 100 000 Goater and Holmes, 1997). The distributional

pattern of the trout and salmon parr parasites may be due to inequalities in the

microhabitats within the host or in the chance of the host being infected. On

first inspection the first possibility seems improbable, as populations of both

hosts are likely to be genetically fairly uniform. However, the possibilty that

the fish hosts may have different levels of immunity or resistance as a result of

intervention by the parasites cannot be excluded. It seems more probable,

however, that the overdispersion is mainly due to the two fish species being

unequally exposed to infestation as a result of variation in their dietaries. The

availability of infected food items to the fish will be influenced by a number of

factors Thomas, 1962). Of primary importance is the spatiotemporal distri-

bution of the intermediate hosts. As populations of these are patchily

distributed and unequally infested Thomas, 1958 a, b; 1964 a, b, c) the para-

sites must therefore be regarded as having foci of infestation. This fact, coupled

with the occurrence of multiple infections in individual intermediate hosts,

must contribute to the overdispersion. The other major contributory factors are

differences in the dietaries of individual fish due to differences in age, sex,

season and feeding territories due to their position in the social hierarchy. It



22 J D THOMAS

may be suggested that the variance/mean ratios are lower in the case of salmon

parr than the trout because their feeding territories overlap to a much greater

extent than those of trout (Armstrong

e t a l . ,

1999). Anderson (1974) also

attributed overdispersion of C a r y o p h y l l a e u s l a t i c e p s in the bream, A b r a m i s

b r a m a , to contagious distribution of the tubificid intermediate host in the sed-

iment and to differences in the feeding behaviour of individual fish. This

author also points out that the total fish population could have an overdispersed

parasite population by compounding a series of essentially random processes.

In the case of parasites, such as monogenetic trematodes, that are transmit-

ted directly by host aggregation, favourable temperatures and overdispersion in

the distribution of the infective larvae can result in highly overdispersed dis-

tributions. These factors may result in epizootics and host death (Dogiel, 1961;

Kennedy, 1975).

4 S P A T IO T E M P O R A L A S P E C T S O F T H E PA R A S IT IC F A U N A

4 1 Q u a n t i ta t i v e D a t a

The stations are a major factor in determining the percentage prevalence of the

dominant trout parasites (Table 7). Thus the parasitic fauna of the trout from the

Pysgotwr (Station D) is characterised by the absence of

P. s im i le , N . ru t i l i ,

nematodes other than

C a p i l l a r i a

sp., and also by having a significantly lower

prevalence ofD. s a g i t t a t a than the trout from the other two stations. The preva-

lence rates for the three trematode species are also significantly lower at Station

A on the Teifi than at Station B on the Teifi. Comparisons of the parasite abun-

dance (Table 8, Figure 3) show similar trends. When transformed the abundance

values for C . f a r i o n i s , C . m e t o e c u s and P . s i m i l e were all significantly lower at

Station A on the Teifi than at Station B on theTeifi while the converse is the case

with

N . r u t i l i

and the nematodes (mainly

C . t r u t t ae .

Plerocercoids of D.

d i t r e m u m were only found in trout at Station A on the Teifi. However, the values

for both prevalence (1.5 ) and mean abundance (0.3) for this parasite were very

low (Tables 7 and 8). The maximum number of plerocercoids in any fish was

only four.

D . s ag i t t a t a

was significantly (P < 0.001) less abundant

a n d C . m e t o e -

c u s significantly (P < 0.001) more abundant in the brown trout in the Pysgotwr

(Station D) than in the brown trout from the two stations on the Teifi (Table 8).

P h y l l o d i s t o m u m s i m i l e did not occur in the urinary bladders of salmon parr.

The prevalence values for

D . s a g i t t a t a a r e

higher for salmon parr at Station A

on the Teifi A than for those at Station B whereas the converse is the case with

C . f a r i o n i s a n d C . m e t o e c u s (Figure 4.). In these respects the salmon parr

resemble the trout. Although the abundance values of the dominant parasites in

salmon parr at Stations A and B are much lower than corresponding values for



ECOLOG Y OF FISH PARASITES 3

¢)

0

I:::

t-

0

q~

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[- ,

oO

o~

e,.

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0

Z

. . . . . . . ~ o

V ~ V V

~ v ~ v ~ v

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24 J D THOMA S

i

B A D

S T A T I O N S

10

0 9

0 8

0 7

0 6

0 5

0 4

0 3

0 2

0 1

0 0

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STA3qONS

07

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0 5

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000

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STATIONS STATIONS

3o

~ ~o

F igu r e 3 The mea n abundance (_+ 95 C.L.) of parasites foun d in brow n trout at the

three stations. (Station B on the Teifi; Station A on the Teifi; Station D on the Pysgotwr).

trout they show similar spatial trends (Table 9; Figure 5) . Thus

D . sagi t ta ta N.

r u t i l i and nema tode s are mor e abundant in salm on parr at Stat ion A on the Teif i

A than at S tat ion B whereas the converse i s the case wi th C. metoecu s and C.

f a r i o n i s (Table 9; Figure 5) . However, stat ist ical analyses (Table 9) revealed

that the d i f ferences were o n ly s ign i f icant in the case o f D . sagit ta ta.




101

8O

o

_z O

~ 50

~ 4

=,

20

PARASITES

Figure 4 The percentage prevalence of the dominant parasites of the salmon parr at

Stations A and B on the Teifi. DS, D sagittata; CF, C farionis; CM, C metoecus; PS,

P simile; NR, N rutili; NEM , nemanodes; TO T. PA R, total parasites.

Table 9 Th e means of transformed lOgl0 (1 + x) numbers of salmon parr parasites

and the results of statistical analyses

D sagittata C farionis C metoecus N rutil i Nematodes Totalparasites

Teifi Station B 0.0167 0.130 0.303 1.729 0.186 0.835

Teifi Station A 0.092 0.073 0.092 1.922 0.258 0.885

F values 5.34 0.39 1.36 0.41 0.31 0.15

P values 0.022 0.53 0.24 0.52 0.58 0.70

The ab undance o f the he lmin th pa ras i t e s m ay be de te rmined by a numb er o f

interactive factors such as s tat ions , seasons, the age, s ize, sex and wellbeing (as

mea s u red by the ad ipos e index o r cond i t ion f ac to r ) o f the hos t f is h (F igu re 1).

In v iew of the com plex i ty of these in terac tions m ul t ip le regress ion analys is was

us ed to eva lua te the ex ten t to wh ich thes e cou ld p red ic t pa ras i t e abundance .

The r e s u l t s o f these ana lys es s how tha t the ma in p red ic to r s o f the t r ans fo rme d

to ta l nu m be r of paras i tes in t rou t, as the response , a re s ta t ions, seasons an d age

of the trout as these contr ibute 38.0 , 40.8 and 20.0 , respectively, to the total

var iance (Table 10). The sex of the t rou t and the a d ipose index are a lso s ign i f i-

cant predictors (P = 0.001 a nd 0.011, respectively ) al thou gh their contr ibution to

the to ta l var iance i s min ima l (0 .72 and 0 .44 , respect ive ly) . In contras t the

condit ion fac tor wa s not a s ignif icant predicto r (P = 0.867). Wh en individual par-

as i te taxa w ere inc luded as the response in the equat ion , s ign if ican t re la t ionships



26 J D THOMAS

0 2 2

0 1 2

0 02

-T -

S T A T I O N

~o

d 02

o~

o

z

=

o o

r~ r

B A

S T A T I O N

15

4

13

12

~0

8

B A B A

S T A T I O N S T A 1 ] O N

0 r

0 6

O 5

0 4

o

0 3

A

S T A T I O N S T A T I O N

16

15

~4

13

12

u

9

i i

B A

F igu r e 5 The mean abundance (_+ 95 C.L.) of parasites found in salmon parr at the

two stations on the Teifi (= Teifi B) and Station 2 (= Teifi A).

between the transformed parasite numbers and the condition factor or adipose

index (P = 0.0 44 and P = 0.018 , respectively) w ere on ly found in the case o f the

most abundant parasite, C. metoecus (Table 10). Both of these relationships

were positive but they contribute little to the total variance (0.48 and 0.46 ,

respectively). In contrast, stations, seasons and age were also hig hly significant

predictors of numbers of

C. metoecus

contributing 4.0 , 88.2 and 6.3 ,

respectively, to the total variance. The sex of the trout was also a significant

predictor of the numbers of C. metoecus (P -- 0.00 5) although its contribution to

the total variance was minimal (0.54 ). The seasons also contributed 48.78 ,

52.5 , 33.7 , 5.4 and 3.2 of the total variance, respectively, wh en D . sag i t -

ta ta C. ar ion is P simi le N. ru t i l i

and nematodes were the main responses in the

multiple regression equ ation. The relatively low variance values in the last three

taxa can be attributed to their absence or dearth at Station D. As a result the




Table 10 The results o f multiple regression analyses of transformed num bers o f

parasites (total numbers of parasites and C. metoecus of brown trout as the response, and

stations, seasons, age, sex, condition fac tor and adipose index as predictors (note that the

of variance accounted for by each fac tor is conditional on the factors entered earlier in

the table)

Predictors Coefficients S.D. P variance

Total

p r sites

Constant 4.013 0.976 0.000

Stations (3) -3.125-0.190 0.182-0.187 0. 29 6- -0 .0 00 38.00

Months ( 1 2 ) -3.07 9-0.7 98 0.355-0.300 0.000-0.008 40.83

Ag e 1.077 0.071 0.000 19.98

Sex -0.3 79 0.116 0.001 0.72

Condition factor 0.014 0.086 0.867 0.02

Adipose index 0.239 0.094 0.011 0.44

R.Sq.= 56.1 ; F = 85.96; P = < 0.000

C metoecus

Constant 0.867 0.532 0.103

Stations (3) -0.0 41 -0.5 98 0.099-0.102 0.678-0.000 4.04

Months (12) -0.04 1-0.5 50 0.181-0.194 0.002-0.000 8 8. 21

Age 0.316 0.039 0.000 6.26

Sex -0.1 78 0.063 0.005 0.54

Condition facto r 0.095 0.047 0.044 0.48

Adipose index 0.122 0.051 0.018 0.46

R.Sq.=51.9 ; F = 72.71; P =< 0.000

R Sq = Sum of squares

s ta t ions contr ibu ted 46 .2 , 94 .2 and 50 .1 of the to ta l var iance in the cases

o f P simile, N. rutili and nema todes , respect ive ly .

The r e su l ts o f mu l t ip le r eg ress ion ana ly ses ca r r i ed ou t wi th the sa lm on pa r r

da ta show tha t the on ly s ign i f i can t p r ed ic to r s o f the t r ans fo rm ed num ber o f

to ta l paras i tes were seasons , condi t ion fac to r and the ad ipose index . These c on-

t r ibu ted 79 .0 , 8 .2 and 6 .6 of the to ta l var iance respec t ive ly (Table 11) . In

con t r a s t s t a t ions , age , sex and we igh t w ere no t s ign i fi can t p r ed ic to r s o f pa ra -

s it e abundance . Wh en ind iv idua l pa ras i t e s were inves t igated a s the r e sponse in

t h e m u l t i p l e r e g r e s s i o n e q u a t i o n s i g n i f i c a n t r e l a t i o n s h i p s b e t w e e n t h e

t r ans fo r med pa ras i t e num ber s and the cond i t ion f ac to r o r ad ipose index (P =

0 .000 and P = 0 .023 , r e spe c t ive ly ) were on ly found in the case o f the mo s t

abundan t paras i te , N. rutili (Table 11) . As was the case wi th to ta l paras i tes bo th

o f these r e l a t ionsh ips we re pos i tive . Mu l t ip le r eg ress ion an a ly ses show ed ,

however , t ha t seasona l chang e wa s a ma jo r f ac to r in p r ed ic t ing the number s o f

a l l the ind iv idual paras i tes in the case of the sa lmon par r . Thus i t contr ibu ted



28 J D THOMAS

Table 11

The results of multiple regression analyses of transformed numbers of total

parasites and N. rutili in salmon parr, as the response, and stations, seasons, age, sex,

weight, condition factor and adipose index as predictors (note that the variance

accounted for by each factor is conditional on the factors entered earlier in the table)

Predictors Coefficients S.D. P variance

otal paras i tes

Constant 0.016 0.433 0.971

Stations (2) -0.016 0.018 0.356 2.00

Seasons (12) 0.884-0.109 0.1704).285 0.521-0.000 78.96

Age 0.192 0.110 0.083 1.30

Sex -0.043 0.057 0.444 2.05

Weight -0.006 0.004 0.140 0.88


Adipose index 0.100 0.047 0.033 6.60

R.Sq.= 20.4 ; F = 4.33; P = < 0.000

N rutil i

Constant -1.226 1.026 0.233

Stations (2) -0.032 0.042 0.439 0.27

Months ( 1 2 ) -1.585-0.167 0.65-0.402 0.860-0.000 63.34

Age 0.321 0.261 0.221 0.05

Sex -0.113 0.135 0.400 3.04

Weight -0.018 0.010 0.075 1.30


Adipose index 0.254 0.111 0.023 9.62

R.Sq.= 16.8 ; F = 3.42, P = < 0.000

R S q = S u m o f sq u a r e s

48.3 , 71.2 , 69.7 , 63.34 and 61.3 to the total variance in the cases of

D . s a g i t t a t a , C . f a r i o n i s , C . m e t o e c u s , N . r u t i li

and nematodes, respectively.

Multiple regression analyses shows that the stations are clearly major fac-

tors in determining the abundance of individual parasites as well as total

parasites in trout (Table 10). Thus, the stations contribute 17.5 , 29.3 , 4.0 ,

46.2 , 50.1 , 94.2 and 38.0 of the total variances in the cases of D.

s a g i t t a t a , C . f a r i o n i s , C . m e t o e c u s , P . s i m i l e ,

nematodes,

N . r u t i l i

and total par-

asites, respectively. As salmon parr were restricted to the two Teifi stations,

stations are much less important predictors as they contribute only 0.3 , 6.7 ,

25.4 , 0.3 , 27.9 and 2.0 of the total variances in the cases of D . s a g i t ta t a ,

C . f a r i o n i s , C . m e t o e c u s , N . r u t i li , nematodes and total parasites, respectively

(Table 11).

The mean abundance of each of the dominant trout parasites varies signifi-

cantly on a seasonal basis (Figure 6 and Table 12). In the cases ofD. s a g i t t a t a ,

C . f a r i o n i s , C . m e t o e c u s , P . s i m i l e ,

nematodes (mainly

C . t r u t t ae

and total




14

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MONTH

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Figure

The mean m onthly changes (_+ 95 C.L. ) in the abundance of the dominan t

parasi tes o f the brown trout in the Teifi .



30 J D THOMAS

a3

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Figu re The

mean monthly changes(_+ 95 C.L .) in the abundance of the dominant

p r sites of the s lmo n p rr in the Teifi

parasites the abundance values d ecl ine fro m winter high s in the late spring and

summer months but begin to increase again in the autumn. However, these

trends are not apparent in the case of

N rut i l i

With the exception of

D sagi t tata the

mea n abundances of individua l par-

asites in the salmo n parr, although mu ch lo we r than those o f trout, also s how

significant seasonal fluctuations Table 13, Figure 7). The prevalence of

D sagi t ta ta was much less in salm on p arr than the trout and it was only

encountered during the months o f January, September, O ctober and November.



32 J D THOMAS

How ever, with the exception of

C. metoecus

there were no sum mer troughs in

abundance values of salm on parr parasites.

Multiple regression analyses confirms that seasonali ty was also a major

factor in predicting the abundance of individual parasites such as D. sagit-

ta ta C. far ionis C. metoe cus

and P.

s imile

in trout as i t contributed 48.78 ,

52.46 , 88.21 and 33.74 , respectively, to the total variance in each case

(Table 10). In contrast, the abundances of N. rutil i and nematodes, chiefly C.

tru t tae were much less inf luenced by seasonal i ty as i t contr ibuted only

5.45 and 3.22 , respectively, to the total variance. M ultiple regression

analyses also showed that seasonali ty was a major factor in predicting the

numbers o f D. sagittata C. fari oni s C. meto ecus N. rutil i and nematodes in

salmo n parr as i t contributed 48.3 , 71.2 , 69.7 , 63.3 and 61.3 to the

total variance, respective ly (Table 11). Ho wev er, there wer e no well-defin ed

seasonal trends, with winter highs and s um me r lows except in the case of C.

metoecus

(Figure 7).

4 2 Physicochemical Factors tha t m ay Influence the Distribution

and Abundance of the Parasites and their Fish Hosts

The nature o f the parasitic com mu nity in aquatic eco system s is determined by

interactions involving the definitive host fish, the intermediate hosts and the

physicochemical fac tors (Wisniewski , 1958; Dogie l , 1961; Chubb, 1970;

Kennedy, 1978c; Esch et al. 1988; Kenne dy and Hartvigsen, 2000). The major

physicoche mical factors that ma y influence the distr ibution and abundance of

the parasitic fauna in aquatic ec osys tem s are summ arised in Table 4 and Figure

1 and their possible involvement is discu ssed below.

4.2 .1 . Water f lo ws and wate r types

As a result of evolutionary pressure, trout and salmon have b eco m e adapted to

live in the sediment-producing erosion zone, which is the f irst of three major

zones in river classification systems (Dobson and Frid, 1998). In this zone,

which is the major source of both water and sediment, the slope is typically

steep and deposit ion o f sediment is therefore localised or ephemeral b ecause o f

the high shear velocity. The water types in this zone are diverse and include

succession s of riffles, fast reaches, sm all pools and backw aters with d epositing

sediments. In the older classification systems, base d on biological parameters,

which we re deve loped for temperate-zone rivers, this w as described as the trout

zone (Carpenter, 1928). Th e seco nd majo r zone, kno wn as the sedimen t trans-

fer zone, is characterised b y a reduction in gradient. As a result the sedim ents,

consisting o f sand and gravel, are transported w ith little net loss or gain. H ere




the pools and backwaters are larger, the flow more uniform and riffles and fast

reaches are absent. This zone is inhabited by minnows, grayling and some trout

and is succeeded by the sediment deposition zone, where roach, bream and

barbel predominate.

The presence of localised, often ephemeral, depositing zones in reaches

occupied by trout in rivers is of paramount importance because it determines

the distribution of both the free-living stages of the parasites and their hosts.

The parasitic stages, which emerge from the eggs, are planktonic in nature and

are therefore particularly vulnerable to currents. This consideration may

explain the following gradation in the prevalence and intensities of infection of

D. sagittata

in brown trout at the three stations: Station A > Station B > Station

D. Thus, the water flow in Station A in the Tregaron Bog area is hardly

detectable much of the time because of the very gentle gradient. The Teifi at

Station B is a much larger river than the Pysgotwr at Station D and because it

has a gentler gradient and a reduced shear force it has a much greater surface

area of sheltered microhabitats consisting of backwaters, pools and undercut

banks with depositing sediments. It is likely that the low flow at station A is

also responsible for the fact that it is the only station where D. ditremum was

found. The almost lentic conditions prevailing at this station are favourable to

both the planktonic coracidium larvae of this species and its copepod inter-

mediate host. The completion of the life cycle of B. claviceps may also be

facilitated by the fact that the eel has a preference for sheltered habitats, with

depositing sediments, frequented by copepod intermediate hosts.

The intermediate hosts of other parasites including C. farionis C. metoecus

P. simile N. rutili C. truttae and CapiIlaria species Table 5) are also gener-

ally found in association with depositing sediments. The highly erosive nature

of the substrate may, therefore, be partly responsible for the absence of P.

simile N. rutili and C. truttae from Station D. In contrast to the other parasites

the trout at Station D are more heavily infected with C. metoecus than the trout

at the two stations on the Teifi. This suggests that the second intermediate hosts

may be mayflies or stoneflies that are well adapted to live in more turbulent

waters with eroding sediments. The species involved might include

Ecdyonurus torrentis Baetis rhodani Paraleptophlebia submarginata and

Leuctra spp. as Awachie 1968) found these to be infected with dead or dying

metacercariae of C. metoecus. However, Gammarus pulex which Awachie

1968) considered to be the major second intermediate host of C. metoecus

was absent from the Pysgotwr.

It would appear, therefore, that some trematode species, such as C. metoe-

cus are better adapted for life in fast-flowing waters than others. This is also the

case with some of the nematode parasites of freshwater fish. Thus, Moravec

1994) lists Cucullanus truttae Paraquimpera tenerrima and Cysdicoloides

ephemeridarum as being adapted to live in regions of rivers where the water is

fast-flowing, while Raphidascaris acus is better adapted to still or fast-flowing



34 J D THOMAS

waters. However, these parasites may be locally distributed because the inter-

mediate hosts have preferences for particular water types. Thus, C.

ephemeridarum

is abundant in the more erosive habitats that support mayflies

but tends not to coexist with

Cystidicola farion is

which uses gammarids as

intermediate hosts. Likewise, C. truttae is restricted to stretches of fiver where

depositing conditions provide favourable habitats for its intermediate host,

which are larval lampreys. It is not surprising that none of the nematode

species described by Moravec 1994) as being planktophilous because they use

copepods or brachiurids as intermediate hosts and therefore are characteristic

of still or very slow-flowing waters were found in the Teifi or Pysgotwr.

The increase in availability of depositing sediments in the second and third

major river zones favours the distribution and abundance of macrophytes, the

molluscan and crustacean intermediate hosts of helminth parasites and cyprinid

and other non-salmonid fish. It can therefore be hypothesised that species

richness and diversity of the helminth parasites would increase at the supra-

community level but that the converse would be the case with the helminth

parasites of trout because of the reduction in the densities of both definitive and

suitable intermediate hosts.

Lentic water bodies may be more favourable for the transmission of the

helminth parasites in some fish. Thus, Landry and Kelso 1999) found that

median parasite abundances in the largemouth bass,

Micropterus salmoides

were higher in lakes than in rivers or swamps although the abundance of

Proteocephalus amploplitis was higher in riverine sites. As species diversity is

higher in the littoral zone of lentic water bodies than in the profundal zone it

can be postulated that the helminth parasites of fish occupying these zones

would show a similar trend. There is evidence in support of this hypothesis as

Knudsen

et al.

1997) found that the normal morph of the Arctic charr,

Salvelinus alpinus

which feeds in the littoral zone, has a much richer helminth

fauna than the dwarf morph that inhabits the profundal zone.

Fish inhabiting lentic water bodies also tend to have a higher prevalence of

allogenic helminth species than fish in lotic water bodies. There are two main

reasons for this. Firstly, the larvae of allogenic species are more planktonic in

nature than those of autogenic species and birds, which are generally the defin-

itive hosts. Secondly, birds are more abundant in lentic than in lotic habitats. As

trout have evolved to exploit lotic habitats their helminth communities are

characterised by a dominance of autogenic species. In contrast, allogenic

species are more prevalent than autogenic species in cyprinid fish as they have

evolved to exploit lentic habitats and the depositing conditions encountered in

lowland reaches of lotic ecosystems.

Kennedy 1978c) attempted to relate the parasitic fauna of brown trout in

nine British lakes to various physicochemical parameters. However, the only

significant correlations were those between the size of the lake and the number

of parasite species harboured by trout and between the altitude of the lake and




t h e n u m b e r o f s p e c i e s p r e se n t. T h e r e la t io n s h i p b e t w e e n t h e p a ra s it ic f a u n a o f

t h e f is h a n d t h e s iz e o f t h e w a t e r b o d y i s i n a c c o r d w i t h t h e f in d i n g s o f D o g i e l

1961) and i s p rob ab ly a t t r ibu tab le to g rea te r hab i t a t and b io log ica l d ive rs i ty .

The nega t ive r e la t ionsh ip b e tw een l ake a l t i tude and pa ras i ti c f aun a w as a t tr ib -

u ted to the h igher a l t i tude l akes be ing r e la t ive ly smal le r than those a t lower

a l ti tude . Ho we ver , the re were no s ign i fi can t re l a t ionsh ips b e tw een the num ber

o f p a r a si ti c s p e c i e s a n d g e o g r a p h i c a l p o s i ti o n , a g e , d e g r e e o f i s o la t i o n o r

C a C O 3 l e v e ls o f th e l a k e s. K e n n e d y 1 9 7 8 c ) a n d E s c h et al 1988) the re fo re

c o n c l u d e d t h a t h e l m i n t h c o m m u n i t i e s o f f r e s h w a t e r fi sh w e r e s t o c h a s t ic

a s s e m b l a g e s w h o s e c o m p o s i t i o n s a r e la r g e ly d e t e r m i n e d b y h i g h r a t es o f d i s-

pe r s ion o f the pa ras i t e s and hos t f i sh by b i rds and human ac t iv i ty . A l though

these conc lus ions were based on r e la t ive ly smal l s amples i t i s ev iden t tha t

research a imed a t re la t ing the paras i t ic fauna to l imnological condi t ions should

be ca r r i ed ou t in r e la t ive ly und i s tu rbed hab i t at s .

4 2 2 Water temperature and photoperiod

A s t e m p e r a t u r e l im i t s t h e g r o w t h a n d d e v e l o p m e n t o f p o i k i lo t h e r m i c o r g a n -

i sms inc lud ing he lm in th pa ras i te s i t wo u ld s e em log ica l to hypo thes i s e tha t the

he lmin th com m uni t i e s shou ld be r iche r in t rop ica l f r e shwate r f i sh than in t em-

pera te zon e f i sh bec aus e the average t empe ra tu res w i l l t end to be h igher in the

f o r m e r c a s e . H o w e v e r , C h o u d u r y 2 0 0 0 ) a n d P o u l i n 2 0 0 1 b ) f o u n d t h e o p p o -

s i t e t r end in con t r as t to the majo r i ty o f an imal and p lan t a s semblages . The

reasons fo r th i s apparen t anomaly a re no t known and r equ i r e inves t iga t ion .

O b s e r v a t i o n s m a d e b y T h o m a s 1 9 6 6 ) in a t ro p i c al la k e i n G h a n a m a y p r o v i d e

s o m e c l u es . T h e s e s h o w t h at s p e c i e s r i c h n es s i s m u c h h i g h e r a m o n g t a x a w i t h

h i g h d i s p e r s i v e p o t e n t i a l s u c h a s t h e O d o n a t a , H e m i p t e r a , C o l e o p t e r a a n d

D i p t e r a t h a n a m o n g t a x a w i t h p o o r e r d i s p e r s i v e p o w e r s s u c h a s t h e

Eph em eroptera , Tr ichoptera, Anne l ida , Crus tacea and Mollusca . The m os t p lau-

s ib le exp lana t ion fo r th i s phenom enon i s tha t wa te r bod ies in s avanna a reas o f

Af r ica a re o f t en ephem era l du e to s evere s easona l d rough t . The s e lec tive m ech-

an i sms wou ld the re fo re f avour t axa w i th h igh d i spe r s ive powers . In con t r as t

P la tyhe lmin thes and the o rgan i sms invo lved as in te rmed ia te hos t s o f he lmin th

paras it e s , such as the Mo l lusca and Crus tacea , w ou ld be d i s advan taged .

As b o th the f i sh hos t s and pa ras i t e s a r e po ik i lo the rmic i t i s to be exp ec ted

t ha t t h e ir r e p r o d u c t io n a n d p o p u l a t i o n d y n a m i c s w o u l d a l s o b e a f f e c t e d b y

seasona l changes in t empera tu re in the t empera te zones . In the case o f the

sa lm on id hos t s the re i s am ple ev ide nce in suppor t o f th i s hypo thes i s . Thus ,

e x p e r i m e n t a l w o r k o n t h e b r o w n t r o u t h a s s h o w n t h a t a lt h o u g h g r o w t h o c c u r s

i n t h e t e m p e r a t u r e r a n g e o f 4 - 1 9 ° C t h e o p t i m u m g r o w t h o c c u r s b e t w e e n 1 3

and 14 °C E l l io t , 1989a). A g rowth mod e l fo r the b row n t rou t E l l io t , 1989b)

wh ich as su m ed tha t the ini ti a l s i ze o f the f ry and the wa te r t empe ra tu re a r e the



3 6 J D T H O M A S

1 2 3 .4

t

5 6 7 8 9 1 0 1 1 1 2

M o n t h

Figure 8 Seasonal changes in the condition factor (+ 95 C.L.) of brown trout ov er

a 12-m onth period.

t ,3

¢,,,

O

I . -

t..

Z

I -

Z

0

O

1 2 _

1 2

•

i i

4 5

6 7 8 9 1 0 1 1 1 2

M O N T H S

Figure 9 Seaso nal chang es in th e con dition fa ctor (__.95 C.L.) of the salmon parr

over a 12-month period.

c h i e f f a c t o r s a f f e c ti n g g r o w t h w h e n f o o d i s n o t l i m i t i n g g a v e a n e x c e l l e n t f i t t o

t h e d a t a. D u r i n g t h e c o u r s e o f t h e p r e s e n t i n v e s t ig a t i o n o n t h e T e i f i i t w a s f o u n d

t h a t th e w a t e r t e m p e r a t u r e s w e r e f a v o u r a b l e f o r g r o w t h f r o m m i d - A p r i l u n t i l

S e p t e m b e r ( T h o m a s , 1 9 62 ). T h i s p e ri o d c o i n c i d e d w i th t h e t im e w h e n t h e

c o n d i t io n f a c t o rs o f th e t r o u t r e a c h e d m a x i m u m v a l u es ( F i g u re 8 ) a n d w h e n

t h e i r i m m u n e r e s p o n s e i s m o s t e f f e c t iv e ( S e c o m b e s a n d C h a p p e l l , 1 9 9 6) .

H o w e v e r , te m p e r a t u r e is n o t t h e o n l y c l i m a t ic f a c t o r th a t m a y i n f l u e n c e g r o w t h

a n d t h e t i m i n g o f r e p r o d u c t i o n i n s a l m o n i d f i sh a s t h e r e is a l s o e v i d e n c e t h a t

p h o t o p e r i o d i s a l s o i m p l i c a t e d ( P o r t e r et al. 1 9 9 8 ) . T h e s e a u t h o r s c o n s i d e r t h a t

a l th o u g h t h e r e is e v i d e n c e f o r a n e n d o g e n o u s , c i r c a n n u al c l o c k t h i s m e c h a n i s m




is synchronised or entrained by photoperiod changes. Changes in photoperiod

provide a more reliable feed-forward or predictive signal than temperature for

organisms that live in the temperate areas of the world. In the case of salmonids

it ensures that the fry emerge at a time when local enviromental factors such as

food, water flow and temperature are optimal for their survival.

The present results show that the seasonal cycle in radiation levels, man-

ifested by changes in temperature and photoperiod, is the major factor in

predicting the total number of parasites of both trout and the salmon parr as

it contributed 40.8 and 79.0 to the total variance, respectively.

Seasonality was also a major factor in predicting the abundance of individ-

ual parasite species such as

D . s a g i t t a ta C . f a r i o n i s C . m e t o e c u s

and P.

s i m i l e

in trout as it contr ibuted 48.78 , 52.46 , 88.21 and 33.74 ,

respectively, to the total variance in each case. In contrast, seasonality was

less influential in determining the abundance of

N. ru t i l i

and nematodes,

chiefly

C. t ru t t ae

in trout as it contributed only 5.45 and 3.22 , respec-

tively, to the total variance in each case. Although, with the exception of C.

m e t o e c u s

there were no well-defined cyclical seasonal trends in the abun-

dance of salmon parr parasites, seasonality was nevertheless an important

factor in predicting their numbers.

In view of the fact that parasite abundance values in the definitive host can

be influenced by a number of factors, including stations as well as the age

and sex of the host care must be taken in evaluating claims that they show

statistically significant seasonal trends. However, there have been a number

of attempts at classifying species of helminth parasites into those that may

exhibit irregular fluctuations, without marked seasonal changes, and those

that show marked seasonal cycles in prevalence or abundance (Kennedy,

1975; Chubb, 1977, 1979, 1980,1982; Forbes e t a l . 1989). Seasonal cycles

are more l ikely to occur in the case of species that are univoltine. This is the

case with populations of smaller monogeneans such as

D a c t y l o g u r u s v a s t a -

to r

in carp which build up in spring and summer and decline in winter when

they may overwinter as eggs (Dogiel, 1961; Chubb, 1977). In contrast, D.

s a g i t t a t a

may have different life history strategies with life spans of 1, 2 to

3 years depending on geographical location (Dogiel, 1961; Paling, 1965).

Egg production and development take place at all times although they are

optimal when the temperatures are higher in the summer (Gannicott and

Tinsley, 1998b). However, mortality of both the larvae and adults is also

higher at this time (Paling, 1965; Gannicott and Tinsley, 1998a). If mortality

exceeds recruitment in the summer then a summer trough in abundance may

occur, as was the case with the

D. sag i t t a ta

populations in trout in the pres-

ent investigation. However, tendencies for seasonal fluctuations to occur

will be buffered in those populations with longer life spans. As a result

marked seasonal cycles in abundance or prevalence of

D. sag i t t a ta

popula-

tions are not generally observed (Paling, 1965; Campbell, 1974). As a result



38 J D THOMAS

of the ir r e l a t ive ly long- te rm su rv iva l r a t e s, ex tend ing ove r m any yea r s , th is i s

a l s o o f t e n t h e c a s e w i t h l a r v a l p a r a s it e s s u c h a s s p e c i e s o f D i p l o s t o m u m a n d

D i phy l l obo t h i um

Chubb , 1980) .

P o p u l a t i o n s o f N. ruti l i a r e c h a r a c t e r i s e d b y h a v i n g g r a v i d i n d i v i d u a l s

p r e s e n t t h r o u g h o u t t h e y e a r i n t h e t e m p e r a t e z o n e a l t h o u g h p e a k e g g o r

l a rv a l p r o d u c t i o n o c c u r s d u r i n g t h e w a r m e r se a s o n C h u b b , 1 9 8 2 ).

P o p u l a t i o n s o f a n o t h e r a c a n t h o c e p h al a n ,

P om phor hynchus l aev i s

i n d a c e

b e h a v e in a si m i l a r m a n n e r K e n n e d y , 1 9 7 5 ). D e s p i t e th e r e d u c t i o n i n a b u n -

d a n c e o f N. rutili i n t h e tr o u t d u r in g J u l y i t m u s t b e c o n c l u d e d t h a t t h e re w a s

n o e v i d e n c e o f a m a r k e d s e a s o n a l c y c l e i n a b u n d a n c e a n d p r e v a l e n c e o f t h is

pa ras i t e in s a lmo n id po pu la t ions in the Te if i. Th i s sugg es t s tha t mor ta l i ty and

r e c r u i t m e n t a r e in a s t a te o f e q u i l i b r iu m m o s t o f th e t i m e . T h i s p r o c e s s i s

a i d e d b y t h e p r e s e n c e o f a d u l t s t h r o u g h o u t t h e y e a r. I n c o n t ra s t , t h e p r e v a -

l e n c e a n d a b u n d a n c e o f

N. ruti l i

in ba rbe l ,

Barbus barbus

i n t h e D a n u b e

b a s i n s h o w e d m a r k e d s e a s o n a l c h a n g e w i t h p e a k s f r o m F e b r u a r y t o A p r i l a n d

t r o u g h s f r o m J u l y t o A u g u s t M o r a v e c a n d S c h o l z , 1 9 9 4 ). A s re c r u i t m e n t

p e a k s f r o m M a y t o J u l y it w o u l d a p p e a r t h at t h e tr o u g h s f r o m J u l y t o A u g u s t

w e r e c a u s e d b y h i g h m o r ta l it y .

Phyl lod i s tomum s p e c i e s re s e m b l e N. rutili in not having a d is t inct annual

cyc le o f r ep roduc t ive act iv i ty . Thus , C happe l l 1969) foun d tha t a l though the

r a te o f e g g p r o d u c t i o n o f

P f o l i um

wa s h igher in the sum m er than in the w in te r

the s t i ck leback , Gasteros teus aculeatus b e c a m e i n f e c t e d t h r o u g h o u t t h e y e a r.

T h e s e f in d i n g s a r e i n a c c o r d w i t h t h o s e o f P i e tr o c k et al. 1 9 9 9 ) a s t h e y f o u n d

j u v e n i l e s a n d g r a v id P hy l lods t om um f o l i um i n b l u e b r e a m , Abram is ba l lerus

and ruf fe ,

Gymnocephalus cernuus

in a l l s easons . They the re fo re conc luded

tha t in fec t ion migh t occur a t a l l t imes . However , these au tho r s found tha t P .

f o l i u m

in the ru f f e exh ib i t ed a we l l -de f ined s easona l c yc le w i th the p reva lence

a n d a b u n d a n c e v a l u e s b e i n g s i g n i f i c a n t l y h i g h e r i n t h e w i n t e r t h a n i n t h e

s u m m e r m o n t h s a s w a s t h e c a s e w i t h P. simile in the t rout in the Teif i in the

p resen t inves t iga t ion . In con t r as t , t he p reva lence and abundance va lues fo r

th is pa ras i te in the b lue b ream var ied i rr egu la r ly th rou ghou t the yea r w i thou t

exh ib i t ing an annua l cyc le .

A c c o r d i n g to C h u b b 1 9 8 2 ) n e m a t o d e s su c h a s Capi l lar ia s p . a n d

Raphiascar is acus have two genera t ions a yea r whereas Cucullanus truttae and

t h e t w o C r ep i dos t om um s p e c i e s a p p e a r t o b e u n i v o l t i n e w i t h w e l l - d e f i n e d

per iods fo r m a tu ra t ion , ov ipos i t ion , s en esce nce and dea th . I t i s no t su rp r i s ing

the re fo re tha t C. metoecu s C . far ion i s a n d C. truttae e x h i b i t w e l l - d e f i n e d

a n n u a l c y c l e s c h a r a c t e r i s e d b y h i g h p r e v a l e n c e a n d a b u n d a n c e v a l u e s in th e

d e f i n i t iv e f i sh h o s t d u r i n g t h e c o l d e r m o n t h s o f th e y e a r a n d l o w v a l u e s

d u r i n g t h e w a r m e r m o n t h s o f t h e y e a r. A s p o i n t e d o u t b y D o g i e l 1 9 6 1 ) a n d

C h u b b 1 9 7 7 , 1 9 7 9 , 1 9 8 0 , 1 9 8 2) s u c h a n n u a l c y c l e s a r e t y p i c a l a n d w i d e -

s p r e a d i n p a r a s i te s o f f r e s h w a t e r f i s h a n d o t h e r e x a m p l e s a r e p r o v i d e d b y

B u n o d e r a s a c c u la t a B u n o d e r a l u c io p e r c a A s y m p h y l o d o r a t i nc a e




Al loc raed ium i soporum Sphaeros toma bramae Cam al lanus lacus t ri s and

Echinorhynchus gadi .

The similarities in the life histories of digenetic trematodes of temperate

zone fish such as C. metoecu s C . far ion i s and B unoder a l uc i oper ca have

been discussed by a number of authors Awachie, 1968; Awachie and Chubb,

1964; Andrews and Chubb, 1980; Forbes

et al .

1989). Typically, juvenile

worms invade their fish hosts from late summer to autumn and mature during

the winter and early spring. During the summer months the gravid worms

suffer heavy mortality and disappear from their definitive hosts by August.

There has been much discussion regarding the mechanisms that may cause

the seasonal cycles in their prevalence and abundance. As these cycles are

negatively correlated with temperature, some authors Awachie and Chubb,

1964; Awachie, 1968; Chubb, 1977, 1979, 1980, 1982) suggested that it is

the causative factor. They postulated that the disappearance of C. metoecus

and

C. far ion i s

from their trout host in the late summer was caused by an

increase in water temperature above 10 °C, which was considered to be the

critical upper level for the survival of adult parasites. They therefore pro-

posed that these parasites were of northern origin, stenothermal and probably

relicts of the ice age.

Despite these correlations several arguments can be advanced in support of

the view that temperature may not be directly responsible for driving the sea-

sonal cycle by causing mortality of the adult worms. Firstly, if

temperature-induced mortality reduces the fitness of the species it is to be

expected that the parasites would have become adapted to the higher summer

temperatures as a result of natural selection. The fact that parasites such as C.

metoecus and C. far io nis can survive high summer temperatures in their inter-

mediate hosts indicates that their genome is amenable to these selective

pressures. Secondly, it was found that some adult C. metoecus and C. far io -

nis albeit in smaller numbers, did survive in the salmonids in the Teifi,

particularly in the salmon parr, during the warm summer months although

their abundance was significantly less than in the winter months. Thirdly,

some C r e p i d o s t o m u m species such as C. cooper i living in perch, P er ca

f l aves cens in Lake Opeongo, Ontario, Canada can survive high summer tem-

peratures as adults. Thus, Cannon 1972) found the maximum prevalence of

these parasites in the summer and the lowest in the autumn and early winter.

Fourthly, as pointed out by Kennedy 1975), this hypothesis is not supported

by experimental evidence.

It seems more likely therefore that the annual cyclical changes in worm

abundance of parasites such as C. metoecus have resulted from selective

pressures that favour the avoidance of the definitive host during the summer

because the conditions in the gut become highly unfavourable at this time.

Although the high summer temperatures are correlated with the increased

worm mortality it does not follow that it is the causative mechanism. One



4 0 J D T H O M A S

f ac to r tha t m ay m ake i t d i f f i cu l t fo r the pa ras i t e s to su rv ive in the gu t a t th i s

t i m e i s t h e e n h a n c e m e n t o f th e h o s t s i m m u n e r e s p o n s e a s a r e s u l t o f

i n c r e a s e d t e m p e r a t u r e . T h i s v i e w i s s u p p o r t e d b y l a b o r a t o r y e x p e r i m e n t s

a n d f i e ld o b s e r v a t i o n s w h i c h s h o w t h a t th e i m m u n e r e s p o n s e o f t e le o s t fi sh

t o h e l m i n t h p a r a s it e s i s e n h a n c e d b y i n c r e a s e in t e m p e r a t u r e ( K e n n e d y a n d

H i n e , 1 9 6 9; K e n n e d y , 1 9 7 2 ; R a w s o n a n d R o g e r s , 1 9 7 2 a , b ; A v t o l i o n , 1 9 7 3 ;

S e c o m b e s a n d C h a p p e l l , 1 9 9 6 ; B e r n s t e i n et al . 1998) . The f ac t tha t t e l eos t

f i s h a r e h i g h l y c o m p e t e n t i m m u n o l o g i c a l l y b o t h i n i n n a t e i m m u n i t y a n d i n

t h e e x p r e ss i o n o f th e c o m b i n a t o r i a l i m m u n e s y s t e m m a y h a v e b e e n u n d e r-

e s t i m a t e d i n th e p a s t ( B e r n s te i n et a l . 1998) . Thus , C hu bb (198 0) s t a t ed tha t

i t s e e m s u n l i k e l y t h a t th e i m m u n e r e a c t i o n o n t h e p a r t o f th e f i sh h o s t p l a y s

a n y s i g n if i c a n t s e a s o n a l r o l e i n t h e s e a s o n a l d y n a m i c s o f la r v a l p a r a s i t e s .

H o w e v e r , o n e w e a k n e s s i n t h e f is h a r m o u r y i s t h a t th e r e j e c t i o n t i m e o f p a r -

a s i t e s i s m u c h l o n g e r a t l o w e r a m b i e n t t e m p e r a t u r e t h a n i s t h e c a s e w i t h

m a m m a l s .

S e a s o n a l c h a n g e s i n t h e h o s t m e t a b o l i s m a n d d i e t m a y a l s o b e i m p o r t a n t

f ac to r s in in f luenc ing s easona l changes in pa ras i t e abundance . E l l io t t (1994)

has sh ow n tha t the m etabo l i c r a t e and the tu rnover o f food in the a l imen ta ry

cana l o f b row n t rou t inc rease w i th t empera tu re and tha t 1 3 -14 °C i s the op t i-

m a l t emp era tu re r ange fo r g rowth . I t i s pos s ib le the re fo re tha t the more m ob i le

in tes t inal paras i tes such as C . m e t o e c u s a n d C . fa r i o n i s w h i c h l a c k s t r o n g

adhes ive s t ruc tu res w i l l be more r ead i ly eges ted when the t empera tu res a r e

h igh in the sum mer . C i r cums tan t i a l ev idence in suppo r t o f th is hypo th es i s i s

p r o v i d e d b y t h e f a c t th a t N. ruti l i which i s a rmed w i th a p robosc i s tha t pene-

t r a tes in to the in tes tina l wa l l , does no t exh ib i t a ma rked sum m er t rough in i t s

a b u n d a n c e u n l i k e t h e C r e p i d o s t o m u m spec ies . The dec l ine in f eed ing r a te

d u r in g t h e s p a w n i n g p e r i o d m a y a l s o i n fl u e n c e p a r as i te a b u n d a n c e . M o r a v e c

(1994) has sugges ted tha t th i s may be r espons ib le fo r the lo s s o f the au tumn

g e n e r a t i o n o f C y s t i d i c o l o i d e s t e n u i s s i m a a n d a d e c l i n e i n a b u n d a n c e o f

R a p h i d a s c a r i s a c u s in t rout in the autumn and winter .

O l d e r w o r k e r s h a v e i n v o k e d c y c l i c a l c h a n g e s i n d i e t a ri e s t o e x p l a i n c y c l i -

c a l c h a n g e s i n th e p r e v a l e n c e a n d a b u n d a n c e o f p a ra s i te s i n c l u d in g

E c h i n o r h y n c h u s t r u tt a e in trou t (Awach ie , 1965) and P o d o c o t y l e sp . in f loun -

d e r s ( M a c K e n z i e a n d G i b s o n , 1 9 7 0 ) . M o r e r e c e n t l y , P i e t r o c k et al . (1999)

a l s o c o n c l u d e d t h a t t h e c y c l i c a l c h a n g e s i n a b u n d a n c e o f P f o l i u m in the

ru f f e was c aused b y d ie t r a the r than b y the annua l t em pera tu re cyc les a lthough

the l a t te r was co r re la ted w i th it . Th i s co nc lus ion w as based on the obse rva t ion

tha t a l though the in fec t ive s t ages were ava i l ab le th roughou t the yea r the s ea -

s o n a l c y c l e s i n a b u n d a n c e o f P. fo l i um w a s o n l y o b s e r v e d i n th e r u f f e a n d n o t

in the o the r hos t , the b lue b ream. T he m os t p laus ib le r eason fo r th is d i f f e rence

i s th a t t h e r u f fe i n g e s t e d m o r e o f th e i n t e r m e d i a t e h o s t s t h a n t h e b l u e b r e a m

d u r in g t h e s p ri n g a n d s u m m e r . P r o l o n g e d p e r i o d s o f f a s ti n g m a y a l s o h a v e a

m a j o r i m p a c t o n p a r a s i t e a b u n d a n c e . T h u s , a c c o r d i n g t o D o g i e l ( 1 9 6 1 ) t h e




catf ish, Siluris glanis, loses i t s in tes tina l paras it es in the win ter , excep t fo r

s co l eces o f Proteocephalus, becaus e i t does no t f eed a t t hi s ti me . K enne dy

1972) a l s o f ound t ha t t he r a t e o f l os s o f pa r as i te s i nc r eas ed u nde r con d i t ions

of hos t s ta rva tion . The fac t tha t the Eu ropean ee l

Anguilla anguilla

a l so ceases

t o f eed i n the w i n t e r w h en t he t emp er a t u r e f a ll s be l ow 9 - 1 0 ° C T hom as ,

1962) m ay be pa r t l y r e s pons i b l e fo r i ts depaupe r a t e f auna K e nne dy and

Gutgan , 1996) .

The re a re a l so m any o ther exam ples , c i t ed by Chub b 1977 , 1979 , 1980 ,

1982), in w hich ma tura t ion a nd reprod uct ive ac t iv i ty of the h e lm in th paras it es

and the i r hos t f ish a re synchronised . Th e se lec tive advan tage of such syn chro-

nous behaviour a re apparen t in the case of paras i t es where t r ansmiss ion i s

d i rec t as the hos t f i sh aggrega te dur ing spaw ning thus grea t ly increas ing the

probabi li ty o f success fu l t ransmission . Exam ples a re provided by mo noge net ic

t r ema t odes s uch a s

Dactylogyrus vastator

in carp and

Mazocraes alosae

in

s had . W her e i n t e r med i a t e hos t s a r e i nvo l ved i n t r ans mi s s i on t he s e l ec ti ve

advantages o f sync hron y are l ess obvious . How ever , i t can be pos tu la ted tha t

t he r e l ea se o f eggs by t he pa r a s it e du r i ng r edd f o r ma t i on by s a lmon i ds m ay

i n c r e a s e t h e p r o b a b i l i t y o f s e d i m e n t - d w e l l i n g i n t e r m e d i a t e h o s t s b e i n g

i n f ec t ed . T h i s may be t he ca s e w i t h Echinorhynchus salmonis, Philonema

agubernaculum

a n d

Philonema onchorhynchi

w h e n t h e i r s a l m o n i d h o s t s

Onchorhynchus tshawytscha, Salmo salar and Onchorhynchus nerka,

r espec-

t ively, are spaw ning. The re is a lso evide nce that ma turat ion and e gg produ ct ion

o f

C. truttae are

s ynch r on i s ed w i th t he ons e t o f s paw n i ng ac t iv i ty by t he hos t

f ish at least in Lampetra species M oravec, 1994) . As the adul t lam prey s spawn

in microhab i ta ts a l r eady occu pied by the prev ious gen era t ions of la rva l l am-

preys w hich a re the in te rm edia te hos t s th is w ould b e se lec t ive ly advantageous .

In th i s conn ec t ion i t would a l so be o f in te res t to ascer ta in wh ethe r ov ipos i t ion

by P. simile mi gh t be s ynch r on i s ed w i t h r edd f o r ma t i on and s paw n i ng by t rou t

a s t h is w ou l d i nc r eas e t he p r obab i l i ty o f t he s ed i m en t - dw e l l i ng , sphae r i id

in te rm edia te hos t s becom ing in fec ted .

O t he r ca s e s o f s yn ch r ony be t w een hos t m a t u ra t ion on t he one h and and pa r -

as i t e m atura t ion e .g ., Caryophyllaeus laticeps in Leuciscus leuciscus,

Pro teoceph alus filicollis in Gasterosteus aculeatus and Triaenophorus crassus

in Esox lucius , r ap i d g r ow t h e . g ., Camallanus oxycephalus in Morone

chrysops , incre ased suscep t ibi l ity to infect io n e .g ., Archigetes iowensis in

Cyprinus carpio on t he o t he r ma y a l s o be l i nked t o a l ow er ed hos t im m un i t y

Chub b, 1979,1980, 1982) . Picke r ing and Pot t inger 1987) pro vide evid enc e in

s upport o f t h is hypo t hes i s a s t hey f ound ma r ked r educ t ions i n t he nu m ber o f

c i rcu l a ti ng l ymph ocy t e s in t he b l ood o f s exua l ly m a t u r e ma l e and f em a l e t rou t

dur ing the spawning season . This e f fec t was a t t r ibu ted to cor t i so l suppression

of lym pho ida l ac t iv i ty . Cor t iso l appears to in f lue nce reproduc t ion by sens it is -

ing the gonad s to s t e ro ids and ind i rec t ly by regula t ing me tabol i sm. P icke t ing

and Po t t inger 1987) have sugg es ted tha t the cos t s o f increased suscept ib i l ity



42 J D THOMAS

to disease resulting from this mechanism may have contributed to the evolution

of semelparity in some salmonid species. Moiler (1997) has discussed both

cost and benefits of reproductive suppression of immunity, which is a common

feature in all vertebrates, and suggests that parental suppression of the immune

system is a necessary cost that has to be incurred to allow successful oogene-

sis and reproduction.

The above discussion makes it possible to formulate a unifying hypothesis,

based on evolutionary considerations, to account for the seasonal cycles in the

prevalence and abundance of univoltine parasites such as C m e t o e c u s and C.

f a r i o n i s During the summer months it can be postulated that it will be the adult

stages of helminth parasites, inhabiting the gut of fish, which will be under

greatest threat as a result of the enhanced immunity and the increased turnover

rate of the gut contents. Parasites with relatively poorly developed adhesive

structures will be particularly vulnerable. In contrast, the larval stages in the

immunologically and metabolically benign intermediate hosts will be under

less intense selective pressure and therefore have a higher survival rate than the

adults in the summer months. The summer would therefore be the opportune

time for the parasites to leave the definitive host and concentrate their repro-

ductive efforts in their invertebrate intermediate hosts. However, with the onset

of autumn the gut environment of salmonids and other autumn spawning fish

become more favourable because of a lowering of host immunity and gut

turnover rates as a result of the onset of reproductive activity and a fall in meta-

bolic rate, respectively. Late autumn would therefore be the optimal time for

the more vulnerable parasites to reinvade the gut environment. As the parasites

are poikilotherms the ambient temperature will influence their growth and

reproduction. On evolutionary grounds it might be expected therefore that

somatic growth and reproductive output of both the definitive host and para-

sites would increase in parallel with the rise in temperature in spring. The

predictions based on this model are in accord with the observed cyclical

patterns.

A corollary to this hypothesis is that the parasites will use predictive signals

to activate the appropriate genes. One possibility is that the parasites may use

a rise in temperature to trigger enhanced reproductive activity prior to death.

However, as temperatures fluctuate a great deal it may prove to be an unreli-

able signal. A more reliable signal is provided by changes in photoperiod,

possibly modulated by seasonal changes in temperature, and it is for this

reason that the majority of organisms in the temperate zone have evolved

mechanisms to use it as the key predictive signal. However, as this appears to

be unavailable to gut parasites it seems plausible, as suggested by Forbes

e t a l

(1989), that they might use the seasonal changes in the host s metabolism,

endocrine or immune mechanisms instead. There is empirical evidence that

parasites use seasonal changes in the host s endocrine cycle, which are set by

changes in photoperiod and modulated by temperature, as a reliable predictive




s igna l to s e t the i r annua l r ep roduc t ive cyc le Kearn , 1998). O ne o f the bes t

e x a m p l e s o f a p a r a si te a d a p ti n g p h y s i o l o g i c a l ly to a n a r r o w w i n d o w o f o p p o r -

tun i ty fo r t r ansmis s ion i s p rov ided by

P o l y s t o m a i n t e g e r r i m u m .

This pa ras i t e

uses the endocr ine m echan i sm o f i ts host , the co m m on f rog , to t rigger egg p ro -

duc t ion thus a l low ing i t to synchron i se ov ipos i t ion w i th i ts hos t when the f rog

en te r s the wa te r to ov ipo s i t Kearn , 1998) . I t m us t be con c lud ed the re fo re tha t

t h e p r e s e n t h y p o t h e s i s i s a t v a r i a n c e w i t h t h e s u g g e s t i o n o f V e r b e r n g a n d

V e r n b e r n g 1 9 7 4 ) th a t t h e t h e r m a l t o l e r a n c e s o f t r e m a t o d e s s h o u l d a g r e e

c lose ly w i th tha t o f the i r r e spec t ive hos t s .

Fur the r r e sea rch i s neede d to t e s t th is hypo thes i s wh ich foc uses on pa ras i te s

t h a t b e c o m e g r a v i d in s p ri n g a n d e a rl y su m m e r . C h u b b 1 9 8 2 ) i n c lu d e d t h r e e

o the r ca tegor ies o f l i fe h i s to ry st ra teg ies : 1 ) g rav id in l a te sp r ing - sum m er ; 2 )

g r a v i d f r o m s p ri n g to a u t u m n d u r i n g t h e w a r m e r m o n t h s o f th e y e a r; a n d 3 )

g r a v i d t h r o u g h o u t t h e y e a r a l t h o u g h p e a k e g g o r l a r v a l p r o d u c t i o n o c c u r s

d u r in g t h e w a r m e r s e a s o n . M o d e l s d e s i g n e d t o a c c o u n t f o r t h e s e d if f e r e n c e s

wi l l have to t ake in to accoun t s easona l changes in c l ima te , the l i f e h i s to ry

s t ra teg ies o f bo th the pa ras i te s and hos t s , and in pa r t i cu la r the t ime o f spaw n-

ing o f the d ef in i t ive f i sh hos ts .

4 . 2 . 3 . Water chemi s t r y

I t can be hypo thes i s ed that the spe c ies r i chnes s and abundance o f he lmin th pa r -

a s it e c o m m u n i t i e s i n f r e s h w a t e r f i s h w o u l d b e p o s i ti v e l y c o r re l a te d w i t h t h e

n u t r i e n t s t a t u s o f t h e w a t e r b o d i e s , a s m e a s u r e d b y p H , c o n d u c t i v i t y , b a s e

ca t ion and mic ronu t r i en t concen t r a t ions , up to c r i ti ca l th resho lds F igu re 1 ).

T h i s h y p o t h e s is , w h i c h w a s t e st e d b y r e fe r e n c e t o c o m m o n l y u s e d m e a s u r e s o f

com m un i ty s t ruc tu re , i s suppo r ted by the r esu lt s . Thus , a com par i son o f the

h e l m i n t h p a r a s i te c o m m u n i t i e s o f t ro u t i n th e R i v e r T e if i a n d P y s g o t w r s h o w s

t h a t t h e s p e c i e s r i c h n e s s a n d t h e S h a n n o n - W i e n e r a n d B r i l lo u i n d i v e r s i ty

i n d i c e s a r e m u c h h i g h e r i n t h e fo r m e r c a s e T a b l e 1 4). In c o n t ra s t , t h e

B e r g e r - P a r k e r i n d e x , w h i c h p r o v i d e s a m e a s u r e o f t h e re l a ti v e a b u n d a n c e o f

t h e d o m i n a n t s p e c i es , i s h i g h e r f o r t h e h e l m i n th c o m m u n i t y i n t h e P y s g o t w r

than i s the ca se in the Te if i. A l though bo th r ive r s a r e o l igo t roph ic o r nu t r i en t

poor the pH , conduc t iv i ty , base ca t ion and mic ronu t r i en t concen t r a t ions a re

m uch low er in the Py sgo tw r than the Te i f i Tab le 1 ).

O t h e r w o r k e r s h a v e a l s o f o u n d t h a t w a t e r c h e m i s t r y c a n b e a m a j o r f a c t o r

in in f luenc ing the d i s tr ibu t ion and abun danc e o f he lm in th pa ras i t e s in fi sh .

T h u s , C o n e

et a l .

1 9 9 3 ) f o u n d t h a t t h e p a ra s i te c o m m u n i t i e s i n th e A m e r i c a n

eel ,

A n g u i l l a r o s t r a t a

i n h a b i ti n g a c i d i c w a t e r s p H 4 . 5 - 5 . 0 ) w e r e c h a r a c -

t e r is e d b y t h e a b s e n c e o f d i g e n e t i c t re m a t o d e s , l o w e r s p e c i e s r i c h n e s s a n d

f e w e r m u l t i p l e i n f e c t i o n s c o m p a r e d w i t h t h o s e i n l e s s a c i d i c l i m e d w a t e r s .

K e n n e d y et a l . 1 9 9 4 ) a n d Y e o m a n s et a l . 1 9 9 6 ) a l s o f o u n d t h a t i n c r e a s e d



44 J D THOM AS

Table 14 Community structure indices for the helminth parasites of brown trout and

salmon parr in two river systems in West Wales

St~ion

Stat. A Sta t.B Stat .B Stat .D S ta t.A Stat.B

Fish species Trout Trout

Year 1950 1950

No. fish examined 209 685

No. helminth species 10 9

No. autogenicspecies 8 8

No. allogenic species 1 0

Component population

Dominantspecies CM CM

Berger-Parker index 0.449 0.542

Slope 'a ' of geometric series -0.485 -0.356

Simpson diversity ndex (I/D) 2.806 2.565

Shannon-Wiener ndex (H) 1.690 1.607

Equitability ndex (H/Hmax) 0.602 0.622

Brillouin's index (BI) 1.166 1.119

BI max 1.942 1.781

BI equitability ndex 0.600 0.628

Infrapopulation

Mean no. parasite spp.per fish

( ± S.D.)

Maximum no. parasite spp.

Mean no. individualhelminths

(± S.D.).

Fish with no parasites

Fish with 1 parasite sp.

Fish with 2 parasite spp.





Mean B.I. _+ S.D. (all fish)

Mean B.I. ± S.D. (infectedfish)

Maximum BI

Trout Trout S. parr S.parr

1998 1950 1950 1950

18 269 15 273

5 4 5 5

5 4 6 6

0 0 0 0

NR CM NR NR

0.889 0. 973 0. 92 5 0.825

-0.678 -0.934 -0.442 -0.571

1.258 1.055 1 .167 1.441

0.639 0. 205 0. 51 8 0.966

0.319 0. 10 2 0. 223 0.416

0.417 0. 14 2 0.32 6 0.634

1.346 1 .384 1.555 1.595

0.310 0. 10 3 0.2 10 0.397

2.74± 3.07 -+ 1.50± 1.14± 1.33± 1.34±

1.03 1.24 0.82 0.04 0.64 0.93

5 6 3 4 2 4

33.60± 34.52± 12.37 24.27 12.47 10.50

31.3 31.7 ± 10.0 ± 11.7 ± 14.0 ± 10.1

0.96 1.31 6.25 15.24 13.33 14.29

9.57 8.91 50.0 58.36 60.0 51.28

29.67 22. 77 31. 25 23.7 9 13. 33 23.08

39.23 29.78 125 2.23 13.33 8.42

15.31 24.23 0 0.37 0 2.93

5.26 11.39

1 61

0.557 0.6 02 0.10 9 0.066 0.1 32 0.142

_+0.319 ±0.322 ±0 .204 ±0.134 -+0.245 ±0.232

0.562 0.611 0 .12 4 0.0 78 0.1 52 0.165

±0.316 _+0.316 -+0.242 _+0.142 ±0.258 ±0.242

1.328 1.3 36 0. 793 0. 64 3 0. 68 7 0.994

CM = C metoecus; NR= N rutili

levels of eutrophication were accompanied by population increases in fish

parasites such as L i g u l a and trichodinids, respectively.

The t endency for the richness and diversity of helminth parasite co mmu ni-

ties to be positively correlated with the nutrient status of water bodies is

attributabl e to the fact that the latter favours a corres pondi ng en han ce me nt in




benthic invertebrates, zoo plankton and fish that m ay serve as intermediate or

definitive hosts M oss, 1988). T here is a great deal of cum ulative evidence that

the distr ibution and abundance of molluscs, which are obligatory hosts to

digenetic trematodes, and crustacea, w hich are often hosts to digenetic trema-

todes, cestodes, acanthocephala and nematodes, are strongly correlated with

pH and associated bas e cation concentration Okland, 1990). As so m e sphaeri-

ids such as Pisidium species are m ore tolerant to low pH condit ions than other

mo lluscs Ok land and Okland, 1986; Okland,1 990) this helps to explain the

preponderance of Crepidostomum species in trout inhabiting acidic waters.

However, due to the complexity of the interactions between the physico-

chemical interactions it is not surprising that the relationship between trophic

state and species richness is not always clear-cut. Thus, Ch ubb 1964, 1970)

found that the species r ichness of helminth f ish paras i tes was 14 for

mesotrophic Llyn Tegid compared wi th 16 for o l igotrophic Llyn Padarn.

Wisniew ski 1958) and Esch 1971) also found that the species r ichness of

helminth parasites o f fish was higher in oligotrophic than in eutrophic w aters

although the latter had prop ortionately m ore allogenic sp ecies than the former.

As the trophic status of water continues to increase from oligotrophic to hyper-

eutrophic i t is to be expected that the species r ichness of helminth parasite

com mu nities in part icular f ish species would reach an optim um level. As the

communities of helminth parasites of salmonid and coregonid f ish and their

intermediate h osts have evolve d in oligotrophic waters the y are generally intol-

erant of eutrophic conditions. I t wo uld be predicted therefore that the optimum

species r ichness for these helminth communit ies would precede those for

percid and cyprinid fish on the trophic scale as the latter are more tolerant of

eutrophication and better adapted to lentic conditions.

5 THE RELATIONSHIPS BETWEEN PARASITE AB UN DA NC E AN D

THE AGE AN D SIZE OF THE FISH HOSTS

5 1 Qua ntitative Data

There are strong, statistically significant tendencies for the mean abundanc e of

parasites to increase with the length and w eight of the brown trout Table 15).

The F values indicate that these relationships are particularly strong in the case

of the nematodes. In contrast to the trout the relat ionships b etw een the size of

the salmon parr and the mean abun dance of parasites wer e less clear Table

16). Thus, there were statistically significant tendencies for the mean abun-

dance of

D. sagittata C. meto ecus

and

C. farion is

to increase w ith the length

of the salmo n parr P < 0.05, < 0.05 and < 0.002, respectively). How ever, there

were n o stat ist ically significant relat ionships b etw een the mean abundance of



46 J D THOMAS

Table 15

The regress ion equa t ions sh owing the rela t ionsh ips be twe en the t ransformed

num ber of parasi tes { Og l0 1 +x)} and log e In) of the length cm) and log e hi) weight of the

trout g)

Regres s ion equa t ions F P

N u m b e r s t r. ) o fD .

sagittata

= -1 .46 + 0.575 In leng th 104.55 < 0.001

N u m b e r s t r. ) o f C far ionus = -0 . 83 4 + 0 .353 In leng th 39 .57 < 0 .001

N u m b e r s t r. ) o f C metoecus = -2.3 1 + 1.51 In leng th 65.11 < 0.001

Nu mbe rs t r .) o f P. simile = -1 .64 + 0.642 In leng th 92.88 < 0.001

N u m b e r s t r. ) o fN .

rutili

= -3 .90 + 1.85 In len gth 165.33 < 0.001

Num ber s t r .) o f nem atod es = -7 . 20 + 2 .78 in leng th 759 .51 < 0 .001

N u m b e r s t r. ) o fD .

ditremum

= -0 . 036 + 0 .013 In leng th 3 .87 < 0 .049

Num ber s t r ) o f a l l pa ras i tes = -17 .3 + 7 .71 In leng th 698 .19 < 0 .001

N u m b e r s t r. ) o f

D sagittata

= -0 .58 7 + 0.191 In wei ght 96.95 < 0.001

N u m b e r s t r. ) o f C far ionus = -0 .29 1 + 0 .116 In weigh t 35 .53 < 0 .001

Nu mb er s Ix.) of C metoecus = -0 . 275 + 0 .432 In weig h t 44 .05 < 0 .001

Num ber s t r .) o f P. simile = -0 .6 95 + 0 .220 In weig h t 91 .47 < 0 .001

N u m b e r s t r. ) o f N rutili = -1 .36 0 + 0 .680 In weigh t 191 .20 < 0 .001

Num ber s t r .) o f nem atod es = -3 . 16 + 0 .965 In weigh t 776 .49 < 0 .001

N u m b e r s t r. ) o f D ditremum = -0 .0 13 + 0 .004 In weig h t 2 .70 < 0 .100

Num ber s t r .) o f a l l pa ras i tes = -5 . 82 + 2 .600 In weig h t 652 .84 < 0 .000

Table 16 The regress ion equa t ions showing the re la t ionsh ips be tween the t ransformed

nu mb er o f parasi tes { og10 1 +x) } and log e In) of the leng th cm) and log e In) weight o f the

sa lmon par r g )

Regres s ion equa t ions F P

N u m b e r s t r. ) o fD . sagittata = - 0 .352 + 0.147 In len gth

N u m b e r s t r. ) o f C far ionis = - 0 .942 + 0.423 In leng th


C metoecus

= -2.9 1 + 1.26 In len gth

N u m b e r s t r . )

ofN ru t i l i

= 0.351 - 0 .700 In leng th

Num ber s t r .) o f nem atod es = - 0 .502 + 0 .273 In leng th

Num ber s t r .) o f al l pa ras i tes = 0 .572 + 0 .105 In leng th

N u m b e r s t r. ) o fD . sagittata = - 0 .127 + 0.046 In wei ght

N u m b e r s t r. ) o f C far ionis = -0 . 1 2 8 + 0 . 0 8 0 In w e ig h t


C metoecus

= 0.143 + 0.047 In weight

Numbers t r . ) ofN ru t i l i = 2.43 - 0 .21 6 In wei ght

Nu mbe rs t r .) o f nem ato des = 0 .293 - 0 .032 In weigh t

Nu mbe rs t r .) o f a l l pa ras i tes = 0 .978 - 0 .044 In weig h t

3.99

4 .35

9 .98

1 68

0 .89

0 .13

3.52

1 39

0 .12

0.93

0.11

0.21

0 .047

0 .038

0 .002

0 .299

0 .347

0 .718

0.061

0 .239

0.731

0.335

0 .738

0.651




1

9

8O

7

6

4

3

2

1

D S C F C M P S

N R N E M A L L P

D Y E A R

E ] Y E A R 2

Y E A R 3

• Y E A R 4

B Y E A R 5

I I Y E A R 6

F i g u r e 1 0

The relationship between the percentage prevalence of the dominant par-

asites and the age of the trout. DS,

D.sagittata;

CF,

C. farion is;

CM,

C. metoecus;

PS, P.

simile;

NR,

N. rutili;

NEM, nematodes;ALLP,all parasites.

N. ru t i l i

nematodes and the total parasites and the length of the salmon parr

(Table 16). Neither were there any statistically significant relationships

between the mean abundance of any of the parasite species and the weight of

the salmon parr (Table 16). In contrast there were non-significant tendencies

for the mean abundance of

N. rut i l i

and nematodes to decrease with increase in

length or weight of the salmon parr (Table 16).

The percentage prevalence values for

D. sag i t ta ta C . me toecus and C . f a r io -

nis P. s im ile

and nematodes in trout tend to increase with the age of the host

(Figure 10). However, in the cases of

C . m e t o e c u s a n d C . f a r io n i s

there is a ten-

dency for the values to reach an asymptote from age 3 years onwards. In contrast,

the percentage prevalence values for N. rut i l i tend not to increase with the age of

the trout. All the trout of 4 years and over were infected with one or more para-

site species and the prevalence values for 1-3-year-old trout were over 90 .

Table 17 shows that, with the exception ofN.

ru t i li and D. d i t r em um

there

were highly significant statistical tendencies for the mean abundance of all the

parasite species to increase with the age of the trout (P < 0.001 in all cases).

These trends (Figure 11) show however that there were tendencies for the

mean abundance of the parasite species to reach asymptotic values from the

age of 3 years onward. The only exceptions to this rule

are D. d i t r em um

prob-

ably due to inadequate data, and the nematodes, where the mean abundance

continues to increase up to the age of 5 years.

The prevalence data for the parasites of the salmon parr (Figure 12) show

similar trends with those observed in the trout. Thus, the prevalence values for

all the parasites tend to increase with age. However,

N. ru t i l i

and

C . fa r i o n i s

provide exceptions to this rule as their mean abundances do not increase sig-

nificantly (P = 0.213 and 0.074 respectively) with the age of the salmon parr

(Table 17). The tendencies for the mean abundance to increase with age are



48 J D THOMAS

+

o

o

~ v

V

0

~o

0

~ O0

~ v

~ ~v

~ ~ v

E

~

~o ~

Z~v

oo

m..



E C O L O G Y O F F I S H P A R A S I T E S 4 9

O 4

E3

2

O

==

: E

I x

i i i i i i

I

3 4 5 6

A G E I N Y E A R S

¢n

z

o

o

O

z

i i ~ i p

2 3 4 5 0

A G E IN Y E A R S

o

o 6o

ILl

O

4o

O

20

O 0

z

1 -

i

1

i t i i i

2 3 4 5 6

A G E IN Y E A R S

,

o2 0

O

~ 0

O

z 1

t

i i i i i

1 3 4 5

A G E I N Y E A R S

6

O 0.03

LL 0 02

0

I

0

0 01

0 0 0

Z

t

i i i i i i

1 0 3 4 5 6

A G E I N Y E A R S

2

O 10

~ 0

O

z

T

i i i i i

1 2 3 4 5 5

A G E IN Y E A R S

o

O 35

kU

Z 2 5

J

O

~ 15

O 5

Z

T T

i i i i

3 4 5 6

A G E IN Y E A R S

5

7o

o~

o

I 2 I

i i i

3 4 5

A G E IN Y E A R S

F i gu r e

T h e r e l a t i o n s h i p b e t w e e n t h e p a r a s i t e a b u n d a n c e a n d t h e a g e o f t h e t r o u t



50 J D THOMAS

8 0

o

O

2

D S C F C M P S

P A R A S I T E S

N R N E M T O T P A R

F i g u r e 1 2 The relationship between the percentage prevalence of the dominantpar-

asites and the age of the salmon parr. DS,

D sagittata;

CF,

C far ion i s ;

CM,

C me t o e c u s ;

PS, P. simile; NR, N rutil i; NEM, nematodes;TOT.PAR., all parasites.

more marked in the cases of

C m e t o e c u s

and nematodes Figure 13 and Table

17). However, as N r u t i l i is the most abundant parasite in salmon parr the rela-

tionship between the intensity of total parasite infection and host age is only

statistically significant at P < 0.05.

The present results are in accord with the general rule that the relationship

between the age, or size, of fish and the prevalence or abundance of their

helminth parasites tend to be positive in most cases Bangham, 1944; Thomas,

1958b; Dogiel, 1961; Hicks and Threlfall, 1973; Cannon, 1972; Hine and

Kennedy, 1974; Zelmer and Arai, 1998; Zhokov, 1998).

5 2 C a u s a t i v e M e c h a n i s m s

The statistically significant tendencies for the prevalence or abundance of

most of the helmith parasites of trout to increase with size or age of the trout

may be attributable either to changes in feeding behaviour or to an increase in

available space and nutrients in the microhabitat of the parasite. The possi-

bility that the increase in parasite load with age is due to an increased

probability of ingesting infected intermediate hosts as a result of increased

food intake has been suggested by a number of previous workers Walkey,

1967; Hine and Kennedy, 1974; Muzzall, 1980; Amin, 1985). However, as the

trout age and increase in size their dietary and habitat preferences also change.

Thus, they select larger food items, become more piscivorous and tend to




spend more t ime in t ransmiss ion s i t e s as soc ia t ed w i t h depos i t ing sed iment

Th om as , 1962) . T hes e chang es f ur ther increase t he probabi l it y o f them

inge st ing in fect iv e larvae. T he particularly strong trend for nem atod e abun-

dance to increase w ith age can be attributed to the increased tenden cy o f the

trout to ingest m ore fi sh and am m oco ete larvae as they get o lder Tho m as,

1962) . F ish , inc luding m inn ow s and salmon ids , and larval lampreys are obl i -

gate intermediate hosts for

R . a cu s

and

C . t r u t t a e

respect ive ly . The lack o f a

s igni f icant re lat ionship between the age of trout and the abundance of N.

r u t i l i suggests that the probabi l i ty of ingest ing infect ive larvae i s approxi -

mat e ly t he same f or t rout o f a l l ages . In v i ew of t he pos i t ive corre la t ion

be t ween t he si ze o f t he prey and the s i ze o f the fi sh Thom as , 1962) i t s eems

• - e -

= 1 1 : :

3

1 0

o

i

1 o

I I I f I l

0 1 2 0 1 2

A G E O F S A L M O N P A R R A G E O F S A L M O N P A R R

4 ~

3 ~

2 - -

o

T

i i t

0 1 2

A G E O F ~ A L MO N P A R R

®

Z

o _

2 0

i

3

1 r i i

0 1 2 3

A G E O F S A L M O N P A R R

O

• T

i I t

0 1 2


3

~ < e o

o ~

O

- 1 5

I

t i i

0 1 2 3


F i g u r e 13 The relationship between the parasite abundance and the age o f the salmon

parr.



52 J D THOMAS

p r o b a b l e t h a t t h e y o u n g e r t r o u t b e c o m e i n f e c t e d b y i n g e st in g s m a l l e r o s t ra c o d

i n t e rm e d i a t e h o s t s w h i l e t h e o l d e r tr o u t b e c o m e i n f e c t e d b y i n g e s t in g l a rg e r

S i a l i s l a rvae wh ich inhab i t depos i t ing s ed imen t . D iverge nce in feed ing behav-

i o u r b e t w e e n d i f fe r e n t m o r p h s o f l ak e r e s i d e n t A r c t ic c h a r r S a l v e l i n u s

a l p i n u s )

o v e r a n e x t e n d e d p e r i o d o f ti m e h a s a l s o b e e n u s e d t o e x p l a i n d i v e r-

gence in the i r pa ras i t i c f auna (Cur t i s

e t a l . ,

1 9 9 5 ) . T h u s , m o r p h s f e e d i n g

p r e d o m i n a n t l y i n t h e l i m n e t i c z o n e w e r e i n f e c t e d m a i n l y w i t h c e s t o d e s

w h e r e a s b e n t h i c f e e d e r s w e r e m o r e h e a v i l y i n f e c t e d w i t h C . f a r i o n i s a n d

a c a n t h o c e p h a l a . H e l m i n t h o l o g i c a l c o n s i d e r a t i o n s m a y m a k e i t n e c e s s a r y t o

q u e s t i o n c o n v e n t i o n a l v i e w s re g a r d in g t h e f e e d i n g b e h a v i o u r o f h o s t f i sh

such as the ee l . Thus , 63 o f the spec ia l is t pa ras i t e s o f the Eu ropea n ee l

A n g u i l l a a n g u i l l a L. ) u se p lank ton ic in te rmed ia te h os t s a s do s evera l o f the

c o m m o n e r g e n e r a l i s t s p e c i e s ( K e n n e d y

e t a l .

1992) . As a r e su l t these au thor s

a r g u e t h a t t h e w i d e l y a c c e p t e d v i e w t h a t e e l s a r e e x c l u s i v e l y b e n t h i c f e e d e r s

requ i res r e inves t iga t ion . O ne pos s ib le exp lana t ion fo r th is apparen t an om aly

i s t h a t ' p l a n k t o n i c ' f o o d o r g a n i s m s a r e m u c h c o m m o n e r i n t h e i n te r st it ia l

spaces in the s ed imen ts o f lo t i c hab i ta t s than h i the r to be l i eved bu t tha t they

m a y h a v e b e e n o v e r l o o k e d d u r i n g t h e e x a m i n a t io n o f t h e s t o m a c h c o n t e n t s

b e c a u s e t h e y a r e s m a l l a n d e a s i l y d ig e s t e d .

T h e f a c t t h a t t h e r e l a t i o n s h i p s b e t w e e n t h e p r e v a l e n c e a n d a b u n d a n c e o f

he lmin th pa ras i t e s and the leng th , w e igh t and a ge o f the s a lm on par r a re le s s

c lea r -cu t than in the t rou t can be a t t r ibu ted to smal le r r anges in the l eng th ,

we igh t an d ag e o f the l a t te r spec ies . As a r e su l t i t i s to be exp ec te d tha t the re

w ou ld be l e s s va r ia t ion in the d ie t o f the s a lm on parr . Th i s hy po th es i s i s sup -

p o r t e d b y e m p i r i c a l e v i d e n c e ( T h o m a s , 1 9 6 2) . T h e f a c t th a t th e f e e d i n g

t e r r it o r i e s o f t h e s a l m o n p a r r o v e r l a p t o a g r e a t e r e x t e n t th a n t h e t r o u t

( A r m s t r o n g

e t a l . ,

1 9 9 9 ) w o u l d a l s o r e s u lt i n t h e d i e ta r i e s o f th e f o r m e r

spec ies be ing l e s s va r iab le . The r esu l t s ob ta ined b y H icks and Thre l f a l l (1973)

f o r s p e c i e s o f s a l m o n i d a n d c o r e g o n i d f i s h r e s e m b l e t h o s e f o r t r o u t a n d

sa lmon par r in the p resen t s tudy . Thus , they found tha t in the case o f s a lmon id

s p e c i e s o l d e r fi s h t e n d e d t o h a r b o u r m o r e p a r a s it e s t h a n y o u n g e r f i sh w h e r e a s

th i s was no t the case w i th pa ras it e s o f co reg on id f i sh . Th ey a l so a t t r ibu ted

these d i f f e rences to the f ac t tha t the d ie ta r i e s o f the co rego n id f i sh chan ge ve ry

l i t t l e w i th age un l ike the s a lmon id spec ies they had s tud ied . However , an

inc rease in d ie ta ry inpu t r e la ted to s i ze may no t be the on ly f ac to r in de te r -

m i n i n g p a r a s i t e a b u n d a n c e . T h e r e i s e v i d e n c e t h a t t h e a v a i l a b i l i t y o f

c o l o n i s i n g s p a c e m a y b e a k e y f a c t o r a s w e l l. T h u s P o u l i n

e t a l .

( 1 9 9 1 ) f o u n d

tha t the s i ze o f the b roo k t rou t,

S a l v e l i n u s f o n t i n a l i s ,

wa s pos i t ive ly co r re la ted

w i t h t h e n u m b e r o f a c q u i re d c o p e p o d s . I n c o n t r a s t th e r e w a s n o s t a t i st ic a l ly

s i g n i f i c a n t r e l a t i o n s h i p b e t w e e n t h e n u m b e r s o f c o p e p o d s a c q u i r e d a n d t h e

leve l o f ac t iv i ty o f the f i sh , the t ime spen t nea r the bo t tom o r the d i s t ance f rom

the pa ras i t e r e lea se s it e .

P o u l i n a n d V a l t o n e n ( 2 0 0 1 ) f o u n d t h a t w h e n t h e f i s h h o s t s a c c u m u l a t e




paras i te s in a p red ic tab le way , p ropor t iona l to the i r s ize , the pa ras i t e com m u-

n i t ie s con fo rm to a nes ted pa t t e rn . On the o the r hand , wh en f i sh hos t s do no t

accum ula te pa ras i t e s in a p red ic tab le way , p ropor t iona l to the i r s i ze , pos s ib ly

as a r e su l t o f d ie ta ry spec ia l i s a tion p reven t ing the m f rom sam pl ing av a i l ab le

paras i te species , the paras i te com m unit ie s exhib i t an ant i -nes ted pat tern . M eta-

a n a l y s i s c a r d e d o u t b y P o u l i n ( 2 0 0 0 ) o n 7 6 d i f f e r e n t h o s t - p a r a s i t e s p e c i e s

revea led tha t the overa l l m ean co r re la t ion be tw een f i sh leng th and the in tens i ty

o f pa ras i t e in fec t ions was weak ly pos i t ive bu t non- s ign i f i can t fo l lowing co r -

r ec t ions fo r s am ple s ize. T hese r esu l t s im p ly approx im ate equ a l i ty be tw een the

num bers o f nes ted and an t i -nes ted comm uni t i e s . I t i s no t su rp r is ing the re fo re

t h a t t h e r e a r e e x c e p t i o n s t o t h e r u l e t h a t t h e p r e v a l e n c e o r a b u n d a n c e o f

he lm in th pa ras i te s co r re la te pos i t ive ly w i th the age and s ize o f the f ish hos t s

(Dog ie l , 1961; K ennedy , 1968 ; Zh okh ov and Pugach eva , 1998 ; Pou l in , 2000) .

K e n n e d y ( 1 9 6 8 ) g i v e s a s p e c i f i c e x a m p l e . H e f o u n d t h a t t h e a b u n d a n c e o f

C a r y o p h y l l a e u s l a t i c e p s i n d a c e w a s i n d e p e n d e n t o f a ge , a s w a s t h e c a s e w i t h

N. ru t i l i in trou t in the p resen t s tudy . Th ese pa t t e rns m ay a l so b e exp la ined on

the bas i s o f d ie ta ry cons ide ra t ions . W hen the re a re p ro fo und cha nges in d ie t

w i th age as i s the case w i th the p ike ,

E s o x l u c i u s

t h e r e m a y b e c o n f l i c t i n g

t r ends . Thus , Dog ie l (1961) found tha t the p reva lence o r abundance o f 11

( 5 5 ) o f t h e 1 8 p a r a s i t e s in th i s f i sh in c r e a s e d w i t h a g e w h e r e a s 1 1

d e c r e a s e d w i t h a g e a n d 3 3 w e r e i n d e p e n d e n t o f a g e .

Chan ges in he lmin th f auna o f f i sh can a l so occur a s a r e su lt o f hab i ta t change

resu lt ing f rom migra t ion . T h is has been w e l l docum en ted in the case o f mig ra -

t o r y s a lm o n i d f is h b y D o g i e l ( 1 9 6 1 ) a n d M o l l o y

et a l .

(1993) . Ho wev er , no t a ll

the changes in he lmin th f aun a a re a t t r ibu tab le to change in d ie t. Thus , acco rd -

i n g t o P a l i n g ( 1 9 6 5 ) t r o u t i n L a k e W i n d e r m e r e b e c o m e i n f e c t e d w i t h t h e

m o n o g e n e t i c t re m a t o d e

D . s a g i t t a t a

on ly a f t e r mig ra ting in to the dee per wa te r

o f the l ake and you ng t rou t in nu r se ry s t reams a re un in fec ted . I t i s p robab le tha t

t h e a b s e n c e o f D. sag i t ta ta f rom the t rout in the feed er s t ream is a t t ributable to

the vu lne rab i l ity o f the onco mirac id ia in tu rbu len t wa te r s . Acc ord ing to Dog ie l

(1961) D a c t y l o g y r u s v a s t a t o r i s on ly found in you ng ca rp bec ause they a re p re -

dominan t ly su r face dwel le r s un l ike the adu l t s . The dec rease in p reva lence o f

G y r o d a c t y l u s r a r u s in s t ick lebacks w i th age (Kennedy , 1970) may b e a t t ribu t-

ab le to the shor t l i f e span o f the pa ras i t e and to cha nge s in hos t dens i ty ,

as soc ia ted w i th m atu ra t ion , a l though the invo lvem en t o f age r esi s tance canno t

be ru led out . In contras t , the larvae of D i p l o s t o m u m s p a t h e c u m which a l so

a t tach to the sk in o f the f i sh to ga in en t ry in to the bo dy t i s sues , have a long l i fe

span and as a r e su l t the ir m ean abundance shows a s t rong pos i t ive r e la tionsh ip

with the age of the f ish (Kennedy, 1970) . This sugges ts that th is paras i te does

l it tl e ha rm to the ir f ish hos t s a lthough Sec om bes and C happe l l (1996) p rov ide

ev idence to the con t ra ry .

T h e a l t e r n a t i v e e x p l a n a t i o n f o r t h e p o s i t i v e r e l a t i o n s h i p s b e t w e e n t h e

abu nda nce o f pa ras i t e s and the s i ze , o r age , o f f i sh l ike the t rou t i s tha t i t is



54 J D THOMAS

d u e t o h e l m i n t h p a r a s i t e s i n t r o u t b e i n g r e g u l a t e d i n a d e n s i t y - d e p e n d e n t

m anne r b y spa t ia l o r nu t r ien t l imi ta t ion . T he f ac t tha t the pa ras i te de ns i ty pe r

square m et re o f a l imen ta ry cana l r ema ins v i r tua l ly co ns tan t in 1 -, 2 - , 3 - and

4-ye ar -o ld t rou t (Tho m as , 1964a) suppo r t s th i s hyp o the s i s a s i t sugge s t s tha t

s p a c e o r n u t r i e n t a v a i l a b i l i t y m a y b e l i m i t i n g f a c t o r s . B r o w n ( 1 9 8 6 ) a l s o

f o u n d t h a t th e n u m b e r o f p a r a s i te s h a r b o u r e d w i t h in c r e a s i n g i n f e c t i o n

dosa ge r each ed a p la teau , p rop or t iona l to the l eng th o f the f ish , in l abora to ry -

m a i n t a i n e d r a i n b o w t r o ut . H e s u g g e s t e d t h a t t h is e f f e c t w a s d u e t o an

i n c r e a s e i n a b s o l u t e s u r f a c e a r e a a v a i l a b l e f o r a t t a c h m e n t w i t h i n c r e a s e i n

f i sh s i ze . Ac cord ing to A1-H ussa in i (194 9) the in tes tina l l eng th o f m any f i sh

s p e c i e s i n c re a s e s i n d i r e c t p r o p o r t io n t o b o d y l e n g t h a n d t h e a b s o l u t e s u r f a c e

a r e a a v a i l a b l e t o t h e p a r a s i te s f o r a t t a c h m e n t i n c r e a s e s a s t h e s q u a r e o f a n y

inc rea se in in tes tina l l eng th .

5 3 Eco log ica l Re levance and D ens i ty Dependence

The impor tan t ques t ion o f whe the r popu la t ions o f he lmin th pa ras i te s o f fi sh a re

r e g u l a te d i n a d e n s i t y - d e p e n d e n t m a n n e r a n d w h e t h e r t h e y c o n f o r m t o th e r

o r K s t ra teg ies has been w ide ly d i s cus se d (Kennedy , 1974 , 1977 ; H o lm es e t

a l .

1977; Esch

e t a l .

1977 ; Kennedy and Rumpus , 1977 ; F igu re 1 ) . In o rde r

to r eso lve th i s ques t ion en to m olog is t s and f i she ry b io log i s t s have r eso r ted to

us ing K fac to r ana lyses (E l l io t , 1994). Unfo r tuna te ly , the com plex i ty o f the

i n f ra p o p u l a ti o n , c o m p o n e n t p o p u l a t i o n a n d s u p r a p o p u l a t i o n s t ru c t u re s a n d

the p rob lems o f acqu i r ing l i f e t ab le da ta over s evera l yea r s has made i t ve ry

d i f f icu l t to use th i s approac h to r eso lve th is qu es t ion w i th ce r ta in ty in the case

o f he lm in th f i sh pa ras it e s .

W hen d i s cus s ing th i s ques t ion Ke nne dy (1977) , l ike m any o the r rev iewers ,

u s e d t h e B r a d l e y ( 1 9 7 4 ) c l a s s i f i c a t i o n a s a f r a m e w o r k f o r d i s c u s s i o n .

Ac cord ing to th i s c la s s if i ca t ion popu la t ions can theo re t i ca l ly be r egu la ted by :

(1 ) t r ansmis s ion ; (2 ) caus ing dea th o f the hos t ; (3 ) hos t im m uni ty o r p remuni -

t ion ; and (4) in t r aspec i f ic o r in te r spec ies com pet i t ion m ed ia ted by exp lo i ta t ion

o f r e s o u r c e s, i n t e r fe r e n c e o r b y e x p l o it a ti o n o f th e h o s t s i m m u n e r e s p o n se .

There i s a genera l consen sus tha t a lthough the t r ansmis s ion r a te can in f luence

popu la t ion s ize i t doe s no t ac t in a r egu la to ry manner . R egu la t ion b y pa ras i te -

induced hos t m or ta li ty appears on ly to occur com m only in na tu re w hen the fi sh

i s the in te rmed ia te h os t o f the pa ras it e (Kennedy , 1977). As the p reva lence and

a b u n d a n ce o f

D . d i t r e r n u m

p le roce rco ids wa s ex t r em ely low in the Te i fi trou t

a n d t h e r e w a s n o e v i d e n c e o f p a r a s i t e - i n d u c e d m o r t a l i t y t h e s e c o n d o f

Brad ley s op t ions can a l so be exc luded . Kennedy (1977) a l so exc luded bo th the

i m m u n e r e s p o n s e a n d i n te r sp e c i e s c o m p e t i t i o n f r o m i n v o l v e m e n t in t h e r e g u -

la tion o f pa ras i t e in f r apopu la t ions in f ish . I f these a s sum pt ions a re co r rec t th is

l eaves on ly in t r aspec ies com pet i t ion as a r egu la to ry mech an ism. A ccord ing to




K e n n e d y 1 9 7 7 ) th is m e c h a n i s m o p e r a te s b y c a u s in g a d e n s i t y -d e p e n d e n t

r e d u c t io n o f t h e n a t a li ty r a t e b u t h e c o n c l u d e d t h a t a s it is u n c o m m o n t h e

m ajo r i ty o f f i sh pa ras it e popu la t ions a re un regu la ted and h ence uns tab le . Esch

and Fernand es 1993) have a l so a rgued tha t the mor ta l i ty r a te o f pa ras i te s in

m os t f i sh l iv ing un der na tu ra l cond i t ions i s dens i ty independen t . Th i s op in ion

i s a l s o s h a r e d b y K e n n e d y e t a l 1986) and they cons ide r tha t in te r spec ies

com pet i t ion i s a f a r g rea te r s t ruc tu ring fo rce in the m ore d ive r se , spec ies - r ich

h e l m i n t h c o m m u n i t i e s in t h e a li m e n t a r y c a n a l s o f b i rd s a n d m a m m a l s t h a n i n

t h e c o m p a r a t i v e l y p o o r c o m m u n i t i e s o f f r e s h w a t e r fi sh . T h e s e v i e w s a r e r e m -

i n i sc e n t o f th o s e e x p r e s s e d b y A n d r e w a r t h a

e t a l

as they a l so pos tu la ted tha t

the popu la t ion s i ze o f som e f ree - l iv ing o rgan i sms such as thr ips and g ras shop-

per s a r e de te rmined b y non- s tab i l is ing f ac to r s R ick le f s , 1973) . As i t i s to be

expec ted tha t such popu la t ions wou ld dwind le to ex t inc t ion r a the r f r equen t ly

E h r l ic h a n d B i r c h 1 9 6 7 ) s u g g e s t e d t h e y c o u l d b e r e - e st a b l is h e d b y c o l o n i sa -

t ion f rom su r round ing sub-popu la t ions . Thus , popu la t ions cou ld be main ta ined

be lo w resource l imi ta tion th rough the ba lance o f loca l ex tinc t ion and r eco lon i -

s a ti on . H o w e v e r , a s p o i n t e d o u t b y R i c k l e f s 1 9 7 3 ) t h e te n d e n c y f o r t h e

p o p u l a t i o n s t o i n c r e a s e t h r o u g h c o l o n i s a t i o n i s d e n s i t y d e p e n d e n t a n d t h e

m o s a i c m o d e l d i f fe r s f ro m t h e c o n v e n t i o n a l d e n s it y - d e p e n d e n t m o d e l i n t h a t

the spa t i a l componen t s , immigra t ion and emigra t ion , r ep lace b i r th and dea th

ra tes , respect ively .

K e n n e d y a n d G u e g a n 1 9 9 6 ) a n d K e n n e d y a n d H a r t v i g s e n 2 0 0 0 ) h a v e

con t inued to h o ld the v iew tha t popu la t ion s i zes o f f ish pa ras i te s a r e de te rmined

b y n o n - s t a b i l i s i n g f a c t o r s o n t h e b a s i s o f t h e i r s t u d i e s o n t h e s t r u c t u r e o f

he lmin th communi t i e s in ee l s and t rou t . Accord ing to these au tho r s he lmin th

com m uni t i e s in bo th o f these spec ies a r e ve ry s imi la r and they cons ide r them to

be unsa tu ra ted s tochas ti c a s sem blages and i so la tion i s t in na tu re . Accord ing to

B u s h e t a l 1 9 9 7 ) th e u s e o f t h e te r m i s o la t io n i st c o m m u n i t y H o l m e s a nd

Pr ice , 1986) imp l ies tha t the communi t i e s a r e no t in equ i l ib r ium as they a re

unsatura ted due to lo w t ransmiss ion ra tes and that spec ies are indiv idual ist ica lly

d i spe r sed and insensi t ive to the p resence o f o the r gu i ld m em bers .

H o w e v e r , m o r e r e c e n t r e se a r c h f i n d in g s i n t h e f ie l d s o f i m m u n o l o g y a n d

p a r a s i t o l o g y m a k e i t n e c e s s a r y t o r e a s s e s s t h e v i e w s e x p r e s s e d b y K e n n e d y

1 9 7 7 ) a n d K e n n e d y a n d H a r t v i g s e n 2 0 0 0 ) . A l t h o u g h t h e e x i s te n c e o f a n

i m m u n e r e s p o n s e i n f is h h a s b e e n k n o w n f o r s o m e t im e i t i s p o s s i b l e th a t i ts

i m p o r t a n c e a s a r e g u la t o r y m e c h a n i s m h a s b e e n u n d e r e st im a t e d . K e n n e d y a n d

W a l k e r 1 9 6 9 ) s h o w e d t h at C a r y p h y l l a e u s l a t i c e p s i n d a c e w e r e r e j e c t e d a f te r

an in i t i a l pe r iod o f e s t ab l i shmen t . The f ac t tha t the pe r iod o f e s t ab l i shmen t

decreased and the speed o f re j ec t ion inc reased w i th a r i se in t em pera tu re i s sug -

g e s t i v e o f a n a n t i b o d y m e c h a n i s m o f r e s is t a n c e, a l t h o u g h a t t h e t im e t h e y

cou ld f ind no ev idence o f c i r cu la t ing an t ibod ies . However , in these ea r l i e r

s tud ies the use o f p rec ip i t a tion t ech n iques to d e tec t an t ibod ies was suspec t a s

f i sh on ly pos ses s IgM W i l son and War r, 1992). M ore r ecen t s tud ies, u s ing



5 6 J D T H O M A S

agg lu t ina tion and EL ISA as says , o r enum era t ion o f an t ibody -sec re t ing ce l l s,

a r e w i t h o u t s u c h c o n c e r n s a n d h a v e b e e n u s e d t o d e m o n s t r a t e a n t i b o d y p r o -

duc t ion in r espon se to in fes ta t ion by acan thocepha la , nem atodes , m onog enea ,

d igene a and ces tode s in f i sh Sec om bes and Chappe l l , 1996) . Howe ver , the re

wa s no co r re la t ion be twe en wo rm b urden and an t ibod y ti tr e.

P r o t e c t i v e i m m u n e r e s p o n s e s t o h e l m i n t h s h a v e b e e n d e m o n s t r a t e d i n a

n u m b e r o f c a s e s o f th e m o r e i n v a s iv e h e l m i n t h p a r a si te s i n c lu d i n g

Gyrodactylus salaris

and

D. spathecum

Sec om be s and Chappe l l , 1996) . I t has

bee n pos tu la ted tha t a s the gu t is re la t ive ly non-ag gres s ive imm uno log ica l ly a

s tab le r e la t ionsh ip wou ld be more l ike ly to deve lop in the case o f pa ras i t e s

inhab i t ing the gu t than in those inhab it ing t i s sue Sec om bes and Chappe l l ,

1996). Neve r the les s, the re is now accum ula t ing ev idence fo r the ex i s tence o f

int raepi thelial lym pho cyte s IEL) and lamina propr ia lym pho cyte s LP L) in the

te leos t gu t M cM il lan and S ecom bes , 1997) . These au thors sugges t tha t by fu r -

t h er in g o u r u n d e r s ta n d i n g o f th e b a s i c i m m u n o l o g y o f th e t e l e o s t g u t

in fo rmat ion w i l l u l t ima te ly be made ava i l ab le fo r op t imisa t ion o f o ra l vacc i -

na t ion r eg imens . Th is w ou ld invo lve ta rge ting the im m une ce l ls in the in tes t ine

fo r s t imu la t ion and the es tab l i shmen t o f m ucosa l , an t igen - spec i f i c an t ibody

responses bo th in the gu t m uco sa and sys temica l ly . I t m us t be conc luded the re -

f o r e t h a t a s f is h h a v e e v o l v e d so p h i s ti c a t ed i m m u n e m e c h a n i s m s S e c o m b e s

and C happe l l , 1996) th is m ay ena b le them to r egu la te the dens i ty o f he lmin th

paras i tes .

T h e r e i s a ls o a g r e a t d e a l o f a c c u m u l a ti n g e v i d e n c e , s u m m a r i s e d b e l o w ,

s u g g e s t i n g t h a t e x p l o i t a t i v e a n d i n t e r f e r e n c e c o m p e t i t i v e m e c h a n i s m s a n d

cros s imm uni ty m ay be m ore impor tan t in r egu la t ing he lmin th pa ras i te s o f f i sh

t h an w a s b e l ie v e d in t h e p a st . T h u s , B r o w n 1 9 8 6 ) s h o w e d th a t a s y m p t o t i c

leve ls were r eached w hen r a inbow t rou t were in fec ted w i th inc reasing n um bers

o f

Pomphorhynchus laevis.

H e the re fo re su gges ted tha t the d i r ec t re la t ionsh ip

b e t w e e n w o r m b u r d e n a n d t h e l e n g th o f th e f i sh h o s t w a s w h o l l y c o n s i s te n t

w i th the ac t ion o f den s i ty -depe nde n t p roces se s w i th in each f i sh s ize c lass .

Th is m echan ism , tog e the r w i th in te r spec i fi c compet i t ion , m ay a l so be r espon-

s ib le fo r the obse rved pos i t ive re la t ionsh ip be tw een f i sh s i ze and pa ras it e loa d

and fo r the a lmos t con s tan t pa ras it e den s i ty pe r square me t re obse rved in the

a l imen ta ry cana l o f t rou t Tho ma s , 1964a) . Dens i ty depend enc e r egu la t ion

due to spac e l imi ta t ion has a l so been invok ed to exp la in the dec l ine in num bers

o f

L. thecatus

in the g reen sunf i sh Uga nsk i and N icko l , 1982 ; Ew ald and

Nickol, 1989),

Pomphorhynchus laevis

in dace Kennedy , 1975)

and E. cras

sum

in t rout Ke nnedy , 1996) .

B a t e s a nd K e n n e d y 1 9 9 0 ) h a v e p r o d u c e d di r ec t e x p e r im e n t a l e v i d e n c e o f

a s y m m e t r i c a l i n te r s p e ci e s c o m p e t i ti o n o r a m m e n s a l i s m i n v o lv i n g


a n d

Acanthocephalus anguillae

i n r a i n b o w t r o u t in

w h i c h t h e l a t te r s p e c i e s w a s d i s a d v a n t a g e d b u t n o t t h e fo r m e r . S p a t i a l e x c l u -

s i o n o f h e l m i n t h s p e c i e s r e s u lt i n g f r o m a c t iv e s i t e s e le c t i o n b y t h e d o m i n a n t




com pe t i t o r has a l s o bee n r epo r t ed i n na t u r a l popu l a t i ons ( C happe l l , 1969;

W i l l i ams e t a l . 1987). T h e r e a r e a l so m any r epo r t s ( D og i e l , 1961; T hom as ,

1964a; Chappel , 1969; Whi t f i e ld , 1979; Kennedy , 1985; V ida l -Mar t inez

and K e nned y , 2000 ; K enn edy and H a r t v i g s en , 2000 ) o f s ign i f i can t nega t i ve

assoc ia t ion s involv in g pa i r s o f he lm in th paras i t es in f i sh hos t s . As a r esu l t ,

K e n n e d y ( 1 9 9 2 ) a n d V i d a l -M a r ti n e z a n d K e n n e d y ( 2 00 0 ) a p p e a r t o h a v e

m od i f i ed t he i r v i ew s r ecen t l y . T h ey now pos t u l a t e t ha t com pe t i t i ve i n t e r ac -

t i o n s m a y b e p o t e n t i a l d e t e r m i n a n t s o f c o m m u n i t y s t r u c t u r e e v e n i n t h e

l o w - d i v e r si t y h e l m i n t h c o m m u n i t i e s fo u n d i n f is h f r o m t h e t e m p e r a t e a n d

t r op i ca l zones , t hough i t i s no t ye t c l ea r t o w ha t ex t en t t h i s po t en t i a l i s

r ea l i s ed i n na t u r e . K ennedy and H ar t v i g s en ( 2000) have c i t ed ev i dence ,

b a s e d o n c o m m u n i t y s t r u c t u r e , s u g g e s t i n g t h a t e v e n t h e r e l a t i v e l y l o w -

d i v e r si ty h e l m i n t h c o m m u n i t i e s in t h e i n t e s ti n e s o f e e l s a n d t r o u t m a y b e

s a t u ra t ed . A cco r d i ng t o S r i vas tava ( 1999) s a t u r a ti on s ugg es t s t he ac t i on o f

i n t e r s pec i e s compe t i t i on . L i t t l e i s know n abou t t he na t u r e o f t he mecha -

n i s m s t h a t m i g h t b e i m p l i c a t e d in c a u s i n g t h e e f f e c t o b s e r v e d d u r i n g

i n t ra s pec i fi c com pe t i ti on . T h ey m ay i nc l ude exp l o i t a ti on o f r e s ou r ces , i n te r -

f e r e n c e a n d u s i n g t h e h o s t s i m m u n e r e s p o n s e t o t h e p a r a s it e s a d v a n t ag e .

B a t e s and K enn edy ( 1990) s ugge s t ed t ha t t he mos t t enab l e exp l ana t i on f o r

t h e e x c l u s io n o f A . a n g u i l l a e f r om t he gu t o f r a inbow t r ou t by P . l a e v i s w a s

t he dev e l opm en t o f a hos t - m ed i a t ed exc l u s i on zone a r ou nd i nd i v idua l s o f P.

l ae v i s . A s i mi la r exam pl e i s p r ov i ded by D a c t y l o g y r u s v a s t a t o r . This paras i te

induce s ce l lu la r reac t ions in the g i ll s o f the f i sh hos t wh ich prevent se t tl ement

by o ther spec ies (Ho lmes , 1973).

Al though there a re a l so many examples of pos i t ive as soc ia t ions (Rohde ,

1991; Dorocu e t a l . 1995) involving species o f helminth paras i tes these c an be

a t t r i bu t ed t o t he ove r l app i ng and ove r d i s pe r s ed na t u r e o f f avou r ab l e

t ransm iss ion s i tes. T his resul ts in an inc rease d proba bi l i ty of a f ish acqu ir ing

m ore than o ne spec ies o f parasi te a t the sam e t ime. I t i s impor tan t to r ea l ise

however tha t pos i t ive as soc ia t ions do no t p rec lude the poss ib i l i ty o f in te r -

spec ies comp et i t ion occur r ing .

T h e o c c u r r e n c e o f c h a r a c t e r d i s p l a c e m e n t a n d n i c h e d i v e rs if ic a t io n i n

coex i s t ing s pec i e s o f pa r a s it e s can be c i t ed a s c i r cums t an t i a l ev i dence f o r t he

ex i s t ence o f s t r ong s e l ec ti on p r e s s u re s d r i ven by i n t e r s pec i e s com pe t i t i on

(Tho m as , 1958a; M acK enz ie and Gibson , 1970; W hi t f ie ld , 1979). On the

o ther hand , th e ex i s tence of n iche d iver s if i ca tion and the res t r i c t ion o f spec ies

to prefer red s i tes has a l so been c i t ed as ev ide nce tha t in te r spec ies com pet i t ion

se ldo m occu rs in na ture (K enned y , 1974) . Ho wever , a l though chara c te r d i s -

p l a c e m e n t a n d c o m p e t i t i o n n i c h e d i v e r s i f i c a t i o n w i l l c l e a r l y r e d u c e t h e

in tens i ty of in te r spec ies com pet i t ion th i s does n o t ex c lude the poss ib i l ity tha t

i t ma y occu r . Fu r t he r r e s ea r ch is c l ea r l y nee ded t o a s ce r ta i n t he ex t en t t o

w h i ch i n t e rs pec i e s compe t i t i on be t w een he l m i n t h pa ra s it e s o f f i s h ma y ac t a s

a dens i t y r egu l a t o r y m ech an i s m and t o a s ce r t a in t he caus a t i ve mechan i s ms .



58 J D THOMAS

The above evidence suggests that the use of the word isolationist to describe

populations of helminth parasites in trout in the Teifi is unjustified. It would

appear, to the contrary, that the helminth parasites of the Teifi trout conform to

the term interactive community (Holmes and Price, 1986). This term was

coined to characterise a community that fits the assumptions of the competition

hypothesis at the infracommunity level. These include the assumptions that the

parasites have a high transmission rate, that host immunity and interspecies

competition may act in a density-dependent manner and that communities are

in equilibrium. Bush e t a l . (1997) concluded that care should be taken in the

use of the terms isolationist and interactive community and that further empir-

ical work is required to evaluate their usage.

It can be concluded therefore that the above arguments support the views

held by Anderson (1982) on population regulation of helminth parasites.

Anderson considered the host s immune response causes a proportional reduc-

tion in the establishment, survival and reproduction of helminth parasites

following infection and thus acts in a density-dependent manner. As the dis-

tribution of the parasites becomes more aggregated the regulatory impact of the

density-dependent processes will become more pronounced. Anderson (1982)

also considered that competition between parasites might be important as a

density-dependent mechanism. He therefore concludes that density-dependent

processes acting on infrapopulations regulate macroparasite abundance and

that the severity of these processes is a major determinant of the observed

stability of many helminth infections despite severe perturbations due to cli-

mate or human intervention. Field studies involving the gathering of life table

data are needed to further validate these conclusions.

It was suggested by Thomas (1958b) that the absence of any clear evidence

of age-related resistance to the parasites of trout and salmon parr is indicative

of an old and stable relationship. This implies that the fish hosts and the para-

sites have evolved effective immune and immunosuppression or

immunoavoidance mechanisms, respectively, and that these are in balance.

The introduction of novel parasites or new genetic strains of the hosts could

therefore be potentially harmful. An example is provided by the emergence of

G y r o d a c t y l u s s a l m o n i s as a pathogen of salmonids, especially in Norway.

Using carefully controlled experimental infections, Bakke e t a l . (1990) demon-

strated innate and acquired resistance in Baltic (Neva) stocks where the

parasite was indigenous whereas the Norwegian stocks were highly suscepti-

ble. That the resistance has a genetic basis is also demonstrated by the

heterogeneity of the responses to G. sa lar i s shown by different races of rain-

bow trout and salmonids other than Norwegian

S . s a l a r

(Secombes and

Chappell, 1996). Care should therefore be taken during stocking of water

bodies so as not to alter the genetic composition of the native fish stock or to

introduce novel parasites.




6 R E L A T IO N S H IP S B E T W E E N PA R A SIT E A B U N D A N C E A N D T H E

W E L L B E I N G O F T H E F IS H H O S T S

6 1 I n t r o d u c t i o n

The symbols ~ - are generally used to depict host-parasite relationships

implying that parasites always harm their hosts while the parasites themselves

benefit. Damage suffered by the host may include mechanical injury, tissue

changes as a result of the immune response, toxicity due to toxic metabolic

endproducts, sterilisation and loss of nutrients and other resources due to com-

petition. Parasites may also act as vectors of other pathogens. As a result the

metabolism and behaviour of the host may be impaired and death may result.

Despite these potentially harmful effects host-parasite systems have con-

tinued to coexist and coevolve in nature. However, this balance is being

disturbed in a world that is constantly being subjected to increasingly fre-

quent anthropogenic influences. As a result epidemics caused by parasites

have tended to become more commonplace. It is predictable therefore that par-

asitology, linked to human and veterinary medicine, and with its focus on the

more strongly negative aspects of host-parasite relationships should have

emerged as an applied science. As a result of the focus on man-made epidemics

population biologists may well have overemphasised the role of parasites in

influencing population structure and genetics in natural habitats.

In order to get a more balanced view of host-parasite relationships it is nec-

essary to investigate more cases where the environment has not been unduly

disturbed by man. One such opportunity arose when it became possible to

investigate the salmonid fish and their helminth parasites in the River Teifi

more than 50 years ago. At this time the environment was relatively undis-

turbed and the Teifi was considered to be one of the best brown trout rivers in

the country.

6 2 P a t h o l o g y

Of the salmonid parasites encountered in the present investigation only N.

ru t il i C . t ru t t ae and D iphy l l o bo th r ium d i t r em um

were observed to be causing

pathological damage to the host tissues. In the case of

N. ru t i l i

damage

occurred at the point of attachment in the intestine as a result of the proboscis

penetrating the tunica propria, the stratum granulosum and even into the cir-

cular muscle coat. Outwardly, a circular layer of hypertrophied tissue around

the proboscis indicated parasitism by

N. rut i l i .

The hyperaemia of the sur-

rounding tissue often spreads to the muscular layers and in some cases causes

acute inflammation and metaplasia. Some encapsulated juveniles were



6 0 J D T H O M A S

o b s e r v e d in t h e g u t w a l l o f so m e t ro u t T h o m a s , 1 9 6 4a , c ). W h e n t h e g re e n

sunfish, Le po mis cyanellus, wa s l igh tly pa ras it i s ed by N. rutili i t w a s o b s e r v e d

tha t the pa ras i t e s pene t r a ted deep ly in to the in tes t ina l wa l l and connec t ive

t i ss u e d e v e l o p e d a r o u n d th e p r o b o s c i s a s i n t ro u t A d e l m e g u i d et al., 1995).

H o w e v e r , w h e n i n f e c ti o n s w e r e h e a v y > 5 0 c y st a c a n t h s) t h e p a r a si te s e v o k e d

g o b l e t c e l l h y p e r p l a s i a a n d t h e r e l e a s e o f s u b s t a n t i a l q u a n t i t i e s o f m u c u s .

Under these cond i t ions pene t r a t ion was sha l lower and pa ras i t e s appeared to

chan ge the i r s it e s o f a tt achm en t f r equen t ly . Ad e lm egu id et al. 1995) sug-

ges ted tha t the m ucus co ver ing and the p resum ed p resenc e o f an t ibod ies in the

m u c u s c o m b i n e d t o c r e a t e a p r o t e c ti v e b a rr ie r t h a t r e d u c e d t h e n u m b e r o f p ar -

as i t e s tha t cou ld become es tab l i shed . The f ac t tha t the abundance o f

N. rutili

d o e s n o t i n c r e a se w i t h a g e i n t h e tr o u t m a y b e d u e t o a c q u i r e d i m m u n i t y o r t o

d ie ta ry changes as soc ia ted w i th age .

A d u l t s o f

C. truttae

w e r e m o s t l y f o u n d i n t h e p y l o r ic c a e c a e o f t h e

s a l m o n i d s w h e r e t h e y p e r f o r a t e t h e m u c o s a w i t h th e i r p e ri b u c c a l t e e th t o f e e d

on t is sue o r hos t b lood . Acco rd ing to M oravec 1994) any pa thogen ic i ty caused

by th is spec ies is due m ain ly to me chan ica l dam age and pos s ib ly in f l amm at ion

of the in tes tina l muco sa . How ever , Ru sse l l 1980) conc lude d tha t the r a te o f

f o o d i n g e s ti o n a n d g r o w t h o f r a i n b o w t r o u t w e r e n o t i n f l u e n c e d b y C. truttae

i n f e c t i o n s e x c e p t p o s s i b l y w h e n t h e y w e r e h e a v y . A c c o r d i n g t o M o r a v e c

1 9 9 4 ) o t h e r n e m a t o d e s s u c h a s

C. ephemer idarum

m a y a l s o c a u se m u c o s a l

d a m a g e .

D i phy l l obo t hr i um d i t r em um

l a r v a e w e r e f o u n d t o h a r m t r o u t b y

caus ing adhes ions o f the pe r i tone um Thom as , 1964c) .

T h e r e i s e v i d e n c e f r o m o t h e r s t u d i e s t h a t s o m e o f t h e o t h e r p a r a s it e s

enco un te red in s a lmon ids in the Te if i m ay ha rm the i r hos t s. Thus , in the case

of the sangu inivorous paras i te , D. sagittata, haem ato log ica l pa ramete r s such as

h a e m a t o c r i t c o u n t s , e ry t h r o c y t e c o u n t s , m e a n c o r p u s c u l a r h a e m o g l o b i n a n d

m ean ce l l vo lum es a ll show ed s ign i fi can t nega t ive co r re la t ion w i th the in ten -

s i ty o f in fes ta tion Ron ga , 1995). Pa ras i t e - induced da m age to the g il ls may

cau se epi thel ia l les ions , necros is and mu cus secre t ion . As a resul t the osm oreg-

u l a t o ry a n d r e s p i r a to r y m e c h a n i s m s m a y b e i m p a i re d .

There a re a l so r epor t s o f f r ee -l iv ing gu t t r ema todes be ing pa thogen ic . Thus ,

Dav is 1953) obse rved tha t m ass in fes ta t ions o f t rou t w i th C . f a r i o n i s m i g h t

cause genera l in f l amm at ion o f the a l imen ta ry cana l . A l thou gh the re i s no ev i -

dence tha t P. simile i s pa thogen ic i t has been r epor ted tha t the congener ic

spec ies

P lysteri

m ay cause nephr ic duc t l e s ions Ho f fman , 1998). In the case

o f n e m a t o d e s M o r a v e c 1 9 9 4 ) a n d H o f f m a n 1 9 9 8 ) h a v e s u m m a r i s e d t h e e v i -

dence tha t Raphidascaris acus, C. ephemeridarum and Capillaria s pp . m a y b e

pa thoge n ic to f ish .

I t i s s ignificant that it is helminth paras i tes inhabi t ing t i s sues such as the ey e

Diplos tomum), t h e b l o o d s y s t e m Sanguinicola) and the pe r iv i s ce ra l cav i ty o f

f ish Diphyl lobothr ium and Ligula) tha t a re c las sed as be ing am ong s t the mos t

pa thoge n ic o f f i sh pa ras i te s P ike and Lew is , 1994).




T h e r e a r e a l s o re p o r t s o f fi s h m o r t al it ie s b e i n g p o s s i b l y c a u s e d b y s o m e o f

the he lmin ths e nco un te re d in the p resen t s tudy inc lud ing D. sag i t t a ta R o n g a ,

1995) ,

C . f a r i o n i s

Hoffman , 1998) ,

D . d i t r e m u m

Hickey and Har r i s , 1947 ;

Chubb, 1980; Hoole , 1994) , Rap h idasca r i s acus C . t ru t tae and Cap i l l a r ia spp.

M o r a v e c , 1 9 9 4 ; H a m m a r , 2 0 0 0 ) . H o w e v e r , t h e s e p a r a s i t e s a p p e a r e d n o t t o

cause s evere hos t r eac t ion o r m or ta l ity am ong the s a lm on ids in the R iver Te if i.

These r esu l t s sugges t tha t the s a lmon ids in the R iver Te i f i have evo lved

m e c h a n i s m s t o p re v e n t h y p e r i n fe c t i o n a n d m o r ta l it y . O n e o f t h e m o s t i m p o r -

t a n t o f t h e s e i s t h e i m m u n e r e s p o n s e . T e l e o s t f i s h a r e h i g h l y c o m p e t e n t

i m m u n o l o g i c a ll y , b o t h i n i n n a te i m m u n i t y a n d i n th e e x p r e s s io n o f t h e c o m -

b i n a t o r i a l i m m u n e s y s t e m . W h e n s t i m u l a t e d b y a n t i g e n s t h e y p r o d u c e

a n t i b o d i e s o f h i g h s p e c i f i c i t y a n d a f f i n i t y b y a p r o c e s s o f c o l l a b o r a t i o n

be tw een T ce ll s , B ce l ls and an t igen p resen t ing ce l l s Be m s te in e t a l . 1998).

They d i f f e r , however , f rom mammals in two impor tan t r e spec t s . F i r s t ly , they

l a c k l y m p h n o d e s a n d a s e c o n d c la s s o f i m m u n o g l o b u l i n s c o m p a r a b l e t o Ig G

and the mechan i sm o f muta t ion co r re la ted w i th the c las s sh i f t . As a r e su l t

t h e y c a n n o t m o u n t a s e c o n d a r y i m m u n e r e s p o n s e i n v o lv i n g a s w i t c h t o a d if -

f e ren t c l a s s o f an t ibod ies show ing h igher a f f in i ty fo r the an t igen . Second ly ,

lowe r ambien t t empera tu res can r esu l t in a longer r e jec tion t im e com pared w i th

m a m m a l s . H o w e v e r , f i s h h a v e e x c e l l e n t i m m u n o l o g i c a l m e m o r i e s a s e v i -

den ced b y the f ac t tha t they can be suc ces s fu l ly vacc ina ted aga ins t pa r t i cu la r

pa ras i t e s R ichards and Ch ubb 1996 ; W oo , 1997 ; Berns te in et a l . 1998) . The

i m m u n e r e s p o n s e h a s a l s o b e e n i n v o k e d t o e x p la i n t h e a p p a r en t r e j e c t io n o f

pa ras i te s and res i s t ance to r e in fec t ion in w i ld f ish popu la t ions Ken nedy and

Walker , 1969) .

As the immune r esponse i s gene t i ca l ly de te rmined hos t r e s i s t ance to pa ra -

s i t ism can deve lop by na tu ra l o r a r ti fi c ia l s e lec t ion . I t f o l lows the re fo re tha t a s

the w i ld t rou t , s a lm on pa r r and the i r pa ras it e s hav e co evo lv ed in the R iver Teif i

fo r man y gene ra t ions i t i s to be expe c ted tha t they w i l l have acq u i r ed a me as -

u r e o f i m m u n i t y . T h i s e x p l a i n s t h e a b s e n c e o f h o s t m o r t a l i t y a n d p a r a s i t e

ep idemics . I t f o l lows the re fo re tha t the re i s a danger in s tock ing r ive r s w i th

new s tr a ins o f s a lm on id f ish , a s they a re l ike ly to have a lowe r r esi s t ance to the

endemic pa ras i t e s than the ind igenous r ace . In add i t ion the s tocked f i sh may

a l so in t roduce nove l pa ras i t e s to wh ich the r es iden t f i sh migh t have a low

res i s t ance . Fevo lden et a l . 1 9 9 3 ) g i v e e x p e r i m e n t a l e v i d e n c e s h o w i n g t h a t

s tr a ins o f s a lm on id spec ies va ry in the i r re spon ses to s t r e s s and d i s ease .

6 3 S t a t is t ic a l A n a l y s e s o f t h e R e l a ti o n s h i p s b e t w e e n P a r a s it e

A b u n d a n c e a n d t h e C o n d i ti o n F a c t o r a n d A d i p o s e In d e x

As the r eg res s ion equa t ion , b ased on a p lo t o f log e we igh t ag a ins t log e length

f o r t r o u t , w a s y = - 4 . 1 7 9 7 3 + 2 . 8 7 8 7 6 x t h e v a l u e o f 2 . 8 7 8 7 6 w a s u s e d t o



62 J D THOMAS

c a l c u la t e t h e c o n d i t i o n f a c t o r

( W / L 2 87876 ) .

1 0 0, w h e r e W = t h e w e i g h t i n g r a m s

a n d L = t h e l e n g t h i n c m . F i g u r e 8 s h o w s t h a t th e c o n d i t i o n f a c t o r v a ri e s s i g -

n i f i c a n t l y P < 0 . 0 0 1 ) o n a s e a s o n a l b a s i s w i t h th e v a l u e s r i si n g f r o m A p r i l u n ti l

A u g u s t o r S e p t e m b e r a f te r w i n te r l o w s a n d t h e n d e c l in i n g d u r i n g t h e s p a w n -

i n g a n d p o s t - s p a w n i n g p e r i o d f r o m O c t o b e r t o D e c e m b e r . L i n e a r r e g r e ss i o n s,

i n w h i c h t h e lO g l0 l + x ) t r a n s f o r m e d v a l u e s f o r n u m b e r s o f p a r a s i t e s w e r e

p l o t t e d o n t h e y - a x i s a g a i n s t v a l u e s f o r c o n d i t i o n f a c t o r s o n t h e x - ax i s . T h e s e

r e v e a l th a t w i t h t h e e x c e p t i o n o f N . r u t i l i t h e c o n d i t i o n f a c t o r t e n d s t o d e c l i n e

s i g n i f i c a n t l y P < 0 . 0 0 1 i n a ll c a s e s ) a s t h e n u m b e r o f p a r a s i te s i n c r e a s e s

T a b l e 1 8 ). T h e o v e r a l l t e n d e n c y f o r c o n d i t i o n f a c t o r to d e c l in e w i t h i n c r e a s e

i n th e t o ta l n u m b e r o f p a r a s i te s i s s h o w n i n F i g u r e 1 4 a. I n c o n tr a s t , t h e c o n d i -

t i o n f a c t o r i n c r e a s e s s i g n i f ic a n t l y P < 0 . 0 0 2 ) a s n u m b e r s o f N .

r u t i l i

i n c r e a s e .

H o w e v e r , th e a d i p o s e i n d e x w a s s i g n i f i c a n t l y p o s i t i v e l y c o r r e l a te d w i t h t h e

t r a n s f o r m e d v a l u es f o r t h e n u m b e r s o f

D . s a g i t ta t a , C . m e t o e c u s ,

n e m a t o d e s

a n d t o ta l p a r a s it e s T a b l e 1 9 ) . A s m i g h t b e e x p e c t e d t h e a d i p o s e i n d e x w a s s i g -

n i f i c a n t l y p o s i t i v e l y c o r r e l a t e d w i t h t h e c o n d i t i o n f a c t o r y = 1 0 . 5 + 0 . 1 3 5 x , P

< 0 . 0 0 1 ) .

Table 18

Th e regression equations relat ing to the transfo rm ed num be r o f parasites

lOglo 1 + x) ) to the condi t ion factor CF) of the brow n t rout

Regress ion equat ions F P

Num bers tr .) o fD .

sagit tata

= 1 .1 30 - 0 . 0 8 5 C F

Num bers t r. ) o f

C. far io n is

= 0 .867 - 0 . 062 CF

Num bers t r. ) o f

C. me toecus

= 8.78 - 0 .622 CF

Nu mb ers t r .) of P .

s im i l e

= 0.867 - 0 .059 CF

Num bers t r. ) o fN .

ruti l i

= 0.131 + 0.127 CF

N u m b e r s tr .) n e m a t o d e s = 2 . 5 4 - 0 . 1 5 3 C F

Nu mb ers t r. ) of tota l paras ites = 14 .3 -0 .8 6 5 CF

31.88

17.94

178 06

10.98

10.12

20.83

85.31

< 0.001

< 0.001

< 0.001

< 0.001

< 0 .002

< 0.001

< 0.001

Table 19

Th e regression equ ations show ing the relat ionships betw een the

t ransformed num ber of paras ites log10 1 + x) ) and the adipose index AI) of t rout

Re gressio n equations F P

Num bers tr .) o fD .

sagit tata

= 0 .0797 + 0 .0713 AI

Nu mb ers t r. ) o f

C . fa r io n i s

= 0 .130 + 0 .0335 AI

Nu mb ers t r. ) of

C. me toecus=

0.1.76 + O. 170 A I

Nu m bers t r. ) o f P.

s im i l e

= 0 .188 + 0 .0204 AI

Num bers t r. ) o f N. ruti l i = 1.36 + 0.0682 AI

Num bers tr .) o f nematodes - - 0 . 420 + 0 .246 A I

N um bers t r. ) o f al l parasites = 3.95 + 0.606 A I

11 99

2.77

6.35

0 .70

1 58

29.53

22.09

0.001

0 .096

0 .012

0 .402

0 .209

0 .000

0 .000



E C O L O G Y O F F I S H P A R A S I T E S 6 3

1 5

- -

1 4 - -

n -

O

1 3 - -

, , <

Z 1 2

_o

I - -

Z

o

L

o

- -

9 - -

8 - -

a )

R e g r e s s i o n P l o t

Y = 1 1 . 1 7 4 5 - 8 . 01 E - O 2 X

R - S q = 6 . 9

° . • •

• I o

• b .

. : ~ . - . ~ . - : . * ,. .

~ . . , . : , - . o , o . . . . . . , • .

l

. , :, , . . : .

O

- ~ . ~ _ g . ~ . g . . : . , : ~ . . . . • .

I : ' . ' ~ ~ ' : ¢ = . # ' .

• ' : • ; • ' 2 .

~ • . . ° •

I I I

5 1 0 1 5

T O T A L N O . T R . ) O F P A R A S I T E S

n -

O

r--

c)

1 6 - -

1 5 - -

1 4 - -

1 3

1 2

11

1 0 - -

9 - -

8 - -

I

0

b )

R e g r e s s i o n P l o t

Y = 1 2 . 5 3 9 3 - 0 . 3 1 4 6 8 4 X

R - S q = 1 . 3

. I • *

• • * * •

I • . •

| •

• I i • • I •

I . : : ' • . . . ' : * - • .

, , . : . : : . ; * . . . ~ : , ,

I • * * i • *

• l I . = l e . * I I ;

I

• : . . . i . . . . . .

• e ~ • • o • •

• * .

• ** . **

1

T O T A L N O . T R ) O F P A R A S I T E S

Figure 4

T h e r e l a t i o n s h i p b e t w e e n t h e c o n d i t i o n f a c to r o f t h e tr o u t a ) a n d t h e

s a l m o n p a r r b ) a n d t h e t o t a l p a r a s i t e a b u n d a n c e t r a n s f o r m e d l o g ]0 1 + x ) .



64 J D THOMAS

A s t h e r e g r e s s i o n e q u a t i o n , b a s e d o n a p l o t o f l o g e w e i g h t a g a i n s t l o g e

l e n g th f o r th e s a l m o n p a r r w a s y = - 3 . 7 9 9 1 8 + 2 . 7 6 1 3 5 x t h e v a lu e o f 2 . 7 6 1 3 5

w a s u s e d t o c a l c u l a te t h e c o n d i t io n f a c t o r W / L 2 7 6 1 3 5 ) . l O 0 w h e r e W = th e

w e i g h t i n g r a m s a n d L = t h e l e n g th i n c m . U n l i k e t h e b r o w n t r o u t th e c o n d i t i o n

f a c t o r s h o w e d n o s i g n i f i c a n t se a s o n a l v a r i a t io n a l t h o u g h t h e m e a n v a l u e s

t e n d e d t o b e s l ig h t ly h i g h e r a n d m o r e v a r i a b le i n J a n u a r y a n d M a r c h F i g u r e

9 ). R e g r e s s i o n a n a l y s e s , w h e r e t h e lo g 10 1 + x ) t r a n s f o r m e d v a l u e s f o r p a r a -

s it e n u m b e r s a r e p l o t t e d o n t h e y - a x i s a g a i n s t v a l u e s f o r c o n d i t i o n f a c t o r s o n

t h e x - a x is w e r e u n d e r t a k e n . T h e s e r e v e al th a t w i th t h e e x c e p t i o n o f N . r u t i l i ,

t h e c o n d i t i o n f a c t o r t e n d s t o d e c l i n e s i g n i f i c a n t l y w i t h i n c r e a s e s i n n u m b e r s

o f C . f a r i o n i s , C . m e t o e c u s , n e m a t o d e s a n d th e t o ta l p a r a s i t e s P = 0 . 0 0 8 ,

< 0 .0 0 1 , < 0 . 0 0 1 a n d 0 . 0 5 1 , r e s p e c t i v e l y ) a s t h e n u m b e r o f p a r a s i t e s i n c r e a s e

T a b l e 2 0 ) . I n c o n t r a s t , t h e c o n d i t i o n f a c t o r te n d s t o i n c r e a s e a s n u m b e r s o f N .

ru t i l i i n c r e a s e a l t h o u g h th i s t r e n d i s n o t st a t is t ic a l l y s i g n i fi c a n t . T h e t e n d e n c y f o r

t h e c o n d i t i o n f a c t o r o f t h e s a l m o n p a r r t o d e c l in e w i t h i n c r e a s e i n th e t o t al

n u m b e r o f p a ra s i te s is s h o w n i n F i g u r e 1 4 b. I n c o n t ra s t , t h e re g r e s s i o n e q u a t i o n s

r e la t in g t h e a d i p o s e in d e x t o t h e t r a n s f o r m e d n u m b e r s o f N . r u t i l i a n d t h e t o t a l

n u m b e r s o f p a r a s i t e s in d i c a t e s i g n i f i c a n t p o s i t i v e r e l a t i o n s h i p s T a b l e 2 1 ) .

Table 20 Th e regression equ ations relating the transfo rm ed num bers of parasites

log10 1 + x) ) to the condi t ion factor CF) of the sa lmon parr

Reg ress ion equat ions F P

Num bers t r. ) o fD . sagittata = 0 . 0 4 4 3 - 0 . 0 0 1 9 3 C F

Num bers t r. ) o f C. far ion is = 0 .619 - 0 . 0400 CF

Num bers t r. ) o f C. metoecus = 2.85 - 0 .208 C F

Num bers t r. ) o fN . rutili = 1 .50 + 0 .0194 CF

Num bers t r. ) o f nematodes = 1 .20 - 0 . 0819 CF

Nu m bers t r .) of tota l paras ites = 1.35 - 0 .0420 CF

0.12 0.728

7.12 0.008

56 .67 0 .000

0.15 0.699

15 07

0 .000

3.83 0.051

Table 21 Th e regression equ ations relat ing the transform ed num bers of parasites

logl0 1 + x) ) to the adipose index AI) of the sa lmo n parr

Reg ress ion equat ions F P

Num bers t r. ) o fD . sagittata = -0 .0221 + 0 .0195 AI

Nu mb ers t r. ) of C. far ion is = 0.134 - 0 .0033 AI

Num bers t r. ) o f C. metoecus = 0 .547 - 0 . 116 AI

Num bers t r. ) o f N. rutili = 1.09 + 0.297 A I

Nu m bers t r. ) o f nem atodes = 0.185 + 0.0021 AI

Nu m bers t r . ) o f total parasi tes = 0.591 + 0.113 A I

2.59

0.01

3.06

7.37

0 .00

5 .70

0 .109

0.921

0.081

0.007

0.965

0.018




I n v i e w o f t h e c o m p l e x i t y o f t h e i n t e ra c t i o n s t h a t m i g h t i n f l u e n c e t h e

c o n d i t i o n f a c t o r t h e r e la t i o n s h i p s w e r e a l s o i n v e s t i g a te d b y m e a n s o f m u l t i-

p le r eg res s ion ana lyses . Th e r esu l t s fo r t rou t (Tab le 22 ) sho w tha t i t i s ma in ly

s t a ti o n s , s e a s o n s , a g e a n d s e x o f th e t r o u t t h a t p r e d i c t t h e c o n d i t i o n f a c t o r

va lues . Th ese acco un t fo r 5 .4 , 79 .1 , 14 .1 and 1.3 , r e spec t ive ly , o f the

t o t a l v a r i a n ce , m a k i n g a t o t a l o f 9 9 . 9 6 , w h e n t h e t r a n s f o r m e d t o t a l n u m b e r

o f pa ras i t e s i s inc lude d in the equa t ion . In con t r as t , t he l a t t e r f a i l to mak e a

s i g n i fi c a n t c o n t r i b u t i o n t o t h e t o ta l v a r i a n c e ( P v a l u e = 0 . 5 4 1 ) a n d a c c o u n t

f o r o n l y 0 . 0 4 o f t h e t o ta l . W h e n t h e in d i v i d u a l p a r a s it e ta x a a r e i n c l u d e d in

t h e e q u a t i o n ( T a b l e 2 2 ) o n l y o n e , n a m e l y

C . m e t o e c u s

has a s ign i f i can t p re -

d i c t iv e v a l u e ( P = 0 . 0 0 7 ) . I n n u m e r i c a l t e r m s t hi s i s b y f a r t h e m o s t a b u n d a n t

s p e c i e s o f p a ra s i te . I t i s n o t e w o r t h y t h a t t h e n u m b e r s o f th i s s p e c i e s s h o w a

s i g n i f i c a n t p o s i t i v e c o r r e l a t i o n w i t h t h e v a l u e s f o r c o n d i t i o n f a c t o r .

Ne ver the les s , the con t r ibu t ions to the to ta l va r i ance m ade b y the s ix pa ras i t ic

t a x a a s a w h o l e a n d b y C . m e t o e c u s in pa r t i cu la r a r e on ly 1 .62 and 0 .88 ,

r e spec t ive ly .

The r esu l t s fo r the s a lmon pa r r show s imi la r t r ends to those fo r the t rou t

(Tab le 23 ). Thus , s t a t ions, s eason s and ag e a re the majo r p red ic to r s o f cond i -

t ion f ac to r , a s they con t r ibu te 18 .14 , 78 .14 and 2 .44 , r e spec t ive ly , to the

to ta l va r i ance compared w i th the non- s ign i f i can t (P = 0 .236) con t r ibu t ion o f

on ly 0 .69 m ade by the to ta l pa ras i te s (Tab le 23 ) . W hen the ind iv idua l pa ra -

s it e ta x a a r e i n c l u d e d i n t h e e q u a t i o n o n l y t h e n u m b e r s o f t h e m o s t a b u n d a n t

parasit ic taxon, N. rut i l i corre la ted s ignif icant ly (P = 0 .013) wi th the values for

cond i t ion f ac to r (Tab le 23 ) . As wa s the cas e w i th the t rou t i t i s o f in te res t tha t

th i s co r r e la t ion i s a l so pos i t ive . However , the con t r ibu t ion made to the to ta l

va r i ance b y the f ive pa ras i ti c t axa as a w ho le and by N. ru t i l i in par t icu lar are

o n l y 2 . 8 6 a n d 1 . 7 5 , r e s p e c t i v e l y , c o m p a r e d w i t h 1 8 . 1 4 , 7 6 . 9 a n d

2 .44 m ade by s t a tion , s eason and age , r e spec t ive ly .

W h e n i n t er p r e ti n g t h e p o s s i b l e i m p a c t o f t h e p a r a s it e s o n t h e c o n d i t i o n

f a c t o r s a n d a d i p o s e i n d i c e s o f t h e t r o u t a n d s a l m o n p a r r i t i s n e c e s s a r y t o

c o n s i d e r t h e i n te r a c t io n s b e t w e e n t h e s e a n d o t h e r p a r a m e t e r s i n c l u d i n g s ta -

t ion , s eason , s i ze and age o f the fi sh . Th e s ign i f i can t nega t ive coe f f i c i en t s

ob ta in ed fo r the l inea r r eg res s ions r e la t ing c ond i t ion f ac to r o f the t rou t to the

n u m b e r s o f p a r a si t e s i n t h e v a r io u s t a x a, e x c e p t f o r N. ru t i l i s u g g e s t t h a t t h e

i n c r e a s e i n n u m b e r s o f p a r a s it e s m i g h t b e t h e c a u s a l f a c t o r r e s p o n s i b l e f o r

the dec l ine in the cond i t ion f ac to r . How ever , th i s conc lus io n i s inva l ida ted by

t h e f a c t th a t t h e c o n d i t i o n f a c t o r o f th e t r o u t a n d t h e n u m b e r s o f a l l t h e p a r -

a s i t e t a x a , e x c e p t f o r N. ru t i l i s h o w d i f f e r e n t s e a s o n a l t r e n d s . T h u s , t h e

c o n d i t i o n f a c t o r is m a x i m a l i n A u g u s t a n d S e p t e m b e r ( F i g u r e 8 ) a t a ti m e

w h e n t h e a b u n d a n c e s o f th e p a r a si t e t a xa , e x c e p t f o r

N. ru t i l i

t e n d t o b e m i n -

imal .

The mul t ip le r eg res s ion ana lyses show tha t the t rou t ' s cond i t ion f ac to r i s

predic ted m ainly by season, age , s ta t ion and sex , accou nt ing for 79 .1 , 14 .1 ,



J D THOMAS

Table 22 T h e re s u l ts o f m u l t ip l e r e g re s s io n a n a ly s e s o f th e c o n d i t io n f a c to r o f th e

brow n t rou t a s the response and s ta t ions , seasons , sex , age and pa ras i te a s the p red ic to rs

Pred ic to rs Coeff ic ien ts S .D. P Tota l va r iance

Co ns tan t 10 .834 0 .114 0 .000

S ta t io n s (3 ) -0 .0 2 4 - ( -0 .1 9 7 ) 0 .0 6 2 -0 .0 7 2 0 .00 0 5 .3 5

M onths (12) -0 .30 4 - 1 .566 0 .119 -0 .115 0 .000 77 .84

Ag e -0 .2 3 4 0 .0 27 0 .0 0 0 1 3.8

Sex 0.142 0.040 0.001 1.30

D. sag i t ta ta

-0 .05 1 0 .046 0 .268 0 .12

C. f a r io n i s

-0 .05 0 0 .047 0 .283 0 .05

C. me to e c u s 0 .052 0 .019 0 .007 0 .88

P. s imi le

-0 .0 4 3 0 .0 39 0 .2 63 0 .1 4

N. ru t i l i 0 .034 0 .023 0 .133 0 .20

Ne m a to d e s -0 .0 3 8 0 .0 2 6 0.1 4 5 0 .2 3

(Tota l pa ras i te s ) (0 .006) (0 .010) (0 .541)

5.44)

79.06)

14.12)

1.35)

(0 .04)

T h e v a l u e s f o r t ot a l p a r a s i t e s a r e g i v e n i n p a r e n t h e s e s . ( N o t e t h a t t h e p e r c e n t a g e o f th e v a r i a n c e a c c o u n t e d f o r b y

e a c h f a c t o r i s c o n d i ti o n a l o n t h e f a c t o r s e n t e r e d e a r l i e r i n t h e t a b l e .)

R . S q . = 4 4 . 1 ; D . F . = 2 1 ; F = 4 2 . 8 3 ; P = < 0 . 0 0 1

Table 23

T h e re s u l ts o f m u l t ip l e r e g res s io n a n a ly s e s o f th e c o n d i t io n f a c to r o f th e

s a lmo n p a r r a s th e r e s p o n s e a n d s t a tio n s , s ea s o n s , s e x, a g e a n d p a ra s i t e a s th e p re d ic to r s

Pred ic to rs Coeff ic ien ts S .D. P Tota l va r iance

Co ns tan t 16 .617 0 .955 0 .000

Sta t ions (2 ) 0 .309 0 .064 0 .000 18 .14 (18 .14)

M o n th s (1 2 ) -1 .3 3 8 , -4 .3 3 3 0 .4 8 8 -0 .6 8 0 0 .0 5 0 -0 .0 0 0 7 6 .9 0 (7 8 .6 3 )

A ge 1.055 0.348 0.003 2.44 (2 .44)

Sex -0 .0 68 0 .220 0 .756 0 .10 (0 .10)

D. sag i t ta ta

0.137 0.874 0.876 0.01

C. f a r io n i s

-0 .4 0 7 0 .3 22 0 .2 0 7 0 .5 0

C . m e t o e c u s -0 .2 44 0 .181 0 .178 0 .49

N. ru t i l i 0.247 0.099 0.013 1.75

Ne m a to d e s -0 .1 3 8 0 .23 8 0 .5 63 0 .1 0

(Tota l pa ras i te s ) (0 .354) (0 .236) (0 .134) (0 .69)

T h e v a l u e s f o r t o ta l p a r a s i t e s a r e g i v e n i n p a r e n t h e s e s . ( N o t e t h a t t h e p e r c e n t a g e o f t h e v a r i a n c e a c c o u n t e d f o r b y

e a c h f a c t o r i s c o n d i t io n a l o n t h e f a c t o r s e n t e r e d e a r l i e r i n th e t a b l e . )

R S q . = 5 5 . 6 ; D . E = 1 8 ; F = 1 8 .7 5 ; P = < 0 . 0 0 1 .

5 . 4 a n d 1 . 3 o f t h e t o t a l v a r i a n c e , r e s p e c t iv e l y , c o m p a r e d w i t h o n l y a n o n -

s i g n i f i c a n t c o n t r i b u t i o n o f 0 . 0 4 m a d e b y t h e t o t a l p a r a s i te s . H o w e v e r w h e n

i n d i v i d u a l p a r a s i t i c t a x a a r e s u b s t i t u t e d f o r to t a l p a r a s i t e s i n t h e m u l t i p l e

r e g r e s s i o n eq u a t i o n o n l y o n e , n a m e l y C . m e t o e c u s t h e m o s t a b u n d a n t p a r a s it e ,

i s s i g n i f i c a n t ly p r e d i c t i v e o f t h e c o n d i t i o n f a ct o r. T h e f a c t t h a t th e n u m b e r s o f




C . m e t o e c u s a re s ign i f i can t ly pos i t ive ly co r re la ted w i th cond i t ion f ac to r o f

the t rou t sugges t s tha t th i s pa ras i t e may no t adver se ly a f f ec t the cond i t ion

fac to r o f i t s hos t . The fo l lowing obse rva t ions a l so imply tha t th i s conc lus ion

can b e ex ten ded to o the r pa ras i t e s. F i r s t ly , in the cas e o f

N . r u t i l i

the re was a

s ign i fi can t pos i t ive r e la t ionsh ip be tw een the nu m bers o f th i s pa ras it e and the

cond i t ion f ac to r . Th i s conc lus ion i s va l id as , un l ike the o the r pa ras i t e s , N .

r u t i l i

a b u n d a n c e v a l u e s a r e i n d e p e n d e n t o f h o s t a g e o r s e a s o n . S e c o n d l y , t h e

ad ipose index w as s ign i f ican t ly pos i t ive ly co r re la ted w i th numb ers o f

D . s a g i t -

t a ta C . m e t o e c u s

nem atode s and to ta l pa ras it e s .

The r esu l t s fo r s a lmo n par r a re in acco rd w i th th ose fo r t rou t . F i r st ly , l inea r

reg res s ion ana lyses showed tha t the re was a s ign i f i can t pos i t ive r e la t ionsh ip

b e t w e e n t h e n u m b e r s o f

N . r u t i l i

and the con d i t ion f ac to r o f s a lmon-par r . As

e x p l a i n e d a b o v e f o r t r o u t , l i n e a r r e g r e s s i o n a n a l y s e s a r e o n l y v a l i d f o r N .

r u t i l i

b e c a u s e n u m b e r s o f th is s p e c i e s ar e i n d e p e n d e n t o f a g e a n d s e a so n ,

u n l i k e t h e o t h e r p a r a s i t e s p e c i e s . S e c o n d l y , m u l t i p l e r e g r e s s i o n a n a l y s i s

s h o w s th a t t h e c o n d i t i o n f a c t o r o f t h e s a l m o n p a r r is p r e d i c t e d m a i n l y b y

s e a s o n , s t at io n a n d a g e . T h e s e f a c t o r s a c c o u n t f o r 7 8 . 6 , 1 8 .1 , a n d 2 . 4

o f the to ta l va r iance , r e spec t ive ly , com pare d w i th on ly a non- s ign i f i can t con-

t r ib u t i o n o f 0 . 7 m a d e b y t h e t o t a l p a r a s it e s . W h e n i n d i v i d u a l p a r a s it i c t a x a

a r e s u b s t i t u t e d f o r t o t a l p a r a s i t e s i n t h e m u l t i p l e r e g r e s s i o n e q u a t i o n o n l y

o n e , n a m e l y

N . r u t i l i

the mos t abundan t pa ras i t e , was a s ign i f i can t p red ic to r

o f th e c o n d i t io n f a c to r . A s w i t h t ro u t t h e n u m b e r s o f t h e m o s t a b u n d a n t p a r -

a s i te o f th e s a l m o n p a r r w e r e p o s i t i v e l y c o r r e l a t e d w i t h t h e c o n d i t i o n f a c to r .

S e c o n d l y , t h e a d i p o s e i n d e x o f t h e s a l m o n p a r r w a s s i g n i fi c a n t ly p o s i t i v e l y

c o r r e l a t e d w i t h n u m b e r s o f

N . r u t i l i

a n d t o t a l p a ra s i te s . I t m u s t b e c o n c l u d e d

the re fo re tha t these s t a ti s ti ca l ana lyses p ro v ide no ev ide nce tha t the he lmin th

paras i te s o f e i the r the b row n t rou t o r s a lmon par r a f f ec t the w e l lbe ing o f the i r

h o s t s a s m e a s u r e d b y t h e c o n d i t i o n f a c t o r a n d a d i p o s e i n d e x . T o t h e c o n t r a r y

t h e r e s u lt s i n d i c a t e t h a t t h e r e a r e s i g n i f ic a n t p o s i t i v e re l a t i o n s h ip s b e t w e e n

p a r a s i te a b u n d a n c e a n d t h e c o n d i t i o n f a c t o r s a n d a d i p o s e i n d i c e s o f b o t h

trout and sa lmon parr .

Tw o poss ib le reasons can be a dvan ced to expla in these resul ts. F irst ly , th ey

m ay b e caused b y behav ioura l d if fe rences. I t has long be en know n tha t s a lmon id

f i sh popu la t ions a re s t rong ly h ie ra rch ica l in the i r behav iour (E l l io t t , 1994 ;

A r m s t r o n g e t a l . 1999) . As a resul t i t i s to be ex pecte d that the dom inant , m ore

aggre ssive f ish, with highe r androgen lev els (Pott inger and Carrick, 2000), w ou ld

tend to occupy the op t ima l home ranges . I t can be pos tu la ted tha t such home

ranges w ou ld p rov ide the f i sh w i th the bes t r e fuges f rom p reda to rs and f as t cu r-

rents in t ime s of spate and a lso the bes t oppor tuni t ies for obta in ing h igh-q ual i ty

food . A l though sa lmon id f i sh need a va r ie ty o f hab ita ts in the ir hom e ranges

including pools , fas t reaches , r i f f les and the shel tered habi ta ts wi th depos i t ing

sed imen ts on the edg e o f cu r ren t s, the l a t te r may be r anked as the m os t impor -

tant. I t w as fou nd that these depos i t ing sedim ents are the prefer red microhabi ta ts



68 J D THOMAS

of am m ocoe te la rvae (the in te rmed ia te hos t s o f C . t r u tt a e , S p h a e r i u m c o r n e u m

( the in termedia te hos ts of P . s im i l e , L y m n a e a p e r e g r a o r P i s i d i u m spp. ( the

in te rmed ia te hos t s o f

C . m e t o e c u s

and o s t racods ( the in termedia te hos ts of N.

ru t i l i

(Thomas , 1964c) . I t can therefore be pos tu la ted that the dominant t rout

w ould tend to ea t propor t ionate ly mo re infect ive larvae than the subordinate t rout

no t on ly bec ause o f the i r l arge r s i ze bu t a l so because they wo u ld t end to spend

m ore t ime in mic rohab i ta t s w i th depos i ting s ed imen ts . A l though the re i s more

over lap in the hom e ranges o f s a lmo n par r than b rown t rou t (Arms t rong e t a l . ,

1999) the sam e arguments can be appl ied . I t m ay be sug ges ted therefore that the

pos i t ive co r re la tion be tw een the cond i t ion f ac to r and abundance o f N. ru t i l i in

sa lmon par r m ay b e due to the dominan t , b e t t e r- cond i t ioned f i sh spend ing m ore

t ime in habitats wi th depos i t ing sedim ent favoured by os t racods and

S i a l i s

la rvae

wh ich a re the in te rmed ia te hos t s o f N. ru t i l i .

I t m i g h t a l s o b e p o s t u l a t e d t h a t a s t h e d o m i n a n t , l a r g e r t r o u t t e n d t o

s p e n d p r o p o r t i o n a te l y m o r e t i m e i n m i c r o h a b i ta t s w i t h d e p o s it i n g s e d i m e n t

t h an t h e i r s u b o r d i n a t e s t h e y w o u l d a l s o t e n d t o b e c o m e m o r e h e a v i l y p a r a -

s i ti s e d w i t h m o n o g e n e t i c p a r a s it e s . T h e r a t i o n a l e f o r t h is a r g u m e n t i s t h a t

t h e e g g s o f


w o u l d t e n d t o a g g r e g a t e i n d e p o s i t i n g s e d i m e n t s

w i t h d e t r i t u s . T h e s e e g g s h a t c h o u t a t n i g h t t o p r o d u c e i n f e c t i v e

o n c o m i r a c i d i a a t a t i m e w h e n t h e t r o u t a r e r e s t i n g ( G a n n i c o t t a n d T i n s l e y ,

1 9 9 7 ) . I t w o u l d b e p r e d i c t e d t h e r e f o r e t h a t t h e a b u n d a n c e o f


w ou ld be pos i t ive ly co r re la ted w i th s i ze and co nd i t ion f ac to r o f the trou t. The

r e s u l ts s u p p o r t t h is h y p o t h e s i s a s th e a b u n d a n c e o f D . s a g i t t a t a wa s s ign i f i -

c a n t l y c o r r e l a t e d w i t h t h e s i z e o f tr o u t a n d s a l m o n p arr. H o w e v e r , m u l t i p le

r e g r e s s i o n a n a l y s e s s h o w e d th a t t h e re l a t io n s h i p s b e t w e e n t h e c o n d i t i o n f a c -

t o r s o f t h e s a l m o n i d s p e c i e s a n d t h e a b u n d a n c e o f t h is s p e c i e s w e r e

n o n - s i g n i f i c a n t ( T a b l e s 2 2 a n d 2 3 ) .

Second ly , the o the r pos s ib i l i ty i s tha t the pa ras i t e s may he lp to p romote

som at ic g rowth o f the s a lm on id f i sh by p rov id ing the m wi th nu t r it iona l b ene-

f its . As the pa ras it e s r e sp i r e anaero b ica l ly the hos t s m ay seques te r the am ino

acids and c arb ox yl ic ac ids , inc luding lac t ic , succin ic and shor t -chain C2, C 3

and C 4 ac ids r e leased by the pa ras i t e s a s end p roduc t s o f the ir m e tabo l i sm.

Paras i te s m ay a l so benef i t the hos t s by r e leas ing d iges t ive enzy m es , ac t ing as

s inks fo r po ten t i a l ly tox ic heav y meta l s (Sures and S ida l l , 1999) and by co m -

pe t i t ive ly exc lud ing pe rhaps po ten t i a l ly more ha rmfu l pa ras i t e s . However , i t

s eem s p rob ab le tha t on ba lance the nu t r i tiona l d i s advan tage s o f pa ras i t ism to

t h e h o s t w o u l d o u t w e i g h t h e a d v a n ta g e s .

T h e r e i s a l s o e v i d e n c e t h a t s o m e p a r a s i t e s h a v e e v o l v e d m e c h a n i s m s t o

enhan ce the som at ic growth of the hos t. Al thoug h th is m ight appear to be to the

hos t s a dvantage th is i s no t the case as the paras i te a lso inhib its the reproduct ive

growth of the hos t . As a resul t the paras i tes benef i t f rom addi t ional space and

energy r esu l ting f rom the enhanced somat ic g rowth o f the hos t by the m ore e f f i-

c ien t channe l ling o f ene rgy fo r the i r own g row th and r ep roduc t ion . A




wel l -documen ted example o f such cases is p rov ided by a b i rd s ch i stosome spec ies

tha t p romotes somat ic g rowth and inh ib i t r ep roduc t ive g rowth o f Lymnaea stag-

nalis

(de Jong-Br ink , 1995) . According to de Jong-Br ink (1995) the paras i te

achie ves this by releasing a cercarial facto r that cause s schis tosom in, a cyto kine -

l ike fac tor, to be re lease d by the h aem atocy tes and c onnect ive t i s sue cel ls of the

h o s t s i m m u n e s y s te m . T h e s c h i s to s o m i n t h en b i n d s t o c e l ls o f t h e n e u r o -

endocr ine regula tory sy s tem thus inhibi ting the develo pm ent of the reproduct ive

syst em o f the host . I t thus appe ars that the parasites hav e evo lved survival s trate-

g ies that enable them to benef i t f rom the s t ress re spon se that they evok e in thei r

hos t . According to Ecker t (1991) the p lerocercoids of

Spirometra mansonoides

use a m ore d i r ec t approach as they apparen t ly enhan ce the g row th o f roden ts by

produc ing a subs tance wh ich mimics the ac t ion o f mamm al ian g rowth ho rmone .

P l e r o c e r c o i d s , s u c h a s t h o s e o f

Ligula

can r esu l t in h igh pa ras i t i s a t ion

i n d i c e s ( w e i g h t o f p a r a si t e /w e i g h t o f p a r a si t e + h o s t ). A c c o r d i n g t o H o o l e

(1994) , the l i t er a tu re dea l ing w i th the e f f ec t s o f l igu los i s on f i sh g row th and

genera l cond i t ion i s inconc lus ive a l though the r educ t ion o f gonada l deve lop-

m ent in l igulosed f ish is wel l docum ented . T here is ev ide nce that it i s associa ted

wi th a l t e ra t ions in the ce llu la r compo s i t ion o f the m esoade nohy poph ys i s reg ion

of the p i tu it a ry g land . H ow ever , the b iochem ica l mech an ism invo lved r emains

to be e luc ida ted . In th is con nec t ion i t wo u ld be in te rest ing to asce r ta in w he the r

the pa ras i te i s capab le o f man ipu la ting the hos t s im m une and neuro -endoc r ine

sys tems as i s the case w i th s ch i s tosom es in Lym naea stagnalis.

I n t h e c a s e o f t h e s a l m o n i d s i n t h e p r e s e n t c a s e s t u d y f u r th e r r e s e a r c h i s

n e e d e d t o e x p l a i n t h e p o s i t iv e r e la t io n s h i p s b e t w e e n t h e a b u n d a n c e o f c e r ta i n

p a r a s i t e s a n d t h e c o n d i t i o n f a c t o r s a n d a d i p o s e i n d i c e s o f t h e fi s h . T w o

h y p o t h e s e s n e e d t o b e t e s t e d . T h e f i r s t p o s t u l a t e s t h a t t h e r e l a t i o n s h i p i s

a t t ri b u t a b l e t o s o c i a l l y d e t e r m i n e d d i f f e r e n c e s i n f i sh b e h a v i o u r w h e r e a s t h e

s e c o n d p o s t u l a t e s t h a t i t i s d u e t o p a r a s i t e - i n d u c e d g r o w t h e n h a n c e m e n t .

M u c h w o r k c l e a r l y r e m a i n s t o b e d o n e t o e l u c i d a t e h o w t h e p a r a si t e s o f f is h

a n d o t h e r a n im a l s c a n m a n i p u l a t e t h e h o s t s i m m u n e a n d n e u r o - e n d o c r i n e

s y s t e m f o r th e i r o w n b e n e f i t . T h e p o s s i b i l i t y th a t p a r a s it e s m a y a l s o i n h ib i t

r e p r o d u c t i o n o f t h e i r f i sh h o s t a s w e l l a s p r o m o t i n g g r o w t h s h o u l d a l s o b e

i n v e s ti g a te d . B i r d s h a v e b e e n v e r y w e l l s t u d i e d i n th i s r e s p e c t a n d t h e n e g a -

t i v e e f f e c t s o f p a ra s i t e s o n a w i d e r a n g e o f th e i r f it n e s s c o m p o n e n t s ,

i n c l u d i n g t i m i n g o f r e p r o d u c t i o n , b r o o d s i ze , o f fs p r i n g s iz e a n d n u m b e r o f

c l u t c h e s h a v e b e e n r e c e n t l y r e v i e w e d ( M O ile r, 1 9 9 7 ). T h e r e i s e v i d e n c e t h a t

f i s h m a y a l s o i n c u r m o r e s u b t l e r e p r o d u c t i v e c o s t s f r o m p a r a s i t e s a s t h e

l a t te r m a y a d v e r s e l y a f fe c t t h e i r se x u a l b e h a v i o u r ( M c L e n n a n a n d S h i r e s,

1 9 9 5 ). H o w e v e r H a m i l t o n a n d P o u l i n ( 1 9 9 5 ) a n d S t o t t a n d P o u l i n ( 1 9 9 6 )

c o u l d f i n d n o e v i d e n c e t h a t p a ra s i te l o a d h a d a n y i n f l u e n c e o n m a l e a g g r e s -

s i o n o r p a r e n t a l c a r e i n m a l e u p l a n d b u l l i e s,

Gobiom orphus breviceps.

T h e y

s u g g e s t t h a t t h e s e d i f f e r e n c e s a r e a t t ri b u t a b l e t o t h e s e f i s h o c c u p y i n g h a r sh ,

u n p r e d i c t a b l e e n v i r o n m e n t s .



7 0 J D T H O M A S

6 4 R e a s o n s fo r t h e A b s e n c e o f H a r m f u l E f fe c t s d u e t o P a r a s it e s

The statistical analyses carried out failed to produce any evidence that the par-

asites had a detrimental effect on either the salmon parr or the trout in the Teifi.

This situation is not unique. Thus, Chubb (1973) states that most British fresh-

waters are not troubled with regular parasite problems, although parasites are

always present in abundance . Following an extensive long-term study in North

America Lemly and Esch (1985) also concluded that mortality of centrarchid

fish due to infection by U v u l i fe r a m b l o p l i t is was a rare event occurring only in

one of 43 aquatic habitats studied. Other authors have also cited a number of

case studies supporting the view that parasite infections are generally relatively

harmless to their long-term fish hosts when living under natural conditions

(Allison, 1982; Holmes, 1982; Crompton, 1991; Dorocu

et al .

1995; Bakke and

Harrris, 1998; Scholz, 1999). It can be postulated that these apparently benign

relationships between host and parasites in natural ecosystems have evolved

because it is disadvantageous for the parasite to kill the definitive host in which

it is reproducing. The host may also derive some metabolic and other benefits

from benign parasites as mentioned above. This concept can be rationalised by

reference to R0, the basic reproductive rate of the parasite which natural selec-

tion will tend to maximise. Maximising R0 will involve trade-offs between

production of transmission stages (which ideally should be high) and damage to

the host (which ideally should be small). R 0 will therefore be clearly max-

imised by the host surviving as long as possible. It can be postulated therefore

that as a result of long-term coevolution the virulence of the parasite to its host

will become attenuated and that the parasite will become adapted to the immune

defence of the host and even use it to its own advantage.

E Thomas e t a l . (2000) have recently stressed the role of the environment

in determining the outcome of host-parasite interactions. They cite some cases

where the parasites can be detrimental to host fitness in one environment but

beneficial in another and also review other cases where parasitised individuals

enjoy a selective advantage over unparasitised conspecifics.

6 5 R e a s o n s f o r s o m e P a r a s i te s C a u s i n g D e t r i m e n t a l E f fe c ts

The following reasons can be advanced to explain why parasites may become

more pathogenic and reduce the longevity of their hosts under certain circum-

stances. Firstly, selective pressure will favour parasites modifying the

behaviour of the intermediate host if this results in increasing the probability

of it being eaten by the definitive host. In such cases it may be said that the par-

asite gene is being phenotypically expressed in the host s body and Dawkins

(1990) gives many examples of this phenomenon. In this case, the intermedi-

ate hosts are acting as vehicles for transmission, rather than for reproduction.




H o w e v e r , t im i n g i s cr it ic a l a s d e v e l o p m e n t m u s t b e c o m p l e t e d f ir st . It w o u l d

b e c l e a r l y d i s a d v a n t a g e o u s f o r t h e p a r a s i t e t o k i l l i t s h o s t p r e m a t u r e l y .

Examples o f such l a rva l pa ras i t e s , wh ich inhab i t pa ren te ra l o rgans , inc lude

Diplostomum

spp . , me tace rca r iae o f

Uvulifer ambloplitis

a n d t h e m e t a c e s t o d e

l a r v a e o f Diphyllobothrium ditremum a n d Triaenophorus crassus. The f o r m e r

m a y c a u s e b l i n d n e s s w h i l s t t h e l a tt e r m a y r e d u c e h o s t a c t iv it y . H o w e v e r , ev e n

i n t h e s e c a s e s t h e r e i s e v i d e n c e t h a t t h e p a r a s i t e s m a y n o t b e h i g h l y

d e t r im e n t a l t o th e h os t . T h u s , K e n n e d y 1 9 8 3 ) c o n c l u d e d th a t th e e m p i r ic a l

ev idence sugges ted tha t d ip los tomias i s has l i t t l e o r any s ign i f i can t impac t on

n a t u r a l f i s h p o p u l a t i o n s . R a t h e r s u r p r i s in g l y R a h k o n e n a n d K o s t i 1 9 9 7 )

f o u n d t h a t t h e re w a s a s li g ht , p o s i ti v e c o r r e la t i o n b e t w e e n t h e n u m b e r s o f D .

ditremum

l a r v a e i n m u s c l e a n d t h e c o n d i t i o n f a c t o r f o r e a c h a g e g r o u p o f

b r o w n t r o u t e x a m i n e d i n L a k e I n ar i, F i n la n d . T h i s w a s t h e c a s e d e s p i t e t h e

p r e s e n c e o f s e v e r e c h r o n ic g r a n u l o m a t o u s p e r it o n it is a s s o c i a t e d w i t h t h e p a r-

a s i t e s . T h e r e w a s n o e v i d e n c e t h a t h e a v i l y p a r a s i t i s e d f i s h w e r e b e i n g

e l i m i n a t e d f r o m t h e p o p u l a t i o n . P u k k i n e n a n d V a l t o n e n 1 9 9 9 ) c a m e to a

s i m i la r c o n c l u s i o n w h e n s t u d y in g t h e e f f e c t s o f Triaenopho rus crassus l a rvae

o n t h e w h i t e f i s h

Coregonus laveratus.

T h e s e r e s u l t s s u g g e s t t h a t l o n g - t e r m

c o e v o l u t i o n h a d o c c u r r e d i n t h e s e c a se s .

Second ly , pa ras i te s inhab i t ing t i s sues o f o rgan sys tem s o the r than the gu t

t e n d t o b e m o r e p a t h o g e n i c t h a n g u t -i n h a b it in g f o r m s b e c a u s e t h e y d i r e ct l y

u t i l is e and dam age ho s t t i s sue thus genera ting a st ronger imm une r esponse . I t

i s no t surpr is ing the refore that i t i s paras i tes l iv ing on the e ye

Diplostomum),

i n t h e b l o o d s y s t e m Sanguinicola), the b o d y c a v i t y a n d v i s c e r a t a p e w o r m

larvae such as

Ligula, Schistocephalus an d Diphyllobothrium), the

s w i m b l a d -

d e r Angu illicola crassus) and g i l l s Gyrod actylus salaris a n d s e a l ic e ) w h i c h

o c c u p i e d p r i d e o f p l a c e i n a r e c e n t s y m p o s i u m d e a l in g w i t h p a r a si ti c d i s e a s e s

of f ish P ike and Le wis , 1994).

T h i r d ly , p a r a s i t e s m a y b e p a t h o g e n i c b e c a u s e o f t h e ir n o v e l t y to t h e i r f is h

h o s ts . W h e n n o v e l s p e c i e s o r g e n e t i c s t r a in s o f p a r a s it e s a r e i n t r o d u c e d i n t o

a n e w a r e a s u s c e p t i b l e e n d e m i c h o s t s m a y s u f f e r m o r t a l i t y b e c a u s e t h e y

h a v e l o w l e v e l s o f r e s is t a n c e o r i m m u n i t y t o t h e p a r a si te s . E x a m p l e s o f c a s e s

w h e r e p a r a s i te s i n t r o d u c e d i n f a r m e d f i sh h a v e c a u s e d p a r a s it e e p i d e m i c s i n

w i l d o r f a r m e d fi s h a r e g i v e n b y F r y e r 1 9 6 8 ) , K e n n e d y a n d F i t c h 1 9 9 0 ) ,

B a u e r 1 9 9 1 ) , W i ll i am s an d J o n e s 1 9 9 4 ) , K e n n e d y 1 9 9 4 ) a n d H o f f m a n

1 9 9 8 ) . A c c o r d i n g t o K e n n e d y 1 9 9 4 )

Anguillicola crassus

i s n o t p a t h o g e n i c

to i t s coev o lve d hos t , Angui l lajaponicum, i n J a p a n b u t b e c a m e p a t h o g e n i c t o

An guilla anguilla f o l l o w i n g i t s a n t h r o p o g e n i c i n t r o d u c t i o n i n t o e e l p o p u l a -

t ions in con t inen ta l Europe and Br i t a in . S imi la r ly ,

Gyrodactylus salmonis

a p p e a r s n o t t o h a v e b e e n p a t h o g e n i c t o s a l m o n i d s i n th e B a l t i c s e a b o a r d b u t

f o l l o w i n g i t s i n t r o d u c t i o n i n t o N o r w a y b y i n f e c t e d f i s h f r o m S w e d e n i t h a s

c a u s e d d e v a s t a t i n g e p i d e m i c s i n s a l m o n p a r r p o p u l a t i o n s i n a t l e a s t 3 7

N o r w e g i a n ri v e rs M o , 1 9 9 4 ). H o w e v e r , c h a n g e s i n t h e g e n e t i c c o m p o s i t i o n



7 2 J D T H O M A S

of the fi sh ( Johnsen an d Jensen , 1991) and env i ronm en ta l ch anges in the r ive r

s y s t e m s m a y h a v e b e e n c o n t r i b u t o r y f a c t o r s i n c a u s i n g t h e e p i d e m i c s

( H e g g b e r g e t a n d J o h n s e n , 1 9 8 2 ) . T h e s e e x a m p l e s c a n b e e x t e n d e d t o o t h e r

t a x a in c l u d in g b i rd s a s D o b s o n a n d M c C a l l u m ( 1 9 9 7 ) h a v e s h o w n h o w p a r -

a s i te s f r o m b i r d i n t r o d u c t io n s c a n p l a c e r a r e, t h r e a t e n e d n a t i v e b i rd s p e c i e s

unde r inc reased th rea t. The ever - inc reas ing danger s o f f i sh pa ras i t e s , inc lud -

i n g t h e c e s t o d e

B o t h r i c e p h a l u s a c h e i l o g n a t h i ,

s p r e a d i n g g l o b a l l y d u e t o

i n a d e q u a t e c o n t r o l o f f i sh i m p o r t a t io n s h a v e a g a i n b e e n s t r e s se d r e c e n t l y b y

Scho lz (1999) .

I n e n d e m i c a r e as w h e r e t h e h o s t s a n d p a r a s it e s h a v e c o e v o l v e d o v e r l o n g

p e r i o d s n e w l y i n t ro d u c e d p o p u l a t io n s o f a s u s c e p t i b l e h o s t s p e c i e s m a y s u f fe r

h i g h m o r t a l i t y b e c a u s e t h e y h a v e a l o w e r r e s i s t a n c e o r i m m u n i t y t o t h e

ende m ic pa ras i te s .

F o u r th l y , p a r a si te s p e c i e s m a y b e c o m e m o r e p a t h o g e n i c a n d c a u s e m o r ta l -

i t y i f t h e h o s t p o p u l a t i o n s a r e p l a c e d i n a n e w e n v i r o n m e n t t h a t i s h i g h l y

favourab le to t r ansmis s ion . Examples a re p rov ided by f i sh f a rms and smal l ,

c l o s e d s y s t e m s s u c h a s p o n d s o r s m a l l la k e s. T h e r e a r e n u m e r o u s r e p o r t s o f

ep idem ics and f i sh mor ta l it i e s w hen hos t f i sh a re l iv ing a t h igh dens i t i e s under

these cond i t ions (Dog ie l , 1961 ; Morav ec , 1994 ; Ron ga 1995 ; Ho f fma n , 1998 ;

Scho z 1999 , Rahkonen

e t a l . ,

1996) . An ana logous example i s p rov ided by

T r i c h o s t r o n g y l u s t e n u i s w h i c h i s k n o w n t o b e p a th o g e n i c t o r e d g r o u s e i n w e t

m oors b u t is o f li t tl e impor tanc e in d ry m oors w here the su rv iva l o f the in fec -

t ive l a rvae is low (Do bson and M cC al lum , 1997).

The re i s a l so some ev ide nce tha t pa ras i te s m ay have de le te r ious e f f ec t s on

f i sh in ha r sh na tu ra l eco sys tem s . Thus , P ukk inen and Va l tonen (1999) c la im

tha t bac k ca lcu la t ions r evea led tha t, am ongs t the o lde r wh i te f ish , the sm al le r

ones ha rboured m ore pa ras it e s than the l a rge r ones . Ho f fma n e t a l . (1986) a l so

f o u n d t h a t t h e r e w a s a n i n v e r s e r e l a t i o n s h i p b e t w e e n t h e c o n d i t i o n f a c t o r ,

p a c k e d c e l l v o l u m e , r e d b l o o d c e ll c o u n t a n d h a e m o g l o b i n l e v el an d t h e n u m -

b e r s o f c e s t o d e s E u b o t h r i u m s a l v e l i n i ) in the arc t ic char t. Ho we ver , the whi te

b lood ce l l coun t inc reased w i th inc reas ing pa ras i t e in tens i ty ind ica t ing the

d e v e l o p m e n t o f im m u n i ty . T h e s e a u t h or s c o n c l u d e d t h a t t h e d e c l in e i n c o n d i -

t io n f a c t o r m i g h t b e c a u s e d b y c o m p e t i ti o n f o r f o o d r a t h e r t h an b y p a r a si te s .

T h e e n v i r o n m e n t b e i n g h i g h l y o l i g o t r o p h i c e x a c e r b a t e d t h i s . A y a l a

e t a l .

(1992) a l so c la im tha t

N e o c h i n o r h y n c h u s c y l i n d r a t u s

in the la rge -m outh ba s s ,

M i c r o p t e ru s s a l m o i d e s ,

m ay harm the ir hos t s by lower ing p ro te in d iges t ib i l i ty

and am ino ac id ava i l ab il ity .

F i fth ly , pa ras i te s can bec om e mo re ha rmfu l to the hos t a s a re su l t o f dam age

t o t h e in n a t e a n d a d a p t iv e a r m o f th e i m m u n e s y s t e m c a u s e d b y d e t r im e n t a l

c h a n g e s i n t h e e n v ir o n m e n t . E x a m p l e s a r e p r o v i d e d b y l o w w a t e r te m p e r a t u re

(Chubb , 1982 ; Hard ie

e t a l . ,

1 9 9 4 ; L e M o r v a n

e t a l . ,

1998; Berns te in

e t a l . ,

1998) , specif ic pol lu tants including hea vy metals (Dunier , 1996 ) and am m onia

(Hurv i tz e t a l . , 1997) , genera l hab i ta t deg rada t ion (B akke and Har r r is , 1998)




a n d s tr e ss d u e to o v e r c r o w d i n g o r s t a rv a t io n W a a g b o

e t a l .

1 9 9 4 ) . T h e

i m m u n e r e s p o n s e m a y a l s o b e su p p r e s s e d b y r e p r o d u c t iv e a c t iv i ty M ¢ l l e r,

1 9 9 7 ). H o w e v e r , a c c o r d i n g to D e m e r s a n d B a y n e 1 9 9 7 ) al t h o u g h c h ro n i c

s t re s s is i m m u n o s u p p r e s s i v e a c u t e s t r e ss m a y h e l p e n h a n c e b o t h c e l l u l ar a n d

h u m o r a l c o m p o n e n t s o f in n a t e d e f e n c e s i n r a in b o w t ro u t. I t m a y a l s o b e s u g -

g e s t e d t h a t i m m u n o s u p p r e s s i o n r e s u l t i n g f r o m l o w e r i n g i n t e m p e r a t u r e ,

r e p r o d u c t i v e a c t i v i t y a n d c h a n g e s i n d i e t m a y b e r e s p o n s i b l e f o r s e a s o n a l

changes in pa ras i t e numbers .

6 6 C o n c l u s io n s

D e s p i t e t h e f a c t t ha t s o m e o f th e h e l m i n t h p a r a s i te s e n c o u n t e r e d d a m a g e d t h e

t i ss u e s o f t h e ir s a l m o n i d h o s t s t h e r e w a s n o e v i d e n c e t h a t t h e y c a u s e d m o r t al -

i ty o r tha t they had a de t r im en ta l e f f ec t on the g row th o f the i r hos ts . To the

con t r a ry i t wa s found tha t pa ras i te a bundan ce w as s ign i f ican t ly co r r e la ted w i th

t h e c o n d i t i o n f a c t o r a n d a d i p o s e i n d e x i n s o m e c a s e s . F u r t h e r r e s e a r c h i s

n e e d e d t o t e s t th e f o l l o w i n g h y p o t h e s e s t o a s c e r ta i n t h e p o s s i b l e m e c h a n i s m s

tha t migh t exp la in these pos i t ive r e la tionsh ips . F i r s t ly , they m ay b e due to the

h ie ra rch ica l beha v ioura l pa t t e rns o f s a lm on id f i sh . As a r e su lt the la rger , dom -

i n an t f i s h te n d t o i n g e st m o r e i n f e c t e d i n t e rm e d i a t e h o s t s b e c a u s e t h e y s p e n d

m ore t ime in the tr ansmis s ion s i te s wh ich a re the s ed ime n t -depos i t ing m ic ro -

hab i t a t s f avou red by the in te rmed ia te hos t s . Secon d ly , i t i s pos tu la ted tha t the

pos i t ive r e la t ionsh ips may be due to the pa ras i t e s man ipu la t ing the immune

a n d n e u r o e n d o c r i n e s y s t e m o f t h e h o s t s to s t i m u l a te t h e i r s o m a t i c g r o w t h a n d

inh ib i t r ep roduc t ion . I t i s a rgued tha t these apparen t ly ben ign r e la t ionsh ips

b e t w e e n t h e h e l m i n t h p a r a si te s a n d t h e ir s a l m o n i d h o s t s h a v e e v o l v e d b e c a u s e

i t is d i s advan tageous fo r the pa ras i te to k i ll t he ho s t on w h ich i ts b io log ica l f i t-

nes s depends . Fu r the r w ork i s a l so needed to deve lop a be t t e r under stand ing o f

the benef i t s tha t the hos t ma y de r ive f rom i t s pa ras i te . Ho s t -pa ras i t e r e l a t ion -

s h ip s c a n n o t b e a d e q u a t e l y d e s c r i b e d b y t h e s i m p l e + a n d - s ig n s. I t m a y b e

s u g g e s t e d t h a t t h e a p p a r e n t l y b e n i g n r e l a t i o n s h i p s b e t w e e n p a r a s i t e s a n d

sa lmon id f i sh in the Te i f i a r e a t t r ibu tab le to the f ac t tha t hos t s and pa ras i t e s

have co evo lved a t l eas t s ince the l a s t i ce age . How ever , the ev ide nce sug ges t s

tha t th i s de l i ca te ba lance cou ld be eas i ly upse t by an th ropogen ic in f luences

inc lud ing the in t roduc t ion o f new g ene t i c s t r a ins o f e i the r hos t s o r pa rasi t e s

dur ing s tock ing o r by hab i t a t des t ruc t ion and po l lu tion . I t is p robab ly t rue to

s a y t h a t m o s t o f t h e m a j o r d i s e a s e e p i d e m i c s i n t h e w o r l d t o d a y h a v e b e e n

cause d by inadver ten t hum an in terven t ion .

T h e m e d i c a l a n d v e t e r i n a r y im p o r t a n c e o f p e r si s t e n t e p i d e m i c s i n a n th r o -

p o g e n i c a l l y d i s t u r b e d e n v i r o n m e n t s m a y h a v e c a u s e d p a r a s i t o l o g i s t s t o

d e v e l o p a n e x a g g e r a t e d v i e w o f t h e h a r m f u l e f f e c t s c a u s e d b y p a r a s it e s . I n

o r d e r t o o b t a in a m o r e b a l a n c e d v i e w f u r t h er w o r k t o a s s e s s th e i m p a c t o f



74 J D THOMAS

paras i t e s on hos t evo lu t ion in na tu ra l popu la t ions i s the re fo re ind ica ted . In

th is c onn ec t ion i t i s o f in te res t tha t a r ecen t s tudy on the im pac t o f b lo od pa r -

a s i t e s o n b i r d s p e c i e s d i d n o t s u p p o r t a r o l e f o r p a r a s i t e s i n t h e o v e r a l l

m a i n t e n a n c e o f g e n e t i c v a r ia t i o n v i a f r e q u e n c y - d e p e n d e n t s e l e c t i o n (P o u l i n

e t a l . 2000) .

7 S E X B IA S IN P A R A S I T IS M A N D C A U S A T I V E M E C H A N I S M S

7 1 I n t r o d u c t i o n

The ques t ion o f wh e the r the re i s a s ex b ias in pa ras i t i sm i s impo r tan t in v iew

o f it s r e le v a n c e t o th e w i d e l y c it e d H a m i l t o n - Z u k ( H a m i l to n a n d Z u k , 1 9 8 2)

and immunocompetence (Fo l s tad and Kar te r , 1992 ; Zuk 1992 ; H i l lga r th and

W i n g fi e ld , 1 9 9 7) h y p o t h e se s . T h e H a m i l t o n - Z u k h y p o t h e s i s is b a s e d o n t h e

fo l lowing as sumpt ions :

1 . A se t o f pa ras i t e s w i l l adve r se ly a f fec t hos t f i tnes s and suscep t ib i l i ty to

paras i tes i s inher i tab le .

2 . The expres s ion o f s econd ary s exua l cha rac te rs is pa r t ly depen den t on hos t

cond i t ion and the re fo re on pa ras i t e r e s i s t ance genes . Hami l ton and Zuk

a r g u e d t h e r e f o r e t h a t e l a b o r a t e m a l e s e c o n d a r y s e x u a l c h a r a c t e r s h a v e

e v o l v e d t h ro u g h f e m a l e c h o i c e b e c a u s e th e y p r o v i d e h o n e s t i n f o rm a t i o n

abo u t he r i t ab le r es i s t ance to pa ras it e s .

3 . F e m a l e s a re a b l e t o e v o l v e a d i s c r im i n a t o r y p r e f e r e n c e f o r s e c o n d a r y

sexua l ch a rac te rs tha t r evea l gene t i c suscep t ib i l i ty to pa ras i ti sm.

S o m e o f t h e m a i n a s s u m p t i o n s a n d p r e d ic t io n s b a s e d o n th e i m m u n o c o m p e -

t e n c e a n d H a m i l t o n - Z u k h y p o t h e s i s a re a s f o l lo w s :

1. M a l e v e r t e b r a t e s w i l l b e m o r e v u l n e r a b l e t o i n f e c t i o n t h a n f e m a l e s

b e c a u s e t e s t o s te r o n e i s i m m u n o s u p p r e s s iv e .

2 . M a l e a n im a l s t h a t n e e d h ig h t e s t o s te r o n e le v e l s t o p r o d u c e s e c o n d a r y

sexua l cha rac te r s w i l l be m ore v u lne rab le to pa ras it i sm.

3 . Spec ies ha rbour ing ha rm fu l pa ras i t e s ove r the i r evo lu t ionary h i s to ry w i l l

be m ore l ike ly to evo lve ex t ravagan t s ex ua l ly d imorph ic t r ai t s (Scha l l and

Staats, 1997).

4 . W hen spec ies w i th ex t r avagan t s exua l ly d imo rph ic t ra i ts a r e com pared

w i t h o t h e r s w i t h m o r e s u b d u e d d i m o r p h i c t ra i ts t h e m a l e s i n th e f o r m e r

case w i l l be mo re heav i ly pa ras it i sed .

5 . In fec t ions w i l l r edu ce t e s tos te rone l eve l s thus caus ing s econda ry s exua l

charac te r s to be poor ly expres sed .



7 6 J D T H O M A S

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7 8 J D T H O M A S

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v a r i a n c e w e r e v e r y s m a l l ( 0 . 7 2 , 4 . 8 4 a n d 0 . 5 4 , r e s p e c t i v e l y ) c o m p a r e d

w i t h o t h e r v a r ia b l e s s u c h a s s e a s o n , s t a t io n a n d a g e o f t h e tr o u t.

T a b le 2 6 s h o w s t h a t a l t h o u g h t h e f e m a l e t r ou t i n t h e s a m p l e a r e s ig n i f i c a n t ly

l o n g e r th a n th e m a l e s a n d a l s o h a v e a t e n d e n c y t o b e h e a v i e r , th e i r m e a n c o n -

d i t i o n f a c to r w a s s i g n i f i c a n t l y l e s s t h a n th a t o f m a l e s .

U n l i k e t h e t r o u t t h e r e w e r e n o s i g n i f i c a n t d i f fe r e n c e s b e t w e e n e i t h e r t h e

p r e v a l e n c e o r a b u n d a n c e v a l u e s f o r t h e t o t a l n u m b e r s o f p a r a si te s o r th e n u m -

b e r s o f i n d i v i d u a l p ar a s it e s f o u n d i n m a l e a n d f e m a l e s a l m o n p a r r ( T a b l e 2 7 ,

F i g u r e 1 6 ). M u l t i p l e r e g r e s s i o n a n a l y s e s a l s o r e v e a le d t h a t t h e s e x o f th e

s a l m o n p a rr is n o t a s i g n i f ic a n t p r e d i c t o r o f t h e t o t a l n u m b e r s o f p a r a s it e s o r o f

t h e n u m b e r s o f in d i v i d u a l p a r as it e s p e c ie s f o u n d ( P = 0 . 4 4 0 - 0 . 9 8 0 ) . A s w i t h

t h e t r o u t t h e c o n t r i b u t i o n s m a d e t o t h e t o ta l v a r ia n c e b y t h e t o t a l n u m b e r o f

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F igu re 6 The m ean abundance (_+ 95 C.L.) of the parasites of m ale and female

salm on parr.



80 J D THOMAS

p a r a s i t e s a n d n u m b e r s o f i n d i v i d u a l p a r a s it e s p e c i e s w e r e v e r y s m a l l

(0 .00 5-3 .04 ) com pared w i th o the r va r i ab les such as s eason , s t a tion and age

of the t rou t.

The r esu l ts fo r trou t a r e in acco rd w i th the fo l lowing c ases in wh ich f em ale

f i sh were a l so more heav i ly pa ras i t i s ed than males : F lo r ida Gar f i sh in fec ted

w i t h m e t a c e r c a r i a e o f

O dner i o t rem a i ncom m odum

( L e i g h 1 9 6 0 ) ,

Rut i lus

rutilus in fec ted w i th Caryophaeidesfennica (Borgs t r6mand Ha lvor sen , 1968) ,

Leu ciscus leuciscus

i n f e c te d w i t h

Caryophyllaeus laticeps

(Kennnedy, 1968) ,

Eso x lucius i n f e c t e d w i t h Triaenophorus nodulosus (Borgs t r6m, 1970) , Salmo

sa l ar

i n c o a s t a l L a b r a d o r i n f e c t e d w i t h

Bunodera luc iopercae

a n d

Diplostomu m spathaceum

(H icks and Threl fu l l , 1973) ,


i n f e c t e d w i t h

Neoechinorhynchus cyl indratus

(Eure , 1974) ,

Fundulus hetero-

clitus

in fec ted w i th

Eustrongylides

sp . (Hirschf ie ld

et a l.

1983) and whi te f i sh ,

Coregonus laveratus


Diphyl lobothr ium d i tremum

(Ta lonen

et

al.

2000) .

In con t r ast , ma le f i sh we re mo re heav i ly pa ras i ti s ed : than the f emales in the

fo l lowing cases : b rown t rou t f rom 5 to 7 yea r s o ld in feo ted w i th

Discocotyle

sagit tata

(Pal ing , 1965, 1969) ,

S. salar


~ ubo t hr i um crassum

(H ick s and Thre l fu l l , 1973) , sexua l ly m atu re b ro wn t rou t , in fec ted w i th a va r i-

e ty of funga l patho gen s and ectoparas i tes (P icker ing and 'Ch r is tie , 1980) , three

species of c ichl ids infected wi th helminths (Batra , 1984) and rays infected w i th

Calicotyle kroyeri

(W i l li ams and Jones , 1994) . Re im chen ' and N os i l (2001) in

an ex tens ive 15 -year s tudy on s ex -b iased pa ras i ti sm in th reesp ine s t i ck leback ,


a l so found tha t the overa l l pa ras i t e p reva lence was

grea te r in ma les than in f emales . However , the exces s d id no t occur fo r each

s p e c i e s o f p a r as it e . M a l e s h a d h i g h e r p r e v a l e n c e o f th e c e s t o d e

Cyathocephalus truncatus

and the t r ematod e

Bunodera

sp . re la t ive to fem ales ,

w h i l e f e m a l e s h a d h i g h e r p r e v a l e n c e o f t h e c e s t o d e Schistocephalus sol idus

and nem atodes . Sex b ias in f i sh pa ras it e s has a l so been r epor ted to change s ea -

sona l ly . Thus ,

M onobo t hr i um u l m er i

o c c u r r e d o n l y i n m a l e

Er i m yzon

oblongatus

f r o m F e b r u a r y t o M a y b u t b y J u n e i t w a s c o m m o n e r i n f e m a l e f is h

(Gr imes and Mil ler , 1976) .

The abse nce o f s ex b ias in pa ras i t ic in fec t ion o f f i sh has a l so been no ted in

t h e s t i c k l e b a c k ,

Gasteros teus aculea tus

( B a k k e r an d M u n d w i l e r , 1 9 9 9 ) ,

Onchorhynchus mykiss (Va l le s R io s and Ru iz Cam pos , 1992) and in juve n i l e

s a l m o n p a r r f r o m t h e T e i f i i n t h e p r e s e n t i n v e s t i g a t i o n . H a l e y ( 1 9 5 8 ) ,

D u d z i n s k i a n d M y k o t o w y c z ( 1 9 6 3 ) a n d S c h a lk a n d F o r b e s (1 9 9 7 ) h a v e a ls o

c o m m e n t e d o n t h e a b s e n c e o f s ex b i a s in p a r a si ti s m o f j u v e n i l e m a m m a l s .

S imi la r conf l i c t ing r esu l t s have been enc oun te red in am ph ib ia and r ep t il e s .

T h o m a s ( 1 9 6 5 ) f o u n d t h a t th e i n t e n si ty o f in f e c ti o n o f

Mesocoel ium monodi

was s ign i f i can t ly h igher in f emale A g a m a l izards than in the larger males . In

c o n tr a st , m a l e f r o g s w e r e f o u n d t o b e m o r e h e a v i l y p a r a si ti s e d t h a n f e m a l e s

( H i c k m a n , 1 9 6 0 ; L e e s , 1 9 6 2 ) . U s i n g d a t a f r o m 3 3 s t u d i e s M c C u r d y

et al .




(1998) foun d no overa l l d i f fe rence in p reva lence o f pa rasi te s b e tw een m ale and

fem ale b reed ing o r non-b reed ing b i rds . How ever , they found tha t in fec t ions by

H o m o p r o t e u s t h e

m o s t c o m m o n g e n u s o f b l o o d p a r a s it e , w e r e s i g n i f ic a n t ly

c o m m o n e r a m o n g b r e e d i n g f e m a l e s t h a n b r e e d i n g m a l e s . A g a i n , w h e n t h e

a n a l y s e s w e r e r e s t ri c te d t o b r e e d i n g b i r d s o f p o l y g y n o u s s p e c i e s f e m a l e s w e r e

m o r e l i k e l y to b e i n f e c t e d th a n m a l e s. A f t e r e x a m i n i n g e v i d e n c e o f s e x b i a s in

3 8 p u b l i s h e d s t u d ie s o f m a m m a l s S c h a l k a n d F o r b e s ( 1 9 9 7 ) f o u n d n o s e x b i a s

in the case o f he lmin th pa ras i te s a l though the re wa s a ma le b ias in pa ras it i sm

overal l and for ar thropod paras i tes in part icu lar. T he y conc lud ed how ev er that,

on average , d i f f e renc es in pa ras i t i sm be t w een the s exes a re smal l and s tat is t i-

ca l ly s ignif icant m ale b iase s in paras i t ism are not a general ru le . Sher idan e t a l .

(2000) ca m e to a s imi la r conc lus ion w i th regard to a r th ropods as these au thor s

s ta te : ' ove ra l l ma le and f emale a r th ropods d id no t d i f f e r in p reva lence o r in

in tens ity o f pa ras i te in fec t ions ' .

T h i s r e v i e w i l lu s t ra t e s t h e d a n g e r o f g e n e r a li s in g f r o m o n e e x a m p l e a s

W e d e k i n d a n d J a k o b s e n ( 1 9 9 8 ) a t t e m p t e d w h e n t h e y f o u n d a m a l e - b i a s e d s u s-

c e p t i b il it y t o h e lm i n t h i n f ec t io n i n o n e s p e c i e s o f c o p e p o d . T h e y c o n c l u d e d

tha t ' the pa t t e rn (m ale s ex b ias) s een in ma ny ve r teb ra tes can be ex tended to an

inver teb ra te hos t tha t l acks t e s tos te rone ' . H ow ever , f rom the abov e ev iden ce i t

mu s t be co nc lud ed tha t s t a ti s ti ca lly s ign i fi can t ma le b iases in pa rasi t ism do n o t

occ ur a s a ge nera l ru le fo r e i the r ve r teb ra tes o r inver teb ra te hos t s.

M a l e v e r t e b r a t e s w i l l b e m o r e v u l n e r a b l e t o i n fe c t io n b e c a u s e t e s to s t e ro n e i s

i m m u n o s u p p r e s s i v e

M any in f luen t ia l r ev iewers suppor t th i s v iew (Gl ick , 1986; G ros sman , 1990 ;

S la te r Schreck , 1993 ; Z uk and M cK ean , 1996 ; K le in and Ne lson , 1999;

Kle in , 2000a , b ) wh i le o the r s c la im tha t oes t rogen enhances im m uni ty (Ha ley ,

1958; Do bso n, 1961a, b ; Lees and Bass , 1960; Ha l l

e t a l .

1978; Brown, 1994).

M o r e r e c e n t l y D u f f y e t a l . ( 2 0 0 0 ) h a v e p r o v i d e d f u r t h e r e x p e r i m e n t a l e v i -

d e n c e t h a t t h i s h o r m o n e s u p p r e s s e s b o t h c e l l a n d h u m o r a l i m m u n i t y i n a

spec ies o f songb i rd . There i s a l so ev idence tha t t e s tos te rone may benef i t the

paras i te s d i r ec t ly by enhanc ing the i r deve lopme n t , g rowth and su rv iva l i n v i t ro

(F leming , 1985) and i n v i v o ( H a r d e r e t a l . 1992)

Ho we ver , the fo l lowing exper im en ta l r e su l t s a re in conf l i c t w i th the w id e ly

acc epte d v iew that tes tos teron e is imm unosu ppress ive . F i rs tly, a l though tes tos -

t e ro n e , o e s t ro g e n a n d p r o g e s te r o n e m a y s u p p r e s s p a rt s o f t h e i m m u n e s y s t e m

they may a l so under ce r ta in cond i t ions have a s t imu la to ry e f f ec t (Gros sman ,

1990) . Second ly , t e s tos te rone , d ihydrox y tes tos te ro ne and oes t rad io l enhance d

c e l l -m e d i a t e d im m u n i t y t h r o u g h d i r e ct a c ti o n o n t h e i m m u n e c e l ls o f b o t h

male and f emale S ibe r ian hams te r s (B ib io and Ne lson , 2001) . Th i rd ly , s ec -

o n d a r y a n t i b o d y p r o d u c t i o n i n r e d w i n g b l a c k b i r d s w a s n o t s u p p r e s s e d b y



82 J D THOMAS

testosterone either at physiological levels or above normal concentration

(Hasselquist

e t a l .

1999). Fourthly, testosterone was found not to suppress

existing immunity against

P l a s m o d i u m c h a b a u d i

malaria in female mice

although it appeared to prevent the development of protective immunity

(Wunderlich

e t a l .

1992). Fifthly, Klein and Nelson (1997) concluded that

circulating testosterone does not mediate sex differences in immunocompe-

tence or body mass in P e r o m y s c u s c a l i f o r n ic u s . Sixthly, there was no evidence

that a higher androgen concentration in polygynous male voles influenced sex

or species differences in immune function (Klein and Nelson, 1998).

Seventhly, Hillgarth and Wingfield (1997) pointed out that many sexual char-

acters in birds are not under the control of testosterone and concluded that there

is little evidence that circulating levels of testosterone are immunosuppressive

in wild birds. Visco (1973) and Hillgarth and Wingfield (1997) also concluded

that there is no evidence that increasing testosterone levels can influence par-

asite intensity. There are also conflicting views regarding the claim that

oestrogen is beneficial to parasites as Wang and Belosevic (1994) found that

oestradiol increases the susceptibility of goldfish to trypanosomes while

Sonnex (1998) has suggested that it may also enhance the pathogenicity of

many urogenital microorganisms.

It must be concluded therefore that the evidence that testosterone is

immunosuppressive or that sex hormones in general can influence the immune

response or parasite burdens is equivocal. The cautionary note that it remains

to be seen whether natural levels of testosterone or any other steroid can influ-

ence parasite intensity in free living wild birds by Hillgarth and Wingfield

(1997) is therefore very opportune and can be extended to all other animal

taxa.

Many reasons can be advanced to explain the apparently conflicting effects

of testosterone and other sex hormones on the immune mechanisms and the

parasites when animals are kept under experimental conditions. These include

variation in the nature of the host or parasite genotypes, the dosage rate of the

hormone used, interactions between hormones, the handling and maintenance

regimens and the physiological state of the animal when treated. Klein e t a l .

(1997) have demonstrated that both the genotype and the social environment of

voles may influence the immune function. Thus male meadow voles had higher

immune responses than females when housed in pairs whereas the converse

was observed in the case of the prairie vole. Wedekind (1992, 1994) has also

suggested that the parasite genotype may influence the nature of the immune

response and the development of secondary sex characters in roach.

The immune function can also be influenced by changing photoperiod

(Nelson

e t a l .

1998) and by seasonal changes in general (Nelson and Demas,

1996; Pickering, 1989; Pottinger and Carrick, 2000). Seasonally induced stres-

sors may influence the hypothalamic-pi tuitary-interrenal axis, resulting in

elevated levels of glucocorticoids, inhibition of sex hormones and modulation




of the im m une sy s tem in t rou t and o the r an imals P icke t ing , 1989 ; N e l son and

De m as , 1996) . Thus , S la te r and Schrec k 1993) have show n tha t co r t i so l m ay

a c t s y n e r g i s t i c a l l y w i t h t e s t o s t e r o n e t o s u p p r e s s t h e d e v e l o p m e n t o f l e u c o -

cy tes in f i sh under

n v t r o

c o n d i ti o n s . A c c o r d i n g to B r o w n 1 9 9 4 ) , h o w e v e r ,

p o t e n t m o d u l a t o r s o f th e i m m u n e s y s t e m s u c h a s c o r t i c o st e r o id s m a y a c t i n

e i th e r a s t i m u l a t o ry o r i n h i b it o r y m a n n e r d e p e n d i n g o n a n u m b e r o f fa c t o r s

i n c lu d i n g t h e c o n c e n t ra t io n u s e d o r l en g t h o f e x p o s u r e . I t m u s t b e c o n c l u d e d

t h e r e f o re th a t m u c h w o r k re m a i n s t o b e d o n e t o i m p r o v e o u r u n d e rs t an d i n g o f

t h e in v o l v e m e n t o f th e e n d o c r i n e s y s t e m i n i n fl u e n c in g t h e i m m u n e m e c h a -

nism in ver tebra tes in gene ra l and f ish in par ticu lar.

De sp i t e ou r l imi ted under s tand ing o f the sub jec t the pos s ib i l i ty tha t the

e n d o c r i n e a n d i m m u n e s y s t e m s m a y b e i m p l i c a te d i n i n fl u e n c in g t h e p a ra s it e

f auna o f the s a lm on ids in the R iv er Te i f i can b e cons ide red . I t can b e hypo th -

es i s ed tha t the absence o f s ex b ias in the p reva lence and abundan ce o f pa rasi te s

o f s a lm on pa r r i s a t tr ibu tab le to these f i sh be ing juven i l e s . As a r e su l t i t can b e

p o s t u l a t e d t h at t h e e n d o c r in e a n d i m m u n e s y s t e m s w o u l d b e id e n t ic a l i n m a l e

and fem ale juv eni le par r, unl ike adul t f i sh Sch alk and Forbes , 1997). How ever ,

th is hyp o thes i s r equ i r es exper im en ta l v e r i f ica t ion as the m ajo r i ty o f the ma le

s a l m o n p a r r h a d e n l a r g e d p r e c o c i o u s l y d e v e l o p e d t e s te s d u r in g t h e b r e e d i n g

s e a so n . I f a n d r o g e n s w e r e i n f a c t i m m u n o s u p p r e s s i v e t h e n a m a l e b i a s i n p a r-

a s i ti s m o f t h e s a l m o n p a r r w o u l d t h e r e fo r e b e e x p e c te d . T h e l a c k o f s e x b i a s i n

paras i t i sm o f the s a lm on pa r r the re fo re p rov ides c i r cums tan t i a l ev ide nce tha t

a n d r o g e n s m a y n o t b e s t r o n g l y i m m u n o s u p p r e s s i v e a s c l a i m e d b y Z u k a n d

M c K e a n 1 9 9 6 ) , K l e i n a n d N e l s o n 1 9 9 9 ) a n d K l e i n 2 0 0 0 a , b ) . T h e p o ss i b il -

i ty tha t the pa ras i t i c f auna o f ma le and f emale s a lmon pa r r migh t have been

i n f lu e n c e d b y b e h a v i o u r a l d i f f e r e n c e s b e t w e e n t h e s e x e s c a n b e e x c l u d e d , a s

the re we re no s ign i f i can t d i f f e rences be tw een the i r mean s i zes o r d ie ta r i e s.

The pos s ib i l i ty tha t the s t rong f emale b ias in p reva lence and abundance o f

pa ras i te s in m a tu re Te i f i t rou t m ay b e a t t r ibu tab le to s exua l d i f f e rences in the

e n d o c r i n e o r i m m u n e s y s t e m s m a y a l s o b e c o n s i d e re d . P o t t i n g e r a n d C a r ri c k

2000) found tha t p lasma t e s tos te rone l eve l s in r a inbow t rou t were h igher in

f e m a l e t h a n i n m a l e t r o u t f r o m S e p t e m b e r t o Ja n u a r y . I f t e s t o s t e r o n e i s

i m m u n o s u p p r e ss i v e, a s c l a im e d b y G r o s s m a n 1 9 9 0) , Z u k a n d M c K e a n

1996) , K le in and Ne l son 1999) and K le in 2000a , b ), then it f o l low s tha t th is

obse rva t ion m igh t exp la in the f em ale s ex b ias in pa ras it i sm.

A c ons ide ra t ion o f l i fe h i s to ry s t r a teg ies he lps to exp la in w hy f em ale t rou t

have h igher t e s tos te rone l eve l s than the i r ma le con spec i f i c s . It is we l l know n

tha t androgens p rom ote dom inan t soc ia l behav iour in ve r t eb ra tes inc lud ing f ish

and ma m m als and tha t it i s genera l ly the males tha t a r e the dom inan t s ex w i th

the h igher androgen l eve l s M unro and P i tche r , 1985) . How ever , in the case o f

t h e b r o w n t r o u t f e m a l e s a r e la r g er t h a n t h e m a l e s p r e s u m a b l y b e c a u s e o f t h e

h i g h e r e n e r g y c o s t s o f p r o d u c i n g o v a c o m p a r e d w i t h s p e rm s . T h e y t h e r e f o re

need to be hav e aggres s ive ly to ob ta in f avo urab le f eed ing t e r ri to r i es . A l thoug h



8 4 J D T H O M A S

i t i s the m ale t rout that dem arcate ter r i tor ies dur ing the reprodu ct ive seaso n the

fem ale t rou t a l so has to beh ave aggres s ive ly . Thus , i t i s the f em ale t rou t r a the r

than the male tha t mak es the dec i s ions regard ing the t iming , loca t ion and con-

s t ruc t ion o f r edds . Fem ale t rou t ma y cons t ruc t an av erage o f 5 .7 r edds du r ing

the b reed ing s eason and may thus mate w i th s evera l d i f f e ren t ma les (Bar laup

e t a l . 1994) . Fur therm ore , i t i s the fem ale t rout that in i t ia te m at ing b y ovipo s i t -

i n g i n re d d s . T h e y m a y a l s o h av e t o c o m p e t e w i t h f e m a l e c o n s p e c i f i c s f o r t h e

key r esource fo r succes s fu l r ep roduc t ion , nam ely the op t ima l m ic rohab i ta t s fo r

r edd fo rmat ion . I t i s no t su rp r i s ing the re fo re tha t they have h igher androgen

leve l s than m ales du r ing the b reed ing s eason . The re i s an in te res ting s imi la r -

i ty h e r e b e t w e e n t h e t r o u t a n d b i r d s s u c h a s W i l s o n s a n d r e d - n e c k e d

pha la rope . In these b i rd spec ies the f emales , w h ich a re l a rge r and ha ve b r igh te r

p lumage than the males , have more t e s tos te rone in the i r ovar ies than males

have in the ir t e s te s p r io r to incuba t ion (Hohn , 1970). H owe ver , wh en the m ales

s tar t to incuba te the pos i t ion is reve rsed (H i l lgar th and Win gf ie ld , 1997) .

There i s a t l eas t one o the r exp lana t ion fo r f emale s ex b ias tha t a l so invo lves

h o r m o n e s . P o t t i n g e r a n d C a r r i c k ( 2 0 0 0 ) a l s o f o u n d t h a t t h e fe m a l e h o r m o n e

oes tr ad io l-1713 leve l s we re s ign i f i can t ly g re a te r in f em ale than in male r a in -

b o w t r o u t t h r o u g h o u t t h e s t u d y p e r i o d a n d t h a t th i s d i ff e r e n c e w a s m a x i m a l

d u r i n g t h e r e p r o d u c t i v e o r p o s t - r e p r o d u c t i v e p e r i o d ( S e p t e m b e r a n d

January ) . P rev ious s tud ies had shown tha t oes t r ad io l -17 [3 and t e s tos te rone

have d iam et r i ca l ly op po sed e f f ec t s on s t r es s r e spon s ivenes s in t rou t, w i th the

fo rm er enhanc ing , and the l a t te r suppres s ing the co r t i so l r e sp ons e to a s tr e s -

s or. A s t h e r e i s e v i d e n c e t h a t s t re s s h o r m o n e s , c o r t i c o s t e r o id s , m a y r e d u c e

i m m u n i t y t o p a r a s it i s m ( P i c k e r i n g a n d P o t t in g e r , 1 9 8 5 , 1 9 8 7 ) t h e r a i s e d

l e v e l s o f oe s tr a d io l -1 7 [ 3 i n f e m a l e t r o u t m a y e x p l a i n t h e f e m a l e s e x b i a s i n

t r o u t p a ra s i ti s m . S e x u a l d i m o r p h i s m i n th e g l u c o s t e r o i d r e s p o n s e t o s t r e ss ,

w i t h t h e f e m a l e b e i n g m o r e r e s p o n s i v e th a n t h e m a l e , h a s a l s o b e e n o b s e r v e d

i n m a m m a l s ( A l o i s i

e t a l .

1994 ; Sp ined i

e t a l .

1 9 9 4 ) . I t m a y b e s u g g e s t e d

t h a t th e i n c r e a s e d s e n s i ti v i ty o f t h e f e m a l e t r o u t t o s tr e s s m a y b e d u e t o th e

f a c t th a t i t i s o f t e n th e f e m a l e t h a t m a k e s t h e d e c i s i o n s r e g a r d in g t h e t im i n g

a n d e x a c t l o c a t i o n o f r e p r o d u c t i v e a c t iv i ty . I t is v i t a l l y i m p o r t a n t t h e r e f o r e

tha t the f em ale shou ld be ab le to r espon d sens i t ive ly to env i ronm en ta l s igna l s

t h a t a r e u n f a v o u r a b l e t o r e p r o d u c t i o n . I t i s p o s s i b l e h o w e v e r t h a t th i s

r e s p o n s e h a s i n c u r r e d a n a s s o c i a t e d c o s t , n a m e l y a n i n c r e a s e d s u s c e p t i b i l i ty

t o p a r a s i t i s m . A r e d u c t i o n i n t h e a u t o i m m u n e r e s p o n s e m i g h t b e a n o t h e r

t r a d e - o f f r e s u l ti n g f r o m t h e s u p p r e s s io n o f t h e i m m u n e r e s p o n s e ( R a b e r g

e t

a l .

1 9 9 8 ). T h i s r e s p o n s e m i g h t b e p a r t ic u l a r l y b e n e f i c i a l d u ri n g t h e r e p r o -

d u c t i v e s e a s o n .

T r o u t h o r m o n e s h a v e a l s o b e e n i n v o k e d t o e x p la i n t h e m a l e b i a s in p r e v a -

l e n c e a n d a b u n d a n c e o f e c t o p a r a si t ic i n f e ct i o n r e p o r t e d b y P a l i n g ( 1 9 6 5 ) i n

t h e c a s e o f


a n d b y P i c k e r in g a n d C h r i st i e ( 1 9 8 0 ) f o r a v a r ie t y o f

e c t o p a r a s i te s a n d f u n g a l p a t h o g e n s . T h e p e r i o d o f e n h a n c e d s u s c e p t i b i li t y in




m a l e t r o u t c o i n c i d e d w i t h a m a r k e d s e x u a l d i m o r p h i s m i n th e s k i n s tr u c t u re

c h a r a c t e r i s e d i n t h e m a l e b y d e r m a l a n d e p i d e r m a l t h i c k e n i n g a n d a l m o s t

t o ta l d e p l e t i o n o f m u c u s - s e c r e t i n g c e l l s (P i c k e t i n g , 1 9 7 7 ; P o t t i n g e r a n d

P icke t ing , 1985a) . Th i s k ind o f s exua l d im orph ism in sk in s t ruc tu re has a l so

b e e n d e s c r i b e d f o r a n u m b e r o f o t h e r f i s h s p e c i e s ( P o t t i n g e r a n d P i c k e t i n g ,

1 9 8 5 a) . T h e s e c h a n g e s i n th e s k i n s t ru c t u re w e r e c l o s e l y c o r r e la t e d w i t h t h e

r is i ng p h a s e o f 1 1 - k e t o t e s to s t e r o n e p r o fi l e a n d d i s a p p e a r e d d u r in g t h e p o s t -

s p a w n i n g p e r i o d w h e n g o n a d s r e g r e s s a n d c i r c u l a t i n g a n d r o g e n s r e t u m t o

basa l l eve l s (Po t t inger and P icke t ing , 1985a). Po t t inger and P icke t ing (1985b)

h a v e s h o w n t ha t 1 1 - k e t o t es t o s te r o n e a p p e a r e d t o p r o m o t e b o t h e p i d e r m a l a n d

d e r m a l t h i c k e n i n g a n d r e d u c e t h e n u m b e r s o f g o b l e t c e ll s w h e r e a s t e s t o s -

t e r o n e s t i m u l a t e d e p i d e r m a l t h i ck e n i ng . H o w e v e r , a s t e s t o s te r o n e l e v e l s w e r e

h igher in fem ales du r ing th i s pe r iod (Po t t inger and Car r ick , 2000) p resum ab ly

o t h e r m e c h a n i s m s m u s t h a v e b e e n i n v o l v e d i n i n h i b i t i n g t h e c h a n g e s

d e s c r i b e d i n t h e s k i n o f m a l e t r o u t f ro m o c c u r r in g i n f e m a l e t r o u t. A s p o i n t e d

o u t b y P o t t i n g e r a n d P i c k e r i n g ( 1 9 8 5 a ) t h e f u n c t i o n a l s i g n i f ic a n c e o f d e m u -

c i f i ca tion i s f a r f rom c lea r, pa r t i cu la rly in v iew o f the su ppo sed p ro tec t ive ro le

o f th e m u c u s l a y e r ( B l a c k s t o c k a n d P i c k e t i n g , 1 9 8 2) . T h e y a l s o p o s t u l a t e d

t h a t t h e t h i c k e r in t e g u m e n t w o u l d b e a d v a n t a g e o u s t o t h e m a l e t r o u t d u ri n g

the t raum at ic spawning season . How ever , i t cou ld a l so be a rgued tha t a th icker

i n t e g u m e n t w o u l d a l s o b e s e l e c ti v e l y a d v a n t a g e o u s t o t h e fe m a l e w h i l e r e d d

cut t ing a t th is t ime.

F u r t h er w o r k i s r e q u i re d t o e l u c i d a t e t h e c a u s a t iv e m e c h a n i s m s r e s p o n s i b le

fo r the ab ove cases o f apparen t m a le b ias in in fec t ion by ec toparas i t e s and fo r

i ts ab sence in the p resen t and o the r inves t iga t ions ca r r i ed ou t on f i sh pa ras it e s .

I t c a n b e h y p o t h e s i s e d t h a t t h e c a s e s w h e r e m a l e b i a s h a s b e e n r e p o r t e d m a y

h a v e b e e n d u e t o t h e o n c o m i r a c i d i a o f D s a g i t t a t a f ind ing the sk in o f ma le

t r o u t m o r e a t t ra c t i v e o r e a s i e r to p e n e t r a t e t h a n t h a t o f t h e f e m a l e t ro u t .

A l te rna tive ly , the male t rou t m igh t be m ore to le ran t than f em ale t rou t fo l low -

ing in fec tion . I f Pa l ing s (1969 ) c la im tha t the oncom irac id ia o f D s a g i t t a t a d o

no t loca te the i r hos t s by us ing o l f ac to ry s igna l s i s accep ted then we a re l e f t

w i th the l a s t tw o hypo these s .

The conf l i c t be tw een the p resen t r e su l t s and those o f Pa l ing (1965) m igh t be

a t t ribu tab le to the inc reased vu lne rab i l i ty o f m a le f i sh be ing r es t r ic ted ov er a

per iod w hen they a re matu re and sexua l ly act ive. Thus , P o t t inger and P icke t ing

(1985a) found tha t changes in the sk in s t ruc tu re , wh ich were though t to be

respons ib le fo r inc reased vu lne rab i li ty o f m a les to pa ras it ism, we re c lose ly co r -

r e la ted w i th the r i s ing phase o f 11 -ke to tes tos te rone p ro f i l e . These changes

d i s a p p e a r e d d u r i ng t h e p o s t- s p a w n i n g p e r i o d w h e n g o n a d s r e g r e s s e d a n d c i r-

cu la t ing androgen s r e tu rned to basa l l eve ls . Con sequen t ly , i f the w in dow fo r

sex b ias to occur was na r row and f a i l ed to over lap the main in fec t ion pe r iod

t h e n n o d i f f e r e n c e s i n t h e i n f e c ti o n r a t es o f m a l e s a n d f e m a l e s w o u l d b e

e x p e c t e d . H o w e v e r , P a l i n g ( 1 9 6 5 ) w a s u n a b l e t o f i n d s u p p o r t f o r t h i s




h i g h e r p r o b a b i l i ty o f b e c o m i n g i n f e c t e d w i th t h e m o n o g e n e a n

Pseudodiplorchis americanus

(T insley , 1989) . S imi la rly , ma le w oo d mice ,

Apodemus sylvaticus are

cons id e red to have h igher in fec t ions o f ec toparas i t ic

t ic k s a n d f l u k e s t h a n f e m a l e s b e c a u s e th e y c o v e r m o r e g r o u n d a n d e a t m o r e o f

the inver teb ra te p r im ary hos t (Lang ley and Fa i fl ey , 1982). R e im chen and N os i l

( 2 0 0 1 ) a l s o c o n s i d e r e d th a t t h e p r e p o n d e r a n c e o f C. truncatus and Bunodera

sp . in ma le s t i ck lebacks and S . solidus a n d n e m a t o d e s i n f e m a l e s w a s b e s t

e x p l a in e d o n t h e b a s i s o f d i f fe r e n c e s b e t w e e n t h e f e e d i n g n i c h e s o f t h e t w o

sexes r a the r than b y invok ing r ep rod uc t ive cos t s . Thus , the f em ale f i sh u t il i s e

f o o d i te m s f r o m t h e p e l a g i c z o n e , w h e r e t h e p r im a r y h o s t o f Schistocephalus

solidus

t ends to occur , to a g rea te r ex ten t than m ale f ish . In con t ras t , m a le f i sh

u t il is e m o r e f o o d i te m s f r o m t h e b e n th i c z o n e , w h e r e t h e h o s t s o f

C. truncatus

and

Bunodera

occur , than do f em ale f i sh .

Sex differences in immune function will be more pronounced among

polygynous than monogamous species

The a rgumen ts fo r advanc ing th is hypo thes i s a l so h inge on the as sumpt ion tha t

t e s t o s t e r o n e i s i m m u n o s u p p r e s s i v e . I t w a s p o s t u l a t e d t h a t b e c a u s e p o l y g y -

n o u s m a l e s n e e d h i g h e r t e s t o s t e r o n e l e v e l s t h a n m o n o g a m o u s m a l e s t h e i r

i m m u n e m e c h a n i s m s w o u l d b e i n h i b i t e d t o a g r e a t e r e x t e n t a n d t h e y w o u l d

the re fo re be mo re vu lne rab le to pa ras it i sm. Ho wev er , K le in and N e lson (1997 ,

1998) foun d no ev idenc e to suppo r t th is hypo thes i s and conc lude d tha t h igher

a n d r o g e n c o n c e n t r a t i o n s i n p o l y g y n o u s m a l e v o l e s d i d n o t i n f l u e n c e s e x o r

spec ies d i f f e rences in the im m une func t ion .

When species with extravagant sexually dimorphic traits are compared with

others with more subdued dimorphic traits the males in the former case will

be more heavily parasitised

T h i s i s l i n k e d t o a n o t h e r r e l a t e d , b u t u n t e s t a b l e , h y p o t h e s i s w h i c h s t a t e s :

Spec ies ha rbour ing ha rmfu l pa ras i t e s over the i r evo lu t ionary h i s to ry w i l l be

m o r e l i k e l y t o e v o l v e e x tr a v a g an t s e x u a l ly d i m o r p h i c t r a i ts . B o t h h y p o t h e s e s

a re based on the as sumpt ions tha t t e s tos te rone i s imunosuppres s ive and tha t

spec ies w i th ex t r avagan t s exua l ly d imo rph ic t r a i ts w ou ld have h igher l eve l s o f

te s tos te rone than spec ies w i th more subd ued d imo rph ic t ra it s. Ho wev er , the re

i s li tt le suppor t fo r the hyp o thes i s invo lv ing ex tan t spec ies . Thus , Scha l l and

S t a a t s ( 1 9 9 7 ) c o u l d f i n d n o a s s o c i a t i o n b e t w e e n p a r a s i t i c l o a d a n d c o l o u r

wh en invest iga t ing spec ies of Anolis l izards in the Car ibbea n islands. Like wise ,

U n d e r h i l l a n d K a l e i t a S u m m e r s ( 1 9 9 5 ) f o u n d t h a t g r o u p s o f b i r d s w i t h th e

h ighes t b r igh tnes s s co re had in fec t ion r a tes s im i la r to the du l l e s t g roup . Bo th



88 J D THOMAS

Hillgarth and Wingfield (1997) and Hamilton and Poulin (1997) conclude that

support for this hypothesis is ambiguous and the latter authors state that the

generality of the Hamilton and Zuk hypothesis in respect to parasite mediated

sexual selection across taxa is thrown into doubt by these results . This con-

clusion is not surprising as other environmental factors as well as parasitism

may influence the sexual dimorphism in plumage colour. Thus Badyaev

(1997), for example, found that species occupying lower elevations are more

sexually dimorphic in plumage than species at higher elevations.

Incre ased pa ras i t ic in fec t ions wi l l reduce tes tos terone levels the express ion

o f s e c o n d a r y s e x u a l c h a r a c te r s a n d s e l ec t io n b y t h e o p p o s i t e s e x

There are several examples of parasites appearing to reduce the levels of testos-

terone in the host. These include the trematode S c h i s t o s o m a m a n s o n i in mice

(Isserhoff

et al .

1986) and mites infecting male chickens (De Vaney

et al .

1977). Parasitic infections may also cause corticosteroid levels to increase in

rats (Chernin and Morinan, 1985). Although the effects of parasites on steroid

levels in brown trout appear not to have been investigated it is likely that their

effects would be similar to those induced by environmental stress such as con-

finement (Pickering, 1989). According to this author most forms of

environmental stress activate the hypothalamic-pituitary-interrenalaxis of the

trout. This causes an elevation of blood cortisol levels followed by a marked

suppression of the plasma levels of both testosterone and oestradiol. As a

result normal sexual development will be impeded in both sexes and the fish

become more susceptible to disease.

The evidence that parasitic infections affect traits under sexual selection is

conflicting. Studies that fail to support Hamilton and Zuk s prediction include

that of Berg

et al.

(1995) as they found no reduction in two sexually dimorphic

features in male sockeye salmon,

O n c h o r h y n c h u s n e r k a

with increased levels

of infection with the nematode P h i l o n e m a o n c h o r h y n c h i . Likewise, Bronseth

and Folstad (1997) found a positive relationship between the size of the pec-

toral fin in male three-spined stickeback and the intensity of prevalent

parasites. Nevertheless, these authors argue that as the results show that the

large fins are indicative of the individual s ability to tolerate increased parasitic

exposure, they provide support for the contention that secondary sexual char-

acters can provide information about the host s ability to tolerate parasitic

infection.

In contrast, other results appear to support Hamilton and Zuk s original

prediction. Thus, Houde and Torio (1992) found that orange spots were less

bright in infected male guppies and as a result they were significantly less

attractive to the females than non-infected males. In the case of the Arctic

charr, Liljedal et al . (1999) found that the intensity of infection by a nematode




spec ies , the den s i ty o f c i r cu la ting g ranu loc y tes and sp leen m ass w ere a l l neg -

a t iv e l y a s s o c i a te d w i t h e j a c u la t e q u a l i ty a n d r e d s p a w n i n g c o l o r a ti o n o f m a l e

f ish . Ba kke r and Mu ndw i le r (1999) a l so found tha t smal l pec to ra l f in s in ma le

t h r e e - s p i n e d s t i c k e b a c k w e r e a s s o c i a t e d w i t h i n f e c t i o n b y t h e p a r a s i t e

P o m p h o r h y n c h u s l a e v i s .

L o p e z ( 1 9 9 8 ) a l s o c l a i m e d t h a t s e c o n d a r y s e x u a l

c h a r a ct e rs w e r e d i s p l a y e d m o r e p r o m i n e n t l y b y r e si st a n t m a l e g u p p i e s t h a n b y

non- res i s t an t m a les . In the case o f b i rds , H i l lga r th and Wing f ie ld (1997) s t a te

tha t ' t he re i s inc reas ing empi r i ca l ev idence tha t ma le b i rds w i th h igh mat ing

succes s and we l l deve loped s econdary charac te r s have lower pa ras i t i c in ten -

s i ty ' . How ever , in 9 o f the 13 cases c i t ed by them the r esu lt s f a i l ed to supp or t

the hypo thes i s .

A l t h o u g h t e s ts o f th i s h y p o t h e s i s h a v e f o c u s e d o n m a l e s r a th e r t h a n o n

females , one s tudy invo lv ing f emale s t i ck lebacks has shown s imi la r t r ends .

T h u s , M c L e n n a n a n d S h i r e s (1 9 9 5 ) w e r e a b l e to s h o w t h at t h e a b u n d a n c e s o f

t w o h e l m i n t h s p e c i e s w e r e n e g a t i v e l y c o r r e l a t e d w i t h t h e in t e n s i ty o f t h e

female ' s aggres s ive r esponse to in t rud ing f emales and pos i t ive ly co r re la ted

wi th the in tens i ty and du ra t ion o f the f em ale ' s cour t sh ip .

C o m p a r a b l e s t u d ie s o n b i r d s a l s o a p p e a r t o s u p p o r t th e v i e w t h a t p l u m a g e

br igh tnes s s e rves as an ind ica to r o f cond i t ion an d as an hones t adv er t i s emen t

o f r e si s tance to pa rasi ti sm. T hus male h ouse f inches su rv iv ing an ep idem ic had

s ign i f i can t ly r edder p lumage than males tha t d id no t su rv ive (No lan

et a l .

1998) . Ho we ver , wh en Ha m i l ton and Pou l in (1997) r eana lysed , 199 s epara te

da ta s e t s they conc luded tha t ' a s a who le in t r aspec i f i c co r r e la t ions be tween

paras i t e load and m ale sho wine s s p rov ided v e ry l it tl e suppor t fo r the hypo th -

e s is w i t h o n l y t h e e f f e c t o f p a ra s i te s o n f i sh m o r p h o l o g y m a t c h i n g t h e

H a m i l to n a n d Z u k p r e d i c t i o n ' .

U n f o r t u n a t e l y , n o c o m p a r a b l e s t u d i e s h a v e b e e n m a d e t o i n v e s t i g a t e t h e

pos s ib le e f f ec t s o f pa ras i ti sm on s econ dary s exua l cha rac te r s o f b row n t rou t .

The t rou t is s exua l ly d imorph ic and s ec ond ary s ex charac te r s such as the s i ze

o f t h e k y p e a n d t h e c o l o u r a n d s iz e o f t h e a d i p o s e f i n c o u l d b e r e a d i ly q u a n ti -

f i ed in the m ale t rou t. Ho weve r , a s bo th m ales and f ema les have d i s tinc t ive and

prominen t co lou red pa t t e rns i t i s pos s ib le tha t these cou ld ac t a s s igna l s o f

hea l th , w e l lbe ing and r es i s t ance to pa ras i t i sm to m em bers o f the oppos i t e s ex .

7 3 C o n c l u s i o n s

Sta t is t ica l t e s ts inc lud ing m ul t ip le r eg res s ion a na lyses hav e r evea led tha t the

s e x o f t h e b r o w n t r o u t h a s a s i g n if ic a n t i n f l u e n c e o n t h e t o t a l n u m b e r o f p a r-

a s i t e s a n d m o r e s p e c i f i c a l l y o n

P. s imi l e

n e m a t o d e s ,

C . m e t o e c u s

and N .

rutil i . In a l l cases the b ias w as in f avour o f the f em ale t rou t. H owe ver , the con-

t r i b u t i o n s m a d e b y t h e h o s t s e x t o t h e t o t a l v a r i a n c e w e r e v e r y s m a l l

( 0 . 5 4 - 4 . 8 4 ) c o m p a r e d w i t h t h o s e m a d e b y s e a s o n a l c h a n g e o r s ta t io n . T h i s



90 J D THOMAS

scenario can be extended to other taxa as strong sex bias in parasitism is

uncommon. Despite this much has been written about sex bias in parasitism

and this information has been used as a basis for testing the Hamilton-Zuk

and immunocompetence hypotheses. However, on the whole, the present

review fails to support predictions 1-5 of the above hypotheses. It was also

concluded that statistically significant male biases in parasitism are not a

general rule. The linked hypothesis that male bias in parasitism is due to the

immunosuppressive action of testosterone also lacks sound experimental sup-

port and is therefore invalid. This conclusion helps to explain the lack of

support for hypotheses 3 and 4 as they are also based on the assumption that

testosterone is immunosuppressive.

The fifth hypothesis, which states that increased parasitic infection will

reduce testosterone levels, the expression of secondary sexual characters and

selection by the opposite sex is supported by some experimental evidence and

therefore has more validity. However, it is not supported by all the

experimental results. This is not surprising in view of the fact that parasites

vary in their pathogenicity and testosterone levels can also be influenced by a

number of other environmental factors. The most likely explanation for the

decline in testosterone levels and in the development of secondary sexual char-

acters in parasitised animals is that they are caused by increased corticosteroid

levels due to stress. There is evidence that high corticosteroid levels cause a

depression of the immune system, a lowering of sex hormone levels and hence

result in less well developed secondary sexual characters.

Taken as a whole the arguments of the Hamilton-Zuk hypothesis seem

sound. Parasites may adversely affect vertebrate host fitness in general and

secondary sexual characters in particular to varying degrees and susceptibil-

ity to parasitism will be inherited. However, the predictions used to verify it

which are based on the proposition that testosterone is immunosuppressive

seem flawed and are highly questionable. Before this hypothesis can be

properly assessed it is clearly necessary to have a better understanding of

how the endocrine and immune systems are influenced by parasitism in both

male and female animals. It is also necessary to know how important para-

sitism is as a selective force. The statistical analysis carded out on the Teifi

trout failed to produce any evidence that the parasites had a detrimental

effect on the trout. This situation is not unique. Thus, Chubb (1973) states

that most British freshwaters are not troubled with regular parasite prob-

lems, although parasites are always present in abundance . Allison (1982)

also cites a number of case studies in support of the view that parasite infec-

tions are relatively harmless to those animal hosts with which they have a

long-term relationship. However, those same parasites may have seriously

detrimental effects on newly introduced host species or when the parasites

themselves are introduced into new regions. It can be postulated that these

apparently benign relationships are a consequence of long-term coevolution.



ECO LO GY OF FISH PARASITES 9

This concept can be rationalised by reference to R 0, the basic reproductive

rate of the parasite which natural selection will tend to maximise.

Maximising R 0 will involve trade-offs between production of transmission

stages (which ideally should be high) and damage to the host (which ideally

should be small). R0 will therefore be clearly maximised by the host surviv-

ing as long as possible. However, in cases where death of the host is an

integral part of the transmission cycle or where the transmission efficiency

may be enhanced by modifying host behaviour in such a way as to shorten its

life the circumstances are different.

Other environmental factors such as seasons (climate) or location may

well be more important selective mechanisms in determining the nature of

secondary sex characters than parasites. Thus, Badyaev (1997), for example,

found that bird species occupying lower elevations are more sexually dimor-

phic in plumage than species at higher elevation. One other criticism of this

hypothesis is that it focuses on the male s secondary sex characters as signals

of health and wellbeing. A more balanced approach would also involve

assessing the signals used by males to assess the health and wellbeing of

females.

It is necessary to focus on particular host species in order to elucidate the

causative mechanisms responsible for sex bias in parasitism or the lack of it as

in salmon parr. In the case of the Teifi trout, for example, three hypotheses have

been advanced to explain the female sex bias in parasitism. These include

testosterone immunosuppression, corticosteroid-based immunosuppression

and behavioural differences between the sexes. Further endocrinological and

immunological research is clearly needed to evaluate the possible involve-

ment of the first two hypotheses. However, on the basis of the evidence

presented it would appear that the last two hypotheses have the most credence

and could be tested under experimental conditions. Reimchen and Nosil (2001)

also favour the ecological hypothesis and state that their results, combined

with those in the literature suggest that ecological differences between the

genders may be a more important component to patterns of parasitic infections

in natural populations than currently appreciated . Niche partitioning between

the sexes is widespread in the animal kingdom and may have evolved as a

result of the selective pressure imposed by intraspecific competition (Schluter,

1994). It is strongly advocated therefore that further studies should be carried

out to test the behaviour hypothesis under natural conditions by comparing

microhabitat selection, the feeding niches and the selection of intermediate

hosts, in particular, by the two sexes for a wide range of species. However, the

possible involvement of immunosuppression in causing sex bias can also be

tested under controlled conditions in the laboratory by providing male and

female trout of the same age with identical doses of infective larvae. The lack

of sex bias in the case of the salmon parr suggests that there are no differences

between the sexes in either their feeding niches or immune mechanisms.



9 2 J D T H O M A S

Evidence in support of the former hypothesis is given by Thomas 1962). The

fact that the majority of the male salmon parr are precocious and have enlarged

testes may be cited as circumstantial evidence against the hypothesis that

testosterone is immunosuppressive.

8 T H E H E L M I N T H F A U N A O F T R O U T A N D S A L M O N P A RR :

C O M P A R A T I V E A S P E C T S

At the ecological level the heminth parasites common to both the trout and

salmon parr share many spatial and temporal patterns. Thus,

C . m e t o e c u s

exhibit summer troughs and winter highs, unlike N. ru t i l i , in both fish

species. However, the abundance of

C . f a r i o n i s

does not vary seasonally in

the case of salmon parr although it does so in the trout. Likewise

D . s a g i t -

t a ta

and

N. ru t i l i a re

more abundant in both trout and salmon parr at Station

A than at Station B.

As with trout there were significant tendencies for the abundances of D.

sag i t t a ta , C . me toecus

and

C. f a r io n i s ,

but not

N. rut i l i ,

to increase with the

length of salmon parr. However, unlike the trout, there were no statistically sig-

nificant relationships between the abundances of any of the parasite species

and the weight of the salmon parr. This absence of relationship can be attrib-

uted to the much smaller range in weight of the salmon parr compared with

trout. With the exception of

N. ru t il i and D. d i t r emum the

abundances of all the

parasite species in trout increased significantly with age. This was also the case

with the helminth parasites of salmon parr with the exception of

N. ru t i l i

and

C. far io nis .

As with the trout the abundance values of the dominant parasite, N.

rut i l i ,

were significantly positively correlated with both the condition factor

and the adipose index. There was no evidence therefore that the helminth par-

asites had an adverse effect on the wellbeing of either fish species as measured

by the condition factor and the adipose index.

However, the helminth communities of salmon parr and the brown trout

Tables 3 and 14; Figure 17) also differ in many important respects. Firstly,

although the trout and salmon parr share five species

D. sag i t t a ta , C . f a r io n i s ,

C . me toecus , N . ru t i l i

and

C . e p h e m e r i d a r u m )

the trout has a richer helminth

fauna as it is also parasitised by

P. s imi l e , D . d i t r emu m , R . acus , C . tru t t ae and

species of

Capi l lar ia .

Secondly, at the component population level both the

Simpson and Shannon Wiener diversity indices and the equitability index are

much higher for the trout than the salmon parr. In contrast, the Berger-Parker

predominance index is higher for the salmon parr than trout. Thirdly, the

Brillouin and maximum Brillouin indices are higher in trout than in salmon

parr at both the component and infrapopulation levels. These results are to be

expected as species richness, the mean number of parasites per fish and the




m a x i m u m n u m b e r o f p a r a s it e s p e r fi s h a t t h e in f r a p o p u l a ti o n l e v e l a re m u c h

h i g h e r f o r t r o u t t h a n s a l m o n p ar r. I n c o n t r a st , m o r e s a l m o n p a rr w e r e w i t h o u t

a n y p a r as it es ( 1 3 . 3 - 1 4 . 3 ) c o m p a r e d w i t h t r ou t ( 1 . 0 - 1 . 3 ) . W i t h t h e e x c e p -

t i o n o f N . r u t i l i t h e d o m i n a n t p a r a s it e i n th e c a s e o f t h e s a l m o n p a rr , t h e

a b u n d a n c e v a l u e s o f s h a r e d p ar a s it e s p e c i e s w e r e m u c h h i g h e r f o r t r ou t . T h i s

t r e n d w a s p a r t ic u l a r ly m a r k e d i n t h e c a s e o f D . sa g i t t a t a .

A l t h o u g h i t c a n b e p o s t u l a t e d t h a t t h e s e d i f f e r e n c e s a re a t tr i b u ta b l e t o th e

s a l m o n p a rr h a v i n g a h i g h e r l e v e l o f i m m u n i t y o r r e s i s t a n c e t h a n t r o u t i t i s

m o r e p r o b a b l e t h a t t h e y a r e c a u s e d b y d i f f e r e n c e s i n a g e d i s t r ib u t i o n a n d t h e

n i c h e s o c c u p i e d b y t h e t w o s p e c i e s ( F i g u r e s 1 8 a n d 1 9 ). T h u s , n e a r l y a l l o f t h e

s a l m o n p a r r a r e i n t h e 1 o r 2 y e a r a g e c a t e g o r y w h e r e a s m a n y o f t h e b r o w n

t r o u t a r e m u c h o l de r . T h e e v i d e n c e t h a t p a r a s it e a b u n d a n c e i n c r e a s e s w i t h a g e

B R O W N T R O U T S A L M O N P A R R

C H A R A C T E R

D I S P L A C E M E N T

N I C H E D I V E R S I -

F I C A T I O N

H A B I T A T )

N I C H E D I V E R S I -

F I C A T I O N

F E E D I N G )

P A R A S I T I C

F A U N A

L A R G E R G A P E ;

M A N D I B L E S E X T EN D T O

P O S T E R IO R M A R G I N O F

E Y E ; B O D Y S T O C K I E R ;

C A U D A L P E D U N C L E

T H I C K E R A N D C A U D A L

F I N L E S S I N D E N T E D

S M A L L E R , M O R E

R O U N D E D G A P E ;

M A N D I B L E S E X T E N D T O

M I D D L E O F E Y E ; B O D Y

M O R E S L E N D E R ;

C A U D A L P E D U N C L E

N A R R O W E R ; C A U D A L

F I N M O R E I N D E N T E D

T E N D T O O C C U P Y M I D -

W A T E R P O S I T I O N IN

L A M I N A R F L O W ;

T E R R I T O R I E S I N C L U D E

P O O L S , B A C K W A T E R S

A N D S L A C K W A T E R S

U N D E R B A N K S

T E N D T O O C C U P Y

R I F F L E Z O N E S , C L O S E

T O S E D I M E N T S ; E X C E P T

U N D E R S P A T E O R

D R O U G H T C O N D IT I O NS

A V O I D B A C K W A T E R S

A N D S L A C K W A T E R S

U N D E R B A N K S

D I E T H A S H I G H E R ' S

O F Lymnaea, Sphaerium,

Asel lu s Gamm arus and

a m m o c o e t e L A R V A E

A S S O C I A T E D W I T H

D E P O S I T I N G S E D I M E N T ,

W H I C H A C T A S

I N T E R M E D I A T E H O S T S

D I ET D O M I N A T E D B Y

R I F FL E A N D F A S T

R E A C H F A U N A ( e. g. ,

s p e c i e s

o f Ancylus,

Br achycen t ru s B aet is

Eph emere l la Ecdyonur us

and Simulium

P R E V A L EN C E S A N D

A B U N D A N C E V A L U E S

F O R D.sagittata, C .farionis,

C.metoecus

P.simile,

N.rutili, R.acus

and C.trut tae

H I G H E R T H A N F O R

S A L M O N P A R R

P.simile, R.acus

C.trut tae

A B S E N T ; P R E V A L E N C E S

A N D A B U N D A N C E

V A L U E S F O R

D.sagi t ta ta

C ar i oni s C.m etoecus and

N.rutili L O W E R T H A N

T R O U T B U T T H O S E F O R

C.ephemeridarum H I G H E R

F i g u r e 1 7 S u m m a r yof the differences in the niche requiremen ts and parasitic fauna

of the brow n trout and salmon parr.



94 J D THOMAS

Figure 18 Differences in the morphological features of the salmon parr a) and brown

trout b). The major differences include the larger maxillary bone of the trout and hence its

wider gape, the more rounded gape o f the salmon parr, the more rounded, elongated body

and more pronounced forked tail o f the salmon parr. These adaptations allow the parr to

occupy habitats close to the substrate in fifties and also to enter spaces between sm all cob-

bles in w inter. The trout anatomy is better adapted for life in laminar flow in midwater.

has a l read y been g iven . As m ost he lm inth paras i tes are t ransmi t ted or a l ly i t i s

mor e l i ke ly however tha t t he d i f fe rences be tween the pa rasi ti c fauna o f t he two

salmonid species are main ly a t t r ibu table to d i fferences in habi ta t se lec t ion

and d ie tar ies. The se in turn are linked to d i fferences in charac ter d isp lacem ent

and n iche d ivers i f ica t ion F igures 17 and 18).

Ther e i s a g rea t dea l o f cumula t ive ev idence tha t d i f fe rences be twee n the

c o m mu n i t y s t ru ct u r e o f h e lmi n t h p a ra s i te s o f f is h s p e c ie s a r e d e t e rm i n e d

largely by d i fference s in the i r feed ing beh aviou r Dogie l , 1961; F ior i l lo and

Font , 1996; Carn ey and Dick , 1999) . Th e la t te r au thors postu la te tha t the feed-

i n g n i c h e s o f p e r c h s p e c i es a n d t h e i r h e l mi n t h p a ra s i te s h a v e r e ma i n e d

conservat ive for mi l l ions of years and tha t as a resu l t paras i tic assem blages are

predic tab le and not mere ly s tochast ic assemblages . Niche d ivers i f ica t ion has

a l so been invoked to exp la in d i f fe rences in t he he lmin th comm uni t i e s o f d is -

t inc t mo rphs in popula t ion s of lake- inhabi t ing arc tic charr Curt i s et al. 1995;



E C O L O G Y O F F IS H P A R A S I T E S 9 5

I l l

.1

Z

i i i

..J

a .

1

75

5

5 I

DS CF CM PS NR NE

P R S I T E S

Figure 19 The percen tag e p reva lence va lues fo r the m ajor pa ras i te s and to ta l pa ras i te s

o f th e b ro w n t ro u t in 1 9 9 8 . D S D. sagittata; C F C. farion is; C M C. metoecus; PS P.

simile; NR N. rutili;

N E n e ma to d e s .

K n u d s e n et a l. 1997) as we l l a s s ex b ias in the pa ras i t i sm o f t rou t and o the r

spec ies l ike the th ree - sp ined s t i ck leback Re im chen and Nos i l , 2001) . Chan ges

in the food w eb s a t t ribu tab le to env i ronm en ta l s t re s s , such as inc reased ac id -

i t y M a r c o g l i e s e a n d C o n e , 1 9 9 6) , c o m p e t i ti o n f o r f o o d D u b o i s

et aL

1996)

a n d c a n n i b a l is m H a m m a r , 2 0 0 0 ) h a v e a ls o b e e n i n v o k e d t o a c c o u n t fo r

d i f f e rences in the pa ras it ic he lmin th f auna o f f r eshwa te r fish. A ccord ing to D ue

and Cur t is 1995) the absence o f the ces toda Cyathocephalus truncatus n e m a -

t o d e s o f t h e g e n u s Cysdicola and f r eshwate r acan thocepha lans f rom f i sh in

G r e e n l a n d c a n b e a t t ri b u te d t o t he a b s e n c e o f M y s i d a e , A m p h i p o d a ,

E p h e m e r o p t e r a a n d O d o n a t a , w h i c h a c t a s in t e rm e d i a t e h o s t s .

Th e sa lm on parr and t rout are both ter ri toria l S tuar t , 1953). Ho we ver , there

i s ev idence tha t the home ranges o f s a lmon par r over lap to a g rea te r ex ten t

A r m s t r o n g

et al .

1999) and tha t the t rou t has the compet i t ive advan tage

Kal leberg , 1958) . The t rou t t end to occupy midwate r pos i t ions in l aminar

f low on the ed ge o f cu rren t s w hen f eed ing bu t the l a rge r t rou t pa r t icu la r ly a l so

s p e n d m o r e t i m e i n p o o l s, b a c k w a t e r s a n d i n d e e p e r w a t e r u n d e r b a n k s , w h i c h

are the tr ansmis s ion zones fo r he lmin th pa ras i te s , than do the s a lmon par r. In

con t ras t , f eed ing s a lmon par r t end to spend more t ime r es t ing on the sub-

s t r a te , u sua l ly in r i f f l e s , w i th the pec to ra l f in ou t s t r e tched , the t a i l r ig id ly

ex tended and the do r sa l p ro f i l e s l igh t ly concave wh i le wa i t ing to in te rcep t

d r if t. A cco rd ing to Va ld im ars son and M etca l f e 1998 ) s a lm on parr , un l ike

t rou t , be com e noc tu rna l du r ing the w in te r and s eek r e fuge du r ing the d ay in the

in te rs t it i al spaces in g rave l beds in f low ing wa te r . Th ese au thor s c i t e ev iden ce

tha t th i s behav iou ra l pa t t e rn has ev o lved to r educe p reda t ion .



96 J D THOMAS

Morphological differences such as the larger body size and wider gape of

the trout, combined with their wider habitat range, also help to explain why

trout have more catholic dietaries than the salmon parr. As a result invertebrates

such as

L y m n a e a S p h a e r i u m

and

G a m m a r u s

associated with depositing sed-

iments as well as ammocoete larvae and fish, are commonly encountered in the

trout dietary but are rare or absent from that of salmon parr Thomas, 1962). In

contrast, the salmon parr occur predominantly in riffles or fast reaches where

their small rounded gape enables them to ingest some of their main food items

such as

A n c y l u s

and

S i m u l i u m

by suction Figure 18). As

S p h a e r i u m

fish

species and ammocoete larvae are the intermediate hosts of P. s imi le R. acu s

and

C. truttae

respectively, this helps to explain their absence in salmon parr.

The fact that the salmon parr spend less time in microhabitats with low flows

and depositing sediments in the transmission sites may also help to explain

why the two

C r e p i d o s t o m u m

species and

D. sagi t ta ta are

less prevalent or

abundant in them than the trout. Ostracods, which are the intermediate hosts of

N. rutili commonly occur in the interstitial spaces in gravel beds. The tendency

for the salmon parr to occupy these habitats, particularly in winter

Valdimarsson and Metcalfe, 1998), may help to explain why

N. ruti l i

is the

dominant parasite for this fish.

It seems likely that the nocturnal habits of the salmon parr in winter result

in a reduced level of feeding and that this may be a factor contributing to this

species having a helminth community with a lower species richness and diver-

sity than sympatric brown trout. In contrast, the trout remains a diurnal or

crepuscular feeder throughout the year. There is both experimental Kennedy,

1972) and circumstantial evidence Dogiel, 1961) that a reduction in feeding

rate or starvation of fish hosts will result in a corresponding reduction or loss

of the helminth fauna. The fact that the eel is a nocturnal feeder and that it stops

feeding during the winter months when the temperature falls below 10 °C

Thomas, 1962) may partly account for the impoverished and isolationist

nature of its intestinal helminth community Kennedy and Hartvigsen, 2000).

.

C H A N G E S I N T H E H E L M I N T H F A U N A A N D T H E IR H O S T S

B E T W E E N 1 95 0 A N D 19 98: C A U S A T I V E M E C H A N I S M S A N D

P O L L U T I O N B I O I N D I C A T O R S

9 .1 . C o m p a r i s o n o f P r e v a le n c e A b u n d a n c e a n d D i v e rs i ty o f

H e l m i n t h P a r a s i t e s i n 1 9 5 0 a n d 1 9 9 8

A comparison of Figures 10 and 19 reveals that the prevalence values for par-

asites of trout of various age groups have changed dramatically between 1951

and 1998. Although

C. me toecus

was one o f the most prevalent trout parasites




in the 1950s both

C . m e t o e c u s

and

C . f a r i o n i s

were conspicuous by their

absence in the 1998 fish sample. With the exception of N. ru t i l i the prevalence

values for trout parasites in the sample taken in 1998 were less than the corre-

sponding ones in the 1950 sample.

The community structure analysis of brown trout parasites (Table 14) also

reveals that major changes had occurred between 1950 and 1998. Thus, species

richness had declined from 8 to 5 and at the component population level N.

ru t i l i

had replaced

C . m e t o e c u s

as the dominant parasite. The various compo-

nent population indices, including the Berger-Parker index, Simpson s

diversity index, Brillouin s index, and the equitability index and the slope a

of the geometric series had all decreased. At the infrapopulation level (Table

14) the mean number of parasite species per fish and the maximum number of

parasite species per fish had halved between 1950 and 1998. During 1998 the

percentage values for fish with no parasite species or with one or two parasite

species only were less than in 1950 whereas the converse was true for the per-

centage values for fish with three to six parasites only. These results were

reflected in the mean Brillouin s indices for all fish and infected fish. The

maximum Brillouin s index was also lower in 1998 than in 1950.

9 2 R e a s o n s fo r t h e D e c l i n e in P a r a s it ic F a u n a b e t w e e n 1 9 5 0 a n d

1 9 9 8

Several reasons can be advanced to explain why the helminth parasites of trout

had declined in prevalence, abundance and diversity from 1950 to 1998.

Firstly, the decline is partly due to the catastrophic decline in brown trout den-

sity and to a change in the age structure since 1950 (Figure 20). Thus, the

trout population in 1998 consisted mainly of juvenile fish in the first and

second year and older, mature fish were uncommon. It is possible that the

change in age structure is due to a shift from what was predominantly a

brown trout life history strategy to that of the migratory sea trout. This change

may be regarded as an adaptation to the River Teifi and its tributaries becom-

ing harsher and more erosive in character as a result of changes in land use.

Many of the juvenile fish in the 1998 sample may therefore have been sea

trout parr and it is noteworthy that trout in the year classes 4-6 were absent

from the sample (Figure 20). As the prevalence, abundance and diversity of

helminth parasites in fish are positively correlated with age it is possible that

the lower values in the 1998 sample may be partly due to the preponderance

of juvenile fish.

Another possible reason for the decline in prevalence, abundance and diver-

sity of parasites from 1950 to 1998 is that the intermediate hosts have become

less abundant. Preliminary sampling in 1997 had revealed that S . c o r n e u m t h e

intermediate hosts of P. s im i l e (Thomas, 1957, 1958a, b), which were abundant



9 8 J D T H O M A S

60

50-

40-

D

O

n,

~-

3 0

u_

O

o~

20-

10-

A g e c la s s

l iB

1 9 9 8

D A 1950

~ i i i i i i ~

i i i i ~

2

3 4 5 6

AGE OF TROUT IN YEARS

F i g u r e 2 0 The percentage of brown trout in various age groups in 195 0 and 1998.

in the sedim ents o f s i tes 1-8 in 1943 Jones 1 943) and also in the 1950s

Thomas, 1956, 1958, 1962, 1964a, b, c) , had apparently disappeared. The

absen ce of this sp ecies from the f ish and invertebrate sampling sites 1 -7 on the

Teif i w as co nfirm ed by qualitative sam pling o f the fauna at e igh t sites in 1998

Table 28, Figure 21). S. co r n eum wa s only foun d in deposi t ing sedim ent in a

backwater at s ite 8 in the vic inity o f a sm al l ox-b ow lake that may have acted

as a refugium . As this s pec ies w as n ot found during the cour se of a very thor-

oug h survey o f the Teif i in 1981 by Jenkins

e t a l .

1984) i t would appear that

it has been in serious decl in e in i ts populat ion density betw een 1950 and 1981.

A s

Sph a e r i u m c or n eum

was ident i f ied as the mol luscan host of P .

s im i l e

by

Tho ma s 1956, 1958a) the presence of adult P . s im i l e in the trout in 1 998 w as

unexpected. It m ust be conc lud ed therefore that P. s im i l e mu st be using another

m ol lusc , probably spec ies of P i s i d i um as its intermediate host. It m ay b e sug -

gested that this low level of intermediate host specif ic ity may be a general

characteristic of the parasites of salmonid fish. This feature may be attributa-

ble to the high leve ls o f uncertainty in the environment in wh ich the f i sh and

their parasites have evolved.

Sm al l numbers o f

P i s i d i u m

spe cies, w hic h are potential intermediate hosts

o f

P sim i l e

and also

C . a r i o n i s

and

C. m etoecus

were patchily distributed at

all stations Table 28). T he

P i s i d i u m

species l isted in Table 28 and Figure 21

were also recorded by Jenkins e t a l . 1984) . Quantitat ive samples, taken with

the cyl indrical corer, con firm that both the bivalve and gastropo d m ollu scs,

inc luding L ymn aea p er e g r a t h e intermediate host o f C. me toecus according to




Table 28 T h e n u m b e r s o f p o te n t i a l i n t e r m e d i a t e h o s t s o f h e l m i n t h p a r a s i t e s , s a m p l e d

b y n e t ti n g , i n S e p t e m b e r 1 98 1 a n d M a y 1 9 9 8

Y e a r s t a t i on num be r )

1981 1981 98 98 98 98 98 98 98

1 a n d 2 ) 8 ) 1 a n d 2 ) 3 ) 4 ) 5 ) 6 ) 7 ) 8 )

M o l l u s c a

Potamopyrgusjenkinsi

Sm ith) - - - 465 55 - 2 - 52

Lymnaeaperegra MU ller) 1 14 48 27 11 - 4 4 1

Lymnaea p alustris

M iiller) - - 1 - 1 - 2

Planorbis carinatus

M~iller) - 70 9 22 53 3 3 9 6

P. con tortus

L.) - - - 60 50 2 3 4 -

Ancylusfluviatilis M Ulle r) - 288 - 1 14 - 7 3 -

Pisidium casertanum

Poli) 5 12 -

P. personatum M a im ) . . . . 1

P. obtus ale

La m a rc k ) - - -

P millium

He ld) - - - 5 1 - 1 - 1

P. subtrunca tum

M aim ) 4 5 - 7 - 1 7 - 1

P. hibern icum

W este r lun d) 113 3 - 2 4 - 4 - 1

P. nitidum

Jeny ns) 13 2 7 5 5 - 10 - 1

P. pulch ellum Je nyns ) -

1

i s id ium

spp . 77 3 9 - 1 - 22 - 1

Sphaerium corneum L .) . . . . 10

S. lacustre M iille r) . . . . 6

C r u s t a c e a

Os trac od a - 7 11 7 12 3 5 9 7

C o p e p o d a 2 5 1 4 5

Asellus meridianus

Ra c o v i t z c ) 900 335 - 4 4 1 6 1 1

Asellus aquaticus

L.) - - 1 90 35 45 109 10 6

Gamm arus pulex L. ) 2 730 -

Crangonyxpseudogracilis

Bo us field ) - - 1 - 5 15 9 2 11

aAbundant n 1943 Jones, 1943) and in 1950 Thom as, 1958a,

Note:

1981 values based on Jenkins

et al.

1984)

b,1964b, c).

A w a c h i e 1 9 6 8 ) , w e r e o v e r d i s p e r s e d a n d p r e s e n t a t v e r y l o w d e n s i t i e s i n t h e

d e p o s i t i n g s e d i m e n t s F i g u r e s 2 1 a n d 2 2 ) . T h e o c c u r r e n c e o r a b u n d a n c e o f

o t h e r p o t e n t i a l i n t e r m e d i a t e h o s t s f o r h e l m i n t h p a r a s i t e s h a s a l s o c h a n g e d

s i n c e 1 9 5 0 o r 1 9 8 1 . T h u s , A s e l l u s m e r i d i a n u s h a s b e e n l a r g e l y r e p l a c e d b y A .

a q u a t i c u s

w h i l e

G a m m a r u s p u l e x t h e

m o s t i m p o r t a n t i n t e r m e d i a t e h o s t f o r C .

m e t o e c u s a c c o r d i n g t o A w a c h i e 1 9 6 8 ) , w a s a b s e n t f r o m a l l t h e s a m p l e s a n d

a p p e a r s t o h a v e b e e n r e p l a c e d b y

C r a n g o n y x p s e u d o g r a c i l i s

T a b l e 2 8 ; F i g u r e

2 3 ) . A c c o r d i n g t o A w a c h i e 1 9 6 5 )

G a m m a r u s p u l e x

a l s o s e r v e s a s t h e i n t e r -

m e d i a t e h o s t o f a c a n t h o c e p h a l a n p a r a s i t e s o f t r o u t s u c h a s

E c h i n o r h y n c h u s



100 J.D. THOMAS

t6

o

tn

, , ~ 10o -

2 a 4 5 6 7

S T A r K 3 N S

I 2 3 4 5 6 7 8

STATIONS

1 2 3 4 5 6 7 B

S T A ~

o i

~ a l o

i o - - - - - -

tu ~ i i v i i , i

I 2 3 4 6 6 7 8

~ S T A T I O N S

• l oo - ~

i -

1 0 0 -

8

c~

i o

|

I 2 3 4 s e 7

S TA TK ~ S

i

i i , , ~ , i

1 2 3 4 5 6 7 a

S T A T I O N S

Figure 2 The mean densi t ies ± S .E.) o f the poten t ia l sphaer i id hosts of helminth

parasites at the various stations in the Riv er Teif i in 1998.



E CO LO G Y O F F IS H P ARAS ITE S 1 1

50O

4OO

3~0

20O

100

0 - - - - ~

i i

1 2

i i i i i

3 4 5 7 8

S T A T I O N S

i i

1 2 3

i i i

5 6 7

S T A ~

a

250

200

I~0

100

~0

0

- -

1

I I [ I I I

2 3 4 5 6 7

STATIONS

. . 3

140

120

100

w -....

i r i i

1 2 3 4 5

STATIONS

I I I

7 8

9

•

t o

5 o

J

~ O -

3 o -

I 1 o -

o -

D

S T A T I O N S

F i g u r e 2 2

The m ean densities _+ S.E.) o f the potential gastropod hosts of helm inth

parasites at the various stations in the River Teifi in 1998.

t ruttae.

I t i s l i k e l y t h a t t h e d e a r t h o f s u i t a b l e

P i s i d i um

h o s t s p e c i e s a n d th e

a b s e n c e o f

Gamm a r u s p u l ex

m a y e x p l a in t h e a b se n c e o f

C r e p i d o s t omum

s p e c i e s i n t h e t r o u t c o l l e c t e d i n 1 9 9 8 . H o w e v e r , o s t r a c o d s , t h e i n t e r m e d i a t e

h o s t s o f

N . r u t i l i

L a s s ie r e , 1 9 8 8 ; D e z f u l i , 1 9 9 6 ) , w e r e c o m m o n i n t h e g r a ve l

a t a l l s ta t i o n s a l t h o u g h

S ia l i s u t a r i a

a n d t h e o t h e r i n t e r m e d i a t e h o s t w e r e v e r y

p a t c h i l y d i s tr i b u t ed F i g u r e 2 3 ) . T h e s e o b s e r v a t i o n s e x p l a i n t h e fa c t t h a t N .

r u t i l i

w a s t h e d o m i n a n t p a ra s i te i n t h e t r o u t c o l l e c t e d i n 1 9 9 8 . C o p e p o d s , t h e

i n t er m e d i a t e h o s t o f D . d i tr emum w e r e v e r y a b u n d a n t a t S t a t i o n s 1 a n d 2 i n t h e

B o g a r e a T a b l e 2 8 ) . A s c o r m o r a n t s a re f r e q u e n t v i s it o r s t o t h e T r e g a r o n B o g

a r e a c o n d i t i o n s w o u l d a p p e a r t o f a v o u r t h e t r a n s m i s s i o n o f D . d i t r emu m .

H o w e v e r , t h e d e ar t h o r a b s e n c e o f o l d e r f i s h c o n t r a i n d i c a t e s th i s .



1 0 2 J .D . T H O M A S

to

i

1 2 3 4 5 8 7 8

~ A T ~

to

1 ~ 0 -

~

l o 0 -

~o-

i i f t i i L

1 2 3 4 6 e 7

S T A T I O N S

1 0 0 - -

o -

1 2 3 4 5 6 7

S T A T I O N S

9OO

5

~ o

4c0

i 1 0 o -

0 -

t

E l l l

1 2 3 4 5

~ A ~

~ r ~ _ _

i ] i

7 8

4 O - -

tO 3O

° ~

2 3 4 5 6 7 8

~ A ~

4 0 -

O

3 0 -

1o

0

ii

J i f i i ~ J

1 2 3 4 5 6 7 8

S T A T I O N S

to

2 ~ 0 -

=0oo-

1 ~ 0 -

1 ~ o -

1 2 3 4

S T A T I O N S

i I I

6 7 8

1 0 0 -

i i J i

1 2 3 4 5 6 7 s

S T A T I O N S

F igure 23 The mea n densities _+ S.E.) o f other potential hosts of he lminth parasites

at the various stations in the River Teifi in 1998.



ECOLOGY OF FISH PARASITES 1 3

A m m o c o e t e l ar v ae , t h e in t e r m e d i a te h o s t s o f t h e n e m a t o d e C u c u l l a n u s T . )

t r u t t a e ( M o r a v e c , 1 9 9 4 ), w h i c h c o e x i s t e d w i t h S . c o r n e u m , w e r e a b u n d a n t in

depo s i t ing s ed im en ts in the 1950s and f ea tu red in the food o f the t rou t a t tha t

t ime (Tho mas , 1962). H owe ver , by 1998 they had beco m e very r a re and h igh ly

o v e r d i s p e r s e d ( F i g u r e 2 3 ) . T h i s o b s e r v a t i o n e x p l a i n s t h e m u c h l o w e r

p r e v a l e n c e a n d a b u n d a n c e v a l u e s fo r C . t r u t t a e in the t rou t exam ined in 1998

compared w i th 1950 (F igures 10 and 19) . R h a p h i a s c a r i s a c u s t h e o n l y o t h e r

nem atode fou nd in 1998 occur red in on ly one t rout . As th i s nematod e has a f i sh

i n te r m e d i a t e h o s t t h e l o w p r e v a l e n c e v a l u e m a y b e a t t ri b u ta b l e t o t h e a b s e n c e

of p i s c ivo rou s l a rge r f i sh in the s am ple .

9 3 E l u c id a t io n o f E n v i ro n m e n t a l F a c to r s t h a t M a y h a v e C a u s e d t h e

D e c l in e i n t h e I n t e r m e d i a t e H o s t s

In o rde r to e luc ida te the po s s ib le cause s fo r the dec l ines in pa ras it e d ive r s i ty

a n d i n t h e n u m b e r s o f in t e rm e d i a t e h o s t s s u c h a s S . c o r n e u m and o the r s ed i -

m e n t d w e l l e r s s u c h a s a m m o c o e t e l a r v a e a n d G a m m a r u s p u l e x t h e

phys icochemica l f ac to r s tha t migh t be impl ica ted were inves t iga ted .

The r e la tive ly low range o f amm onia , n it rit e, n itr ate, phosph a te and B O D

values (Table 1) indicate that nei ther f iver i s l ike ly to suf fer f rom e utrophicat ion

or o rgan ic po l lu tion . To the con t ra ry , the nu t r i en t and o rgan ic load ing m ay be

benef ic ia l in these ac id w a te r s a s they f ac i li ta t e the r e lease o f bases an d hen ce

deacid if ica t ion dur ing decompos i t ion in the sediments (Davison, 1986, 1987) .

C h a n g e s i n p H a s s o c i a t e d w i t h c h a n g e s i n t h e v o l u m e o f w a t e r a r e m o r e

l ike ly to be ha rmfu l . T he p H va lues , wh ich va r ied be tw een 5 .5 and 7 .7 and 4 .8

and 6 .9 in the Te i fi and Pysg o twr , r e spec t ive ly , we re inver se ly co r re la ted w i th

wate r l eve l o r vo lume (Tab le 1 ) . However , the re i s ev idence tha t in t imes o f

h e a v y s p a t e t h e p H v a l u e s o f t e n d e c l i n e d t o v a l u e s e v e n l o w e r t h a n t h o s e

g iven in Tab le 1 (Wade , ve rba l communica t ion ) . I t i s we l l e s tab l i shed tha t

under these cond i t ions the m ob i l i s a t ion o f heav y meta l s , such as a lumin ium ,

z inc , l ead and co ppe r in to the l ab il e , ion ic fo rm wi l l be f avo ured (Hu tch inson

and Sprague , 1986 ; Howel l s e t a l . 1990) .

The r esu l t s o f ana lyses ca r r i ed ou t on s ed ime n t co res in the R iv er Te i f i

sugges t tha t heavy m eta l tox ic i ty m ay be invo lved in caus ing the dec l ine in the

d i s t ri b u t i o n a n d a b u n d a n c e o f i n t e r m e d i a t e h o s t s . T h u s , a c c o r d i n g t o t h e

U n i t e d S t a t e s E n v ir o n m e n t a l P r o t e c t io n A g e n c y ( U S E P A ) g u i d e l in e s ( G i e s y

a n d H o k e , 1 9 9 0 ) f o r s e d i m e n t s t h e m e t a l c o n c e n t r a t i o n s ( F i g u r e 2 4 a - d ) a r e

i n d ic a t iv e o f m o d e r a t e p o l l u t i o n i n th e c a s e o f c o p p e r a n d c h r o m i u m ( > 2 5

m g / k g d r y w e i g h t ) a n d o f h e a v y z i n c ( > 2 0 0 m g / k g d r y w e i g h t ) a n d l e a d p o l -

l u t i o n ( > 6 0 m g / k g d r y w e i g h t ) . T h e s e c o n c e n t r a t i o n s a l s o f a l l w i t h i n t h e

ac t ion l eve l s o f 40 and 20 0 mg/kg fo r lead and z inc , r e spec t ive ly , acco rd ing

to the equ i l ib r ium par ti tion ing approach o f W ebs te r and R idgw ay (1994) . Th ey



104 J D THOMAS

are also outside the limits of tolerance (250 and 800 mg/kg for lead and zinc,

respectively) set by the Ontario M inistry o f the Environment (Giesy and H oke,

1990).

The levels of metal pollution found in the River Teifi sediments are com-

parable to those in the sediments of industrial ly polluted aquatic habitats .

Thus, Che and Cheung (1998) found lead and zinc levels of 100-155 and

226--421 mg/kg, respectively, in the Mai Po marshes in Hong Kong whilst

B u b b et a l . (1991) found lead and zinc levels of 100-15 5 and 226-421 mg/kg,

respectively, in the R iver Yare, N orfolk.

H eav y metals such as lead and zinc are readily accum ulated by invertebrates

and hence b y their f ish predators (W oodw ard et a l . 1994). As low pH condi-

t ions favour the mobilisation of heavy metals , such as aluminium, zinc and

lead, into the labile, ionic forms (Muniz, 1991) it might be expected that the

rate of bioaccumulation and hence toxicity would be enhanced by increased

acidity. How ever, the relationship b etw een pH and m etal toxicity is not simple.

In the ca se o f copper, for exa mp le, although the conce ntration of the Cu 2+ ion,

wh ich is the m ajor toxic species, increases with increase in H + concen tration

its toxicity is reduced by com petition from H + at the active sites (O Sulliva n e t

al . 1989). It is also notew orthy that high H ÷ concentrations on their o w n can

also be toxic to aquatic organisms as they disturb acid-base hom eostasis and

ionic regulation (Wood, 1987).

Although nothing specific can be said about the toxic effects of heavy

metals in the sediments as the pore water concentrations are unknown some

conclusions can be drawn from the chemical analysis of the water column

(Table 1). The total hardness values for both the Pysgotwr and the Teifi are

very lo w (2 .5-5.1 m g 1-1 and 6 .5-2 5.5 mg 1-1, respectively). As a result Table

1 shows that the environmental quality standards (EQS) for aluminium, zinc,

lead and cop per (100, 8, 4, and 1 lag 1-1, respective ly) are of ten ex cee ded in

these base-deficient rivers (D epartment of the Environment and Welsh Office,

1989).

The potential dangers to the biota of base-deficient water bodies from alu-

minium toxicity are well docum ented (Turpenny, 1989; H ow ells et a l . 1990;

Merret et a l . 1991; Departm ent o f W ater Affairs and Forestry, 1996). T oxicity

due to aluminium is most l ikely to occur during episodic, spate condit ions

wh en toxic aluminium and H + concentrations r ise by an order of ma gnitude

whilst C a 2+ concentrations, wh ich h ave an am eliorating effect, fall (R eader and

Dempsey, 1989) . I t i s most toxic a t pH 6 .5-5 .0 when the hydroxy forms

AI(OH)2+ and AI(O H) 2÷ predo min ate but within that range the to xicity is inde-

pendent of pH (How el ls et a l . 1990).

The pH values fall to 5.5 and 4.8 in the Teifi and Pysgotwr, respectively,

under spate condition s (Table 1). It is proba ble that under these con ditions the

alum inium concentrations (Table 1) will exceed the target water quality range

(5 lag l-l), th e ch ronic effe ct value (1 0 lag 1-1) and the acu te ef fect value (I 00 lag



E C O L O G Y O F F I S H P A R A S I T E S 1 0 5

~ ~ z

, ~ - ~ _ o

I ~

~:~ ~ t

i i

I I I I I I I I

( 3 ' s - / + 6 )1 /8 w ) S N O I I V E I I N ~ O N O O O r- -J 7

~-4 I

I I I I I I

8 g g o g g

09

Z

O

( : : r s - / + 6 )I /SL U) SNO I / VE I . L N= I O NO O O NI Z

.Q

, - ~

, I I I - ~

~ - ~

/

, i , q - ~

, I i I - ~ i

i i i i - ~

I I I

o

( '3 S - / + B )l/8 W ) S N O I / ~ I / N : I O N O O I /I rl ll ~ O E IH O

i I I I ~.

I 1 I - ~

I I

I - ~

~ - ~ , - ~

, - ~ , - ~

~ -E ~ - -T--

r 1 -

( ' 3 3 - / + 8 )l /Su J ) SNO I 2 VEM .N= IO NO 0 E F I d d O O

~J ~ O

+ l



1 0 6 J D T H O M A S

1-1 spec i f i ed by Sou th Af r i ca W ate r Qu a l i ty Gu ide l ines Dep ar tmen t o f W ate r

Af fa i r s and Forest ry , 1996) . Acc ord ing to Bod e t e t a l . 1 9 8 8 ) w h e n t h e p H i s

be tw een 4 .0 and 5 .6 a lum in ium a t concen t r a t ions o f 100 lag 1-1 i s acu te ly tox ic

to fi sh . The tox ic e f f ec t s peak a t pH 5 .2 -5 .6 wh ich a re w i th in the r anges fo r the

Te i fi and Pysgo tw r . Tox ic i ty va lues g iven by Turpen ny 1989) fo r r a inbow

t rou t a r e even low er 40 pg 1-1 LCs0 24 h ) and sub le tha l e f f ec t s in the fo rm o f

r e d u c e d g r o w t h r a te s h a v e b e e n r e p o r t e d f o r b r o w n t r o u t w h e n t h e a l u m i n i u m

con centra t io ns w ere 2 0 lag 1-1 Kel ly , 1988) . Inv er tebra tes v ary in thei r sus -

c e p t i b il i ty t o a lu m i n i u m t o x i c i ty w i t h m e m b e r s o f t h e C l a d o c e r a a n d

E p h e m e r o p t e r a b e i n g m o s t v u l n e r a b l e a n d t h e P l e c o p t e r a a n d S p h a e r i i d a e

be ing m os t r e s i s tan t M er re t e t a l . 1991; Wren and S tephenson, 1991) . In the

case o f the Sphaer i idae the apparen t a lum in ium res i s t ance un der na tu ra l con-

d i t ions may be due to the bac te r i a l genera t ion o f a lka l in i ty in the depos i t ing

sed ime n ts where they l ive J . G . Jones , 1985 ; Th om as and Love , unpub l i shed

data) .

I n v i e w o f th e a b o v e c o n s i d e r a ti o n s i t s e e m s p o s s i b l e th a t h i g h a l u m i n i u m

concen t r a t ions in t ime o f spa te in the base -de f ic ien t r ive r s inves t iga ted may

have co n t r ibu ted to the dec l ine in bo th the b rown t rou t and the i r he lmin th pa r -

as i tes . Ho we ver , fur ther research is required to tes t th is hypo thes is as inorganic

and o rgan ic l igands such as humic subs tances may ac t a s complex ing agen t s

a n d m o d i f y a l u m i n i u m t o x ic i t y B o d e t

e t a l .

1988) . There i s ev idence that

h u m i c s u b s t a n c es H S ) m a y r e d u c e t h e t o x i c i ty o f a lu m i n i u m t o r a i n b o w t r o u t

and o the r f i sh and tha t the su rv iva l r a t e s o f inver teb ra tes , wh ich can inges t

H S - m e t a l c o m p l e x e s , m a y a l s o b e e n h a n c e d u p t o a c r i t i c a l t h r e s h o l d

Tho ma s , 1997). As bo th the Py sgo tw r and the Te if i a r e dys t roph ic and the re -

fo re ri ch in hum ic su bs tances th is m ay he lp to exp la in w hy the f auna appe ar s

no t to have su f f e red even m ore f rom h eavy m eta l po l lu t ion a l though the b row n

t ro u t h a v e d i s a p p e a r e d f r o m t h e P y s g o t w r .

O t h e r h e a v y m e t a l s, w h i c h m a y h a v e c o n t r i b u te d t o t h e d e c l i n e o f t h e f a u n a

in the Tei fi, a r e z inc , l ead and cop per w h ich o ccur a t concen t r a tions o f 11 -109 ,

2 - 5 a n d 1 . 7 - 5 . 0 lag 1 -1 , r e s p e c t i v e l y . T h e c o r r e s p o n d i n g v a l u e s f o r t h e

Pysg o tw r , wh ich a re 2 -18 , 2 and 1 -2 lag 1 -1 , r e spec t ive ly a re much low er

re f l ec t ing the lower l eve l o f min ing ac t iv i ty in th i s ca tchmen t . In con t r as t ,

z i n c , l e a d a n d s i l v e r w e r e b e i n g m i n e d i n t h e E s g a i r m w y n , C w m - m a w r a n d

A bb ey Co nso l s m ines in the upper ca tchm en t o f the Te ifi in the n ine teen th cen -

tury. Carpen te r 1926) found tha t the e f f luen t s f rom the Esg a i rm w yn m ine

we re caus ing r ap id de te r io ra t ion in the f auna o f the Marchnan t , a headw ate r o f

the Te if i, and s t r e s sed tha t the re w as a g rave d anger o f even tua l in ju ry to the

main r ive r. As po in ted ou t by Jones 1940 , 1958) pe r s i st ence i s one o f the main

c h a r a ct e ri st ic s o f h e a v y m e t a l p o ll u t io n a n d t h e p r o b l e m h a s r e m a i n e d t o t h e

p resen t day . Thus , a l though m uch o f the main r ive r qua l i ty was c las sed as

Grad e 1A in 1980 Na t iona l W ate r Qu a l i ty Survey ) som e t r ibu ta r ie s and the

m a i n r i v e r u p s tr e a m o f T r e g ar o n w e r e d e s i g n a t ed G r a d e 2 b e c a u s e o f e l e v a te d




concen t r a t ions o f z inc o rig inat ing f rom the de re l ic t mine work ings in the uppe r

ca tchmen t . More r ecen t ly , Ha l l (1998) found tha t the env i ronmen ta l qua l i ty

s ta n d a rd s ( E Q S ) f o r z in c , l e a d o r c o p p e r w e r e b r e a c h e d o n 1 3 o c c a s i o n s i n

Na n t L lues t , a smal l t r ibu ta ry o f the Te i fi , nea r S t r a ta F lo r ida A bbey , bo th

d o w n s t r e a m a n d u p s t re a m o f th e i np u t f ro m C w m - m a w r m i n e ( S N 7 3 6 6 7 3 ).

A l t h o u g h t h e i n v e rt e b ra t e f a u n a a p p e a r e d u n a f f e c t e d d u r in g t h e b r i e f s u rv e y

per iod som e o f the s a lm on id f i sh show ed ev idenc e o f b lack - ta il ing a t t r ibu tab le

to me ta l poisoning. In v iew o f Hal l s f indings i t i s not surpr is ing to f ind that the

concen t r a t ions o f z inc , l ead and copp er in the R iver Te i f i wa te r co lum n (Tab le

1 ) o f t e n e x c e e d t h e E Q S s e t b y t h e E n v i r o n m e n t A g e n c y . T h e s e a r e 8 , 4 a n d 1

~tg 1-1 , respec t ively , for sof t wa ters w i th h ardne ss < 50 m g 1-1 . A s w i th a lu-

m in ium the ava i l ab il i ty o f these me ta l s to aqua t i c o rgan i sm s inc reases w i th

decreas ing wa te r ha rdnes s , pH , a lka l in i ty and ca lc ium concen t r a t ions . The i r

ava i l ab i l i ty the re fo re t ends to inc rease du r ing ep i sod ic spa te even t s ( Jones ,

1943 , 1958 ; Ke l ly , 1988) . However , a l though the i r tox ic i ty inc reases w i th

decreas ing wa te r ha rdnes s the r e la t ionsh ip i s no t l inea r a s the e f f i c i ency o f the

c a r ri e r -m e d i a t e d t r an s p o r t s y s t e m d e c r e a s e s w i t h f a ll in g p H b e c a u s e o f c o m -

pe t i t ion be tw een the m eta l ions and the H ÷ ion (W ren an d S tephenson , 1991 ;

Gerhard t , 1993 ; O Su l l iva n e ta l . 1989) .

A s w a s t h e c a s e w i t h t h e R i v e r Y s t w y t h d u r i n g i t s r e c o v e r y p h a s e ( J o n e s ,

1940) the conc entra t ion o f z inc exc eed s that of lead indicat ing that z inc is m ore

per s i s ten t and the re fo re m ore l ike ly to be a danger to the aqua t i c com m uni ty .

Th i s danger i s exace rba ted by the f ac t tha t a l though z inc i s l e s s tox ic than

copper i t has a lower t endency to adso rb . As a r e su l t a g rea te r p ropor t ion i s

l ikely to ex is t in so lu t ion .

A l thou gh the re i s a g rea t dea l o f tox ico log ica l da ta ava i l ab le fo r z inc and

o t h e r m e t a ls e v a l u a t i o n i s o f t e n h a m p e r e d b e c a u s e o f d i f f e r e n c e s in p h y s i c o -

chemical condi t ions (e .g . , temperature , water hardness , ca lc ium concentra t ions

a n d w a t e r f l o w ) , t im e s , g e n o t y p e a n d p h y s i o l o g i c a l s t a te o f t h e a s s a y a n i m a ls .

Ac cord ing to the da ta p resen ted by K e l ly (1988) the LCs0 21 d z inc va lues fo r

s a l m o n p a r r u n d e r p h y s i c o c h e m i c a l c o n d i t io n s r e s e m b l i n g t h o s e f o r t h e T e if i

r anged f rom 0 .34 to 1 .45 m g 1-1 o f z inc. These com pare w i th va lues o f 0 .6 -4 .76

m g 1 ~ LCs0 48h fo r r a inbow t rou t. Bo th va lues a r e abo ve the concen t r a t ion

ranges fou nd in the Te if i. Ho wev er , acco rd ing to Jones (1962) z inc ma y b e f a tal

to the ova and a lev ins o f r a inbow t rou t a t concen t r a t ions o f 10 -20 pg 1 1 w h i c h

are w i th in the r ange o f conc en t r a t ions foun d in the Te if i.

The m ajo r i ty o f the LC50 va lues ob ta ined in tox ic i ty t e s ts fo r z inc ca r r ied o u t

on aqua t i c inverteb ra tes c i t ed by K e l ly (1988) a r e a l so genera l ly we l l above the

z i n c c o n c e n t r a t i o n s f o u n d i n t h e T e i f i , t h e e x c e p t i o n s b e i n g Tubifex a n d

Daphnia spp . wh ich appear to be h igh ly suscep t ib le to zinc . F ree - l iv ing t r ema-

tode l a rvae a l so appear to be vu lne rab le to z inc . Thus , the ce rca r i a l encys tm en t

i n th e c a s e o f Notocotylus attenuatus and the su rv iva l time and in fec t iv i ty o f

Echinoparyphium recurvatum cerca r i ae were impa i r ed a t z inc concen t r a t ions



108 J D THOMAS

of 4-10 lag 1 - 1 and 0 .01-10 .0 l ag 1 - 1 respect ively Evans , 1982a, b) . More

recent ly i t has be en sho wn tha t the surv ival o f S c h i s t o s o m a m a n s o n i mirac id ia

and ce r ca r i ae o f

D i p l o s t o m u m s p a t h a ce u m a re

i mpa i r ed w he n z i nc concen t r a -

t ions exce ed 100 lag 1 l M orley

e t a l .

2001a, b) . In the case of the la t ter

s pec ie s i t w as s how n t ha t i nc r eas ing ha r dnes s and dec r eas i ng t emper a t u r e

M o r l e y e t a l . 2001b) r edu ced t ox i ci ty . O bs e r va t i ons by J ones 1940 ,

1949 ,1958 , 1962) i n z i nc - po l l u t ed W el sh r i ve rs s how i ng t ha t o l i gochae t e

w or ms , l eeches , mo l l u s cs and c r us t acea a r e mor e s us cep t i b l e t o z i nc t han

l i thoph i lous insects are in accord wi th toxicolog ical data Kel ly , 1988).

Th e concen t ra t ions of l ead in the Teif i wa ter co lum n 2-5 .4 lag 1-1) a re low

com pared wi th mo re heav i ly po l lu ted r iver s such as the Derw ent 65 lag 1 - 1 ;

Kelly, 1988) an d the Y stw yth 50 lag l - i ; Jones , 1940) . Th ese relat ively low

con cen trat ions are at t r ibutable to the fact that lead pol lut ion is less pers is tent

than tha t caused by z inc Jones , 1940). Fu r thermo re , m os t o f the so lub le l ead

t ends t o be r em oved by t he s ed i men t s o r by s us pended pa rt icu l a te o r gan i c and

i no r gan i c ma t t e r s uch a s hyd r ous ox i des , c l ays and humi c s ubs t ances .

How ever , a l thoug h the so lub le l ead con cent ra t ions in the Tei f i m ay a ppear to

be low th ey fa ll w i th in the TQ R ta rge t qua l ity r ange) 0 .2 lag 1-1), the CE V

chro nic ef fe ct value) 0 .5 lag 1 l ) a nd the A EV acu te ef fec t value) 4 .0 lag 1-1)

se t by the South Af r ican Water Qual i ty Guide l ines for water w i th hardness l es s

than 60 m g 1-1 ca lc ium carbonate Dep ar tmen t o f Water Af fa i r s and Fores t ry ,

1996).

I t is d i f f i cu l t how eve r to draw any f i rm conc lus ions f rom the above va lues

as the tox ico logy of l ead i s com pl ica ted by the fo l lowing con s idera t ions. Thus ,

i t can exis t in several oxida t ion s tates 0 , I, II and IV) and also form co m plex es

wi th organ ic and inorgan ic l igands . Le ad spec ia t ion and hen ce i ts b iova i lab i l-

i ty can b e i n f l uenced by a n um ber o f phy s i cochem i ca l f ac to r s i nc lud i ng pH .

U nd er ac id condi t ions i t i s the lowe r ox ida t ion s ta te , Pb I I) , tha t is the m os t

s tab le und er norm al ox id i s ing condi t ions and i ts so lub i l i ty i s cont ro l l ed by th e

ava i lab il i ty o f the su lpha te ion . Ac cord ing to Gerhard 1993) and W ren an d

Stephenson 1991) there i s ev idenc e tha t lower ing pH increases l ead up take by

inver tebra tes and the e f fec t is var iab le and d epen den t on spec ies . Fur therm ore ,

there i s unce r ta in ty r egard ing ho w aquat ic an imals seques te r lead . Inver tebra te

lead l eve ls appear to b e l a rge ly in f luenced by sed imen t lead con cent ra t ions and

sur face adsorp t ion m ay accoun t for a l a rge propor t ion o f l ead in ben th ic inver-

tebrates W ren and S tephenson , 1991). W he n absorbed on m ucu s cover ing

gi ll s i t m ay ind uce coag ula t ion and de a th by suf foca t ion . A l tho ugh lead b ioac-

cum ula tes in ind iv idua l o rganism s there is no ev iden ce tha t it b ioma gni f ies in

the aquatic food cha in W ren and S tephenson , 1991).

How ever , i t would appear f rom the acu te tox ico log ica l da ta for lead , sum -

m ar i s ed by K e l l y 1988) , t ha t t he LC s0 f o r s a l mon i d fi s h and aqua t i c

i nve rt eb ra t es a r e o f t en o r de r s o f m agn i t ude h i ghe r t han t he am b i en t l e ad con -

cen t r a t i ons i n t he T e i f i . O n t he w ho l e t he r e f o r e t he p r e s en t r e s u l t s w ou l d




appear to suppor t the conc lus ions o f W ren and S teph enson 1991) tha t the con-

cen t r a t ions a t wh ich l ead i s acu te ly tox ic to aqua t i c o rgan i sms a re genera l ly

m u c h h i g h e r th a n a m b i e n t c o n c e n t ra t io n s .

A w o r d o f c a u t i o n i s n e e d e d h e r e h o w e v e r a s s o m e t a x a s u c h a s

G am m arus

spec ies a r e pa r t i cu la r ly vu lne rab le to l ead tox ic i ty . Thus , the LCs0 28 d va lue

f o r

G am m arus p seudo l im naeus

w as 0 .028 4 m g 1-1 . In co ntras t ,

Crangonyx

pseudograci l i s wh ich has an LCs0 48 h o f 43 .8 m g 1 -1 fo r l ead , i s muc h m ore

t o le r an t , w h i c h i s i n c o m m o n w i t h m o l l u s c s s u c h a s

Lymnaea and Pi s id ium

s p e c i e s W r e n a n d S t e p h e n s o n , 1 9 91 ). A s l e a d m a y a l s o i n d u c e h a rm f u l s u b -

le tha l e f f ec t s i t i s pos s ib le tha t these obse rva t ions on l ea d tox ic i ty unde r ac id ic

s p a t e c o n d it i o n s m a y h e l p t o e x p la i n t h e r e p l a c e m e n t o f

G am m arus pu lex

b y

Crangonyx

in the upp er Te if i. Fu r the r w ork on the sub- le tha l e f f ec t s o f l ead

tox ic i ty i s ind ica ted pa r t i cu la r ly a s under ae rob ic cond i t ions methy la t ion o f

l ead can occur . There i s ev idence tha t o rganometa l l i c l ead spec ies a r e o f t en

m ore tox ic than ino rgan ic l ead spec ies Ke l ly , 1988) .

C o p p e r i s o n e o f t h e m o s t t o x ic o f th e h e a v y m e t a l s. A c c o r d i n g t o S o u t h

A f r i c a n W a t e r Q u a l i t y G u i d e l i n e s t h e T Q R , t h e C E V a n d A E V v a l u e s f o r

cop per in so f t wa te r s w i th ha rdnes s l e s s than 60 m g C aC O 3 a re l e s s than 0 .3 ,

0 .53 an d 1 .6 lag 1-1 , respe ct ive ly D epa r tm ent o f W ater Affa i rs and Fores t ry ,

1996) . As the copper concen t r a t ions in the wa te r co lumn o f the Te i f i exceed

these va lues copper tox ic i ty i s a po ten t i a l p rob lem par t i cu la r ly du r ing ac id ic

e p i s o d e s i n t i m e s o f s p a t e w h e n s p e c i a t i o n t o t h e t o x i c C u 2+ i s f a v o u r e d .

H o w e v e r , t h e t o x i c i ty o f c o p p e r i s i n h ib i te d b y t h e p r e s e n c e o f h u m i c a c i ds ,

wh ich a re abundan t in these dys t roph ic wa te r s , and a l so by amino ac ids , sus -

p e n d e d s o l id s , H ÷ a n d o t h e r m e t a l s. T h e a c u t e t o x i c i t y l e v e l s f o r c o p p e r

s u m m a r i s e d b y K e l ly 1 9 8 8 ) a re h o w e v e r m o r e th a n a n o r d e r o f m a g n i t u d e

h i g h e r t h a n t h e S o u t h A f r i c a n g u i d e l in e s . T h u s , t h e L C s 0 9 6 h v a l u e s f o r

copper , in the case o f adu l t and juv en i l e r a inbo w t rou t in so f t , ac id ic , con t in -

uo us ly f lowin g wa te r we re 28 .9 lag 1-1 and 17-3 8 lag 1-1 , r e spec t ive ly . The

m e t o x r a n g e f o r zi n c, c o p p e r a n d le a d g i v e n b y T u r p e n n y 1 9 8 9 ) a s a f r a c ti o n

of the p re d ic ted LCs0 48 h va lues fo r s a lm on id f i sh a re even h igher r ang ing

f rom 0 .26 to 0 .49 m g 1 -1 . M ol luscs a r e pa r t icu la r ly suscep t ib le to copp er tox -

ic i ty and as in the case o f s a lmon ids suscep t ib i l i ty dec l ines w i th matu r i ty .

Thus , the LCs0 96 h fo r juve n i l e

Potamopyrgus jenk ins i

wa s 0 .054 m g 1-1 com -

pared w i th 0 .079 mg 1 l fo r adu l t s Ke l ly , 1988) . Evan s 1982a , b ) a l so foun d

tha t the l a rvae o f d igene t i c t r ematodes as we l l a s the i r hos t s were adver se ly

a f f ec ted by sub- le tha l concen t r a t ions o f copper . Thus , a coppe r concen t r a t ion

o f 0 .01 lag 1-1 cau sed a red uct io n o f snai l ac t iv i ty and shed ding of

Notocotylus

at tenuatus c e r c a r ia e E v a n s , 1 9 8 2 a ) w h i l e a c o p p e r c o n c e n t r a ti o n o f 0 . 0 1 - 1 0

lag 1-1 red uc ed the surv ival t im e a nd infec t iv i ty o f

Echinoparyphium recurva-

rum Evans , 1982b) .

Th i s r ev iew ind ica tes tha t heavy m eta l tox ic ity , invo lv ing a lumin ium , z inc ,

l ead and copper , i s po ten t i a l ly a cause fo r conc ern fo r the uppe r Te if i wh ereas



110 J D THOMAS

a l u m i n i u m a l o n e s e e m s t o b e a p r o b l e m f o r th e u p p e r T o w y . I t i s v e r y im p o r -

tant therefore that fur ther research should b e unde r taken in the f ie ld to ascer ta in

the va r ia t ion in the r ange o f concen t r a t ion o f the tox ic me ta l spec ies encoun-

te red in the wa te r co lum n and in the po re w a te r a t d i f f e ren t s easons and du r ing

e p i s o d i c s p a t e e v e n t s . T h i s w o r k s h o u l d b e f o l l o w e d u p w i t h t o x i c o l o g i c a l

s tudies , und er s imu lated natura l condi t ions , to ascer ta in poss ib le sub- le thal and

acu te e f f ec t s o f the heav y meta l s on s a lm on id f i sh and we l l - s e lec ted rep resen -

ta t ives o f the inver teb ra te f auna . A t ten t ion shou ld b e g iven to the pos s ib i l i ty o f

synerg i s t i c and on togene t i c e f f ec t s invo lv ing the meta l s and py re th ro ids and

a l so tha t the f auna may have become hab i tua ted to me ta l tox ic i ty . The deve l -

o p m e n t o f r e s is t a n c e t o m e t a l t o x i c it y is a w e l l - k n o w n p h e n o m e n o n . T h u s ,

M a s o n ( 1 9 9 6 ) c i te s th e e x a m p l e o f

sel lus

having an LCs0 48 h o f 3 .50 m g 1-1

fo r l ead in con tam ina ted wa te r com pared w i th 0 .28 m g 1-1 in the con t ro l r iver .

The p y re th ro ids , cyperm eth r in and f lumeth r in , de r ived f rom sheep d ipp ing

(Arm strong and Phi l l ips , 1998) w ere a lso presen t in m easu rable concen tra t ions

o f up to 11 .7 and 19 .6 l ag /kg , r e spec t ive ly , in the s ed im en t p o re w a te r a t

S ta t ions 2 , 5 and 7 (F igu re 25a , b ) . H ow ever , a s these pes t i c ides b ind r ead i ly

to minera l s and humic subs tances the i r b ioava i l ab i l i ty i s r educed excep t to

s e d i m e n t - f e e d in g o r g a n is m s . C y p e r m e t h r in i n th e w a t e r c o l u m n i s v e r y t o x ic

to the majo r i ty o f f r e shwate r o rgan isms inc lud ing m ayf ly l a rvae (24 h LCs0 0 .6

lag 1-1 ; S te ph en son , 1982 ) ,

G a m m a r u s p u l e x

(24 h LCs0 0 .009 lag 1-1 ;

S teph enson , 1980) an d f ish (9 6 h LCs0 1 .2 lag 1-1 for bro w n t rout ; S tephe nson ,

1982). M ol luscs a r e how ever l e s s suscep t ib le to cyperm eth r in as the 96 h LCs0

fo r

Lymnaea acum inata

i s 0 .36 m g 1-1 ( S ingh an d Agarw al , 1986) . D ur ing the

t i m e o f t h e p r e s e n t in v e s t i g a t i o n t h e c o n c e n t r a t i o n s o f c y p e r m e t h r i n a n d

f lumeth r in in the w a te r co lu m n w ere l e s s than 0 .002 lag 1 -1 . Ho we ver , the

W e l sh E n v i r o n m e n t A g e n c y fo u n d th a t 2 1 o f t h e s it e s i n v e s ti g a te d in W e l sh

r ive r s du r ing 1997 f a i l ed to mee t the env i ronmen ta l qua l i ty s t andards fo r

cyperm eth r in (Env i ronm en t Agency , W ales, 1998). I t i s the re fo re ev iden t tha t

the inver tebra te and f ish com m uni t ies in the Teif i, and o ther rivers whe re sheep

fa rming i s the dom inan t fo rm o f ag r icu ltu re , a r e under s e r ious th rea t f rom

ep isod ic po l lu t ion by py re th ro ids de r ived f rom sheep d ipp ing .

The o the r under ly ing an th ropogen ic r eason s fo r the pos s ib le dec l ine in the

b rown t rou t popu la t ions and the i r pa ras i t e s in the Te i f i a r e summar i s ed in

Table 29 . Th e environm ental fac tors that are im pl ica ted in teract syn ergis t ica l ly

to the de t r imen t o f the aqua t i c env i ronm en t . The eco log ica l th rea t posed by

a c i d d e p o s it i o n h a s b e e n w e l l r e v i e w e d b y a n u m b e r o f p e o p l e ( H o w e l l s a n d

M orr is , 1989; M ason , 1992) . Un for tunate ly , the hard , base -def ic ie nt , roc ks

and ac id ic so i ls have mad e the Te i fi and the Ty wi ca tchm en ts pa r t i cu la rly sus -

c e p t i b l e t o a c i d i f i c a t i o n . T h i s t e n d e n c y h a s b e e n f u r t h e r e x a c e r b a t e d b y

chang es in land use . These hav e inc luded a f fo res ta t ion o f the ca tchm en ts o f

som e o f the m ajo r t r ibu ta r i e s w i th c on i f e rou s t rees and the lo s s o f h il l f a rms .

There i s ev idence tha t the p inna te l eaves o f con i f e rous t r ees f ac i l i t a t e the




T h e r e i s a ls o e v i d e n c e th a t t h e c o m m u n i t y o f m i c r o o r g a n i sm s a n d i n v e rt e -

b r a t e s a s s o c i a t e d w i t h d e p o s i t i n g s e d i m e n t s p l a y a k e y r o l e i n t h e

d e a c i d if i c a ti o n o f b o t h t h e s e d i m e n t p o r e w a t e r a n d t h e o v e r l y in g w a t e r. T h e

deac id i f i ca t ion p roces s invo lves a lka l in i ty p roduc t ion b y m ic robes us ing NO3

S O 4, Fe ( I I I ) , Mn ( IV) and va r ious ca rbon compounds as t e rmina l e l ec t ron

a c c e p t o r s ( J . G . J o n e s , 1 9 8 5 ; S c h i n d l e r 1 9 8 6 ) . T h i s m u t a l i s t i c p r o c e s s i s

enhance d b y the p resence o f tub icu lous ch i ronom id l a rvae and tub i f i c id worm s

w h i c h c a u s e b i o t u r b a t i o n ( P e l e g r i a n d B l a c k b u r n , 1 9 9 5 ; T h o m a s a n d L o v e ,

unpub l i shed da ta ) .

An o ther m a jo r f ac to r in caus ing the de c l ine o f the b row n t rou t and the ir pa r -

as i t e s has been the in tens i fi ca t ion o f sheep f a rming . Be tw een 1950 and 1996

t h e t o t a l s h e e p p o p u l a t i o n i n t h e U K d o u b l e d f r o m 2 0 . 4 t o 4 1 . 5 m i l l i o n

(Arms t rong and Ph i l l ip s , 1998) . Sheep f a rming i s pa r t i cu la r ly impor tan t in

W ales and Sco t l and as 50 -60 o f ho ld ings ca r ry sheep . Un fo r tuna te ly , the

s h e e p c a n b e v e r y h a r m f u l t o l o ti c h a b it a ts a s t h e y d e s t ro y a n d d a m a g e v a l u -

a b l e r i p a r i a n t r e e s , s u c h a s a l d e r a n d w i l l o w , a n d c a u s e e r o s i o n i n t h e

ca tchmen t in genera l and to the banks in pa r t i cu la r . As a r e su l t the inpu t o f

a l loch thono us o rgan ic m at te r i s r educe d , the banks a re des tab i l i s ed and inver -

t eb ra tes and s a lmon id f i sh a re dep r ived o f impor tan t r e fug ia inc lud ing those

prov ide d by undercu t banks and t r ee roo t s . Such ' de ad zo nes ' a r e imp or tan t a s

they f ac i l it a t e the re ten t ion o f s il t and o rgan ic mat te r w h ich a l low sed im en ts to

b e c o m e a n o x i c a n d b a s e f o r m a t i o n t o o c c u r.

I t i s p o s s i b l e a l s o t h a t i n c r e a s e d e r o s i o n r e s u l t i n g f r o m o v e r g r a z i n g b y

sheep m ay f ac i l i ta t e the r e lease o f heavy m eta l s f rom so i ls pa r ti cu la r ly in the

u p p e r c a t c h m e n t o f th e T eifi w h e r e t h e m e t a ll if e ro u s E s g a i r m w y n , C w m - m a w r

and Abb ey Co nso l s m ines a re loca ted . Mine t a il ings a re s t il l p r esen t in these

m ines and as po in ted ou t by Jones (1940 , 1958 , 1962) one o f the ou t s tand ing

fea tu res o f po l lu t ion by he avy m eta l s i s it s pe rs i s tence . T here i s a l so som e c i r-

cum s tan t i a l ev idenc e tha t sheep g raz ing m ay have con t r ibu ted to ac id i f i ca tion

of s t r eams and l akes in Norway as in tens i f i ca t ion o f sheep g raz ing a t h igher

leve l s co in c ided w i th inc reased a c id i f ica t ion (Maso n , 1992) .

9 4 H e l m i n t h P a r a s it e s a n d o t h e r A q u a t i c O r g a n i s m s a s P o l lu t io n

B i o i nd i c a to r s

As a resu l t o f eve r - inc reasing l eve l s o f an th ropogen ic e nv i ronm en ta l po l lu t ion

i t h a s b e c o m e o b l i g a t o r y to m o n i t o r p h y s i c o c h e m i c a l p a r a m e t e r s t o e v a l u a te

wate r qua l i ty on a rou t ine bas i s and a l so when po l lu t ion inc iden t s a r e sus -

p e c t e d . H o w e v e r , b e c a u s e o f th e i r e p i s o d i c o r t ra n s i t o ry n a t u re , p o l l u t i o n

i n c id e n t s m a y e a s i l y b e o v e r l o o k e d w h e n u s i n g s u c h m e t h o d s . I t h a s t h e r e f o re

b e e n s t re s s e d b y m a n y a q u a t i c b i o lo g i s t s i n c lu d i n g H y n e s ( 1 9 6 0 ) a n d M a s o n

( 1 9 9 6 ) t h a t t h e p h y s i c o c h e m i c a l i n v e s t i g a t i o n s m u s t b e c o m p l e m e n t e d b y



114 J D THOMAS

us ing b io ind ica to r s under bo th f i e ld and l abo ra to ry cond i t ions . B iom oni to r ing

a l so has the added advan tages o f mak ing i t pos s ib le to iden t i fy the po l lu t ion

s o u r c e a n d o f p r e d ic t in g t h e p o s s i b l e c o n s e q u e n c e s t o t h e c o m m u n i t y o f th e

type o f po l lu t ion invo lved .

T h e r e h a s b e e n m u c h d i s c u s s i o n r e g a rd i n g t h e k i n d s o f o r g a n i sm s t h a t

m igh t be us ed as b io ind ica to r s o f po llu t ion . I t m ay b e sugge s ted tha t the fo l -

lowing c r i t e r ia shou ld be me t whe n se lec t ing b io ind ica to r s :

1 . I t shou ld be pos s ib le to p red ic t the k ind o f aqua t i c com m uni ty tha t one

m i g h t e x p e c t i n a n o n - p o l l u t e d a q u a t i c e n v i r o n m e n t f r o m t h e r e l e v a n t

p h y s i c o c h e m i c a l d a t a a n d t h e n u s e t h e s e d a t a a s a b a s i s f o r c o m p a r i s o n

wi th po l lu ted hab i ta t s .

2 . T h e b io m o n i t o r in g m e t h o d s h o u l d b e r o b u s t a n d h a v e g e n e r a l a p p l ic a t io n

in a range o f habi ta ts .

3 . The s e lec ted o rgan i sms shou ld be h igh ly r espons ive to the pa r t i cu la r po l -

lu tan t o r the typ e o f po l lu t ion be ing inves tiga ted .

4 . T h e e c o - p h y s i o lo g i c a l , b i o c h e m i c a l a n d b e h a v i o u r a l r e s p o n s e s s h o w n b y

the o rgan i sms to the po l lu tan t shou ld be under s tood .

5 . The b io ind ica to r s s e lec ted shou ld be r ead i ly acces s ib le and iden t if i ab le .

6 . I t s h o u l d b e p o s s i b l e t o a p p ly t h e m e t h o d w i t h o u t c a u si n g u n d u e e n v i ro n -

m e n t a l d a m a g e .

7 . The b io t i c index used shou ld be cos t e f f ec t ive w i th r espec t to the r esources

avai lable .

M a n y p a r a s i t o l o g i s t s i n c l u d i n g K h a n a n d T h u l i n ( 1 9 9 1 ) , P o u l i n ( 1 9 9 2 ) ,

M a c K e n z i e

e t a l

( 1 9 9 5 ) , Y e o m a n s

e t a l

( 1 9 9 6 ) , K e n n e d y ( 1 9 9 7 ) , C h u b b

( 1 9 9 7 ) a n d L a n d s b e r g e t a l (1998) have d i s cus se d the pos s ib i l i ty o f u s ing f i sh

paras i t e s a s b io ind ica to r s o f po l lu t ion . U nfo r tuna te ly , a l though f i sh pa ras i te s ,

i n c o m m o n w i t h o t h e r a q u a t ic o r g a n is m s , m a y r e s p o n d t o p o l lu t i o n , t h e a rg u -

m e n t s p r e s e n t e d b e l o w s h o w t h a t t h e y a r e n o t i d e a l b i o i n d i c a t o r s p e c ie s .

As po in ted o u t by K enne dy (1997) f i sh pa rasi t e s f a i l to s a t i s fy even the f i r s t

o f the above c ri te r ia . Thus , Ha r tv igsen and Ken ned y (1993) s t a te tha t the

p r e d i c t i v e v a l u e o f t h e ir s t u d ie s h a v e f o u n d e r e d o n t h e e r ra t ic a n d u n p r e -

d ic tab le occur rence o f man y f i sh he lmin th spec ies . Th i s s i tua t ion l ed K ennedy

(1978a , b , 1981 , 1985) and Ken ned y e t a l (1986) to a rgue tha t he lm in th c om -

muni t i e s in f r eshwate r f i sh a re fundamen ta l ly s tochas t i c a s semblages , the i r

c o m p o s i t i o n b e i n g d e p e n d e n t o n c h a n c e i n t ro d u c t i o n s o f p a r a s it e s i n t o

loca l i t i e s and on chance co lon i sa t ion and ex t inc t ion even t s . These a rgumen ts

a r e s u p p o r t ed b y E s c h

e t a l

( 1 9 8 6 ) a n d D o b s o n ( 1 9 9 0) .

W hi le i t i s to be ex pec ted tha t the f r ee - liv ing s tages o f the pa ras it e s w ou ld

be h igh ly suscep t ib le to po l lu tan t s th i s does no t me an , un fo r tuna te ly , tha t they

are idea l cand ida tes fo r b iom oni to r ing fo r the fo l low ing r easons . F i r s tly , pa r -

a s i te s a r e r e n o w n e d f o r t h ei r e x c e p t i o n a l l y h i g h r a te s o f re p r o d u c t i o n . A s




r e p r o d u c t io n m a y b e s p r e a d o v e r a lo n g p e r i o d i t m a y w e l l n o t b e s e r io u s l y

a f f ec ted by po l lu tion , a s th i s i s o f t en ep i sod ic in na tu re . Fu r the rm ore , onc e the

endop aras i t e s have en te red the i r in te rmed ia te o r de f in i t ive hos t s they r ece ive a

m e a s u r e o f p r o t e c t i o n f r o m t h e d i r e c t e f f e c t s o f e n v i r o n m e n t a l p o l l u ti o n .

A l t h o u g h f i s h e c t o p a r a s i t e s w i l l p o t e n t i a l l y b e i n g r e a t e r d a n g e r t h a n

e n d o p a r a s i t e s f r o m e x p o s u r e t o p o l l u t a n t s m u c u s s e c r e t e d b y t h e h o s t w i l l

p rov ide them wi th so m e p ro tec t ion . In add i t ion the h igh l eve l o f mo b i l i ty o f the

h o s t f is h e n a b l e s t h e m t o m o v e a w a y f r o m h e a v i l y p o l lu t e d a r e as . A s a r e s u l t

i t i s pos s ib le to env i s age metapopu la t ions a t d i f f e ren t s t ages o f deve lopmen t

su rv iv ing in spa t i a l ly d i s con t inuous hab i t a t s desp i t e po l lu t ion . In the case o f

d igene t i c t r ematodes the quan t i fi ca t ion o f the suprapopu la t ion , wh ich inc ludes

a l l deve lopmen ta l phases o f a pa ras i t e a t a pa r t i cu la r t ime and p lace , i s an

ex t r em ely d i f f i cu l t t a sk , pa r t icu la r ly in cases wh ere a l l the de f in i t ive and in te r -

m ed ia te ho s t s have ye t to be iden t i fi ed . The l i fe h i s to ry s t r a teg ies adop ted by

helm inth paras i tes help to expla in thei r evo lu t ionary succ ess . Un for tunate ly , as

th is t ends to m akes them les s re spons ive to po l lu t ion than f r ee- l iv ing o rgan i sms

the i r u se as b io ind ica to r s i s fu r the r con t r a ind ica ted .

Un l ike f r ee - l iv ing o rgan i sm s r e la t ive ly l it tl e i s kno wn abo u t the eco -p hys i -

o log ica l, b iochem ica l and behav ioura l r e sponses sho wn b y the va r ious s t age in

the l i f e cyc le o f the pa ras it e s to the po l lu tan t s . Th i s i s ma in ly d ue to the shor t

l i f e span o f the f r ee - liv ing s t ages and the d i f f i cu l ty o f cu l tu r ing the pa ras i t ic

s tages . As a resul t it is d i f f icu l t to predic t how the var ious ph eno type s in the l i fe

cyc le m igh t r e spo nd to pa r t icu la r po l lu tan ts .

The use o f f i sh pa ras i te s a s b io ind ica to r s o f po l lu tion a l so f a i l s to s a t i sfy the

four th c r it e rion , na m ely tha t the b io ind ica to r s s e lec ted shou ld be r ead i ly acces -

s ib le , widely d is t r ibuted and ident i f iab le . Unl ike f ree- l iv ing inver tebra tes , f i sh

hos t s such as t rou t and h ence the i r pa rasi t e s t end to be r es tr i c t ed to the upp er

reaches o f rive r s and a re r ep laced by c oar se f i sh in the low er reaches . As f i sh

paras i t e s gene ra l ly exh ib i t overd i spe r sed d i s tr ibu t iona l p a t t e rns i t i s neces sa ry

to s am ple a l a rge nu m ber o f f i sh in o rde r to ob ta in r e l i ab le da ta. Iden t i fi ca t ion

may a l so be d i f f i cu l t a s s ib l ing spec ies such as C fa r i o n i s a n d C m e t o e c u s

may coex i s t a s adu l t s . Larva l s t ages genera l ly p resen t even g rea te r p rob lems

with ident i f ica t ion .

Unfo r tuna te ly , the s amp l ing o f fi sh , such as t rou t , in o rde r to ob ta in pa ra -

s i to log ica l da ta to mon i to r po l lu t ion i s unaccep tab le a s l ike o the r s a lmon id

spec ies they a re under th rea t o f ex t inc t ion . F u r the rm ore the ga the r ing o f such

d a t a w o u l d b e v e r y t i m e c o n s u m i n g a n d n o t c o s t e f f e c t i v e w i t h r e s p e c t t o

resource ava i lab i li ty . I t m us t be co nc lud ed the re fo re tha t a s none o f the abo ve

cr i te r i a a r e m e t the pos s ib i l i ty o f u s ing f i sh pa ras it e s fo r b iom oni to r ing po l lu -

t ion is hard to jus t i fy .

I t i s no t su rp ri s ing the re fo re tha t o the r b io t i c ind ices , such as the Saprob ien

index M ason 1996) , the B M W P ind ices M ason , 1996) and those based on the

River Inverteb ra te P red ic t ion and C las s if i ca tion Sys te m RIV PAC S) W r igh t e t



E CO LOG Y OF F IS H P A RA S ITE S 7

po ten t ia l ly tox ic subs tances in the wa te r co lumn and on the use o f b io t i c ind ices

b a s e d o n B M W P , A S P T a n d R I V P A C S s c o r e s . A s h e a v y m e t a l s a n d o r g a n i c

toxicants tend to accu m ulate in sediments (Thom as , 1997) thei r imp or tance m ay

b e s e r i o u s l y u n d e r e s t i m a t e d w h e n o n l y t h e w a t e r c o l u m n i s m o n i t o r e d . T h e

b io t i c ind ices cu r ren t ly use d by the E nv i ronm en t Ag ency a re a l so inappropr iate

fo r mon i to r ing the e f f ec t s o f m e ta l po l lu tion as they w ere des igned to iden t i fy

cases o f o rgan ic po l lu t ion . Consequ en t ly , they g ive a g rea t dea l o f w e igh t to

oxyg en-depe nden t , rheoph i lous , ri f fl e - inhab i t ing o rgan i sm s wh ereas s ed im en t

dwe l le r s, wh ich a re l ike ly to encoun te r h igher concen t ra t ions o f hea vy m eta l s,

a re v i r tua l ly ignored . I t i s sugges ted the re fo re tha t the Env i ronmen t Agency

shou ld rou t ine ly m on i to r s ed imen ts fo r heav y meta l s and o rgan ic tox ican t s and

a l s o d e v e l o p b i o m o n i t o r i n g m e t h o d s t h a t g i v e g r e a t e r w e i g h t t o s e d i m e n t -

dwel l ing o rgan i sms known to be suscep t ib le to heavy meta l po l lu t ion . These

inc lude o l igochae te worms , ch i ronomid l a rvae , amph ipods , b iva lve mol luscs

and am m oec e te la rvae (Gerhard t 1993 ; Ph ipp s e t a l . , 1995).

9 5 F is h P a r a s i te s a s S o u r c e s o f I n f o r m a t i o n o n P o l l u t i o n

As s ta ted abov e i t i s d i ff i cu l t to use pa ras i t e s a s b io ind ica to r s o f po l lu t ion

bec aus e o f the co m plex i ty and va r iab i li ty o f the i r in te r r e la t ionsh ips w i th the

env i ronmen t . De sp i te these l imi ta tions va r ious pa ras ito log i s t s have sug ges ted

t h a t t h e y m a y h a v e s o m e i n fo r m a t i o n a l v a l u e a s b i o i n d ic a t o r s o f t h e f o ll o w i n g

fo rm s o f po l lu t ion .

H e a v y m e t a l p o l l u t i o n . A s h e a v y m e t a ls o f t e n b i o a c c u m u l a t e a t h i g h er c o n -

cen t r a t ions in the pa ras i t e s than in the i r f i sh hos t s s evera l au tho r s (R iggs an d

Esch , 1987 ; Sures e t a l . , 1994 ; Chubb , 1997 ; Landsberg e t a l . , 1998) have

adv oca ted the i r u se as s ens i tive b iomarker s .

A c i d i f i c a t i o n . C o n e e t a l . 1 9 9 3 ) foun d that the pa ras i t e comm uni t i e s in the

Amer ican ee l ,

A n g u i l l a r o s t r a t a ,

inhab i ting ac id ic w a te r bod ies w i th pH va lues

o f 4 . 5 - 5 . 0 w e r e c h a r a c t e r is e d b y t h e a b s e n c e o f d ig e n e t ic t r e m a t o d e s , l o w e r

spec ies r i chnes s and f ewer mul t ip le in fec t ions compared w i th those in l e s s

a c id i c , l im e d w a t e rs . S u b s e q u e n t s t u d ie s b y M a r c o g l i e s e a n d C o n e ( 1 9 9 6 ) o n

t h e h e l m i n th p a r a si te s o f e e ls s h o w t h at c o m p o n e n t c o m m u n i t y d i ve r si ty , a s

m e a s u r e d b y s p e c ie s ri c hn e s s, S h a n n o n - W i e n e r i n d e x a n d H i l l s n u m b e r ,

dec reased w hen the pH wa s le s s than 5 .4. These au thor s a rgued the re fo re tha t

the pa ras it i c he lmin th f auna r e f l ec t s d i f fe rences in the food w ebs in these con-

t r a s t i n g h a b i t a t s a n d c o n c l u d e t h a t p a r a s i t i c a s s e m b l a g e s m a y b e g o o d

ind ica to r s o f env i ronmen ta l s t re s s . Th ese f ind ings a re in accord w i th those in

t h e p r e s e n t i n v e s t ig a t i o n a s t h e p a r as i ti c c o m m u n i t y o f th e t r o u t f r o m t h e

Pysg o twr , the m os t ac id ic r iver , had the low es t spec ies d ive r s ity ind ices .

E u t r o p h i c a t i o n .

In the in it ia l s t ages an inc rease in eu t roph ica t ion o f l en t ic

w a t e r s f a v o u r s t h e g r o w t h o f p h y t o p l a n k t o n p o p u l a t io n s a n d h e n c e t h o s e o f



1 1 8 J D T H O M A S

organ i sms a long the foo d cha in w h ich ben ef i t f rom th i s inc lud ing zoop lank ton ,

p lank t ivo rous f i sh and p i s c ivo rous b i rds . I t i s no t su rp r i s ing the re fo re tha t

K e n n e d y

et a l .

1 9 9 4 ), K e n n e d y 1 9 9 5 ) a n d Y e o m a n s

et aL

1996) found tha t

inc reased l eve l s o f eu t roph ica t ion we re pos i t ive ly co r re la ted w i th popu la t ion

increases in f ish paras i tes such as

L i g u l a

and t r i chod in ids , r e spec t ive ly . One

m i g h t a l s o p r e d i c t t h at c o m m u n i t i e s o f fi s h p a r a s it e s w o u l d b e c o m e m o r e

species r ich and d iverse wi th eutrophicat ion increas ing u p to a cer ta in level and

then dec l in ing as the wa te r bod ies beco m e hyper t roph ied .

Organic pol lu t ion . This m ay take the fo rm o f inc reased load ing w i th was te

organic mat ter of huma n o r animal or ig in or organic pes t ic ides . The form er harm

the environment b y oxy ge n depletion w here as the lat ter act as toxicants . Ye om ans

et al.

1996) and Landsberg

et a l .

1998) d iscuss the po ss ib i l ity of us ing t r icho-

din ids as indicators of enhanced organic loading . However , as poin ted out by

M a c K e n z i e et a l . 1995 ) m an y o f the s tudies associating cha nge s in f ish parasites

with the ef fects of specif ic pollu tants h ave be en specula t ive and inconclus ive .

M a n y a u t h o rs , i n cl u d in g M a c K e n z i e

et a l .

1995) , have sugge s ted tha t fi sh

paras i te s w ou ld be idea l b io ind ica to r s o f spec i fi c po llu tan ts , a s they w ou ld be

e x p e c t e d t o b e h i g h l y s e n s i t i v e . H o w e v e r , i t h a s a l s o b e e n s u g g e s t e d

Kup erman , 1993) tha t the m onog ene t ic f luke , D i p l o z o o n p a ra d o x u m and the

c e s t o d e C a r y o p h y l l a e u s l a t i c e p s a r e s u i ta b l e b i o i n d i c a t o r s o f p o l l u t i o n b y

chem ica l p rodu c t s o f the coa l ta r indus t ry in Ru ss ia becau se o f the i r in sens i -

t iv i ty to the tox ican t s . As a r e su l t the pa rasi t e s a re foun d to be m ore abundan t

in the po l lu ted zones . How ever , th is au thor do es no t appear to have con s ide red

the pos s ib i l ity tha t th i s pheno m enon migh t b e a t t r ibu tab le to the f i sh im m uni ty

be ing lo we red by the tox ican t s . The re a re man y conf l i c t ing r epor t s regard ing

the ef fects o f pol lu t ion o n d isease prev alence and mor ta li ty . So m e o f these indi-

ca te tha t po l lu t ion r esu l t s in an inc rease in d i s ease p reva lence and mor ta l i ty

w h e r e a s o t h e r s c o m e to th e o p p o s i t e c o n c l u s i o n W i ll ia m s a n d J o n e s , 1 9 9 4 ;

M a c K e n z i e et a l . 1995 ; Landsb erg et a l . 1998) . I t i s not therefore p oss ib le to

genera l i s e and fu r the r work on spec i f i c cases i s needed be fo re any f i rm con-

c l u s io n s c a n b e d r a w n . T h e d i s s e m i n a t i o n o f p a t h o g e n i c p a r a s it e s b y t h e

s t o c k in g a n d d u m p i n g o f f is h m a y a l s o b e r e g a r d e d a s a n o t h e r f o r m o f p o ll u -

t ion Ke nned y, 1975; W il l iams and Jon es , 1994) .

10 IN T E R A C T I O N S B E T W E E N S P E C IE S O F H E L M I N T H P A R A S I T E S

I N F I S H

1 0 1 I n t r o d u c t io n

T h e q u e s t i o n o f w h e t h e r i n t e rs p e c i es c o m p e t i ti o n m a y b e i n v o l v e d i n re g u la t -

ing popu la t ion dens i t ie s F igu re 1 ) and in f luenc ing the cour se o f evo lu t ion




r e m a i n s a c o n t r o v e rs i a l s u b j e c t i n e c o l o g y i n g e n e r al a n d i n h e l m i n t h o l o g y i n

p a r t i c u l a r ( R o h d e , 1 9 9 8 ; V i d a l - M a r t i n e z a n d K e n n e d y , 2 0 0 0 ) . I n o r d e r t o

reso lve th i s ques t ion i t i s neces sa ry to de f ine the t e rm c lea r ly . In te r spec ies

c o m p e t i ti o n i s b e s t d e f i n e d a s a n y i n te r a c ti o n b e t w e e n t w o o r m o r e p o p u l a -

t ions , wh ich adver se ly a f f ec t s the i r g rowth and su rv iva l . Th i s de f in i t ion i s

based on the e f f ec t s caused by the in te rac t ions and does no t inco rpora te the

causa t ive mechan i sms in i t i a l ly a s th i s can l ead to confus ion . These e f f ec t s

m a y b e c a u s e d e i t h e r b y a f r e e - fo r - a l l , e x p l o i t at iv e ( s c r a m b l e ) c o m p e t i ti o n

fo r foo d o r a s a r e su l t o f con tes t ing space , w i th i ts a s soc ia ted r esources . The

var ious s t r a teg ies use d fo r con tes t ing space f a l l under the head ing o f in te r f e r-

ence compet i t ion and inc lude th rea t , d i r ec t phys ica l aggres s ion , t e r r i to r i a l

mark ing w i th s cen t s and the r e lease o f an tagon i s ti c , a l l e lopa th ic subs tances o r

an t ib io t i c s tha t m ay r epe l o r ha rm o the r spec ies . Pa ras it e s m ay a l so man ipu la te

t h e h o s t to h a r m o t h e r m e m b e r s o f t h e p a r as i te c o m m u n i t y i n d i r e ct ly b y s t im -

u la t ing c ros s - im m uni ty to wh ich the y r emain pa r t ia l ly o r com ple te ly r esi s tan t .

A t the in t r aspec ies l eve l th is phen om enon i s know n as concom i tan t imm uni ty .

Ev iden ce tha t in te r spec ies com pet i t ion is occur r ing in na tu re ma y be d i r ec t

o r c i r cums tan t i a l an d can b e c las s i f ied under the fo l low ing head ings :

a

b.

D i rec t ev idence . Th i s i s base d on the obse rva t ion tha t the b io log ica l f itnes s

o f bo th spec ies i s adver se ly a f f ec ted wh en they a re coex i s ting . U sua l ly th is

c r i te r ion can on ly b e s a t i s f i ed by exper imen ta t ion .

C i rcums tan t i a l ev idence .

1 . Nic he d ivers if ica t ion including resourc e part it ioning in space or t ime,

habitat segreg ation or interactive s ite selection w he n the spec ies coexist .

2 . Cha rac te r d i sp lace m en t o r m orpho log ica l d i f f e rences pa r t i cu la rly in

t h o s e a n a t o m i c a l f e a t u r e s c o n c e r n e d w i t h f e e d i n g .

3 . Com pet i t ive exclus ion of a species by another in the same feeding guild.

4 . E x t e n s i o n o f a s p e c i e s r a n g e f o l lo w i n g t h e e x p a n s i o n o f i ts fe e d i n g

niche.

T h e e v i d e n c e o f c o m p e t i t i o n a m o n g h e l m i n t h p a r a s it e s o f f is h is r e v i e w e d

be lo w u s ing these c r it e ri a .

10 2 Ev id en ce o f In te r sp ec ies C o m p et i t i o n

10.2.1. Direct evidence

I n a p i o n e e ri n g s t u d y H o l m e s ( 1 9 6 1 , 1 9 6 2 ) d e m o n s t r a te d e x p e r i m e n t a l l y th a t

i n t e r s p e c i e s c o m p e t i t i o n o c c u r r e d b e t w e e n Hymenolepis d iminuta a n d

Moniliformis moniliformis (= dubius in ra ts . S ince then s imi lar s tudies have

c o n f i r m e d t h a t i n te r s p e c ie s c o m p e t i ti o n a l s o o c c u r s b e t w e e n o t h e r h e l m i n t h



120 J D THOMAS

spec ies under exper imen ta l cond i t ions M apes and Co op , 1971; S i lve r et al .

1980; Hol land, 1984; Bates and Kennedy, 1990) . The la t ter au thors s tudied

i n t e r a c t i o n s b e t w e e n t h e a c a n t h o c e p h a l a n s

P om phor hynchus l aev i s

a n d


in exper imen ta l ly in fec ted r a inbow t rou t and found

t h at t h e e s t a b li s h m e n t o f b o t h s p e c i e s w a s u n a f f e c t e d b y t h e p r e s e n c e o f th e

o the r spec ies . However , i t was found tha t a f t e r e s tab l i shmen t had occur red

A. angui l lae

w a s n u m e r i c a l ly d i s a d v a n t a g e d b y t h e p r e s e n c e o f P .

laevis

w h e r e a s t h e c o n v e r s e w a s n o t t h e c a s e . T h i s t y p e o f e x t r em e , a s y m m e t r ic a l

in te rac t ion shou ld the re fo re be c las sed as ammensa l i sm ra the r than compet i -

t ion . Ac cord ing to Ba tes and Kenne dy 1990) the mos t t enab le exp lana t ion fo r

th i s phenomenon i s tha t i t i s caused by an exc lus ion zone a round ind iv idua l s

o f

P. laevis

p o s s i b l y m e d i a t e d b y t h e h o s t, i n w h i c h t h e s u r v i va l o f

A. ang ui l -

lae

i s r e d u c e d . T h e y t h e r e f o r e s u g g e s t e d t h a t i n r i v e r s w h e r e

P. laevis

domina tes f i sh in f r acommuni t i e s , in te r spec ies compet i t ion , o r ammensa l i sm,

m i g h t m a k e i t i m p o s s i b l e f o r A. angui l lae to become es tab l i shed . Th is sug -

ges t ion can be ex tr apo la ted to o the r acan thocepha la spec ies a s Ken nedy 1985 ,

1 9 9 2) s h o w e d th a t e x a m p l e s o f c o - o c c u r r e n c e o f t w o o r m o r e a c a n t h o c e p h a l a

spec ies w i th in f r eshw ate r loca l it i e s in Br i t a in we re f a r f ewer than e xpec ted .

10.2.2. Circumstant ial evidence indicat ing interspecies com pet i t ion

In o rde r to eva lua te th i s ev idence i t is nece s sa ry to cons ide r the con cep t o f the

niche. Th e term niche is bes t consid ered as a multidimensional space , determ ined

by a l a rge num ber o f phys ica l and b io t i c va riab les, w i th in wh ich spec ies ex is t

Hutchinson , 1957) . Each d im ens ion represents a fac tor that inf luences the b io-

log ica l f i tness o f the spec ies . In th is con tex t i t i s bes t no t to m ake a d i s t inc t ion

b e t w e e n p a r a m e t e r s w h i c h b e n e f i t t h e o r g a n i s m d i r e c t l y , s u c h a s f o o d

r e s o u r c e s , a n d t h o s e w h i c h m a y h a r m i t s u c h a s a l l e l o p a t h i c c o m p o u n d s o r

p reda to r s . However , the pa ramete r s tha t a r e g iven mos t a t t en t ion in pa ras i t e

eco log y a re the spec ies , age and sex o f the hos t , mic rohab i ta t s , t ime an d nu t r i-

e n t r e q u i r e m e n t s . M i c r o h a b i t a t s e l e c t i o n m a y b e b a s e d o n l o n g - t e r m ,

gene t i ca l ly f ixed behav ioura l pa tt e rns hab i ta t s eg rega t ion ) o r on shor t - te rm,

in teract ive s i te se lec t ion induc ed b y the presen ce o f a potent ia l com pet i tor . Th e

c i r cums tan ti a l ev idence ind ica ting tha t in te rspec ies com pet i t ion m ay b e occur -

r ing amo ng f i sh pa ras i t e comm uni t i e s i s d i s cus se d be low.

10.2.3. Habitat segregation

Althou gh 12 species of helm inth paras i tes occu rred in the t rout only s ix , nam ely

D. sagittata C. far ion is C. me toec us P. simile N. rutili an d C. truttae w e r e

commonly encoun te red and the p resen t ana lys i s i s r e s t r i c ted to them. Two o f




these, D. sagi t ta ta and P s imi le wh ich occ ur on the g i l ls and in the ur inary b lad-

der , r e spec tive ly , a r e com ple te ly i so la ted f rom the gu t - inhab it ing spec ies and

cann ot therefore in teract wi th them directly . I t i s a lso unl ikely that cross - im m u-

n i ty w i l l in f luence the su rv iva l o f these spa t i a l ly s eg rega ted spec ies .

C o m p e t i t i v e i n t e r a c t i o n s a r e h o w e v e r p o s s i b l e b e t w e e n t h e f o u r g u t -

i n h a b i t i n g s p e c i e s . A l t h o u g h t h e s e a r e r e s t r i c t e d t o t h e r e g i o n b e h i n d t h e

s tom ach the re i s ev ide nce tha t they have hab i t a t p re fe rences w h ich a re p roba-

b ly based on gene t i ca l ly fixed behav ioura l pa t te rns F igu re 26 ). Thus , bo th C .

m e t o e c u s a n d C. t ru t ta o c c u r r e d p r e d o m i n a n t l y i n th e p y l o r i c c a e c a re g i o n o f

the in tes t ine , whi le

C . fa r i o n i s

a n d

N. ru t i l i

f avoure d the pos t -py lo r i c r eg ion .

As the ava i l ab le su r f ace a rea o f the f i sh in tes t ines i s r e l a t ive ly sm al l the m ean

dens i t i e s o f he lm in th p a ras i t e s pe r square me t re a r e r e la t ive ly h igh . These

we re es t ima ted to be 10 000 , 10 000 , 14 000 a nd 16 000 fo r 1 -, 2 - , 3 - and 4 -

y e a r - o l d tr o u t, r e s p e c ti v e ly . T h e s e v a l u e s c o m p a r e w i t h m a x i m u m d e n s it ie s o f

54 000 , 46 000 , 77 000 and 61 00 0 fo r 1 -, 2 - , 3 - and 4 -yea r -o ld trou t , r e spec -

t ively . I t i s notewor thy that the paras i te dens i t ies per square metre vary l i t t le

w i th age desp i t e the f ac t tha t the mean pa ras i t e abund ance va lues 19 .6 , 24 .4 ,

48 .3 and 56 .6 for 1- , 2-, 3- and 4-yea r -o ld f ish , respect ive ly) increase m arke dly

with the age of the f ish . This ob serv at ion is a t t r ibutable to the fac t tha t the sur -

f ace a rea o f the gu t inc reases a s the f ish g rows . The f ac t tha t dens i ty chang es

a re min imal w i th age sug ges t s tha t space m ay be a l im i t ing f ac to r. Th ese h igh

dens i t i e s , wh ich a re ind ica t ive o f a r e source - r i ch hab i t a t where p re -d iges ted

f o o d i s c o n t i n u o u s l y a v a i l a b l e , e x c e e d t h o s e o f f r e e - li v i n g , b e n t h i c

w

I -

it

0

1 0 0 . 0 0

9 0 . 0 0

8 0 . 0 0

7 0 . 0 0

6 0 . 0 0

5 0 , 0 0

4 0 . 0 0

3 0 . 0 0

2 0 . 0 0

1 0 . 0 0

0 . 0 0

N R N R N E N E C M CM

* P C t p P C P C P P C P C P P C

*PC - presumablypylo ric tp pc - post-pylodc

C F

P C

C F

P P C

F i g u r e 2 6 The distribution patterns in percentage s of the m ajor parasites ke y as in

Figure 19) in the pyloric PC ) and post-pyloric PPC ) region of the trout gut.



22

J D T H O M A S

inver teb ra tes, such as those in the R iver W ye 50 0-2 2 000 p e r m 2 accord ing to

Edwards and Brooker , 1982) .

A c c o r d i n g t o R e a d 1 9 5 6 ) a n d S m y t h 1 9 6 2 ) t h e p y l o r i c c a e c a r e g i o n

immedia te ly pos te r io r to the py lo r i c sph inc te r i s the mos t f avourab le mic ro -

habi ta t for the gut paras i tes of sa lmonid f ish . I t i s re la t ively ca lm and as the

pancreas opens in to i t i t i s r i ch in d iges t ive en zym es and h igh ly nu t r i tive food .

In con t r as t the con ten t s o f the pos t -py lo r i c cae ca r eg ion a re sub jec t to g rea te r

movemen t and have a lower nu t r i en t con ten t . These changes a long the l eng th

of the in tes t ine r esemble those desc r ibed fo r o the r t e l eos t f i sh w i th py lo r i c

caec ae such as the g reen sunf i sh

Lepomis cyanellus)

Richardson and N icko l ,

1999) . These au thor s found tha t p ro te in , f r ee amino ac id , l ip id and ca rbohy-

d ra te concen t r a t ions , pH and aminopep t idase ac t iv i ty were a l l h igher in the

caec ae than in the in tes tina l r eg ion and sugges t tha t th i s was the r eason fo r the

c a e c a e o f L. cyanellus b e i n g t h e p r e f e r r e d h a b i t a t o f t h e a c a n t h o c e p h a l a n

Leptorhynchoides thecatus.

A c c o r d i n g to K e n n e d y 1 9 9 6 ) th e p y lo r i c c a e c a is

a l so the p re fe r r ed s i t e fo r Eubothrium crassum in the b rown t rou t and r ap id

grow th o f th i s pa ras i te on ly occur s in th i s r eg ion o f the gu t .

In the p resen t inves t iga t ion i t is m a in ly

C. metoecus

a n d t h e n e m a t o d e C .

truttae w h i c h o c c u p y w h a t a p p e a r s t o b e t h e o p t i m a l r e g i o n i n t h e g u t f o r p a r -

as i te s , nam ely the py lo r i c caec a r eg ion F igure 26 ) . A s these spec ies a r e no t

conge ner ic the ex ten t o f n iche ov er lap w i l l be l e s s than fo r cong ener ic spec ies

such as

C. metoecus

a n d

C. farionis.

Thus ,

C. rnetoecus

and

C. truttae

o c c u p y

d i f f e ren t mic rohab i t a t s w i th the fo rmer spec ies mov ing f r ee ly in the py lo r i c

lume n w hereas the l a t te r is genera l ly a t t ached to the m uco sa by i t s pe r ibucca l

t ee th . I t is the re fo re p os s ib le tha t bo th C. metoecus and C. truttae wil l have a

com pet i tive advan tage over N. rutili and C. farionis, as the l a tt e r tend to o ccu py

the l e s s f avourab le pos t -py lo r i c r eg ion o f the gu t . To wha t ex ten t these d i s tr i -

b u t i o n a l p a t t e r n s a r e d u e t o i n n a t e b e h a v i o u r a l p a t t e r n s o r t o s h o r t - t e r m

behav ioura l r e sponses due to the p resenc e o f po ten t i a l comp e t i to r s r emains to

b e e lu c i d a t e d ex p e r im e n t a l ly . H o w e v e r , C h a p p e l l 1 9 6 9 ) ha s d e m o n s t r a t e d

act ive s i te se lec t ion in the c ases

of Proteocephalusfilicollis and N. rutili

in the

s t ick leback. It appears that the forme r species has a com pet i t ive advantage o ver

the l a t t e r a s wh en the tw o spec ies coe x i s t the f avoured an te r io r loca t ion in the

g u t is o c c u p i e d b y P fillicolis w h e r e a s N. rutili a t t aches m ore pos te r io r ly . In

c o n t r a s t , i n s i n g l e - s p e c i e s i n f e c t i o n s t h e d i s t r i b u t i o n b e c o m e s m u c h m o r e

wid esp rea d in the gu t.

10.2.4. Associations between different pairs of helminth species in

infracommunities

This a spec t o f pa ras i te com m uni ty s t ruc tu re has r ece ived a g rea t dea l o f at t en -

t ion A nd erso n and Valtonen, 1990; Lo tz and Font, 1991, 1994; Pou lin, 2001 a).




)C2 t e s ts w e r e c a r r i e d o u t o n t h e i n f r a p o p u l a t i o n s o f t h e t r o u t c o l l e c t e d i n t h e

p r e s e n t i n v e s t i g a t i o n t o a s c e r t a i n w h e t h e r t h e r e w e r e s t a t i s t i c a l l y s i g n i f i c a n t

t e n d e n c i e s f o r p a r a s i t e s p e c i e s t o c o e x i s t o r n o t . T h e r e s u l ts T a b l e 31 ) , s h o w

t h a t i n n e a r l y a l l c a s e s t h e a s s o c i a t i o n s a r e s i g n i f ic a n t l y p o s i t iv e P < 0 . 0 5 ).

T h e o n l y e x c e p t i o n s t o th i s ru l e a r e p r o v i d e d b y N . r u t il i/ C m e t o e c u s and N.

r u t i l i / C f a r i o n i s

a s i n t h e s e c a s e s t h e a s s o c i a t i o n s a r e n e g a t i v e a l t h o u g h t h e X2

v a l u e i s o n l y s t a ti s ti c a l ly s i g n i f i c a n t P < 0 . 0 5 ) in th e f o r m e r c as e . R o h d e

1 9 9 1 ) a l so f o u n d w h e n i n v e s t ig a t i n g m o n o g e n e t i c p a r a s it e s i n m a r i n e f i s h t h a t

3 5 o f t h e s t a t i s t i c a l l y s i g n i f i c a n t a s s o c i a t i o n s f o u n d w e r e p o s i t i v e c o m p a r e d

w i t h t w o n e g a t i v e s . H o w e v e r , c a r e i s n e c e s s a r y i n e v a l u a t i n g s u c h d a t a a s a

h i g h p r o p o r t i o n o f r a r e p a r a s it e s p e c i e s , w i t h a l o w p r e v a l e n c e i n t h e c o m p o -

n e n t c o m m u n i t y , c a n p r o d u c e a n e x c e s s o f s p u r io u s n e g a t i v e a s s o c ia t io n s ,

w h e r e a s a l a rg e p r o p o r ti o n o f c o m m o n s p e c ie s c a n l e a d t o a n e x c e s s o f p o si -

t iv e a s s o c i a t i o n s L o t z a n d F o n t , 1 9 9 4 ).

W h e n t h e t r o u t w e r e s e g r e g a t e d i n t o a g e g r o u p s t h e

N . ru t il i/ C f a r i o n i s

a s s o c i a t i o n s w e r e f o u n d t o b e s i g n i f i c a n t l y n e g a t i v e P < 0 . 0 5 ) in t h e c a s e o f

4 - y e a r - o l d t ro u t. T h e a s s o c i a ti o n s b e t w e e n C . m e t o e c u s / C t r u tt a e w e r e a l so

f o u n d t o b e s i g n i f i c a n t l y n e g a t i v e P < 0 . 0 5 ) i n th e c a s e o f 3 - y e a r - o l d tr o u t

T h o m a s , 1 9 6 4 a ) .

R e g r e s s i o n a n a l y s e s , u s i n g t r a n s f o r m e d n u m b e r s o f t r o u t p a r a s i t e s , a l s o

i n d i c a te t h a t w i t h t h e e x c e p t i o n o f

N . r u ti li /C f a r i o n i s

a n d

N . r u t il i/ C m e t o e -

c u s t h e p a i r s o f p a r a s i te s p e c i e s t e s t e d e x h i b i t s t a t i s t ic a l l y s i g n i f ic a n t p o s i ti v e

a s s o c i a t i o n s T a b l e 3 2) . N e i t h e r o f t h e a b o v e n e g a t i v e a s s o c i a t io n s w a s s ta t is -

t i ca l l y s i gn i f i c an t P > 0 . 05 ) .

R e s u l t s o b t a i n e d f r o m ~ 2 t e st s, u s i n g 2 x 2 c o n t i n g e n c y ta b l e s , o n i n f r a p o p -

u l a t io n s o f p a r a si te s i n s a l m o n p a r r o f a l l a g e s r e s e m b l e t h o s e f o r tr o u t a s w i t h

t h e e x c e p t i o n o f

D . s a g i t ta t a / C f a r i o n i s

a l l t he as soc i a t ions were pos i t ive Tab l e

3 3 ) . H o w e v e r , o n l y t h e p o s i t i v e a s s o c i a t i o n s i n v o l v i n g t h e n e m a t o d e s a n d

t h e o t h e r p a r a s it e s p e c i e s a n d

N . r u t i l i / C f a r i o n i s a r e

s t a t i s ti ca l l y s i gn i f i can t

Table 31 The X results and P values of 2 x 2 contingency tests for the parasites of

the brow n trout

D. sagittata C. farionis C. me toecus P. simile N. rutili

Parasites )~2 p ~2 p ~2 p ~2 p Z2 p

D. sagittata

C. farionis

+4.89 0 .027

C. metoec us

+17.65 0.000 +34.33 0.059

P. s i m i l e

+1 2.2 0 0 .000 +3.35 0 .067 +31.28 0 .000

N. rutili

+23.47 0.000 -0.913 0.339 -5.451 0.020

Nematodes +40.18 0.00 0 +5 .76 0.0 16 +0.400 0.529

+47.8 0.000-

+47.63 0 .000 +263.39 0.000



1 2 4 J D T H O M A S

a~

: =

. . ~ . =




P < 0 . 0 5 ). R e g r e s s i o n a n a l y s e s u s in g t r a n s f o r m e d n u m b e r s o f s a lm o n p a r r

p a r a s i t e s a l s o s h o w s t a t i s t i c a ll y s i g n i f i c a n t p o s i t i v e r e l a t i o n s h i p s b e t w e e n C .

t r u t t a e l D s a g i t t a t a C . t r u t t a e l C f a r i o n i s a n d C . t r u t t a e / N r u t il i .

I n a d d i t i o n

C . f a r i o n i s / C m e t o e c u s a re s i g n i f ic a n t l y p o s i t i v e l y a s s o c i a t e d P = 0 . 0 0 8 )

w h e r e a s C . m e t o e c u s / C t r u t ta e a r e s i g n i f i c a n t l y n e g a t i v e l y a s s o c i a t e d P <

0 . 0 2 4 ) T a b l e 3 4 ) .

R e g r e s s i o n a n a l y s is w a s a l s o a p p l i e d t o a n a l y s e t h e n a t u r e o f t h e a s s o c i a -

t io n s b e t w e e n C . m e t o e c u s C . f a r i o n i s C . t r u t ta e a n d N . r u t i l i i n t h e p y l o r i c

a n d p o s t - p y l o r i c r e g io n s o f t h e t r o u t i n te s ti n e s . T h e t r o u t w e r e s e g r e g a t e d i n t o

11 b l o c k s o n th e b a s is o f a g e a n d s e a s o n T h o m a s , 1 9 6 4 b ) . T h e r e s u l ts f r o m g 2

t e st s T a b l e 3 5 ) s h o w t h e a s s o c i a ti o n s b e t w e e n C . m e t o e c u s / C f a r i o n i s C .

m e t o e c u s / N r u t i l i

a n d

C . m e t o e c u s / C t r u t t a e

i n t h e p y l o r i c c a e c a r e g i o n w e r e

s i g n i fi c a n t ly n e g a t i v e e x c e p t f o r o n e p o s i t iv e c a s e i n v o l v i n g N . r u t i l i a n d C .

m e t o e c u s . T h e o n l y o t h e r s i g n i f i c an t p o s i t i v e r e l a t io n s h i p w a s t h a t i n v o l v i n g N .

r u t i l i / C t r u t t a e i n t h e p y l o r i c r e g i o n . I n c o n t r a s t , a l l t h e o t h e r s t a t is t i c a ll y s i g -

n i f i ca n t a s s o c i a t i o n s i n v o l v i n g C . m e t o e c u s / N r u t il i C . f a r i o n i s / N r u t i li a n d

C . f a r i o n i s / C t r u t ta e i n t h e p o s t - p y l o r i c r e g i o n w e r e n e g a t i v e .

Table 33 Th e X results and P values of 2 × 2 contingency tests for the parasites of

the salmo n parr.

D. sag i t ta ta C. fa r ion i s C. m e toecu s N. ru ti li

Parasite ~2 Z2 Z2 p ~2 p

D. sag i t ta ta

C . f a d o n i s

4) .013 0.908

C. me t o e c u s +0.186 0.667 +3.574 0.059

N. rut i l i +0.232 0.630 +4.044 0.044 + 1. 7 85 0.181

N e m ~ o d e s + 1 1 . 3 2 9 . 0 0 1 + 6.9 74 0 .0 08 + 1 0 . 5 2 3 0.001 +5.080 0.024

Table 34

Th e regression coefficients C) and the P values, based on transformed

values, as measures of positive +) and negative -) associations between parasites of

salmon parr

D. sag i ta t ta C. fa r io n i s C. m e toec us N. ru ti li

C P C P C P C P

D. sa g i ta t ta

C . f a r i o n i s -0.022 0.703

C. me t o e c u s -0 .001 0 .9 2 1 +0 .079 0 .008

N. ru t i l i

+0 .007 0.278 +0.030 0.094 +0.050 0.160

Nematodes +0 .049 0 .0 0 1 + 0 .0 9 1 0 .029 -0 .186 0 .024

+0.487 0.000



1 2 6 J D T H O M A S

A c o n s i d e r a t i o n o f t h e l i f e h i s t o r y s t ra t e g ie s c a n h e l p t o e x p l a i n t h e l a r g e

n u m b e r o f s i g n i f i c a n t p o s i ti v e a s s o c i a t io n s b e t w e e n t h e p a r a s it e s. A s e x p l a i n e d

e a r l i e r t h e t r a n s m i s s i o n s i te s f o r a l l t h e h e l m i n t h s p e c i e s t e n d t o b e l o c a t e d i n

m i c r o h a b i t a t s w h e r e t h e c u r r e n t s a r e r e l a t i v e l y l o w a n d w h e r e t h e s e d i m e n t s

a r e d e p o s i t in g . T h e l o w c u r r e n t s p e e d i s f a v o u r a b l e f o r o n c o m i r a c i d i a l tr a n s -

m i s s i o n a n d t h e i n t e r m e d i a t e h o s t s o f t h e o t h e r h e l m i n t h p a r a s i t e s l i v e i n

d e p o s i t in g s e d i m e n t s. T h i s h e l p s to e x p l a i n w h y t h e m o n o g e n e t i c t r e m a t o d e ,

D . s a g i t t a t a t e n d s t o b e p o s i t i v e l y a s s o c i a t e d w i t h t h e o t h e r s p e c i e s .

O v e r l a p p i n g t r a n s m i s s i o n s i te s m a y a l s o e x p l a i n o t h e r c a s e s o f p o s i t iv e a s s o -

c i a t io n s b e t w e e n h e l m i n t h p a ra s i te s i n s a l m o n i d f is h i n c l u d i n g N. ru t i l i and C .

f a r i o n i s D o r o c u et a l . 1995). H ow eve r it i s imp or t an t t o bea r i n m ind t ha t pos -

i t i v e a s s o c i a t i o n s d o n o t r u l e o u t t h e p o s s i b i l i t y t h a t c o m p e t i t i o n m a y b e

o c c u r r i n g b e t w e e n t h e c o e x i s t i n g p a r a si te s .

W h e n a l l t h e t r o u t a r e t a k e n i n to a c c o u n t th e o n l y p a ra s i te s w h i c h w e r e s i g -

n i f i c a n t l y n e g a t i v e l y a s s o c i a t e d w e r e t h e m o s t a b u n d a n t p a r a s i te s , n a m e l y C .

m e t o e c u s a n d N. rut i l i . I n o t h e r c a s e s w h e n t h e e n t i re g u t is t a k e n i n t o a c c o u n t

t h e s i g n i fi c a n t n e g a t i v e a s s o c i a ti o n s i n v o l v e p a ra s i te s w h i c h t e n d t o o c c u p y t h e

s a m e r e g i o n o f th e g u t s u c h a s C. me toecu s /C t ru t t ae a n d N. ru t i l i /C f a r ion i s

i n t h e t r o u t a n d C. m e toecu s /C t ru t t ae i n t h e s a l m o n p a r r. O n t h e o t h e r h a n d

w h e n t h e p y l o r i c a n d p o s t -p y l o r ic r e g i o n s o f t h e g u t a r e c o n s i d e r e d s e p a r a te l y

s i g n if i c a n t n e g a t iv e a s s o c i a ti o n s a r e a l s o f o u n d b e t w e e n p a r a s it e s w h i c h m a y

t e n d t o c o e x i s t in t h e s a m e r e g i o n o f th e g u t o r n o t. W h e n t a k e n t o g e t h e r th e s e

r e s u l ts s t r o n g l y s u g g e s t th e e x i s t e n c e o f i n t e rs p e c i e s c o m p e t i t i o n b e t w e e n t h e

h e l m i n t h p a r a s i te s i n t h e g u t o f s a l m o n i d f i sh .

O t h e r n e g a t iv e a s s o c i a ti o n s i n v o l v i n g h e l m i n t h p a r a s it e s w h i c h h a v e b e e n

r e p o r t e d i n c l u d e t a p e w o r m s a n d a c a n t h o c e p h a l i d s i n t h e g u t o f C o r e g o n u s

a lbu la t he m o n o g e n e a n O c t o b o t h r i u m m e r l a n g i a n d t h e c o p e p o d C l a v e l l a

Table 35 A summ ary of the results of regression analyses carried out on the num bers

of parasites log 1 + x) transformed) of the brown trout located in the pyloric region and

post-pyloric region o f the intestine

Pyloric caeca region

Post-pyloric caeca region

C.M. C.E N.R. C.M C.E N.R.

C . M .

C.E

N . R . - - 0

C . T .

- 0 + 0

T h e t r o u t w e r e s e g r e g a t e d o n t h e b a s i s o f a g e a n d s e a s o n i n to 1 1 b l o c k s . , - , i n d i c a t e t h e n u m b e r o f s t a t is t i c a l ly

s i g n i f i c a n t n e g a t i v e a n d p o s i t i v e c o r r e l a t io n s r e s p e c t i v e l y .

0 , n o s i g n i f i c a n t c o r r e l a t io n s .

C . M .

= C . m e t o e c u s , C E = C . f a r i o n i s ,

N . R .

= N . r u t i l i ,

C . T .

= C . t r u t t a e .




devas ta t r ix in G adus m er l ang i a n d t h e m o n o g e n e a n Ancyrocephalus van-

benedeni

a n d th e c o p e p o d

Ergas i lus na nnus

in

M ugi l sa l i ens

Dogiel , 1961).

W h a t a p p e a r t o b e c l e a r e x a m p l e s o f c o m p e t i t i v e e x c l u s i o n h a v e a l s o b e e n

repor ted in the case o f pa ras it e s in fou r spec ies o f ch imaer id r a tf ish . Each o f

t h e s e s p e c i e s c o n t a i n s t w o d i f f e r e n t s p e c i e s o f t h e c e s t o d a r i a n g e n u s

Gyrocotyle a t the com pon en t popu la t ion l eve l W hi t fi e ld , 1979). Ho we ver , a t

the in f r apopu la t ion l eve l on ly one pa ras i t e spec ies i s genera l ly found as the

s m a l l e r s p e c i e s is c o m p e t i t i v e l y e x c l u d e d b y i ts l a rg e r c o u s i n W h i t fi e l d ,

1 9 7 9) . M o r e r e c e n t e x a m p l e s o f n e g at iv e a s s o c i a ti o n s b e t w e e n h e l m i n t h p a r -

a s i te s o f f i sh i n c l u d e th e c o n g e n e r i c m o n o g e n e a n s p e c i e s Protopolys toma

f iss i l i s and P . s impl icis i n t h e u r i n a r y b l a d d e r o f t h e t o a d , Xenopus wi t t e i

J a c k s o n

et a l.

1998) , and

Neoechinorhynchus go lvani and Sp i rocamal lanus

rebecae in the c ichl id f ish , Cichlasoma synspi lum i n s o u t h e a s t e r n M e x i c o

Vida l -Mar t inez and Kennedy , 2000) and E.crassum and C. metoecus in the

b row n t rou t Ken nedy and Har tv igsen , 2000) . The se r esu l ts ind ica t ing hab i ta t

s eg rega t ion p rov ide s t rong c i r cums tan t i a l ev ide nce tha t in te r spec i fi c com pet i -

t io n b e t w e e n h e l m i n th p a r a s i te s m a y b e a c o m m o n o c c u r r e n c e.

10.2.5. E viden ce ba sed on comm unity s tructure: nul l hypothes is b ased on

the concep t o f nes tedness

T h e a n a l y s is o f th e d e g r e e o f o r d e r o f s p e c i e s a s s e m b l a g e s i n t e r m s o f n e s te d

subse t s has r ece ived a g rea t dea l o f in te res t over the l a st decade . In the con tex t

o f pa rasi t e com m uni t i e s a nes ted pa t te rn occu r s whe n pa ras it e spec ies found in

depau pera te in f r acom m uni t i e s r ep resen t non- random subse t s o f p rogres s ive ly

r icher ones . This im pl ies that the d is t ribut ion of d i f ferent paras ite species am ong

hos t indiv iduals i s not mutua l ly indep end ent Pou l in and Val tonen, 2001) . To

com pl ica te the p ic tu re the re i s a l so ev idence o f an t ines ted pa t te rns. T h i s co r re -

s p o n d s t o s i t u a t i o n s i n w h i c h p a r a s i t e p o p u l a t i o n s a r e a l w a y s a b s e n t f r o m

inf racom mu ni t ie s r i che r than the depaupera te com m uni t i e s in wh ich they occur

Pou l in and G u6gan , 2000) . The l a tt e r au tho r s found tha t an t inestednes s w as as

com m on as nes tednes s and tha t the re was a con t inuum f rom o ne to the o ther .

I t has been a rgued tha t a s nes tednes s i s a depar tu re f rom randomness i t i s

i n d i c a t i v e o f s t r u c t u r i n g p r o c e s s e s a t w o r k a n d t h a t o n e o f t h e s e m i g h t b e

in te r spec ies com pet i t ion . Pou l in 2001a) has how eve r s t r e s sed tha t a l though

t h i s m i g h t b e t h e c a s e i t d o e s n o t r e v e a l t h e c a u s a t i v e m e c h a n i s m . I n f a c t

Pou l in and Va l tonen 2001) have sh own tha t va r ia tion in fi sh s ize and i ts e f f ec t

on pa ras i te a ccum ula t ion a re su f f i c ien t to genera te nes tednes s . Th ey conc luded

tha t a s nes ted pa t t e rns a re mo re a conse quen ce o f the w ay pa ras it e s w ere accu-

m u l a t e d b y t h e h o s t r a t h er t h a n o f t h e e c o l o g i c a l p r o c e s s e s a c ti n g a m o n g t h e

paras i t e spec ies , they have l imi ted use in pa ras i t e communi ty s tud ies . These

proc es ses a re ve ry d i f f e ren t f rom those tha t genera te n es tednes s in f r ee - l iv ing



128 J D THOMAS

communi t i e s . Accord ing to Tokesh i (1999) nes ted d i s t r ibu t ion in f r ee - l iv ing

c o m m u n i t ie s i s m o r e l i k e ly t o b e s e e n i n a s e t o f sp e c i e s w i t h c o m p l e t e n ic h e

par t i t ion ing w i th r espec t to mic rohab i ta t s , pos s ib ly ind ica t ing pas t bu t no t

p resen t com pet i t ion . T he case fo r u s ing nes ted pa tt e rns in pa ras i t e com m uni ty

s tud ies i s fu the r w eake ned b y the ques t ionab le v a l id i ty o f s t a ti s ti ca l m e thods

used to t e s t fo r dev ia t ions f rom random expec ta t ions ( Jons son , 2001) . Pou l in

a n d V a lt o n en ( 2 0 0 1 ) f o u n d t h a t n e st e d n e s s w a s n o t a c o m m o n p a t te r n w h e n

us ing the r a the r conse rva t ive Bo nfe r ron i co r rec t ion .

10.2.6. Evidence based on community structure: saturation models of

parasite communities

Dove (1999) p roposed an index o f in te rac t iv i ty based on the non l inea r r e la -

t io n s h ip b e t w e e n t h e n u m b e r o f h o s t s e x a m i n e d a n d t h e e s ti m a t e d c o m p o n e n t

c o m m u n i t y r i ch n e s s. T h e n u m b e r o f r e c o r d e d p a r a si te s p e c i e s i n c r ea s e s w i t h

t h e n u m b e r o f h o s t s e x a m i n e d u n t il a n a s y m p t o t e c o r r e sp o n d i n g t o th e t r u e

c o m p o n e n t c o m m u n i t y r i c h n e ss i s r ea c h e d . B y f it ti n g a g r o w t h c u r v e t o th e

o b s e r v e d d a t a, D o v e ( 1 9 9 9 ) w a s a b l e to c r e a te t w o p a r a m e t e r s , t h e a s y m p t o t e

and the g rad ien t o f the cu rve be fo re the asympto te . Th i s g rad ien t , wh ich i s

r e la ted to the mean in f racom m uni ty r i chness , bec om es s teeper a s it app roaches

t h e a c t u a l c o m p o n e n t c o m m u n i t y r i c h n e s s . H e t h e r e f o r e s u g g e s t e d t h a t t h e

p r o d u c t o f t h e t w o t e rm s c o u l d p r o v i d e a m e a s u r e o f t h e d e g r e e o f in t er a c ti v -

i t y i n p a r a s i t e c o m m u n i t i e s w i t h h i g h v a l u e s i n d i c a t i n g i n t e r a c t i v e

c o m m u n i t ie s . H o w e v e r , a c c o r d in g t o P o u l in ( 2 0 0 1a , b ) D o v e s ( 1 9 9 9 ) i n d e x

requ i res fu r the r t e s ting b e fo re i t can be accep ted .

T h e c u m u l a t i v e r e l a t i o n s h i p s b e t w e e n i n f r a c o m m u n i t y a n d c o m p o n e n t

c o m m u n i t y r i ch n e s s h a v e a l s o b e e n i n v e st ig a t ed b y a n u m b e r o f p e o p l e i n c lu d -

ing S r ivas tava (1999) . There a re two po ss ib le s cenar ios . In the f i rs t case the

re la t ionsh ip i s l inea r sugges t ing tha t the number o f spec ies in the in f r acom-

m u n i t y i s g e n e r a l l y p r o p o r t i o n a l t o t h e n u m b e r a v a i l a b l e i n t h e c o m p o n e n t

communi ty and tha t spec ies in te rac t ions have a neg l ig ib le e f f ec t . The cu rv i -

l i n e a r r e l a t i o n s h i p i n t h e s e c o n d c a s e s u g g e s t s t h a t t h e i n f r a c o m m u n i t y

r ic h n e ss b e c o m e s i n cr e a si n g ly i n d e p e n d e n t o f t h e c o m p o n e n t c o m m u n i t y rich

ness a s the la t ter increases . This resul t su gges ts that spec ies sa tura t ion is tak ing

p lace in the in f r acommuni t i e s and tha t spec ies in te rac t ion may be occur r ing .

P o u l i n ( 1 9 9 8 ) a n d K e n n e d y a n d G u 6 g a n ( 1 9 9 6 ) p r o v i d e e x a m p l e s o f c a s e s

c o n f o r m i n g t o t h e f i r s t a n d s e c o n d s c e n a r i o s , r e s p e c t i v e l y . H o w e v e r , b o t h

Rohde (1998) and S r ivas tava (1999) have po in ted ou t tha t cu rv i l inea r r e la -

t i o n s h i p s c a n r e s u l t f r o m p r o c e s s e s o t h e r t h a n c o m p e t i t i o n . E x p e r i m e n t a l

ve r i f ica t ion is the re fo re nece s sa ry be fo re it can be con c lude d tha t in te r spec ies

com pet i t ion i s occur r ing .




10 3 Me chan isms of Co m pet i t ive In te rac t ions

Th e s t r ength of explo i t a tive com pet i t ion a t the in te r spec ies l eve l w i l l be n u l li -

f i ed to som e ex ten t by c harac te r d i sp lacem ent , n iche d iver s if i ca tion , c l imate

and po pula t ion r egula t ion by in t r aspec i f ic compet i t ion , p reda t ion an d hyp er -

paras it ism. How ever , befo re i t can b e fu l ly as sessed i t w i l l be nec essary to

obta in m ore d e ta i l ed in form at ion regard ing the nu t r i t iona l r equi rem ents o f the

paras it es a t the b ioche m ica l leve l .

One in te res t ing f ea ture of the numer ica l o r func t iona l r esponses of adul t

he lm in th paras it es to coex i s tence i s tha t ma ny are asy m m et r ica l in na ture .

Typ ica l ly one h e lm in th spec ies incur s severe r educ t ion in num bers w hi l s t the

o ther spec ies i s una f fec ted S i lver

e t a l . ,

1980; Dash, 1981; Holland, 1984;

Bate s and Ken ned y, 1990; Poul in , 2001a). Su ch resul ts s trong ly sugg es t inter -

f e r e n c e c o m p e t i t i o n r a t h e r t h a n e x p l o i t a t i v e c o m p e t i t i o n . I n t e r f e r e n c e

com pet i t ion has a l so bee n invoked to expla in w hy the presenc e of a G yr o co t y l e

species in par t icular species of chim aer id rat fish resul ts in the v i r tual exclus io n

o f o the r congene r i c s pec ie s W i ll iams

e t a l . ,

1987). M ore re cent ly , i t has a lso

been sugges ted tha t the h igh preva lence , un i form d i s tr ibu t ion an d the presen ce

o f exac t l y one m a l e and one f em a l e o f t he nema t ode , Z o n o t h r i x c o l u m b i a n u s,

i n m any o f t he i nd i v i dua l bee t le T r o p i st e r u s c o l u m b i a n u s ) hosts is at tr ibuta-

b l e t o i n t e r fe r ence com pe t i ti on A da ms o n

e t a l . ,

1992). S t rong asym m et r ica l

num er ica l r esponses a re a l so the n orm in the case o f la rva l d igene t i c spec ies in

m ol luscs w i th the do m inant l a rvae caus ing subs tan t ia l r educ t ions in the abun-

danc e of the subord ina te spec ies Kur i s and Laf ferty , 1994).

The na ture of the ch em ica l s involved in in te r fe rence compet i t ion r ema ins to

be e luc ida ted . I t is p oss ib le tha t tox ic ex cre tory product s o r a l l e lopa th ic sub-

s tances might be impl ica ted in the semi -c losed hab i t a t s where the he lmin th

paras i tes live. Lyon s 1978) sugg es ted that the excret ion o f e thyl a lcohol by the

acan t hocepha l an

M o n i l i f o r m i s d u b i u s

might be impl ica ted in the d i sp lace-

m e n t o f

H y m e n o l e p i s

spec ies in r a t s . I t has a l so been sugges ted tha t the

excre t ion of H ÷ by ces tode paras it es m ay g ive the ir t r anspor t sys tem s an advan-

tage ov er those of the i r hos t s and o th er paras i te spec ies M et t r ick , 1975).

Fur ther work i s needed to ascer ta in whether he lmin th paras i t es a l so secre te

m ore spec i f ic k i l le r f ac tors as de m ons t ra ted in the case o f bac te ri a , p ro tozoa ,

p lan ts and t adpoles Thom as e t a l . , 1975) . In the c ase o f larval d igenet ic t rema-

todes the exc lus ion m ech ani sm involved i s usua l ly preda t ion Sousa , 1992).

On e o f the pred ic t ions f rom the genera l p remise of n iche theo ry is tha t i f the

food supply i s invar iab ly superabunda nt s e lec t ive pres sures f avo ur increased

spec i fi c ity , spec ia l is a t ion tow ards a n ar row er n iche bread th and an inc rease in

the s t r ength o f in te r fe rence r esponses in o rder to m ain ta in spa t ia l r equi re -

m e n t s . T h i s w o u l d f a v o u r c o e x i s t e n c e a n d n i c h e p a c k i n g . S u k h d e o a n d

Suk hde o 1994) have shown tha t a par t i cu la r g lyc ine -conju ga ted b i l e sa l t ac id

of hos t o r ig in t r igger s spec i fi c s it e s e lec t ion by a nem atode spec ies . I t can a l so



130 J D THOMAS

be pos tu la ted tha t s e lec t ive p res su res wou ld f avour d ive r s i f i ca t ion o f ac t ive

t r anspor te r s in coex i s t ing s ib l ing he lmin th spec ies . Th i s hypo thes i s r ece ives

som e suppor t f rom the work o f Ug lem (1972) on congener ic acan thocepha la in

the l a rge - sca led sucker f ish ,

Catastomus macrocheilus

In som e cases in te r fe rence r eaches the ex t r eme fo rm o f p reda t ion . An exam -

p l e i s p r o v id e d b y

Phyllodistomumfolium

p r e y i n g o n

Myxidium lieberkuhni

in

the u r ina ry b ladd er o f the p ike ,

Esox lucius

(Dogiel , 1961) . As a resul t these

paras i te s t end no t to coex i s t .

A s p o i n t e d o u t b y D o b s o n ( 1 9 8 5 ) p a ra s it e s m a y a l s o m a k e u s e o f th e h o s t s

i m m u n e m e c h a n i s m t o e x c l u d e o t h e r s p ec i e s. A n e x a m p l e i s p r o v i d e d b y t h e

deve lop m en t o f hos t -genera ted exc lus ion zones a roun d the acan thocepha lan P .

laevis

i n t h e e e l g u t t h a t p r e v e n t s s e t t l e m e n t b y

A anguillae

( B a t e s a n d

Kennedy , 1990) . The monogenean

Dactylogyrus vastator

a l so induces ce l lu la r

r eac t ions in the g i l l s o f i t s hos t s , man i fes ted by the p roduc t ion o f cop ious

mucus and ep i the l i a l hyperp las ia , wh ich p reven t s e t t l emen t by o the r spec ies

(Holm es , 1973) . There a re a l so o the r examples o f c ros s - imm uni ty be ing e f f ec -

t ive aga ins t congen er ic he lmin th pa ras i te s (H ynem an , 1962).

1 0 4 M e c h a n i s m s w h i c h R e d u c e t h e S e v e r it y o f E x p l o i ta t iv e

C o m p e t i t i o n

10 4 1 Character displacement and diversification of ood niche

T h e m o u t h p a r t s o f th e t w o p a r a s i te s

C metoecus

a n d

C truttae

tha t p redomi-

na te in the py lo r ic reg ion o f t rou t a re ve ry d i f fe ren t. In the ca se o f

C metoecus

the mou th , wh ich i s su r rounded by a g lobu la r o ra l sucker , f i r s t l eads in to a

s h o r t p r e - p h a r y n x f o l l o w e d b y t h e ro u n d e d m u s c u l a r p h a ry n x , o e s o p h a g u s

and bifurc ate gut. Th e nutr it ional hab its o f

C metoecus

appear no t to have been

s tud ied in de ta i l bu t i t i s l ike ly tha t in common wi th d igenean gu t b rowser s

t h e y i n g e s t h o s t e p i t h e l i u m , f o o d d e b r i s a n d m u c u s c o n t a i n i n g n u t r i e n t s .

How ever , i t i s l ike ly tha t a s in o the r d igen e t i c t r em atodes (W hi t fi e ld , 1979),

th is food so urce w i l l be supp lem en ted b y tr ans in tegumen ta l t r anspor t o f so lu -

b l e f o o d i t e m s v i a t h e s y n c y t i a l t e g u m e n t a r y c y t o p l a s m . I n t h e c a s e o f

gu t -dwel l ing s t r igeo ids l ike

Apatemon

i t has been shown tha t the adhes ive

organs a re impl ica ted in bo th d iges t ive and abso rp t ive p roces ses (Whi t f i e ld ,

1979) . The f eed ing mechan isms o f

C truttae are

v e r y d i f fe r e n t f ro m t h o s e o f

C metoecus

as i t has a rm atu re fo r t i s sue pene t r a tion . T he m ou th i s su r rounde d

b y a n a r ro w c u t ic u l a r fl a n ge , w h i c h i s a r m e d a t it s b a s e b y a r o w o f n u m e r o u s

s m a l l te e th . T h e m u s c u l a r o e s o p h a g u s i s e x p a n d e d a t th e a n t e r io r e n d t o f o r m

a la rge pseud obu cca l capsu le , the inner su r face o f wh ich i s d iv ided by su tu res

in to s evera l s c le ro t in i sed p la tes. The oeso phag us i s a l so expand ed pos te r io r ly

befo re opening in to the tubular, s traight gut. W ith in the hos t the head en d o f the




p a r a si te b e c o m e s a t t a ch e d t o t h e m u c o s a o f t h e i n te s ti n e o r p y l o r i c c a e c u m

w h i c h i s th e n p e r f o r a te d b y t h e p e r ib u c c a l t e et h . A c c o r d i n g t o M o r a v e c 1 9 9 4 )

th is pa ras i t e f eed s on hos t t i s sue inc lud ing b lood .

The two p redom inan t pa ras it e s in the pos t -py lo r ic reg ion o f the in test ine , N .

rutili a n d C. fario nis exh ib i t a r a the r s imi la r pa t t e rn o f r e source pa r t it ion ing

and ch arac te r d i sp lacem en t to the two d om inan t pa ras i t e s in the py lo r ic reg ion .

T h u s , t h e a n a t o m y o f C. far io nis i s ve ry s imi la r to tha t o f C. metoecus w i t h

w h i c h i t w a s o n c e c o n f u s e d T h o m a s , 1 9 5 8b ) . H o w e v e r , C. far ion is t ends to be

larger and has a re la t ively larger ventra l suck er than

C. meto ecus.

I t is pos s ib le

tha t these d i f f e rence s have evo lved as adap ta t ions to su rv ive in the l e s s s t ab le

env ironm ent in the po s ter ior in tes t ine . N ever the less , i t i s to be ex pec ted that it s

f eed ing n iche w i l l be ve ry s im i la r to tha t o f the cong ener ic spec ies .

L i k e

C. truttae N. ruti li

p e n e t r a te s t h e m u c o s a w i t h i t s p r o b o s c i s c a u s i n g

t h e t i ss u e s i n c l o s e p r o x i m i t y t o i t t o b e c o m e h y p e r t ro p h i e d . A s w i t h c e s t o d e s

t h e A c a n t h o c e p h a l a l a c k a n a l i m e n t a r y c a n a l. A s a re s u l t f o o d i n th e f o r m o f

d i s so lved o rgan ic m at te r is s eques te red t r ans in tegumen ta l ly th rough in fo ld ings

ca l l ed the po re cana l s in the syncy t ia l hypod ermis . Th ese a re m ain ly loca ted in

the metasomal r eg ion , wh ich p ro t rudes in to the gu t lumen , r a the r than in the

p r e s o m a o r p r o b o s c i s r e g io n .

10.4.2. Temporal diversification

Time, v iew ed as a pa ras i te r e source g rad ien t , m ay a l so r educe any in te r spec ies

c o m p e t i t io n . A s a r e s u l t c o m p e t i t io n b e t w e e n

N. rutili and C. truttae

on the

one hand , and C. me toecus a n d C. far ion is on the o the r, w ou ld v i r tua l ly cease

i n th e w a r m e r m o n t h s o f t h e y e a r w h e n t h e n u m b e r s o f th e l a tt e r t w o s p e c i e s

d e c l i n e . A m o r e c o m p l e t e t e m p o r a l s e g r e g a t i o n h a s a l s o b e e n r e p o r t e d f o r

c o n g e n e r i c n e m a t o d e s , Cucul lanus he terochrous a n d C. minutus w h i c h

deve lop in the in tes tine o f the f lounder ,

Plat ich thyes f l esus

a t d i f f e ren t t imes

of the yea r M acK enz ie and G ibson , 1970).

10.4.3. lntraspecif ic interactions

S o f a r a s n u t ri e n t r e s o u r c e s a r e c o n c e r n e d n i c h e o v e r l a p i s g re a t e r b e t w e e n

ind iv idua l s o f the s am e spec ies than be tw een ind iv idua l s o f d i f f e ren t spec ies .

A s a r e s u lt i t is t o b e e x p e c t e d t h at e x p l o i ta t iv e c o m p e t i t io n w o u l d b e m u c h

s t ronger a t the in t r aspec ies than a t the in te r spec ies l eve l. Com pet i t ion m ode ls

based on the log i s t i c equa t ion show tha t th i s d i f f e rence may a l low spec ies to

c o e x i s t M i l le r, 1 9 6 7 ). A l t h o u g h B r o w n 1 9 8 6 ) h a s p r o v i d e d e x p e r i m e n t a l

e v i d e n c e t h a t t h e e s t a b l i s h m e n t a n d s u r v i v a l o f Pomphorhynchus laev i s in

Onchorhychus myki s s i s dens i ty dependen t , op in ion s eems d iv ided r egard ing



132 J D THOMAS

the imp or tance of in t raspec i f ic com pet i t ion amon g paras i ti c he lm in ths of f ish

i n nat u re . A cco r d i ng t o B a t e s and K en nedy 1990) how ev e r cau t ion is neede d

in in te rpre ta t ion wh ere th resholds a re c i t ed as the o n ly ev idence for in t raspe-

c i f ic comp et i tion . Dens i ty dep end ence regula t ion due to space l imi ta tion has

how eve r been i nvoked to exp l a i n t he dec l i nes i n num ber s o f L . the c a tus in the

green sunf i sh Uganski and Nickol , 1982; Ew ald and Nickol , 1989) and a l so in

E . c r a s s u m i n t he b r ow n tr ou t du r i ng e s t ab l i s hmen t K en nedy , 1996). I n

cont ras t , the surv iva l o f L . t h e c a t u s i n t he l a r ge - mo u t h bas s, M i c r o p t e r u s

s a l m o i d e s a n d E . c r a s s u m in the brown t rout , fol lowing es tabl ishm ent , is said

to be dens i ty indep end ent Lead abrand and Nickol , 1993; Kenned y , 1996).

Al thoug h Esch and Feruand es 1993) a rgue tha t the mor ta l i ty r a te o f mo s t par -

as it es in f i sh un der na tura l cond i t ions i s de ns i ty indepen dent m ore quant i t a tive

s tud ies a re r equi red to va l ida te th i s c la im. Recent s tud ies by Morand et al .

1999) o n ec toparas i t es o f mar ine f i sh appear to suppor t the so-ca l led aggre-

ga t ion m od el o f coexis tence w hich pred ic t s tha t in te rspec ies in te rac t ions a re

we ake r than in t raspec ies in te rac t ions thus f ac i li ta t ing c oexis tence .

1 0 . 4 .4 . P r e d a t i o n h y p e r p a r a s i t i s m a n d c l i m a t e

Predat ion or hyperpa ras i t ism ma y regula te popula t ions in a den s i ty -depen dent

manne r . A l t hough c l ima t i c f ac to r s ac t i n a d ens i t y - independ en t m anne r t hey

m ay g r ea t ly in f l uence t he ou t com e o f compe t i ti on . T hus , Pa r k 1954) s how ed

t ha t w hen t em per a t u r e and hum i d i ty w er e va r i ed the ou t co m e o f compe t i t ion

b e t w e e n T r i b o l i u m popu lat ions bec am e probabi l ist ic rather than determ inis t ic .

10 5 Ev o lu t ionary Asp ec ts o f In te rspec ies C om pe t i t ion

The re a re conf l i c ing v iews regard ing the im por tanc e of in te r spec ies in te rac-

t ions in shaping communi t i es o f he lmin th paras i t es in f i sh . Kennedy e t a l .

1986) sugges ted , on the bas i s o f f i e ld surveys , tha t in te r spec ies com pet i t ion

has b een a f a r g rea te r s t ruc tur ing force in the d iver se , spec ies - r ich he lmin th

com mu ni t ie s in t he gu t o f b ir d s and m am m al s t han i n the com par a t ive l y poo r

com m uni t i es o f f r eshwa ter f ish . However , it appears tha t there a re excep t ions

to this rule as Ke nn ed y 1985, 1992) claim s that eve n within the species-poor ,

i so la t ion i s t communi t i es in the ee l in tes t ines in te r spec ies compet i t ion may

occu r be t w een acan t hocepha l a s pec i e s causi ng mi c r ohab i ta t w i d t h t o change

wh en paras i te spec ies coexis t . M ore re cen t ly severa l au thors a l so appear to be

cha l lenging the no t ion tha t in te r spec ies in te rac tions a re no t impo r tan t de te r -

mina nts o f com m un i ty st ruc ture of gu t - inhabi ting he lm in th paras it es in f i sh .

Thus , K enn edy 1985 , 1992) and Vida l -Mar t inez and Ke nne dy 2000) pos tu-

la te tha t compet i t ive in te rac t ions may be po ten t ia l de te rmina nts o f co m m un i ty




s t ruc tu re even in low-d ive r s i ty he lm in th in f r acom m uni t i e s fou nd in t em pera te

zone and t rop ica l f i sh , thou gh i t i s no t ye t c l ea r to wha t ex ten t th is po ten t i a l i s

r ea l i sed in natu re . Ke nned y and Ha r tv igsen 2000) a l so c i t e ev iden ce base d on

c o m m u n i t y s t r u ct u re IC R m ax . = m a x i m u m n u m b e r o f s p e c i e s p e r h o s t a n d

C C R = t o t al n u m b e r o f s p e c i e s p e r s a m p l e ) s u g g e s ti n g t h a t e v e n t h e re l a ti v e ly

spec ies -poo r he lmin th com m uni t i e s in the in test ines o f ee l and trou t a r e s a tu -

r a ted and sugge s t ive o f in te r spec ies in te rac tion . Pou l in 1999) a l so s ta t e s tha t

dominan t pa ras i t e s may be impor tan t in shap ing pa ras i t e communi t i e s e i the r

b y d i re c t c o m p e t i t i o n o r b y a c t i n g o n t h e h o s t p h e n o t y p e c a u s i n g i t t o b e c o m e

a l e s s su i t ab le hab i t a t . The nega t ive as soc ia t ions and ev idence o f s a tu ra t ion

c i t e d i n t h e p r e s e n t r e v i e w p r o v i d e s u p p o r t f o r t h e a b o v e a r g u m e n t s a n d

s t rong ly sugges t tha t in te r spec ies com pet i t ion m ay be a ma jo r s e lec t ive m ech-

an i sm in the case o f gu t - inhab i ting he lmin th pa ras it e s .

H o w e v e r , w h e n R o h d e 1 9 9 1 ) a n d M o r a n d et al 1 9 9 9 ) c o n s i d e r e d t h e

m onoge ne t i c g i l l pa ras it e s o f ma r ine f i sh they cam e to the oppos i t e conc lus ion ,

nam ely tha t in te r spec ies comp et i tion w as o f no g rea t impor tance . The ev iden ce

c i te d b y t h e m i n s u p p o r t o f t hi s v i e w i n c l u d e s t h e p r e p o n d e r a n c e o f p o s it iv e

as soc ia t ions , the h igh p reva lence o f uno ccu p ied n iches o r non- sa tu ra t ion , and

the in s ign i f ican t e f f ec t s o f po ten t i a l ly com pet ing spec ies on mic rohab i t a t s an d

in fec t ion in tens i t i e s . These conc lus ions imply tha t monogene t i c t r ematodes

have a low p robab i l i ty o f loca t ing the i r hos t s and tha t the i r popu la t ion dens i -

t ie s m a y b e d e t e r m i n e d m a i n l y b y t r a n sm i s s io n s u c c e s s.

I t m a y b e s u g g e s t e d t h e r e f o r e t h a t t h e c o n t r a s t i n g v i e w s r e g a r d i n g t h e

i m p o r t a n c e o f in t e r sp e c i fi c c o m p e t i t i o n a s a r e g u la t o r y m e c h a n i s m i n m o n o -

gene t i c and d igene t i c t r ematod es m ay b e a t t r ibu tab le to d i f fe rences in the ir l i fe

h i s t o r y s t r a t e g i e s . T h u s , u n l i k e m o n o g e n e t i c t r e m a t o d e s t h e d i g e n e a h a v e

e v o l v e d m e c h a n i s m s t h a t a l l o w t h e m t o u s e i n t e r m e d i a t e h o s t s i n t h e f o o d

cha in to inc rease the p ro bab i l i ty o f t ransmis s ion . A s a r e su l t th i s mak es the i r

popu la t ions m ore suscep t ib le to s a tu ra tion and he nce r egu la t ion b y bo th in te r -

spec ies and in t r aspec ies com pet i t ion .

R o h d e 1 9 9 1 ) a l s o c o n s i d e r s t h at i n tr a s pe c i fi c c o m p e t i t i o n m a y o c c a s i o n -

a l ly o c c u r w i t h in p o p u l a t i o n s o f m o n o g e n e a a s e v i d e n c e d b y t h e e x p a n s i o n o f

m i c r o h a b i ta t s w h e n i n f e c ti o n d e n s it ie s o f m o n o g e n e a n s a r e h ig h . H e a r g u e s

h o w e v e r t h at t h e r e i n f o r c e m e n t o f r e p r o d u c t iv e b a r ri e rs h a s b e e n o n e o f t h e

ma in m echan i sms d r iv ing the evo lu t ion o f m ic rohab i t a t r e st r ic t ion , o r n iche

seg rega t ion , in mon ogen ea . H ow ever , th is a rgum en t i s no t exc lus ive and o the r

se lec t ive advan tages l inked to m ic rohab i t a t r e s t r ic t ion suc h as r e source pa r t i -

t ion ing and charac te r d i sp lacem en t canno t be ignored .

Var ious wo rker s inc lud ing Schad 1963a , b , 1966) and Pe t t e r 1966) have

sugges ted tha t mic rohab i t a t s eg rega t ion and charac te r d i sp lacemen t in coex-

i s ting he lm in th pa ras i t e s have a r i s en as a r e su l t o f in te r spec ies com pet i t ion .

Ho we ver , a s the re is a genera l con sensu s tha t spec ia t ion occur s w hen pop u la -

t ions are a llopat r ic , i t seem s unl ikely that in terspecies com pet i t ion co uld be the



134 J D THOMAS

p r i m a r y c a u s e f o r t h e e v o l u t i o n o f c o n g e n e r i c , s i b l in g s p e c i e s . N e v e r t h e l e s s , i t

i s p o s s i b l e t h a t i n t e r s p e c i e s c o m p e t i t i o n m a y c a u s e f u r t h e r d i v e r g e n c e s

b e t w e e n t h e s p e c i e s a f te r t h e y b e c a m e s y m p a t r ic .

T h e p r e s e n t re v i e w s u p p o r t s o n e o f t he g e n e r a l is a t io n s m a d e b y M i l le r

1 9 6 7 ) t h a t i n t e r s p e c i e s c o m p e t i t i o n t e n d s t o b e a s y m m e t r i c a l . T h i s a u t h o r

a l so p r o d u c e d e v i d e n c e th a t s u p e r i o r c o m p e t i t o r s t e n d t o b e l a r g er , h a v e a

m o r e r e s t ri c t ed s p a ti al d i s tr i b u ti o n a n d h a v e s t r o n g e r in t e r f e r e n c e m e c h a n i s m s

t h a n t h e l e s s e f f e c t i v e c o m p e t it o r . I t w o u l d b e o f i n te r e st t o a s c e r t a in w h e t h e r

t h e s e g e n e r a l i s a t i o n s c a n b e a p p l i e d t o h e l m i n t h p a r a s it e s . I n t h e c a s e o f p a r a -

s i te s i t i s n e c e s s a r y t o c o n s i d e r t h e p o s s i b i l i ti e s t h a t i n t e r f e r e n c e m a y b e

m e d i a t e d v i a a l l e lo p a t h i c c h e m i c a l s a s w e l l as th e i m m u n e m e c h a n i s m s o f t h e

h o s t. F u r t h e r i m m u n o l o g i c a l a n d b i o c h e m i c a l r es e a r c h i s t h e r e f o r e r e q u i r e d t o

a s c e r ta i n t h e n a t u r e a n d m a g n i t u d e o f t h e e x p l o i ta t i v e a n d i n t e r f e r e n c e m e c h -

a n i s m w h i c h h e l m i n t h p a r a s i te s m a y e x p l o i t d u r i n g e i t h e r i n t ra - o r i n t e r s p e c i e s

c o m p e t i t i o n .

CKNOWLEDGEMENTS

F i r st a n d f o r e m o s t I w i s h t o th a n k t h e l a t e P r o f e s s o r G . E R e e s f o r s ti m u l a t in g

m y i n t er e s t i n p a ra s i to l o g y . T h a n k s a r e a ls o d u e t o t h e S a l m o n a n d T r o u t T r u st

f o r f in a n c i a l s u p p o r t, t h e E n v i r o n m e n t A g e n c y , W a l e s f o r b o t h f i n a n c i a l a n d

t e c h n i c a l s u p p o r t , t o M r P . M a r t i n , M r D . H i t c h i n , D r D . R . R o b i n s o n

U n i v e r si ty o f S u s s e x) a n d M r I s a ac N e w t o n o f M I N I T A B f o r a ss i st a nc e w i th

s t a ti s ti c a l m e t h o d o l o g i e s a n d to M r J . B a s s a n d D r M . L a d l e I n s t it u t e o f

F r e s h w a t e r E c o l o g y ) f o r a ss i s ta n c e w i t h t h e i d e n t i fi c a t io n o f f r e s h w a t e r a q u a t i c

i n v e r t e b r a t e s .

REFERENCES

Adam son, M .L., Buck, A. and No ble, S. 1992). Transm ission pattem and intraspecific com -

petition as determinants of population structure in pinworms Oxy urida, Nem atoda).

Journal o f Parasitology 78, 420--426.

A1-Hussaini, A .H . 1949). On the fun ctional mo rphology of the alimentary tract of som e fish

in relation to differences in their feeding habits. 1. Anatom y and histology. Quarterly

Journal o f Microscopic Science 90 109-139.

Allison, A .C . 19 82 ). Coevo lution between ho sts and infectious disease agents, and its

effec t on virulence. In: Popu lation Biology o f Infectious D iseases R.M. Anderson and

R.M . M ay, eds), pp. 245-268. New Yo rk: Springer Verlag.

Aloisi, A.M ., Steenbergen, H.L., Vandepoll, N.E. and Farabollini, F. 1994). Sex-dependent

effects o f restraint on n ociception and p ituitary-adrenal hormon es in the rat. Physiology

and B ehaviour 55, 789-793.




A lv a re z P e l l i t e ro , M .E (19 78 ). T h e l i f e h i s to ry o f Raphidascaris acus i n th e n a tu ra l e n v i -

r o n m e n t o f t h e r i v er s o f L e 6 n ( N W S p a i n) .

4th International Cong ress of Parasitology,

1 9 -2 6 A u g u s t , 1 9 7 8 , Wa rs a w . S h o r t C o mmu n ic a t io n s , S e c t io n H , p . 4 9 . O rg a n i s in g

C o m m i t t e e .

A m in , O .M . (1 9 8 5 ) . T h e r e l a t io n s h ip b e tw e e n th e s i z e o f s o me s a lmo n id f is h e s a n d th e

in tens i ty o f the i r acan tho cepha lan in fec t ions .

Canadian Journal o f Zoology

6 3 , 9 2 4 -9 2 7 .

An dersen , K .I . and Va ltonen, E .T . (1990) . On the in fracom m uni ty s t ruc tu re o f adu l t ces todes

in f reshw ate r f i sh . Parasitology 101 , 257-264 .

A n d e r s o n , R . M . ( 1 9 7 4 ) . P o p u l a t i o n d y n a m i c s o f t h e c e st o d e Caryophyllaeus laticeps

(P a l l a s , 1 7 8 1 ) in th e b re a m

Abramis brama

(L . ) .

Journal of Anim al Eco logy

4 3 ,

3 0 5 - 3 2 1 .

A n d e rs o n , R .M. (1 9 8 2 ) . E p id e m io lo g y . In : Modern Parasitology ( E E . G . C o x , e d . ) p p .

2 0 4 -2 5 1 . O x fo rd : B la c k w e l l S c ie n t i f ic P u b l i c a t io n s .

A n d e rs o n , R .M. a n d M a y , R .M. (1 9 7 9) . P o p u la t io n b io lo g y o f in fe c t io u s d i s e a se s . P a r t 1

and 2.

Nature London)

2 8 0 , 3 6 1 -3 6 7 , 4 5 5 -4 6 1 .

And rews , C . and Chubb , J .C . (1980) . Ob serva t ions on the deve lopm ent o f

Bunodera luciop-

ercae

(M ii l le r, 1776) (Trem atoda : Al lo c read i idae ) under f ie ld and lab ora to ry cond i t ions .

Journal ofF ish D iseases 3 , 4 8 1 -4 9 3 .

A rm s t ro n g , A . a n d P h i l l ip s , K . (1 9 9 8 ). A s t r a te g ic r e v ie w o f s h e e p d ip p in g .

Research and

Development Technical Report P170.

5 8 p p . S w i n d o n : E n v i r o n m e n t A g e n c y R D

D is s e m in a t io n C e n t re .

A rm s t ro n g , J .D . , H u n t in g fo rd , F .A . a n d H e rb e r t , N .A . (1 9 9 9 ) . In d iv id u a l sp a c e u s e s t r at e -

g ie s o f w i ld j u v e n i l e A t l a n t i c s a lmo n .

Journal o f Fish Biology

55, 1201 - 1212

A v t a l i o n , R . A . , W o j d a n i , A . , M a l i k , Z . , S h a h r a b a n i , R . a n d D u c z y m i n e r , M . ( 1 9 7 3 ).

In f lu e n c e o f e n v i ro n me n ta l te mp e ra tu re o n th e imm u n e re s p o n s e in f is h .

Current Topics

in Microbiology and Immunology

61 , 1 -35 .

A w a c h i e , J . B . E . ( 1 9 6 5 ). T h e e c o l o g y o f

Echinorhynchus truttae

Schrank , 1788

(A c a n th o c e p h a la ) in a t ro u t s tr e a m in N o r th W a le s. Parasitology 5 5 , 7 4 7 -7 6 2 .

A w a c h ie , J .B .E . (1 9 6 8) . O n th e b io n o m ic s o f Crepidostomum metoecus (Braun , 1900) and

Crepidostomum farionis

(MUlle r, 1784) (Trem atoda : A l loc re ad i ida e ) .

Parasitology

58,

3 0 7 - 3 2 4 .

Aw achie , J .B .E . and Chubb , J .C . (1964). Ob serva t ions on the occurrence and d is t r ibu t ion o f

Crepidostomum metoecus (Braun , 1900) in the Br i t i sh Is le s . Parasitology 54, 29.

A y a la , C .E . , K o h le r, C .C . a n d S t i c k n e y , R .R . (1 9 9 2) . P ro te in d ig e s t ib i l i t y a n d a min o a c id

a v a i l a b i l i t y o f f i s h -m e a l f e d to l a rg e m o u th b a s s in fe c te d w i th in t e s t in a l a c a n th o c e p h a -

lans .

Progressive Fish Culturist

5 5 , 2 7 5 -2 7 9 .

Bady aev , A.V. (1997) . Al t i tu d ina l va r ia t ion in sexua l d im orph ism : a new pa t te rn and a l te r -

na t ive hypotheses .

Behavioural Ecology

8 , 6 7 5 -6 9 0 .

Bak ke , T .A. and Harr is , P .D. (1998). Dise ases and pa ras i te s in wi ld At la n t ic sa lmon

Salmo

salar)

p o p u la t io n s .

Cana dian Journal o f Fisheries an d Aquatic Sciences

5 5 , 2 4 7 -2 6 6 .

Bak ke , T .A. , Jansen , P .A. and H ansen , L .P . (1990) . Dif fe rences in hos t re s is tance o f At lan t ic

s a lmo n , Salmo salar L . s to c k s to th e mo n o g e n e a n Gyrodactylus salaris M a l m b e r g ,

1957. Journal ofFis h Biology 3 7 , 5 7 7 -5 8 7 .

B a k k e r , T .C .M. a n d M u n d w i le r , B . (1 9 9 9 ) . P e c to ra l f in s i z e in a f i s h s p e c ie s w i th p a te rn a l

ca re : a cond i t ion-d epen den t sexua l tra i t revea l ing in fec t ion s ta tus .

Freshwater Biology

4 1 , 5 4 3 - 5 5 1 .

B a n g h a m , R .V . (1 9 4 4 ). P a ra s i t es o f N o r th W is c o n s in f is h .

Transactions of the Wisconsin

Aca dem y o f Science, Arts an d Letters.

3 6 , 2 9 1 -3 2 5 .

Bar lau p , B .J . , Lura , H. , Saegrov , H. and Sun dt , R .C. (1994) . In te r -sp ec i f ic and in t ra -spe cf ic

v a r i a b i l i t y in f e m a le s a lm o n id s p a w n in g b e h a v io u r.

Canadian Journal of Zoology

72 ,

6 3 6 - 6 4 2 .



136 J D THOMAS

B a t e s , R . M . a n d K e n n e d y , C . R . 1 9 9 0 ). I n t e r a c t i o n s b e t w e e n t h e a c a n t h o c e p h a l a n s


a n d


in ra inbow t rou t : te s t ing an

e x c lu s io n h y p o th e s i s .

Parasitology

100, 435

444.

B a t ra , V . 1 9 8 4 ) . P re v a le n c e o f h e lmin th p a ra s i t e s in th re e s p e c ie s o f c i c h l id s f ro m a ma n

m a d e l a k e in Z a m b i a . Zoological Journal o f the Linnean Society 8 2 , 3 1 9 -3 3 3 .

Bauer , O .N. 1991) . S pread o f pa ras i te s and d isease o f aqua t ic o rgan isms by acc l imat iza t ion :

a sh or t rev iew. Journal ofFish Biology 3 9 , 6 7 9 -6 8 6 .

Ba ylis , H.A . 1931).

Gamm arus pulex

as an in te rmedia te hos t fo r t rou t pa ras i te s .

Annals and

Magazine o f Natural History 10) , 7 , 431-435 .

B e r g , O . K . , F o o t e , C . J . a n d Q u i n n , T . P . 1 9 9 5 ) . F i s h a g e , n e m a t o d e Philonema

oncorhynchi)

i n fe c tio n , an d d e v e lo p me n t o f s e x u a l d imo rp h i s m b y th e a d u l t ma le s o c k -

e y e s a lmo n ,

Onchorhynchus nerka,

i n w e s te rn A la s k a .


73,

1 9 9 9 -2 0 0 4 .

Berns te in , R .M . , Sch lu te r , S .F . and March a lon is , J . J . 1998) . Imm uni ty . In :

The Physiology

o f Fishes.

D.H. E v a n s , e d .) , 2 n d e d n , p p . 2 1 5 -2 4 2 . B o c a R a to n : C R C P re s s .

Bib io , S .D. and Ne lson , R .J . 2001) . Sex s te ro id horm ones enhance imm une func t ion in

m a l e a n d f e m a l e S i b e r i a n h a m s t e rs .

Am erican Journal o f Physiology - Regulatory

Integrative and Comparative Physiology

280 , R207-R213 .

Blacks tock , N. and P icke t ing , A.D . 1982) . Chang es in the concen tra t ion and h is tochem is t ry

o f e p id e rma l mu c o u s c e l l s d u r in g th e a l e v in a n d f ry s t a g e o f th e b ro wn t ro u t

Salmo

trutta. Journal o f the Zoological Society o f London

197 , 463-471 .

Bod e t , I , Lym an, W.J ., Reeh l , W .E an d Rose nb la t t , D.H . 1988) .

Environmental Inorganic

Chemistry.

Ne w Yo rk: P e rg a m o n P re s s.

B o rg s t r tm ,R . 1 97 0) . S tu d ie s o n th e h e lmin th fa u n a o f No rwa y XV1 . Triaenophorus nodu-

losus

Pal las , 1760) Ces tod a) in Bo gs tad La ke . 111. Occurren ce in p ike ,

Esox lucius L.

Nytt m agasin fo r zoologi

18 , 209-216 .

B o rg s t r tm , R . a n d Ha lv o rs e n ,O . 1 96 8) . S tu d ie s o n th e h e lmin th f a u n a o f No rwa y . X1 .

Caryophyllaeidesfennica

S c h n e id e r ) C e s to d a : C a ry o p h y l l id e a ) in L a k e B o g s t ra d .

Nytt

magasin fo r zoologi 16 , 20-23 .

B ra d le y , D . J . 1 9 7 4 ) . S ta b i l i t y in h o s t -p a ra s i t e p o p u la t io n s . In :

Ecological Stability

M . B .

Us h e r a n d M.H. W i l l i a ms , e d s ) p p . 7 1 -8 8 . L o n d o n : C h a p m a n a n d H a l l.

Bronse th , T . and Fo ls tad , I . 1997) . The e ffec t o f pa ras i te s on cour tsh ip dance in th reesp ine

s t i c k le b a c k s : M o re th a n m e e t s th e e y e ? Canadian Journal o f Zoology 7 5 , 5 8 9 -5 9 4 .

Brooker , M.P . 1984) . Con serva t ion o f wi ld l i fe in r ive r corr idors .

Nature in Wales

2 , 11-20 .

B r o w n , A . F . 1 9 8 6 ). E v i d e n c e f o r d e n s i t y - d e p e n d e n t e s t a b l i s h m e n t a n d s u r v i v a l o f


M ii ll e r , 1 77 6) Ac a n th o c e p h a la ) in la b o ra to ry - in fe c te d

Salmo

gairdneri R ic h a rd s o n a n d i t s b e a r in g o n w i ld p o p u la t io n s in Leuciscus cephalus L.).

Journal ofFish Biology

2 8 , 6 5 9 -6 6 9 .

Bro wn , F.J. 1927). O n

Crepidostomumfarionis

Mii l l . =

Stephanophiala laureata

Z e d e r ) ,

a d is tom e paras i te o f the t rou t and g ray l ing . 1 . The l i fe h is to ry .

Parasitology,

19, 86-99.

B ro w n , R .E . 1 9 9 4 ) . An Introduction to Neuroendocrinology. C a m b r i d g e : C a m b r i d g e

Un iv e r s i ty P re s s .

Bubb , J .M . , Rudd , T . and Les te r, J .N. 1991) . Dis t r ibu t ion o f heav y-m eta ls in the River Yare

a n d i t s a s s o c ia t e d B ro a d s .

Science o f the Total Environment

102, 189-208.

Bush , A.O . , Laffe r ty , K.D . , Lo tz , J .M . and Shos tack , A.W . 1997) . Pa ra s i to logy me e ts eco l-

o g y o n i t s o wn t e rms : Ma rg o l i s

et al.

rev is i ted .

Journal o f Parasitology

8 3 , 5 7 5 -5 8 3 .

C a m e ro n , P .G . a n d Ho lm e s , J.C . 1 9 9 7 ) . P a ra s i te me d ia te d n a tu ra l s e le c t io n . In :

Hos t

Parasite Evolution: General Principles an d Avian M odels D.H.C la y to n a n d J .Mo o re ,

e d s ) , p p . 9 -2 9 . Ox fo rd : O x fo rd Un iv e r s i ty P re s s .

C a m p b e l l , A .D . 1 9 74 ). T h e p a ra s i t e s o f f is h in L o c h L e v e n .

Proceedings of the Royal

Society o f Edinburgh

B , 7 4 , 2 3 -3 6 4 .




Can non, L .R.G. 1972). S tudies on the eco logy of the papi l lose al locreadid t rematodes o f

the ye l low perch in Algonquin Park , Onta r io . Canadian Journal o f Zoology 50,

1231-1239 .

Carney, J .P. and Dick , T.A. 1999). Enteric helminths o f perc h Perca fluviatilis L.) and

ye l low perch Percaflavescens M itchill): S tochastic o r predictable assem blages? Journal

o f Parasitology 85 , 785 -795 .

Carpenter , K.E. 1926). T he lead m ine as an act ive agent in r iver pol lut ion. Annals of

Applied Biology 13 , 385-4 01 .

Carpenter, K.E. 1928). Life in Inland W aters with Special Reference to Animals. L o n d o n :

S idgwick and Jackson .

Ch app el , L.H. 1969). Com peti t ive exc lusion betw een two intestinal parasi tes of the three-

spined st ickeback, Gasterosteus aculeatus L. Journal o f Parasitology 55 , 775 -778 .

Che, R.G.O. and Ch eung , S .G. 1998). H eav y metals in Metapenaeus ensis, Eriocheir

sinensis

and sediments f rom the Mai Po marshes , Hong Kong.

Science of the Total

Environment 214 , 87-97 .

Chernin, J . and Morinan, A . 1985). An alys is o f s ix serum com pon ents f rom rats infected

with tetrathyridia o f M esocestoides corti. Parasitology 90, 441--447.

Cho udhu ry, A. and Dick, T .A. 2000). Richness and diversi ty of helminth comm uni t ies in

tropica l freshw ater f ishes: em pirical evidence. Journal o f Biogeography 27 , 935 -956 .

Chu bb, J .C. 1964). A p rel iminary co m par ison o f the specif ic com posi t ion of the paras ite

fauna o f the fi sh of Llyn Padarn, Caernarvonshire , an ol igot rophic lake, and L lyn Tegid

Bala La ke ) , Merionethshire. Wiadom sci Parazytolgiczne 10, 499.

Chu bb, J .C. 1970). T he paras i te faun a of Br i t i sh f reshw ater fi sh. In: Aspects of Fish

Parasitology. Symposia o f the British Society fo r P arasitology 8 A.E.R. Taylor, ed.) pp.

1 1 9 1 4 4 .

Ch ubb , J.C. 1973). Influ enc e o f parasi tes on freshw ater fishes in Britain. Verhandlungen -

lnternationale Vereinigung fu er Theoretische und Angew andte Limnologie 18 ,1628-

1632.

Chub b , J .C . 1977) . Seasona l occ ur rence o f he lmin ths i n f r eshwate r f ishes . Pa r t I .

M o n o g e n e a . Advances in Parasitology 15, 133-199.

Chub b , J .C . 1979) . Season a l occur rence o f he lmin ths i n f reshw ate r f i shes . Pa r t I I .

Trematoda. Advances in Parasitology 17, 141-313.

Chu bb, J .C. 1980). Seasonal occurre nce of helminths in f reshwater f ishes. Pa r t I I I . Larval

Ces toda and Nem atoda . Advances in Parasitology 18, 1-120.

Chu bb, J .C. 1982). Seasonal occu rrence of helminths in f reshwater fi shes . Par t IV. Ad ul t

Ces toda , Nematoda and Acanthocepha la . Advances in Parasitology 20, 1-292.

Ch ubb , J .C. 1997). Fish parasites as indicators o f env ironm ental quality: a secon d per-

spective. Parassitologia 39, 255.

Co ne, D.K., Marcogliese, D.J. and W att, W .D. 1993). Me tazo an parasite com m un it ies of

yel low eels Anguilla rostrata) in acidic and l imed r ivers of Nova-Scot ia . Canadian

Journal o f Zoology 71, 177-184.

Crawford, W .W. 1943). C olarad o trematode studies. I . A further contribution to the l i fe his-

t o ry o f Crepidostomumfarionis Miiller). Journal o f Parasitology 29 , 379-384 .

Crom pton , D .W.T . 1991) . Nu t r it i ona l in t e r ac t ions be tw een hos t and pa ras i te s . In :

Parasite-Host Associations: Coexistence or Conflict. C.A.Tof t , A. Aeschl imann and

L.Bol is , eds), p p. 22 8-2 57 . O xford : Ox ford Sc ience Publications .

Curt is , M .A., B fru bf , M. and Stenzel, A. 1995). Parasi tological evid ence for special ized

foraging beh aviou r in lake-res ident Arct ic char Salvelinus alpinus). Canadian Journal

o f f i s h andAquat ic Science 52 suppl . 1) , 18 6-1 94 .

Dash , K .M. 1981) . In t e rac t i ons be tween Oesophogostomum venulosum in sheep.

International Journal o f Parasitology 11 , 201-20 7 .



138 J D THOMAS

D av is , H .S . (1 9 5 3 ) .

Culture and Diseases of Game Fishes.

B e r k e l e y : U n i v e r s i t y o f

C a l i fo rn ia P ress .

D av i so n , W. (19 86 ). S ew ag e s lu d g e as an ac id i ty f il t e r fo r g ro u n d w a te r f ed l ak es .

Nature

London)

3 2 2 , 8 2 0 -8 2 2 .

D av i so n , W . (19 87 ). In t e rn a l e l emen ta l cy c les a f fec t in g th e lo n g - t e rm a lk a l in i ty s t a tu s o f

l ak es : im p l i ca t io n s fo r l ak e r es to ra tio n .

Schwizerische Zeitschriftfiir Hydrologia

49,

186-201 .

Daw kins , R . (1990) . Paras i tes , des ide rata l i s t s and the pa radox o f the o rga n ism. Parasitology

Sympo sia o f the British Society o f Parasitology (Vol. 27) 100, 63 - 73 .

d e Jo n g -B r in k , M. (1 9 9 5) . H o w sch i s to so m es p ro f i t f ro m th e s t r e s s r e sp o n ses th ey e l i c i t i n

thei r hosts .

Advances in Parasitology

35 , 177-256 .

D em ers , N .E . an d B a y n e , C . J . (1 99 7 ). T h e im me d ia t e e f fec t s o f s t r e s s o n h o rm o n es an d

p l a s m a l y s o z y m e i n r a i n b o w t r o ut .

Developmental and Comparative Immunology

21 ,

3 6 3 -3 7 3 .

D e p a r t m e n t o f t h e E n v i r o n m e n t a n d W e l s h O f f ic e ( 1 9 8 9) .

Water and the Environment.

Circular 7/89 (Circ u lar 16 /89 We lsh Off ice) , 30 Marc h , 1989.

D ep ar tmen t o f W ate r A f fa i r s an d F o res t ry (1 99 6 ) .

South African W ater Quality G uidelines.

Volume 7. Aquatic Ecosystems, p p . 1 -8 1 . D ep ar tm en t o f W ate r A f fa i r s an d F o res t ry .

D e V an ey, J .A . , E l i sd a le , M H . , S tee l , E .G . , H o g an , B .E an d D e l v an P e te r sen , H . (1 9 9 7 ) .

E f fec t o f t h e n o r th e rn fo w l mi t e

Ornithonysus sylviarum

o n w h i t e l eg h o rn ro o s t e r s .

Poultry Science 56 , 1585-1590 .

Dezfuli , B.S. (1996).

Cypria reptans

(C ru s t acea : O s t raco d a) a s an in t e rmed ia t e h o s t o f

Neoechinorhynchus rutili ( A c a n t h o c e p h a l a : E o c a n t h o c e p h a l a ) i n I t a l y . Journal of

Parasitology 8 2 , 5 0 3 -5 0 5 .

D o b s o n , A . P . ( 1 9 8 5 ) . T h e p o p u l a t i o n d y n a m i c s o f c o m p e t i t i o n b e t w e e n p a r a s i t e s .

Parasitology 9 1 , 3 1 7 -3 4 7 .

D o b s o n , A . P. ( 1 9 9 0 ). M o d e l s o f m u l t i -s p e c i e s p a r a s i t e - h o s t c o m m u n i t i e s . I n :

Parasite

Communities: Patterns and Processes

(G .W. E sch , A . B u sh an d J .M. A h o , ed s ) , p p .

2 6 1 - 2 8 7 . L o n d o n : C h a p m a n a n d H a l l.

D o b so n ,A .P an d H u d so n , P . J. (19 92 ). R eg u la t io n an d s t ab i l i ty o f a f r ee l i v in g h o s t -p a ras i t e

sy s t em: Trichostrongylus tenuis in red g rouse. 11 . popu lat ion models . Journal of Animal

Ecology,

6 1 , 4 8 7 - 4 9 8 .

D o b so n ,A .P . an d McC al lu m , H . (1 9 9 7 ) . T h e ro l e o f p a ras i t e s in b i rd co n se rv a t io n . In :

Ho st-Para site Evolution: General Principles and Avian Mod els

( D . H . C l a y t o n a n d

J .Mo o re , ed s ) , p p . 1 5 5 -1 7 3 . O x fo rd : O x fo rd U n iv er s i ty P ress .

D o b so n , C . (1 9 6 1 a) . C er t a in asp ec t s o f th e h o s t -p a ra s i t e r e l a t io n sh ip o f Nematospiroides

dubius

( B a y l i s ). I . R e s i st a n c e o f m a l e a n d f e m a l e m i c e t o e x p e r i m e n t a l i n f e c ti o n s .

Parasitology

51 , 173-179 .

D o b so n , C . (1 9 6 1 b ) . C er t a in asp ec t s o f th e h o s t - p a ra s i t e r e l a t io n sh ip o f

Nematospiroides

dubius

(B ay l i s ) . II . T h e e f fec t o f sex o n e x p er im en ta l i n fec t io n in th e r a t ( an ab n o rm al

host ) . Parasitology 5 1 , 4 9 9 - 5 1 0 .

D o b so n , M. an d F r id , C . (1 9 9 8 ) .

Ecology o f Aquatic Systems.

H a r l o w : A d d i s o n W e s l e y

L o n g m a n .

D o g ie l , V .A (1 9 6 1 ). E co lo g y o f th e p a ras i t e s o f f r e sh w ate r f i sh . In : Parasitology o f Fishes

(V .A . D o g ie l , G .K .P e t ru sh ev sk i an d Y u . I . P o ly an sk i , ed s ) , p p . 1 -4 7 . E d in b u rg h an d

L o n d o n : O l i v e r a n d B o y d .

D o ro cu ,M . , C ro m p to n , D .W.T ., H u n t in g fo rd , F .A . an d Wal t e r s , D .E . (19 95 ). T h e eco lo g y o f

e n d o p a r a s i t i c h e l m i n t h i n f e c t i o n s o f b r o w n t r o u t

Salmo trutta)

a n d r a i n b o w t r o u t

Onchorhynchus mykiss) i n S co t l an d . Folia P arasitologica 4 2 , 2 9 -3 5 .

D o v e , A .D .M . (1 9 9 9 ) . A n ew in d ex o f in t e rac t iv i ty in p a ras i t e co mm u n i t i e s . International

Journal fo r Parasitology

2 9 , 9 1 5 -9 2 0 .



140 J D THOMAS

E w a ld , J .A . a n d N ic k o l , B .B . 1 9 89 ). Av a i l a b i l i t y o f c a e c a l h a b i ta t a s a d e n s i ty -d e p e n d e n t

l imi t o n s u rv iv o rs h ip o f Leptorhynchoides thecatus in g reen sunf ish , Lepom is cyanellus.

Parasitology

98, 447--450.

Fergu son , A. 1989) . Ge ne t ic d i f fe rences am ong brown t rou t , Salmo trutta, s tocks and the i r

imp o r ta n c e fo r th e c o n s e rv a tio n a n d m a n a g e m e n t o f th e s p e c ie s . Freshw ater Biology 21 ,

35--46.

Fevolden , S .E . , Nordm o, R. , Refs t ie , T . and R oed , K.H. 1993) Disease res is tance in At lan t ic

s a l m o n Salmo salar) s e le c te d fo r h ig h o r lo w re s p o n s e s to s t r e s s . Aquaculture 109,

2 1 5 - 2 2 4 .

F io r i l lo , R .A . a n d F o n t , W .E 1 9 9 6 ). He lm in th c o mm u n i ty s t ru ctu re o f fo u r s p e c ie s o f

Lepomis Os te ic h th y e s : C e n t ra rc h id a e ) f ro m a n o l ig o h a l in e e s tu a ry in s o u th e a s te rn

L o u i s i a n a . Journal o f the Helminthological Society o f Washington 6 3 , 2 4 -3 0 .

F le m in g , M.W . 1 9 8 5 ) . S te ro id a l e n h a n c e m e n t o f g ro wth in p a ra s i t ic l a rv a e o f Ascaris

suum:

v a l id a t io n o f a b io a s s a y .

Journal o f Experimental Zoology

2 3 3 , 2 2 9 -2 3 3 .

F o l s t a d , I . a n d K a r te r, A . J . 1 9 9 2 ). P a ra s i t e s , b r ig h t ma le s a n d th e immu n o c o m p e te n c e

h a n d ic a p . American Naturalist 139 , 603-622 .

Forb es , K.C. , Ensor , D.M . and Chu bb , J .C . 1989) . Tow ards a hyp othes is fo r seasona l m a t-

u ra t ion o f he lmin ths in the f i sh de f in i t ive hos t .

Parazitologiya

2 3 , 2 8 8 -2 9 5 .

Free land , W.J . 1976) . Pa tho gens and the evo lu t ion o f p r imate soc ia l i ty . Biotropica 8 , 12-24 .

F ry e r , G . 1 9 6 8 ). T h e p a ra s i t ic c o p e p o d

Lernaea cyprinacea

in Br i ta in .

Journal o f Natural

History 2 , 5 3 1 -5 3 3 .

Ga n n ic o t t , A .M . a n d T in s le y , R .C . 1 9 9 7 ). E g g h a tc h in g in th e mo n o g e n e a n g i l l p a ra s i t e

Discocotyle sagittata

f ro m th e r a in b o w t ro u t

Onchorhynchus mykiss). Parasitology

114 , 569-579 .

G a n n i c o t t , A . M . a n d T i n sl e y , R . C . t 9 9 8 a ) . E n v i r o n m e n t a l e f f ec t s o n t r a n s m i s s i o n o f


M o n o g e n e a ) : e g g p ro d u c t io n a n d d e v e lo p me n t .

Parasitology

117,

4 9 9 - 5 0 4 .

Gan nico t t , A.M . and Tins ley , R .C. 1998b) . Larv a l su rv iva l charac te r is t ic s and beha v iour o f

t h e g i l l m o n o g e n e a n Discocotye sagittata. Parasitology 117 , 569-579 .

Ge rh a rd t , A . 1 99 3) . R e v ie w o f imp a c t o f h e a v y me ta l s o n s t r e a m in v e r t e b ra te s w i th s p e c ia l

e mp h a s i s o n a c id c o n d i t io n s . Water, A ir a nd Soil Po llution 6 6 , 2 8 9 -3 1 4 .

G ie s y , .E a n d Ho k e , R .A . 1 99 0) . F re s h w a te r s e d ime n t q u a l i ty c r i t e ri a : t o x ic i ty b io a s s e s s -

ment . In :

Sediments: Chem istry and Toxicity o f In-Place P ollutants.

R .B a u d o , J . Ge i s y

a n d H . M a n ta u , e d s ) . C h e l s e a, Mic h ig a n : L e wis P u b l i s h e r s.

G in e t s in s k a y a , T .A . 1 96 1 ). T h e l i f e c y c le s o f fi s h h e lmin th s a n d th e b io lo g y o f th e i r la rv a l

s tages . In: Parasitology o f Fishes V.A. Dogie l , G.K . Pe t rushe vsk i and Yu. I. Po lyan sk i ,

e d s ) , p p . 1 4 0 -1 7 9 . E d in b u rg h : O l iv e r a n d B o y d .

Gl ic k , B . 1 9 8 6 ) . T h e b u r s a o f f a b r i c iu s . In : Avian Physiology E D. S tu rk ie , e d . ) , p p .

87-1 01 . New York: Spr inger Ver lag .

Goa te r , C .P . and Holm es , J.C . 1997) . Pa ras i te m edia ted na tu ra l se lec t ion In : Host-Parsite

Evolution, G eneral Principles andA vian Models D.H .C la y to n a n d J . Mo o re , e d s ) , p p .

9 -2 9 . O x fo rd : Ox fo rd Un iv e r s i ty P re s s .

G o d w i n , H . a n d C o n w a y , V .M . 1 9 3 9 ). T h e e c o l o g y o f a r a is e d b o g n e a r T r e g a r o n ,

C a rd ig a n s h i re . Journal o f Ecology 2 7 , 3 1 3 -3 5 9 .

Gr im e s , L .R . a n d M i l le r , G .C . 1 97 6) . S e a s o n a l p e r io d ic i ty o f th re e s p e c ie s o f c a ry o p h y l -

lae id ces todes in the c ree k chubsucker ,

Erimyzon oblongus

M itch i l l ) , in No rth C aro l ina .

Journal o f Parasitology 62, 434--441.

Grossm an , C .J . 1990) . Are the re under ly ing imm une-en docr ine in te rac tions respon s ib le fo r

imm u n o lo g ic a l s e x u a l d imo rp h i s m ?

Progress in Neuro-endocrine immu nology

3 , 7 5 -8 2 .

Ha le) ,, A.J . 095 8) . Sex d i f fe rence in the res is tance o f hamste rs to in fec t ion wi th the ra t nem-

a tode , Nippostrongylus muris. Experimental Parasitology 7 , 338-348 .




H a l l, D . 1 9 9 8 ) . M e t a l m i n e s u r v e y o f C w m M a w r M i n e o n t h e N a n t L l u e s t n e a r

Pontrhydfendigaid. Technical M emo Reference tmw /97_60, 10 pp. Llanelli, Environm ent

Ag ency , Wales .

Hall , R.D. , Gross, W .B. and Turner, E.C. 1978). Prel im inary observa tions on the north ern

fow l m ite infestat ions on estrog eniz ed roosters and in relation to ini tial eg g pro du ction

in hens. Poultry Science 57, 1088-1090.

H am ilton, W .D. 1980). Sex verus nonse x versu s parasite. Oikos, 35 , 68-76 .

Ha m ilton, W.D. and Zuk, M . 1982). Heri table t rue f itness and bright birds: a role for par-

asi tes? Science 218 , 384-387 .

Ham il ton, W.J. and Poulin , R. 1995). Parasi tes , aggress ion and dom inance in male upland

bullies. Journal ofFish Biology 47 , 302-307 .

Ham ilton, W .J. and Poulin, R. 1997). Th e H am ilton-Z uk hypothesis revisi ted: A me ta-phy s-

ical approach. Behaviour 134 , 299-3 20 .

Ham mar, J . 2000). Cannibals and parasi tes: c onfl ict ing regulators o f bim oda li ty in high lat-

i tude A rct ic charr , Salvelinus alpinus. Oikos 88, 33--47.

Harder, A. , W underlich, F. and Marinovski, P. 1992). Effects of testosterone on Heterakis

spumosa infect ions in m ice. Parasitology 105 , 335-3 42 .

Hardie, L.J. , Fletcher, T.C. and Secombes, C.J. 1994). Effect of temperature on ma crop hag e

ac t iva t ion and the p roduc t ion of macrophage ac t i va t i ng f ac to r by r a inbow t rou t

Onchorhynchus mykiss) leucocytes. Developmental and Comparative Immunology 18,

57--66.

Ha r tvigsen, R. and Kennedy, C.R. 1993). Pat terns in the com posi t ion and r ichness of

helminth c om m uni t ies in the brow n t rout. Journal ofFis h Biology 43 , 603 -615 .

Hasselquist , D. , Marsh, J .A. , Sherman, P.W . and Wingfield, J .C. 1999). Is avian hum oral

imm unoc om petence suppressed by tes tos terone?

Behavioural Ecology and Sociobiology

45 , 167-175 .

Heggberget,T .G. and Johnsen B.O. 1982). Infes ta t ions by Gyrodactylus sp. o f At lant ic

salmon, Salmo salar L., in N orw egia n r ivers. Journal ofF ish Biology 21, 15-26.

Herber t, C. and Coh en, S . 1993). S t ress and im mu ni ty in human s: a meta-analyt ic review.

Psychosomatic Medicine 55 , 364-379 .

Hickey , M .D. and Harr is , J .R. 1947). Prog ress of the Diphyllobothrium ep izoo t i cs a t

Poulaphouca Reservoir . Co. Wickow, Ireland. Journal o f Helminthology 22, 13-28.

Hickman, J .L. 1960). Cestodes o f som e Tasmanian Anura. Annals an d Magazine of Natural

History 13, 1-23.

Hicks , EJ . an d Threl fa ll , W . 1973). M etazoan paras ites of sa lmo nids and coregonids f rom

coas tal Labrador. Journal ofFish Biology 5 , 399-415 .

Hildrew, A.G. and Orm erod, S.J. 1995). Acidification: causes, cons equ ence s and solutions.

In: The Ecological Basis fo r Rive r Management D.M. Harper and A.J .D. Ferguson,

eds) , pp. 1 47 -16 0. Chichester: J oh n W iley.

Hil lgarth, N. and W ingfield, J .C. 1997). Parasi te m ediate d sexual selection; en do crine

aspects . In: Host-Pa ras i te Evolution: General Pr inciples and Avian Models

D.H .Clayton and J .Moore, eds) pp. 78-10 4. O xford: Oxfo rd Un ivers i ty Press .

Hine , P .M . and Kennedy , C .R . 1974) . Th e popula t i on b io logy of t he acan thocepha lan

Pomphorhynchus laevis Miil ler) in the R iver Avon. Journal ofFish Biology 6 , 665-6 79 .

Hirshf ie ld , M.E. , M or in, R.P . and Hepn er , D.J . 1983). Increa sed prevalence of larval

Eustrongylides

N e m a t o d a ) i n t h e m u m i c h o g ,

Fundulus heteroclitus

L . ) f r o m t h e

d i scharge cana l o f a pow er p l an t in t he C hesapeake Bay . Journal of Fish Biology 23,

135-142 .

Ho ffman , G.L. 1998). Parasites o f North Am erican Freshwater Fishes. I t haca and Lond on:

Co m stock Publ i shing A ssocia tes .

Ho ffm an, R. , Kennedy, C.R. and Meder, J. 1986). Effects ofEu bothriu m salvelini Schrank,



1 4 2 J D T H O M A S

1790 on arc tic charr,

Salvelinus alpinus

L.) . in an a lp ine lake .

Journal ofF ish D iseases

9 , t5 3 -1 5 7 .

H o h n , E .O . 1 97 0) . G o n a d a l h o rmo n e c o n c e n t ra t io n s in n o r th e rn p h a la ro p e s in r e l a tio n to

n u p t i a l p lu ma g e .


4 8 , 4 0 0 -4 0 1 .

H o l l a n d , C . 1 9 8 4 ) . In t e ra c t io n s b e tw e e n

Monil i formis

A c a n t h o c e p h a l a ) a n d

Nippostrongylus N e m a to d a ) in th e s ma l l i n t e s t in e o f l a b o ra to ry r at s . Parasitology 88 ,

3 0 5 - 3 1 5 .

Ho lme s , J .C . 1961) . Effec ts o f concurre n t in fec t ions on Hymenolepis diminuta C e s to d a )

a n d

Moniliformis dubius

A c a n t h o c e p h a l a ) . I . G e n e r a l e f f e c ts a n d c o m p a r i s o n w i t h

c ro w d in g .


4 7 , 2 0 9 -2 1 6 .

Ho lme s , J .C . 1962) . Effec ts o f concu rren t in fec t ions on

Hymenolepis diminuta

C e s to d a )

a n d

Monili formis dubius

A c a n th o c e p h a la ) . I I . E f fe c t s o n g ro w th .

Journal of

Parasitology

4 8 , 8 7 -9 7 .

Holm es , J .C . 1973) . S i te se lec t ion by pa ras i t ic he lmin ths : in te rspec ies in te rac t ions , s i te seg-

re g a t io n , a n d th e i r imp o r ta n c e to th e d e v e lo p me n t o f h e lmin th c o m mu n i t i e s .

Canadian

Journal o f Zoology 5 1 , 3 3 3 -3 4 7 .

H o lm e s , J.C . 1 98 2) . Imp a c t o f in fe c tio u s d i s e a s e a g e n t s o n th e p o p u la t io n g ro w th a n d g e o -

g ra p h ic a l d i s t r ib u t io n o f a n im a l s . In :

Population Biology o f Infectious Diseases

R .M.

A n d e rs o n a n d R .M . M a y , e d s ) , p p . 3 5 -7 1 . B e r l in : S p r in g e r V e r l ag .

H o lm e s , J .C . a n d P r i c e , P .W. 1 9 8 6 ). C o m mu n i t i e s o f p a ra si t e s . In : Community Ecology:

Patterns and Process J . K i k k a w a a n d D . J . A n d e r s o n , e d s ), p p . 1 8 7 - 2 1 3 . O x f o r d :

B la c k w e l l S c ie n t i f i c P u b l i c a t io n s .

H o lm e s , J .C . , H o b b s , R .P. a n d L e o n g , T .S . 1 9 7 7 ) . P o p u la t io n p e r s p e c t iv e : c o m mu n i ty

o r g a n i z a t i o n a n d r e g u l a t i o n o f p a r a s i t e p o p u l a t i o n s . I n : Regulation o f Parasite

Populations

G .W. E s c h , e d . ) , p p . 2 0 9 -2 4 5 . N e w Y o rk : A c a d e m ic P re s s .

H o o le , D . 1 9 9 4 ) . T a p e w o rm in fe c t io n in f is h : p a s t a n d fu tu re p ro b le m s . In :

Parasitic

Diseases of Fish

A .W. P ik e a n d J .W. L e w is , e d s ) p p . 1 1 9 -1 4 0 . T re s a i th : S a ma ra

P u b l i s h in g L td .

H o p k in s , C .A . 1 95 9) . S e a s o n a l v a r ia t io n s in th e in c id e n c e a n d d e v e lo p me n t o f th e c e s to d e

Proteocephalusfilicollis

Rud. 1810) in


L.).

Parasitology,

49,

5 2 9 - 5 4 2 .

H o p k in s , S .H . 1 9 3 4 ) . T h e p a p i l lo s e a l lo c re a d i id a e .

Illinois Biological Monograph

13,

1 8 0 .

H o u d e , A .E . a n d T o r io , A . J . 1 9 9 2 ) . E f fe c t o f p a ra s it e in fe c t io n o n m a te c o lo u r p a t t e rn a n d

fe ma le c h o ic e in g u p p ie s .

Behavioural Ecology

3, 346-351.

Ho we l ls , G. , Da lz ie l , T .R.K. , Reader , J .P . and So lbe , J .E 1990) . EIF AC wate r qua l i ty c r i -

t e r i a fo r E u ro p e a n f r e s h w a te r f i s h : r e p o r t o n a lu min iu m.

Chemistry and Ecology 4,

117-173 .

H o w e l l s , G . a n d Mo r r i s , R . 1 9 89 ). C o m me n ta ry a n d c o n c lu s io n s . In :

Ac id Toxicity and

Aquatic Animals

R . Mo r r i s , E .W. T a y lo r , D . J .A . B ro w n , a n d J .A . B ro w n , e d s ) , p p .

2 6 5 -2 7 6 . C a m b r id g e : C a m b r id g e U n iv e r s i ty P re s s .

Hurv i tz , A. , Bercov ie r , H. and VanRijn, J . 1997) . Effec t o f amm onia on the su rv iva l and the

i m m u n e r e s p o n s e o f r a i n b o w t r o u t

Onchorhynchus mykiss,

W a l b au m ) v a c c i na t e d

aga ins t Streptococcus iniae. Fish and Shellfish Immu nology 7 , 4 5 -5 3 .

H u t c h i n s o n , G . E . 1 9 5 7 ). C o n c l u d i n g r e m a r k s .

Co ld Spring H arb or Symposium in

Quan titative Biology

2 2 , 4 1 5 -4 2 7 .

H u tc h in s o n , N . J . a n d S p ra g u e , J.B . 1 9 8 6 ). T o x ic i ty o f t ra c e me ta l m ix tu re s to A me r ic a n

f lagf ish

Jordanellafloridae)

i n s o f t a c id ic w a te r s a n d imp l i c a t io n s fo r c u l tu ra l a c id i f i-

ca t ion .

Cana dian Journal o f Fisheries an d Aquatic Sciences

43, 647--655.

H y n e m a n , D . 1 96 2 ). S tu d ie s o n h e lmin th imm u n i ty I I . In f lu e n c e o f

Hymenolepis nana

C e s to d a : H y m e n o le p id a e ) in d u a l in fe c tio n s w i th

H. diminuta

i n w h i t e m ic e a n d ra t s .




Experimental Parasitology

1 2, 7 -1 8 .

Hy nes , H.B.N, (1960)

The B iology o f PoUuted Waters.

Liverpoo l : L ive rpoo l Univers i ty Press .

I s s e rh o f f, H . , S y lv e s te r, E W . a n d H e ld , W.A . (1 9 8 6 ) . E f fe c t s o f

Schistosoma mansoni

o n

a n d r o g e n r e g u l a t e d g e n e e x p r e s s i o n i n t h e m o u s e .

Molecular and Biochemical

Parasitology 1 8 , 4 0 1 -4 1 2 .

J a c k s o n , J .A . , T in s l e y , R .C . a n d H in k e l , H .H . (1 9 9 8 ). M u tu a l e x c lu s io n o f c o n g e n e r i c

mo n o g e n e a n s p e c ie s in a s p a c e - l im i t e d h a b i t a t.

Parasitology

117 , 563-569 .

Jenk ins , R .A. , W ade , K.R. and Pugh , E . (1984) . M acro in ver teb ra te -h ab i ta t re la t ionsh ips in

the R iver Te ifi ca tchment an d the s ig n if icance to conse rva t ion . Freshwater Biology 14,

2 3 - 4 2 .

Johnsen , B .O. and Jensen , A.J . (1991) . The

Gyrodactylus

s to ry in N o rw a y .

Aquaculture

98,

2 8 8 - 3 0 2 .

Jones , J .G. (1985). D ecom pos i t ion in lake sed iment : bac te r ia l ac t ion and in te rac t ion .

FBA

Annual Report 1985,

p p . 3 1 -4 4 . K e n d a l : T i tu s W i l s o n .

J o n e s , J .R .E . (19 40 ). A s tu d y o f th e z in c -p o l lu te d R iv e r Y s tw y th , N o r th C a rd ig a n s h i re ,

Wa le s .

Annals o f App lied Biology

2 7 , 3 6 8 -3 7 8 .

Jones , J .R .E . (1943). The fauna o f the River Te if i, W es t W ales .

Journal o f Animal Ecology

12 , 15-123 .

Jones , J .R .E . (1949) . A n eco log ic a l s tudy o f the Rive r Rhe ido l , Nor th Ca rd igansh ire , W ales .

Journal o f Animal Ecology 18 , 67-88 .

J o n e s , J .R .E . (1 9 5 8 ). A fu r th e r s tu d y o f th e z in c -p o l lu te d R iv e r Y s tw y th .

Journal o f Animal

Ecology

27 , 1 -14 .

Jones , J .R .E . (1962) . F ish and r ive r po l lu t ion . In :

River Pollution 2: Causes and Effects

(L .K le in , e d . ) , p p . 2 5 4 -3 1 0 . L o n d o n : B u t t e rw o r th a n d C o .

J o n s s o n , B . (1 9 8 9 ) . L i fe h i s to ry a n d h a b i t a t u s e o f N o rw e g ia n b ro w n t ro u t

Salmo trutta).

Freshwater Biology 2 1 , 7 1 -8 6 .

Jonsson , B . G. (2001). A nu l l mo de l fo r random iza t ion te sts o f nes tedness in spec ies a ssem-

b lages .

Oecologia

127 , 309-313 .

Kak a j i , V.L . (1969) . S tud ies on the he lmin th pa ras i te s o f Ind ian f ishes. Pa r t IL S om e t rem atode

parasites of freshw ater f ishes o f U ttar Pradesh.

Indian Journal o f Helminthology

21 , 49-80 .

Ka l leberg , H. (1958). Obse rva t ions in a s t ream tank o f te r r i to r ia l i ty and com pet i t ion in juv e-

n i l e s a l m o n a n d t r o u t

Salmo salar

L . a n d

S.trutta

L.) .

Rep ort of the Institute o f

Freshwater Research Drottningholm 3 9 , 5 5 -9 8 .

Kearn , G.C. (1998) .

Parasitism a nd the Platyhelminthes.

L o n d o n : C h a p ma n a n d H a l l .

Ke l ly , M . (1988) .

Mining and the Freshwater Environment.

L o n d o n : E l s e v i e r A p p l i e d

Sc ience .

K e n n e d y , C .R . (19 6 8) . P o p u la t io n b io lo g y o f th e c e s to d e Caryoph yUaeus laticeps (Pa l la s ,

1781) in dace

Leuciscus leuciscus

L . o f th e R iv e r A v o n .

Journal of Parasitology

54,

5 3 8 - 5 4 3 .

K e n n e d y , C .R . (1 9 7 0) . T h e p o p u la t io n b io lo g y o f h e lmin th s o f B r i t is h f r e s h w a te r f i sh . In :

Aspects of Fish Parasitology

(A .E .R . T a y lo r a n d R . Mu l le r , e d s )

Symposium of the

Brit ish Society of Parasitology

8 , p p . 1 4 5 - 1 5 9 . O x f o r d : B l a c k w e l l S c i e n t i f ic

P u b l i c a t io n s .

K e n n e d y , C .R . (1 9 7 2) . T h e e f fe c t s o f t e mp e ra tu re a n d o th e r f a c to r s u p o n th e e s t a b l i s h me n t

a n d s u rv iv a l o f


( A c a n t h o c e p h a l a ) i n g o l d f is h ,

Carrasius aura-

tus. Parasitology

6 8 , 2 8 3 -2 9 4 .

K e n n e d y , C .R . (19 74 ). P o p u la t io n b io lo g y o f p a ra s i t e s w i th s p e c ia l re fe re n c e to th e e f fe c ts

o f e c o s y s te m c h a n g e s d u e to h u ma n a c t iv i ty .

Proceedings of the First International

Congress o f Ecology,

4 pp .

K e n n e d y , C .R . (1 9 7 5) . T h e d i s t r ib u t io n o f s o m e c ru s ta c e a n f i s h p a ra s i te s in B r i t a in in r e l a -

t io n to th e in t ro d u c t io n a n d mo v e me n t o f f r e s h w a te r f i s h .

Journal of the Institute of



1 4 4 J D T H O M A S

Fishery M anagement 6, 36-41.

Ken nedy, C.R. (1977). Th e regulation o f fish parasite populations. In: Regulation o f Parasite

Populations (G.W. Esch, ed. ), pp. 63 -10 9. New York: Ac adem ic Press.

Kennedy, C.R. (1978a). Studies on the bio log y o f Eubothrium salvelini and E. crassum

(Ces toda :Pseudophyl l i dae ) i n r es iden t and migra tory Salvelinus alpinus and Salmo

trutta and in S. salar in Nor th No rwa y and in the i slands of Spi tsbergen and Jan M ayen.

Journal ofFish Biology 12, 147-162.

Kennedy, C.R. (1978b). The parasi te faun a of resident c harr Salvelinus alpinus f rom A rc t ic

islands, with special refe rence to Bea r Island. Journal ofF ish Biology 13 , 457 -466 .

Kennedy, C.R. (1978c). A n analysis o f the me tazoa n parasitocoenoses of brow n trout Salmo

trutta

fro m B rit ish lakes.


13 , 255 -263 .

Kennedy, C .R. (1983). Problem s of disease assessm ent in natural f ish pop ulat ion s: a po pu -

l a t ion eco lo g i s t s v i ew of d ip los tomias i s . Proceedings o f the Firs t International

Conference o f lchthyoparasitology, Ceske Budejovice,

pp. 46-47.

Kennedy, C .R. (1985). Si te aggre gation by species o f Ac anth oc eph ala in f ish, with special

referen ce to eels, Anguilla anguilla. Parasitology 90 , 375 -390 .

Kennedy , C .R . (1992) . F i e ld ev idence fo r i n t e rac t i ons be tween the acan thocepha lans

Acanthocephalus anguillae and A. lucii in eels, Anguilla anguilla. Ecological

Parasitology 1, 122-134.

Kenned y , C .R . (1994) . Th e eco log y of i n troduc t ions . In : Parasit ic Diseases of Fish

(A.W.Pike and J.W. Lewis, eds) , pp. 189-208. Tresai th: Samara Publishing Ltd.

Kennedy, C.R. (1995). T he ec olog y of f i sh paras ites : the impact of paras ites on ec osystems.

IVth International Symposium o f Fish Parasitology. Program and Bo ok o f Abtracts, p.

18. M unich: Univers i ty o f Munich.

Ken nedy, C.R. (1996). Establishme nt, survival and site selection o f the ces tod e

Eubothrium

crassum in brow n trout, Salmo trutta. Parasitology 112 , 347-3 55 .

Kennedy, C.R. (1997). Freshwater fish parasites and environmental quality: an overview and

caution. Parassitologia 39 , 294-254 .

Kennedy, C.R. , Bush, A.O. and Ah o, J.M. (1986) . Patterns in helminth com m uni t ies : why

are f ish an d birds different? Parasitology 9 3 , 2 0 5 - 2 1 5

Kennedy, C.R .and Fitch, D.J. (1990). Colonizat ion, larval survival and epid em iolog y o f the

n e m a t o d e Anguillicola crassus in the eel, Anguilla anguilla, in Britain. Journal ofFish

Biology 36, 117-131.

Kennedy, C.R. an d Gu tgan , J .E (1996) . The num ber of niches in intes tinal helminth co m -

muni t ies ofAnguilla anguilla: are there e no ug h spaces fo r parasites? Parasitology 113,

2 9 3 - 3 0 2 .

Kennedy, C .R.an d Hartvigsen, R.A. (2000). Rich ness and diversity o f intestinal m etaz oan

com mu ni t ies in brown t rout, Salmo trutta com pared to those of eels , AnguiUa anguilla

in their Eu rop ean heart lands. Parasitology 121, 55-64.

Kennedy, C.R. and Hine, P .M . (1969) . Po pulat ion biolog y of the ces tode Caryophyllaeus

laticeps (Pallas) in the R iver Av on. Journal ofFish Biology 1 , 209-21 9 .

Kennedy, C.R., Laffoley, D.d A., Bishop, G., Taylor, M. and Jones, P. (1986). Structure and

organ isat ion of paras i te com m uni t ies of f reshwater f i sh of Jersey, Cha nnel I s lands .

Journal ofFish Biology 29 , 215-226 .

Kennedy, C.R., Nie, P., Kaspers, J. and Paulisse, J. (1992). Are eels Anguilla ang uilla L.)

planktonic feeders? Eviden ce f rom parasi te com mu ni t ies .


41,

5 6 7 - 5 8 0 .

Kenned y , C .R . and Ru mp us , A . (1977) . Lo ng t e rm chang es i n t he s i ze o f the

Pomphorhynchus laevis (Acanthocephala) population in the Rive r Avon. Journal ofFish

Biology 10, 35-42.

Kenned y , C .R . an d Walker, P . J . ( 1969). Ev iden ce fo r an imm une r esponse b y dace ,




Leuciscus leuciscus t o in fe c t io n s b y th e c e s to d e Caryophyllaes laticeps. Journal of

Parasitology

5 5 , 5 7 9 -5 8 2 .

Ke n n e d y , C .R . , Wy a t t , R . J . a n d S ta r r, K . 1 9 9 4 ). T h e d e c l in e a n d n a tu ra l r e c o v e ry o f a n

unm anaged coarse f i she ry in re la t ion to changes in land use an d a t tendan t eu t roph ica t ion .

In: Rehabilitation o f Freshwater Fisheries I .G. Cox , ed . ), pp . 366-375 . Ox ford : F ish ing

N e w s B o o k s .

Kh a n , R .A . a n d T h u l in , J . 1 9 9 1 ) . In f lu e n c e o f p o l lu t io n o n p a ra s i t e s o f a q u a t i c an ima l s .

Advances in Parasitology 311, 20 1-2 38 .

K le in , S .L . 2 0 0 0 a ) . T h e e f fe c ts o f h o rmo n e s o n s e x d i ff e re n c e s in in fe c tio n : fro m g e n e s to

behav iour . Neuroscience and Biobehavioural Reviews 2 4 , 6 2 7 -6 3 8 .

K le in , S .L . 2 0 0 0 b ) . Ho rm o n e s a n d ma t in g s y s te ms a f fe c t s e x a n d s p e c ie s d i f f e re n c e s in

imm u n e fu n c t io n a mo n g v e r t e b ra te s.

Behavioural Processes

51 , 149-166 .

K le in , S .L . , Ha i r s to n , J .E . , De Vr ie s , A .C . a n d Ne l s o n , R . J . 1 9 9 7 ). S o c ia l e n v i ro n me n t a n d

s te ro id h o rm o n e s a f fe c t s p e c ie s a n d s e x d i f f e re n c e s in imm u n e fu n c t io n a mo n g v o le s .

Hormones and Behaviour

3 2 , 3 0 -3 9 .

K le in , S .L a n d Ne l s o n , R . J. 1 9 9 7 ) . S e x d i f f e re n c e s in immu n o c o m p e te n c e d i f f e r b e twe e n

t w o

Peromyscus

spec ies .

American Journal o f Physiology - Regulatory Integrative an d

Comparative Physiology 4 2 , R 6 5 5 - R 6 6 0 .

Kle in , S .L a n d Ne l s o n , R . J. 1 9 9 8 ). S e x a n d s p e c ie s d i f f e re n c es in c e l l -me d ia te d imm u n e

respon ses in vo les . Canadian Journal o f Zoology 7 6 , 1 3 9 4 -1 3 9 8 .

K le in , S .L . a n d Ne l s o n , R . J. 1 9 9 9 ). S o c ia l i n t e ra c tio n s u n m a s k s e x d i f f e re n c e s in h u mo ra l

imm u n i ty in v o le s.

Animal Behaviour

5 7 , 6 0 3 -6 1 0 .

Kn u d s e n , R . , Kr i s to f fe rs e n , R . a n d Am u n d s e n , P .A . 1 9 9 7 ) . P a ra s it e c o mm u n i t i e s in two

sym patr ic morp hs o f Arc t ic charr ,

Salvelinus alpinus

L.) , in nor the rn No rway .

Canadian

Journal o f Zoology

7 5 , 2 0 0 3 -2 0 0 9 .

K u p e r m a n , B . I . 1 9 9 3 ). F i s h p a r a si t e s as b i o i n d i c a t o r s o f w a t e r p o l l u t io n .

Canadian

Translation o f Fisheries and Aqua tic Scien ces

N o . 5 5 9 8 , 6 p p . O t t a w a , N a t i o n a l

R e s e a rc h C o u n c i l .

Ku r i s , A .M a n d L a f fe r ty , K .D . 1 9 9 4 ). C o m m u n i ty s t ru c tu re : la rv a l t r e ma to d e s in s n a i l

hosts .

Annual Review o f Ecology an d Systematics

25 , 187-217 .

L a n d ry , R .C . a n d K e l s o , W .E . 1 99 9) . P h y s ic o c h e m ic a l in f lu e n c e s o n p a ra s i t e s o f a g e -0

l a r g e m o u t h b a s s i n t h e A t c h a f a l a y R i v e r B a s i n , L o u i s i a n a .

Journal of Freshwater

Ecology

1 4, 5 1 9 -5 3 3

L a n d s b e rg , J .H . , B la k e s le y , B .A . , R e e s e , R .O . , M c R a e , G . a n d F o rs t c h e n , E R . 1 9 9 8 ) .

Paras i te s o f f i sh as ind ica to rs o f env ironmenta l s t re ss . Environmental Monitoring and

Assessment

5 1 , 2 1 1 -2 3 2 .

Lang ley , R . and Fa i r ley , J .S . 1982) . Seaso na l va r ia t ions in the in fes ta t ions o f pa ras i te s o f

w o o d m o u s e

Apodemus sylvaticus

p o p u la t io n s in th e W e s t o f I r e l a n d .

Journal o f Zoology

198 , 249-261 .

L a s s i e r e , O . L . 1 9 8 8 ). H o s t p a r a s i te r e l a t i o n s h i p s b e t w e e n l a r v a l

Sialis lutaria

M e g a l o p t e r a ) a n d Neoechinorhynchus rutili A c a n t h o c e p h a l a ) Parasitology 97 ,

3 3 1 - 3 3 8 .

L a s s i e re , O .L . a n d C ro mp to n , D .W.T . 1 98 8) . E v id e n c e o f p o s t - c y c l i c t r a n s mis s io n in th e

l i f e -h i s to ry o f Neoechinorhynchus rutili Ac a n th o c e p h a la ) Parasitology 9 7 , 3 3 9 -3 4 3 .

Lead abrand , C .C. and Nick o l , B .B. 1993) . E s tab l ishment , su rv iva l , s i te se lec t ion and deve l-

o p m e n t o f

Leptorhynchoides thecatus

i n l a r g e m o u t h b a s s ,

Micropterus salmoides.

Parasitology

106 , 495-501 .

L e e s , E . 1 9 6 2 ). T h e i n c i d e n c e o f h e l m i n t h p a r a s i t e s i n a p a r t i c u l a r f r o g p o p u l a t i o n .

Parasitology

5 2 , 9 5 -1 0 2 .

Lees , E . and Bass , L . 1960) . Sex horm ones as a poss ib le fac to r in f luenc ing the leve l o f pa r-

as i t iza t ion in f rogs .

Nature London

188 , 1207-1208 .



146 J D THOMAS

L e ig h , W.H . 1 9 6 0 ). T h e F lo r id a G a r , a s th e in t e rme d ia te h o s t fo r Odhneriotrema incom-

modum Leidy , t 856) f rom Alligator mississippiensis. Abstrac t , Journal o f Parasitology

46 5 ,Sec t io n 2 ) 16.

Lem ly , A.D . and Esch , G.W. 1985) . B lack spo t caused by Uvulifer am bloplitis T re ma to d a )

a mo n g ju v e n i l e c e n t ra rch id s in th e P ie d m o n t a re a o f N o r th C a ro l in a . Proceedings o f the

Helm inthological Society of Washington 5 2 , 3 0 -3 5 .

LeM orvan , C . , Trou taud , D. and Descha ux , E 1998) . D if fe ren t ia l e f fec ts o f temp era tu re on

spec i f ic and non-spec i f ic imm une de fences in f ish . Journal o f Experimental Biology 201,

1 6 5 -1 6 8 .

Li l jed a l , S . , Fo ls tad , I . and Sk ars te in , F . 1999) . Seco nda ry sex t ra i t s , pa ras i te s , im m uni ty

and e jacu la te qua l i ty in the Arc t ic charr . Proceedings o f the Royal Society of London

Series B. Biological Sciences 266 , 1893-1898 .

L o p e z , S . 1 9 98 ). A c q u i re d re s i s ta n c e a ffe c ts ma le s e x u a l d i s p la y a n d fe m a le c h o ic e in g u p -

p ies .

Proceedings of the Royal Society of London Series B. Biological Sciences

265 ,

7 1 7 - 7 2 3 .

Lotz , J .M . and Font , W .E 1991) . T he ro le o f pos i t ive and nega t ive in te rspec ies a ssoc ia t ions

in th e o rg a n iz a t io n o f c o mm u n i t i e s o f h e lmin th s o f b a t s .

Parasitology

103 , 127-138 .

L o tz , J .M. a n d F o n t , W .E 1 9 9 4 ). E x c e s s p o s it iv e a s s o c ia t io n s in c o mm u n i t i e s o f in t e s t in a l

h e lmin th s o f b a t s : a r e f in e d n u l l h y p o th e s i s a n d a t e s t o f th e f a c i l it a t io n h y p o th e s i s .

Journal of Parasitology 80, 398--413.

Lyo ns, K.M . 1978). The Biology o f Heminth Parasites. Stud ies in Bio lo gy no . 102 . Londo n:

E d w a r d A r n o l d .

M a c K e n z ie , K . a n d G ib s o n , D . 1 9 7 0 ) . E c o lo g ic a l s tu d ie s o f s o me p a ra s i t e s o f p l a i c e ,

Pleuronectes platessa L ) a n d f lo u n d e r Platichthys flesu s L). Symposium of the British

Society o f Parasitology

8 , 1 -47 .

M a c K e n z i e , K . , W i l l ia m s , H . H . , W i l l i a m s , B . , M c V i c a r , A . M . a n d S i d d a l l , R . 1 9 9 5) .

P a ra s it e s a s in d ic a to r s o f w a te r q u a l i ty a n d th e p o te n t i a l u s e o f h e lmin th t r a n s mis s io n in

ma r in e p o l lu t io n s tu d ie s. Advances in Parasitology 35 , 86-144 .

M agurran , A.E . 1988) . Ecological Diversity and its M easuremen t. L o n d o n : C r o o m H e l m .

M ahoney , R . 1966) . Laboratory Techniques in Zoology. L o n d o n : B u t t e rw o r th P re s s .

M a p e s , C . J. a n d C o o p , R .L . 1 9 7 l ) . E f fe c t o f c o n c u r re n t a n d t e rmin a te d in fe c t io n s o f

Haemonchus contortus

o n th e d e v e lo p m e n t a n d re p ro d u c t iv e c a p a c i ty o f

Nematodirus

battus. Journal of Comparative Pathology 8 1 , 4 7 9 - 4 9 2 .

M arcog l iese , D.J . and Cone , D.K. 1996) . On the d is t r ibu t ion and abundance o f ee l pa ras i te s

in N o v a S c o t i a : i n f lu e n c e o f p H .

Journal o f Parasitology,

8 2 , 3 8 9 -3 9 9 .

M a r g o l i s , L . a n d M o r a v e c , E 1 9 8 2 ). Ramellogammarus vancouverensis B o u s f i e l d

A m p h i p o d a ) a s a n i n t e r m e d i a t e h o s t f o r s a l m o n i d p a r a s i t e s i n B r i t i s h C o l u m b i a .

Canadian Journal o f Zoology 60 , 1100-1104 .

M a s o n , B . J . 1 9 9 2 ) .

Acid Rain: Its Causes and its Effects on Inland Waters.

O x f o r d :

C la re n d o n P re s s .

M ason , C .E 1996) . Biology of Freshwa ter Pollution. H a r l o w : L o n g m a n G r o u p .

M c C u rd y , D .G . , S h u t le r , D . M u l l i e , A . a n d F o rb e s , M.R . 1 9 9 8 ) . S e x -b ia s e d p a ra s i t i s m o f

av ian hos ts : re la t ions to b loo d pa ras i te taxon and the m at ing sys tem.

Oikos

8 2 , 3 0 3 -3 1 2 .

M c L e n n a n , D .A . a n d S h i re s , V .L . 1 99 5) . C o r re l a t io n b e tw e e n th e l e v e l o f in fe c t io n w i th

Buno dera inconstans and Neoechinorh ynchus rutili a n d b e h a v io u ra l in t e n s i ty in f e m a le

b ro o k s t i c k le b a c k s .


8 1 , 6 7 5 ~ 5 8 2 .

M c M i l l a n , D .N . a n d S e c o m b e s , C .J . 1 99 7) . I s o la t io n o f r a in b o w t ro u t Onchorhynchus

mykiss) i n t e s t in a l in t r a e p i th e l ia l l y mp h o c y te s IE L ) a n d m e a s u re me n t o f th e i r c y to to x ic

activity . Fish and Shellfish Immunology 7 , 5 2 7 -5 4 1 .

Merret,W.J., Rutt, G.E , W eatherley, N.S ., Thom as, S.P. and Orrnerod, S.J. 1991). Th e respons e

of macroinvertebrates to low pH and increased a lum inium concentra tions in Welsh s treams:




multiple episo des and chro nic exposure. Archivfiir Hydrobiologie 121, 115-125.

Merri tt , S.V. and Pratt , I . 1964). Th e l ife history ofNeoechinorhynchus rutili an d its devel-

opm ent in the intermediate host Acan thocepha la: Neo echinorhy nchidae) .

Journal of

Parasitology 51J, 39 4-4 00 .

M etcal fe , J .L . 1989). B iological water qual i ty assessme nt of running wa ters base d on

macroinvertebrate com m unit ies: history and presen t status in Eu rope. Environmental

Pollution 60 , 101-139 .

Met tr ick, D .E 1975). Correla tions betwee n the amino acid poo ls of Hymenolepis diminuta

and the rat intestine. Canadian Journal of Zoology 53 , 320-331 .

Miller , R.S. 1967). Pat tern and proces s in com peti t ion. Advances in Ecological Research

4 1-74 .

M o,T.A. 1994). S ta tus of Gyrodactylus salaris problems and r esea rch in Norway . In :

Parasitic Diseases ofFish A.W.Pike and J.W. Lew is, eds) , pp. 43-5 6. Tresaith: S am ara

Publ i shing Ltd.

M¢ller , A .E 1997). Parasit ism and the evo lut ion o f ho st l i fe history. In: Host-Parasite

Evolution: General Principles andAvian Models. D.H. C layton and J . M oore, eds), pp.

195-2 27. Ox ford: Oxfo rd Univers i ty Press .

M ol loy, S . , Hol land, C. and Poole , R. 1993). Helm inth parasi tes of brown and sea trout,

Salmo trutta L. f rom the West coast o f Ire land. Bio logy and environment. Proceedings

of the Royal Irish Academy 93B, 137-142 .

M orand, S . , Poulin , R. , Rohd e, K. and Hay wa rd, C. 1999). Agg regat ion and species co ex-

istence o f ectoparasites o f m arine f ishes.

International Journal for Parasitology

29,

6 6 3 - 6 7 2 .

M oravec , E 1982) . A con t r ibu t ion to t he b iono m ics o f Crepidostomum metoecus

Trematoda: Allocreadiidae).

Vestnik Ceskoslovenske Spolecnosti Zoologiske

46, 15-24.

M orave c, E 1994). Parasitic Nematodes of Freshwater Fishes of Europe. Dordrech t :

Kluw er Aca dem ic Publ ishers .

M oravec , E and Scholz , To 1994) . Seasona l occur rence and matura t i on of

Neoechinorhynchus rutili

Aca nthoceph ala) in barbel,

Barbus barbus

Pisces) o f the

J ih l ava R iver , Czech Republ i c . Parasite - Journal de la Societ~ Francaise de

Parasitologie 1 , 271-2 78 .

Morley, N.J. , Crane, M. and Lewis, J .W . 2001a). Toxicity of cadm ium an d zinc to miracidia

o f

Schistosoma mansoni. Parasitology

122, 81-85.

Mo r l ey , N . J . , Crane , M . and Lew is , J .W. 2001b) . Toxic i t y o f cad m ium and z inc t o

Diplostomum spathaceum

Trematoda: Diplotomatidae) cercarial survival.

International

Journal for Parasitology 31 , 1211-1217 .

M oss, B. 1988). Ecology of Freshwaters: Man and Medium. Oxford: Blackwell Scientif ic

Publications.

M un iz, I .E 1991). Freshw ater acidif icat ion: i ts effects on species and com m un it ies of

freshwater microbes, plants and animals. In: Acidic Deposition: Its Nature and Impacts

ET. Las t and A. Wat l i ng , eds ) , pp . 227-254 . Edinburgh : The Roya l Soc i e ty o f

Edinburgh.

M unro, A.D. and Pi tcher, T .J. 1985). S teroid horm one s and agonis t ic behav iour in a c ich-

lid teleost,

Aequidens pulcher. Hormones and Behaviour

19 , 353-3 71 .

M uzzal l , EM . 1980). Ec olog y and seasonal abund ance of three acanthoc ephalan species

in fec t ing whi t e sucker s i n sou th-eas t New Hampshi r e .


66,

127 - 1 33 .

Nelson , R.J. and Dem as, G.E. 1996). Season al chan ges in imm une funct ion. Quarterly

Review of Biology 71 , 511-5 48 .

Nelson , R.J ., Dem as, G.E. and Klein, S .L . 1998). Ph otoper iodic mediat ion of seasonal

breeding and immune function in rodents: a multifactorial approach. American Zoologist



148 J D THOMAS

38, 226-237.

No lan, EM ., Hill , G.E. and Stoehr, A.M.(1998). Sex, size and plum ag e redness pred icts

ho use f inc h survival in an epidemic. Proceed ings o f t he Royal Soc i e t y o f London S er i es

B. Biological Sciences 265 , 961 -965 .

Nt il ler, W. (1928) . Z u we lchem T rematoden gehOrt Cercaria arhopalocerca N/311er 1925 .

Si t zungs Berichte der Gesel l schaf t Naturforschender Freunde zu Berl in 1927 8-10 ,

162-164 .

No rm an, J .R. , revised b y Gree nw ood , P.H. (1963). A His tory o f Fishes. Lon don : Ernest Ben

Ltd.

No r tham, J .I . and Ro cha, N .E (1958) . O n the s ta ti st ical analys is of wo rm cou nts in chick-

ens. Exp erimen tal Parasi tology 7 , 428-4 38 .

Okland, J. (1990). La kes and Snail s. Oestergeest , Netherlands: W.Backhyus.

Okland, J . and Okland, K .A. (1986). Th e effect o f acid depo si t ion on ben thic animals in

lakes and streams. Experient ia 42 , 471-4 86 .

O Sullivan,T.N. , Smith, J .D. an d Thom as, J.D. (1989). Cop per molluscicides for the control

o f schistosomiasis. Effects of inorganic com plex es on toxici ty. Environmental Science

and Technology 23 , 1101-1106 .

Paling, J .E . (1965). Th e populat ion dy nam ics of the m ono gen ean gi ll paras ite Discocotyle

sagittata on W indermere t rout, Salm o trut ta L. Parasi tology 55 6 6 7 - 6 9 4 .

Paling, J .E . (1969) . T he m anne r o f infect ion of t rout gil ls by the m ono gen ean paras ite

Discocotyle sagi ttata. Journ al of Zoology, L ond on 159 , 293-3 09 .

Park, T. (1954). Exp erim ental studies o f interspecies com peti t ion. II . Temperature, hum id-

i ty and co mp et i tion in two species o f Tribolium. P hysiological Zoolog y 27, 177-238.

Pelegt i , S .P . and Blackburn, T .H. (1995) . Effects of Tubi fex tubi fex (Ol igochae t a :

Tubificidae) on N -m ineral iza t ion in freshw ater sediments, m easu red with 15N isotopes.

Aqu at ic Microbial Ecology 9 , 289-2 94 .

Petter , A.J. (1966). Equil ibre des esp~ces dans les populat ions de nematodes parasi tes du

co lon des tortues terrestres. M~moires Museum Nat ional d His tor ie Naturel le 39, 1-252.

Phipps, G.L . , Mattson, V .R. and Ankley, G.T. (1995). Relative sensit ivi ty o f three fres hw a-

t e r ben th i c macro inver t ebra t es t o t en con taminan t s . A r c h i v e s o f E n v i r o n m e n t a l

Contamination an d Toxicology 28 , 281-286 .

Picke ting, A.D . (1977). S easonal c han ges in the epidermis o f the brow n trout , Salm o trutta

L . Journal o fF i sh B io logy 10 , 561-5 66 .

Picke ting, A.D. (1989). Environmental stress and the survival of the brow n trout , Salmo

trut ta . Fresh wa ter Biology 21 , 47-55 .

Picke ting, A.D . and Christie,P. (1980). Sexual differences in the incide nce and severi ty o f

ectoparasitic infestation o f the brow n trout, Salmo t ru tta L . Journal o fF i sh B io logy 16,

6 6 9 - 6 8 3 .

Picketing, A .D. and Pottinger, T.G. (1985). Cortisol can increase the susceptibility o f bro w n

trout, Salm o trut ta L., to disease w ithou t redu cing the white blo od cel l cou nt . J o u r n a l o f

Fish B iology 27 , 611-619 .

Picketing, A.D . and Pottinger, T.G. (1987). Lym ph oc yto pen ia and interrenal act ivi ty d uring

sexual maturation in the brow n trout, Salmo t rut ta L . Journ al ofFish Biology 30, 4 1 - 5 0 .

Piet rock, M. , Mat theis , T . , Kr iger , R. and Meinel t , T . (1999) . Seasonal dynamics of

P h y l l o d i s t o m u m f o l i u m (von Olfers, 1916) (Trematoda, Gorgoderidae) in blue bream,

Abram is ba l l e rus (L.) and the ruffe, Gymnocephalus cernuus (L .) f rom the Od er River

(Germany/Poland). Acta Parasi tologica 44, 165-169 .

Pike, A.W. and Lewis, J .W. (1994). Parasi tic Disea ses ofFish . Tresaith: Sam ara Publishing

Ltd.

Porter , M.J.R. , R andall, C.F., Bro m age , N.R . and Thorpe, J .E. (1998). T he role o f melatonin

and the pineal gland o n the develop me nt and smol ti fication of Atlant ic sa lmon (Sa lmo




salar parr. Aqu acultu re 168 , 139-155 .

P o t t in g er , T .G . an d C ar r i ck , T .R . (2 0 0 0 ) . C o n t ras t in g seaso n a l mo d u la t io n o f t h e s t r e s s

resp o n se in ma le a n d fem ale r a in b o w t ro u t. Journal ofFis h Biology 5 6 , 6 6 7 -6 7 5 .

P o t t in g er , T .G . an d P ick er in g , A .D . (1 9 8 5 a) . C h an g es in th e sk in s t ru c tu re as so c ia t ed w i th

e lev a ted an d ro g en l ev e l s i n m a tu r in g ma le b ro w n t ro u t,

Salmo trutta L. Journal ofF ish

Biology 2 6 , 7 4 5 -7 5 3 .

P o t t in g er, T .G . an d P ick er in g , A .D . (1 9 8 5 b) . T h e e f fec t s o f 1 1 -k e to tes to s t e ro n e an d t e s to s -

t e ro n e o n th e sk in s t ru c tu re o f b ro w n t ro u t, Salmo trutta L. General and Com parative

Endocrinology

5 9 , 3 3 5 -3 4 2 .

P o u l in , R . (19 9 2) . T o x ic p o l lu t io n an d p a ras i t i sm in f r esh w ate r f ish . Parasitology Toda y 8,

5 8 - 6 1 .

Poul in , R . (1996) . He lmin th g rowth in ver tebra te hosts : Does hos t sex m at ter? International


2 6 , 1 3 1 1 -1 3 1 5 .

Poul in , R . (1998) .

Evolutionary Ecology o f Parasites: Fr om Individuals to C omm unities.

L o n d o n , C h ap man an d H a l l .

P o u l in , R . (19 9 9) . P a ras i t i sm an d sh o a l s i ze in ju v en i l e s t i ck leb ack s : co n f l i c tin g p ressu res

f ro m d i f f e ren t ec to p aras i t e s . Ethology 105 , 959-968 .

P o u l in , R . (2 0 0 0 ). V ar i a tio n in th e in t r asp ec i f i c r e l a t io n sh ip b e tw een f i sh l en g th an d in t en -

s i ty o f p a ra s i t e i n fec t io n : b io lo g ica l an d s t a t i s t ica l cau ses . Journal ofFish Biology 56 ,

1 2 3 -1 3 7 .

Poul in , R . (2001 a) . In teract ions betw een specie s and the s t ructu re o f helm in th comm uni t ies .

Parasitology 122, 3- S 11.

P o u l in , R . (2 0 0 1 b ) . A n o th er lo o k a t t h e r i ch n ess o f h e lmin th co m mu n i t i e s in t ro p ica l f r e sh -

wa ter f i sh . Journal o f Biogeography 2 8 , 7 3 7 -7 4 3 .

P o u l in ,R . , C u r ti s , M.A . an d R au , M .E . (1 9 9 1 ) . S i ze , b eh av io u r, an d acq u i s i t i o n o f ec to p ar -

as i t i c co p e p o d s b y b ro o k t ro u t ,

Salvelinusfontialis. Oikos

61 , 169-174 .

P o u l i n , R . a n d G u t g a n , J . E ( 2 0 0 0 ) . N e s t e d n e s s , a n t i n e s t e d n e s s , a n d t h e r e l a t i o n s h i p

b e tw ee n p rev a len ce an d in t en s i ty in ec to p aras i t e a s semb lag e s o f mar in e f i sh : a sp a t i a l

mo d e l o f sp ec ies co ex i s t en ce . International Journal of Parasitology 3 0 , 1 1 4 7 -1 1 5 2 .

P o u l in , R . , Marsh a l l , L . J . an d S p en cer , H .G . (20 0 0) . G en e t i c v a r i a t io n an d p rev a len ce o f

b lo o d p a ras i t e s d o n o t co r re l a t e am o n g b i rd sp ec ies . Journal o f Zoology 2 5 2 , 3 8 1 -3 8 8 .

Poul in , R . and Val tonen , E .T . (2001) . Ne sted asse m blage s resu l t ing f rom ho st s ize var ia t ion :

th e case o f en d o p aras i t e co mmu n i t i e s in f i sh h o s t s . International Journal o f Parasitology

3 1 , 1 1 9 4 -1 2 0 4 .

P u k k in en , K . an d V a l ton en , E.T. (19 9 9) . A cc u m u la t io n o f p l e ro ce rco id s o f

Triaenophorus

crassus i n th e seco n d in t e rmed ia t e h o s t Coregonus laveratus an d th e i r e f f ec t o n th e

g ro w th o f th e h o s t . Journal ofF ish B iology 55 , 115-126 .

R ab erg , L . , G rah n , M . , H asse lq u i s t , D . an d S v en sso n , E . (1 9 9 8 ) . O n th e ad ap t iv e s ig n if i -

can ce o f s t r e s s -in d u ced imm u n o su p p ress io n .

Proceedings of the R oyal Society of London

B. Biological Sciences 265 , 1637-1641 .

R ah k o n en , R . , A a l to , J . , K o sk i , E , S a rk k a , J . an d Jun tu n en , K . (1 9 9 6) . C es to d e l a rv ae

Diphyllobothrium dendriticum as a cau se o f h ea r t d i sease l ead in g to m o r ta l i t y in h a tch -

e ry r ea red sea an d b ro w n t ro u t . Diseases of Aquatic Organisms 25 , 15-22 .

R ah k o n en , R . an d K o sk i , E (19 9 7) . O ccu r ren ce o f ces to d e l a rv ae in b ro w n t ro u t a f t e r s to ck -

in g in l a rg e r eg u la t ed l ak e in n o r th e rn F in lan d . Diseases of Aquatic Organisms 31 ,

55--63.

R aw so n , M.V . an d R o g ers , W .A . (1 9 7 2 a). T h e se aso n a l ab u n d an ce o f A n cy ro ce p h a l in ae

(Mo n o g en ea ) in la rg em o u th b ass in W al t e r E G eo rg e R ese rv o i r . Proceedings o f the

Helminthological Society of Washington 39 , 159-162 .

R a w s o n , M .V . a n d R o g e r s , W . A . ( 1 9 7 2 b) . S e a s o n a l a b u n d a n c e o f a n c y r o c e p h a l i n a e n

( M o n o g e n o i d e a ) p a r a s it e s o f b l u e g i ll , Lepomis macrochirus (Raf.) . Journal o f Wildlife



150 J D THOMAS

Diseases

8 , 174-177 .

R e a d , C.P . 1 9 5 6 ). C a r b o h y d r a t e m e t a b o l i s m o f

Hymenolepis diminuta. Experimental

Parasitology

5 , 3 2 5 -3 4 4 .

R e a d e r , J .E a n d De m p s e y , C .H . 1 9 8 9 ). E p i s o d ic c h a n g e s in wa te r q u a l i ty a n d th e i r e f f e c t s

on f ish . In :

Acid Toxicity and Aquatic Animals

R . M o r r i s , E .W. T a y lo r , D . J .A . B ro wn

a n d J .A .B ro wn , e d s ) , p p . 6 7 -8 4 . C a m b r id g e : C a m b r id g e Un iv e r s i ty P re s s .

R e im c h e n , T .E . a n d N o s i l , E 2 0 0 1 ). E c o lo g ic a l c a u s e s o f s e x -b ia s e d p a ra s i t i s m in th ree -

sp ine s t ick leback .

Biological Journal of the Linnean Society

73, 51~53.

R ic h a rd s , G .R . a n d C h u b b , J .C . 1 9 9 6 ) . Ho s t r e s p o n s e to in i ti a l a n d c h a l l e n g e in fec t io n s ,

fo l lo win g t r e a tme n t , o f

Gyrodactylus bullatarudis

a n d

G. turnbulli

M o n o g e n e a ) o n th e

g u p p y

Poecilia reticulata). Parasitological Research

8 2 , 2 4 2 -2 4 7 .

R ic h a rd s o n , D . J. a n d N ic k o l , B .B . 1 9 9 9 ). P h y s io lo g ic a l a t t rib u te s o f th e p y lo r i c c a e c a a n d

an te r io r in tes t ine o f g reen sunf ish

Lepomis cyanellus)

p o te n t i a l ly in f lu e n c in g m ic ro -

h a b i t a t s p e c i f i c i t y o f


A c a n t h o c e p h a l a ) .

Comparative

Biochemistry and Physiology A - Molecular and Integrative Physiology

122 , 357-384 .

Rick le fs , R .E . 1973) .

Ecology.

L o n d o n : T h o ma s N e l s o n a n d S o n s.

R ig g s , M.R . a n d E s c h , G .W. 1 98 7) . T h e s u p ra p o p u la t io n d y n a m ic s o f

Bothriocephalus

acheilognathi

i n a N o r th C a ro l in a c o o l in g r e s erv o i r : a b u n d a n ce , d i s p e r s io n a n d p re v a -

lence .


7 3 , 8 7 7 -8 9 2 .

R o b e r t s o n , J. 1 9 5 3 ) . T h e p a ra s it e s o f b ro wn t ro u t

Salmo trutta

L . ) a n d o th e r f r e s h wa te r

f ish .

Unpublished report of the Brown Trout Research laboratory,

S c o t ti s h H o m e

Dep ar tme nt , pp 1 -30 . BTS C. 81 34 . FW .53) .

R o h d e , K . 1 9 9 1 ). In t r a s p e c i fi c a n d in t e r s p e c i f i c in t e ra ct io n s in lo w d e n s i ty p o p u la t io n s in

resourc e r ich hab i ta ts .

Oikos

6 0 , 9 1 -1 0 4 .

Roh de , K. 1998) . Is the re a f ixed num ber o f n iches fo r endop aras i te s o f f i sh?

International


28 , 1861-1865 .

Rong a , E . 1995) . The eco logy , pa tho logy and t rea tment o f


Leuckar t ,

1842) in an in tens ive aquacu l tu re sys tem. Ph .D. Thes is , Univ ers i ty o f L ive rpo o l .

Ru ssell , L.R . 1980). Effects of

Truttaedacnitis truttae

Nem atoda : CucuUanidae) on g rowth

a n d s w i m m i n g o f r a in b o w t r o u t,

Salmo gairdneri. Canadian Journal of Zoology

58,

1 2 2 0 -1 2 2 6 .

S a d le r , K . a n d L y n a m, S . 1 98 6) . S o m e e f fe c ts o n th e g ro wth o f b ro wn t ro u t fro m e x p o s u re

to a lu m in iu m a t d i f f e re n t p H l e v e ls .

CERL Report TPRDI_/I_/2982/R96.

L e a th e rh e a d ,

S u r rey , UK: C e n t ra l E le c t r i c i ty R e s e a rc h L a b o ra to r i e s .

S c h a d , G .A . 1 96 2) . He lm in th p a ra s i t i s m in a f lo c k o f d o me s t i c g e e s e in t ro d u c e d to a rc t i c

s u mm e r c o n d i t io n s in C a n a d a .


40 , 1 -4 .

Schad , G.A. 1963a). Nich e d ive rs i f ica t ion n a pa ras i te spec ies f lock .

Nature

198, 404--406.

S c h a d , G .A . 1 9 6 3 b ). T h e e c o lo g y o f c o -o c c u r r in g c o n g e n e r i c p in wo rms in th e to r to i s e

Testudo graeca. Proceedings of the XVI International Congress of Zoology

1 , 2 2 3 - 2 2 4 .

S c h a d , G .A . 1 96 6) . Imm u n i ty , c o m p e t i t io n a n d n a tu ra l r e g u la t io n o f h e lmin th p o p u la -

t ions .

American Naturalist

10 , 359-364 .

S c h a lk , G . a n d F o rb e s , M .R . 1 9 97 ). M a le b ia s e s in p a ra s i ti s m o f ma mm a ls : e ff e c ts o f s tu d y

type , hos t age , and p a ras i te taxon .

Oikos

7 8 , 6 7 -7 4 .

Scha l l , J .J . and S taa ts , C .M . 1997) . Pa ras i te s and the evo lu t ion o f ex t ravaga n t m ale char-

ac te rs :

Anolis

l i z a rd s o n C a r ib b e a n i s l an d s a s a t e s t o f th e Ha m i l to n - Z u k h y p o th e s i s .

Oecologia

111 , 543-548 .

S c h in d le r, D .W. 1 9 8 6 ). T h e s ig n i f i c a n c e o f in - l a k e p ro d u c t io n o f a lk a l in i ty .

WaterAir and

Soil Pollution

3 0 , 9 3 1 -9 4 4 .

S c h lu te r , D . 1 9 94 ). E x p e r im e n ta l e v id e n c e th a t c o mp e t i t io n p ro m o te s d iv e rg e n c e in a d a p -

t ive rad ia t ion .

Science

2 6 6 , 7 9 8 -8 0 0 .

Scholz ,T . 1999) . Pa ras i te s in cu l tu red and fe ra l f i sh .

Veterinary Parasitology 84,

3 1 7 - 3 3 5 .




S eco m b es , C .H . an d C h ap p e l l , L .H . (1 9 9 6 ) . F i sh imm u n e resp o n ses to ex p er im en ta l an d

n a tu ra l i n fec t io n w i th h e lm in th p a ras i t e s . Annual Review ofF ish Diseases 6 , 167-177 .

S h er id an , L .A .D . , P o u l in , R . , W ard , D .E an d Z u k , M . (2 0 0 0 ) . S ex d i f f e ren ces in p a ras i t ic

in fec t io n s amo n g a r th ro p o d h o s ts : i s th e re a ma le b i as ? Oikos 8 8 , 3 2 7 -3 3 4 .

S h y k o f f , J .A . a n d S ch m id t -H emp e l , P. (19 91 ). G en e t i c r e l a t ed n ess an d eu so c ia l i t y : p a ras i t e -

m e d i a t e d s e l e c t i on o n t h e g e n e t i c c o m p o s i t i o n o f g r o u p s. Behavioural Ecology and

Sociobiology

2 8 , 3 7 1 -3 7 6 .

S i lv e r , B .B . , D ick , T .A . an d W elch , H .E . (1 9 8 0 ) . C o n cu r ren t i n fec t io n s o f Hymenolepis

diminuta

a n d

Trichinella spiralis

i n th e r a t i n t es t in e .


66 ,

786--791.

S in g h , D .K an d A g arw al , R .A . (1 9 86 ). P ip e ro n y l b u to x id e sy n erg i sm w i th tw o sy n th e t i c

p y re th ro id s ag a in s t Lymnaea acuminata. Chem osphere 1 5, 4 9 3 -4 9 8 .

S la t e r, C .H . an d S ch reck , C .B . (1 9 9 3 ) . T es to s t e ro n e a l t e r s t h e imm u n e resp o n s e o f ch in o o k

s a l m o n ,

Onchorhynchus tshawytcha. General and Comparative Endocrinology

89 ,

2 9 1 - 2 9 8 .

Sm yth, J.D. (1962). Introduction to Anim al Parasitology. L o n d o n : T h e E n g l i sh U n iv er s i t i e s

Press .

S o n n e x , C . ( 1 9 98 ) . I n f l u e n c e s o f o v a r i a n h o r m o n e s o n u r o g e n i t a l in f e c t i o n . Sexually

Transm itted Infections 74 , 11-19 .

S o u sa , W.P . (1 9 9 2 ) . In t e r sp ec ies in t e rac t io n s amo n g l a rv a l p a ras i t e s o f f r e sh w ate r an d

ma r in e sn a i l s . American Zoologist 3 2 , 5 8 3 -5 9 2 .

S p in ed i , E ., S a las , M. , C h i sa r i , A . , P e ro n e , M . , C ar in o , M. an d G a i l l a rd , R .C . (1 9 9 4 ). S ex -

d i f fe r e n c e s i n t h e h y p o t h a l a m o - p i t u i t a ry - a d r e n a l a x i s r e s p o n s e t o i n f l a m m a t o r y a n d

n eu ro en d o cr in e s tr e s so rs - ev id en ce fo r a p i tu i t a ry d e fec t i n th e au to immu n e d i sease - su s -

cep t ib l e f ema le l ew is r a t .

Neuroendocrinology

6 0 , 6 0 9 -6 1 7 .

S r iv as t av a , D . (1 9 9 9 ). U s in g lo ca l - r eg io n a l r i ch n ess p lo t s t o t e s t sp ec ies sa tu ra t io n : p i t f a l l s

an d p o ten t i a l s . Journal of Animal Ecology 86 , 1 -16 .

S tep h en so n , R .R . (1 9 80 ). T h e acu te to x ic i ty o f cy p erme th r in (WL 4 3 4 6 7 ) to th e f r esh w ate r

sh r imp Gam marus pulex) a n d t h e l a r v a e o f t he m a y f l y Cloeon dipterum) in con t inuous

f low tes ts .

Confidential Shell Research Report No.TLGR-80.079,

S i t t in g b o u rn e : S h e l l

R esea rch .

S tep h en so n , R .R . (1 9 8 2 ). A q u a t i c to x ico lo g y o f cy p ermeth r in .1 . A c u te to x ic i ty o f so me

f resh w ate r f i sh an d in v er t eb ra t es in l ab o ra to ry t e s t s.

Aquatic Toxicology

2 , 175-185 .

S to n er , J .H . an d G ee , A .S . (1 9 8 5 ) . E f fec t s o f fo res t ry o n w a te r q u a l i ty an d f i sh in W elsh

r iv e r s an d l ak es .

Journal o f the Institute o f Water Engineers a nd S cientists

3 9 , 2 7 -4 5 .

S to t t , M.K . an d P o u l in , R . (1 9 9 6 ) . P a ras i t e s an d p a ren ta l ca re in ma le u p lan d b u l l i e s

(E leo t r id ae ) . Journal ofF ish B iology 4 8 , 2 8 3 -2 9 1 .

S tu a r t , T .A . (1 9 5 3 ) . S p aw n in g mig ra t io n , r ep ro d u c t io n an d y o u n g s t ag es o f l o ch t ro u t

Salmo trutta L.) . Scientific Investigations o f the Fishery Division o f Scotland 5 , 1 -39 .

S u k h d eo , M.V .K . an d S u k h d eo , S .C . (1 99 4) . O p t im al h ab i t a t se l ec t io n b y h e lmin th s w i th in

th e h o s t en v i ro n m en t . Parasitology 1 09 , 4 1 - 5 5 .

Sures , B . an d S ida l l , R . (1999) . Pomphorhynchus laevis: t h e in t es t in a l acan th o cep h a lan as

a lea d s ink fo r i t s f i sh host .


9 3 , 6 6 -7 2 .

S u r e s , B . , T a r a s c h e w s k i , H . a n d J a c k w e r t h , E . ( 1 9 9 4 ) . L e a d a c c u m u l a t i o n i n


and i t s host .


8 0 , 3 5 5 -3 5 7 .

T a l o n e n , A . , R i t a , H . a n d P e l t o n e n , H . ( 2 0 0 0) . A b u n d a n c e a n d d i s t r i b u t i o n o f

DiphyUobothrium ditremum C rep l in (C es to d a : P seu d o p h y l l id ae ) p l e ro ce rco id s in b en th ic

w h i t e f i sh , i n n o r th e rn F in n i sh L ap lan d . Journal ofFis h Biology 57 , 15-28 .

T h o m as , E , P o u l in , R . , G u eg an , J .F . , M ich a lak i s , Y . an d R en au d , F . (2 0 0 0) . A re th e re p ro s

an d co n s to b e in g p a ras i t i zed ? Parasitology Today 16 , 533-536 .

T h o m as , J .D . (1 9 5 6 ). L i fe -h i s to ry o f Phyllodistomum simile N y b el in . Nature, London 178,



152 J D THOMAS

1004.

Thom as , J .D. 1957) . Occ urrence o f


Braun, 1900) in Brita in .

Nature, London 180 , 1492-1493 .

T h o m a s , J .D . 1 9 5 8 a ). S tu d ie s o n th e s t ru c tu re , li f e h i s to ry a n d e c o lo g y o f th e t r e ma to d e

Phyllodistomum simile

N y b e l in , 19 2 6 G o rg o d e r id a e : G o rg o d e r in a e ) f ro m th e u r in a ry

b la d d e r o f th e b ro w n t ro u t , Salmo trutta. Proceedings o f the Zoological Society of

London 130, 387--435.

T h o m a s , J .D . 1 9 5 8 b ) . S tu d ie s o n


B r a u n ) a n d

C. far ionis

M til le r ) pa ras i te s in Salmo trutta and Salmo salar in B r i ta in . Parasitology 4 8 , 3 3 6 -3 5 2 .

T h o m a s , J.D . 1 9 6 2 ) . T h e fo o d a n d g ro w th o f b ro w n t ro u t (Salmo trutta L . ) a n d i t s f e e d in g

re la t io n s h ip s w i th th e s a lmo n p a r r

(Salmo salar

L . ) a n d th e e e l

(Anguilla ang uilla

L.) in

the R iver Te if i, W es t W ales .


31 , 175-205 .

T h o m a s , J.D . 1 9 6 4 a ). A c o m p a r i s o n b e tw e e n th e h e lmin th b u rd e n s o f ma le a n d fe ma le

brown t rou t ,

Salmo trutta

L . f ro m a n a tu ra l p o p u la t io n in th e R iv e r T e if i , W e s t W a le s.

Parasitology

5 4 , 2 6 3 -2 7 2 .

T h o m a s , J .D . 1 9 6 4 b ). S tu d ie s o n p o p u la t io n s o f h e lmin th p a ra s i t e s in b ro w n t ro u t (Salmo

trutta

L.).


3 3 , 8 3 -9 5 .

Tho ma s , J.D. 1964c) . S tud ies on the g rowth o f t rou t ,

Salmo trutta

f ro m fo u r c o n t ra s t in g

hab i ta ts .

Proceedings o f the Zoological Society o f London

142 , 459-509 .

T h o m a s , J .D . 1 96 5) . S tu d ie s o n s o m e a s p e c ts o f th e e c o lo g y o f Mesocoelium monodi, a

t r e ma to d e p a ra s i t e o f r e p t i l e s a n d a m p h ib ia .

Proceedings of the Royal Society o f London

145 , 471-494 .

T h o ma s , J .D . 1 96 6 ). S o m e p re l im in a ry o b se rv a t io n s o n th e f a u n a a n d f lo ra o f a s ma l l ma n -

ma de lake in the W es t Afr ic an savanna .

Bulletin de l Institut Fran~a is d Afrique Noire 28

A ) , 5 4 2 - 5 6 2 .

Thom as , J .D. 1997) . Th e ro le o f d is so lve d o rgan ic mat te r , pa r t icu la r ly f ree am ino ac ids and

h u m ic s u b s ta n c e s , i n f r e sh w a te r e c o s y s te ms .

Freshwater Biology

38 , 1 -36 .

Thom as , J.D., Lou gh , A.D. and Lod ge , R .W. 1975) . The chem ica l eco log y

of Biomphalaria

glabrata

Say) , the sna i l hos t

ofSchistosoma mansoni

S a m b o n : th e s e a rc h fo r f a cto r s in

m e d ia c o n d i t io n e d b y s n a i ls w h ic h in h ib i t t h e i r g ro w th a n d re p ro d u c t io n .

Journal of

Applied Ecology

1 2, 4 2 1 -4 3 7 .

Tins ley , R .C. 1989) . Th e e ffec ts o f hos t sex on t ransm iss ion success .

Parasitology Today

5 ,

1 9 0 -1 9 5 .

T o k e s h i , M. 1 9 9 9 ) .

Sp ecie s Coexistence: Ecological a nd Evolutionary Perspectives.

O x fo rd : O x fo rd S c ie n c e .

Turpenny , A.W .H. 1989) . F ie ld stud ies on f ishe r ies in ac id wa te rs in the UK . In :

A c i d

Toxicity and Aquatic Animals

R . M o r r i s , E .W. T a y lo r , D . J .A . B ro w n a n d J .A .B ro w n ,

e d s ) , p p . 4 5 -6 6 . C a m b r id g e : C a m b r id g e U n iv e r s i ty P re s s.

U g a n s k i , R . L . a n d N i c k o l , B .B . 1 9 8 2 ). S i t e s e l e c ti o n , g r o w t h a n d s u r v i v a l o f


A c a n th o c e p h a la ) d u r in g a p re p a te n t p e r io d in

Lepomis

cyanellus. Journal o f Parasitology 68 6 8 6 - 6 9 0 .

U g le m , G .L . a n d B e c k , S .M. 1 9 7 2 ). H a b i t a t s p e c i f i c i ty a n d c o r re l a t e d a m in o p e p t id a s e

ac t iv i ty in the acan thoceph a lans

Neoechinorhychus cristatus and N. crassus. Journal o f

Parasitology 58 9 1 1 - 9 2 0 .

U n d e rh i l l , L .G . a n d K a le i t a S u m me rs , B . 1 9 95 ). B lo o d p a ra s it e s in b r ig h t b i rd s : te s t in g th e

H a m i l to n -Z u k h y p o th e s i s in s u b -S a h a ra n A f r i c a w i th a n imp ro v e d s t a t i s ti c a l me th o d .

Ostrich 66,

1 0 -1 4 .

Va ld imarsson , S .K. and M etca l fe , N.B. 1998) . She l te r se lec tion in juve n i le At lan t ic sa lmon ,

o r w h y d o s a lmo n s e e k s h e l te r in w in te r?

Journal ofFish Biology 52

4 2 - 4 9 .

V a l l e s R io s , M.E . a n d R u iz C a m p o s , G . 1 9 9 2 ) . P re v a le n c e a n d in t e n s i ty o f h e lmin th p a ra -

s i tos is f rom the d iges t ive t rac t o f

Oncho rhynchus mykiss

P is ce s : S a lmo n id a e ) f ro m B a ja




California, Mexico. Revista de Biologia Tropical 45 , 579-584 .

Valtonen, E.T. 1979). Neoechinorhynchus rutili MUller, 1780) in the whitefish Coregonus

nasus Pallas sensu Svardson) f ro m the B ay o f Bothnia . Journal o f Fish Diseases 2

9 9 - 1 0 3 .

Venberg, W.B. and Venberg, E J . 1974). M etabol ic pat tern of a t rem atode and i t s host : a

study in the evolution o f phy siolog ical responses. In: Symbiosis in the Sea W.B.Venberg,

ed.) , pp. 161 -172. C olum bia: Univers i ty of Sou th Carolina.

Vidal-Ma rtinez, V .M . an d Kenn edy, C.R. 2000). Potential interactions be tw een the intes-

tinal helminths o f cich lid fish Cichlasoma synspilum from Sou theastern Mexico. Journal

o f Parasitology 86 , 691-695 .

Visco, R.J. 1973).

Eimeria tenella

infe ctio n in testosterone injected chicks.

Journal of

Parsitology 59 , 613-614 .

W aagbo , R. , Glette, J . , Sandnes, K. and Hem re, G. I . 1994). In f luence of die tary carbohy -

drates o n blood-c hem istry, im m un ity and disease resistance in Atlan tic salmon,

Salmo

salar L. Journal ofFish Diseases 17 , 245-25 8 .

W a l k e y , M . 1 9 6 7 ) . T h e e c o l o g y o f Neoechinorhynchus rutili Miiller). Journal of

Parasitology 53 , 795 -801 .

W ang, R . and Be losev ic , M. 1994) . Es t rad io l i nc reases suscep t ib il i ty o f go ldf i sh to

Trypanosoma danilewskyi. Developmental and Comparative Immunology 18, 377-387.

Webster , J . and Ridgway, I . 1994). The applicat ion o f the equil ibrium parti tioning app roach

fo r establishing sediment quality criteria at tw o UK sea disposal an d outfall sites. Marine

Pollution Bulletin 28 , 653-6 61 .

W edekind, C. 1992). Detai led inform ation abo ut parasites revealed by sexual ornam enta-

tion. Proceedings o f the Royal Society London B 247 , 169-174 .

W edekind, C . 1994). M ale choic e and matern al select ion for specific parasi te resistance

before, during and after fertilization. Proceedings of the Royal Society London B 249,

3 0 3 - 3 1 1 .

W edekind, C. and Jakobsen, P.J. 1998 ). M ale-biased suscep tibility to helminth infection: an

experimental test with a cop epo d. Oikos 8 1 , 4 5 8 - 4 6 2 .

Whitfield, P.J. 1979). The Biology o f Parasitism: An Introduction to the Study o f Associated

Organisms. L o n d o n : E d w a r d A r n o ld .

Wil liams, H.H., Col in , J .A. and Halvorsen, O. 1987). B iolog y o f gyroc otyl ideans wi th

e m p h a s i s o n r e p r o d u c ti o n , p o p u l a t io n e c o l o g y a n d p h y l o g e n y . Parasitology 95,

173-207 .

W ill iams, H .H. and Jon es, A . 1994).

Parasitic Wo rms ofF ish.

Lo ndo n: Taylor and Francis .

W ilson, M.R. and Warr , G.W. 1992). F ish imm unog lobul ins and the genes that enco de

them. Annual Rev iew ofF ish Diseases 2 , 201-22 1 .

W isn iewski , W.L . 1958) . Charac t e r i sa t ion o f t he pa ras i t o fauna o f an eu t rophic l ake

Paras i t o fauna o f t he b iocoeno s i s o f Dru zno Lak e - Pa r t 1 ) . Acta Parasitologica

Polonica 6, 1-64.

W oo, P.T.K. 1997). Im m un izat io n again st parasit ic diseases o f f ish. Fish Vaccinology 90,

2 3 3 - 2 4 1 .

Wo od, C.M. 1987). The physio logica l prob lem s of f ish in acid waters. In:

Ac id Toxicity and

Aquatic Animals R. Morr i s , D.J .A. Brown, E .W. Taylor and J .A. Brown, eds) , pp.

125-152 . Soc i e ty fo r Exper imenta l B io logy Seri es . Cam br idge : Cam br idge Univer s it y

Press.

W oodw ard, D.E , Brnmbaug h, W .G., Deloney , A.J. Little, E.E. and Smith, C.E. 1994). Effects

on rainbow-trout fry o f a metal-contaminated diet of benthic invertebrates fro m the Clark

Fork River, Montana. Transactions o f the American Fisheries Society 123, 51-6 2.

W ren, C.D . and Stephenson, G.L . 1991). The effects of acidif icat ion on the accum ulat ion

and to xici ty o f metals to freshwater invertebrates. Environmental P ollution 71 , 205-241 .



154 J D THOMAS

W right , J .E , Furse , M.T. and Arm itage , ED . 1993) . RIV PAC S - a techn ique fo r eva lua t ing

th e q u a l i ty o f r iv e r s in th e U .K .

European Wa ter Pollution C ontrol

3 ,1 5 -2 5 .

W u n d e r l i c h , E , B e n te n , W .E M . , B e t te n h a e u s e r, U . S c h m i t twre d e , A .E a n d Mo s s m a n , H .

1 9 9 2 ) . T e s t o s t e r o n e - u n r e s p o n s i v e n e s s o f e x i s t i n g i m m u n i t y a g a i n s t

Plasmodium

chabaudi ma la r i a . Parasite Imm unology 14 , 307-320 .

Yeom ans , W.E. , Chu bb , J .C . , Sw ee t ing , R .A . , Sm ith , S . and W hit f ie ld , EJ . 1996) . F ish pa r-

a s i t e s a s in d ic a to r s o f e n v i ro n me n ta l d e g ra d a t io n . Institute of Fisheries Management

Annual Study Conference

1996 , 81-119 .

Z e lme r , D .A . a n d Ara i , H .E 1 9 98 ). T h e c o n t r ib u t io n o f h o s t a g e to th e a g g re g a te d d i s t r i-

b u t i o n o f p a r a s i t e s i n y e l l o w p e r c h ,

Perca f lavescen s

f r o m G a r n e r L a k e , A l b e r t a ,

C a n a d a .


8 4 , 2 4 -2 8 .

Z h o k h o v , A .E a n d P u g a c h e v a , M .N . 1 99 8) . S p a t i a l s t ru c tu re o f ma r i t a h e m ip o p u la t io n s in

th e t r e ma to d e

Phyllodistomum elongatum

T re ma to d a : Go rg o d e r id a e ) : a b u n d a n c e a n d

d is t r ibu t ion in popula t ion s o f f ive f i sh spec ies .

Russian Journal o f Ecology

2 9 , 4 1 6 -4 2 1 .

Zuk , M. 1992) . T he ro le o f pa ras i te s in sexua l se lec t ion : curren t ev idence and fu tu re d i rec -

t ions .

Advances in the Study of Behaviour

2 1 , 3 9 -6 8 .

Zuk , M. and Mc Kea n , K.A. 1996) . Sex d i f fe rences in pa ras i t ic in fec t ions : pa t te rns and

p ro c e s s e s .

International Journal o f Parasitology

2 6 , 1 0 0 9 -1 0 2 3 .



iology of the Schistosome Genus

r i c hob i l h a r z i a

P. H o r a k 1, L . K o l ~ o v 2 a n d C . M . A d e m a 3

1Department o f Parasitology, Charles University, Vini n6 7, CZ-12844

Prague 2, Czech Republic

2Department of Tropical Medicine, 3rd Clinic o f Infectious and Tropical

Diseases, Faculty Hospital Bulovka, Charles University, CZ-12800 Prague 2

and Institute fo r Postgraduate Medical Education, Rusk6 85, CZ-10005

Prague 10, Czech Republic

3Department o f Biology, University o f New Mexico, 167A Castetter Hall,

Albuquerque, NM 87131-1091, USA

A b s tr a c t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 56

1. I n t ro d u c t io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 56

2. L if e C y c le s a n d H o s ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 57

2 .1. G e n e r a l l if e c y cl e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 7

2 .2 . Exp e r i m e n ta l l if e cyc l e s a n d in vitro c u l t iv a t i o ns . . . . . . . . . . . . . . . . . . . . . 1 59

3. S y s t e m a t i c s o f t h e G e n u s richobilharzia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 6 0

3 .1 . I n t r o d u c t o r y n o t e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 60

3 .2 . H i s to r ic a l o v e r v i e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161

3 .3 . D i a g n o s i s o f t h e g e n u s richobilharzia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 6 3

3 .4 . M a i n d i a g n o s t i c c r i te r ia ; t r a d i t io n a l a n d n e w a p p r o a c h e s i n s p e c i e s

d i a gn o s is . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 63

3 .6 . F in al n o t e s o n s y s t em a t i c s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 75

3 .6 . O v e r v i e w o f s p e c ie s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 76

4. D e v e l o p m e n t in I n t e rm e d i a t e H o s t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 78

4 .1 . H o s t - f i n d i n g a n d p e n e t r a t i o n b y m i r a c i d i a . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 78

4 .2 . I n t r a m o l l u s c a n d e v e l o p m e n t : s t a g e s a n d i n f e c t io n c o u r s e . . . . . . . . . . . . . 181

4 .3. E f fe c ts o n t h e s n ai l h o s t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 82

4 .4 . I n t e r na l d e f e n c e r e a c t i o n s o f s n a il i n t e r m e d i a t e h o s t s . . . . . . . . . . . . . . . . . 1 83

5. D e v e l o p m e n t in V e r t e br a t e H o s t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

5 .1 . H o s t - fi n d in g . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 7

5 .2 . P e n e t r a t i o n o f t h e v e r t e b r a t e s k in . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 87

5.3. C e r c a r i a - s c h i s t o s o m u l u m t r a n s f o r m a t i o n a n d i m m u n e e v a s i o n . . . . . . . . 1 90

5.4. M i g r a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 90

6. V e r t eb r a t e I m m u n e R e s p o n s e a n d P a t h o l o g y . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 96

6 .1 . C o m p a t i b l e h o s t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 96

A D V A N C E S I N P A R A S I T O L O G Y V O L 5 2 Copyright © 2002 Elsevier Science Ltd

0 0 6 5 3 0 8 X ll rights of reproduction in any form reserved



15 6 P. HOR /~K L. KOl. .h l~OV ~ A N D C.M . AD E M A

6 .2 . I n c o m p a t i b l e h o s t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203

7 Epidemiology of Cercarial Dermatit is 208

7 1 Distribution 209

7 .2 . E p i d e m i o l o g y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 0

7 3 Identif ication of potential transmiss ion sites for cercarial dermatitis . . . . . 2 1 1

7 .4 . C o n t r o l . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 3

7 .5 . P r o p h y l a x i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 4

8 . C o n c l u s i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . 2 1 5

A c k n o w l e d g e m e n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 6

References

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 6

A B S T R A C T

richobilharzia

is the largest genus within the family Schistosomatidae, cov-

eting o ver 40 sp ecies of avian parasites. To clarify the existing confusion in the

systemat ics of the genus, w e recomm end combining know ledge of l i fe cycles

and developm ental stages, snail/bird hosts , cytog enetical and mo lecular data

together w ith mo rpholo gical cri teria for the characterization of part icular

species. The high specifici ty of

richobilharzia

for the intermediate host is a

likely reflection of the ability to avoid the internal defence of specific snails.

The sp ectrum of final hosts birds) seems to be much wider. The infection of

birds - trichobilharziasis - m ay lead to consid erable tissue injuries, cause d by

eggs of the parasite or migration of immature/mature worm s through the body.

Mo s t richobilharzia visceral species) migrate through the viscera of the

host, but nasal species display a neurotropic mo de o f migration. Du e to a low

specif ic i ty of penetrat ing cercariae , mamm als inc luding humans) can be

attacked. This leads to cercarial dermatitis, predominantly in sensitized hosts.

Exper imenta l infec t ions indica te tha t richobilharzia never mature in an

incom patible mam malian) host . How ever, not al l cercariae and schistoso-

mula are necessarily trapped and eliminated in the skin, and parasites may

migrate throughout the viscera and the nervous system o f mam mals. These

findings suggest that the pathogenicity of

richobilharzia

may have been

underestimated in the past and health risks associated with trichobilharziasis

nee d to be studied further.

1 I N T R O D U C T I O N

Schistoso mes are evolutionarily successful parasitic flatw orms that are unusual

amon g flukes becau se they are dioecious and inhabit the circulatory system of

vertebrates. The parasites are best know n as hum an p athogens in tropical and

subtropical countries over 200 million peo ple suffering from schistosom iasis;



BIOLOGY OF TRICHOBILH RZI 57

WHO estimation). A recent discovery revealed that they parasit ize not only

wa rm-b loode d vertebrates mam mals and birds) , but also reptiles, i .e . croco-

diles

Griphobilharzia;

Pla t t e t

al.,

1991).

Compared to mammalian schis tosomes, represented by the wel l -known

genus

Schistosoma,

the genera that infect birds m ay se em to be o f less impor-

tance. H owever, as parasites o f birds, the mem bers o f

Trichobilharzia

the

largest genus of the fam ily Schistosom atidae) caus e trichobilharziasis of ducks

and geese Wojcinski et aL, 1987; Graczyk et al., 1993), a disease comparable

with schistosom iasis in humans. F rom a medical viewpoint, these parasites are

the causative agent of cercarial dermatitis in humans, an inflamm atory reaction

of the skin which is now considered as an emerging disease de Genti le et al.,

1996). M oreover, schistosom ula of

Trichobilharzia

spp. have been repeatedly

repor ted f rom the lungs and other organs of mammals , inc luding nervous

tissue in the case of T. regenti. The obligatory migration of the lat ter parasite

through the central nervous sy stem of birds and mam mals is occasion ally

associated with neurom otor disorders. Clearly, such properties justify contin-

ued attention towards these rather underestimated infections.

The last review of Trichobilharzia was published nearly 20 years ago Blair

and Islam, 1983). This paper provides updated information on the genus,

including descriptions of new species, their molecular characterization, dis-

coveries in parasite behaviou r host-finding), penetration of the host skin,

imm une evasion by the parasite , parasite migration and associated pathology

in vertebrate hosts, and new data on outbreaks of cercarial dermatitis.

2 LIFE CYCLES AN D HOSTS

2 1 General Life Cycle

The members of

Trichobilharzia

have a tw o-host life cycle similar to that of the

related genus

Schistosoma,

with water snails and birds as the intermediate

and final hosts , respe ctively Figure 1). W here as the cercarial larvae of

Trichobilharzia spp. released from water snails are encountered relatively fre-

quently in conn ection w ith outbreaks of cercarial dermatitis, reports describing

adult wo rm s are rare. This is partly due to the fact that Trichobilharzia adults

possess a thin, threadlike body 20- 100 pm diameter) and live hidden inside

the host . The adult worm s can b e recovered only by m eans o f a complica ted

examination of birds. Co nsequently, reports on these flukes from birds are lim-

ited and data on the l ife cycles are known mainly from experimental infections

of both the intermediate and the f inal hosts.

The cy cle starts with the eggs. The ma ture and fertilized fem ale depend ing

on the species, located either in the visceral organs or in the nasal m ucos a of



158 P. HOR, .K, L. KOLAROV., . AND C.M. AD EM A

Figure 1

The life cycle o f

Trichobilharzia

sp. The miracidium leaves the egg either in

water or in the nasal host tissues) and infects an appropriate intermediate snail host. Inside,

the parasite multiplies asexually. The resulting life stage, cercariae, emerges from the snail

and searches for the final host - a bird. Once the bird is found, the cercariae penetrate the

skin and develop into schistosomula. The parasite then migrates to a preferred location

within the host, where sexual maturation, mating and egg laying take place.

the host ) conta ins a s ingle egg. A s imi lar s i tua t ion wi th o nly one u ter ine egg i s

w e l l k n o w n f ro m o t h e r s c h i s t o s o me s , e . g .S ,

manson i

see Loker , 1983) .

Usual ly , the egg of v iscera l

Trichobilharzia

i s deposi ted in the c i rcula t ion

capil laries) of the final host and needs to pass throu gh differe nt t issues in order

to reach the lum en o f t he in t e s tine and , subsequen t ly , l eave the hos t w i th

faeces . In the nasa l species o f

Trichobilharzia

eggs are dep osi ted in the nasa l

mucosa . The eggs ma tu re w i th in the hos t and the re l eased eggs con ta in fu l ly

deve lope d mirac id ia tha t a re ab le to ha tch . As an ex cept ion , mirac id ia o f nasa l

sch i s tosomes , e .g .T , regenti hatch from the eggs wi th in the host t i ssues and

awai t water contac t Hor~ik

et al .

1998a). S imi l a r behav iour can be exp ec ted

f rom o the r nasa l sch i s tosomes and indeed , mi rac id i a o f T .

arcuata

hatch in

contac t wi th e i ther water or physio logica l sa l ine Is lam, 1986b) . Not a ll l a rvae

reach the ou t s ide env i ronmen t . Some eggs a re t rapped in the t i s sues , where

they t r igger host reac t ions granulom as) and are dest royed.

Onc e in the water , the mirac id ium leaves the egg and search es for the in ter-

me dia te host , i .e . a wate r snai l. Th e l i fe span of mirac id ia of T.

szidati

i s about

20 h at 20 °C Neuhaus, 1952a). Th e species of

Trichobilharzia

usual ly have a

na r row spec i f i c ity towards the in t e rmed ia t e hos t , u s ing on ly one o r c lose ly

re la ted) snail species for la rval developm ent . Upo n f inding a proper mol lus can

hos t, t he m i rac id ium pene t ra t e s and deve lops in to a mothe r spo rocys t i n t he




he ad - fo o t r eg ion o f the sna il . The l a t te r s t age p rodu ces daugh te r spo ro cys t s

wh ich l eave the hea d- fo o t r eg ion and mig ra te to the hepa topancreas wh ere fu r-

the r deve lopm en t w i th sub sequen t r e lease o f ce rca riae con t inues. The p repa ten t

pe r iod w i th in the sna il s i s va r iab le abo u t 3 - 10 we eks ) and dep ends on s evera l

f ac to r s , inc lud ing t empera tu re . De ta i l s on sna i l - f ind ing and in t r amol luscan

deve lopm en t a re p rov ided in s ec t ion 4 .

I t is hypo th es ized tha t a s e t o f spec ia l ized g lands s e rves fo r the pas sage o f

cerc ar iae through the snai l t i s sues for T.

s z i da t i

see Neu haus , 1952a) in o rde r

to l eave the snai l. On ce in the w a te r, the ce rca r iae n eed to f ind and in fec t a

p rope r f ina l hos t qu ick ly b ecau se o f the i r sho r t l i f e span . I f a ve r teb ra te hos t i s

foun d the ce rca r iae pene t r a te the sk in, t r ans fo rm to s c h i s tosom ula and s ta r t to

migra te to the p re fe r r ed loca t ion fo r egg l ay ing . Depend ing on the pa ras i t e

spec ies , tw o d i f fe ren t rou tes a re em plo yed to r each these p laces : mig ra t ion v ia

the b lood c i rcu la t ion o r pas sage th rough the ne rvous t is sues pe r iphera l ne rves

and the cen t r a l ne rvo us sys tem ) . Th e f i r s t rou te i s typ ica l fo r v i s ce ra l spec ies

e .g .T . f r an k i , T . e l v ae ; t he second one i s u sed by the nasa l s ch i s tosome T .

regent i . Deta i l ed in fo rmat ion r egard ing hos t - f ind ing , pene t r a t ion , mig ra t ion

and as so c ia ted pa tho log ies i s p resen ted in s ec t ions 5 and 6 .

2 2 E x p e r i m e n t a l L i fe C y c le s a n d

n V i t r o

C u l t i v a t i o n s

A s m e n t i o n e d a b o v e , c e rc a r i ae o f T r i c h o b i l h a r z i a spp . a re f r equen t ly encou n-

te red in the env i ronm en t . Ho wev er , th i s s t age lacks d i s t ingu i sh ing charac te r s

and the m orpho log ica l cha rac te ri za t ion o f o the r deve lopm en ta l s tages p r ima-

r i ly adu l t s ) i s neces sa ry fo r spec ies d iagnos i s . Fo r tuna te ly , pa ras it e l i f e cyc les

can be r ea l i zed exper ime n ta l ly i f a p rope r f ina l hos t b i rd ) can be s e lec ted .

F requen t ly , b i rds o f the f am i ly Ana t idae r ep resen t a su i tab le hos t. B i rds can be

in fec ted pe rcu tan eou s ly by expo s ing the fee t to ce rca r iae ) or , in som e cases,

b y a p p l y i n g c e r c a ri a e p e r o r a l ly M a c y e t a l . , 1955). W i th com pat ib le in te rm e-

dia te snai l ) and f inal b i rd) hos ts avai lable in the laboratory , the w ho le l i fe

c y c l e c a n b e m a i n t ai n e d e x p e r i m e n t a l l y f o r m a n y y e a r s M e u l e m a n e t a l . ,

1984b) . The f eas ib i l i ty o f ma in ta in ing pa ras i t e l i fe cyc les can be r es t r ic ted by

1 ) l a w s i n t e n d e d t o p r o t e c t a n i m a l s , w h i c h d o w n - r e g u l a t e o r p r o h i b i t t h e

b reed ing o f exper im en ta l ducks and o the r b i rds and 2 ) f a i lu re o f long- te rm

main tenance o f sna i l s in the l abora to ry due to unknown reasons . As f a r a s

T r i c h o b i l h a r z i a

spp . f rom Europe i s concerned , hos t sna i l s such as

L y m n a e a

s t a g n a l i s

and

S t a g n i c o l a

spp . , and r ecen t ly a l so

R a d i x p e r e g r a / R , o v a t a , a re

eas i ly kep t in the labora to ry . By co mpar i son , the m ain tenance o f R . aur i c u l ar i a

and o the r sna il s phys id and sm al l p lanorb id spec ies ) i s m ore d i f fi cu lt .

T h e r e a r e s e v e ra l p o s s i b l e w a y s t o s i m p l i fy t h e e x p e r i m e n t a l c y c l e a n d t o

r e p l a c e c e r t a i n p h a s e s o f t h e s n a i l - p a r a s i t e c o - e x i s t e n c e . L a r g e l y , t h e s e

a p p r o a c h e s a i m t o a v o i d u n d e s i r a b l e p r o p e r t i e s o f t h e m o l l u s c a n h o s t t h a t




pa tho log ies caused by pene t ra t ing an d mig ra t ing worm s) . Cerca r i a l de rmat i t i s

i s s o m e t i m e s a s s o c i a t e d w i t h s u b s e q u e n t g e n e r a l iz e d s y m p t o m s . I t c a n n o t b e

e x c l u d e d t h a t s u c h s y m p t o m s a r e s p e c i e s - r e l a t e d , d e p e n d i n g o n p a r a s i t e

s p e c i e s - s p e c i f i c ) a n t i g e n s , s u r v i v a l , a n d m i g r a t i o n w i t h i n v e r t e b r a t e s .

A l thou gh l im i ted da ta a r e ava i l ab le on m ig ra t ion o f pa r ti cu la r spec ies o f v i s -

c e r a l

Trichobilharzia

a n d c l i n i c a l c o n s e q u e n c e s , i t i s e v i d e n t t h a t n a s a l

s ch i s tosomes T .

regenti

invade the ne rvous t i ssues o f b i rds and ma m m als and

m ay cau se neu rom oto r d i so rde r s inc lud ing pa ra lys is ) .

How ever , the iden t i fi ca t ion o f

Trichobilharzia

specie s is ve ry d i f f icu l t wo rk ,

c o m p l i c a t e d b y t h e e x i s te n c e o f s y n o n y m s , i n c o m p l e t e d e s c r i p ti o n s o r i n c o r-

r e c t p a ra s i t e i d e n t i f i c a ti o n s e .g . l i b e r a l a n d i n c o r r e c t u s e o f th e n a m e T.

ocellata -

s e e b e l o w ) . I n th e i r t h o r o u g h r e v i e w o f t h e t a x o n o m y , B l a ir a n d

I s la m 1 9 8 3 ) n o te d th a t se v e r a l s y n o n y m s a n d i n c o m p l e t e d e s c ri p t io n s o c c u r

a m o n g t h e 4 0 s p e c i e s o f

Trichobilharzia.

His to r i ca lly , th i s m ay in pa r t be du e

to the po or desc r ip t ion o f the type spec ies , T.

ocellata.

A l t h o u g h t h e c e r c a r ia e

we re iden t i fi ed by La Va le tt e in 1855 , and the co r respond ing adu l t s by B rum pt

in 1931, there i s s ti ll no c on sen sus on w hat T.

ocellata

and

Cercaria ocellata

ac tua l ly is Oden ing , 1996 ; s ee be low ) . A t p resen t, the re i s no dou b t tha t the

spec ies compos i t ion w i th in the genus needs majo r r ev i s ion .

3 2 H i s to r ic a l O v e r v i e w

Trichobilharzia

w as desc r ibed for the f ir s t t ime a t the larval cercar ia l) s tage by

La Valett e 1855) w ho charac te r i zed Cercaria oeellata f r o m Lymnaea stagnalis

co l l ec ted nea r Ber l in in Germ any . Subsequen t ly , the ce rca r iae w ere r epor ted by

severa l o ther au thors e .g . Ss in itzin, 1910) , even f rom oth er in termed ia te hos ts ,

e .g . f rom Radix ovata see Math ias , 1930 ; Wesenberg -Lund , 1934) , o r f rom

mu l t ip le lym nae id , phys id , p lanorb id and hydrob id /b i thy n id sna i ls K i l i a s and

Fr ick , 1964; van den Broc k , 1965). The adu l t worm s w ere found by Skr jab in

a n d Z a k h a r o v 1 9 2 0 ) i n R u s s i a i n t h e v i sc e r a l b l o o d v e s s e l s o f a d uc k . T h e

sch i s tosom e wa s nam ed as T . kossarewi and a new genu s , Trichobilharzia, w a s

es tab l i shed . In 1931, Brum pt pe r fo rm ed exper imen ta l in fec t ions w i th

C. ocel-

lata

a n d o b t a i n e d a d u l t w o r m s w h i c h w e r e c o n s i d e r e d t o b e i d e nt ic a l t o t h o s e

of T.

kossarewi

Skr jab in and Z akharov , 1920 . D ue to the l aw o f p rio ri ty , the

type spe c ies wa s renam ed T.

ocellata.

Since then , however , dou b t s concern ing

the desc r ip t ion of T. ocellata f rom d i f fe ren t in te rmed ia te hos t s lymn ae ids , o r

even o the r sna il f ami l i e s) have be en r a i sed . The ce rca r iae tha t em erge f rom d i f -

f e r e n t l y m n a e i d s m a y v a r y i n s i z e a n d b e h a v io u r . T h u s , C. ocellata p r o b a b l y

rep resen t s a co l l ec t ive t e rm fo r s evera l spec ies s ee Sz ida t , 19 42 fo r r ev iew) .

I t should be n oted that the d escr ip t ion o f the typ e species , T.

ocellata,

i s con-

f u s i n g f o r s e v e r a l r e a s o n s . 1 )

C. ocellata

La Vale t te , 1855 , a s o r ig ina l ly

d e s c r i b e d s h o w s f e a t u r e s c o m m o n t o a l l

Trichobilharzia

cerca r i ae . The on ly




3 .3 . D i a g n o s i s o f t h e G e n u s r i c h o b i l h a r z i a based on Far ley , 1971;

B la i r an d I s lam , 1983 ; K ha l i l, 2002 )

A m o n g t h e m e m b e r s o f t h e fa m i l y S c h is to s o m a t i d a e a ls o c o m p r i si n g

Schistosomatium, Heterobilharzia, S ch is to so m a , Bivitellobilharzia,

Austrobilharzia, Orientobilharzia, Ornithobilharzia, Macrobilharzia,

Griphobilharzia, Bilharziella, Jilinobilharzia, Gigantobilharzia a n d

Dend ritobilharzia , t h e g e n u s Trichobilharzia i s t he l a r ges t i n t e r ms o f

number o f s pec i e s . I n t he adu l t s t age , ma l e s and f ema l e s a r e s i mi l a r and

thread like . Ora l and vent ra l suckers a re presen t in bo th sexes and the pos te r io r

end o f the bod y i s spa tu la te . The gyn aeco pho r ic cana l is shor t and does no t

ex t end t o t he pos t e r io r end o f t he body . T es te s a r e num er ous , occupy i ng s pace

pos t e r io r to t he gynaeco phor i c cana l on e i the r s ide o f t he com m on caecum .

T he e l onga t e s em i na l ves i c le i s l oca l ized i n t he an t e r io r pa r t o f t he body ,

be t w een t he ace t abu l um and gynaeco phor i c cana l. T he ma l e s pos s ess s ma l l

c i r rus an d the i r gen i ta l pore i s a t the an te r io r end o f the gyn aeco pho r ic cana l .

A n e l onga t e and co i l ed ova r y occu r s i n t he an t e r io r pa r t o f t he f em a l e body .

T he s emi na l r ecep t ac le is w e l l f o r m ed and l ie s i mm ed i a t e l y pos t e ri o r to t he

ovary . The oo type i s an te r io r to the ovary wi th the u te rus opening imm edia te ly

pos te r io r to the ace tabulum . Adul t s a re paras i t es o f b irds .

The pos i t ion and va l id i ty of the genus among o ther sch i s tosomes i s wel l

suppor ted by m olecu lar da ta . Phylog enet ic ana lyses based o n par ti a l s equences

o f 28S r D N A p l ace t he genus o f Trichobilharzia in the c lade o f b i rd sch is to-

som es Sny der and Loker , 2000).

3 .4 . M a i n D i a g n o s t ic C r it e ri a ; T r a d i t io n a l a n d N e w A p p r o a c h e s in

S p e c i e s D i a g n o s i s

Tradi tiona lly , the m orph olog y of par t icu la r deve lopm enta l s tages i s used as a

d iagnos t i c c r it e rion . Arguably , the adul t m orpho logy i s the m os t va luab le char -

acter is t ic for species ident i f icat ion Blai r and Is lam, 1983). Addi t ional ly , eggs ,

m i rac id ia and ce rcar iae can a l so provide d iagnos t i c charac te ri s ti cs . How ever ,

d i f fe ren t spec ies ma y exhib i t very s imi la r morph ologica l f ea tures , and o the r

l i fe cy c le da ta in te rm edia te hos t -spec i f i c ity , l a rva l behaviour , s i t e o f f ina l

l oca t i on w i t h i n b i r d s ) may a l s o be r equ i r ed . T he r e f o r e , any new s pec i e s

descr ip t ion should conta in no t on ly the charac te r s o f adul ts , bu t a l so of o ther

deve lopm enta l s t ages eggs , mi rac id ia , cercar iae) , da ta on spec i f i c i ty towards

interm edia te and f inal hos ts , organ specif ic i ty wi th in bi rds and, facul tat ively,

behav i ou r o f m i r ac id i a and ce r ca ri ae . A dd i t iona l t e chn i ques m ay h i gh l igh t

fur ther d i f fe rences be tw een spec ies , e .g . chae to taxy charac te r iza t ion of sur -

face pap i l l ae of mi rac id ia and cercar iae by s ta in ing wi th s i lver n i t r a te ) and

ka r yo l o gy cha r ac te r iza t ion o f ch r omo s om es in t he m i to t ic m e t aphas e p la te ) .



164 R HOR ~ K L. KOLAI~OVA AND C.M . ADEMA

Recently, molecu lar taxonom y has prov ed to be a powerful tool for diagnosis;

the rDN A o f four species has been sequenced see section 3.4.8.) .

The following overview provides descriptions of the main morphological

structures of particular develo pm ental stages and those that are important for

species identification are discussed. In addition, current knowledge regarding

intermediate hosts, location within birds and karyolog ical and molec ular char-

acterization is summarized.

3.4.1. Eggs

The eggs Figure 2) can be spindle-shap ed T.

paroce llata, T. franki ,

crescen-

tic T. ocellata, T. arcuata or even ovo id T. corvi, T.filiformis . Usually, they

have a projection/small ho ok at one end. At the t ime o f release from the bird,

the eggs already contain a miracidium. In certain cases, the miracidium hatches

from the egg within the bird host T. regenti; see Hor~ik et al., 1998a). Some

species produ ce similar eggs e.g.T. salmanticensis and T. parocellata . Thus,

although the size and shape of eggs are important criteria, they cannot be the

reason for synon ym ization used for T. elvae and T. ocellata by McM ullen and

Beaver, 1945) or spec ies determ ination use d for T. ocellata by S luiters, 1983).

Figure

Shape of the eggs of

Trichobilharzia ocellata

left) an d T.

franki

right). Scale

bar = 30/am. Reproduced w ith permiss ion f rom Kock 2000).




Nevertheless , eggs represent a va luable tool for qu ick ident i f ica t ion of species

wi th d i f fe ren t egg m orpho logy tha t occur sympa t r ica l ly wi th in the same b i rd

host e .g . v iscera l duck schis tosom es of T.

ocel la ta

and T.

f ranki .

3 .4 .2 . Mira cid ia

These py r iform larvae Figure 3) are covered by a mosa ic epi the l ium, com-

posed of in terce l lu lar r idges and c i l ia ted p lates. T he la t te r a re usual ly arranged

in four t iers of 6:9:4:3 = 22 cells . Th is pattern ma y differ in som e species e.g.

6:7:5 :4 = 2 2 in T.

corvi;

seeY. Ito, 1960, cited by Bla ir and Islam, 1983). Two

la te ra l ho rns a re loca ted be tween the f i r s t and second t ie r . The an te r io r

papi l la te rebra tor ium) conta ins te rminal or lateral openings of the penetra tion

glands. Generally, two glan d stuctures are visible: the apical gland one or two

cel ls) and the la tera l g land two ce l ls) . The poster ior par t of the bod y is f i l led

Figure 3

Miracidium of

Trichobilharzia regenti.

General morphology left ) and the

arrangement of ciliated plates right). Scale bar = 25 ~ma. Reproduced with permission

from Hor~k

et al.

1998a).



166 R HORAK L. KOLAROVA AND C.M. ADEMA

with clusters of germ cells these multiply and differentiate to produ ce daugh-

ter sporocysts) . Part icular species possess different numbers of these germ

cell clusters, e.g. one in T.

regenti,

two in T.

ocellata

from Japan, three in

T. corvi.

Some authors doubt the usefulness of miracidial morphology for species

identification, mainly because only a few structures are present to help deter-

minat ion. Usual ly , the ar rangement of ci l iated pla tes, m orph ology of

penetration glands and nu mb er o f clusters o f germ cells were used fo r dist in-

guishing species. Contrary to the report on heterogeneity in the pattern of

ciliated plates in T. indica see Baugh, 1978), we feel that the first two char-

acters m entione d ab ove ma y represent valid criteria. Ho wev er, these cannot be

used as a stand-alone marker in the absence of addit ional information con-

cerning oth er stages or the life cycle. Althoug h considere d valid in the past, the

value of the numb er of groups of germ cells has been diminished b y the obser-

vation that a single mass of germinal cells divided into three groups due to

contraction of miracidia of T. salman ticensis see Simon-Martin and Simon-

Vicente, 1999).

3.4.3. Sporocysts

The sporocyst stage is usually not mentioned in descriptions of species of

Trichobilharzia

an exce ption is, for example, T.

australis;

see Islam, 1986a).

This is based on the fact that no distinguishing features are present and mor-

pholog y does not help in diagnosis. For som e species T.

szidati;

see Neuhaus,

1952a) spination of the anterior end of daughter sporocysts is mentioned.

Bec ause o f insufficient data and the ab sence o f special structures, we regard

sporocysts to b e of low value for species identification.

3.4.4. Cercariae

The apharyn gate ocellate furcocercariae Figure 4) were the f irst stage of

Trichobilharzia that was described C. ocellata La Valette, 1855). Th ey are

composed of the body and tai l with furcae. The surface tegument contains

spines. Typically, two pigm ented eye spots can b e found in the f irst half of the

body; their ultrastructure has been studied by van de Roe me r and Haas 1984).

The anterior end is occupied by a head organ, wh ich contains ducts and open-

ings of the penetration glands. The cercariae have five pairs of penetration

glands: two pairs are located dorsally over the acetabulum and three pairs fur-

ther towards the distal part of the body. The glands differ in their content.

Additional to the main penetration glands there are also some other, smaller

glands present in the cercarial bod y Ne uhaus, 1952a). The intest ine is



BIOLOGY OF

TRICHOBILH RZI

67

inconspicuous. The excretory s ystem is typically com pose d of 213+3+ 1)] = 14

flam e cells; ) indicates the flam e cell on one side of the tail, [ ] represen ts the

pattern of cells on one side of the cercaria = bod y and tail the excretory

system is symmetrical along the longitudinal axis, see Figure 4). Different pat-

terns occur in som e species: 213+4+ 1)]=16 in T.

arcuata

see Islam, 1986b)

and T. austral i s see Blair and Islam, 1983), 213+2+ 1)]=12 in T. corv i see J.

Ito, 1960, cited by Blair and Islam, 1983). Moreover, several descriptions list

two ciliary clusters within the excret ory ducts T.

szidati T. regenti T. sa lm an -

ticensis; see Kol~i~ov~i and Hor~ k, 1996; Ho r~k et al . 1998a; Simon-Martin

and Simon-Vicente, 1999).

Unfortunately, the cercariae o f different species closely resemble each other

and they cannot usually be used for species identification. Their size cannot be

used for diagnosis. Some morphological structures may indicate, but do not

prove, the taxonomic posi t ion of cer ta in species , e .g . the number and

P

Figure 4 Cercaria of Trichobilharzia regenti. General morphology left) and excretory

system with flame cells right). F, flame cell; CP, ciliary patches within excretory ducts.

Scale bar = 100 lam. Reproduced with permission from HorLk et al. 1998a).



168 R HOR,a,K, L. KOI_, .ROV,~,AND C.M. ADEMA

organizat ion of f lame cel ls in the body. Because severa l species of

Trichobilharzia have similar patterns of flame cell organization, other markers

have been sought. The distribution of surface sensory papillae chaetotaxy) has

bee n cons idered a valuable tool in distinguishing species of cercariae e.g.

Richa rd, 1971; B ay ss ad e- D uf ou r and O w-Y ang, 1975; Kol~i~ov~i and Hor~ik,

1996). T hese pa pillae can be o bse rved by staining cercariae w ith silver nitrate

or examining the wo rms under the scanning electron micro scope Koc k and

Btickeler, 1998). Chaetotaxy can be used to distinguish certain species with

typical papillae patterns, but the value of this meth od is limited beca use 1) the

distr ibution of papil lae is known for a small numb er of species only 2) minor

differences in papillae positions occur frequently, thus challenging the speci-

f icity of this marker and 3) the method requires experienced examiners and

many cercariae need to be assessed usually not all papil lae typical of the

species are visible in one specimen). T wo recent papers clearly demonstrated

that chaetotaxy in Trichobilharzia s tudies can be problemat ic : Kock and

B6ckeler 1998) did not find any difference when com paring sen sory papil lae

of T. ocellata and T. franki; and, surprisingly, Gay et al. 1999) were able to

identify T. f rank i f rom R. auricularia and T. ocellata from L. stagnalis and the

pattern of T.f rank i was n ot identical with that reported by K ock and B tickeler

1998).

Evidently, ei ther description of new species or determination of known

species based exclusively on cercarial mo rpholog y should be avoided. Also,

olde r data should be evalu ated carefully, e.g. the findings o f T. ocellata and T.

szidati f rom Radix peregra or R. auricularia are probab ly not valid see sec-

tions 3.2 and 3.4.6).

3.4.5. Adults

The isolation of adults from different host organs is a complicated matter and

requires a t tent ion due to the wo rm s ize usually , the specimens measu re

betw een 5 and 10 m m in length and 20--100 ~tm in diameter) and intimate co n-

tact with the host tissues. It is rare to obtain a whole worm intact; frequently

only fragments of adults can be recovered. The measurements of the body

length/width and of inner organs are generally of l imited value for species

determination. The w orm s are able to contract or relax their bo dy such that the

diameter and corresponding length) of bod y parts m ay be substantial ly mod -

if ied and the shape deformed.

The adults Figure 5) represen t the stage that is m ost imp ortant in species

diagnosis Blair and Islam, 1983). Bo th sexes have a filiform body of almo st

uniform width. The b ody can be covered by tubercles or spines. U sually, the

posterior end is spatulate. The oral opening is situated subterminally and sur-

rounded b y an oral sucker. The head part of the bo dy has several long sensory



BIOLOGY OF

TRICHOBILH RZI

69

O S I ~ . O S

OE 0

[~VS

~ ~ - E R S ~

°

Figure 5 An terior and posterior end of a ma le left) and a female right) of

Trichobilharzia regenti.

A, acetabulum;CG, canalis gynaecophorus;E, egg; EC, excretory

duct; GO, genital opening; GP, genital papilla; I, intestine; O, ovary; OD, oviduct; OE,

oesophagus; OS, oral sucker; OT, ootype; RS, receptaculumseminis; T, testes; U, uterus;

VD, vitelloduct; VI, vitellaria; VSE, vesicula seminalis externa; VSI, vesicula seminalis

interna. Scale bar = 100 pro. Reproducedwith permissionfrom Hofftket al. 1998a).

cilia. The acetabulum lies very close to the anterior end and i t is covered by

spines. In males, there is a short canalis gynae coph orus, which is usually dec-

orated with spines. As an exception to the rule, the canalis m ay be used for

diagnosis, as it is unusually long in T. ana t ina see Fain, 1955, 1956b). Th e

digestive tract lacks a pharynx, and a long oesophagus terminates just b efore

the acetabu lum whe re intestinal bifurcation occurs. The place o f reunion of two

intestinal branches provides an important taxonom ic marker; in som e species

the reunion is located near the anterior end o f the seminal vesicle of males T.

szidati, T. elvae, T. corvi , wh ereas it is situated posterior to the semina l vesi-

cle in T. brevis and T. austral is . The un ited caecum runs in curves to the end o f

the body. The reproduetion apparatus of m ales is com posed o f nume rous testes

that l ie just behind the canalis g ynaecop horus and fi ll up the b ody to the pos-

ter ior end. The number of tes tes var ies in mature males; however , a

m inim um -m ax im um range can aid in species identification. The ducts leading

forward from the testes terminate in the seminal vesicle, located betwee n the



170 R HORAK L. KOLAROVA AND C.M . ADEM A

ace tabulum and cana l i s gynaecophorus ; the gen i t a l pap i l l a i s loca ted a t the

beginn ing of the cana l i s gynaecop horus . In f em ales , the pos te r io r par t o f the

bo dy is f i l led w ith vitellaria; towa rds the ante rior semin al recepta cle, the ovary,

oo type and u te rus occur . The gen i t a l opening i s s i tuated jus t beh ind the ace tab-

u lum. O nly on e egg i s found w i th in the u te rus .

The fo l lowing fea tures seem mos t appropr ia te fo r spec ies iden t i f i ca t ion :

type of sur face t egumenta l s t ruc tures ( sp ina t ion , tuberc les ) , sp ina t ion and

l eng t h o f cana l i s gynaecophor us i n r e l a t i on t o t he body , p l ace o f caeca l

r e u n i o n , p o s it io n o f m a l e g e n i ta l p a p il la , n u m b e r o f te s te s ( m i n i m u m -

max i mum r ange ) and p r opo r t i ons ( s i ze and s hape ) o f i n t e r na l o r gans . T he

m easurem ents o f ind iv idua l bodies and organs ( l ength and wid th) may be con-

s idered in form at ive bu t can not be used as indepen dent c ri te r ia . These f ea tures

are eas i ly in f luenced by a t l eas t two fac tor s : f r equent ly occur r ing cont rac-

t ion /re laxa tion of the bo dy p ar ts ( inc lud ing shr inkage ca used b y f ixa t ives ) and

in t raspec i f i c var iab i l i ty in the s i ze of worms (e i ther w i th in the same hos t

organ i sm or in d i f f e ren t fina l hos ts ) .

3 .4 .6 . Spe c t rum o f in termed ia te hos t s

Larval s tages of

Trichobi lharz ia

spp. develop in f reshw ater pulm ona te snails o f

two fam i li es : Ly m naeid ae (a l l over the wor ld) and Phy s idae (mo s t ly in Nor th

Am er ica) . A t p resen t , the u se o f a p leuroc er id sna il ,

Sem isu lcosp i ra l ibert ina ,

by T. corv i (see J. I to , 1960, c i ted by Blai r and Is lam , 1983) is the only exce p-

t ion know n. I t is bel ieved that par t icular species of

Trichobi lharz ia

have ra ther

nar row spec i f ic i t ies towards the i r in te rm edia te hos ts , paras i ti z ing e i ther on ly

one snai l species or several, c losely related species (Blai r and Is lam , 1983) . For

instance, T. f r a n k i develops exc lus ive ly in R. aur icu lar ia ( see Mt i l l e r and

Kimmig, 1994), T. regenti in R. peregra and R. ovata (see Hor~ik et aL , 1998a)

and so on . Two im por tan t aspec t s o f in te rmed ia te hos t spec i f i c ity should be

noted : (1) som e spec ies o f Trichobi lharz ia m ay share one sna il spec ies ( e .g .L .

s tagna l i s )

as interm edia te ho s t (Szidat , 1942; Ne uha us , 1952b; Far le y 1971;

Bla i r and I s l am, 1983); and (2) l abora tory exper ime nts c lear ly showe d tha t

mi rac id ia o f so m e spec if ic , wel l -def ined spec ies ( e .g .T . f r anki ) p refer

R. aur ic-

u lar ia as interm ediate hos t . How ever , such beh avioural s tudies sho we d that , to

som e deg ree , T . f r a n k i i s a lso at t racted to other , c los ely related snai l species

such as R. ovata . M o r eove r , the behav i ou r a l p r e f e r ence f o r pa r t i cu l a r hos t

spec ies cor re la tes w i th the success o f paras it e de ve lop m ent in the sna il s; a f t e r

exp osu re to the paras i tes , T .

f r a n k i

deve loped in 100 of

R. aur icu lar ia

and

10 o f R . ova ta (see K ock , 2001).

The l a rva l s t ages of Tr ichob i lhar z ia spp. ' or Tr ichob i lhar z ia oce l la ta

have a l so been repo r ted f rom sna il s o f the f ami ly P lanorb idae ( e .g . A n i s u s sp.

with T.

o c e l l a t a

r epo r t ed by B ee r and G er man , 1994 ) , Phys i dae and



IOLOGY OFTRICHOBILHARZIA 7

H y dr ob i i dae / B i t hyn i i da e K i l ia s and F r i ck , 1964 ; van den B r oek , 1965).

How ever , cau t ion i s war ran ted ; e i ther Tr ichob i lhar z ia spp . w i th unk no wn l i fe

cyc le s and probab ly no t T.

oce l la ta )

m ay dev elop wi th in these sna il s o r the

cercar iae be long to anoth er genu s e .g . Gigan tob i lhar z ia spp. ; see D6nges ,

1965).

The sys tem at ic r e la tionsh ips of the in te rme dia te hos t s sna il s ) a re a l so fu ll

o f confus ions and remain to be reso lved . Cur ren t ly , the des igna t ions a t the

genu s an d species levels are in f lux. Unfor tuna tely, this fur ther com plicates the

s tudy o f hos t spec i f i c i ty of spec ies o f

Trichobi lharz ia .

C once r n i ng t he f ami l y

of lymnaeid sna i l s , one approach i s tha t a l l spec ies be long to the genus of

L y m n a e a ,

w h er eas ano t he r app r oach recogn i zes s eve r a l va l i d gene r a e .g .

Radix , S tagn ico la , Ga lba) .

T hi s s econd v i ew , s uppor t ed by m o l ecu l a r da ta

Bargues et a l . , 2001) , i s adopted for th i s r ev iew. Morphologica l ly , the spec ies

are d i s t inguished by the shape a nd s ize of the she l l. How ever , th is can hard ly

separate c lose ly r e la ted forms such as R. ovata and R. peregra . Addi t iona l mor -

phologica l f ea tures such as the co lour of the man t le R a d i x species) , surface

s cu l p t u r e s o f t he s he l l R a d i x a n d S t a g n i c o l a s pec i e s ; J ack i ew i cz and

Koralew ska-Batura, 1995), an d the exam inat ion of the penis and internal repro-

duct ive organs Jack iewicz , 1988) can be used to he lp d iagnos is a t the spec ies

level . Recent ly , m olecu lar t echniques have been appl ied to inves t iga te the phy-

l ogeny o f l ymnae i d s na i l s . C ompar a t i ve ana l y s i s o f 18S r D N A s equences

Bargues and Mas-Coma, 1997; Bargues et al . , 1997) y ie ld ed th ree c lades ,

c o m p o s e d o f L y m n a e a - S t a g n i c o l a , R a d i x a n d G a l b a w i t h i n t he l ym nae i ds .

M or e r ecen tl y , a rev i ew o f E u r opean l ym nae i ds B a r gues et a l . , 2001) , which

a l so cons idered an ex tens ive ana lys is o f ITS-2 sequences , conf i rm ed the group-

ing in to these th ree c lades , whi le show ing he te rogen ei ty wi th in the genus o f

Radix . B as ed o n s upport f r om t he mo l ecu l a r da ta , s eve ra l o t he r names w e r e

in t roduced in addi t ion to

R. aur icular ia , R. ovata

and

R. pereg ra.

Interes t ingly,

the m olecu lar ana lys i s sugges ted tha t sna i ls p rev iou s ly de te rm ined to be R .

p e r e g r a

a n d

R. ovata

us ing morphologica l f ea tures ) and tha t se rve as the

interm edia te hos ts o f T. regent i see HorS_k et al . , 1998a), be long to two othe r

separa te species : R. labiata and R. lagotis . Unfor tuna te ly , it s eem s d i f f icu l t to

d i s tinguish these ne wly ann oun ced spec ies from the m orphologica l v iewpoin t,

and the i r rou t ine d iagnos i s in malaco logy and paras i to logy i s ques t ionable .

Taken toge ther , a he te rog enei ty in suscept ib i l ity wi th in cer ta in sna il popu la-

t ions for in fec t ion by

Tr ichob i lhar z ia

spp. and o the r t r ema t odes ) m ay be due

to the occu r rence of c ryp t ic sub)spec ies o f sna i ls , c las si f ied by t r ad it iona l

m ethod s as be longing to one spec ies . However , ITS-2 da ta do no t d i s t inguish

be t w een r e s i s t an t and s us cep t i b l e i nd i v i dua l s o f t he s ame s na i l s pec i e s

Bargues et a l . , 2001) , and prob ably oth er gen et ical ly l inked factors play a role

in hos t -p aras i t e comp at ib i l ity .



172 P. HORAK, L. KOL. .ROV,, ,AND C.M. ADEMA

3.4.7. S pectrum of bird hosts a nd fina l location

It seems that the spe ctrum of final hosts suitable birds) is broad er than that of

intermediate hosts . This can par t ly be due to the fact that cercar iae of

Trichobilharzia

possess an abil ity to penetrate practically any warm -blooded

animal Haas and van de Roemer, 1998). Yet unkn own factors the imm une

response might be on e of them) allow the subsequent development and matu-

ration of Trichobilharzia

parasites in birds, but not in mammals. Because

larval p arasite stages, i.e. cercariae, released from snails have bee n enc ou ntere d

frequently, these were used to experimentally infect birds. F rom the success-

ful develop men t of, fo r examp le, T.

physellae

in canaries, m allards an d pigeons

McMullen and Beaver, 1945) and T.

corvi

in chic ken s J. Ito, 1960, cited by

Blair and Islam , 1983), it is clear that species o f Trichobilharzia do n ot specif-

ical ly depend on water bi rds , as might be deduced from their aquat ic

intermediate snail hosts. T his fact has be en c onfirme d by exam ining naturally

infected birds. Concerning the spectrum of bird orders, besides Anseriformes,

some species of Trichobilharzia have been found in Podicipe diformes T.

aureliani; see Fain, 1956b), Ciconiifo rme s T. rodhaini; see Fain, 1955),

Coraciiformes T. cerylei; see Fain, 1956b) and Passe riforme s e.g.T. corvi; see

Yamaguti, 1941).

Once inside the final host, the parasites mature and lay eggs in a specific

site. Generally, the species of Trichobilharzia can be divided into two main

groups: visceral schistosom es e.g.T. brevis, T. stagn olae, T. szidati, T. franki)

and nasal schistosomes e.g.T.

arcuata, T. australis, T. regenti).

Whereas the

nasal sch istosome s exclusively inhabit the nasal soft tissues, the visceral par-

asites may inhabit different si tes within the body. This preference is not

particularly strict and parasites can usually be found in blood vessels of the

intestine T.

franki;

see Mtiller and Kim mig , 1994), cloa ca T.

kegonsensis;

see

Brackett, 1942), liver T.

franki;

see Mfiller and K imm ig, 1994), and in portal

(T. querquedulae;

see Mc Leod , 1937) and mesen terial T.

maegraithi;

see

Kruatrachue et al., 1968) vessels. Som e species T. szidati, T. stagnicolae, T.

elvae and T. physe llae)

have b een discovered within the tissues of the intestinal

wall including muscles) and associated vessels M cM ullen and Beaver, 1945;

Neuhaus, 1952a).

3.4.8. Cytogenetical and molecular analyses

To date, karyological studies and rDNA sequencing have been applied to

Trichobilharzia for species characterization. So far, karyotypes from nine

species isolates) have been character ized, i .e . T,

physellae

Short and

Menzel, 1960), T.

stagnicolae

A Sh ort an d M enz el, 1960), T.

stagnicolae B

Short and Menzel, 1960),

Trichobilharzia

sp. 1 Barshene

et al.,

1989),



BIOLOGY OF

TRICHOBILH RZI

73


s p . 2 ( B a r s h e n e

e t a l . ,

1989) , T.

s z i d a t i

( B a r s h e n e a n d

Staniavichiute, 1993), T. s z i d a t i (Spakulov~i e t a L , 1996), T. f r a n k i ( S p a k u l o w i

e t a l . ,

1997) and T.

r e g e n t i

( S p a k u l o v ~

e t a l . ,

2001). Spakulov~i

e t a l .

( 1 9 9 7 )

h a v e r e v i e w e d t h e v a r i a b i l i t y i n c h r o m o s o m e p a t t e r n s f o r t h e g e n u s

T r i c h o b i l h a r z i a . G e n e r a l l y , t h e s p e c i e s s h o w s i m i l a r p a t te r n s o f c h r o m o -

s o m e s in m e t a p h a s e p l a te s , h a v i n g 2 n = 1 6 w i t h 1 4 a u t o s o m e s a n d 2

g o n o s o m e s . T h e s e x - d e t e r m i n i n g m e c h a n i s m i s Z Z i n m a l e s a n d Z W i n

females . On ly T .

s t a g n i c o l a e

B ( S h o r t a n d M e n z e l , 1 9 6 0 ) w a s f o u n d to p o s -

ses s 2n = 18 . Th e f i f th au toso m e pa i r i s u sua l ly s a te l l i ted (Spaku lov~i e t a l . ,

1 9 9 7 ) . T h e m a i n d i f f e r e n c e s b e t w e e n s p e c i e s c a n b e o b s e r v e d i n t h e s e x

c h r o m o s o m e s . C h a r a c te r iz a t io n o f T. r e g e n t i , t h e o n l y n a s a l s c h i s t o s o m e

a m o n g t h e s e o t h e r w i s e v i s c e ra l s c h i s to s o m e s , d i s c l o s e d t h e p r e s e n c e o f o n e

o r t w o su p e r n u m e r a r y B c h r o m o s o m e s i n m o r e t ha n 6 0 o f t h e a n a l y z e d

ce l l s f rom m ale an d f em ale sp oroc ys t s (Spaku lov~i e t a l . , 2 0 0 1 ), th e m o d e o f

f o r m a t i o n o f w h i c h i s u n c l e a r . A t p r e s e n t , k a r y o l o g i c a l m a p p i n g s h o u l d b e

c o n s i d e r e d a s a s u p p l e m e n t a r y d i a g n o s t i c t o o l , a s i t c a n n o t b e u s e d a s a

s t a n d - a l o n e m e t h o d f o r s p e c i e s i d e n t i f i c a t i o n . T h i s i s b a s e d o n t h e l i m i t e d

n u m b e r o f s p e c ie s / is o l a te s o f T r i c h o b i l h a r z i a t h a t w e r e k a r y o l o g i c a l l y c h a r -

ac te r i zed . Moreo ver , the o lde r desc r ip t ions do no t con ta in in fo rmat ion on s ex

c h r o m o s o m e s ( S h o r t a n d M e n z e l , 1 9 60 ; B a r s h e n e e t a l . , 1 9 8 9; B a r s h e n e a n d

S t a n i a v i c h i u t e , 1 9 9 3 ) o r s a t e l l i te s ( B a r s h e n e

e t a l . ,

1 9 8 9 ; B a r s h e n e a n d

S tan iav ich iu te , 1993) . Ho we ver , r e -exam ina t ion o f the o lde r desc r ip t ions and

charac te r i za tion o f add i t iona l sp ec ies o f T r i c h o b i l h a r z i a m a y a l l o w f u t u re u s e

o f k a r y o t y p e s f o r d e t e rm i n a t i o n o f sp e c i e s .

Recen t ly , the va l id i ty o f spec ies and phy logene t ic r e la t ionsh ips have been

t e s te d b y s e q u e n c i n g r D N A . T h i s a p p r o a c h w a s i n i ti a te d b y t h e s t u d y o f e v o -

lu t ionary re la t ionsh ips am ong the Sch i s tosom at idae (Snyd er and Loker , 2000)

i n w h i c h p a r ti a l s e q u e n c e s o f t h e 2 8 S r R N A g e n e w e r e o b t a i n e d a n d u s e d i n

phy lo gene t ic ana lyses . A c lea r ly de f ined pos i tion o f the genu s T r i c h o b i l h a r z i a

T . o c e l l a t a

as the r ep resen ta t ive o f the genus ; s tr a in i so la ted in Germ any f rom

L . s t a g n a l i s ) w i t h i n t h e c l a d e o f a v i a n s c h i s t o s o m e s w a s c o n f i r m e d .

Consecu t ive s tud ies , invo lv ing s equence da ta de r ived f rom the in te rna l t r an -

s c r i b e d s p a c e r r e g i o n s 1 a n d 2 ( I T S - l , I T S - 2 ) , r e p o r t e d o n i n t e r s p e c i f i c

d i f f e rences and the pos i t ions o f pa r t i cu la r spec ies w i th in the genus . To da te ,

t h e s e s t u d ie s h a v e b e e n l i m i t e d t o a s m a l l n u m b e r o f E u r o p e a n i s o l a te s o f

T r i c h o b i l h a r z i a (T. o c e l l a t a , T . s z i d a t i , T . f r a n k i , T . r e g e n t i , T r i c h o b i l h a r z i a sp.).

N e v e r t h e l e ss , t w o i m p o r ta n t c o n c l u s io n s c a n b e d r a w n f r o m t h e s e p r e l im i n a r y

data . (1) The European s t ra ins of T. o c e l l a t a and T. s z i d a t i i so la ted f rom L .

s t a g n a l i s

( a n d a l s o fr o m

S t a g n i c o l a p a l u s t r i s ;

s e e K o c k , 2 0 0 0 ) s h o w s e q u e n c e

iden t i ty o f >9 9 and be lo ng to one c lade (pe rhaps spec ies ) (Kock , 2000 ; J .

Rudo l fovf i , J . D vo ~ik and P . HorS_k , unp ub l i shed da ta ). W i th th i s approa ch i t

s h o u l d b e p o s s i b l e t o r e so l v e th e i m p o r t a n t d i l e m m a o f t h e c o m p o s i t io n o f th e

g e n u s T r i c h o b i l h a r z i a (see a lso Od ening , 1996; Ko ck, 2000) . Shou ld T. s z i d a t i



174 R HORAK L. KOLAI~OVA AND C.M . ADEMA

Table 1 Overview o f species with known developmen tal stages and l ife cycles

Trichobilharzia

species Distribution Natural and/or

experimental

bird hosts

Footnote

Nasal species using lymnaeid snails

T. arcuata Islam, 1986

T. australis Blair and Islam, 1983

T. regenti Horfik et al. 1998

Visceral species using lymnaeid snails

T. alaskensis Harkema et al. 1957

T. brevis Basch, 1966

Z elvae Miller, 1923) McMullen and

Beaver, 1945

T. f rank i Mtiller and K imm ig, 1994

T. jequi t ibaensis

Leite

et al.

1978

T. j ianens is Liu et al. 1977

T. l imnaeae

Yamaguti, 1971

T. maegraithi Kruatrachue et al. 1968

T. ocellata

LaValette, 1855) Brumpt,

1931

T. pao i Kung et al. 1960) Tang and

Tang, 1962

T. paro cellata Johnston and Simpson,

1939) Islam and Copem an, 1980

T. salmanticensis Simon-M artin and

Simon-Vicente, 1999

T. stagnicolae Talbot, 1936)

McMullen and Beaver, 1945

T. szidati Neuhaus, 1952

Visceral species using physid snails

T. adamsi Edw ards and Jansch, 1955

T. cameroni Wu, 1953

T. jequi t ibaens is Leite et al. 1978

T. oregonensis Macfarlane and

Macy, 1946) Macy and Moore, 1953

T. physel la e

Talbot, 1936) McMullen

and Beaver, 1945

Australia Anseriformes,

Columbiformes

Australia Anseriformes

Europe Anseriformes

N. America

Asia

N. America

Europe

S. America

Asia

Asia

As ia

Europe,

N. America,

Asia

Asia

Australia

Europe

N. America

Europe

N. America

N. America

S. America

N. America

N. America

Anseriformes

Anseriformes

Anseriformes,

Passeriformes

Anseriformes

Anseriformes

Anseriformes

Anseriformes

Anseriformes

Anseriformes

lb,c

2,3

lb , c

2,4

2

la, b

Anseriformes 2,4

Anseriformes

Anseriformes

Passeriformes

Anseri fonnes lb,c

Anseri fonnes

Anseriformes,

Passeriformes

Anseriformes

Anseriformes 2,3

Anseriformes,

Columbiformes,

Passeriformes




Table 1 continued

Trichobilharzia

species Distribution Natural and/or

experimental

bird hosts

Footnote

T. querqu edulae M cLeod, 1937)

McM ullen and Beaver, 1945

Visceral species using pleurocerid snails

T. corv i Yam aguti, 1941) McM ullen

and Be aver, 1945

N. Am erica Anseriformes

A s i a P a s s e r i f o r m e s ,

Galliformes

S y n o n y m y o f t h e f o l lo w i n g s p e c i e s h a s b e e n q u e s t i o n e d :

T . q u e r q u e d u l a e - T. p h y s e l l a e - T . l i m n a e a e

T . k o s s a r e w i ) - T . o c e l l a t a - T . s z i d a t i - T , e l v a e ( s ee s ec t i on 3 .2 . ). B ecau se o f the con f us i on abou t w h a t i s mean t

by T . o c e l l a t a , t h e s p e c i e s w a s d e s c r i b e d a l s o f r o m o t h e r s n a i l fa m i l ie s , e . g . P h y s i d a e , P l a n o r b id a e a n d

H y dr ob i i da e / B i t hyn i i dae ( genus B i t hyn i a ) (K i l i a s and Fr i ck , 196 4 ; van den B r oek , 1965). I n f ac t , t he se f i nd i ngs

m o s t p r o b a b l y r e p r e s e n t o t h e r s p e c i e s o f T r i c h o b i l h a r z i a o r e v e n o t h e r g e n e r a o f b i r d s c h i st o s o m e s .

t T h e s p e c i e s is c h a r a c t e r i z e d b y r D N A s e q u e n c e s a l r e a d y ( S n y d e r a n d L o k e r , 2 0 0 0 ; K o c k , 2 0 0 0 b ; D v o[ ~ik

e t a L ,

2002c).

2 T he o r i g i na l de sc r i p t i on w a s no t ava i l ab l e t o t he au t hor s ; the i n f o r ma t i on i s ba se d on B l a i r and I s l am ( 1983) .

3 T he o r i g i na l de sc r i p t i on w a s no t ava i l ab l e t o t he au t hor s ; the i n f o r ma t i on i s ba se d on F a r l ey ( 1971) .

4 T h e o r i g i n a l d e s c r i p ti o n w a s n o t a v a i la b l e t o t h e a u t h o r s , t h e i n f o rm a t i o n i s b a s e d o n S i m o n - M a r t i n a n d S i m o n -

V i cen t e ( 1999) .

b e s y n o n y m i z e d w i t h T . oce l la ta T. sz idat i a s a j u n i o r s y n o n y m ) , o r s h o u l d T.

oce l la ta r e m a i n a s a c o m p l e x o f s p e c ie s - spec ies inqu i rendae due t o h i s t o r -

i c a l u n c e r t a i n t y a s t o w h a t T . o c e l l a t a i s ) ? T o f i n d a r e l e v a n t a n s w e r i s

imp or t an t becaus e so -ca l l ed T. ocel la ta i s he ld i n s evera l l abo ra to r i e s ac ros s t he

wor ld . 2 ) Tr ichob i lhar z ia sp., T. regenti and T. f r a n k i i s o l a t e d f r o m R a d i x

s p e c i e s

R. ovata , R. peregra , R. aur icular ia)

f o r m o n e c l a d e , b a s e d o n e i th e r

I T S - 1 o r I T S - 2 s e q u e n c e d a t a K o c k , 2 0 0 0 ; D v o [ ~ k et al . , 2002) . I t can be

h y p o t h e s i z e d t h a t t h e c l o s e r e l a t i o n s h i p b e t w e e n t h e s e s p e c i e s i s r e f le c t e d i n

t h e s h a r i n g o f o n e g e n u s o f s n a i ls

Radix )

a s th e i n t e r m e d i a t e h o s t . T h e d i f f e r -

en t l oca t i on w i th in t he f i na l hos t nasa l ti s sue fo r T. regenti and v i s ce ra l ves se l s

for T. f r a n k i ) i s p r o b a b l y o f s u b s i d ia r y i m p o r t a n c e w i t h in t h e f r a m e w o r k o f

r D N A a n a l y si s .

3 5 F i n al N o t e s o n S y s t e m a t i c s

I t is v i t a l t ha t a l l new desc r i p t i ons o f Trichobi lharz ia s p e c ie s s h o u l d b e a s c o m -

p l e te a s p o s s ib l e f r o m t h e v i e w p o i n t o f m o r p h o l o g y , l if e c y c l e s , h o s t

s p e c i fi c it y a n d m o l e c u l a r a n a l y s is ) . N e w d e s c r ip t io n s s h o u l d a l s o b e b a s e d o n

u p - t o - d a t e i n f o r m a t i o n re g a r d i n g t h e l a te s t t a x o n o m i c s i t u a t io n w i t h i n t h e

g e n u s o f Tr ichob i lhar z ia . T w o r e c e n t e x a m p l e s d e m o n s t r a te s o m e o f th e




T a b l e 2 O v e r v i e w o f s p e ci e s w i t h p a rt l y k n o w n d e v e l o p m e n t a l s t ag e s a n d l i f e c y c l e s

i n t e r m e d i a t e h o s ts u n k n o w n )


s p e c i e s

N a t u r a l a n d / o r

e x p e r i m e n t a l

D i s t r i b u ti o n b i r d h o s t s F o o t n o t e

N a s a l s p e d e s :

T . a u r e l i a n i

F a i n , 1 9 5 6 A f r i c a

T . d u b o i s i

F a in , 1 9 5 9 A f r i c a

T . n a s i c o l a F a in , 1 9 5 5 A f r i c a

T . r o d h a i n i

F a in , 1 9 5 5 A f r i c a

T . s p i n u l a t a

F a in , 1 9 5 5 A f r i c a

V i s c e r a l s p e c i e s :

T . a n a t i n a

Fain , 1955

T . b e r g h e i

F a in , 1 9 5 5

T . b u r n e t t i B r a c k e tt , 1 9 4 2) M c M u l l e n

a n d Be a v e r , 1 9 4 5

T . c e r y l e i F a in , 1 9 5 6 A f r i c a

T . f i l i f o r m i s S z i d at , 1 9 38 ) M c M u l l e n E u r o p e

a n d Be a v e r , 1 9 4 5

T . g u a n d o n g e n s i s

T s a i

e t a l .

1979

T . h o r i c o n e n s i s Bracke t t , 1942)

M c M u l l e n a n d B e a v e r , 1 9 4 5

T . i n d i c a

B a u g h , 1 9 6 3

T . k e g o n s e n s i s Bracke t t , 1942)


T . k o s s a r e w i

S k r j a b in a n d Z a k h a r o v , 1 9 2 0

T . k o w a l e w s k i i

E js m o n t , 1 9 2 9 )


T . l i t t l e b i

By r d , 1 9 5 6 ) F a r l e y , 1 9 7 1

T . l o n c h u r a e

F i s c h th a l a n d K u n tz ,

1 9 7 3 ) T s a i

e t a l .

1979

T . s c h o u t e d e n i Fain , 1955

T . w a u b e s e n s i s

Bracke t t , 1942) 5

M c M u l l e n a n d B e a v e r , 1 9 4

T . z o n g s h a n i

T s a i

e t a l .

1 9 7 9 A s i a

A f r i c a

A f r i c a

N . A m e r i c a

A s i a

N . A m e r i c a

A s i a

N . A m e r i c a

E u r o p e

E u r o p e , A s i a

N . A m e r i ca

A s i a

A f r i c a

N . A m e r i ca

P o d i c i p e d i f o r m e s

A n s e r i f o r m e s


C i c o n i i f o r m e s ,






C o r a c i i f o r m e s


N o t m e n t i o n e d 2




A n s e r i f o r m e s 1 , 2 , 3


P a s s e r i f o r m e s 2 , 3

P a s s e r i f o r m e s 2



n o t m e n t i o n e d 2

Synonymy of the following pecieshas bee n questioned:

T. kegonsensis - T. horiconensis - T. burn etti - T waubesensis.

Because it is impossible o be certain hat T.

kossarewi

is a synonymof T.

ocellata

Blair and Islam , 1983 and

section 3.2.), the form erspecies s treated in this table separately as an insufficientlydescribed

Trichobilharzia.

2 The original description was not available o the authors; the information s ba sed on Blair and Islam 1983).

3 The originaldescriptionwas not available o th e authors; the information s based on Farley 1971).



178 P. HOR,~K, L. KOL, ,I~OVA AN D C.M. AD EM A

4. DEVEL OPME NT IN INTERMEDIATE HOSTS

4.1. Host Finding and Penetration by Miracidia

Ad ult avian schistoso me s prod uce eggs that, after maturation in the host, con-

tain fully developed miracidia. The eggs of visceral schistosomes leave the

avian host with the faeces. Within a short time ( 5- 10 min, T. szidati Neuhaus,

1952a; 2-3 h in T.

cameroni

Wu, 1953) of being deposited in surface water,

physiological cues such as increased light and change in osmo tic pressure cause

miracidia to hatch from the eggs (Meuleman et al. 1984b; Xu and Dresden,

1990; Kalbe et aL 1997). A nasal sch istosom e, such as T. regenti deposits eggs

in the nasal cavity of birds and miracidia hatch in the nasal mucosa, whic h m ay

then be released into the water when the bird feeds or drinks (Hor~ik et al.

1998a). T he bo dy su rface of a miracidium is covered w ith plates that bear cilia.

Miracidia are fast swimmers, propelled by the beating action of these cilia.

Miracidia lack a digestive system and cannot feed. The energy for swim ming

act iv i ty is der ived f rom the breakdown of endogenously s tored glycogen,

mainly via the Krebs cycle (Tielens

et al.

1991). Consequen tly, miracidia can

only sw im fo r up to 20 h at 20 °C (T. szidati; see Neuhaus, 1952a) before they

have depleted their energy reserves and die. In order to survive, miracidia mu st

infect a snail within this time interval. Snails are obli gato ry intermediate hosts;

the internal phy siolo gy of a suitable snail provides nutrients and other suppo rt

for the differentiation and asexual reproduction of schistosome larvae.

Miracidia display specialized behaviours that enable them to f ind a host

snail (reviewe d by H aas and Haberl , 1997; H aas, 2000). After hatching from

eggs, miracidia disperse by swimming in a relatively fast and linear fashion.

This increases the chance for individual miracidia to find a host and it mini-

mizes high infection rates in single snails . A preference for certain

environmental conditions (light, temperature and gravity) causes miracidia to

locate to microenvironments that are preferred by snail hosts. Snails release

various secreted/excreted products (SEP), which results in an active space of

(gradients of) snail-generated chemicals around potential hosts. Miracidia are

attracted by the macromolecular components of snail-SEP, which consist of

glycoproteins larger than 30 kDa, termed miracidia-attracting glycopro teins

(MAGs) (Ka lbe

et al.

2000). Upon entry into an active space of a snail ,

miracidia of T.

ocellata

change their l inear swim ming behaviour by increasing

the rate of change o f direction (RC D). Additionally, T.

ocellata

miracidia dis-

play a turn-back respon se (consisting of a sharp 180 ° turn) if the chemical cues

fall below a threshold value (Kalbe et al. 1997; Kock, 2001). In an aquatic

environment, w here currents ma y prevent the formation o f linear chem ical gra-

dients , these markedly non-direc t ional behaviours may be opt imal for

miracidia to locate and ultimately contact a moving snail.




If the appropriate cues are absent at the initial contact with a snail, miracidia

resume their swimming behaviour and move away (contact without return

response). The presence of pertinent macromolecular glycoconjugates in

t he

mucus on the snail s surface causes the miracidia to remain c lose to the skin of

the snail and to display repeated investigation and attach ment behaviours

(MacInnis 1965; Haas e t a l . 1991; Haberl and Haas, 1992). Once attachment

has occurred, clues of undetermined nature trigger penetration, effected by

pulsing movements and release of the contents of apical penetration glands.

These secretions remain to be characterized but they probably contain prote-

olytic enzymes that help miracidia to penetrate through the skin of the snail.

H

r i c h o b i i h a r z i a o c el l a t a

loo

80

6

40

20

0

Lymnaea Lynmaea Planor bariu s Pl anor bts

ontro l

tru ncamla peregra co r n eu s planorbis

[I nc re as e o f R C D ~ r ~ T u r nb a ck s w i m m i n g

Figure 6 Preference in host-finding by miracidia of Trichobilharzia ocellata. The

miracidia employ snail-released chemicals for short-range orientation towards a host. Upon

detection of appropriate cues, the miracidia change their linear swimming behaviour by

increasing the rate of change of direction (RCD). The miracidia also display a turnback

swimming response (a sharp 180° turn) if the chemical cues fall below a threshold concen-

tration.

Trichobi lharz ia ocel lata

initiated host-finding behaviour in response to

snail-conditioned water (SCW) containing chemicals released by the host snail,

L y m n a e a

stagnalis (boxed). SCW derived from non-host snails such as Lymn aea t runeatula Lym naea

p e r e g r a

(both Lymnaeidae),

Planorbar ius ¢orneus

and

P l a n o r b i s p l a n o r b i s

(both

Planorbidae) failed to evoke significant host-finding behaviour. This greatly increases the

likelihood that

Trichobilharzia ocel lata

penetrates a suitable host in which it can develop

successfully. Control = water, n = 189-685, * P < 0.05 versus control, + P < 0.05 versus

response to SCW derived from

Lymnaea stagnalis.

Reproduced with permission from

Kalbe et al. (1997).



180 R HORAK L. KOL~ I~OV ~ AND C.M. ADEMA

I n t e r e s t ing ly , no t a l l s c h i s tosom e spe c ie s pe ne t r a t e a sna i l t h r ough th i s r ou te .

S o m e s c h i s t o s o m e s p e c i e s p r e f e r e n t i a l l y e n t e r t h r o u g h n a t u r a l o p e n i n g s s u c h

a s the m o u th o r r e c tu m o f sna i ls Loke r , 1978 ; X ia a nd Jour da ne , 1991) .

The r e l i a nc e on sna i l - r e l e a se d c he m ic a l s to loc a te a hos t p r ov ide s m i r a c id ia

wi th a degree o f spec i f ic i ty regarding the sna i l tha t they infec t Ka l be

et al.

1996). The M AG s p r oduc e d by d i f f er e n t sna i l spe c ie s m a y ha v e s im i l a r pe p t ide

ba c kb one s , bu t d i f f e r i n sa c c ha r ide c om pos i t ion . M i r a c id ia a r e though t to d i f-

f e r e n t i a t e be twe e n the se g lyc osy la t ion pa t t e r ns in o r de r to p r e f e r e n t i a l ly loc a te

and infec t pa r t icula r sna i l spec ies F igure 6 ; Ka l be et aL 2000; Kock, 2001) .

S uc h se l e c t ive a b i l i t i e s be c om e r e l e va n t a s a pa r t i c u la r sc h i s tosom e spe c ie s

may successfu l ly infec t some sna i l s , but fa i l s to es tabl i sh in o ther sna i l spec ies

tha t prove to be unsui table as a hos t . For ins tance ,

T.franki

es tabl i shes infec t ions

Figure 7 Cross-section showing a critical phase in the interaction between an avian

schistosome

Trichobilharzia regenti

and a snail

Lymnaea stagnalis.

Only hours after pene-

tration, the parasite P) resides in the marg in of the he ad- foo t of the snail HF), and is

developing from a miracidium into a mother sporocyst. The combination o f the biological

properties of both the parasite and the host decides whether the parasite will succeed, or

whether it will be defeated by the host. To survive and establish an infection, the parasite

requires a suitable intramolluscan environment. Also, the parasite must prevent a defence

respons e from the snail. T hese conditions are met within host snails such as Radixperegra

or

Radix ovata.

In this case, however,


penetrated into

Lymnaea

stagnalis

which is unsuitable as host. The parasite will die either from inadequate phys io-

logical conditions such as lack of appropriate nutrients) or due to a defence response from

the snail. Th e aggregation of haemo cytes H; phagocytic snail defence blood cells) indicates

that this parasite will soon be encapsulated and eliminated. Giemsa staining. Author: L.

Trefil, Parasitology, Charles Un iversity, Prague, Cze ch Repub lic.




in the snai ls R a d i x a u r i c u l a r i a a n d R . o v a t a bu t no t in o the r lym nae id sna il s

such as

L y m n a e a s t a g n a l i s

o r

S t a g n i c o l a p a l u s t r is

wh ereas the r ever se pa t t e rn

app lies to T. oc e l l a t a (Kock , 2001) . The r ange o f su i tab le in te rmed ia te hos t s can

be res t r ic ted to species - or even s t ra in- level of the snai l species present in a

g iven env i ronmen t . The augmen ted hos t - f ind ing behav iour in r e sponse to L .

s t agna l i s - r e l e as e d

chem icals increases the l ikel ihood that T.

oc e l l a t a

encounters

a su i t ab le hos t . How ever , a p re fe rence fo r som e sna il s does no t a lways p reven t

miracidia from penetrat ing non-host snails (e.g. Grassi e t a l . 2001 ; K ock , 2001 ;

Figu re 7) . Add i t ional ly , m iracid ia do no t seem to avo id unsu i table s t ra ins of a

pa r t icu la r hos t spec ies . Phys io log ica l and im mu nob io log ica l f ac to rs tha t dec ide

the f a te o f s ch i s tosom e paras it e s w i th in sna il s a r e d i s cus sed be low .

4 2 In t ramol luscan De velopm ent : Stages and In fection Course

The en t ry in to a sna i l hos t marks a t r ans i t ion f rom f r ee - l iv ing to a pa ras i t i c

phase in the l if e cyc le o f an av ian s ch i s tosom e. S tud ies o f the av ian s ch i s to -

some T.

o c e l l a t a

(S lu i ters , 1981; Amen

e t a l .

1 9 9 1 ; A m e n a n d M e u l e m a n ,

1992), supp lem en ted w i th so m e obse rva t ions f rom o the r s ch i stosomes , p rov ide

an ov erv iew o f the pa ras it e s t ages , the asexua l mul t ip l i ca tion and the in fec t ion

co urse w i th in the snail .

Af te r penetra t ing in to a snail hos t , a m iracid ium unde rgoes drama t ic chang es

in morpho logy and metabo l i sm as i t t r ans fo rms in to a mother spo rocys t , the

next larval l i fe stage . Dur ing and a f ter penetra t ion , the paras i te she ds the c i l ia-

b e a r i n g e p i t h e l i a l p l a t e s . A n e w b o d y c o v e r i n g f o r m s f r o m c y t o p l a s m i c

ex tens ions o f ce l l s tha t l i e be low a super f i c i a l musc le l aye r . The ex tended ,

anuc lea r ce l l p ro jec t ions ( t e rm ed in te rce l lu la r r idge s ) fu se to fo rm a syncy t i a l

t egum en t tha t has a con t inuous c y top lasm w i thou t in te rven ing ce l l mem branes ,

a n d t h a t r e m a i n s c o n n e c t e d w i t h t h e l o w e r - l y i n g n u c l e a t e d c e l l b o d i e s

( M e u l e m a n e t a l . 1978) . The syncyt ia l tegument represents a l iv ing in ter face

tha t f ac i l i t a t e s in t ima te metabo l i c in te rac t ions be tween the pa ras i t e and the

i n te r n a l e n v i r o n m e n t o f th e s n a i l h os t . T h e a e r o b i c m e t a b o l i s m p r e s e n t i n

mi rac id ia chan ges to a m ore f e rmen ta t ive metabo l ism. T h i s a l lows sporocys t s to

be f acu l ta t ive anaerobes tha t can ad jus t to the va r i ab le cond i t ions ( f rom ae rob e

to anaerobe) tha t ma y o ccur in s ide the sna i l hos t (T ielens e t a l . 1991, 1992).

A t 4 days pos t - infect io n (p .i .) , m oth er spo rocy s ts o f T.

o c e l l a t a

w e r e p r e s -

en t in subep ide rmal b lo od ves se l s and s inuso ids o f

L. s tagnal i s

close to the s i te

o f pene t r a t ion (S lu i t e r s , 1981) . On ce fu l ly t r ans fo rmed , m other spo rocy s t s

m ig ra ted fu r the r in to the hea d- foo t t i s sues o f the snai l. Add i t iona l ly , ge rmina l

ce l l s in s ide the moth er sp o rocys t s s ta r t ed to deve lop in to daugh te r spo ro cys t s ,

the nex t l a rva l s t age . F rom day 7 to day 11 , ind iv idua l mother spo rocys t s

c o n t a i n e d m a n y m a t u r i n g d a u g h t e r s p o r o c y s t s . M o s t m o t h e r s p o r o c y s t s

r e m a i n e d i n t h e h e a d - f o o t , b u t s o m e m i g r a t e d t o t h e o v o t e s t i s o r d i g e s t i v e



182 P. HOR, ,K, L. KOLAI~OV,, AN D C.M. AD EM A

gland of the host. F rom day 12 onwards, mature daughter sporocysts emerged

from the m other sporocysts and resided in the head -foo t and the regions of the

ovotestis or digestive gland. Individual mother sporocysts degenerated after

releasing man y daughters, however, intact mo ther sporocysts containing devel-

oping d augh ter sporocysts were still p resent at 33 da ys p.i.

On day 19, cercarial development from germinal cells inside individual

daughter sporocysts becam e obvious. D aughter sporocysts now also occurred

in the kidney, but mechanical damage to the organs of the host was not

observed. After about a week, m ature cercaria emerg ed from daugh ter sporo-

cysts, migrated through b lood vessels to the p ulmo nary region an d left the snail

by penetration of the bod y w all. I t is hy pothesized that a set of specialized

glands serves for the passing o f cercariae through the snail tissues for T.

szi-

dati see Neuhaus, 1952a).

The intramolluscan dev elopm ent of T.

oce l la ta

is temperature dependent.

If snails were maintained at 20 °C, the infections reached patency shedding

of cercaria) at about 7 week s p.i. Am en

et al .

1991; Am en and Meulema n,

1992). At 25 °C, the prepaten t time interval decr ease d to 4- 5 wee ks Sluiters

et al .

1980; Sluiters, 1981). Parasite dev elop me nt daug hter sporocy sts and

cercaria) and cercarial shedding w as ob served to con tinue up to 83 days p.i .

Sluiters, 1981); the shedding of cercaria from L. s tagnalis cont inued for

longer than 123 days p.i. with T.

ocel lata

af ter which the exper iment was

terminated Sluiters et al . 1980). A single miracidiu m infection yielded thou-

sands of cercaria, due to the asexual multiplication associated with each

transit ion between the intramolluscan l ife stages. Infection with multiple

miracidia increased the output of cercariae even further Sluiters et al . 1980).

4 3 Effects on th e Snail Host

Infection with an avian schistosome has severe consequences for a snail .

Remarkably, T.

ocel lata

causes little or no apparent physical injury to host

snails; infected snails usually live equally as long as non-infected control

snails Sluiters et al . 1980; Sluiters, 1981). However, avian schistosomes

actively and dramatically mo dify the internal physiolog y of a snail to maxi-

mize the resources such as nutrients and space) that they derive from the host

for reviews see de Jong-Brink, 1995; Thom pson , 1997).

To optimally obtain nutrients, schistosom es induce change s in the metabo -

lism and biochemistry of the host. Infected snails have heightened metabolism

increased heart rate and respiration) and display c han ges in internal levels of

proteins, carboh ydrates, nitrogen and lipids e.g. M ey er et a l . 1986;

Thompson, 1997).

Trichobilharzia ocellata-infected L. s tagnalis

have increased body an d shell

size Mc Clelland and Bourn s 1969; Sluiters

et al .

1980). T he g iant growth or



BIOLOGY OF

TRICHOBILH RZI

83

g i g a n t i s m r e s ul ts f r o m a n i n c r e a s e in t h e h a e m o l y m p h v o l u m e ; t h e d r y

w e i g h t o f i n f e c t e d s n a il s i n c r e a s e s o n l y s l ig h t l y r e l a ti v e t o c o n t r o l s n a il s

( Joos se and van E lke , 1986) . The inc rease in g row th co inc ides w i th the occur -

r ence o f ma tu re dau gh te r spo rocys t s .

T r i c h o b i l h a r z i a o c e l l a t a

causes g igan t i sm

proba b ly to ensu re ade qua te space fo r l arva l deve lopm en t w i th in the sna il . Th i s

p h e n o m e n o n i s c o n s i d e r e d t o r es u l t f r o m p a r a s it e - m e d i a t e d m o d u l a t i o n o f t h e

neuroen docr ino logy o f the snail bu t the under ly ing m echan i sms r emain u nc lea r

(de Jong-Br ink , 1995) . I t shou ld be no ted tha t g igan t i sm does no t occ ur in a ll

s c h i s t o s o m e - s n a i l a s s o c i a ti o n s (T h o m p s o n , 1 9 9 7) .

Generally, schis tosom e infect ion causes paras i tic cas t ra t ion , the cessat ion o f

repro duc tion in a snail host. Thu s, resource s (nutrients and sp ace) that othe rwise

are used for reproduct ion b ec om e avai lab le to the paras ite. I f T.

o c e l l a t a

infects

juve ni le snails, the reprodu ct ive organs of

L . s t a g n a l i s

do no t ma tu re and these

snails nev er pro du ce egg s (Sluiters, 1981). T r i c h o b i l h a r z i a o c e l l a t a retards but

doe s not prevent the developm ent of the reproduct ive organs in o lder L . s t agna l i s .

Ini tial ly , these snai ls even ha ve an increased product ion of eggs , but egg- laying

ceases w hen the in fec tion beco m es pa ten t (Scha ll ig e t a l . , 1991). Parasitic cas-

t ra t ion is ef fec ted in an indirect fashion . Developing cercar iae of T. o c e l l a t a

conta in a fac tor that causes L . s t a g n a l i s to re lease schis tosom in . Schis tosom in

inhibits ov opo sit ion through antagonizing several fem ale gon adotro pic horm one s

(Hord i jk

e t aL ,

1991; Schall ig

e t aL ,

1992; de Jong-B r ink

e t a l . ,

1992, 1995).

H o e k et al . (1997) de m onstrated that infection with T. oc e l l a t a caused changes

in the m R N A express ion profi le of the host , L , s tagnal i s . Am ong the af fected tran-

scr ip ts were severa l neuroendocr ine fac tors . By af fect ing the t ranscr ip t ion of

these factors, T. o c e l l a t a m ay ind ir ec tly change the phys io logy o f the host. The

chan ges that oc cur in the host are generally consid ered to be beneficial to the para-

s i tes . The extent of changes in hos t metabol ism is var iable , cor re la t ing wi th

consecut ive t rans i t ions between the d i f ferent s tages of in t ramol luscan larvae .

Apparen t ly , s ch i s tosom e-m ed ia ted man ipu la t ions o f the hos t phy s io logy and

m etabo l i sm ensu re op t ima l u sage o f hos t re sources fo r la rva l deve lopm en t wh i le

a l lowing the ho s t to r ecover from per iods o f m e tabo l ic exhaus t ion (Thompson ,

1997) . It has been propo sed to v iew an infected snai l as an extended phen otype o f

the paras ite (D awkins , 1990) . Obvious ly , the abi l i ty to sh i f t the resources f rom

hos t reproduct ion towards paras i te d evelopm ent , thus reducing the f i tness of the

hos t to zero , m akes an avian sch is tosom e a severe pathog en fo r snails.

4 4 I n t e r n a l D e f e n c e R e a c t io n s o f S n a i l I n t e r m e d i a t e H o s t s

4 .4 .1 . G e n e r a l c o m m e n t s o n s n a i l l y m n a e i d ) i m m u n o b i o l o g y

N ot a l l snail species are su i tab le hos ts for schis tosom es . For ins tance , d ig enea n

i n f e c t i o n h a s n e v e r b e e n o b s e r v e d f r o m

C r e p i d u l a f o r n i c a t a ,

a m a r i n e



184 R HOR, .K, L. KOLAROV, , AN D C.M. ADEMA

gastropod Pechenik et al. 2001). Field studies show that the incidence of

schistosom e infection in snail populations is usually low Lo y and Haas, 2001).

Potentially, local adaptation reduces the suitability of snails as hosts for sym-

patric strains of schistosomes Mo rand et al . 1996). Ho we ver, snails can also

be naturally resistant to schistosomes e.g. Joube rt

et al.

1990; Grassi

et al .

2001). The resistance has a genetic basis. Selective breeding can yield snail

strains that do not supp ort parasite develop m ent e.g. Richards

et al.

1992;

Langand and Morand, 1998).

Snails possess potent internal defences that are capable of el iminating

invading pathogens, including s chisto som e larvae for review s see: van der

Kna ap and Loker, 1990; A dem a and Loker, 1997; Lardans an d Dissous, 1998).

In combination, the genetic backgrounds of both the parasite and the host

decide the fate of an invading parasite. A snail in which a parasite cannot

develop due to lack of nutrients or inappropriate pH is an unsuitable host.

Other snails may provide the correct internal environment for a part icular

schistosome, but mount an internal defence and eliminate the invader. This

renders the snail immunobiologically incompatible or resistant. In a suitable

snail host, the internal defences fail to eliminate an invading schistosome,

result ing in an imm unobiolog ically comp atible parasite-host association.

Snails and invertebrates in general) lack lym pho cytic defen ces no anti-

bodies and T-cell receptors, no imm unological m em ory) and emp loy internal

defence s of an innate type. Lectins m ediate s elf-non-self differentiation b y pat-

tern recogni t ion of repeti t ive carbohydrate moie t ies tha t character ize the

surface of pathog ens Janeway, 1989). S nail lectins occu r in soluble form, and

associated with the cell mem brane of defence cells. Re cent molecu lar studies

suggest that snails produce com plex and highly diverse lectins Kurachi et al.

1998; Zhang

e t aL

2001). The binding of a snail lectin to pathog en-asso ciated

carbohydrates is thought to activate a snail defence response, comprising

humoral and cellular com ponents van der Knaap et al. 1982, 1983; Richards

and Renw rantz, 1991; Hor~ik and van der Knaap, 1997; Horftk and De m e,

1998; HorLk

et al.

1998c).

The hum oral de fence s of snails include several agglutinins and toxic activ-

i ties for review see A dem a and Loker, 1997). Study of gene expression in L.

s tagnal i s after infection with T. oce l la ta Ho e k et al. 1996, 1997) identified a

cDN A transcr ip t tha t was named mol luscan defence molecule MD M), based

on sequence similari t ies with the haemolin, a soluble immune protein with

opso nic properties, present in insects Schm idt et aL 1993). Planorbid snails

produced increased amoun ts of several parasite-reactive plasma polypeptides

in response to echinostom e parasites. Am ong these are lectins of a large and

diverse gene family of f ibrinogen-related proteins FREPs). FRE Ps have been

found in several planorbid species; no sequence data are available to suggest

that lymna eid snails also em ploy FRE Ps Ad em a et al. 1997; Zhang, 2001).

The fun ctional aspects of both MD M and FR EP s remain to be clarified further.




Ce l l - f r ee p lasm a o f s evera l lym nae id and p lanorb id sna i ls con ta ined an ac t iv -

i ty tha t k i l l ed incompat ib le in t r amol luscan t r ematode l a rvae in v i t ro S a p p

and Loker , 2000) .

H a e m o c y t e s , p h a g o c y t i c c e l l s t h a t c i r c u l a t e i n t h e b l o o d , c o n s t i t u t e t h e

m a j o r c e l l u la r d e f e n c e s o f s n a il s. A c t i v a t e d h a e m o c y t e s m i g r at e t o w a r d s a n d

t h e n p h a g o c y t o s e o r e n c a p s u l a t e p a t h o g e n s . T h e i n t e r n a l i z e d p a t h o g e n s a r e

e l imina ted b y ce l l -med ia ted cy to tox ic i ty . In v i t ro k i ll ing o f incom pat ib le s ch is -

t o s o m e l a r v a e b y h a e m o c y t e s o f

L . s t a g n a l i s

a n d o t h e r s n a i l s i n v o l v e s

l y s o s o m a l e n z y m e s a n d t o x i c c h e m i c a l s s u c h a s r e a c ti v e o x y g e n i n te r m e d i a te s

D i k k e b o o m

et a l .

1 98 8; A d e m a

et a l .

1993, 1994; Hahn

et a l .

2 0 0 1 a ) a n d

n i tr ic ox id e Ha hn e t a l . 2001b) .

Several fac tors such as age o f snails, pol lu t ion a nd the presen ce o f o ther par -

a s it e s r e d u c e t h e fu n c t i o n in g o f th e i n te r na l d e f e n c e s o f sn a il s D i k k e b o o m e t

al .

1985 ; Russo and Lagad ic , 2000) . Genera l ly , however , sna i l s have po ten t

de fenc es tha t succes s fu l ly e l imina te invad ing pa thogens R ichards e t aL 1992;

Gras s i et a l . 2001) . I t i s rem arkab le then that in som e comb inat ions , snai ls fa i l

t o e l im i n a t e a n i n v a d e r a n d b e c o m e i n f e c t e d b y s c h i s t o s o m e p a r a s it e s.

4 .4 . 2. P a r a s i t e -i n d u c e d c h a n g e s i n c e l l u la r a n d h u m o r a l i m m u n i t y

S c h i s t o s o m e s e m p l o y b o t h p a s s i v e a n d a c t i v e s t ra t e g ie s t o s u r v i v e th e i n t e r-

n a l d e f e n c e s o f s na i ls i n o r d e r t o e s t a b l i s h a s u c c e s s f u l in f e c t io n . H o w e v e r ,

c i r c u m v e n t i n g t h e h o s t d e f e n c e s i s li k e l y t o b e a h i g h ly c o m p l e x p r o c e s s th a t

i s s u c c e s s f u l o n l y i n a l i m i t e d r a n g e o f s n a i l s t ra i ns o r s p e c i e s . U p o n e n t r y

in to a sna i l, a s ch i s toso m e wi l l de p lo y it s pa r t i cu la r su rv iva l s t ra t eg ies to try

a n d p r e v e n t a h o s t d e f e n c e r e s p o n s e . O n l y t h e d e f e n c e s y s t e m o f a s u i ta b l e

sna i l is r end ered ine f f ec t ive ; the in te rna l de fen ces o f r e s i s t an t sna i l s rem ain

u n a f f e c t e d a n d e l i m i n a t e t h e s c h i s t o s o m e p a r a s it e . I t i s l i k e l y th a t t h is l e a d s

t o th e r e s tr i c te d i m m u n o b i o l o g i c a l c o m p a t i b i li t y b e t w e e n s c h i s t o s o m e s a n d

snails .

A s c h i s t o s o m e c a n p a s s i v e l y d is p l a y s u r f a c e m o i e t i e s t h at a r e n o t r e c o g -

nized as fore ign to evad e recogn i t ion as non-sel f . I f an invading p athog en is not

de tec ted , the in te rna l d e fenc e sys tem o f the sna i l rem ains inac t ive . Indeed , the

c o m p o s i t i o n o f c a r b o h y d r a t e m o i e t ie s o n t h e s u r f a c e o f T .

oce l l a ta

and T.

szi-

da t i c h a n g e s c o n s i d e r a b l y w h e n a m i r a c i d i u m t r a n s f o r m s i n t o a s p o r o c y s t

G e r h a r d u s

et a l .

1991 ; Hor~k , 1995) , bu t the func t iona l s ign i f icance r ema ins

to be de te rmined . Sch i s tosomes may a l so mask the i r su r f ace w i th hos t - l ike

ep i topes . Th i s can be ach ieved by abso rb ing hos t -de r ived f ac to r s on to the su r-

f ace mo lecu la r mask ing) . T r i chob i lharz ia oce l l a ta m ay em ploy th is s t r at egy :

i m m e d i a t e ly a f te r e m e r g i n g f r o m d a u g h t e r s p o r o c y s ts , ce r c a ri a w e r e o b s e r v e d

to acquire hos t - l ike fac tors onto thei r sur face that b ind ant isera ra ised agains t

p lasm a o f the hos t , L. s tagnal i s R o d e r et a l . 1977; van der Knaa p et a l . 1985).



186 P. HORAK L. KOLAROVA AND C.M. ADEM A

S c h i s t o s o m e s a l s o d i s p l a y m o l e c u l a r m i m i c r y , t h e e x p r e s s i o n o f h o s t- l ik e

de te rminan t s f rom genes o f the pa ras it e i ts e l f. The qu es t ion has been r a i s ed

wh e ther s imi la r gene p roduc t s p ro tec t the pa ras i te o r wh e the r s eq uenc e s imi -

la r i t i e s be tween pa ras i t e and hos t have r esu l t ed f rom convergen t evo lu t ion

Yosh ino and Bo swe l l , 1986 ; Dam ian , 1987 ; D is sous and Capron , 1995).

Sch i s toso m es a l so ac t ive ly inh ib i t hos t de fenc es . Af te r the in i ti a l obse rva-

t i o n t h a t e c h i n o s t o m e p a r a s i t e s r e n d e r e d h o s t s n a i l s s u s c e p t i b l e t o

s c h i s t o s o m e s f o r w h i c h t h e y w e r e n o r m a l l y r e si s ta n t L i e e t a l . 1976) , i t

w a s d e t e r m i n e d t h a t s c h i s t o s o m e p a r a s i te s a l s o r e d u c e t h e d e f e n s i v e c a p a -

b i l it i e s o f s n a il s L i e a n d H e y n e m a n , 1 9 7 7 ). T h e i n t e r f e r e n c e h y p o t h e s i s

L i e , 1 9 8 2 ) p r o p o s e s t h a t s c h i s t o s o m e s a n d o t h e r t re m a t o d e p a r a s i te s i n t er -

f e r e w i t h t h e f u n c t i o n o f s n a i l h a e m o c y t e s i n o r d e r t o s u r v i v e w i t h i n t h e

hos t . T r i c h o b i l h a r z i a o c e l l a t a m e d i a t e s i n t e r f e r e n c e i n d i r e c t l y b y r e l e a s i n g

s e c r e t e d a n d / o r e x c r e t e d p r o d u c t s S E P ) t h a t i n t e ra c t w i t h th e c e n t r a l n e r v -

o u s s y s t e m C N S ) o f t h e

L . s t agna l i s

t o a f f e c t t h e i n te r n al d e f e n c e s y s t e m o f

t h e s n a il A m e n a n d d e J o n g - B r i n k , 1 9 9 2 ). C o n c o r d a n t w i t h t h e s e f i n d i n g s

i s t h e d e m o n s t r a t i o n o f a lt e re d g e n e e x p r e s s i o n i n th e C N S o f L . s t a g n a l i s

af te r in fec t ion w i th T . o c e l l a t a H o e k e t a l . 1 9 9 7) . A m o n g t h e s u p p r e s s e d

m e s s a g e s w a s th a t o f t he p u ta t iv e d e f e n c e f a c to r M D M H o e k

e t a l .

1996) .

I t i s a s s u m e d t h a t t h i s r e d u c e s t h e e f f i c i e n c y o f h o s t d e f e n c e s , b e n e f i t in g t h e

p a r a s it e . C h a n g e s i n t h e e x p r e s s i o n l e v e l s o f n e u r o e n d o c r i n e f a c t o r s H o e k

e t a l . 1 9 9 7 ) a r e a ls o th o u g h t t o a f f e c t t h e h o s t d e f e n c e s d e J o n g - B r i n k ,

1995) .

T h e S E P r e l e a s e d b y s c h i s t o s o m e s m e d i a t e d i r e c t i n t e r f e r e n c e e f f e c t s

t o w a r d s s n a il h a e m o c y t e s . C o - i n c u b a t i o n o f s n a il h a e m o c y t e s w i th S E P c o l -

l ec ted f rom la rva l s ch i s tosom es o r w i th spo rocys t s inh ib i ts s evera l func t iona l

p roper t i e s o f these de fence ce l l s such as in t race l lu la r p ro te in syn thes i s Lo des

et a l . 1991), haem ocy te mo t i li ty Lod es and Yosh ino , 1990) and p roduc t ion o f

o x y g e n r a d ic a l s C o n n o r s e t a l . 1991) . T r i c h o b i l h a r z i a o c e l l a t a inh ib i t s

p h a g o c y t o s i s A m e n

et a l .

1 9 9 2) , e f f ic i e n c y o f e n c a p s u l a ti o n A d e m a

et a l .

1994) and bac te r i a l k i l ling N uf ez et a l . 1 9 94 ) b y h a e m o c y t e s f ro m L. s tag-

nal i s .

In the la t ter case , the k i l l ing act iv i ty of

L. s tagnal i s

h a e m o c y t e s w a s

i n h ib i te d b y a 4 0 - k D a p r o te i n c o m p o n e n t o f S E P f r o m T. ocel la ta . Intriguingly,

t h e 4 0 - k D a f a c t o r d i d n o t a f f e c t th e b a c t e r i c id a l a c t iv i ty f r o m h a e m o c y t e s o f a

non-hos t snai l

P l a n o r b a r i u s c o r n e u s

Nuf iez and de Jong-Br ink , 1997 ; Nuf iez

e t a L 1997) . This f inding seems to under l ine the fac t that the capabi l i t ies for

imm unom odu la t ion o f s ch i s tosom es a re res t r ic ted to a f f ec t on ly h os t Snail s. A t

th is t ime , s eq uen ce in fo rmat ion i s no t ava i l ab le fo r any cand ida te in te r f e rence

factors .

C l e a r l y , m u c h r e m a i n s t o b e l e a r n e d a b o u t t h e c l o s e a n d s p e c i f i c a s s o c i -

a t i o n b e t w e e n s c h i s t o s o m e s a n d s n a i l s t o u n d e r s t a n d f u l l y h o w t h e l a r v a l

d e v e l o p m e n t i n t h e i n t e r m e d i a t e s n a i l h o s t c u l m i n a t e s i n t h e r e l e a s e o f

ce rca r iae .




5. DEVELOPM ENT IN VERTEBRATE HOSTS

5.1. Host finding

The mature cercariae are released from snails in high quantities, especially on

sunny days preced ed by an overcast period. Cercaria are thought to use secre-

tions of specialized glands to pass through the snail tissues (T. szidati, see

Neuh aus, 1952a). Free-living cercariae nee d to infect a final host quickly as the

parasites have o nly a short life span after emerging from the snail into the water

(1-1 .5 day at 24 °C; Ne uhaus, 1952a). Characterization of the host-finding

behav iour o f T.

ocellata

(Haas 1992, 2001 for reviews) revealed that the cer-

cariae exhibit a posit ive phototactic and a geonegative orientation and can

swim bo th backwards and forwards (Figure 8). A forward sw imm ing response

towards shadow s, water turbulence and touch affords a high probability of con-

tact with a final host (Feiler and H aas, 1988a).

Prior to an initial contact, cercaria e are selectiv ely attracted to, and attach to,

substrates that display physical and chemical properties of wa rm-b looded ver-

tebrate skin. Not al l warm surfaces are equally at tractive; cercariae of T.

ocellata

can differentiate their preferred temp erature w ith a sensitivity of only

1 °C (Feiler and H aas, 1988a). Cercariae also react to chem ical signals.

Trichobilharzia

sp. cercariae released from

Physa acuta

were attracted by

linoleic acid (Graczyk and Shiff, 2000), a fatty acid that also attracts

S. man-

soni

(Shift

et al.,

1993; Shift and Graczyk, 1994). Skin surface lipids such as

ceramides and cholesterol are important stimuli for attachment of T.

ocellata

(Feiler and Haas, 1988b). Feathers covered by the uropygial gland secretions

lack these particular lipids allowing cercaria e to preferentially attach to the skin

of birds. D ue to a similar l ipid com posit ion o f the skin of birds and mam mals,

the cercariae are not able to avoid penetration into m amm als and cause cer-

carial dermatitis (see section 6.2.1 .).

5.2. Penetration of the V ertebrate Skin

After contact with the host the cercariae of T.

ocellata

show several behav-

ioural patterns: attachm ent to the host, enduring contact, leech-like creeping to

a suitable entry site (wrinkles in the skin or openings of hair follicles) and pen-

etration (Figure 8). On average, the creeping be hav iour lasts 8 s, ranging from

0 to 80 s (Haas and H aberl, 1997; H aas and van de Roe me r, 1998). N ot all cer-

cariae init iate penetration efforts following attachment. Appleton and Brock

(1986) est imated that 85.2 of

Trichobilharzia

sp. cercariae (released from

Lymnaea natalensis

attem pted to penetrate m ous e skin. Af ter 1 h, 59 of the

cercariae had procee ded to enter the skin, whereas the remaining 41 were



188 R HORAK L. KOLAI~OV A AND C.M. ADEMA

. . . . . { Stimuli: slladow I~ ~

M I G R A T I O N

h

WA T E R R E S E R VO IR H O S T S K IN

Figure Behaviour of Tnchobilharzia befor e and after the penetration into a v ertebrate

host behaviour of free-l iving cercariae modified after Haas, 1992).

The free-liv ing cercarial stage o f T.

ocellata

shows pho totactic and geonegative orienta-

t ion. Additionally, i t displays four types of behaviour: 1) Resting posture is a motionless

posit ion in which p arasites cling to the w ater surface with the acetabulum, the tai l hangs

downward and the furcae are relaxed; cercariae do no t respond to water currents or touch.

2) Forward swimm ing body first) . This behaviour is st imulated mainly by passing shad-

ows. The d irection of sw imm ing is directed away from the light source; the furcae of the tail

are folded together; only in this phase do cercariae respond to thermal and chemical verte-

brate cues that induce attachment. 3) Back ward swim min g tail first) towards l ight

upward) is st imulated by a contact with inapprop riate substrates. 4) During the passive

phase cercaria e sink down using the furcae as a drag anchor. T he active phase 2 or 3) alter-

nates with the passiv e phase 1 or 4).

Aft er contact with the host, T.

ocellata

shows four patterns of behaviour: 1) at tachment

to the host st imulated by warmth and surface l ipids - ceramides and cholesterol); 2)

endurin g contact; 3) creeping to a suitable entry site; and 4) penetratio n stimulated by

fatty acids). At the start and during p enetration, the contents of the penetratio n glands are

released. The penetration process is accom panied by penetration movements contractions

and elongations of the body, me chanically supported by the spines that cover the body ),

shedding of the tai l and transformation of the tegument. The g land secretions surround the

schistosomulum and l ine the entry tunnel. After the init ial phase of skin infection, visceral

Trichobilharzia

species usual ly enter the lymphat ic or venous sys tem whereas nasal

Trichobilharzia migrate via peripheral nerves.




s t i l l a t t ached by the sucker s to the ep ide rmis . Comparab le obse rva t ions were

m a d e f r o m T. r e g e n t i Hrf idkovf i and HorLk, 2002) . Perhaps cercar iae do not

a l w a y s e n c o u n t e r a p p r o p r i a t e s i g n a l s to i n i ti a t e p e n e t r a t i o n o f t h e h o s t.

Ho we ver , ce rca r iae can a l so es tab l i sh exper imen ta l ) in fec t ion pe ro ra l ly , pen -

e t ra t in g m u c o s a o f t h e o r a l c a v i t y M a c y

e t a l . ,

1955) . Th i s sugges t s tha t

ce rca r iae a re no t h igh ly r es t ri c ted in r ecogn iz ing and pene t r a t ing the d i f f e ren t

ep i the l i a o f a ve r teb ra te .

W hereas wa rmth a lone has no e f f ec t , pene t r a t ion i s s t imu la ted by f r ee f a t ty

ac ids s a tu ra ted ac ids w i th 9 -1 4 C a tom s and unsa tu ra ted ac ids ; the pene t r a -

t ion - s timula t ing e f f ec t o f the l a t t e r ac ids inc reases w i th the num ber o f dou b le

bonds ; Fe i l e r and Haas , 1988a ; Haas and van de Roemer , 1998) . The h igh

leve l s o f such f a t ty ac ids in hum an sk in s t imu la te h igher r a tes o f ce rca r ia l pen -

e t r at ion in humans than in the na tu ra l duck hos t. The na tu re o f s t imu la to ry hos t

s i g n a l s m a y b e s p e c i e s - o r g e n u s - s p e c i f i c ; a n o t h e r b i r d s c h i s t o s o m e ,

A u s t r o b i l h a r z i a t e r r i g a l e n s i s , in i t ia tes penetra t ion in response to f ree s tero ls ,

wh ereas f a t ty ac ids have on ly a w ea k e f f ec t C legg , 1969) .

The ce rca r iae s t a rt the pene t r a t ion p roces s by a t tach ing the head o rgan to the

sk in su rface , in a s imi la r fa sh ion as desc r ibed fo r hum an sch i s tosom es S .

m a n s o n i . L i k e S . m a n s o n i H o w e l l s e t a l . , 1975), T. o c e l l a t a sheds the ta i l a t

th i s t ime by the con t rac t ion o f a sph inc te r musc le a t the ce rca r ia l h indbody

Haa s and van de Ro em er , 1998) . Som et im es the ta i l i s shed ea r l ie r du r ing the

c reep ing p hase . The con ten t s o f the pene t r a t ion g lands a re re leased on to the

sk in . These con ta in p ro teo ly t i c enzymes , inc lud ing e las tase , a 30 -kDa se r ine

prote inase T. o c e l l a t a ; s e e B a h g a t e t a l . , 2001 ; Bahg a t and Rupp e l , 2002) . Th i s

c a n b e o b s e r v e d h i s t o l o g i c a l ly b y a d i s ti n c t l y s is o f t h e s t r a tu m c o r n e u m

B o u r n s e t a l . , 1973 ; Haas and van de Romer , 1998) . Moreover , de tec t ion

wi th f luo resce in - labe l l ed l ec t in s show ed tha t g land depo s i t s su r round the pen-

et ra t ing paras i te T. s z i d a t i and l ine the r esu l t ing en t ry tunne l in the hos t

t issue HorS_k

e t a l . ,

1998b) . The g land sec re t ions con ta in add i t iona l types o f

b i o a c t i v e m o l e c u l e s .

T r i c h o b i l h a r z i a s z i d a t i

releases a lectin specif ic for 13-

1 , 3 - g l u c a n a n d g l y c o s a m i n o g l y c a n s t h a t m a y b e i n v o l v e d i n r e c o g n i t i o n o f

hos t connec t ive t i s sue and ac t iva t ion o f pa ras i te e f f ec to r m olecu les e .g . p ro -

teases ) . O ther than ca rbohydra te -b ind ing p roper t i e s , no add i t iona l ac t iv i t i e s

have been de tec ted fo r th i s l ec t in Hor f tk

e t a l . ,

1997) . Th e ly t ic a t tack on the

sk in and under ly ing t i s sues , com bine d wi th in te rmi t t en t con t rac t ions o f the

bo dy wh ich i s cov ered w i th t egumen ta l sp ines , a l low s ce rca r iae to d i s rup t and

pene t r a te the sk in o f the hos t . Usu a l ly , ce rca r iae o f T . o c e l l a t a pene t r a te in a

near ly su r face -para l le l d i r ec tion to the s t ra tum corneu m befo re en te r ing deeper

t i s s u e l a y e r s . O n a v e r a g e , t h e p a r a s i t e s p a s s t h r o u g h t h e s t r a t u m c o r n e u m

wi th in 4 -5 m in and the s t r a tum ge rmina t ivum i s pene t r a ted a t 3 h p . i. Bou rns

e t a l . ,

1973 ; Ha as and van d e Roem er , 1998).



190 R HOR, ,K, L. KOL,~I~OV, ,AND C.M. ADEMA

5.3. Cercaria Schistosomulum Transformation and Immune Evasion

With the transition from free-living to parasitic life inside the final host, the

parasite undergoes a second transformation, from cercaria to schistosomulum.

This transformation is accompanied by a substantial reconstruction of the sur-

face. The thick cercafial glycoca lyx is shed, which considerably changes the

antigenic properties of the parasite. This is demon strated b y low recognition o f

the parasite s surface by lectin probes and anti-cercarial antibodies. T his state

remains for several hours or even days and may represent a way to escape

recognit ion by the host imm une system (Hor~k

et al.

1998b). The outer tegu-

mental m embrane is replaced by a doub le mem brane (Hor~ik et al. 1998b) that

is typical for all bloo d-dw elling adult tremato des (spirorchids, sanguinicolids,

schistosomes; McLare n and Hockley, 1977). The outer mem brane of human

schistosomes is thought to also have imm une-evasive properties.

Addit ional factors may protect the parasite from immune attack. The cer-

cariae of T.

ocel la ta

possess enzym es that conv ert C20 polyunsaturated fat ty

acids (most notably arachidonic acid) into eicosanoids (lipid mediators) such

as prostaglandins , leukotr ienes and hydroxyeicosate t raenoic ac ids .

Interestingly, eicosanoids are produced at levels similar to those of human

schistosomes (Nevhutalu et al. 1993). These bioactive com pound s m ay cause

vasodilatation in host tissues, and suppress immune functions such as super-

oxide product ion by human neutrophi ls (Nevhuta lu

et al .

1993) and the

migration of epidermal Langerhans cells , which play a key role in the imm une

defence system (Angeli

et al.

2001).

5.4. Migration

Shortly after comp letion o f the transformation, schistosomula o f the visceral

species of

Trichobilharzia

leave the skin and enter the blood vessels of the host

to mature and spend their adult life in the circulatory syst em (see section 5.4.5

for information on nasal species). Adult parasites usually reside in portal or

intestinal veins o f naturally infe cted hosts, sites that are typical also for sp ecies

of the genus

S ch i s to so ma

(for review see Basch, 1991). Base d on this similar-

ity, it is expected that

Trichobi lharz ia

follows the same migration route as

S ch i s to so ma ( for review see Bayssade-Dufour et al. 1994), entering lym-

phatic or ven ous vessels and continuing via the fight heart to the lungs, the left

heart and the systemic circulation to the f inal location. The receptors and

mechanism s that guide the path of migration through the host are not under-

stood (Basch, 1991). Interestingly, the parasites migrate along similar routes in

both ( imm unologically and p hysiologically) compatible f inal (bird) hosts and

incompa tible hosts. H owever, parasites do not start reproduction in incompat-

ible hosts and die at various intervals p.i.



IOLOGY OF

TRICHOBILHARZIA 9

5.4.1. Visceral schistosom es in the skin ph as e

a) C om patible hosts. A compar i s on o f t he num ber o f ce r ca r iae tha t pene t ra t ed

the sk in and the nu m ber of wo rms reco vered from in te rna l o rgans ind ica tes tha t

m an y paras i tes fai l to cross the skin. E l l is et aL (1975) su gge s ted that schis to-

som ula tha t a re unable to break the corn i f i ed l ayer s a re perman ent ly t r apped in

the sk in . The passage of sch i s tosomes th rough the sk in seem s to de pend m ain ly

on the im m un i ty s ta tus of the hos t ( see sec t ion 6.1 .4 .) . Re la t ive to p r imary

infec t ions , the number of T . ocel lata s ch i s t o s omul a t r apped i n t he s k i n o f

ducks inc reased wi th r epea ted cha l leng e in fec t ions (Bourns et al . , 1973; Ellis

et al., 1975; Rau et al., 1975). Suc cessful schis tosom ula of T. ocellata l eave the

duc k sk in wi th in 3 days p .i. (Bourns et aL, 1973). Trichobilharzia migra tes

rap id ly a f te r en te r ing the c i rcu la tion , espec ia l ly in co m par i son w i th S. man soni

(Haas and Pietsch, 19 91) . By day s 3 and 4 p.i ., 36 o f the paras i tes or iginal ly

presen t in the sk in were de tec ted in var ious in te rna l o rgans (Bourns et al.,

1973; H aas a nd Pietsch, 1991).

b ) Inco mp atible hosts . Avian sch i s tosomes , inc lud ing Trichobilharzia spp.,

m ay or m ay n ot be ab le to c ross the sk in o f an inappropr ia te ver tebra te hos t.

Fo r i n st ance , C e r ca r ia pa r oce l la t a d i d no t pene t r a te be yond t he ep i de r mi s o f

hum ans (M acfar lane , 1952). As observed f rom the b i rd sch i s tosom e A. terri-

galensis , f a i lu re to pen e t ra te r esu l t s in incre ased m or ta l i ty o f parasi tes in the

skin (Rai and Clegg, 1968) . In contras t , some schis tosomula of T. ocel lata

l e ave t he mous e s k i n s oon a f t e r pene t r a t i on , a l t hough o t he r s can s t i l l be

extra cted f rom the sk in by day 4 p. i. (Haas a nd Pietsch, 1991) . As in the bi rd

hos t s, surv iva l o f the paras i tes de pend s heavi ly on the im m un e s ta tus of the

host (se e sect ion 6.2.1 .) . In prev ious ly unse ns i t ized rabbi ts T. ocel lata and T.

s tagnicolae surv ived up to 48 h p .i. How ever , m any o f the wo rm s had d ied in

the sk in of sen s i t ized rabbi ts by 6 h p . i. (Ol ivier and Weins tein, 1953).

5.4.2. Visceral schisto som es in the lung ph ase

a) Compatible host . On the w ay towards the sys tem ic c i r cu la t ion , the lungs

represen t the f i r s t t a rge t o rgan tha t i s invaded b y migra t ing sch i s tosom ula , as

rep or ted fo r several species : T. cam ero ni, T. oregonensis, T. pa roc ella ta an d T.

ocellata (Mc M ul len and Beaver , 1945; Wu, 1953; M acy et aL, 1955; I s l am an d

Co pem an, 1986). W ithin 1-2 days af ter pene trat ing the skin T. ocellata invades

the lungs and rema ins there be tw een 4 and 16 days p .i. D ur ing th is t ime the

paras i t es g row and feed on the hos t b lood (Bourns et al . , 1973; Ell is et al. ,

1975; Haas and P ietsch, 1991; HorLk and Kol~i~ov& 2000). On ce in the lungs

the paras it es l eave the v enou s sys tem and proba bly rem ain ex t ravascu lar ly in

the a i r spaces for a cer ta in am oun t o f time. Th ey m igra te f rom a i r cap i ll a r ies

and parabron chi to secon dary bronchi , then invade the bronchia l ep i the l ium



192 R HOR ~ K L. KOLAROVA AND C.M . ADEM A

and ga in en t r ance in to ves se l s (Bourns et al., 1973) . The lun gs represe nt a d i f -

f i c u l t b a r r i e r a n d o n l y s o m e s c h i s t o s o m u l a a r e a b l e t o p a s s t h r o u g h . E v e n

d u r i n g p r i m o i n f e c t i o n s o f c o m p a t i b l e h o s ts , s c h i s t o s o m u l a a re f re q u e n t l y

t r apped dur ing the lung pas sage . In con t ras t to the lungs , a low er recov ery r a te

fo r T. ocel lata wo rm s wa s r epor ted fo r duc k l iver s and in tes t ine ( e .g . Ha as and

Pietsch, 1991).

b) Incompat ible hos t . I n s e v e r a l c a s e s , a v i a n s c h i s t o s o m e s i n v a d e t h e

l u n g s o f i n c o m p a t i b l e h o s t s. T h i s w a s f ir s t d e s c r i b e d f o r s c h i s t o s o m u l a o f T.

s tagnicolae in Sw is s mice , T . ocel lata i n S w i s s m i c e , h a m s t e r s a n d m o n k e y s ,

and T. phys e l l ae in mice a t 4 -7 day in te rva l s p . i . (O l iv ie r , 1953) . A pu l -

m o n a r y p h a s e w a s a l s o r e c o r d e d f r o m m i c e i n f e c t e d w i t h T .

brevis

( B a s c h ,

1966) ,

Trichobi lharz ia

sp . (App le to n and Brock , 1986) and T.

sz idat i

( H o r L k

and Kol~ i~ov~i, 2000) . S im i la r ob se rva t ions w ere r e por te d fo r o the r s ch i s to -

some genera , i . e . Austrobi lharz ia, Bi lharz iel la a n d Orni thobi lharz ia ( B a c h a

et al. , 1982; Hor~ik and Kol~i~ ov~i, 200 0; B ay ssa de -D uf ou r et a l . , 2001) . Th i s

s u g g e s t s t h at l u n g m i g r a ti o n s a r e c o m m o n t o a ll v i s c e r a l s p e c i e s o f s c h is t o -

s o m e s .

The m ig ra t ing s ch i s tosom ula can r each the lungs w i th in 10 h p . i. (T.

ocel-

lata i n m o u s e ; H a a s a n d P i e t s c h , 1 9 9 1 ) . U s u a l l y , t h e s u r v i v a l t i m e i n a n

inco m pat ib le ho s t is shor t. Ho we ver , T.

szidati

w o r m s m a y p e r s is t in t h e m o u s e

lungs for u p to 10 day s p . i. (Hor~ik and Kol~ir ov~i, 2000 ) . H aas and P ie tsc h

(1991) r epo r ted tha t , desp i t e a s ign i fi can t dec rease in pa ras i t e num ber w i th in

the f i r s t 5 days , s ch i s tosom ula o f T .

ocel lata

su rv ived in the lungs o f mice u p

to 6 days p. i .

S u b s e q u e n t ly , w o r m s d i s a p p e a r f r o m t h e i n c o m p a t i b l e h o s t s. T h e f a c to r s

i n f l u e n c i n g s u r v i v a l o f l u n g s c h i s t o s o m u l a a r e p o o r l y u n d e r s t o o d .

Sch i s tosomula o f T . szidati s e e m m e t a b o l i c a l l y a c t iv e i n t h e l u n g s o f i n c o m -

p a t i b l e h o s t s ; t h e i r g u t c o n t a i n s a d a r k p i g m e n t e v i d e n t l y d e r i v e d f r o m

dige s t ion o f ery thro cyte s of the h os t (Hor( tk and Kol~i~ov~i, 2000 ) . P erha ps the

p a r a s i t e s a r e e l i m a t e d b y a h o s t i m m u n e r e s p o n s e . H o w e v e r , e l e c t r o n

m i c r o s c o p y o f T. szidati i n th e l u n g s o f m i c e s h o w e d n o d a m a g e t o t h e t e g u -

m ent and an abs enc e o f hos t im m un e cel ls (Hor~ik and Kol~i~ ov~i, 2000 ) . T he

au thor s hyp o thes ize d tha t fa i lu re o f the pa ras i te d u r ing a p r ima ry in fec t ion o f

a n i n c o m p a t i b le h o s t m a y r e s u l t fr o m s o m e i m m u n o l o g i c a l ly u n r e la t e d f a c t o rs

(absence o f e s sen t i a l nu t ri en ts , e t c . ). A c om par i son o f the pu lm ona ry phase o f

infect ion s how ed that T.

szidati

sch i s tosomula g row and f e ed rap id ly in a duck ,

w h e r e a s i n a m o u s e t h e y s e e m t o b e i n h i b i t e d i n d e v e l o p m e n t ( H o r ~ k a n d

Kol~ir ov~i, 20 00 ). A s su gg est ed b y Kol~i~ ov~i(2001) , surv ival o f paras i tes in the

lungs can a l so be in f luenced by the i r s i ze; s ch i s tosom ula o f ce r ta in spe c ies can

be too l a rge to en te r lung cap i l l a r ie s and to m ig ra te in a non - spec i f i c host .



BIOLOGY OF

TRICHOBILH RZI

93

5.4.3. Visceral schistoso me s in the l iver pha se, f in al location a nd egg

product ion

a) Compatible host . Afte r re -en te r ing the sys tem ic c i rcu la t ion , the p a ras i te s

m igrate to a f inal locat ion . In mos t cases , adul t schis to som es concentra te in the

por ta l o r in tes t ina l ve ins o f the ven ous sys tem . Th is sug ges t s tha t the s ch i s to -

som ula o f v i s ce ra l av ian s ch i s tosom es deve lop in to adu l t s in the po r ta l ve ins ,

s imilar to Schis tosoma spp . The f ew ava i l ab le da ta ind ica te tha t the p repa ten t

p e r i o d f o r Trichobilharzia in fec t ions i s abo u t 12 -14 day s Neu haus , 1952a ;

Basch , 1966 ; Bourns et al. , 1 9 7 3 ; M e u l e m a n et al. , 1984b) . The s t im ul i tha t

g u i d e t h e m i g r a t i o n o f a d u l t w o r m s a n d t h e e x a c t l o c a t i o n f o r e g g - l a y i n g

remain to be fu l ly charac te r i zed . However , adu l t worms o f d i f f e ren t spec ies

appea r to f avour pa r t i cu la r s i t es fo r ov ipos i t ion . Depe nd ing on the spec ies o f

Trichobilharzia, paras i t e eggs have bee n de te c ted in the in tes t ina l w a l l o f va r-

i o u s p a r t s o f t h e s m a l l a n d l a r g e i n t e s ti n e s , i n c l u d i n g t h e c l o a c a o f b i r d s

M cM ul len and Beaver , 1945 ; W u, 1953 ; Yam agu t i, 1971). The m ig ra t ion o f

adu l t s to s i te s where e gg- lay ing o ccur s m ay b e s imi la r to tha t p ropo sed fo r A .

variglandis W ood and Bacha , 1983). The f em ale worm s tr ave l f rom ves se l s o f

the in tes t ina l s e rosa th rough the muscu la r i s ex te rna and c rawl by means o f

bo dy con t rac t ions in to sm al l ve ins o f the mu cosa . Af te r the r e lease o f eggs , the

worms re tu rn to the s e rosa . Th i s a l lows the smal l mucosa l ve ins to con t rac t

a r o u n d t h e n e w l y d e p o s i t e d e g g s , k e e p in g t h e m i n t ha t p l a ce .

The e ggs pas s f rom the m ucosa l ves se l s th rough the connec t ive ti s sue o f the

lamina p ropr ia in to the in tes t ina l lumen . As sugges ted fo r human sch i s to -

s o m e s , t h e p r o g r e s s io n o f e g g s m a y b e d u e t o a c o m b i n a t i o n o f h o s t

in f lamm ato ry r eac t ions an d eg g-der ived p ro teases , r e su l ting in ly s i s o f the t is -

s u es . T h e f in d i ng o f f r e q u e n t a c c u m u l a t i o n s o f l e u c o c y t e s a ro u n d e g g s l o c a t e d

wi th in b lood ves se l s suppor t s th i s v iew W ood and Bacha , 1983). M uscu la r

c o n t r a c ti o n s o f t h e h o s t m a y f u r t h e r h e l p t h e e g g s t o p a s s t h r o u g h t h e c o n n e c -

t ive t i s sue in to the in test inal lume n Bloch , 1980) . F inally, the eggs are re leased

f rom the in tes tines w i th the f aeces whe n the b i rd de feca tes .

I t i s no t c lea r whe the r adu l t av ian s ch i s tosom es spend the i r en t i re l i fe in the

por ta l and /o r in tes tina l ve ins. O n a t l eas t two o ccas ions , adu l t wo rm s have be en

encountered in the in tes t inal t i s sues . Adul t T. ocel lata m igra te to ve ins o f the

s m a l l i n t e s t i n e a n d s u b s e q u e n t l y p e n e t r a t e t h e m u c o s a , s o m e t i m e s e v e n

approach ing the tops o f v i l li Bou rns et aL, 1973) . S imilar ly , N euh aus 1952 a)

reco rde d m atu re ad u l t s o f T.

szidati

i n m u s c u l a r is s u b m u c o s a a n d th e m u c o s a

of the in tes t inal wal l . B oth T. oceIlata and T. szidati d i s a p p e a r e d f r o m t h e h o s t

in tes tines a bou t day 21 p .i . Th i s t ime a l so co inc ides w i th the end o f the pa tency

of in fec t ion ; the b i rd hos t ceases to r e lease pa ras i te egg s in the f aeces Bou rns

et al. ,

1973 ; P . Hor~ ik , unp ub l i shed da ta) . B eca use a l l s ch i s tosom es no rm al ly

occ ur in the b lood sys tem, the i r loca t ion in the in tes t ina l t i s sues m ay rep resen t

a te rmina l phase o f the in fec t ion . Hyp o the t i ca l ly , the f lukes escape f rom the



194 R HOR, ,K, L. KOLAROV, , AN D C.M . AD EM A

b lood ves se l s du r ing th i s phase and a re des t royed in the t i s sues o r en te r the

in tes t ina l lum en , d ie and l eave the host . The dea th o f the adu l t worm s cou ld

e x p l a in t h e o b s e r v e d b r e v i t y o f

Tr i ch o b i l h a r z i a

infect ions .

T h e f a t e o f t h e m a j o r i ty o f a d u l t w o r m s in t h e p o s t p a t e n t p e r i o d r e m a i n s

to be de te rmined , a l though i t i s genera l ly a s su m ed tha t adu l t w orm s d ie soon

af te r depos i t ing the ir eggs . Howeve r , a l imi ted num ber o f worm s m ay l eave the

intest inal area to return to the l iver . Mature T.

p a r o c e l l a t a

we re found in po r ta l

ve ins o f the l ive r in a duck a t 86 day s p .i . ( I s lam and C opem an , 1986), and T.

o ce l l a t a

was ob se rve d in the l a tt e r o rgan eve n a t 248 and 370 da ys p .i. (Bourns

e t a l . , 1973) . In teres tingly , dead a nd dege nerat ing fem ales of T. p h y s e l l a e w e r e

f o u n d w i t h i n t h e i n t e r l o b u l a r b i l e d u c t s ( P e n c e a n d R h o d e s , 1 9 8 2 ) .

Rem arkab ly , adu l t pa ras i te s su rv ive fo r som e time in dead hos t s ; Sz ida t (1938)

r e c o v e r e d l i v i n g w o r m s f r o m d e c o m p o s i n g b i r d s t h a t h a d d i e d s e v e r a l d a y s

earlier.

The f ac to r s tha t de te rm ine the l i f e span o f these pa ras i te s r em ain unc lea r .

Never the les s , the pa tency o f


in fec t ions and po ten t i a l ly a l so the

l i f e span o f adu l t av ian s ch i s tosomes a re cons ide rab ly shor te r than those o f

hum an sch i s tosom es ( fo r r ev iew see Basch , 1991).

b ) I n c o m p a t i b l e h o s t . I m m a t u r e w o r m s a r e r a r e l y f o u n d i n t h e l i v e r o f

n o n - s p e c i f i c h o s t s . H o w e v e r , r a d i o l a b e l l e d T . o c e l l a t a w e r e s p o r a d i c a l l y

de tec ted in the mouse l ive r and in tes t ine on days 2 -5 p . i . (Haas and P ie t s ch ,

1991). T he lon gev i ty o f these pa ras i te s in the l ive r r em ains un know n, b u t

appears to be shor ter than that in the lungs .

5 . 4 .4 . E g g d i s s e m i n a t i o n a n d a t y p i c a l m i g r a t i o n o f v i sc e r a l s c h i s to s o m e s

As oc cur s in hum an sch i s tosomias i s ( fo r r ev iew see Bacha e t a l . , 1982) , par t of

t h e e g g s o f Tr i ch o b i l h a r z i a spec ies f a i ls to l eave the b i rd hos t and i s d i ss em i -

na ted v ia the c i r cu la to ry sys tem to the l iver , lungs and o the r o rgans (M cM ul len

and Beaver , 1945 ; W u, 1953). T he num ber o f eggs in va r ious o rgans , and

as soc ia ted pa tho logy ( s ee s ec t ion 6 ) , inc rease w i th h igher worm burdens . In

heav y in fec t ions , ad u l t f lukes m ay r es ide in a typ ica l loca t ions w i th in the hos t .

T h e i n f e c t i o n b y 3 0 0 - 4 0 0 s p e c i m e n s o f T . p h y s e l l a e resul ted in equal d is t r i -

bu t ion o f worm s over the lungs , live r and in test ine o f a canary (M cM ul len and

Beaver , 1945) . I t i s l ike ly that addi t ional obse rvat ions o f adul t paras ites in a ty p-

ical s i tes , e .g.T, o ce l l a t a in the lungs (B ourns e t a l . , 1973) and Tr i ch o b i l h a r z i a

s p . i n g o n a d a l , g a s t r ic , o e s o p h a g e a l , j u g u l a r , f e m o r a l a n d t h y r o i d a l v e i n s

(Wojc insk i

e t a l . ,

1987) and in in te r lobu la r b i l e duc t s (Pence and Rhodes ,

1982), w ere du e to h igh in fec t ion do ses a l so .




5 . 4 . 5 . N a s a l s c h i s t o s o m e s

So m e sch i s tosom e spec ies ma tu re in the nasa l a rea o f a fina l hos t. O f on ly n ine

s p e c i e s t h a t w e r e d e s c r i b e d t o d a t e ,

S . n a s a l e

b e l o n g s t o t h e g e n u s

S c h i s t o s o m a . T h e o t h e r s a r e r e p r e s e n t a t i v e s o f th e g e n u s T r i c h o b i l h a r z i a

HorS_k

e t a l . ,

1998a) . Excep t fo r T .

r e ge n t i ,

the re a re no de ta i l s ava i l ab le

regard ing the mig ra t ion rou tes to the nasa l t is sues .

a ) C o m p a t i b l e h o s t . The m ig ra t ion rou te o f a nasa l s ch i s toso m e such as T.

r e ge n t i

d i f f e rs d ram at ica l ly f rom those o f v i s ce ra l s ch i s tosome s Hor~ik

e t a l . ,

1999; H rMkov~i and HorS~k, 2002 ) . Af te r penetra t ing the sk in o f a duck, T.

r e ge n t i i n v a d e s p e r i p h e r a l n e r v e s . T h e s c h i s t o s o m u l a t h e n m i g r a t e f u r t h e r

t h r o u g h t h e ce n t ra l n e r v o u s s y s t e m C N S ) , p r o g r e s s in g t h r o u g h t h e s p i na l

co rd and the b ra in . U l t ima te ly , the s ch i s tosom ula loca te to b loo d ves se l s in the

nasa l a rea where they com ple te the ir ma tu ra t ion to adu l t wo rms , m a te and p ro -

duce eggs . The p rogres s ion th rough the ho s t CN S i s fa st: s ch i s tosomu la can be

de tec ted in pe r iphera l ne rves b y day 1 .5 p.i., in the sp ina l co rd by d ay 2 p . i and

in the bra in by da y 12 p. i. Hr~idkov~i and Hor~ik , 2002 ) . Th e n asal are a is

r eached by day 13 p .i. HorSk e t a l . , 1 99 9). E g g s a r e p r o d u c e d b y f e m a l e s a s

ear ly as 14 da ys p . i. HorS_ke t aL , 1999). Con t ra ry to v i s ce ra l s ch i s tosome s ,

m i rac id ia ha tch f rom the eg gs d i r ec t ly in the nasa l so f t t i s sues Hor~ ik e t a l . ,

1998a). Th e l i fe sp an o f T. r e ge n t i i n a d u c k i s e s t im a t e d t o b e 2 3 - 2 5 d a y s . T h e

e n d o f th e p a t e n t p e r i o d a p p e a r s t o b e c h a r a c te r iz e d b y m i g r a t io n o f a d u l ts

f rom ve s se l s in to the su r round ing ex t r avasa l t i s sues o f the nasa l a rea HorLk

e t

aL , 1 9 9 9; K o l ~ o v ~ i e t a l . , 2001) .

b ) I n c o m p a t i b l e h o s t. Infect ion o f T. regent i i n m i c e i s a l so a c c o m p a n i e d b y

i n v a s io n b y s c h i s t o s o m u l a o f t h e C N S . T h e p a r a s it e s e n t e r t h e p e r ip h e r a l

ne rves , mig ra te to the sp ina l co rd by day 2 p .i .) , and r each the b ra in by d ay 3

p .i . Hr~dkov~i and HorLk, 2002 ) . Con trary to the es tabl ishm ent and repro duc -

t ion o f worm s in ducks , the in fec t ion o f mice f a i l s and r esu lt s in the dea th o f

paras i tes in va r ious par ts o f the C N S Hor~ik and Kol~i~ov~i, 2001 ) . Th e p ara-

s i te s t r iggered a hos t imm une r esp onse s ee s ec t ion 6 .2 .2 .) . Th i s can pa r t ly

exp la in the inco m ple te deve lo pm en t o f the worm s Kol~ i~ov~i

e t aL ,

2001) .

A com para t ive s tudy o f the mig ra t ion o f T . r e ge n t i in su i tab le versus unsui t -

a b l e i n c lu d i n g im m u n o d e f i c i e n t an d i m m u n o c o m p e t e n t ) v e r te b r a t e h o s t s

d i s c l o s e d d i f f e r e n c e s i n t h e r a t e o f m i g r a t i o n d u r i n g t h e f i r s t 3 d a y s p . i .

Hr~ idkov~i and H or~k , 2002) . D ur ing th is t ime , wo rm s w ere r ec ove red f rom

the syn sac ra l and tho rac ic sp ina l co rd o f ducks . In s evera l s tr a ins o f m ice

tested , the T.

r e ge n t i

had p rogres sed fu r the r , hav ing r eached the ce rv ica l sp ina l

c o r d a n d m e d u l l a o b l o n g a t a , a n d i n S C I D m i c e , e v e n t h e c e r e b e l l u m .

D i f f e r e n c e s in b o d y s iz e o f th e h o s t m a y a l s o a f f e c t t h e r a te o f m i g r a ti o n , a s

sugges ted fo r v i s ce ra l s ch i s tosom es M cM ul len and Beaver, 1945). The mig ra -

t io n r a te o f w o r m s w a s f a s t e r i n th e C N S o f S C I D m i c e t h an i n t h at o f

im m uno com pete n t BA LB /c and hr /h r ) mice Hr~idkov~i and Hor~ik , 2002) .



1 9 6 P. HO RA K, L. KOL, .I~OV.,~A N D C . M . A D E M A

In te rest ing ly , the h ighes t numbers o f wo rms were found in the synsac ra l sp inal

co rd o f ducks and the tho rac ic sp inal co rd o f mice . M any pa ras it e s r emained in

these loca t ions a l so du r ing the l a t e r phases o f in fec t ion ) and on ly a sm al l pe r -

cen tage o f wo rm s m ig ra ted fu rthe r.

O n r a re o c c a s i o n s , j u v e n i l e s o f T. regent i and T . a r c u a t a w e r e o b s e r v e d in

the lungs o f bo th duck and mur ine hos t s I s lam, 1986b ; Hor~ ik

e t a l .

1999;

Hnidkov~i and H onik , 2002 ) . I f these paras i tes re ta in the a bi l i ty to reach thei r

f inal locat ion , i t can b e hyp othe s ized that these paras i tes use the arter ia l sys te m

o f the hos t to mig ra te f rom the lungs to the nasa l a r ea o f a duck .

6 V E R TE B R AT E I M M U N E R E S P O N S E A N D P A T H O L O G Y

S c h i s t o s o m e s a r e c o n s i d e r e d t o b e h i g h ly p a t h o g e n i c f o r m i g r a to r y w a t e r f o w l

G r a c z y k e t a L 1993). T he genera l p auc i ty o f r epor t s dea l ing w i th c l in ica l

aspec t s , pa tho log y and im m uni ty o f t r ichob i lha rz ias i s ca n be exp la ined in pa r t

b y t h e e a s e w i t h w h i c h t h e p a ra s i te s c a n b e o v e r l o o k e d d u r in g g r o s s n e c r o p s y

due to the i r smal l s i ze and occur ren ce w i th in b lo od ves se l s W ojc insk i e t a l .

1987). T he av a i l ab le da ta focus m os t ly on sym ptom s o f pa ten t in fec t ions in

b i rds. Ho we ver , r ecen t inves tiga t ions have e luc ida ted tha t imm atu re f lukes

a l so may cause s evere t i s sue in ju r i es . There fo re , the spec t rum o f syndrom es is

p r o b a b l y w i d e r t h a n p r e v i o u s l y c o n s i d er e d .

Cerca r ia l de rm at it is in mam ma ls i s bu t one f am i l ia r a spec t o f the pa tho logy

that b i rd schis tosomes cause in incom pat ib le hosts. Desp i te the fa ilure to develop

ful ly , the paras i tes penetra te and migrate in mammals dur ing ear ly phases of

infection in a s imilar fashion to that ob serv ed in avian hosts . T hese nov el findings

warrant that the ro le o f these paras i tes in o ther pathological ch ange s o f t i s sues

and organ s shou ld b e rea sses sed HorS_k and Kol~i~ov~i, 2001 ).

6 1 C o m p a t i b l e H o s t s

6 . 1 .1 . F a c t o r s i n f l u e n c i n g s e v e r i t y o f i n f e c ti o n s

Par t icu la r s ch i s toso m e in fec t ions in w a te r fow l d i f fe r in s ever ity . In genera l ,

p a t h o g e n i c i t y o f e a c h s p e c i e s is d e te r m i n e d b y p a ra s it e b i o l o g y e .g . m e t a b o -

l i sm, f eed ing , mo b i l i ty ) and m orph o log y e .g . s ize ) , p re fe r r ed s i te o f the adu l t

w o r m s , t h e w o r m l o a d a n d t h e d u r a ti o n o f in f e c ti o n . S e v e r e d a m a g e t o t is s u e

and o rgans r esu l ts f rom accum ula t ion o f num erous pa ras i t e s in ves se l s and d i s -

s e m i n a t i o n o f m a n y e g g s o f t h e p a r a si te t o v a r io u s o r g a n s o f th e h o s t

W o j c i n s k i e t a l . 1987) . Whereas mi ld in fec t ions w i th v i s ce ra l s ch i s tosomes

o f t e n a r e s u b c li n ic a l o r e v e n a s y m p t o m a t i c M a c y e t a L 1955; Basch , 1966) ,




even a sm al l nu m ber of nasa l s ch i stosomes in c lose proxim i ty to the bra in m ay

cause severe syndrome s . The sever ity o f in juries ma y progres s w i th t ime as the

paras i tes pers is t in th e hos t .

A l s o i m m a t u r e s c h i s t o s o m e s m a y s e v e r e l y i m p a i r t h e h o s t . I n s o m e

i nst ances , i nvasi on o f t he l ungs by h i gh n um ber s o f v i s ce ra l s ch i s to s omes

induce s suf f i c ien t lung dam age to cause dea th M cM ul len and Beaver , 1945;

W u, 1953). D ur ing the prepa ten t per iod of in fec t ion , m igra t ing sch i s tosomula

o f T. r e ge n t i can m ech anica l ly dam age a nd d es t roy nervous ti ssue . Po ten ti a lly ,

the paras i te a l so r e leases m etabol it es and o ther secre tory or ex cre tory product s

t ha t may be neu r o t ox i c . T he number o f pa r a s i t e s add i t i ve l y i nc r eas es t he

pathology Kol~i~ov~ie t a l . 2001) .

Th e resul t ing cl inical picture i s inf luen ced by inna te suscept ibi l ity and sui t -

abi l ity as wel l as by ac quired imm un i ty o f the hos ts . In the f ie ld , the prevalen ce

o f


i n f ec t i ons d i f f e r s am ong va r i ous av i an s pec ie s e .g .

Apple ton , 1986; Loken e t a l . 1995) a nd usua l ly the preva lenc e in ad ul t s is

lowe r than in you ng b i rds Guth e t a l . 1979). T he s tudy of s e ra f rom b i rds tha t

w er e r epea t ed l y in f ec t ed s how ed t ha t acqu i r ed i mm un i t y inc r eas es w i t h age

and prev ious exposure to T r i c h o b i l h a r z i a parasites . T r i c h o b i l h a r z i a - r e l e a s e d

ant igens evoke imm un e reac tions a round the paras it es. De ad w orm s induce the

s t ronges t r esponses , p robably d ue to the r e lease of l a rge amo unts o f an t igens

Kol~i~ov~i

e t a l .

2001). Sp ec ifica lly, T.

r e g e n t i - i n f e c t e d

bi rds produce an t i -

bodies aga ins t gu t -as soc ia ted an t igens GA A) of adul t wo rm s Koufilov~i and

Kolff fov~, 2002) . I t is o f interes t that repe ated infe ct ions by cerca r iae resul t in

a r edu c t ion o f s ever i ty o f T. o c e l l a t a infect io n in bi rds El l i s e t a l . 1975; Rau

e t a l . 1975). N ever the les s , t r ans fer o f lym pho id ce ll s and /or imm un e serum

did n o t co nve y s ign if i can t l eve ls o f pas s ive im m uni ty to T. o c e l l a t a in ducks

Bo urns a nd El l i s, 1975) .

6 . 1 .2 . C l i n i c a l f e a t u r e s

Th e m ajor i ty o f synd rom es tha t a re usua l ly as soc ia ted wi th t r ichobi lharz ias i s

occu r dur ing the pa ten t phase o f in fec t ion , due to in jur ies to t i ssues and organs

t h a t d e v e l o p i n c l o s e p r o x i m i t y t o t h e s i t e s w h e r e e g g - l a y i n g w o r m s o f

T r i c h o b i l h a r z i a res ide. Howev er , cercar ial invas ion into the skin and the m igra-

t i on o f i mmat u r e pa r a s i t e s a l s o caus e va r i ous d i s o r de r s . Fo r i n s t ance ,

pu l monar y s ympt oms may appea r s ho r t l y a f t e r t he pene t r a t i on by v i s ce r a l

s ch i s to s om es . I n f ec t i ons o f duck s b y T. r e g e n t i s how ed t ha t t he p r epa t en t

phas e can be m an i f e s t ed by neu r om ot o r s ym pt om s ba l ance o r o ri en ta t ion

di sorder s and pareses ) due to the migra t ion of th is nasa l s ch i s tosom e through

the CNS o f the hos t HorS ,k e t a l . 1999).

W hereas b i rds appear to to le ra te m i ld in fec tions wi th v i scera l s ch is tosomes

r e la t ive l y w e l l M acy e t a l . 1955; Basch , 1966), he avy in fec t ions m ay cau se



198 P. HOR.~K, L. KOLAI~OV, , AN D C.M. AD EM A

swelling of feet and legs, em aciation, weigh t loss and stunted growth Ma cy

et

al. 1955; Wojcinski et al. 1987). Moreover, death was ascribed to

Trichobilharzia

infections: in birds infected ex perime ntally with T.

ocellata T.

oregonensis and T. elvae Brumpt, 1931; Macy et al. 1955), and in wildfowl

harbouring T. physe l lae Pence and Rhodes, 1982), Trichobilharzia sp.

Graczyk et al. 1993) and Trichobilharzia sp. + Dendri tobi lharz ia sp.

Wojcinski et al. 1987). T he pa tent perio d of T. regenti infections can be asso-

ciated with bleeding of the nasal muc osa Hor~k et al. 1999).

The dissemination of eggs to various organs and t issues ma y cause non-

typical symptoms during the chronic phase. These include prol i ferat ive

conjunctivitis in Haw aiian goose d ue to Trichobilharzia sp. eggs Schm~ischke

et al.

1992) and neurological problems displayed by birds that have eggs o f

Trichobilharzia sp. in the brain Gra czy k et al. 1993).

6.1.3. Gross pathol ogy

Trichobi lharzia infect ions are ini t ia l ly character ized by skin symptoms.

Penetration of T.

szidati

and T,

regenti

cercariae in skin o f duck freque ntly

leads to rapidly developing ma cular eruptions HorS.ket al. unpub lished data),

follow ed by crust formation and scaling of the affected tissues at 2- 3 days p.i.

Ellis et al. 1975). Subsequently, migrating schistosom ula m ay cause haem -

orrhage, inflammation and subsequent consolidation of the t issue in the lungs

McM ullen and Beaver, 1945) and, in cases o f heavy infections, enlargemen t

and abscessation of the liver M cLe od and Little, 1942).

Patent infections with low num bers o f parasites m ay result in two different

types o f lesions Penc e and Rhod es, 1982). 1) M inor lesions associated with

the eggs o ccu r mo stly in the liver and intestines. The surface of livers of ducks

infecte d with T. brevis Basch, 1966) and T. oregonensis Macy et al. 1955)

displaye d w hite cysts 150 and 175 I.tm in diam eter, respectively. Potentially,

severe infections cause livers to enlarg e and have a pale aspect, an d cross-sec-

tions disclose a friability of the liver tissue Pen ce and Rhodes, 1982). Th e

intestinal mu cos a contains granu loma s evide nt as reddish and soot-like spots),

although w ea k infections are limited to some slo ughing o f the internal intes-

t inal wall M cL eod and Lit t le, 1942). T he egg dissemination by venou s

circulation may also result in lesions in other organs. In Hawaiian geese,

whitish proliferative alterations occurred in the sclera, nictitating membrane

and conjunctiva, accom panied occasionally by microabscesses Schm~ischke et

al.

1992). 2) The accu mu lation of numero us adults in mesen teric veins leads

to major lesions. These enc ompa ss thrombosis, thickening and congestion of

the intestine with a granular f ibrino-haemorrhagic exudate adherent to the

mucosa l surface due to host immu ne reactions), pulmo nary congestion and

hepatomegaly Wojcinski et al. 1987).



BIOLOGY OF

TRICHOBILH RZI

99

O n occas i on , t he p r e s ence o f egg - l ay i ng nas a l s ch i st o s omes caus es haem -

or rhages and pe tech iae in the nasa l cav i ty of b i rds Fa in , 1956a; Hor~ik

et a l . ,

1999); an und e t e r m i ned


spec ies caused rh in i t i s in a swan

Pa lm er and Ossen t , 1984) .

6 . 1 . 4 . H i s t o p a t h o l o g y a n d i m m u n o l o g y

The main pa tho log ica l a l t e ra t ions caused by b i rd sch i s tosomes in a hos t a re

probab ly due to eggs r a ther than to adul t paras it es Sz ida t and Wigand , 1934;

Szidat , 1938) . Neve r theless , in so m e cases , t i ssue les ions can b e a t t ributed also

to imm ature and mature sch i s tosom es Penc e and Rho des , 1982) .

a) Sk in l e s ions . Soo n af ter invas ion 5 m in p.i .) , the paras i tes cau se a dis -

t inc t lys is o f the

s t ra t u m c o r n e u m

in the du ck sk in Bourns

et a l . ,

1973; Haas

and van de R oem er , 1998). L a t e r on , t he pa ra s i te s a r e s u r r ound ed by an

i n f l amm at o r y r eac ti on , the i n tens i ty o f w h i ch depends on t he t i m i ng o f i n f ec -

t ion and im m un e s tatus o f the a f f l i c t ed hos t. In ch ickens and p igeons in i t ia l ly

i n f ec t ed by

Orn i thob i lharz ia cana l i cu la ta ,

t he i n f l amm at i on a r ound t he pa r a -

s i tes was ob serv ed as ear ly as 12 h p.i . Later , cel l inf i l tra t ion his t iocytes and

heterophi l s ) be cam e s t ronger, acco m pan ied by per ivascu lar in f il t ra t ion in the

de r mi s M or a l e s

et a l . ,

1971) . However , the react ion in the skin of ini t ia l ly

i n f ec t ed an i ma l s i s p r obab l y no t s t r ong enough t o p r even t t he s ubs equen t

mi g r a t i on o f s ch i s t o s omul a . T he da t a o f E l l i s

et al .

1 9 7 5 ) o n w o r m l o a d

reduc t ion in duc ks cha l l eng ed by T .

oce l l a ta

sugges t tha t r epea ted in fec t ions

resul t in s t imulat ion o f hos t imm un i ty to the e xtent that i t increases the t rapping

of paras i tes in the hos t skin. A s imilar ef fect was desc r ibed for T r i chob i lharz ia

infe ctio ns o f an in co m pa tible ho st Fig ure 9a; Kou~ilov~i an d Kol~i~ov~i, 200 1)

o r f o r S . manson i in a com pat ib le hos t von L ich tenberg and Ri tch ie , 1961).

b) L ung l e s ions . Lun g les ions a re caused by migra t ing sch i s tosom ula usu-

a l ly v i scera l s ch i s tosomes ) ; the paras i tes occ upy a i r spaces Bou rns

et a l . ,

1973; Ellis et al . , 1975) a nd fee d on re d b lood ce l ls . Dur ing ear ly in it ia l in fec-

t ions , the paras it es evoke on ly we ak in f l amm at ions . Chal l enge in fec t ions of

bi rds led to s t ronger cel lular inf il t ra t ion predo m inant ly lym ph oid cel ls ) arou nd

T. oce l la ta . T he obs e rva t ion o f dead and dy i ng w or ms i n t he cen t r e o f the s e

inf lamm at ions in the lungs con f i rmed the e f fec t iveness of the im m un e response

in im m un e hos t s E l li s

et a l . ,

1975) . Dur ing the chronic phase , the eggs of

T r i chob i lharz ia

i nc it ed mi no r l e s ions , va r y i ng f r om n one t o m ar ked g r anu l o -

m atous r eac t ions W ojc insk i et a l . , 1987) . In heavy infect ions , adul ts of O.

c a n a l i c u l a t a

i nvaded t he l ungs o f p i geons . T he vas cu l a r s y s t em d i s p l ayed

m edia l hype rp las ia , lym pho t ic endar te r i ti s and segm enta l p ro l if e ra t ion of vas -

cu l a r endo t he l ium . T he t is s ue o f t he l ungs con t a i ned g r anu l oma t ous r eac t i ons

cons i s t ing m os t ly of macrop hages , h i s tiocy tes , he te rophi l s and lym pho cytes )

t ha t s u r r ounded r emnan t s o f dead pa r a si te s M or a le s

et a l . ,

1971).



200 R HOR, ,K, L. KOLAROVA AND C.M . ADEMA

Figure 9 Histopath ological findings in com patible and incom patible hosts infected either by

nasal Trichobilharzia regenti) or v iscera l (T. szidati) bird schistosomes. (a) T. regenti schistoso-

mula in the skin of a mouse, reinfected for the fifth time; 4 h p.i. (PAS). The schistosomula

approaches the ep idermis (stratum reticulare). An inflammatory reaction, consisting of eosinophils,

neutrophils and macrophages (arrow) surrounds the parasite. (b) An egg of T.

szidati

in the liver of

a duck, 21 days after prim ary infection (PAS). Usually, eggs are surrounded by infl amm atory cells,

an inner la yer of giant cells and histiocytes, lymphocytes, plasma cells and m acrophages towards

the periphery. (c) An e gg o f T. szidati in the muscularis mucosae of the intestine of a duck (PAS).

The cellular reaction is similar to that in (b). (d)

Trichobilharzia

sp. mature flukes (arrow), located

intravascularly in the intestinal vessels of a naturally infected whooper swan (HE). (e) T. szidati in

the duck intestinal wall - primary infection of lam ina propria; 21 days p.i. (PAS). In certain cases

the worm s (arrow) reside in an extravascular location. (f) Adults o f T. regenti in the duck nasal

mucosa, 16 days after primary infection (HE). W orms are located intra- or extravascularly (arrow).

(g) The eg gs of T.

regenfi

in the duck nasal mucosa, 16 days after primar y infection (HE). Several

miracidia occur free in the mucosa. Some m iracidia are surrounded by a dense accumulation of

eosinophils, heterophils, histiocytes and mono nuclear cells, including volum inous giant cells. (h)

T. szidati schistosomula in the lungs during pri mary infection of a mouse; 3 days p.i. (PAS). The

immune reaction consisted of lym phocytes, neutrophils and macrophages. (i) T. regenti immature

worms in the white ma tter of the thoracic spinal cord during prim ary infection of mice; 3 days p.i.

(HE). No te the slight cellular infiltration around the parasites. Author of F igure 9a,i: P. Koufilov

Department of Tropical Medicine, Charles University, Prague, Czech Republic. Staining: periodic

acid-Schiff reaction (PAS); hematoxylin-eosin (HE).



BIOLOGY OF TRICHOBILH RZI 2 1

c ) L i v e r l e s i o n s . Sch is tosom e eggs F igure 9b ) a r e ca r ri ed to the live r v ia

the po r ta l ve ins du r ing the ch ron ic phase o f in fec t ion e .g . W ojc insk i e t a l . ,

1 9 8 7) . T h e e g g s u s u a l l y c a u s e g r a n u l o m a t o u s r e a c ti o n s in t h e l iv e r G r a c z y k

e t a l . ,

1993) . Ad u l t


a l so cau se l ive r l e s ions . O bs t ruc t ive f ib ro -

s is o f the po r ta l tr i ads m ay d eve lop in case o f hea vy in fec t ions , du r ing w h ich

a d u l ts m a y in v a d e t h e b i l e d u c t s a ls o P e n c e a n d R h o d e s , 1 9 8 2). D e a d w o r m s ,

i f t r a n s p o r t e d t o t h e l i v e r b y t h e c i rc u l a t i o n ) , e l i c i t m i x e d g r a n u l o c y t i c

i n fl a m m a t i o n . T h e s e l a r g e l e s io n s a r e a c c o m p a n i e d b y t is s u e n e c r o s is a r o u n d

t h e w o r m s P e n c e a n d R h o d e s , 1 9 82 ).

d ) I n t e s t i n a l l e s io n s . In test ina l l e s ions a re m os t ly due to eggs . The eggs a re

u s u a l l y l o c a t e d i n c l o s e p r o x i m i t y t o a d u l t w o r m s . W h e r e a s s l i g h t i m m u n e

reac t ions occu r a round v iab le eggs , g ranu lomas a re o f t en as soc ia ted w i th eggs

tha t unde rgo degenera t ion o r minera l i za t ion F igure 9c ; M cL eo d and L i t t le ,

1942 ; W ojc insk i e t a l . , 1 98 7). A d d i t i o n a l p a t h o l o g y m a y b e c a u s e d b y l o o s e l y

a g g r e g a t e d g r o u p s o f a d u l t


w o r m s i n s e r o sa l a n d m e s e n t e r i c

b l o o d v e s s e l s F i g u r e 9 d ; M c L e o d a n d L i t tl e , 1 9 4 2 ), a n d b y a d u l t w o r m s t h at

a re loca ted ex t r avascu la rly in the in tes tina l t is sue F igure 9e ) . Acc um ula t ion o f

n u m e r o u s w o r m s m a y b e a c c o m p a n i e d b y th r o m b i i n t h e v e in s a n d s u b s e q u e n t

ex tens ive haemor rhage and pe r ivascu la r mononuc lea r ce l l in f i l t r a t ion a round

ves se l s Wojc insk i e t a l . , 1987) . Heavy and ch ron ic in fec t ions may r esu l t in

th icken ing o f the in test inal wa l l W ojc insk i

e t a l . ,

1987) s imi la r to tha t cause d

b y A u s t r o b i l h a r z i a v a r i g l a n d i s W o o d a n d B a c h a , 1 9 8 3) .

e ) C N S l e si o n s. T h e nervous t i ssue incu rs dam age f rom eggs o f v i s ce ra l and

nasa l s c h i s tosom es tha t a r e d i s t r ibu ted b y the c i r cu la to ry sys tem. In a s imi la r

w a y t o t h at d e s c r i b e d f o r D e n d r i t o b i l h a r z i a sp . Lev ine e t a l . , 1956 ; W i l son e t

a l . , 1982) , eggs of T r i c h o b i l h a r z i a caused g ranu lomatous encepha l it i s in wa te r -

fowl . D is semina ted g ranu lomas con ta in ing cen t r a l ly loca ted eggs su r rounded

by g ian t ce l l s , macrophages , lymphocy tes , he te roph i l s and f ib rob las t s were

n o t e d i n c l o s e p r o x i m i t y t o t h e b l o o d v e s s e l s o f t h e

c e r e b r u m

a n d

c e r e b e l l u m

G r a c z y k

e t a l . ,

1993).

T h e a f f i n it y o f im m a t u re w o r m s o f n a s a l s c h i s to s o m e s T . r e ge n t i ) fo r ne rv -

o u s t i s s u e c a n c a u s e s e v e r e i n j u r y d u e t o m i g r a t i o n a n d e s t a b l i s h m e n t o f

para s i tes in the CN S Kol~i~ov~i e t a l . , 2 0 0 1 ). T h e p r e s e n c e o f th e w o r m s

induces in f l am m ato ry r eac t ions and pa tho log ica l changes in the ne rvous t i ssue

spong ios i s , eos inoph i l i c pe r ivascu l i ti s and dy s t roph ic and n ec ro t i c changes o f

neurons ) . Usua l ly , more p ronounced in f l ammato ry r eac t ions deve lop a t s i t e s

w i th num erous pa ras i t e s o r a round o lde r , dead and d i s in teg ra t ing w orm s .

f ) N a s a l l e s io n s . T h e l e s i o n s a r e p r o d u c e d b y e g g s a n d a d u l t s o f n a s a l

s c h i s t o s o m e s F a i n 1 9 5 6 a; K o l ~ o v ~ i e t a l . , 2 0 0 1 ) . W h e r e a s t h e e g g s w e r e

de tec ted on ly in the nasa l m ucosa , the adu lt s F igu re 9 f ) w ere loca ted in t ra -

and ex t r avascu la r ly Ko l~ov~ i

e t a l . ,

2001) . Pa tho log ica l chang es o f the ti s sues

su r round ing adu l t worm s have no t be en o bse rv ed to da te , bu t i t i s l ike ly tha t

these w i l l be s imi la r to those de sc r ibed fo r v i s ce ra l s ch i s tosom es in o the r pa r t s



2 2 R HOR, .K, L. KOI_,a.f~OVA AN D C.M. AD EM A

of the body. Ageing of the eggs resulted in various host reactions (Figure 9g),

ranging f rom focal accumulat ion of ce l ls to the format ion of granulomas

(Kol~i~ ov~i et al., 2001), s imilar to those described for visceral schistosomes

(e.g. Woo d and Bacha, 1983). In som e cases, the observation o f free miracidia

surrounded by an inflammatory reaction (Kol~i~ov~i

et al.,

2001) supported

the notion that these miracidia hatch directly in the host tissues (HorLk et al.,

1998a).

g) Other f indings.

Severe infect ions wi th v iscera l species of

Trichobilharzia

ma y result in occurrence of eggs, and both imm ature and adult

parasites in unusual sites (Wojcinski

et al.,

1987). In add ition to the portal and

mesenteric veins (normal locations), parasites were also discovered in caudal

renal , pulmonary, gonadal, gastr ic , oesophageal, jugular, femoral and thy-

roidal veins of birds. Eggs w ere detec ted in liver, co lon, sm all intestine, lungs,

kidney, spleen as well as in tissues of adrenal/gonads, brain, gizzard, proven-

triculus, oesop hagu s, sk eletal muscles and foo t web. Schm~ischke

et al.

(1992)

reported lesions containing

Trichobilharzia

sp. eggs with viable miracidia in

the sclera, nictitating membrane and conjunctiva of geese. Parasites and eggs

can induce imm une reactions and pathology in al l these unusual locations.

6.1.5. Diagnosis and therapy

The diagnosis of

Trichobilharzia

infections is focused primarily on micro-

scopical de tec t ion of eggs in b i rd excrements . Sedimen ta t ion techniques

(Kassai, 1999) facili tate the recovery of eggs with dev eloped miracidia from

faecal samp les of birds infected with visceral schistosomes. Eg g concentrations

are usual ly low, and th is necess i ta tes examinat ion of whole droppings

(Appleton, 1983). This is achieved by filtering and concentration ( by me ans o f

a formol--ether technique) of the sam ples prior to microscop ical examination

(Appleton, 1986). In the case of nasal schistosom es, fresh exudates from nasal

cavit ies are examined for eggs or free miracidia. Samples can be obtained

also by rinsing the nasal cavity with saline or wa ter (Hor~ik, unpub lished data).

In som e cases, tissue biopsies can b e exam ined h istologica lly (Schm~ischke et

al.,

1992).

Necropsy can reveal eggs in intestinal and nasal scrapings; adults and eggs

can be detec ted in squashed t issue samples or in s ta ined cross sec t ions .

Imm unodiagnostic tests are not used routinely in veterinary practice, but they

can be helpful in some cases . Ant ibodies agains t gut-associa ted ant igens

(GA A) of adult f lukes can be detected from ducks harbouring patent T. regenti

infections by means of indirect immunofluorescence and cross-sections of

adult sch isto som es (IFAT) (Kou~ ilov~i and Kohi~ov~i, 2002 ). A ltho ugh sensi-

t ive , th is assay cross-reacted wi th GAA of d i f ferent schis tosome species

(including

Schistosorna).



BIOLOGY OF

TRICHOBILH RZI

2 3

Praz iquante l s eem s to be a h ig h ly e f fec t ive an t ihe lmin th ic for the t r ea tm ent

of b i rd sch i s tosom e infec t ions B lanke spoor and Reim ink , 1991; Schm/ i schke

e t a l . ,

1992; Mtil ler

e t a l . ,

1993; Re imin k

e t a l . ,

1995) . A threefo ld appl icat ion

o f 200 m g t o ducks w i t h pa t en t


infect ion s at 24-h intervals led

to a perm ane nt r educ t ion in the r e lease of eggs wi th v iab le mi rac id ia MUl ler

e t a l . ,

1993). A s ing le dose of 200 m g/kg s ign i fi can t ly r edu ced paras it e load in

c o m m o n m e r g a n s e rs B l a n k e sp o o r

e t a l . ,

2001) . Doses of 22 mg/duck/day ,

appl ied for 1 we ek dur ing prepa tency , p revented the dev e lopm ent o f sch is to-

s omes com pl e t e l y M t i ll er e t a l . , 1993).

6 2 I n c o m p a t i b le H o s t s

6 . 2 .1 . C e r c a r i a l d e r m a t i t i s

Cercar ia l dermat i t i s is an a l l e rg ic r esponse to the pen e t ra t ion of sch i s tosom e

larvae in to m am m al ian sk in Cor t , 1928). I t deve lops a f te r r epea ted contac t s

hos t sens i tizat ion) wi th the cerca r iae Ol ivier, 1949). Ce rcar iae of the gen us

T r i c h o b i l h a r z i a a r e

the mos t com m on causa tive agen t Kohi~ov~i

e t a l . ,

1997).

a ) C l i n i c a l f e a t u r e s a n d g r o s s p a t h o l o g y . T h e s k in s ynd r om es deve lop i n

var ious m am m als , inc lud ing , fo r example , rabbi ts and dogs Herber , 1938;

Au gus t ine and Wel le r, 1949; O l iv ie r , 1953) bu t have m os t ly bee n descr ibe d

from aff l ic te d hu m an s e .g . Cor t , 1928; Vogel, 1930a; Brac ket t , 1940; Ol ivier ,

1949; Hae m m er l i , 1953; G ianot t i and Luvoni , 1958; Bearup and La ngs ford ,

1966; Margono , 1968; Hoef f ie r , 1977; B la i r and Co pem an, 1977; Apple ton and

Lethbr idge , 1979; Eklu-N atey

e t a l . ,

1985; Ba ird and Wear, 1987; W iley

e t a l . ,

1992; Chamot

e t a l . ,

1998). Th e as soc ia ted sym ptom s show only mino r d if -

f e r ences be t w een hum ans and an i ma l s.

Gross ly, cercar ial derm at i t i s represen ts a macu lopap ular skin erupt ion asso-

c ia ted wi th in tense i t ch ing . Cercar ia l pene t ra t ion in to the sk in resu l t s in a

pr ick l ing sensa t ion pr imary i tch ing) wi th in 4-2 0 min , per si s ting for up to 1 h .

Trans i to ry m aculae up to 10 m m in d iameter ) appear a t the s ites o f pene t ra tion

of ea ch cercar ia . Loc a l u r t i ca l r eac t ions have a l so bee n repor ted as d i scre te

i ndu r a ted papu lae t ha t reach 1 - 5 m m i n d i ame t e r . A l t hough t he m acu l ae u s u -

a l ly d i sappear in a f ew hours , they m ay per s i s t to be rep laced by d i s t inc t and

i ndu r a t ed papu l ae o f 3 - 5 m m i n d i ame t e r 10 - 15 h p .i .) T he deve l opm en t o f

papu l ae i s accom pan i ed by i n t ens e it ch ing s econda r y i tch i ng ). A n e r y t hem a-

t ous zone m ay deve l op a r ound t he papu lae w i th a cen t r a l punc t um. W hen t he

papu l ae a r e con f l uen t, t he w ho l e expos ed a r ea ma y be e l eva t ed and oe dem a-

t ous . O n t he s econd o r t h i rd day p .i., v e s i c le s 1 - 2 m m i n d iame t e r ) m ay f o r m

on t he papu l ae and t hes e o f t en rup t u r e w h en r ubbed o r s c r a tched . Papu lae

regress p rogress ive ly a f te r about 4 days and usua l ly d i sappear by d ay 10 p.i. to

leave a p igm ente d spot 1 --4 m m in d iameter ) tha t per s is t s fo r a mo nth or



204 R HORAK L. KOLAI~OVA AND C.M. ADEM A

longer . Sporad ic and in te rmi t ten t p rur itus m ay acco m pan y the sk in e rup t ion ; i t

t ends t o d i s appea r w i t h in s eve ra l days . T he t i m e cou r s e o f s k i n s ym pt om s

dep end s on the sen s i t ivi ty of the af f l ic ted perso n (Olivier , 1949) .

On ly m i ld r eac t ions oc cur dur ing in i ti a l in fec t ions , and the d i sease man i -

f e s t s i t s e l f on l y by deve l opmen t o f macu l ae . I f papu l ae deve l op , t hey a r e

us ua l ly s ma l l ( 1 - 2 mm ) , i nnocuous and i ncons p icuous . U s ua ll y , no s econda r y

i tch ing , oe dem a o r d i f f u s e e r y t hema a r e de t ec ted . Som e t i mes a de l ayed f o r -

mat ion (as l a t e as 8 days p . i . ) o f smal l papulae was no ted . In sens ib i l i zed

hos t s, papulae m ay o ccu r w i th in one h our o f pene t ra t ion by cercar iae . In th is

case , the papulae have ves ic les and increase to 3-8 m m in d iameter . Th ey are

as s oc ia t ed w i t h e r y t he m a ( 10 - 100 m m i n d i ame t e r) , oed em a and i n tens ive

prur itus . The sym ptom s ma y per s i st fo r a r e la t ive ly long pe r iod , a t l eas t 20

days i n one ca s e ( B ech t o ld e t a l . 1997) . Th e ery the m a s tarts to regress by day

3 p .i.; how ever , the s i ze depend s am ong o ther th ings on the ex ten t o f rubbing

or sc ra tch ing induced by the pruri tus . Exc or ia t ion m ay o ccu r w i th severe it ch-

i ng . Pus t u l e s do no t f o r m un l e s s t he l e s i ons become s econda r i l y i n f ec t ed .

Gen era l i zed sk in r eac t ions a re ra re bu t m ay s ta r t by da y 2 p .i . an d per s i st fo r

2 days . Th e rash cons i st s o f smal l (about 2 m m ) , hard and p ink papulae , which

are ve ry mild ly and inte rm it tent ly i tchy (Ol ivier , 1949).

Japanese r i ce p lan te r s f r equen t ly suf fe r cons iderab ly f rom repea ted in fec-

t ions by cercar iae . In severe cases , the pa t i en t s deve lop a chronic type of

d e r m a t i ti s c a l l e d k o g a n b y o i n w h i c h p a p u l o - v e si c u l a r e r u p ti o n s a p p e a r

m ain ly on the dor sa l s ide of hands and f inger s; s loughing and in jury of the sk in

is extens ive (Oda, 1973) .

M ass ive in fec t ions in hum ans m ay a l so cause f ever , l imb swel l ing , nausea

and d ia r rhea . Sk in l esions occu r on ly on par t s o f the body tha t w ere in contac t

wi th cercar iae , inc lud ing par ts und er swim m ing suits . Th e i t ch ing can rang e

f rom negl ig ib le to unbearab le , po ten t i a l ly c rea t ing a no ted insom nia (Cham ot

e t a l . 1998).

Sens ibi l izat ion m ay pers is t for years in hum ans (Ol ivier, 1949). Al tho ug h

few da ta a re ava i l ab le on the deve lopm ent o f r es i s tance aga ins t cercar ia l der -

mat i t i s , Macfar lane (1949) r epor ted immune ind iv idua l s among adul t s , bu t

no t in ch i ld ren . Repea ted contac t s w i th var ious spec ies o f cercar iae might

lead to dese ns ibi l izat ion (Berg an d Rei ter , 1960).

A l l r ep r e s en t a t i ve s o f t he genus T r i c h o b i l h a r z i a a n d o t h e r n o n - h u m a n

s c h is to s o m e s , s e e m t o p r o d u c e s i m i l a r sy m p t o m s w h e n i n f e c t in g h u m a n s

(Brack e t t , 1940; Cor t , 1950; Bat t en , 1956; Ma lek and A rm s t ron g , 1967;

App le ton and Lethbr idge , 1979; W i ley e t a l . 1992) . Th ere are no s ignif icant

d i f f e r ence s be t w een de r m a t i ti s occu r r i ng in f r e s h and s a lt w a t e r bod i e s

(Kol~ifov~i e t a l . 1989) . B y con t r a s t , human s ch i s t o s omes u s ua l l y i nduce

m i lder sk in r eac t ions (Basch , 1991). T hi s d i f f e rence m ay s tem f rom an inab i l-

i ty of T. o c e l l a t a t o p r o d u c e a m o l e c u l e a n a l o g o u s t o t h e 1 6 .8 - kD a

an t i -i n f lamm at o r y f ac to r f r om S . m a n s o n i ( R a m a s w a m y e t a l . 1996). In the



IOLOGY OFTRICHOBILH RZI

2 5

case of the l a t t e r paras it e , the ac t iva tion of the r ec ep tor fo r paras i t e -der ived

pros tag landin D 2 dram at ica l ly r edu ced the sk in hyper sens i t iv i ty r esponse a f t e r

cha l l enge ( A nge l i

e t a l . ,

2001).

Gen eral ly , i t is d i f f icul t to dis t inguish wh eth er skin react ions w ere ca used b y

b i r d o r human s ch i s t o s omes . I n s ome a r eas , b i r d and human s ch i s t o s omes

m ay co -occur , som et imes even in the sam e sna i l spec ies (Nass i, 1987). Th e

s imi la r ity in sym ptom s under l ines the nec ess i ty to co ns ider a l l t r ave ll e r s to be

pos i tive for s ch i s tosomias i s i f they acqu i red cercar ia l derm at i t is in a reas tha t

a r e endem i c fo r hum an s ch is to s omes .

b ) H i s t o p a t h o l o g y a n d i m m u n o l o g y .

Pathologica l e f f ec t s as soc ia ted wi th

penet ra tion of


cercar iae in to m am m als pr imar i ly depe nd on the

sens i tiv i ty o f the a f f l i c ted host s. No m arke d d i f f e rences were no ted for ce l lu -

l a r r esponses e i ther o f var ious m am m al ian spec ies aga ins t one


spec ies o r one m am m al aga ins t d i f f e ren t spec ies ( and genera) o f b i rd sch i s to-

somes . In i t ia l in fec t ions of rabbi t and m ouse sk in by Tr i ch o b i l h a r z i a (F igure

9a ) exh i b i t ed a m i xed i n f l amm at o r y exuda t e w i t h f ew eos inoph i ls and neu -

t rophi ls , s tar t ing by 6 h p . i. (A ug ust i ne and W el ler , 1949; O l ivier , 1953;

Kou~ilov~ a nd Kol~i~ov~i, 2001). Re pea ted infect ion s o f m ice s im ul tan eou s ly

resu l t ed in suba cute oedem atous derma t i ti s and increased num bers o f s ch i s to -

som ula t rapped in the skin (Kou~ilov~i, 2001) , s imi lar to that reco rde d f ro m

m i c e e x p o s e d t o

G i g a n t o b i l h a r z i a

(Bat t en , 1956) and

O r n i t h o b i l h a r z i a

( B a y s s a d e - D u f o u r e t a l . , 2001). Th e in f i lt r a tion by m elanoph ages and s inusa l

hype r p l a s i a , w i t h accumul a t i on o f me l an i n - l aden mac r ophages i n s ubcu t a -

neous l ymp h nodes , w as de t ec t ed on l y 30 m i n a f t e r t he l as t cha l lenge o f mi ce

i n f ec t ed w i t h


sp.; the m obi l i za tion of m elanot ic p igm ent i s

proba bly sec ond ary due to prur i tus an d scra tch ing of the ti s sue (Ba yssade-

D u f o u r

e t a l . ,

2001).

S t rong i n f l amm at i on a r ound the w or ms i n hum ans p r obab l y a ri se s i n hos t s

tha t have been in fec ted r epea ted ly . Th e observa t ions on th is top ic were m ade

from sect ions of biops ies taken f rom s i tes wi th papulae (e .g . Vogel , 1930b;

Bracket t , 1940; Macfar lane, 1949; Haemmerl i , 1953; Gianot t i and Luvoni ,

1958; M argono , 1968; App le ton , 1984). Th e occ ur ren ce of papulae sugges t s

tha t the sk in b iopsies w ere ob ta ined f ro m sens ib il ized subjects . Th e m os t com -

p r e h e n s i v e s t u d y o f H a e m m e r l i ( 1 9 5 3 ) d e s c r i b e d a t h r e e - p h a s e c e l l u l a r

response ( l eucocyt ic , lym pho cyt ic and h i s t iocy t i c ) , w hich l ed to the e l imina-

t i on o f


s ch i st o s omul a . D ur i ng t he l eucocy t i c phas e ( 3 - 9 h

p .i.), the paras it es w ere in tac t . The t egu m ent o f the paras i te s t a rt ed to deg rade

a t 24 h p .i. ( lymp hoc yt ic phase) an d sch i s tosomula were co m ple te ly des t royed

dur ing the h i s tiocy t i c phase (36-52 h p .i.) . Th e process was acc om pan ied by

per ivascu l i t i s and spongios i s o f the a rea sur rounding the paras i t es . T i s sue

repa i r (72 h p .i .) was acco m pan ied by parakera tos i s w i th r educ ed per ivascu lar

in f il tr a t ion in the sur rounding t i s sue ; a f t e rwards , ce ll me lanot ic p igm enta t ion

oc cu rre d (100 h p. i. ).



206 R HO RA K, L. KOL.~,I~OV, .AND C.M. ADEMA

T h e p r o g r e s s io n o f th e s k in r e a c t io n s d e s c r i b e d a b o v e m a y b e d e t e rm i n e d

b y t h e d e g r e e o f h o s t se n s i b il iz a t io n G a y

e t a l . ,

1 9 9 9 ) . W h e r e a s a m i l d

human r eac t ion to T .

o c e l l a t a

and T.

s z i d a t i

c o m p r i s e d o n l y l e u c o c y t i c v as -

c u l a r it i s w i t h p e r i v a s c u l a r d e r m a l i n fi lt r at e s o f l y m p h o m o n o c y t i c a n d

p o l y n u c l e a r t y p e , a s t r o n g r e a c t i o n i n a n o t h e r p a t i e n t w a s c h a r a c t e r i z e d b y

l y m p h o c y t i c v a s c u la r i ti s w i t h l y m p h o c y t i c d e r m a t i ti s t h a t o c c u r r e d a s e a r ly

as 10 h p. i .

T h e u s e o f IF A T- a n d E L I S A - b a s e d m e t h o d s d i s c l o s e d t h at T. s z i d a t i

i n f e c t io n i n m i c e l e d t o p r o d u c t i o n o f a n t i b o d i e s s p e c i f ic f o r c e r c a r i a e o f T.

s z i d a t i a n d S . m a n s o n i Kol~i~ov~ie t a l . , 1 9 9 4 ). H o w e v e r , t h e m o u s e a n t i se r a

d id no t r eac t w i th sk in and lung phase ) s ch i s tos om ula Hor~ ik

e t a l . ,

1998b) .

I t w a s o b s e r v e d t h a t th e p a r a s it e l o s e s t h e m a i n a n t i g e n ic s t ru c t u r e w h e n t h e

c e r c a r i a e l o s e th e c a r b o h y d r a t e - r ic h g l y c o c a l y x d u ri n g p e n e t r a t io n o f t h e

ho s t sk in .

6 .2 .2 . A d d i t i o n a l s y n d r o m e s

T r i c h o b i I h a r z i a i n f e c t i o n s m a y c a u s e o t h e r t y p e s o f s y m p t o m s i n v a r i o u s

s p e c i e s o f m a m m a l s . U n d e r c e r ta i n c i r c u m s t a n c e s e .g . f i rs t c o n t a c t w i t h

c e r c a r i a e ) , t h e t r a n s f o r m e d s c h i s t o s o m u l a c a n e s c a p e a n d m i g r a t e i n t h e

m am m al ian bo dy fo r r ev iew see Hor~ ik and Kol~ i~ov~, 2001) . Sc h i s tosom ula

o f v a r i o u s b i rd s c h i s to s o m e s T r i c h o b i l h a r z i a sp., T. oc e l l a t a , T . s z i da t i , T .

s t a g n i c o l a e , T . p h y s e l l a e , T . b r e v i s a s w e l l a s B i l h a r z i e l l a p o l o n i c a a n d


s p .) w e r e d e t e c t e d i n t h e l u n g s o f m i c e , h a m s t e r s , r a b b i ts ,

r h e s u s m o n k e y s a n d g e rb i l s O l i v ie r , 1 9 5 3 ; A p p l e t o n a n d B r o c k , 1 9 8 6 ; H a a s

a n d P i e t s c h , 1 9 9 1 ; H o r~ ik a n d K o l~ i~ ov ~i, 2 0 0 0 ; B a y s s a d e - D u f o u r

e t a l . ,

2001) , and add i t iona l ly in o rgans such as l ive r , k idney , hea r t and in tes t ines

Ha as and P ie t s ch , 1991) . In som e o f these an imals , in i t i a l in fec t ion r esu l t ed

i n m i n u t e p e t e c h i a e i n t h e l u n g s. D u r i n g t h e e a r l y p h a s e s o f s u c h i n f e c t io n s

i n m i c e t h e m a j o r i t y o f t h e s e l e si o n s w e r e b r i g h t r e d , d is t in c t , d i s c r e t e a n d

a p p a r e n t l y d i s t r i b u t e d a t r a n d o m o v e r th e p l e u r a l s u r f a c e o f t h e lu n g s . I n

som e cases , deeper , la rge r and da rk red haem or rhage s w i th d i f fuse and ind i s -

t i n c t m a r g i n s d e v e l o p e d w i t h p r o g r e s s i o n o f t h e in f e c t i o n O l i v ie r , 1 9 5 3 ) .

T h e l u n g s o f O r n i t h o b i l h a r z i a - i n f e c t e d g e r b i l s c o n t a i n e d n u m e r o u s w h i t i s h

n o d u l e s a l o n g s i d e p u l m o n a r y a n d c o l l a t e r a l a r t e r i e s , a n d t h e p e r i b r o n c h i a l

t re e s . S o m e n o d u l e s w e r e s c a tt e re d i n t h e p a r e n c h y m a B a y s s a d e - D u f o u r e t

a l . , 2001) .

In the lun gs o f T.

s z i da t i - i n i f i a l l y

in fec ted mice , m any s ch i stosomula F igure

9h) re s ided in the a i r spac es on d ay 4 p . i . L . Kol~i~ov~i, unp ubl ish ed data) .

I m m u n e r e a c ti o n s d e v e l o p e d a r o u n d m a n y i n t a c t p a ra s it e s; t h e i n f la m m a t io n s

w e r e m o s t in t e n s e a r o u n d o l d e r s c h i s t o s o m u l a M o r a v c o v ~ a n d K o l ~ o v ~ i ,

2001) .



IOLOGY OFTRICHOBILH RZI

2 7

Pr ev ious ly expos ed m amm al s gene r a l ly deve l op s t r onge r i mm une r e spons es

aga ins t the paras it es . Exam ina t ion o f the lungs o f gerb il s tha t were r e - in fec ted

w i t h


disc losed tha t m os t paras it es suf fe red dam age to the

t egumen t . M or eove r, l ymph ocy t i c vas cu li ti s occu r r ed a r ound l ive w o r ms and

w or m s t ha t had i ncu r r ed s ome t egum en t a l damag e . T he r e s u lt ing pa t ho l ogy

w as accom pan i ed by m ac r ophage a l veol it is i n t he pe r iphe r a l lung pa r en chym a

B ays s ade - D uf ou r e t a l . 2001).

Immature paras i t es o f T .

regent i

a nasa l spec ies o f

T r i c hob i l har z i a a r e

n e u r o t ro p i c a n d a l s o m i g r a t e t h ro u g h t h e C N S o f m a m m a l s . H i s t o lo g i c a l

exam i na t i on d i s c l o s ed bo t h i n t ac t F i gu r e 9 i) and des t r oyed w o r ms i n t he

nervous t is sue of mice Hor~ ik e t a l . 1999). C om pared w i th b irds , mice d i s -

p l ayed mor e v i go r ous ce l l u l a r r e s pons es t o t he pa r a s i t e s . T he s t r ong

inf lam m atory r eac t ions a roun d d i s in tegra t ing paras i tes w ere as soc ia ted wi th

d y s t r o p h i c a n d n e c r o t i c c h a n g e s o f n e u r o n s i n t h e s u r r o u n d i n g t i s s u e s

Kol~i~ov~i

et al .

2001). T he i n t ense i n f l amm at o r y r e s pons e m ay i n pa r t be t he

reason w hy T. r e ge n t i f a il s to deve lop com ple te ly in a non -spec i f i c hos t. Th e

es tab l i shme nt o f T. r e ge n t i in the CNS, and the as soc ia ted pa tho logy , may

lead to chang es in neurobeha vioura l r eac t ions of a f fec ted m am m als , s imi la r to

t h o s e d e s c r i b e d f r o m h u m a n n e u r o i n f e c t i o n s b y t h e g e n u s S c h i s t o s o m a

Scr im geo ur and G ajdusek 1985; Lam ber tucc i , 1993) . How ever , in the l a t t e r

case , the pa tho logy deve lops due to the d i s sem ina t ion of paras i te eggs to the

C N S.

6 .2 .3 . D i a g n o s i s a n d t h e r a p y

Differe nt ial diagn os is o f cercar ial derm at i t i s is di f f icul t . Th e resul t ing les ions

resem ble those tha t r esu l t f rom derm at i ti s o f bac te r i a l e tio logy , contac t der -

m at i t is or insect bi tes f rom chigg ers , f leas and mo squi toe s Ho eff ier , 1977).

How ever , c l in ica l and ep ide m iologica l da ta , toge ther w i th paras i to log ica l and

i mm uno l og i ca l d i agnos t ic m e t hods , ma y com bi ne t o i den t i fy ce r ca r iae a s t he

cor rec t e t io log ica l agent . Th ree c r i t e r ia a re the m os t imp or tan t am ong o ther

c l in ica l and ep ide m iologica l da ta : 1 ) r ecen t h i s to ry of a contac t w i th na tura l

wa ter bodies i.e . w i th in the prev ious 96 h) ; 2 ) dev e lopm ent o f a papular der -

ma t i t is w i t h s eve r e i t ch i ng be t w een 12 and 24 h a f te r expos u r e ; and 3 )

d i s tr ibu tion of these l es ions on ly on par t s o f the bo dy tha t w ere im m ersed in

the wa ter Ap pleton, 1984).

Inf requent ly , s ch i s tosomula can be de tec ted in sk in b iops ies t aken f rom

s i tes wh ere papulae have deve loped . How ever , th is m etho d can on ly be suc-

ces s f u l s ho r t ly a f t e r expos u r e . T he pa r a s i t e s a r e u s ua l l y des t r oy ed i n o r

m igra te ou t o f) the hum an sk in wi th in 24-7 2 h p .i. e .g . Hae m m er l i , 1953).

Addi t iona l ly , labora tory t es ts tha t m oni tor the im m un e reac t ions in pa t ien t s

can a id in the d iagnos i s o f cercar ia l dermat i t is . Cercar ia l dermat i t is m ay be



2 0 8 P . H O R , ,~ K , L . K O I_ ~,I~ O V, . A N D C .M . A D E M A

assoc ia ted wi th increased eos inophi l count s , as observ ed in hu m an v olun teer s

expos ed t o

H e t e r o b i l h a r z i a a m e r i c a n a

(Malek and Arms t rong , 1967) . Sk in

test s have been deve loped , based o n the eva lua t ion of e ry the m a tha t deve lops

a r ound i n j ec t ed an t igens , p r epa r ed b y hom ogen i za t i on o f e i t he r ce r ca ri ae o f

b i rd sch i s tosomes (Macfar lane , 1949) or adul t s o f S . m a n s o n i (Cort , 1936;

August ine and Wel ler , 1949; Moore e t a l . , 1968; Blackburn and Ma, 1971;

W i e d e r m a n n e t a L , 1973; Krampi tz e t a l . , 1974) or S . j a p o n i c u m (Hsii and

Am eel , 1956). Unfor tuna te ly , these t es ts l ack spec i f i c ity and a re f r equen t ly

insensi tive . Therefore , they ca nno t be u sed for def in i t ive d iagnos i s o f cercar -

i a l derma t i ti s (W iederm an

e t a l . ,

1973).

O t he r m e t hods r e l y on de t ec t ion o f an t i body r e s pons es f o r d i agnosi s. T h e

Cercar ienh t i l lenreak t ion , a co m plem ent f ixa t ion t est , IFAT and EL ISA have

been used to as ses s the t i tr es o f spec i f ic an t ibodies aga ins t cercar iae (of e i ther


o r

S c h i s t o s o m a

or aga i n st homo gena t e s o f

S . m a n s o n i

adul ts

(Vogel and M inning , 1949a ,b ; Hen dr icks and Cor t, 1956; Mo ore

e t a l . ,

1968;

Knight and Worms , 1972; Krampi tz

e t a l . ,

1974; Kimmig and Meier , 1985;

Kol~i~ov~i

e t a l . ,

1994; Pilz

e t a l . ,

1995). A l tho ugh these t echniques a re m ore

sens it ive than sk in t est s, they a re no t spec i f ic . Thus , the y cann ot be p er form ed

for a d i f f e ren t i a l d iagnos i s be tw een cercar ia l dermat i t is and hu m an sch i s toso-

mi as i s . R ecen t l y , an I FA T app r oach t o t e s t t he an t i body r eac t i v i t y w i t h

s c h i s t o s o m u l a r a n d a d u l t G A A o f b o t h


a n d

S c h i s t o s o m a

species al low ed the correc t dis t inct ion of ant isera . Thus , this par t icular m eth od

seem s prom is ing for d i f f e ren t i a l d iagnos i s o f cercar ia l dermat i t is cause d by

bird sch isto so m es (Kou~ilov~i an d Kol~i~ov~i, 2002).

A t p r e s en t , t he t he r apy o f ce r ca r i a l de r ma t i t i s i s on l y s ympt oma t i c .

Abi r r i tan t powde rs ma y be app l ied to the sk in and , in se r ious cases, the use of

sys temic an t ih i s t amin ics ( t ab le t s o r be t t e r in ge l s ) o r mi ld cor t i cos te ro ids

shou ld be c ons idere d (Hoe ff ier , 1977).

7 E P I D E M I O L O G Y O F C E R C A R I A L D E R M A T I T IS

C er ca r i a l de r ma t i t i s ha s been r ecogn i zed s i nce h i s t o r i ca l t i mes . I n 1847 ,

Fu j i i ( c i t ed by O da , 1973) r epo r t ed s k i n e r up t i ons i n J apanes e r i ce p l an te r s .

N aeg e l i ( 1923 ) des c r i bed c l i n ica l s ym pt om s o f t h is w a t e r - bo r ne d i s eas e i n

G er m any , hyp o t hes i z i ng tha t it w as caus ed by an i m a l p l anc t on . F i na ll y , i n

1928, C or t i n N or t h A m er i ca i den t i f i ed t he caus a t i ve agen t and t he d i s eas e

w a s n a m e d s c h i s t o s o m e d e r m a t it is . M a n y r e p o r ts h a v e a c c u m u l a t e d s in c e

a n d t h e i n f e c t io n i s p r e s e n t ly k n o w n u n d e r d i f f e r e n t n a m e s i n v a r i o u s a r e a s

o f t he w or l d , e .g . s w i m m er s i tch ( C hr i s t ens en and G r een , 1928), Z e r ka r i en -

Derm at i t is (Vogel, 1930b), derm at i t e des nageu rs (Brumpt , 1931), bo uton de

can icu le des ba ign eurs (De spor tes , 1944/45) , kab ure (Fuj i i, 1847 , c i t ed by




O d a , 1 9 7 3 ), k o g a n b y o ( T a n a b e , 1 9 4 8 ), s a w a h i t c h ( B u c k l e y , 1 9 3 8 ) , e t c . I n

m o s t a r e a s , t h e p a r a s i t e s p e c i e s t h a t c a u s e h u m a n c e r c a r i a l d e r m a t i t i s h a v e

n o t b e e n p r e c i s e l y i d e n t i fi e d d u e t o a v a r ie t y o f p r a c ti c a l p r o b l e m s a n d

t e c h n i c a l d i f f i c u l t i e s ( s e e s e c t i o n 3 ) . T h i s i s u n f o r t u n a t e a s u n e q u i v o c a l

i d e n t i f i c a t i o n o f t h e c a u s a t i v e a g e n t ( i n c l u d i n g d a t a o n l i f e c y c l e s ) i s a p re -

r e q u i s it e f o r e s t i m a t i o n o f h e a l th r i s k s a n d f o r d e s i g n i n g c o n t r o l m e a s u r e s

( s e e s e c t i o n s 3 a n d 6 ) .

7 1 D i s t r ib u t i o n

W i t h t h e ex c ep t i o n o f A n t a r c t i c a , c e r ca ri a l d e rm a t i t is o ccu r s g l o b a l l y (H o e f f ie r ,

1 9 8 2) . It h a s b e e n r e p o r t e d f r o m N o r t h a n d C e n t r a l A m e r i c a ( U S A , C a n a d a ,

H a i t i , S a l v a d o r , M e x i c o , C u b a ) , A u s t r a l i a , N e w Z e a l a n d , A s i a ( F o r m o s a ,

M a l a y s i a , P h i l i p p i n e s ) ( f o r r e v i e w , se e H o e f f i e r , 1 9 8 2 ) , J a p a n ( O d a , 1 9 7 3 ;

S u z u k i a n d K a w a n a k a , 1 9 8 0 ), I n d i a (N a r a i n

e t a l .

1 9 9 4 ; A g r a w a l

e t a l .

2 0 0 0 ) ,

T h a i l a n d ( K u l la v a n ij a y a a n d W o n g w a i s a y a w a n , 1 9 93 ), V i e t n a m ( L a n d m a n n

e t

a l .

1 9 6 1 ) , C h i n a ( L i u

e t a l .

1 9 7 7 ) , I r a n ( S a b h a a n d M a l e k , 1 9 7 9 ) , A f r i c a

( S o u t h A f r i c a; A p p l e t o n , 1 9 8 4) a n d E u r o p e ( D e n m a r k , F i n l a n d , G r e a t B r i ta i n ,

t h e N e t h e r l a n d s , S l o v a k R e p u b l i c , C z e c h R e p u b l i c ) ( f o r r e v i e w s e e K o l~ i~ ov~ i

e t a l .

1 9 8 9 ) , A u s t r i a ( G r a e f e

e t a l .

1 9 7 3 ; D v o ~ i k

e t a l .

1 9 9 9 ) , E u r o p e a n

c o u n t r i e s o f t h e f o r m e r S o v i e t U n i o n ( e . g . R a i s y t e , 1 9 7 4 ; T s y r k u n o v , 1 9 8 7 ;

B e e r a n d G e r m a n , 1 9 9 4) , F r a n c e ( L 6 g e r a n d M a rt in - L 0 eh r , 1 9 9 9) , G e r m a n y

( f o r r e v i e w s e e A l l g 6 w e r a n d M a t u s c h k a , 1 9 9 3 ) , I c e l a n d ( K o hi~ o v~ i

e t a l .

1 9 9 9 ) , I t a l y (N o b i l e

e t a l .

1 9 9 6 ; G o l o

e t a l .

1 9 9 8 ) , N o r w a y ( T h u n e , 1 9 9 4 ) ,

S p a i n ( S i m o n - V i c e n t e , 1 9 8 3 ) , S w e d e n ( T h o r s a n d L i n d e r , 2 0 0 1 ) a n d

S w i tz e r l a n d ( E k l u - N a t e y

e t a l .

1 9 8 5 ; C h a m o t , 1 9 9 8 ) .

P r o b a b ly , t h e d i s e a s e i s m o s t p r o m i n e n t l y d i s tr i b u te d a l o n g t h e m a j o r f ly -

w a y s o f th e m i g r a t o r y b ir d s: f o r e x a m p l e , i n N o r t h A m e r i c a , th e d e r m a t i t is

s e e m s t o c o n c e n t r a t e a l o n g t h e M i s s i s si p p i f ly w a y ( J a rc h o a n d v a n B u r k a l o w ,

1 9 5 2 ) a n d t h e P a c i f i c d i s t r i b u t i o n m a y f o l l o w t h e N e o a r c t i c - H a w a i i a n ,

A s i a t i c - P a l a u a n a n d J a p a n e s e - M a r i a n a n f l y w a y s (C h u , 1 9 58 ). A c c o r d i n g to

t h is v i ew , th e P a l a e a r c t i c - A f r i c a n b i r d m i g r a t i o n ( M o r e a u , 1 9 7 2) m a y i n f l u -

e n c e t h e d i s t r i b u t io n o f c e r c a r i a l d e r m a t i t is i n E u r o p e a n d A f r i c a .

T h e t ra n s i e n t p r e s e n c e o f w a t e r f o w l i s e s se n t ia l f o r e s t a b l is h m e n t o f t h e

p a r a s i t e l if e c y c l e i n a p a r t i c u l a r w a t e r r e s e r v o ir . M o s t o f th e b i r d s p r o b a b l y

b e c o m e i n f e c t e d i n n e s t in g a r e a s; h o w e v e r , i n s o m e c a s e s , b i r d s m a y a l so

t r a n s p o r t m a t u r e ( w i t h i n t h e h o s t ) o r la r v a l ( w i t h i n s n a i ls t r a n s p o r t e d o n b i r d

l e g s) s c h i s t o s o m e s t o a n d f r o m t h e w i n t e r i n g l o c a ti o n s ( W o o d r u f f a n d M u l v ey ,

1 9 9 7 ; W e s s e l i n g h

e t a l .

1 9 9 9 ) . T h u s , b i r d m i g r a t i o n s m a y b e e x p e c t e d t o

i n t r o d u c e c e r t a i n p a r a s i t e s p e c i e s i n t o n e w g e o g r a p h i c a l a r e a s . H o w e v e r , n o

d a t a a r e a v a i la b l e to s u g g e s t th a t a v i a n s c h i s t o s o m e s h a v e e x p a n d e d t h e ir g e o -

g r a p h i c a l r a n g e i n th i s f a s h i o n .



2 1 0 P . H O R . '~ K , L . K O L .,~ I~ O V , , A N D C . M . A D E M A

7 2 E p i d e m i o lo g y

Cercar ia l de rmat i ti s i s a com m on, non -com m unicab le cu taneous d i s ease tha t is

w i d e l y n e g le c t e d . T h e o c c u r r e n c e o f t h e d i s e a s e d e p e n d s u p o n c o m p l e x i n te r-

ac t ions among the pa ras i t e s , mo l luscan and de f in i t ive hos t s , and humans as

they sha re the s am e env i ronm en t un der cond i t ions tha t f avou r pa ras i t e t rans -

m i s s i o n H o e f f l e r , 1 9 8 2 ). D e p e n d i n g o n t h e c a u s a t i v e s p e c i e s , c e r c a r i a l

de rmat i t is ca n dev e lop in f r esh - o r s a l t -wa te r bod ies fo r rev iew se e Hor~ ik and

Kol~i~ov~i, 2001 ) . At presen t , the m os t f re que nt ly re po r ted ce rcar iae be long to

the genus


Hor~ik and Kol~i~ovf i, 2001 ) , larval de velo pm ent of

wh ich t akes p lace on ly in f r eshwate r bod ies .

Cerca r ia l de rm at i ti s occ ur s s easona l ly . I t i s m os t p reva len t du r ing wa rme r

m onths w hen bo th the r e lease o f ce rca r iae f rom sna il in te rmed ia te hos t s and

t h e n u m b e r o f p e o p l e th a t h a v e c o n t a c t w i th w a t e r r ea c h p e a k l e v e l s C o r t

e t

a l . 1940; App le ton and Le thbr idg e, 1979) . In addi t ion to fac tors that re la te to

the b io log y o f the pa rasi t e s, the f r equen cy o f human ce rca r ia l de rm at i ti s a l so

d e p e n d s o n t h e b e h a v i o u r o f b a t h e rs d u r at io n o f sw i m m i n g ), p r e v i o u s c o n ta c t

w i th the paras i te h is tory of cercar ia l derma t i t is ) and , poss ib ly , indiv idua l sus-

c e p t i b i l i t y t o t h e c e r c a ri a e . A m u l t iv a r i a te a n a l y s i s C h a m o t

e t a l .

1998)

s h o w e d t h at t h e t im e o f da y , b a r o m e t r i c p r e s s u re , m a x i m u m a ir t e m p e r a t u r e

a n d d u r a t io n o f s w i m m i n g a c t iv i ty s t r o n g ly p r e d i c t n o t o n l y t h e i n c i d e n c e o f

ce rca r ia l de rmat i t i s bu t a l so the nu m ber o f sk in l e s ions.

A h i s to ry o f ce rca r ia l de rmat i ti s sho u ld be as sum ed i f s trong sk in r eac t ions

occu r ea r ly a f t e r in fec t ion Cham ot e t a l . 1998) . Both sexes and a l l age gro ups

c a n b e a f fe c t e d e q u a l l y u n d e r si m i l ar c o n d i ti o n s C h a m o t

e t a l .

1998) .

H o w e v e r , t h e t i m e i n te r v al o f e x p o s u r e m a y d i f f e r f o r v a r io u s a g e g r o u p s.

C h i l d re n b e t w e e n 5 a n d 9 y e a r s a re a t h ig h e s t r is k b e c a u s e t h e y s p e n d m o r e

t ime in the wa te r du r ing r ec rea t iona l ac t iv i ti e s Ap p le ton and Le thb r idge ,

1979) . In r ice p lanters or p ickers , for ins tance , adul ts were the mos t af fected

grou p A ppleto n , 1984) .

A t p resen t , ce rca r ia l de rm at i t i s i s r ega rde d as an em erg ing d i s e ase de

Gen t i l e

e t a l .

1996). H ig h eu t roph ica t ion o f wa te r r e se rvo i r s A l lg 6w er and

Ef fe l sbe rg , 1991), co lon iza t ion o f pond s by suscep t ib le sna i ls and b y nes t ing

ducks , combined wi th long pe r iods o f sunsh ine in the summer , a r e impor tan t

f ac to r s tha t have l ed to r ecen t inc reases in the num ber o f ou tb reak s o f ce rca r -

i a l de rm at i t is de Ge n t i l e

e t a l .

1996) . A lso , the d i s ease may be acqu i red

wh en c lean ing an aq uar ium con ta in ing f i e ld -co l l ec ted sna il s tha t ha rbor av ian

s c h i s t o s o m e s B a s t e r t

e t a L

1998; F61ster-Holst

e t a l .

2001) .



BIOLOGY OF TBICHOBILH RZI 2

7 3 Id en t i fi ca t io n o f Po t en t ia l T ran sm iss io n S i tes fo r C ercar ia l

D e r m a t i t i s

The occur rence o f ce rca r ia l de rm at i ti s i s de l inea ted b y the d i s t r ibu t ion o f in te r-

m e d i a t e h o s t s i n f e c t e d b y s c h i s t o s o m e s . W i t h r e s p e c t t o s p e c i e s - s p e c i f i c

phys ica l , chem ica l and b io lo g ica l r equ i remen ts , f r e shwate r sna il s l ive in va r i-

ous hab i ta t s , d i f fe r ing in s i ze and o r ig in (na tu ra l o r man-m ade) . Usua l ly , the

dis t ribut ion o f snails wi th in larger habi ta ts i s d iscont inuous , o f ten due to a pref -

e rence fo r aqua t i c vege ta t ion tha t o f f e r s p ro tec t ion and s i t e s fo r egg- lay ing

(Sturrock , 1993) . Ident i f ica t ion o f reservo irs that pose a r isk for hum ans re l ies

o n d e t e c t i o n o f b i r d s c h i st o s o m e s .

T h e e x a m i n a t io n o f w a t e r s a m p l e s m a y d i s c l o s e t he p r e s e n c e o f c e rc a r ia e i n

a pa r t icu la r wa te r body . How ever , th i s i s u sua l ly d i f f icu l t due to low pa ras i te

concen t ra t ions , an d va r ious method s o f ce rca r iom et ry - f il tr a tion , the use o f

p h o t o t a x i c r e s p o n s e e q u i p m e n t a n d c o n t i n u o u s f l o w c e n t r if u g a t i o n - h a v e

bee n dev e loped to de tec t (human) s ch i s tosom es ( fo r r ev iew see Thr ron , 1986);

pe rhaps these m ay a l so be app l ied in the s ea rch fo r b i rd s ch i s tosomes .

Moreover , ce rca r iae can be ' co l l ec ted ' by a t r ap con ta in ing a mat r ix w i th

unsatura ted fa t ty ac ids ( l inole ic ac id) . This subs t ra te s t imulates the a t tach-

m e n t a n d p e n e t r a t io n b y c e r c a r ia e . A n y i m m o b i l i z e d l a rv a e a r e s u b s e q u e n t l y

v i s u a l iz e d f o r c o u n ti n g . T h i s m e t h o d t o m o n i t o r s c h i s t o s o m e - i n f e s te d w a t e r s

w a s p r i m a r i l y d e v e l o p e d f o r S . m a n s o n i (Sh i f t e t a l . 1993 ; Sh i f t and Grac zyk ,

1994), bu t cou ld be app l ied a l so fo r


(Gracz yk and Sh i ft , 2000) .

M olec u la r me tho ds can fu r the r inc rease the s ens i t iv i ty o f de tec t ion , e .g . a

P C R a s s a y b a s e d o n a h i g h l y r e p e a t e d s e q u e n c e o f S . h a e m a t o b i u m a l lows

d e t e c t i o n o f s i n g l e c e r c a r i a e a n d a s l i t t l e a s 1 0 f g o f s c h i s t o s o m a l D N A

( H a m b u r g e r

e t a l .

2001) .

Determ inat ion of f ie ld-co l lec ted cercar ia l species is a com plicate d matter , as

desc r ib ed in s ec t ion 3 . Su rp r is ing ly , the f ind ings o f b i rd s c h i s tosom e ce rca r iae

a r e f r e q u e n t l y c o n f i r m e d b y e x p e r i m e n t a l i n f e c t io n s o f v o l u n t ee r s . S e v e r a l

nove l in s igh t s in to the po ten t i a l pa thog en ic e f f ec t s o f these pa ras i t e s ( s ee s ec -

t ion 5 ) war ran t cau t ion aga ins t pe r fo rm ing exp er imen ta l in fec t ions in hum ans .

The source o f in fec t ion i s iden t i fi ed main ly by exam ina t ion o f wa te r sna il s.

T w o m e t h o d s a r e c o m m o n l y u s e d : c e r c a r i a l e m e r g e n c e a n d d i s s e c t i o n o f

sna il s. Exc lus ive use o f ce rca r ia l em ergen ce un deres t ima tes the va lue o f pa ra -

s i te p reva lence and o ver loo ks pa ras it e s tha t a r e p resen t bu t no t shed b y sna i l s

a t t h e t i m e o f e x a m i n a t io n . T h i s m e t h o d y i e l d e d f a l se r e s u lt s i n 5 9 . 1 o f

cases when com pared w i th the d i s sec tion o f sna il s (Cur t is and H ubbard , 1990).

The occur rence o f the pa ras it e s f luc tua tes du r ing the yea r ; these d i f f e rences a re

due to cyc l i c r ep roduc t ion and changes in the age d i s tr ibu tion w i th in sna il pop-

u la t ions . I t i s r eco m m end ed to exam ine sna i l s o f va r ious s i zes to de te rmine

p a r a si te p r e v a l en c e m o r e a c c u r a t e ly ( H u r l e y e t a l . 1994).

H ig her num bers o f in fec ted sna i ls inc rease the in fec t ion ri sk fo r hum ans .



21 2 R HORA K L. KOL ~.ROVA AN D C.M. AD EM A

However,

Trichobi lharz ia

infection rates in lymn aeids are u sually low, ranging

bet we en 0.3 and 5.2 (Meyer, 1964; van den Broe k, 1965; D rng es, 1965;

Bearup and Langsford, 1966; G raefe

et al. ,

1973; Wills

et al. ,

1976; Kol~ii'ov~

et al . , 1992; MUller and Kim mig , 1994; Hur ley et al. , 1994; Loken et al. ,

1995; Niew iadom ska

et al. ,

1997; V~iyrynen

et aL,

2000; Lo y and Haas, 2001).

Except for L. aur icular ia , prevalenc es that exce ed 5 are exception al and

m ay falsely result from examination of only a low num ber o f snails (L oy and

Haas, 2001). The high prevalences of parasites (22 and 26 ), recorded from L.

aur i c u lar ia in Bohemia and Germany, respectively (Kol~i~ov~i et aL, 1989;

Miiller and K imm ig, 1994), m ay result from disturbances in the ecological bal-

ance of the lakes that were sampled, leading to increased sizes of snail

populations (Kol~i~'ov~i

et al. ,

1989).

The propo rtion of infected snails at any t ime depends upon co mp lex inter-

actions of biotic and abiotic factors, including susceptibility of particular snail

hosts , and number , d is t ribut ion and beh aviour of def in i t ive hosts .

Environmental factors such as temperature are also important (Webbe, 1982).

It appears that mos t snails be com e infected during the first sum me r of their life

(Hoeffier, 1982). Snail infections in the late summ er prob ably secu re survival

of schis tosom es in the water body. It is obv ious that snails containing parasites

overwinter and cercarial shedding starts during warm days of the next spring.

In this way, the parasite infects new birds when they return to their breeding

areas (McMullen and Beaver, 1945; Jarcho and van Burkalow, 1952). On the

other hand, sum me r infections of the snails m ight be responsible for distr ibu-

tion of schistosomes to the bird wintering areas.

Most commonly, infections of birds by avian schistosomes are diagnosed

through faecal examination. This approach is appropriate to detect visceral

schistosomes, but i t wil l fai l to show the presence of nasal schistosomes. The

latter parasites are also common in waterfowl (Rudolfov~i et al. , in press).

Therefore, different methods to examine birds should be applied to obtain

correct values for prevalence of infection (see also section 6.1.5).

The prevalenc e of tr ichobilharziasis in birds can be quite high in comp ar-

ison wi th snai ls . Faecal surveys indica ted the fo l lowing prevalences of

Tr ic hob i lharz ia spp.: 60.5 in spurw ing goo se (Appleton, 1986), 69.6 in

domest ic duck (Liu et al . , 1977), 83.9 in com m on merganser, 2.6 in

Canada goose and 4 .9 in gul ls (Loken et al. , 1995). Guth et aL (1979)

demon stra ted prevalences of 12.0 and 46.3 of v iscera l schis tosomiasis in

adul t and you ng Anser i formes, respect ively . The invest igation o f wi ldfow l

(genus A y t h y a and A n a s dur ing two consecut ive years show ed that preva-

lence of nasal schis tosom es was constant a t 24.0 (Rudolfov~i

et al . ,

in

press).

Migra tory bi rds probably do not acquire heavy infect ions because they

leave the infective habitat, whereas no n-migratory birds ma y suffer severely

from trichobilharziasis and die (Wilson et al . , 1982). Ho wev er, the properties



I O L O G Y O F TRICHOBILHARZIA 2 3

of r es iden t sna i l popu la t ions tha t de te rm ine suscep t ib i l ity o r r e s i st ance can l ead

to d i f ferent infect ion ra tes a t par t icu lar loca l i t ies .

7 4 C o n t r o l

Effec t ive con t ro l o f ce rca r ia l de rmat i t is m us t be ba sed on a na lys i s o f an en t ir e

b io log ica l sys tem . On ly then can the in te r rup tion o f the s ch i s toso m e l if e cyc le

be ach ieved . In te rven t ion e f fo r t s can be d i r ec ted a t the l eve l o f e i the r in te rme-

d ia te o r de f in i t ive hos t s . The con t ro l o f in te rmed ia te h os t s i s u sua l ly a im ed a t

e l imina t ion o f sna i ls and /o r p reven t ion o f sna i l r ep roduc t ion . A t the de f in i tive

hos t l eve l , the foc us i s to e l imina te s ch i s tosom e in fec t ion in b irds .

The co n t ro l o f sna il popu la t ions m ay em ploy chem ica l, mech an ica l and b io -

l o g ic a l a p p r o a c h e s r e v i e w e d b y A l l g 6 w e r a n d M a t u s ch k a , 1 9 9 3) . S i n c e t h e

f i rs t u se o f cop per su lpha te Tay lo r and Bay l i s , 1930) to k i ll sna il s in an e f fo r t

to con t ro l ce rca r ia l de rmat i t is , va r ious chem ica l com pou nds tha t a r e tox ic fo r

sna il s m ol lusc ic ides ) have bee n used fo r th is pu rpose . Ma ny o f these p repa-

r a t io n s a r e d e r i v e d f r o m v a r i o u s c o p p e r c o m p o u n d s e .g . B r a c k e t t , 1 9 3 9 ;

M c M u l l e n a n d B r a c k e tt , 1 94 8). T h e u s e o f th e s e c o m p o u n d s m a y y i e l d i n c o n-

s i s ten t r e su lt s , depend ing on ab io t i c p roper t i e s o f the w a te r to be t r ea ted an d

the exper ience o f pe r sonne l invo lved in the con t ro l fo r r ev iew see B lank espoor

a n d R e i m i n k , 1 9 9 1) . F o r e x a m p l e , t re a t m e n t o f a w a t e r b o d y w i t h c o p p e r s u l-

p h a t e c a n c a u s e c o p p e r t o p r e c ip i ta t e a s c o p p e r c a rb o n a t e s. A c c u m u l a t i o n o f

copp er in the r ese rvo i r s ed imen ts can cause dea th o f va rious aqua t ic o rgan i sms

and r educe the r ec rea t iona l va lue o f the l ake . Su rp r i s ing ly , a f t e r t r ea tmen t

wi th a coppe r -based mol lusc ic ide , sna i ls con t inued to r ep rodu ce and sp read a t

a r ap id ra te B lan kespo or and Re imink , 1991). There i s even ev idenc e tha t,

ove r an ex tended t ime , sna i l popu la t ions dev e lop pa r ti a l) r e s i st ance to cop per

s u l p h a t e B l a n k e s p o o r e t a l . 1985).

A m o n g o t h e r s y n t h e t ic c o m p o u n d s , s u c h a s B - 2 s o d i u m 2 , 5 -d i c h l o r o -4 -

b r o m o p h e n o l ) o r N a P C P s o d i u m p e n t a c h lo r p e n ta t e n ic l o s am i d e ) ,

n i c l o s a m i d e B a y l u s c i d e ® ) is s ti ll th e m o l l u s c i c i d e o f c h o i c e . A l t h o u g h i t is

expens ive , n ic losamide i s h igh ly e f f ec t ive aga ins t a l l l i f e s t ages o f the sna i l

a n d a l s o a g a i n s t s c h i s t o s o m e l a r v a e . W h e r e a s n i c l o s a m i d e i s n o n - t o x i c f o r

hum ans , do m es t i c an imals an d c rops , it i s, un fo r tuna te ly , tox ic fo r f i sh fo r

r e v i e w s e e P e r r e t t a n d W h i t fi e l d , 1 9 9 6) . M o r e o v e r , t h e a p p l i c a t io n o f

n i c l o s a m i d e d i d n o t p r e v e n t t h e r e - c o l o n i z a ti o n o f s i te s b y r e m a i n i n g s n a il s

L a r d a n s a n d D i s s o u s , 1 9 9 8 ). A p r o m i s i n g a l t e r n a ti v e i s p r o v i d e d b y t h e

o n g o i n g d e v e l o p m e n t o f p l a n t m o l l u s c i c i d e s S i n g h a n d S i n g h , 2 0 0 0 ) .

Ho we ver , the ava i l ab i li ty o f these p repara t ions and the i r e f f ec t ivenes s dep end

on the loca l si tua t ion and na t ive f lo ra Per re t t and W hi t f i e ld , 1996) . F ina l ly ,

the app l ica t ion o f va r ious bac te r i a l p roduc t s cou ld be co ns ide red fo r con t ro l o f

sna il s and pa ras i te s . T he e lua te o f B a c i l l u s t h u r i n g i e n s i s i s r a e l e n s i s conta ins a



214 P. HOR,~K, L. KOLAI~OV,, ,AND C.M. ADEMA

water-soluble M-exotoxin which is toxic for

S. mansoni and T. szidati

cercariae

and corresponding snail hosts Hor~iket aL 1996).

The removal of aquatic vegetation and snails from swimming areas can be

an effective control measure e.g. Graefe

et al .

1973). Virtually all snails can

also be eliminated from large bodies of water by mechanical disturbance of the

snail habitat using boats mounted with rototillers or tractors equipped with a

rake), provided that the intervention is performed in shallow littoral) areas

with high concentration of snails at the time of reproduction and early devel-

opment Leighton et al. 2000). Alternatively, small lakes can be emptied

temporarily to dry out the bottom, remove mud and cover places reserved for

bathing with a new layer of river sand Kohi~ov~i

et al.

1989).

Generally, biological control of bird schistosomes aims to regulate or reduce

snail and/or parasite populations. The fitness of schistosome intermediate hosts

can be affected significantly by removal of food sources and introduction of

natural predators e.g. fish) or competing snail species resistant to schisto-

somes) Haas, 1985; Allgfwer and Matuschka, 1993). The introduction of

parasites that attack or compete with larval schistosomes within the snail host,

or that induce high mortality or castration of snails has been explored for

review see Lim and Heyneman, 1972). For example, intramolluscan larvae of

echinostome parasites are predators of schistosome larvae that may co-occur in

the same snail. Introduction of eggs of)

Echinostoma audyi

led to some level

of control o f intramolluscan larvae of T.

brevis

in the snail

Lymnaea rubiginosa

Ow-Yang et al. 1970; Lie and Ow-Yang, 1973). Many factors affect the fea-

sibility of biological control, and these approaches should be taken only under

semi-controlled conditions, such as in small lakes. Also it may take consider-

able time before these approaches yield demonstrable effects. Because of this,

these methods have little practical value.

At the level of definitive hosts, control efforts have explored prevention of

bird contact with infested waters and chemotherapy of birds. Whereas the first

approach e.g. relocation of breeding bird host species to other areas;

Blankespoor and Reimink, 1991) is difficult to implement on a large scale in

the field, the treatment of birds with antihelminthics is rather promising. Based

on a study in which birds were captured and treated with praziquantel to kill

adult worms, Blankespoor and Reimink 1991) concluded that treatment of

birds is more effective than the use of copper sulphate; also it is less expensive

and has no detrimental effects on the environment.

7 5 Prophylaxis

Theoretically, human infections are prevented by prohibiting access to water

that harbours cercariae of avian schistosomes. However, various restrictions in

water activities are usually not respected by bathers Allgfwer and Matuschka,



IOLOGY OFTRICHOBILHARZIA 2 5

1993; Ch am ot et aL, 1998) . So m e protect ion agains t cercar ial derm at i t is can b e

achiev ed by rubbing the sk in to fu l l d ryness im m edia te ly a f t e r wa ter contac t,

befo re cercar ia l pene t ra t ion occurs (Bracke t t , 1939; Haas and van d e Roe m er ,

1998). A tho roug h coa t ing of the bod y w i th vase l ine provides com ple te p ro-

tec t ion aga ins t in fec t ion (M cL eod and L i t tl e , 1942). Th e va lue o f p ro tec t ive

clothing ( long t rousers , hip boots a nd w aders) is unpredictable . Rece nt ly , N,N-

d i e t hy l - m - t o l uam i de ( D E E T ) w as f ound t o have a r epe l l en t e f f ec t aga i n s t

var ious cercar iae of the genus Schis tosoma (Sa la f sky et al., 1999, 2001); w he n

incorp orated in l iposom es ( ' l ipode et ' ) , the appl icat ion on skin was 100 ef fec-

t ive in preve nt ing penetrat ion by cercar iae. A s imilar proph ylact ic ef fect can b e

expec ted aga ins t pene t ra t ion by sch i s tosom e la rvae f rom gene ra tha t cause cer -

car ial derm at i t is .

8 C O N C L U S I O N

T he a s s oc ia t ion be t w een av i an s ch i s t o somes o f t he genus Trichobilharzia and

c e r c a r i a l d e r m a t i t i s i n m a m m a l s h a s b e e n r e c o g n i z e d f o r m a n y d e c a d e s .

How ever , d if f icu l t ies in ob ta in ing adul t paras it es f rom b i rds , co m bine d w i th

ex tens ive morphologica l s imi lar it ies , con t inue to com pl ica te bo th the u nequiv-

oca l i den t i f i ca t i on a t s pec i e s l eve l and t he cha r ac t e r i za t i on o f s pec i f i c

b io log ica l p roper t i es o f d i s t inc t spec ies w i th in the genus Trichobilharzia. The

sys tema t ics o f the genu s requires a m ajor revision, including clar if icat ion o f the

pos i t ion and va l id ity of the type spec ies T . ocellata. New, m ore ex tens ive c r i-

t e r i a t o i den t i f y a s pec i e s o f Trichob i lharz ia , c o m b i n i n g m o r p h o l o g y ,

cha r ac te r is t ic s o f t he l i f e cyc l e and m o l ecu l a r s equence da ta , m ay beg i n t o

resolv e this i ssue.

Spec ies o f Trichobilharzia display a rem arka ble speci f ic i ty towards (species

of ) sna i l in te rmedia te host s. Th e paras i t e mo di f i es the phy s io logy and in te rna l

defen ces of a sna il to com ple te in t r amol luscan deve lop m ent success fu lly . Th e

t ransmiss ion o f a Trichobilharzia spec ies by o n ly cer ta in sna i ls i s thou ght to

ref l ec t the h igh ly spec ia l ized na ture of these co m plex in te rac t ions be tw een the

paras it e and the in te rmed ia te hos t.

As paras i t es , Trichob i lharz ia s pec i e s a r e s e r i ous pa t hogens f o r b i r d s .

C ompar ab l e t o pa t ho l ogy caus ed by pa r a s i t e s o f t he genus Sch i s tosoma in

m am m als , tr i chobi lharz ias is i s acco m pan ied by in jur ies due to paras i tes tha t

mi g r a t e t h r ough t he v i s ce r a o r t he C N S ( i n t he ca s e o f nas a l s pec i e s o f

Trichobilharzia of b i rds . M oreover , adu l t worm s and paras i t e eggs tha t have

beco m e t r apped i n t he t i ss ues evoke t he f o r ma t i on o f g r anu l oma .

T he ab il it y o f ce r ca r i ae t o pene t r a t e in t o m am ma l s is l i nked t o m or e t han

jus t cercar ia l dermat i ti s a lone . S tudy o f p r imary in fec t ions in rodent s r evea led

t ha t s om e i mm at u r e Trichobilharzia w or m s a l so m i g r a te th r ough t he body o f



2 6

R HORh,K, L. KOLAI~OV, ,AND C.M. ADEMA

mam mals. Strikingly, they are also neurotropic in mam mals. The invasion of

nasal species of Trichobi lharzia in to the nervous t i ssues of exper imenta l

rodents potentially led to neuromotor disorders. This suggests that cercarial

dermatitis, the elimination of penetrating cercariae in the skin, represe nts a pro-

tective reaction o f a sensitized organism against the parasite. At present, there

are no data on the pathology o f primary infections in large mam mals and

humans. However, the cosmopolitan occurrence of Trichobilharzia species

and the frequen t expo sure of animals and human s to these parasites cercarial

dermatit is is an emerging disease) provide ample justif ication to intensify

study of clinical and pathological aspects related to trichobilharziasis in mam-

mals, including humans.

In summ ary, species of the genus

Trichobilharzia

display striking transitions

in morphology, a com plex life-cycle and fascinating properties that enable these

parasites to survive in intermediate and final hosts. The inconspicuou s nature o f

their endoparasitic life style m ay have led to a considera ble underestimation of

the pathogenicity and medical/veterinary importance of Trichobilharzia.

A C K N O W L E D G E M E N T S

The work of PH was continually supported by the following grant agencies:

GA of the Char les Univers i ty recent ly 1 23/2000/B/BIO/PrF) , GA of the

Czech Repub lic recently 204/00/1095, 524/00/0622), GA of the Ministry of

Education recently J13/981131 00003, J13/98113100004). The research of

LK was made poss ib le by the fo l lowing grant projec ts : GA of the Czech

Min is t ry o f Hea l th NJ -671 8-3) , G A of the Char les Univers i ty

38 /2000 /C/1LF) . CMA acknowledges suppor t by the Na t iona l Sc ience

Foundation, U SA grant No. 9974930). Fo r cri tical reading and helpful dis-

cussions the authors express thanks to J . Dvo[Sak sequence data) , M.

Spakulov~i karyo types) and J. Rud olfov ~ system atics). W e thank the librari-

ans o f the Faculty H ospital, Bu lovka for providing the older research papers

and K. Skirnisson for providing the m aterial from Icelandic m ute swans.

REFERENCES

Adema, C.M. and Loker, E.S. 1997). Specificityand immunobiology of larval digenean-

snail associations. In: Advances in Trematode Biology B. Fried and T.K. Graczyk, eds),

pp. 229-263. Boca Raton: CRC Press.

Adema, C.M ., van Deutekom-Mulder, E.C., van der Knaap, W.P.W. and Sminia, T. 1993).

NADPH-oxidase activity: the probab le source of reactive oxygen intermediate genera-

tion in hemocytesof the gastropodLymnaea stagnalis. Journal of Leukocyte Biology 54




3 7 9 - 3 8 3 .

A d e m a , C .M . , v a n D e u te k o m -M u ld e r , E .C . , v a n d e r K n a a p , W.P .W. a n d S min ia , T. (19 9 4) .

S c h i s to s o mic id a l a c t iv i t ie s o f Lymn aea stagnalis h e mo c y te s : t h e ro le o f o x y g e n ra d ic al s .

Parasitology 109 , 479-485 .

A d e m a , C .M . , H e r t e l, L .A . , M i l l e r, R .D . a n d L o k e r, E .S . (1 9 9 7 ). A fa m i ly o f f ib r in o g e n -

r e l a t e d p r o t e i n s t h a t p r e c i p i t a t e s p a r a s i t e - d e r i v e d m o l e c u l e s i s p r o d u c e d b y a n

inver tebra te a f te r in fec t ion . Proceedings of the National Academy of Sciences USA 94 ,

8 6 9 1 -8 6 9 6 .

Ag raw al , M .C. , Gu pta , S . and G eorge , J. (2000) . Cerca r ia l de rm at i t i s in Ind ia .

Bulletin of the

Wo rld Health Orga nization 78, 278.

A l lg rw e r , R . a n d E f fe l sb e rg , W. (1 9 91 ). B a d e d e rm a t i t i s e p id e mie m B a g g e r s e e - e in A n la B

z u r Z u s t a n d s a n a l y s e d e r G e w a s s e r s u n d V o r b e r e i t u n g e i n e r n a t u r v e r t r ~ i g l i c h e n

N u tz u n g s k o n z e p t io n .

Das Offentliche Gesundheitswesen

53 , 115-156 .

A l l g r w e r , R . a n d M a t u s c h k a , E R . ( 1 99 3 ). Z u r E p i d e m i o l o g i e d e r Z e r k a r ie n d e r m a t i t is .

Bundesgesundheitsblatt 10 , 399-404 .

A m e n , R . I . a n d d e J o n g -B r in k , M. (1 9 9 2 ) .


i n fe c t io n s in i t s s n a i l

h o s t Lymnaea stagnalis: an in vitro s tu d y s h o w in g d i r e c t a n d in d i re c t e f f e c t s o n th e

s n a i l i n t e rn a l d e fe n s e s y s t e m, v ia th e h o s t c e n t ra l n e rv o u s s y s te m. Parasitology 105,

4 0 9 - 4 1 6.

A m e n , R . I . a n d Me u le m a n , E .A . (1 9 9 2 ) . I s o la t io n o f mo th e r a n d d a u g h te r s p o ro c y s t s o f

Trichobilharzia ocellata f r o m Lymn aea stagnalis Parasitology Research 7 8 , 2 6 5 -2 6 6 .

A m e n , R . I ., T i jn a g e l , J .M.G . , v a n d e r K n a a p , W.P.W. , M e u le ma n , E .A . , d e L a n g e -d e K le rk ,

E .S .M. a n d S min ia , T . (1 9 9 1 ) . E f fe c t s o f Trichobilharzia ocellata o n h e m o c y t e s o f

Lymnaea stagnalis Developmental and C omparative Immunology

15 , 105-115 .

A m e n , R . I . , B a g g e n , J .M.C . , B e z e m e r , P.D . a n d d e J o n g -B r in k , M. (1 9 9 2) . M o d u la t io n o f

th e a c t iv i ty o f th e in t e rn a l d e fe n s e s y s t e m o f th e p o n d s n a i l

Lymnaea stagnalis

b y th e

a v ia n s c h i s to s o me Trichobilharzia ocellata Parasitology 104 , 33-40 .

Ange l i , V. , Faveeuw, C. , Roye , O. , Fon ta ine , J . , Te is s ie r , E . , Capron , A. , Wolowczuk , I . ,

C a p ro n , M . a n d T ro t t e in , E (20 01 ). R o le o f th e p a ra s i t e -d e r iv e d p ro s ta g la n d in D 2 in th e

in h ib i t io n o f e p id e rma l L a n g e rh a n s c e l l m ig ra t io n d u r in g s c h i s to s o mia s i s in fe c t io n .

Journal o f Experimental M edicine 193 , 1135-1147 .

A p p le to n , C .C . (1 9 8 3 ) . S tu d ie s o n Austrobilharzia terrigalensis ( T r e m a t o d a :

S c h i s to s o ma t id a e ) in th e s w a n e s tu a ry , w e s te rn A u s t ra l i a : i n fe c t io n in th e d e f in i t iv e

hos ts , Larus novaehollandiae International Journal fo r Para sitology 1 3 , 2 4 9 -2 5 9 .

A p p le to n , C .C . (1 98 4) . S c h i s to s o me d e rma t i t is - a n u n re c o g n iz e d p ro b le m in S o u th A f r i c a ?

South African M edical Journal 6 5 , 4 6 7 -4 6 9 .

Ap ple ton , C .C. (1986). Occurrence o f av ian Sch is tosom at idae (Trematoda) in Sou th Afr ic an

b i rd s a s d e te rm in e d b y a f a e c a l s u rv ey . South African Journal of Zoology 2 1 , 6 0 -6 7 .

A p p le to n , C .C . a n d B ro c k , K . (19 86 ). T h e p e n e t ra t io n o f ma m ma l ia n s k in b y c e rc a r i a e o f

Trichobilharzia s p . (T re ma to d a : S c h i s to s o m a t id a e ) f ro m S o u th A f r i c a . Onderstepoort

Journal o f Veterinary Research

5 3 , 2 0 9 -2 1 1 .

A p p le to n , C .C . a n d L e th b r id g e , R .C . (1 9 7 9 ) . S c h i s to s o m e d e rma t i t i s i n th e s w a n e s tu ary ,

w e s te rn A u s t ra l i a . Medical Journal o f Australia 131 , 141-144 .

A u g u s t in e , D .L . a n d W e l le r, T .H . (1 9 4 9) . E x p e r im e n ta l s tu d ie s o n th e s p e c i f i c i ty o f s k in

te s ts fo r th e d ia g n o s i s o f s c h i s to s o mia s i s . Journal o f Parasitology 3 5 , 4 6 1 -4 6 6 .

Bacha , W .J.Jr ., R oush , R .Jr . and Ic a rd i , S . (1982). In fec t io n o f the ge rb i l by the av ian sch is -

t o s o m e Austrobilharzia variglandis (M il le r and Northup 1926; Penn er 1953) . Journal of

Parasitology 6 8 , 5 0 5 -5 0 7 .

Bahga t , M . and R uppe l , A. (2002) . Bioc hem ica l com par ison o f the se r ine p ro tease (e las tase )

ac t iv i t ie s in ce rca r ia l sec re t ions f rom T richob i lha rz ia oce l la ta and S ch is tosom a manson i .

Parasitology Research

8 8 , 4 9 5 -5 0 0 .



2 1 8 P. HO R,~K, L. KOLAI~OV , ,A N D C .M . A D E M A

Ba hg at , M., Francklow, K. , D oen ho ff , M.J. , Li , Y.-L., Ra m zy, R.M.R., Kirsten, C. and

Ruppel , A. (2001). Infec t ion indu ces antibodies aga inst the cercarial secretions, but not

agains t the cercar ia l e las tases of Schi s tosoma mansoni , Sch i s tosoma haematob ium,

Schistosoma jap on icu m and Trichobilharzia oceUata. Parasi te Immunology 23, 557-565 .

Baird, J .K. and Wear, D.J. (1987). Cercarial dermatit is? Th e sw im m er s itch. Clinics in

Dermato logy 5 , 88-91 .

Bargues , M .D. and M as-Co ma , S . (1997). P hyloge net ic analys is o f lym naeid snail s based

on 18S rD N A sequences. Mo lecular Biology a nd Evolution 14 , 569-5 77 .

Bargues, M.D., M ang old, A.J. , Mufioz-Antoli , C. , Point ier , J . -P. and M as-C om a, S. (1997).

SS U rDN A characterizat ion o f lym nae id snai ls transmitt ing hum an fascioliasis in Sou th

and Cent ra l A mer ica . Journ al o f Parasitology 83, 1086-1092.

Bargues, M .D., Vigo, M., H orLk, P., Dvo ~ik, J. , Patzner, R.A., Pointier, J.P., Jackiewicz, M .,

M e i e r - B r o o k , C . a n d M a s - C o m a , S . ( 2 0 0 1 ) . E u r o p e a n L y m n a e i d a e ( M o l l u s c a :

Gastropoda), intermediate hosts of t rematodiases, bas ed on nuc lear r ibos om al D N A

ITS -2 sequences. Infect ion, Ge netics and Evolution 16, 1-23.

Barshene, J .V. and Staniavichiute, G.J. (1993). [K aryo type s of Trichobilharzia szidati and

Bilharziel la polonica (Schistosomatidae, Trematoda)]. Parazitologiya 27 , 41-47 . ( i n

Russian)

Barshene, J .V., Staniavichiute, G.J. and O rlovsk aya, O.M. (1989). [Ka ryo logica l investiga-

t i ons on tr ematode s o f t he f ami ly Sch i s tosom at idae i n No r th-Wes t Chuko tka] .

Parazitologiya 23, 496-5 03. ( in Russian)

Basch, P.E (1966). The l i fe cycle of Trichobilharzia brevis, n. sp. , an avian schistosome

f rom M alaya . Zeitsc hri f t f i ir Parasi tenkunde 27 , 242-251 .

Basch, P.E (1991). Schistosomes. Development, Rep rod uction and H os t Relations. N e w

York, Oxford: O xford U nivers i ty Press.

Bastert , J . , Sing, A. , Wollenberg, A. and K orting, H .C. (1998). Aqu arium dermatit is: cer-

carial derm atitis in an aquarist. Dermato logy 197, 84-86.

Ba t t en , P . J . ( 1956). The h i s topa tho logy o f sw imm er s i t ch . I . The sk in l e s ions o f

Schistosomatium douthitti and Gigantobilharzia huronensis in the unsensi t ized m ouse.

Am er ican Journal o f Pa tho logy 32 , 363-377 .

Baug h, S .C. (1978) . The miracidium o f Trichobilharzia indica Baug h, 1963 and i t s hatch-

ing. Revista Iberica di Parasi tologia 3 8 , 7 3 - 9 3 .

Bayssade-Dufour, C. and Ow-Yang, C .K. (1975). Th e senso ry receptors o f two cercariae

f rom Malays i a : Trichobilharzia brevis (Sch i s tosomat idae ) and Haplorch i s pumi l io

(Heterophyidae). Southeast Asian Journal of Tropical Medicine and Publ ic Heal th 6 ,

338-342 .

Ba yssa de-D ufou r, C. , Vuong, P.-N., Farhati , K. , Picot , H. and Albaret, J .-L. (1994). S pee d

of skin penetration and init ial m igrat ion route of infective larvae o f Schistosoma haema-

tob ium in M eriones unguicu la tus. Com ptes Rend us Hebd oma dai res des S~ ances d e

l Acad~ mie des Sc i ences 317, 529-5 33 .

Bay ssade-D ufour , C. , Mar tins, C. and Vuong, P .N . (2001) . H is topathologie d un module

mammif~re et dermati te cercarienne humaine. M~dicine e t Maladies Infect ieuses 31,

7 1 3 - 7 2 2 .

Bearup, A.J. and Langsford, W.A. (1966). Schistosome dermatitis in association with rice

growing in the Northern T erritory of Australia. Medical Journal of Australia 101, 521-52 4.

Bec htold, S. , W intergerst , U. and Butenandt , O. (1997). Badedermati tis du rch Zerkarien.

M o n a t s s c h r ~ K i n d e rh e i lk u n d e 145, 1170-1172.

Beer, S.A. and G erm an, S.M. (1994). [The ecolog ical prerequisites for the spread o f schis-

tosomal de rmat i t i s ( ce rca r i as i s ) i n Moscow and the Moscow a rea . ] M edi t s inska ja

Parazitologiya i Parazitarnye B ole zn i 1, 16 -19. ( in Russian)

Berg, K. and Reiter , H.EH. (1960). Observations on schistosome dermati t is in Denmark.



BIOLOGY OF

TRICHOBILH RZI

2 9

Acta Dermato-venereologica

4 0 , 3 6 9 -3 8 0 .

Bix le r , L .M . , Lerner , J .E , Ivanchen ko , M. , Mc Co rm ick , R .S . , Barnes , D.W. and Bay ne , C .J .

(2 0 0 1 ) . Ax e n ic c u l tu re o f

Schistosoma mansoni

s p o ro c y s t s in lo w-O2 e n v i ro n m e n t s .


8 7 , 1 1 6 7 -1 1 6 8 .

B la c k b u rn , C .R .B . a n d M a , M.H . (1 9 7 1) . S k in r e a c t io n s o f n a t iv e s in th e W e s te rn H ig la n d s

o f N e w G u i n e a t o a

Schistosoma mansoni

an t igen .

Tropical and Geographical Medicine

2 3 , 2 7 8 -2 8 1 .

Bla i r , D. and C opem an, D.B. (1977) . Sch is toso me derm at i t i s in North Queens land .

Medical

Journal of Australia

1, 40.

B la i r , D . a n d I s l a m, K . S . (19 8 3) . T h e l i f e -c y c le a n d m o rp h o lo g y o f

Trichobilharzia aus-

tralis

n . s p . (D ig e n e a : S c h i s to s o m a t id a e ) f ro m th e n a s a l b lo o d v e s s e l s o f th e b la c k d u c k

(Anas superciliosa)

i n Au s t ra l i a , w i th a r e v ie w o f th e g e n u s

Trichobilharzia. Systematic

Parasitology

5 , 89-117 .

B la n k e s p o o r , H .D . a n d R e im in k , R .L . (1 99 1 ) . T h e c o n t ro l o f s w im m e r s it c h in Mic h ig a n :

pas t , p resen t and fu tu re .

Michigan Academician

2 4 , 7 -2 3 .

B la n k e s p o o r , H .D . , C a m e ro n , S .C . a n d C a i r in s , J. Jr . (1 9 8 5 ). R e s i s t a n c e o f p u lmo n a te s n a i l

p o p u la t io n s to r e p e a te d t r e a tme n t s o f c o p p e r s u l f a t e .

Environmental Management

9,

4 5 5 - 4 5 8 .

B la n k e s p o o r , C .L . , R e imin k , R .L . a n d B la n k e s p o o r , H .D . (2 0 0 1 ) . E f f i c a c y o f p ra z iq u a n te l

i n t r e a t i n g n a t u r a l s c h i s t o s o m e i n f e c t i o n s i n c o m m o n m e r g a n s e r s .

Journal of

Parasitology

8 7 , 4 2 4 -4 2 6 .

Bloch, E.H. (1980).

In vivo

mic ro s c o p y o f s c h i s to s o mia s i s . I I . Mig ra t io n o f

Schistosoma

mansoni

in the lungs , l iv e r and in tes t ine .

American Journal o f Tropical Medicine and

Hygiene

2 9 , 6 2 -7 0 .

Bou rns , T .K.R. and El l i s , J .C . (1975) . At te m pts to t rans fe r im m uni ty to

Trichobilharzia

ocellata

(T re ma to d a : S c h i s to s o ma t id a e ) p a s s iv e ly v ia ly mp h o id c e l l s a n d /o r s e ru m.

Transactions of the Royal Society of Tropical Medicine and Hygiene

6 9 , 3 8 2 -3 8 7 .

B o u r n s , T . K . R . , E l l i s , J .C . a n d R a u , M . E . ( 1 9 7 3 ). M i g r a t i o n a n d d e v e l o p m e n t o f


(T re ma to d a : S c h i s to s o ma t id a e ) in i t s d u c k h o s t s.

Canadian

Journal of Zoology

51 , 1021-1030 .

B r a c k e t t , S . ( 1 9 3 9 ) . M e t h o d s f o r c o n t r o l l i n g s c h i s t o s o m e d e r m a t i t i s .

Journal of the

American Medical Association

113, 117-121.

Bracke t t , S . (1940) . Pa tho logy of sch is tosome dermat i t i s .

Archives of Dermatology and

Syphilology

42, 410--418.

B ra c k e t t , S . (1 9 42 ) . F iv e n e w s p e c ie s o f a v ia n s c h i s to s o me s f ro m W is c o n s in a n d Mic h ig a n

wi th th e l i f e c y c le o f

Gigantobilharzia gyrauli

(Bra ckett , 1940).


2 8 , 2 5 -4 2 .

Brum pt , E . (1931) .

Cercaria ocellata,

d 6 te rmin a n t l a d e rma t i t e d e s n a g e u rs , p ro v ie n t d u n e

b i lh a rz ie d e s c a n a rd s .

Comptes Rendus Hebdomadaires des S~ances de l Acad~mie des

Sciences Paris

193 , 612-614 .

B u c k le y , J .J .C . (1 9 3 8) . On d e rma t i t i s in M a la y a c a u s e d b y th e c e rc a r i a e o f

Schistosoma

spindale

Montgomery , 1906 .

Journal of Helminthology

16, 117-120.

B y k h o r s k a y a - P a v l o v s k a y a , I .E . ( 1 96 2 )

Key to the parasites of freshwater fishes of the

USSR.

Z o o lo g ic a l In st i tu t e o f th e Ac a d e m y o f S c ie n c e s o f th e U S S R . (E n g l i s h t r a n s la t io n

OT S , D e p a r tme n t o f C o m me rc e , W a s h in g to n , D .C . No . T T 6 4 -1 1 0 4 0 . 9 1 9 p p .

B y k h o r s k a y a - P a v l o v s k a y a , I .E . a n d R y z h i k o v , K . M . ( 1 9 5 8 ). [ S c h i s t o s o m e s

(S c h i s to s o m a t id a e L o o s s , 1 89 9) f ro m a n a t id s in Ya k u tiy a ].

Parazitologiceskij Sbornik

Zoologiceskovo Instituta Akademii Nauk SSSR

18 , 283-294 . ( in Russ ian)

C h a m o t , E . , T o s ca n i , L . a n d R o u g e mo n t , A . (1 9 9 8 ). P u b l i c h e a l th im p o r ta n c e a n d r i s k f ac -

t o r s f o r c e r c a r i a l d e r m a t i t i s a s s o c i a t e d w i t h s w i m m i n g i n L a k e L e m a n a t G e n e v a ,

S wi tz e r l a n d .

Epidemiology and Infection

120 , 305-314 .



2 2 0 P. H O R A K L . K O L A I~ O V A A N D C .M . A D E M A

C h ik ami , A . (1 9 6 1 ) . [S tu d ies o n


(La Valet te , 1855) in Ja pan . ]

Japanese Journal of Parasitology 10 , 106-118 . ( in Japan ese)

C h r i s t en sen , R .O . an d G reen , W.P. (1 92 8) . S tu d ies o n b io lo g ica l an d m ed ica l a sp ec t s o f

' s w i m m e r ' s i t c h . ' S c h i s t o s o m e d e r m a t i t i s i n M i n n e s o t a . Minnesota Medicine 11,

5 7 3 - 5 7 5 .

C h u , G .W. (1 9 5 8 ) . P ac i f i c a rea d i s t r ib u t io n o f f r e sh -w ate r an d m ar in e ce rca r i a l d e rmat i t i s .

Pacific Science

12 , 299-312 .

Cle gg, J.A . (1965).

In vitro

cu l t ivat ion

of Schistosoma mansoni. Experimental Parasitology

16, 133-147.

C leg g , J .A . (1 96 9) . S k in p en e t ra t io n b y c e rca r i ae o f th e b i rd sch i s to so m e

Austrobilharzia

terrigalensis: the

s t imu la to ry e f fec t o f ch o les t e ro l .

Parasitology

5 9 , 9 7 3 -9 8 9 .

Con nors , V.A. , Lodes , M .J . and Yosh ino , T .P . (1991) . Iden t i f icat ion o f a

Schistosoma man-

soni

sp o ro cy s t ex c re to ry sec re to ry an t io x id an t mo lecu le an d i t s e f f ec t o n su p ero x id e

p ro d u c t io n b y

Biomphalaria glabrata

h e m o c y t e s .

Journal of Invertebrate Pathology

5 8 , 3 8 7 -3 9 5 .

C o r t , W.W. (1 9 2 8 ). S ch i s to so m e d ermat i t i s in th e U n i t ed S ta t es (Mich ig an ) .

Journal of the

American Medical Association

90 , 1027-1029 .

Cort , W.W. (1936) . S tud ies on sch is to som e derm at i t i s . I . The p resen t s ta tus o f the sub ject .

American Journal of Hygiene

2 3 , 3 4 9 -3 7 1 .

C o r t , W.W. (1 9 5 0 ). S tu d ies o n sch i s to so m e d ermat i t i s . X I . S t a tu s o f k n o w led g e a f t e r mo re

th an tw en ty y ea r s .


5 2 , 2 5 1 -3 0 7 .

Cort , W.W., Mc M ullen , D.B. , Ol iv ier , L . and Bracke t t , S . (1940) . S tud ies on sch is to som e

d ermat i t i s . V I I . S easo n a l i n c id en ce o f Cercaria stagnicolae Talbo t , 1936 in re la t ion to

th e l i f e cy c le o f i t s sn a i l h o s t,

Stagnicola emarginata angulata

(S o w erb y ) .

American

Journal of Hygiene

3 2 , 3 3 -6 9 .

Cous tau , C . an d Yosh ino , T .P . (2000) . F luk es wi tho u t snai ls : advanc es in the

in vitro

cu l t i -

v a t io n o f i n t r amo l lu scan s t ag es o f t r emato d es .


9 4 , 6 2 -6 6 .

C u r t i s , L .A . an d H u b b ard , K .M . (1 9 9 0 ). T rem ato d e in fec t io n s in a g as t ro p o d h o s t m is rep -

resen ted b y o b se rv in g sh ed ce rca r i ae .

Journal of Experimental Marine Biology and

Ecology

143 , 131-137 .

D am ian , R .T . (19 87 ). M o lecu la r m im ic ry r ev i s it ed .

Parasitology Today

3 , 2 6 3 -2 6 6 .

Daw kins , R . (1990) . Paras i tes , des id erata l i s t s and the parado x of the o rgan ism.

Parasitology

100, 63 - 73 .

d e G en t i l e , L . , P i co t, H . , B o u rd eau , P ., B ard e t , R . , K er j an , A . , P i r io u , M. , L e G u en n ic , A . ,

B ay ssad e-D u fo u r , C . , C h ab asse , D . an d Mo t t , K .E . (1 9 9 6 ). L e d e rm at i t e ce rca r i en n e en

E u ro p e : u n p ro b lem e d e l a san t6 p u b l iq u e n o u v eau ? Bulletin de l Organisation Mondiale

de la Sant~ 74,

1 5 9 -1 6 3 .

d e Jo n g -B r in k , M . (1 9 9 5 ) . H o w sch i s to so me s p ro f it f ro m th e s t r e ss r e sp o n ses th ey e l i c i t i n

thei r hosts .


35 , 177-256 .

de Jong- Brink , M. , Ho rd i jk , P .L . , Vergeest , D.P .E .J. , Sch al l ig , H.D .EH . , Ki ts , K.S . and

T ermaa t , A . (1 9 9 2 ). T h e an t ig o n ad o t ro p ic n eu ro p e p t id e sch i s to so min in t e r fe res w i th

p er ip h era l an d cen t ra l n eu ro en d o cr in e mec h an i sms in v o lv ed in th e r eg u la t io n o f r ep ro -

d u c t io n an d g ro w th in th e sch i s to so me- in fec ted sn a i l

Lymnaea stagnalis. Progress in

Brain Research

9 2 , 3 8 5 -3 9 6 .

d e Jo n g -B r in k , M. , H o ek , R .M. , S mi t , A .B . , B erg amin -S assen , M.J .M. an d L ag ew eg , W.

(1995).

Schistosoma

paras i tes evoke s t ress response s in thei r snai l host by a cy tok ine- l ike

fac to r i n te r fe r in g w i th n eu ro en d o cr in e m ech an i sms . Netherlands Journal of Zoology 45 ,

1 1 3 -1 1 6 .

De spor tes , C . (1944/45) . La derm at i te des nageurs . Annales de Parasitologie Humaine et

Compar~e

2 0 , 2 6 3 -2 7 8 .

D ik k eb o o m, R . , v an d e r K n aap , W.P .W. , Meu leman , E .A . an d S min ia , T . (1 9 8 5 ) . A co m-



BIOLOGY OF TRICHOBILH RZl 22

parative s tudy on the internal defense sy s tem o f juveni le and adu l t Lymnaea stagnalis.

Immunology 55 , 547-553 .

Dikkeboom, R . , Bayne , C . J . , van de r Knaap , W.EW. and T i jnage l , J .M.G.H. (1988) .

Poss ib l e ro l e o f react ive fo rms of o xygen in in vitro kil l ing of Schistosoma mansoni

sporocys ts by hem ocytes ofL ym na ea stagnalis . Parasitology Research 75 , 148-154 .

Di ssous , C . and Cap ron , A . (1995) . Co nverge n t evo lu t ion of t ropo m yos in ep i topes .

Parasitology Today 11, 45-46.

Drnges , J . (1965) . Schis tosomat iden-Cercar ien S iJddeutschlands . Zeitschrif i f i ir

Tropenm edizin u nd Parasitologie

16 , 305-3 21 .

Dvo fS.k, J. , Sattmann, H., Hor~ik, E an d Kone(3n3~, R. (199 9). Bird sch istos om es fro m fresh -

wate r sna i ls i n Aus t r i a , w i th som e no tes on cur ren t p rob lem s (Digenea ,

Schistosomatidae). Mitteilungen der Osterreichischen Gesellschaft fiir Tropenmedizin

und P arasitologie 21 , 69-76 .

Dvo~ ~ik, J. , Vah~i~owi, ~, Ham pl, V ., Flegr, J. a nd HorS.k, E (2002). Co m pa riso n o f Euro pe an

Trichobilharzia species based on ITS 1 and ITS 2 sequences . Parasitology, 124, 307-313.

Eklu-Natey, D.T. , AI-Khudr i , M. , Gauthey, D. , Dubois , J .E , WiJes t , J . , Vaucher , C. and

Hug ge l , H . (1985). Ep idrm io log ie de l a de rmat it e des ba igneur s e t m orpho log ie de

Trichobilharzia cf. ocellata dans l e l ac L rm an. Rev ue Suisse Zoologie 9 2 , 9 3 9 - 9 5 3 .

Ellis , J.C. , Bo urns , T.K.R. and Rau, M .E. (1975). Migrat ion, dev elop m ent and con dit ion of

Trichobilharzia ocellata (Trematoda: Schistosomatidae) in ho m olog ou s challen ge infec-

tions. Canadian Journal o f Zoology 53 , 1803-1811 .

Fain, A. (1955). R echerch es sur les schis tosomes d oise aux au Ruand a-Urun di (Con go

beige). Revue de Zoologie et de Botanique Africaines 51 , 373-387 .

Fain, A . (1956a). N asa l trichobilharziasis: a ne w avian schistosomiasis.

Nature

177, 389.

Fa in , A . (1956b) . Les sch i s tosomes d o i se aux du genre

Trichobilharzia

Skr j ab in

et

Zakharov, 1920 au Ruanda-Urnndi . Revue de Zoologie et de Botanique Africaines 54,

147-178 .

Farley, J . (1971). A review o f the fam ily Schistosomatidae: excluding the gen us Schistosoma

f r o m m a m m a ls . Journal o f Helminthology 45 , 289-320 .

Feiler , W. and Haas, W. (1988a). Ho st-f inding in Trichobilharzia ocellata cercariae: swim-

ruing and a t tachm ent to the host . Parasitology 96 , 493-505 .

Feiler, W . an d Haas, W . (1988b): Trichobilharzia ocellata: chem ical st imul i o f duck skin for

cercarial attachment. Parasitology 96 , 507 -517 .

Frlster-H olst , R. , Disk o, R. , Rr w ert , J . , Brc kele r , W ., Kreiselmaier, I . and Christophers, E.

(2001). Cercarial dermati t is contracted via contact with an aquarium: case report and

review. British Jo urnal o f Derma tology 145, 638~540.

Gay, P., Ba yssa de-D ufou r, C. , Grenouillet, E , B oure zane , Y. and D ubo is, J.P. (1999). t~tude

exp6rimentale de dermatites cerc arienn es pro vo qu res par Trichobilharzia en France.

M gdicine e t M aladies Infectieuses 29 , 629-637 .

Gerhardus, M.J.T., Bag gen , J .M.C. , v an der Knaap, W .P.W . and Sm inia, T. (1991). Analy sis

of sur f ace ca rbohydra t es o f


miracidia and sporocysts us ing

lectin bind ing techniques. Parasitology 103, 51-59.

Gianotti , E and Luv on i, R. (1958). Ulteriori contributi al ia con os cen za del la pato log ia

cutan ea del le m ond ariso e dei t rapiantatori . Rassegna di M edicina Industriale e d i lgiene

del Lavoro 27 , 101-116 .

Go lo, D. , A cco rdini , A. , Con solaro , S., Mo scon i , M .C. and Ferrari, A . (1998). L a dermati te

de l bagnante de l L ago d i Garda. L lgiene Moderna 110 , 443 -457 .

Grac zyk, T .K. and Shif t, C.J. (2000) . R ecov ery of avian schis tosome cercar iae f rom water

using pe netrat ion st imulant m atrix with an unsaturated fat ty acid. American Journal of

Tropical M edicine an d Hygiene 63 , 174-177 .

G racz yk , T. K., Shift, C . J. , Sladen, W . J. L. and Cranfieldt , M . (1993). A ttemp ts to control



22 2 P. HORAK, L. KOL,~I~OV, ,AND C.M. ADEMA

avian bloo d flukes in a n ational wildfow l refuge and in a captive system. In: Proceedings

of the 24th Annual Conference of the International Association of Aquatic Animal

Medicine F.B. Andrews, ed.), pp. 79-83. Chicago: Ch icago Un iversity Press.

Graefe , G., Asp/Sck, H. and Picher, O. 1973). A ufreten von B ade- derm atitis in t3sterreich

und M6glichkeiten ihrer Bekiimpfung.

Zentralblatt fii r Bakteriologie Mikrobiologie

und Hygiene. I. Abt. Originale A

225, 398--405.

Grassi , L. , Jorda, M.T., Andra de, Z. and Cappa, S.M.G. 2001). Schistosoma mansoni

miracidia are ki l led by the defense sys tem of an Argent ine s t ra in o f

Biomphalaria

straminea. American Journal o f Tropical Medicine and Hygiene

65, 290-292.

Guth, B.D., Blankespoor, H.D., Reimink, R.L. and Johnson, W.C. 1979). Prevalence of der-

mat i t i s -producing schis tosomes in natural bi rd populat ions of lower Michigan.

Proceedings of the Helminthological Society Washington 46, 58-63.

Haas, W. 1985). Bilharzio se: die biolo gisch e und biotec hnisch e Bek~impfung einer

Tropenkrankheit . II . Anwendung sbezogene zool. Grundlagenforschung.

Verhandlungen

der Deutschen Zoologischen Gesellschafi

78, 45-6 0.

Haas, W. 1992). P hysi olog ical analysis of cercarial behaviour.


78,

243-255.

Haas , W. 2000). The behavioral biology of echinos tomes . In:

Echinostomes as

Experimental Models for Biological Research

B. Fried and T.K. Graczyk, eds), pp.

175-197. Dordrecht: Kluwe r Acad emic Publishers.

Haas, W. 2001). Ho st finding mechan isms. In:

Biology Structure Function: Encyclopedic

Reference o f Parasitology

H. Mehlhorn, ed.), edn 2: pp. 382-383 . Heidelberg: Springer-

Verlag.

Haas, W. and Haberl, B. 1997). Host recognitio n by trem atode mirac idia and cercariae. In:

Advances in Trematode Biology

B. Fried and T.K. Graczyk, eds), pp. 197-227. B oca

Raton: CRC Press.

Haas, W. and Pietsch, U. 1991). M igration of


schistosomula in the

duck and in the abnormal m urine host. Parasitology Research 77, 642--644.

Haas, W. and van de Roem er, A. 1998). Invasion of the vertebrate skin by cercariae of

Trichobilharzia ocellata: penetra t ion processes and s t imulat ing hos t s ignals .


84, 787-795.

Haas, W., Gui, M., Haberl, B. and Strobel, M. 1991). M iracid ia

of Schistosomajaponicum:

appro ach and attach men t to the snail host. Journal o f Parasitology 77, 509-513.

Haberl , B. and Haas, W. 1992). Miracidium of

Schistosoma mansoni:

a macromolecular

glycocon jugate as signal for the beha vior after contact with the snail host .

Comparative

Biochemistry and Physiology A - Comparative Physiology

101, 329-333.

Haemm erl i , U. 1953). Sch is tosomen-Derm at i t i s am Zi ir ichsee. Dermatologica 107,

302-341.

Hahn, U.K., Bender, R.C. and Bayne , C.J 2001a). Killing of Schistosoma mansoni sporo-

cysts by haemocytes from resistant

Biomphalaria glabrata:

role of reactive oxygen

species. Journal of Parasitology 87, 292-299.

Hahn, U.K., Bender, R.C. and Bayn e, C.J. 2001b). Involvem ent of nitric oxid e in killing of

Schistosoma mansoni

sporocysts by haemocytes from resistant

Biomphalaria glabrata.

Journal o f Parasitology 87, 778-785.

Hamb urger, J ., He-Na, Ab basi , I . , Ram zi, R.M., Jourdane, J . and Ruppel, A. 2001).

Polymerase chain reaction assay based on highly repeated sequence of

Schistosoma

haematobium:

a po tential tool for m onitoring sch istosome-infested water.

American

Journal o f Tropical Medicine and Hygiene

65, 907-91 1.

Hen dricks, J.R. and Cort, W.W. 1956). A study of the

in vitro

actions of antiserums on the

cercariae of certain bird schistosomes. Journal o f Parasitology 42, 557-564.

Herber, E.C. 1938). Schistoso me derm atitis in dog.

Journal o f Parasitology 24

474-475.



BIOLOGY OF

TRICHOBILH RZI

3

H o e f f i e r , D .E (1 9 7 7) . S w im m e rs i t c h ( c e rc a r i a l d e rma t i t i s ) .

Cutis

19, 461--466.

H o e f f i e r , D .E (1 9 8 2 ). C e rc a r i a l d e rma t i t i s. In :

CR C Handbook Series in Zoonoses

(J .H.

S tee le , ed . ) , Sec t ion C: Paras i t ic Zoonose s (G.V. Hi l l ye r and C.E . Ho pla , eds ) , pp . 7 -15 .

B o c a R a to n : C R C P re s s .

H o e k , R .M . , S m i t , A .B . , F r in g s , H . , V in k , J.M. , d e J o n g -B r in k , M . a n d G e ra e r t s , W.P .M.

( 1 9 96 ) . A n e w I g - s u p e r f a m i l y m e m b e r , m o l l u s c a n d e f e n c e m o l e c u l e ( M D M ) f r o m

Lymnaea stagnalis

i s d o w n - r e g u l a t e d d u r i n g p a r a s i t o s i s .

European Journal of

Immunology 2 6 , 9 3 9 -9 4 4 .

H o e k , R .M. , v a n K e s te re n , R .E . , S mi t , A .B . , d e J o n g -B r in k , M. a n d G e ra e r t s , W.P .M.

(1 9 9 7) . A l t e re d g e n e e x p re s s io n in th e h o s t b ra in c a u s e d b y a t r e ma to d e p a ra s i t e : n eu -

r o p e p t i d e g e n e s a r e p r e f e r e n t i a l l y a f fe c t e d d u r i n g p a r a s i t o s i s .

Proceedings o f the

National Acade my o f Sciences o f the United States o f America 94 , 14072-14076 .

H o rn , P . (1 99 5) . D e v e lo p m e n ta l ly r e g u la te d e x p re ss io n o f s u r fa ce c a rb o h y d ra te re s id u e s o n

la rv a l st a g e s o f th e a v ia n s c h i s to s o me

Trichobilharzia szidati. Folia Parasitologica

42 ,

2 5 5 - 2 6 5 .

Hor~k , P . and Deme, R. (1998) . Lec t ins and sacchar ides in

Lymnaea stagnalis

h a e m o c y t e

re c o g n i t io n .

Comparative Haematology International 8 210-218.

HorS.k, P. and Kol~i?ov~i,L . (2 0 0 0 ) . S u rv iv a l o f b i rd s c h i s to s o me s in ma mma l ia n lu n g s .

International Journal fo r Parasitology 30

6 5 - 6 8 .

Hor~ik , P . and Kol~?ov~i , L . (2001). Bir d sch is tosom es : do the y d ie in m am m alian sk in?

Trends in P arasitology 17, 66---69.

Hor~ik , P . and v an de r Kn aap , W.P .W. (1997) . Le c t ins in sna i l - t re m atode imm une in te rac -

t ions : a rev iew.

Folia Parasitologica 44

1 6 1 -1 7 2 .

HorS_k, P., W eise r, J ., Mike~, L. an d Koki~ov~i,L. (1996). The effect

of Bacillus thuringien-

sis

M -e x o to x in o n t r e m a to d e c e rc a r i a e .

Journal o f Invertebrate P athology 68

4 1 - 4 9 .

Hor~ik, P., Grubho ffer, L. , M ikeL L. and Tich~i, M . (1997). Lec tins o f

Trichob ilharzia szidati

cerca r iae .

Parasite

1 , 2 5 5 -2 6 5 .

Hor~ik, P. , Kol~i~ov~i, L. and D vo ~ik , J . (199 8a).


n. sp.

(S c h i s to s o ma t id a e , B i lh a rz ie l lin a e ) , a n e w n a s a l s c h i s to s o me f ro m E u ro p e .

Parasite 5

3 4 9 - 3 5 7 .

HorSk, P. , Kov~, L. , Kol~i?ov~i,L . a n d N e b e s ~ o v ~ i , J . (1 9 9 8b ) . C e rc a r i a - s c h i s to s o m u lu m

s u r fa ce t r a n s fo rma t io n o f

Trichobilharzia szidati

a n d i t s p u ta t iv e imm u n o lo g ic a l imp a c t .

Parasitology

116 , 139-147 .

HorLk, P . , Ne e lem an , A.P ., van de r Kn aap , W.P .W. and Sm in ia , T . (1998c) . Effec t o f sac -

c h a r i d e s o n p l a s m a m e d i a t e d h a e m a g g l u t i n a t i o n a n d in vitro p h a g o c y t o s i s b y

h a e mo c y te s o f th e s n a i l Lymnaea stagnalis. Comparative Haematology International 8

4 3 - 4 9 .

Hor~k, P., Dvo ~ik , J., Kol~i?ov~i,L. a nd T refi l , L. (1999).


a p a th o g e n

o f th e a v ia n a n d ma m m a l ia n c e n t ra l n e rv o u s s y s te ms .

Parasitology

119 , 577-581 .

H o rd i jk , P .L . , S c h a l l ig , H .D .F .H , E b b e r in k , R .H .M. , d e J o n g -B r in k , M. a n d J o o s s e , J .

(1991). P r im ary s t ruc tu re and o r ig in o f sch is tosom in , an an t i -gonad otrop ic neuro pep t ide

o f th e p o n d s n a i l

Lymnaea stagnalis. Biochemical Journal

2 7 9 , 8 3 7 -8 4 2 .

H o w e l l , M.J . a n d B o u rn s , T .K .R . (1 9 7 4 ) .

In vitro

c u l t u r e o f

Trichobilharzia ocellata.

International Journal fo r Pa rasitology 4 , 4 7 1 -4 7 6 .

H o w e l l s , R . E . , G e r k e n , S . E . , R a m a l h o - P i n t o , F . J . , K a w a z o e , U . , G a z z i n e l l i , G . a n d

Pelle grin o, J . (1975).


t a i l l o ss in r e l a t io n to p e rm e a b i l i ty ch a n g e s

d u r in g c e rc a r i a - s c h i s to s o m u lu m t r a n sfo rma t io n .

Parasitology

7 1 , 9 -1 8 .

Hr~dkov~i, K. and Hor~ik , P . (2002) . N euro tro p ic beh av io ur o f


in

d u c k s a n d mic e .

Journal o f Helminthology

7 6 , 1 3 7 -1 4 1 .

Hs iJ , H.F . and Am eel , D.J . (1956) . In t rad erm al reac t io ns to

Schistosomajaponicum

and S.

mansoni

a n t i g e n s i n s c h i s t o s o m e d e r m a t i t i s c a s e s .

Am erica n Journal o f Tropical



4

P. HOR, .K, L. KOLA FIov /i, AN D C.M. AD EMA

Medicine and Hygiene 5, 841-846.

Hurley, M., Hearnden, M.N., Blair, D. and Kay, B.H. (1994). Larval trematodes in fresh-

water snails at the Ross River Reservoir, Northern Australia, with emphasis on

Trichobilharzia sp(p)., causative agents of swimmer's itch. Australian Journal of Marine

and Freshwater Research 45, 563-567.

Islam, K.S. (1986a). Development of Trichobilharzia australis Blair and Islam, 1983 in the

snail, Lymnaea lessoni Des hayes and in an experimental definitive h ost, the Mu sco vy

duck. Journal of Helminthology60, 301-306.

Islam, K.S. (1986b). The morphology and life-cycle of Trichobilharzia arcuata n. sp.

(Schistosomatidae: Bilharziellinae) a nasal schistosome of water whistle ducks

Dendrocygna arcuata) in Australia. Systematic Parasitology 8, 117-128.

Islam, K.S. and Copem an, D.B. (1986). The m orpho logy and life cycle of Trichobilharzia

parocellata

(Johnston and Simpson, 1939) Islam and Copeman , 1980 from the visceral

blo od vessels of Australian anatids.

Systematic Parasitology

8, 39--49.

Jackiew icz, M. (1988). The penis as a valuable d iagnostic feature in low er taxo nom ic units

of the family Lymnaeidae. Malakologische Abhandlungen - Museum Dresden 13,

23-26.

Jackiewicz, M. and Koralewska-Batura, E. (1995). The shell surface sculpture of

Lymnaeidae (Gastropoda: Pulmonata: Basommatophora). Malakologische

Abhandlungen - Museum Dresden

17, 191-197.

Janeway, C.A. (1989). Approaching the asymptote: evolution and revolution in immunology.

Cold Spring Harbor Symposia on Quantitative Biology 54, 1-13.

Jarcho, S. and van Burkalow, A. (1952). A geographical study of 'swim mer 's itch' in the

United States and Canada.

Geographical Review

42, 212-226.

Joosse, J. an d van Elke, R. (1986).

Trichobilharzia ocellata:

phy siolo gical characterization

of giant g rowth, glyco gen depletion, and absence o f reproductive activity in the inter-

mediate host, Lymnaea stagnalis. Experimental Parasitology62, 1-13.

Joubert, P.H., Kruger, EJ. and Pretorius, S .J. (1990). Susceptibility of South-African Bulinus

africanus populations to infection with Schistosoma haematobium. Transactions of the

Royal Society of Tropical Medicine and Hygiene 84, 100-102.

Kalbe, M., Haberl, B. and Haas, W. (1996).

Schistosoma mansoni

miracidial host-finding:

species specificity of an Egyp tian strain. Parasitology Research 82, 8-13.

Kalbe, M., Hab ed, B. and Haas, W. (1997). Miracidial host-finding in Fasciola hepatica and

Trichobilharzia ocellata is stimulated by species-specific glycoc onjugates released fr om

the ho st snails. Parasitology Research 83, 806-812.

Kalbe, M., Haberl, B. and Haas, W. (2000). Snail host finding by Fasciola hepatica and


compound analysis of 'miracidia-attracting glycoproteins'.

Experimental Parasitology 96, 231-242.

Kassai, T. (1999). Veterinary Helminthology. Oxford: Butterworth-Heinemann.

Khalil, L. E (2002). Fa mily Schisto som atidae Stiles and Hassall, 1898. In Keys to the

Trematoda (D.I. Gib son, and A. Jones and R.A. B ray eds), vol. 1. Wallingford: CA B

International.

Kilias, R. and Frick, W. (1964). Die Zwischenwirtsschnecken wichtiger einheimischer

Hans- und Nutztier-Helminthen.

Angewandte Parasitologie

5, 13-45.

Kimmig, P. and Meier, M. (1985). Parasitologische Untersuchungen, Diagnose und Klinik

der Zerkariendermatitis Hy gien isch e Bede utung ftir Badew asser gem~issigter Zon en.

Zentralblatt fiir Bakteriologie, Mikrobiologie und Hygiene, I. Abt. Originale B. 181,

390-408.

Knight, R. and Worms, M.J. (1972). An outbreak of cercarial dermatitis in Britain.

Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 21.

Kock, S. (2000). Evaluation of the Importance of Different Characters or the Systematic




Classification o f European Trichobilharzia Species. P h .D . T h e s i s . K ie l : U n iv e r s i ty o f

K ie l .

K o c k , S . (2 0 0 1 ) . In v e s t ig a t io n s o f in t e rm e d ia te h o s t s p e c i f i c i ty h e lp to e lu c id a te th e t a x o -

n o mic s t a tu s o f


(D ig e n e a : S c h i s to s o ma t id a e ) .

Parasitology

123 , 67-70 .

K o c k , S . a n d B tc k e le r , W. (1 9 9 8) . O b s e rv a t io n s o n c e rc a r i a l c h a e to ta x y a s a me a n s fo r th e

i d e n t i fi c a t i o n o f E u r o p e a n s p e c i e s o f Trichobilharzia S k r ja b in a n d Z a k h a ro v , 1 9 2 0

(D ig e n e a : S c h i s to s o ma t id a e ) . Systematic Parasitology 43 , 159-166 .

Kol~i~ov~i,L . (2 0 0 1 ) . C e n t ra l n e rv o u s s y s te m a s a t a rg e t o f h e lmin th m ig ra t io n in h u ma n s .

Helminthologia 3 8 , 2 3 7 -2 4 1 .

Kol~ir ov~i,L . a n d H o r~ ik , P . (1 9 9 6 ) . M o rp h o lo g y a n d c h a e to ta x y o f


N e u h a u s , 1 9 52 c e rc a r i a e (T re m a to d a : S c h i s to s o m a t id a e : B i lh a rz ie l l in a e ) . Helminth-

ologia 3 3 , 3 -7 .

Ko l~ov~ i, L. , Gottwaldov~i, V., Gechov~i, D. and Sevcov~, M . (1989). Th e o ccurr ence o f cer-

c a r i a l d e rma t i t i s i n C e n t ra l B o h e mia .

Zentralblattfiir Hygiene und Umweltmedizin

189,

1 -1 3 .

K o l~ ir o v~ i, L . , H o rL k , P . a n d F a j f r l~ , K . (1 9 9 2 ) . C e r c a r i a e o f


N e u h a u s , 1 9 52 (T re ma to d a : S c h i s to s o m a t id a e ) : t h e c a u s a t iv e a g e n t o f c e rc a r i a l d e r-

ma t i t i s i n B o h e m ia a n d Mo ra v ia . Folia Parasitologica 3 9 , 3 9 9 -4 0 0 .

Kol~i~ov~i,L . , S3?kora , J . and Bah , B .A . (1994) . Se ro d iagn os is o f ce rc a r ia l de rm at i t i s wi th

a n t ig e n s o f Trichobilharzia szidati a n d Schistosoma manson i. Central Europ ean Journal

of Public H ealth 2 , 19-22 .

Kol~i~ov~i,L . , Ho rak , P . and S i tko , J . (1997) . Cer ca r ia l de rmat i t i s in focus : sch is tosom es in

th e C z e c h R e p u b l i c .

Helminthologia 34

1 2 7 -1 3 9 .

Koi~ i~ov~, L . , S k irn is son , K. and Hor~ik, P . (1999). Sch is to som e ce rca r iae as the causa t ive

a g e n t o f s w im me r s i t c h in I c e la n d . Journal o f Helminthology 7 3 , 2 1 5 -2 2 0 .

Kol~ i~ov~i, L . , H or~ik, P . and (~ada , F . (2001) . H is to pa th o lo gy of C N S and nas a l in fe c -

t i o n s c a u s e d b y


i n v e r t e b ra te s .


87 ,

6 4 4 - 6 5 0 .

Kou~ilov~i,P . (2 0 0 1) . H i s to p a th o lo g ic a l o b s e rv a t io n o f th e m o u s e s k in a n d C N S d u r in g th e

p r i m a r y i n f e c t i o n a n d r e i n f e c t i o n s b y b i r d s c h i s t o s o m e Trichobilharzia regenti.

Helminthologia 3 8 , 2 4 7 -2 4 8 .

Ko u~ilovL P. a nd Kol~i~ov~,L . (2001) . His topa tho log ica l changes in the mo use sk in in fec ted

w i th Trichobilharzia regenti. Helminthologia 38,167.

Kou~ilov~i, P. an d Kohi~ov~i,L . (2 0 0 2 ). V a r i a t io n s in imm u n o f lu o re s c e n t a n t ib o d y re s p o n s e

a g a in s t

Trichobilharzia

a n d

Schistosoma

a n t ig e n s i n c o m p a t i b l e an d n o n c o m p a t i b l e

hosts . Parasitology Research 8 8 , 5 1 3 -5 2 1 .

K ra m p i tz , H .E ., P ie k a r s k i , G . , S a a th o f f , M. a n d We b e r , A . (19 74 ). Z e rk a r i e n -D e rm a t i t i s.

Miinchener Medizinische W ochenschrift 116 , 1491-1496 .

Krua trachue , M . , Bha ibu laya , M . , Chesdapan , C . and H ar inasu ta , C . (1968). Trichobilharzia

maegraithi s p . n o v . , a c a u s e o f c e rc a r i a l d e rma t i t i s i n T h a i l a n d . Annals of Tropical

Medicine an d Parasitology 6 2 , 6 7 -7 3 .

K u l l a v a n i j a y a , P . a n d W o n g w a is a y a w a n , H . (1 9 9 3) . O u tb re a k o f c e rc a r i a l d e rm a t i t i s i n

T h a i l a n d . International Journal o f Dermatology 3 2 , 1 1 3 -1 1 5 .

Ku rach i , S . , Song , Z .W. , Taka gak i , M. , Yang, Q . , W in te r , H.C. , K urach i , K. and G olds te in ,

I .J . (19 9 8 ) . S ia l i c -a c id -b in d in g e c t in f ro m th e s lu g

Limaxflavus:

c lo n in g , e x p re s s io n o f

t h e p o l y p e p t i d e , a n d t i s su e l o c a l i z a t i o n . European Journal of Biochemistry 254 ,

2 1 7 - 2 2 2 .

L a mb e r tu c c i , J .R . (1 9 9 3 ) .


p a th o lo g ic a l a n d c l in i c a l a s p e c t s . In :

Hum an Schistosomiasis (P . J o rd a n , G . We b b e a n d R .E S tu r ro c k , e d s ) , p p . 1 9 5 -2 3 5 .

W a l l in g fo rd : C A B In te rn a tio n a l .



22 6 P. HOR ,~K, L . KOL, ,ROVA AN D C.M. AD EM A

L a n d m a n n , H . , T h a i , D .D . , Ng o a n , T .V . a n d Ng a , V .B . 1 9 6 1 ) . C e rc a r i e n -De rm a t i t i s b e i

R e i s p f l a n z e r n i n V i e t n a m .

Zentralblatt fiir Bakteriologie, Parasitenkunde,

Infektionskrankheiten und Hygiene 182 , 410-416 .

L a n g a n d , J . an d M o r a n d , S . 1 9 9 8 ). H e r i t a b l e n o n - s u s c e p t i b i l i t y i n an a l l o p a t r i c

h o s t - p a r a s i t e s y s t e m :


M o l l u s c a )

Echinostoma caproni

P la ty h e lmin th d ig e n e a ) .


8 4 , 7 3 9 -7 4 2 .

L a rd a n s , V. a n d D is s o u s , C . 1 9 98 ). S n a i l c o n t ro l s t r a te g ie s fo r r e d u c t io n o f s c h i s to s o mia -

s is t ransm iss ion .

Parasitology Today

14, 413--417.

L a Va le t te d e S t . Ge o rg e , A . 1 8 5 5 ) .

Symbolae ad Trematodum Evolutionis Historiam.

Disse r ta t ion . Bero l ius .

L tg e r , N . a n d Ma rt in -L o eh r, C . 1 9 9 9 ). L a d e rm a t i t e c e rc a r ie n n e : u n d t g r t m e n t d e s b a ig -

nades es t iva les . Actua li t s P harmaceutiques 3 7 7 ) , 4 9 -5 0 .

L e ig h to n , B . J. , Z e rv o s , S . a n d We b s te r , J .M. 2 0 00 ). E c o lo g ic a l f a c to r s in s c h i s to s o me

t ra n s mis s io n , a n d a n e n v i ro n m e n ta l ly b e n ig n me th o d fo r c o n t ro l l in g s n a i ls in a r e c re -

a t io n a l l a k e w i th a r e c o rd o f s c h i s to s o me d e rma t i t i s .

Parasitology International

49,

9 - 1 7 .

L e v in e , N .D . , C la rk , D .T . a n d Ha n s o n , L .E . 1 9 5 6 ) . E n c e p h a l i t i s i n a s wa n d u e to

Dendritobilharzia

s p . T r e m a t o d a : S c h i s t o s o m a t i d a e ) .


42 ,

4 9 6 - 5 0 0 .

Lie , K.J . 1982) . Surv iv a l o f Schistosoma mansoni a n d o th e r t r e ma to d e l a rv a e in th e s n a i l

Biomphalaria glabrata.

A d i s c u s s i o n o f t h e i n t e r f e r e n c e h y p o t h e s i s .

Tropical and

Geographical Medicine

34 , 111-122 .

Lie , K.J . and He ynem an, D. 1977) .

Schistosoma mansoni, Echinostoma lindoense,

a n d

Paryphostomum segregatum: i n t e r fe re n c e b y t r e ma to d e l a rv a e w i th a c q u i re d r e s i s t a n c e

in sna i ls ,

Biomphalaria glabrata. Experimental Parasitology

4 2 , 3 4 3 -3 4 7 .

Lie , K.J . and Ow-Y ang , C .K. 1973) . A f ie ld t r ia l to con tro l

Trichobilharzia brevis

b y d i s -

p e r s in g e g g s o f

Echinostoma audyi. Southeast Asia n Journal of Tropical M edicine an d

Public Health

4 , 2 0 8 -2 1 7 .

Lie , K.J ., H eynem an, D. and Jeong , K.H. 1976) . S tud ies on res is tance in sna i ls . 7 . Ev idence

o f in t e r fe re n c e w i th th e d e fe n s e r e a c t io n in


b y t r e ma to d e l a rv a e .


6 2 , 6 0 8 -6 1 5 .

Lim , H.-K . and Heynem an, D. 1972) . In t ram ol luscan in te r - t rematod e an tagonism : a rev iew

o f f a c to r s in f lu e n cin g th e h o s t -p a ra s i t e s y s t e m a n d i t s p o s s ib le ro le in b io lo g ic a l c o n t ro l .


10 , 191-268 .

Liu , Z . , Chen , M . , J in , G. , Tan , Y. and Yang , F . 1977) . [A survey o f the ae t io log ic a l agen t

o f p a d d y - f i e ld d e rma t i t i s i n J i a n X ia n , J i l i n p ro v in c e , w i th p re l imin a ry o b s e rv a t io n s o f

th e l i f e h i s to ry o f

Trichobilharzia jianensis

sp . nov. Trem atoda : Sch is toso ma t idae ) . ]

Acta Zoologica Sinica

2 3 , 1 6 1 -17 4 . in C h in e s e )

Lod es , M.J . and Yosh ino , T .P. 1990) . The e ffec t o f sch is tosom e excre to ry sec re to ry p rod -

uc ts on


h e mo c y te m o t i li t y .

Journal o f Invertebrate Pathology

56 ,

7 5 - 8 5 .

Lod es , M.J . , Connors , V.A. and Yosh ino , T .P. 1991) . Iso la t io n and fun c t iona l charac te r iza -

t io n o f s n a i l h e m o c y te -m o d u la t in g p o ly p e p t id e f ro m p r ima ry s p o ro c y s t s o f

Schistosoma

mansoni. Molecular and Biochemical Parasitology 49 , 1 -10 .

Lok en , B .R. , Spencer , C .N. and Grana th , W.O.J r. 1995) . P reva lenc e and t ransmiss io n o f

c e r c a r i a e c a u s i n g s c h i s t o s o m e d e r m a t i t i s i n F l a t h e a d L a k e , M o n t a n a .

Journal o f

Parasitology

8 1 , 6 4 6 -6 4 9 .

L o k e r , E .S . 1 97 8) . N o rma l d e v e lo p me n t o f

Schistosomatium douthitti

in the sna i l

Lymnaea

catascopium. Jo urnal o f Parasitology 64,

9 7 7 - 9 8 5 .

L o k e r , E .S . 1 9 8 3 ) . A c o m p a ra t iv e s tu d y o f th e l i f e -h i s to r ie s o f ma m ma l ia n s c h i s to s o me s .

Parasitology 8 7 , 3 4 3 -3 6 9 .




L o y , C . a n d H a a s , W. 2 0 0 1 ) . P re v a le n c e o f c e rc a r i a e f ro m Lymnaea stagnalis sna i ls in a

p o n d s y s te m in S o u th e rn G e rma n y .


8 7 , 8 7 8 -8 8 2 .

M a c fa r l a n e , W .V . 1 9 4 9 ). S c h i s to s o me d e rma t i t i s i n N e w Z e a la n d . P a r t I I . P a th o lo g y a n d

imm u n o lo g y o f c e rc a r i a l l e s io n s .

American Journal o f Hygiene 50,

1 5 2 -1 6 7 .

M acfa r lane , W.V. 1952) . S ch is tosom e derm at i t i s in Aus t ra l ia .

M edical Journal o f Australia

3 9 , 6 6 9 - 6 7 2 .

M ac lnn is , A.J . 1965) . Responses o f

Schistosoma mansoni

mira c id ia to chem ica l a t t rac tan ts .

Journal o f Parasitology 5 1 , 7 3 1 -7 4 6 .

M a c y , R .W. , Mo o re , D . J . a n d P r i c e , W .S . 1 9 5 5 ) . S tu d ie s o n d e rm a t i t i s -p ro d u c in g s c h i s to -

s o me s in th e p a c i f i c n o r th w e s t , w i th s p e c ia l r e fe re n c e to

Trichobilharzia oregonensis.

Transactions of the American M icroscopical Society

7 4 , 2 3 5 -2 5 1 .

M a le k , E .A . a n d A rms t ro n g , J .C . 1 96 7 ). In fe c t io n w i th

Heterobilharzia americana

in p r i -

mates .

American Journal o f Tropical Medicine and Hygiene

16 , 708-714 .

M a rg o n o , S .S . 1 9 6 8 ) . C e rc a r i a o f


Basch , 1966 in Djakar ta a s a

p o s s ib le c a u s e o f s c h i s to s o me d e rma t i t i s .

Medical Journal o f Malaya

2 2 , 3 0 6 -3 1 2 .

M athia s , P. 1930). Sur

Cercaria o cellata

L a Valette .

Annales de Parasitologie Humaine et

Comparde

8 , 151-160 .

M c C le l l a n d , G . a n d B o u rn s , T .K .R . 1 9 69 ). E f fe c t s o f Trichobilharzia ocellata on growth ,

r e p r o d u c t i o n , a n d s u r v i v a l o f

Lymna ea stagnalis. Exp erim enta l Parasitology

24,

1 3 7 -1 4 6

M c L a re n , D . J . a n d H o c k te y , D . J . 1 9 7 7 ) . B lo o d f lu k e s h a v e a d o u b le o u te r me m b ra n e .

Nature 2 6 9 , 1 4 7 -1 4 9

M c L e o d , J . A . 1 9 3 7) . T w o n ew s c h i s t o s o m i d tr e m a t o d e s f r o m w a t e r - b i rd s . Journal of

Parasitology 2 3 , 4 5 6 -4 6 6 .

M c L e o d , J .A . a n d L i t t l e , G .E . 1 9 4 2 ). C o n t in u e d s tu d ie s o n c e rc a r i a l d e rma t i t i s a n d th e

t r e ma to d e f a m i ly S c h i s to s o ma t id a e in M a n i to b a .

Cana dian Journal of Research Section

D ) 20 , 170-181 .

M c M u l le n , D .B . a n d B e a v e r , P .C . 1 9 4 5 ) . S tu d ie s o n s c h i s to s o me d e rma t i t is . IX . T h e l i f e

c y c le s o f th re e d e rma t i t i s -p ro d u c in g sc h i s to s o me s f ro m b i rd s a n d a d i s c u s s io n o f th e

s u b fa mi ly B i lh a rz ie l l in a e T re ma to d a : S c h i s to s o ma t id a e ) .


42 , 128-154 .

M cM ullen , D.B. and Bracke t t , S . 1948) . S tud ies on sch is tosome dermat i t i s . X. Dis t r ibu t ion

a n d e p i d e m i o l o g y in M i c h i g a n . American Journal o f Hygiene 4 7 , 2 5 9 -2 7 0 .

M el l ink , J . J. and van den Bovenkam p, W. 1985) .

In vitro

culture of intramoUuscan s tages of

the av ian sch is tosome

Trichobilharzia ocellata. Zeitschrift iir Parasitenkunde

7 1 ,3 3 7 -3 5 1 .

M eyer , P .O. 1964) . D ie Trem atoden la r ven aus dem G ebie te von ZUrich .

Vierteljahrsschrift

de r Naturforschenden Gesellschafi in Ziirich 109 , 277-372 .

M e y e r , R . , B e c k er , W . a n d K l i m k e w i t z , M . 1 9 8 6 ). I n v e s t i g a t io n s o n t h e k e t o n e - b o d y

m e t a b o l i s m i n Biomphalaria glabrata: i n f lu e n c e o f s t a rv a t io n a n d o f in fe c t io n w i th

Schistosoma m ansoni. Journal o f Comparative P hysiology B -B ioch em ical, Systemic,

and Environmental Physiology

156 , 563-571 .

M e u l e m a n , E . A . , L y a r u u , D . M . , K h a n , M . A . , H o l z m a n n , P .J. a n d S m i n i a , T . 1 9 7 8 ).

U l t r a s t ru c tu ral c h a n g e s in b o d y w a l l o f

Schistosoma mansoni

d u r in g t r a n s fo rma t io n o f

mi ra c id iu m in to m o th e r s p o ro c y s t in s n a i l h o s t Biomphalaria pfeifferi. Zeitschriflfiir

Parasitenkunde

5 6 , 2 2 7 -2 4 2 .

M e u le ma n , E .A . , H u y e r , A .R . a n d L u u b , T.W.J . 1 9 8 4 a ). In j e c t io n o f

Lymnaea stagnalis

w i t h m i r a c i d i a o f

Trichob ilharzia oceU ata. Zeitschrififiir Para sitenkund e

7 0 , 2 7 5 -2 7 8 .

M e u le ma n , E .A . , H u y e r , A .R . a n d M o o i j , J .H . 1 9 8 4 b ). M a in te n a n c e o f th e l if e -c y c le o f


v i a t h e d u c k

Anas platyrhynchos

a n d th e p o n d s n a i l

Lymnaea

stagnalis. Netherlands Jo urnal o f Zoology 34, 414---417.

M o o r e , G . T . , K a i s e r , R . L . , L a w r e n c e , R . S . , P u t m a n , S . M . a n d K a g a n , I . G . 1 9 6 8 ).



228 P. HORAK, L. KOLAI~OV, , AN D C.M. AD EM A

Intradermal and sero logic reactions to antigens from

Schistosoma mansoni

in schisto-

some dermatit is .

American Journal o f Tropical Medicine a nd Hygiene

17, 86-91.

Morales, G.A., Helmboldt, C.E and Penner, L.R. 1971 ). Pathology of experimentally induced

schistosome dermatitis in chickens: the role o f

Ornithobilharzia canaliculata

Rudolphi,

1819) Odhner, 1912 Trem atoda: Schisto som atidae). Avian Diseases 15, 262-2 76.

Morand, S. , Manning, S.D. and Woolhouse, M.E.J. 1996). Par asite-ho st coevolution and

geograph ic patterns of parasite infectivity and host susceptibil i ty. Proceedings of the

Royal Society o f London Series B - Biological Sciences

263, 119-128.

Moravcov~, J. and K ol~ov~i, L. 2001).


development in the lungs of

a non specific host.

Helminthologia

38, 170.

Mo reau , R.E. 1972). The Palaearctic-African B ird Migration Systems. London: Academic

Press.

MiJller, V. and Kim mi g, E 1994).

Trichobilharzia franki

n. sp. - die Ursache ftir

Bad ederm atitiden in siadwestdeutschen Bagg erseen.

Applied Parasitology

35, 12-31.

Miil ler, V., Kim mig , E and Frank, W. 1993). Die Wir kun g von Praziqua ntel auf

Trichobilharzia Digenea, Schistosomatidae), einen Verursacher von Badedermatit is

beim M enschen.

Applied Parasitology

34,187-201.

Naegel i , O. 1923). U ber e inen beim Baden entsehenden Hantausschlag, die sog.

Hundsblattern.

Exanthema caniculare). Schweizerische Medizinische Wochenschrift

49 1221-1122.

Narain, K., Mahanta, R., Dutta, R. and Dutta, E 1994): Padd y field derm atitis in Assa m: a

cercarial dermatitis.

Journal of Communicable Diseases

26, 26-30.

Nassi , H. 1987). Sur quatre furcocercaires 6mises par


en

Guadeloupe.

Annales de Parasitologie Humaine et Compar~e

62, 17-35.

Neuhaus , W. 1952a). Biologie und Entwicklung yon


n. sp.

Trematoda, Schis tosomat idae) , e inem Erreger von Dermat i t i s beim Menschen.

Zeitschrift fiir Parasitenkunde

15, 203-266.

Neuhaus, W. 1952b). De r Einfluf5 des Zwisc henw irtes auf die Gest alt der Cercarie von


Neuhaus , 195 1 und ihre sys temat ische Kennzeichnung.

Zoologischer Anzeiger

148, 275-285.

Nevhu talu, EA., S alafsky, B., Haas, W. and Conway, T. 1993). Schistosoma mansoni and


comparison of secreted cercar ia l e icosanoids .

Journal of


Niew iado msk a, K., Valtonen, E.T. and Sidd all, R. 1997). C ercar iae from

Lymnaea stagnalis

in lake Kuuhankavesi central Finland).

Acta Parasitologica

42, 132-137.

Nob ile, L. , Fioravanti , M.L., Pampiglione, S. , Calderan, M. and Marchese, G. 1996).

Report of

Gigantobilharzia acotylea

Digenea: S chistosomatidae) in si lver gulls

Larus

argentatus)

of the Venice Lagoon: co nsiderations on i ts possible etiological role in the

human dermatit is observed in the same area. Parassitologia 38, 267.

Nufiez, P.E. and de Jong-Brink, M. 1997). The suppressive excreto ry-secreto ry product of


a p ossible factor for d etermining compatibil i ty in p arasite-host

interactions. Parasitology

115, 193-203.

Nufiez, EE., Adem a, C.M. and de Jong-Brink , M. 1994). M odulatio n of the bacterial clear-

ance activity of haemocytes from the freshwater mollusc,

Lymnaea stagnalis,

by the

avian schistosome,

Trichobilharzia ocellata. Parasitology

109, 299-310.

Nufiez, EE., M olenaar, M.J. , Lagew eg, W., Li, K.W. and de Jong-B rink, M. 1997).

Excretory-secretory products o f


and their m odulating effects on

the internal defence system

ofLymnaea stagnalis. Parasitology

114, 135-144.

Oda, T. 1973). Schistos ome dermatitis in Japan. In:

Progress in Medical Parasitology in

Japan

K. Morish ita, Y. Ko miy a and H. M atsubay ashi, eds). Vol. 2, pp. 5 -53 . Tokyo:

Megu ro Parasitological Museum.




Odening, K. (1996) . What Cercaria o cellata actual ly is . Acta Parasitologica Turcica 2 0

(Suppl. 1) , 38 7-3 97 .

Olivier , L. (1949). Sch istoso m e dermatit is , a sensit izat ion ph eno m eno n. American Journal

of H ygiene 49 , 290-302 .

Ol ivier , L . (1953) . O bservations on the migrat ions of avian schis tosom es in mam m als pre-

viously unex posed to cercariae . Journal o f Parasitology 39 , 237-243 .

Olivier, L. and W einstein, P. (1953). Ex perimental schistosome derma titis in rabbits. Journal

o f Parasitology 39, 1-12.

Ow -Yang, C.K. , Lie, K.J. and K wo , E.H. (1970). Th e interspecif ic com peti t ion betwe en

Trichobilharzia brevis and Echinostoma audyi in the snail intermediate host. Southeast

Asian Jou rnal o f Tropical Med icine a nd Public Health 1, 160-161.

Palmer, D. and Ossent , E (1984). Nasal schistosomiasis in mute swan in Switzerland.

Revue Suisse de Zoologie 91 , 709-715 .

Pechenik, J .A. , Fried, B. and Simpkins, H.L. (2001).

Crepidula forn icata

is not a first

intermediate ho st fo r t rematodes: w ho is? Journal o f Experimental M arine Biology and

Ecology 261 , 211-224 .

Pence, D.B. and Rhodes , M.J . (1982) . Trichobilharzia physellae (Digenea :

Schis tosom at idae) f rom endem ic water fowl on the Hig h Plains of Texas . Journal of

W ildlife D iseases 18, 69-74.

Perrett, S. and Whitfield, EJ. (1996). Currently available molluscicides. Parasitology Today

12, 156-159.

P i ca rd , D . and Jousso n , O . (2001) . Gen e t i c va r i ab il it y am ong c e rca r i ae o f t he

Schis tosom at idae (Trematoda: Digen ea) causing sw imm er s itch in Europe. Parasite 8,

2 3 7 - 2 4 2 .

Pilz, J. , Eisele, S. an d Disko, R . (1995). Zerkarienderm atitis (sw im m er s itch). Fallbericht

einer Zerkariendermati tis du rch Trichobilharzia (Digenea, Schistosomatidae). Hautarzt

46 , 335-338 .

Platt, T.R., Blair, D., Purdie, J. and Melville, L. (1991). Griphobilharzia amoena n. sp.

(Digenea: Schistosomatidae), a parasite o f the freshwater croco dile Crocodylus ohnstoni

(Rept i l i a : Crocodyl i a ) f rom Aus t r a l i a , w i th t he e r ec t i on of a new subfami ly ,

Griphobilharziinae. Journal o f Parasitology 77, 65--68.

Rai , S.L. and Cleg g, J .A. (1968). Dea th of schisto som e cercariae durin g penetrat ion o f the

skin. I . Penet ra t ion o f the bi rd skin by Austrobilharzia terrigalensis. Parasitology 58,

199-214 .

Raisyte, D. (1974). [O n Schistosomatidae cercariae of the Nem an delta (preliminary data). ]

Ac ta Parasitologica Lithuanica 12, 125-129. ( in Russian)

Ramaswamy, K. , Salafsky, B. , Potluri , S. , He, Y.-X. , Li , J . -W. and Shibuya, T. (1996).

Secre ti on of an an t i -i n f lamm atory f ac to r by sch i stosomulae o f Schistosoma mansoni.

Journal o f lnflamm ation 46, 13-22.

Ran, M.E . , Bo urns , T.K.R. and Ellis , J.C. (1975). Eg g pro du ction by Trichobilharzia ocel-

lata (T rematoda : Sch i s tosomat idae ) a f t e r i n i t i a l and cha l l enge in fec t ion i n ducks .

Canadian Journal o f Zoology 53 , 642-650 .

Reim ink, R.L. , De G oed e, J .A. and Blankespoor, H .D. (1995). Effic acy o f praziquantel in

na tura l popula t i ons o f ma l l a rds i n fec t ed wi th av i an sch i s tosomes . Journal of


Richard, J. (1971). La ch6totaxie d es cercaires. Valeur syst6matique et phyl6tique.

Mdmoires

du Mu seum National d Histoire Naturelle, S~rie A, Zoologie 67, 1-179.

Richards , E .H. and Ren wrantz , L .R. (1991). T wo lectins o n the sur face of He lix pomatia

hem ocy tes: a Ca2+-dependent , GalNAc-specific lectin an d a Ca2+-independent, man no se

6--phosphate-specif ic lectin whic h reco gn izes act ivated hom olo go us ops onin s. Journal

o f Com parative Physiology B - Biochemical, Systemic, and Environmental Physiology



2 3 0 P. H O R A K L . K O L A R O V A A N D C . M . A D E M A

161 , 43-54 .

Richards , C .S . , Knigh t , M. and Lewis , EA . 1992) . Gene t ics

ofBiomphalaria glabrata and its

e f fe ct o n th e o u tc o me o f

Schistosoma mansoni

infection.

Parasitology Today

8 , 171-174 .

Roder , J .C . , Bourn s , T .K.R. and S ingha l , S .K. 1977) .


c e rc a r i a e

ma s k e d b y a n t ig e n s o f th e s n a i l ,

Lymnaea stagnalis. Experimental Parasitology

41 ,

2 0 6 - 2 1 2 .

Rudolfovf i, J . , S i tko , J . and H o r n , E in p ress ) . Nasa l sch is tosom es in wi ld fow l in the Czech

R e p u b l i c . Parasitology Research.

R u s s o , J. a n d L a g a d ic , L . 2 0 0 0 ) . E f fe c ts o f p a ra s i t is m a n d p e s t i c id e e x p o s u re o n c h a ra c -

te r is t ic s and func t ions o f hem ocyte popula t ions in the f reshw ate r sna i l Lymna ea palustris

G a s t ro p o d a , P u lm o n a ta ) .

Cell Biology a nd Toxicology

16, 15-30.

S a b h a , G .H . a n d M a le k , E .A . 1 97 9) . D e rm a t i t is c a u s e d b y c e rc a ri a e o f Orientobilharzia

turkestanicum

i n th e C a s p ia n a re a o f I r a n .

American Journal of Tropical Medicine a nd

Hygiene

2 8 , 9 1 2 -9 1 3 .

Sa la fsky , B . , Ram aswam y, K. , He , Y.-X. , L i , J. and Sh ibua , T . 1999) . De ve lop m ent and

e v a l u a t i o n o f l i p o d e e t , a n e w l o n g - a c t i n g f o r m u l a t i o n o f

N,N-diethyl-m-toluamide

D E E T ) fo r th e p re v e n t io n o f s c h i s to s o mia s i s .

American Journal o f Tropical Med icine

and H ygiene 6 1 , 7 4 3 -7 5 0 .

Sa la fsky , B . , He , Y-X. , L i , J -T . and Sh ibu a , R . 2001) . Top ica l app l ica t ion o f a long-ac t in g ,

s a fe fo rmu la t io n o f

N,N-diethyl-m-toluamide

D E E T ) to p re v e n t c e rc a r i a l p e n e t ra t io n

th rough the sk in . Helminthologia 38, 246.

Sam uelson, J .C. and Stein , L.D. 1989). Schistosoma man soni: increasing saline concentra tion

s igna ls ce rca r iae to t rans form to sch is tosomula . Experimental Pa rasitology 69 , 23-29 .

S a p p , K .K . a n d L o k e r , E .S . 2 0 0 0 ). A c o mp a ra t iv e s tu d y o f me c h a n i s ms u n d e r ly in g d ig e -

n e a n -s n a i l s p e c i f i c i ty :

in vitro

i n t e ra c t io n s b e tw e e n h e mo c y te s a n d d ig e n e a n l a rv a e .


86 , 1020-1029 .

Scha l l ig , H.D .EH . , Schu t , A. , van de r Kna ap , W.P .W. and de Jong-Brink , M. 1990) . A s im -

p l i f i e d m e d i u m f o r t h e

in vitro

c u l t u r e o f m o t h e r s p o r o c y s t s o f t h e s c h i s t o s o m e

Trichobilharzia ocellata. Parasitology Research 7 6 , 2 7 8 -2 7 9 .

S c h a l l i g , H . D . E H . , S a s s e n , M . J .M . , H o r d i j k , P .L . a n d d e J o n g - B r i n k , M . 1 9 9 1 ).

Trichobilharzia ocellata: i n f lu e n c e o f in fe c t io n o n th e f e c u n d i ty o f i t s i n t e rme d ia te s n a i l

h o s t

Lymnaea stagnalis

a n d c e rc a r i a l i n d u c t io n o f th e r e l e a s e o f s c h i s to s o min , a s n a i l

n e u ro p e p t id e a n ta g o n iz in g f e ma le g o n a d o t ro p ic h o rmo n e . Parasitology 102 , 85-91 .

S c h a l l ig , H .D .E H . , S a s s e n , M.J .M. a n d d e J o n g -B r in k , M. 1 99 2) .

In vitro

r e l e a s e o f th e

a n t i -g o n a d o t ro p ic h o rmo n e , s c h i s to s o min , f ro m th e c e n t ra l n e rv o u s s y s te m o f Lymnaea

stagnalis i s i n d u c e d w i th a me th a n o l i c e x t ra c t o f c e rc a r i a e o f Trichobilharzia ocellata.

Parasitology

104 , 309-314 .

Sch m aschke , R., Ribb eck , R., Eulen berger, K., SchiJppel, K.- E and Schfitze, B. 1992). Eine

d u r c h

Trichobilharzia

s p . T r e m a t o d a : S c h i s t o s o m a t i d a e ) v e r u r s a c h te p r o l i f e r a t i v e

Ko njun ktivit is bei Hawaiig~insen

Branta sandvicensis)

im Z o o lo g i s c h e n G a r te n L e ip z ig .

In: Verhandlungsbericht des 34. lnternationalen Sympo siums iiber die Erkrankungen de r

Zoo- und Wildtiere, Santander/Spanien. p p . 3 5 5 -3 5 9 , B e r l in : A k a d e m ie V e r l a g .

S c h m id t , O . , F a y e , I. , L in d s t ro m-D in n e tz , I . a n d S u n , S .C . 1 9 9 3 ). S p e c i f i c imm u n e re c o g -

n i t io n o f in s e c t h e m o l in . Developmental and Comparative Immunology 17 , 195-200 .

S c r img e o u r , E .M. a n d G a jd u s e k , D .C . 1 98 5) . In v o lv e me n t o f th e c e n tra l n e rv o u s s y s te m in

Schistosoma mansoni and Schistosoma haematobium

in fec t ion .

Brain

108 , 1023-1038 .

Sh if t , C .J. and G raczy k , T .K. 1994) . A chem okine t ic response in

Schistosoma mansoni

cer-

ca r iae . Journal o f Parasitology 8 0 , 8 7 9 -8 8 3 .

Sh if t , C .J . , Chan diwa na , S .K . , G raczy k , T .K. , Chib a tam oto , P . and Brad ley , M . 1993) . A

t ra p fo r th e d e te c t io n o f s c h i s to s o me c e rc a r ia e .


79 , 149-154 .

S h o r t , R .B . a n d Me n z e l , M.Y . 1 9 6 0 ) . C h ro m o s o m e s o f n in e s p e c ie s o f s c h i sto s o me s .




Journ al o f Parasitology 46, 273-287.

Simon-Martin, E and Simon-Vicente, E (1999). The life cyc le o f Trichobilharzia salman

ticensis n. sp. (Digenea: Schistosomatidae), related to cases of human dermatitis.

Research and Review s in Parasitology 59, 13-18.

Simon-Vicente, E (1983). Dermatitis de los banistas en ecosistemas acufiticos de

Salamanca. Revista Ibdrica de Parasitologfa 43, 423--424.

Singh, K. and Singh, D.K. (2000). Toxicity to the snail Limnaea acuminata o f plant-derived

molluscicides in combination with synergists. Pest Management Science 56, 889-898.

Skrjabin, KT and Zakharov, N.P. (1920). [Zwei neue Trematodengattungen aus den

Blutgef~issen der V6gel. (Beitrag zur Kenntnis der Helminthenfauna der V6gel

Russlands).] Izvestnik Donskovo Veterinarnovo lnstituta 2, 1--6. (in Russian)

Sluiters, J.E (1981). De velopm ent of Trichobilharzia ocellata in Lym naea stagnalis and the

effects of infection on the reproductive sys tem of the host. Zeitschrififiir Parasitenkunde

64, 303-319.

Sluiters, J.E (1983). O bservations on the identity of the avian schistoso me Trichobilharzia

ocellata (La Valette, 1855) Brumpt, 1931. Acta Leidensia 51, 53--60.

Sluiters, J .E, Brussaard-Wust, C.M. and Meu leman, E.A. (1980). Th e relationship betwe en

miracidial dose, produ ction of cercariae, and reproductive activity of the host in the co m-

bination Trichobilharzia ocellata and Lymnaea stagnalis. Zeitschrifl fiir Parasitenkunde

63, 13-26.

Sm yth, J.D. (1990). Trem atoda: Digen ea with non-proge netic metacercaria. In:

In Vitro

Cultivation o f Parasitic Helminths (J.D. S myth, ed.), pp. 45-7 6. Bo ca Raton: CR C Press.

Snyder, S.D. and Loker, E.S. (2000). Evolutionary relationships among the

Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma.

Journ al o f Parasitology 86, 283-288.

Spakulov~i, M., Hor~k, P. and Krfil owi, I. (1996). Ka ryo typ e of an avian sc histo som e

Trichobilharzia szidati (Digenea: Schistosomatidae). International Journal for


Spakulovfi, M., HorLk, P. and MO iler, V. (1997). Th e ka ryo typ e of Trichobilharzia franki

Mtiller et Kim mig, 1994 (Digenea: Schistosomatidae), a new Euro pean schistoso me

agent of swim mers itch. Parasite 4, 63-66.

Spakulovfi, M., HorLk, P. and D vo~tk, J. (2001). Th e kary oty pe of Trichobilharzia regenti

Hor(tk, Kol~i~ov~et Dvofiik, 1998 (Dig enea : Schistosomatidae), a nasal avian schi sto-

some in Central Europe. Parasitology Research 87, 479--483.

Ssinitzin, D.T. (1910). Studien tiber die Phylo gen ie der Trematoden. 2. Bucephalus v. Baer

und Cercaria ocellata De la Val. Zeitschr iflfiir Wissenschaftliche Zoolog ie 94, 299-325.

Sturrock, R. E (1993). The intermediate hosts and hos t-para site relationship. In: Human

Schistosomiasis (P. Jordan, G . Web be and R. E Sturrock, eds), pp. 33 -85 . Wallingford:

CAB International.

Suzuk i, N. and Kawanaka, M. (1980).


Basch, 1966, as a cause of an

outbre ak o f cercarial dermatitis in Japan. Japa nese Jou rnal o f Parasitology 29, 1-10.

Szidat, L. (1938). Pseudobilharziella filiformis n. sp., eine neue Vrgelbilharzie aus dem

Hrckerschwan Cygnu s ol or L. Zeitschrifl fi ir Parasitenkunde 10, 535-544.

Szidat, L. (1942). Was ist Cercaria ocellata La Valette? Mo rpho logisc he und entwicklungs-

geschichtliche Un tersuchu nge n tiber den Erreger de r europ~ischen Cercarien-Dermatitis

des Menschen. De utsc he etropenmedizinische Zeitschrifi 46, 482-497,509-524.

Szidat, L. and Wigand, R. (1934). Leitfaden der Einheimischen Wurmkrankkheiten des

Menschen. Leip zig: G. Thie me Verlag.

Tanabe, H. (1948). [On the cause of Kogan byo .] Yonago lgaku Zasshi 1, 2- 3. (in Japanese)

Taylor, E.L. an d Baylis, H.A . (1930). Observ ations an d experiments on a dermatitis-pro-

ducing cercaria and on another cercaria from Limnaea stagnalis in Great Britain.



232 P. HORAK L. KOLAROVA AND C.M . ADEM A

Tr an s ac ti on s o f t h e Ro y a l S o c i e t y o f Tr o pi ca l M e d i c i n e a n d Hy g i e n e 2 4 , 2 1 9 -2 4 4 .

T h 6 ro n , A . (19 86 ). C e rc a r io m e t ry a n d th e e p id e m io lo g y o f s c h i s to s o mia s i s.

Paras i to logy

Today 2 , 6 1 -6 3 .

T h o m p s o n , S .N . (19 97 ). P h y s io lo g y an d b io c h e m is t ry o f s n a i l - l a rv a l t r e ma to d e r e l a t io n -

ships . In:

Advances in Trematode Bio logy

(B. Fr ied and T .K. Graczyk , eds ) , pp . 149-195 .

B o c a R a to n : C R C P re s s .

T h o rs , C . a n d L in d e r , E . (20 01 ). S w im m e r s i tc h in S w e d e n .

He l mi n t h o l o g i a

38, 244.

T h u n e , P . (19 94 ). [C e rc a r i a l d e rm a t i t i s o r s w imm e r s i t c h - a l i t t le k n o w n b u t f r e q u e n t ly

o c c u r r i n g d i s e a s e i n N o r w a y . ] T i d s s k ri ft f o r d e n N o r s k e L c e g e f o re n f o rm i n g 114 ,

1 6 9 4 -1 6 9 5 . ( in N o rw e g ia n )

Tie lens , A.G .M . , van de Pas , EA .M . , van den H euve l , J.M. an d van den Bergh , S .G . (1991) .

T h e a e r o b i c e n e r g y m e t a b o l i s m o f S c h i s t o s o m a m a n s o n i m i r a c i d i a . M o l e c u l a r a n d

Bi o c h e m i c a l Pa r a s i to l o g y

46 , 181-184 .

T ie le n s , A .G .M. , H o re m a n s , A .M .C . , D u n n e w i jk , R . , v a n d e r M e e r , P. a n d v a n d e n B e rg h ,

S .G . (1 9 9 2 ) . T h e f a c u l t a t iv e a n a e ro b ic e n e rg y me ta b o l i s m o f

S c h i s t o s o m a m a n s o n i

sporocys ts .

M o l e c u l a r a n d B i o c h e m i c a l P a r a s it o lo g y

5 6 , 4 9 -5 8 .

T s y rk u n o v , L .P . (1 9 8 7 ) . [S c h i s to s o me d e rma t i t i s . ]

M e d i t s i n s k a j a P a r a z i t o l o g i y a i

Pa r a z i t a r n y e Bo l e z n i (2 ) , 7 3 -7 6 . ( in R u s s ia n )

v a n d e R o e m e r , A . a n d H a a s , W . (1 98 4 ) . F in e s t ru ctu re o f a l e n s -c o v e re d p h o to re c e p to r in

th e c e rc a r i a o f

Trichobilharzia ocel la ta . Ze i tsc hr i f t f i i r Pa rasi ten kun de

7 0 , 3 9 1 -3 9 4 .

v a n d e n B ro e k , E . (1 96 5) . S o m e re c e n t c a s e s o f a v ia n s c h i s to s o mia s i s a n d s c h i s to s o me d e r -

ma t i t i s i n th e N e th e r l a n d s . Tr op ic a l a n d G e o g r a p h i c a l Me d i c i n e 17 , 229-235 .

v a n d e r K n a a p , W.P .W a n d L o k e r , E .S . (1 99 0) . Imm u n e -m e c h a n i s m s in t r e ma to d e s n a il

in te rac t ions .

Paras i to logy Today

6 , 175-182 .

van de r Knaap , W.P .W. , Dodere r , A. , Boerr ig te r -Barendsen , L .H. and Smin ia , T . (1982) .

S o m e p ro p e r t i e s o f a n a g g lu t in in in th e h e m o ly mp h o f th e p o n d s n a i l Lym naea s tagna li s.

Bio log ica l Bu l l e t in 162 , 404-412 .

van de r K naap , W.P .W. , Sm in ia , T ., Schu t te , R . and B oerr ig te r -B arendse n , L .H. (1983) .

C y to p h i l i c r e c e p to r s fo r fo re ig n n e s s a n d s o me fa c to r s w h ic h in f lu e n c e p h a g o c y to s i s b y

inver tebra te leukocy tes :

in vitro

p h a g o c y to s i s b y a me b o c y te s o f th e s n a i l

Ly mn a e a s t a g -

na l i s . Immuno logy

4 8 , 3 7 7 -3 8 3 .

van de r Knaap , W.P .W. , Boo ts , A.M .H. , M eulem an , E .A. an d Sm in ia , T . (1985) . Sea rch fo r

s h a re d a n t ig e n s in th e s c h i s to s o m e -s n a i l c o mb in a t io n Tr ichob i lharz ia oce l la ta -Lymnaea

s tagna li s. Ze i t schr i f t f i i r P aras i t enkunde

7 1 , 2 1 9 -2 2 6 .

V/ iy rynen , T . , S idda l l , R . , Va l tonen , E .T . an d Task inen , J . (2000) . Pa t te rns o f t rem atode pa r-

a s i t is m in ly m n a e id s n a i l s f ro m n o r th ern a n d c e n t ra l F in la n d .

An n a l e s Zo o l o g i c i Fe n n i c i

37 , 189-199 .

V o g e l , H . (1 9 3 0 a ) . C e r c a r i e n -D e rm a t i t i s i n D e u t s c h la n d .

Kl i n i s c h e Wo c h e n s c h r i f t 9

8 8 3 -8 8 6 .

V o g e l , H . (1 9 3 0 b ) . H a u tv e r~ in d e ru n g e n d u rc h

C e r c a r i a o c e l l a t a . D e r m a t o l o g i s c h e

Wochenschr i f l

9 0 , 5 7 7 -5 8 1 .

V o g e l, H . a n d M i n n i n g , W . ( 1 9 4 9 a ). H i i l l e n b i l d u n g b e i B i l h a r z i a - C e r c a r i e n in S e r u m

B i lh a rz ia - in f i z i e r t e rT ie re u n d Me n s c h e n . Ze n t ra lb la t t f i i r Bak te r io log ie M ikrob io log ie

u n d H y g i e n e I . Ab t . Or i g i n a l e B 153 , 91-105 .

V o g e l , H . a n d Min n in g , W. (1 9 4 9 b ) . We i t e re B e o b a c h tu n g e n f ib e r d i e C e rc a r i e n h i i l l e n -

r e a k t io n , e i n e S e r o p r~ i z ip i ta t io n m i t l e b e n d e n B i l h a r z i a - C e r c a r i e n .

Ze i t s c h r i f l f i i r

Tropenmed iz in und Paras i to log ie

1 , 3 7 8 - 3 8 6 .

v o n L ic h te n b e rg , F. a n d R i t c h ie , L .S . (1 9 6 1 ). C e l lu la r r e s i st a n c e a g a in s t s c h i s to s o mu la o f

S c h i s t o s o m a m a n s o n i

in

M a c a c a m u l a t t a

m o n k e y s f o l l o w i n g p r o l o n g e d i n f e ct i o n s.

Am e r i c a n J o u r n a l o f Tr o pic a l Me d i c i n e a n d Hy g i e n e 10 , 859-869 .

W e b b e , G . ( 1 9 8 2 ). T h e i n t e r m e d i a t e h o s t a n d h o s t - p a r a s i t e r e l a ti o n s h i p s . In :



BIOLOGY OF

TRICHOBILH RZI

3 3

Schistosomiasis, Epidemiology, Treatment and Control P. Jord an an d G. W ebbe, eds) ,

pp . 16 -49 . Lond on: W i ll iam H einemann M edica l Books .

Wesenberg-Lund, C. 1934). Contributions to the dev elop m ent o f the trem atod a digenea.

Par t I I : The biology of the f reshwater cercar iae in Danish f reshwaters . M~moires de

l Acad~m ie Royale d es Sciences et de s Lettres de Danem ark, Copenh ague, Section des

Sciences 3, 1-223.

Wesselingh, E E , C ad6e, G.C. and Renem a, W. 1999). F lying high: on the ai rborne dis-

persal o f aquatic orga nism s as i llustrated by the distribution histories o f the gastro po d

genera Tryonia and Planorbarius. Geologie en Mijnbouw 78 , 165-174 .

W iederm ann , G. , As p6 ck, H. , Gra efe, G. , Picher, O. and Peharn, E 1973). Hauttests m it

Schistosoma mansoni-Antigen bei F~il len von Cercar ien-Derm at i ti s . Zentralblatt fiir

Bakteriologie, M ikrobiologie und Hygiene L Abt. Originale A 224, 128-132.

W iley, R., W olfe , D., Flahart, R., Kon igsberg, C . an d Silverman P.R . 1992 ). Cercarial d er-

mati tis outbrea k at State P a r k - D elaware, 1991.

Mo rbidity a nd M ortality W eekly Report

41 , 225-228 .

W il ls , W. , Fr ied, B. , Carrol l , D .E an d Jone s , G.E. 1976 ) . Schis to som e derm at i t is in

Pennsylvania. Public Health Report 91, 469--470.

Wilson, R.B. , New, J.C. and Scholtens, R.G . 1982). Granu lom atous encephalit is cau sed by

schistosomiasis in swans. Journal o f the Am erican Veterinary M edical Association 181,

1386-1387 .

Wo jcinski , Z. W ., Barker, I . K. , Hunter , D. B. and Lum sde n, H. 1987). A n outbreak o f

schis tosomiasis in At lant ic brant geese , Branta bernicla hrota. Journal o f Wildlife

Diseases 23 , 248-255 .

W ood, L .M. and Bach a, W.J .J r. 1983). Dis tr ibution o f eggs and the host response in chick-

ens infected wi th

Austrobilharzia variglandis

Trematoda).


69,

6 8 2 - 6 8 8 .

W ood ruff , D.S. an d Mulvey, M. 1997). Neo tropica l schistosomiasis: A frican aff ini ties of

the snai l host Biomphalaria glabrata Gastropoda: Planorbidae). Biological Journal of

the Linnean Society 60 , 505-516 .

W u, L .-Y. 1953). A s tudy o f the li fe his tory of Trichobilharzia cam eroni sp. nov. Fam ily

Schistosomatidae). Canadian Journal o f Zoology 31 , 351-373 .

Xia , M.Y. and Jourdane, J . 1991). P enet ra t ion and m igrat ion routes of Schistosomajapon-

icum m iracidia in the snai l Oncomelania hupensis. Parasitology 1113, 77- 83 .

Xu, Y .Z . and Dresden , M.H. 1990) . T he ha t ch ing of sch is tosome eggs . Experimental

Parasitology 70 , 236 -240 .

Yamagut i, S . 1941). [S tudies on the helminth fauna of Japan. P ar t 32. Trem atodes o f

birds.] Japanese Journal of Zoology 9, 32 1-34 1. in Japanese)

Yamaguti, S. 1971). Synopsis of Digenetic Trematodes of Vertebrates. Tokyo: Ke igaku

Publ i shing Co.

Yoshino, T . E and Bosw el l , C. A. 1986). A nt igen shar ing between larval t rematodes an d

t h e i r s n a i l h o s t s : h o w r e a l a p h e n o m e n o n i n i m m u n e e v a s i o n ? Symposium o f the

Zoological S ociety of London 56 , 221-238 .

Zh ang , S.-M., L6onard, EM ., A dem a, C.M. and Loker, E.S. 2001). Parasi te resp onsiv e

IgS F mem bers in the snail Biomphalaria glabrata: characterizat ion o f nov el gen es with

t a n d e m l y a r r a n g e d I g S F d o m a i n s a n d a f i b r i n o g e n d o m a i n , lmmunogene t i c s 53,

6 8 4 - 6 9 4 .



The Consequences of Reducing Transmission of

l asm od i um fa lc i p ar um in frica

R o b e r t W . S n o w 1 2 a n d K e v i n M a r s h ~ 3

1Centre o r Tropical Medicine University o f Oxford John Radcliffe

Hospital Headington Oxford OX3 9D U UK

2The Wellcom e Trust~Kenya Medical Research Institute Collaborative

Programme P.O. Box 43640 Nairobi Kenya

3Centre fo r Geographic Medicine Kenya Medical Research Institute

P. O. Box 230 Kilifi Kenya

A b s tr a ct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 35

1. I n tr o d uc t io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 36

2. The Age Pa t te rns o f Seve re Ma la r i a M orb id i t y : D eve lop ing Func t i ona l

I m m u n i t y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 38

3. T h e E ff ec ts o f A g e o n t h e R is k o f D i se a se O u t c o m e s . . . . . . . . . . . . . . . . . . . . . . 2 40

4. Ra tes o f Paed ia tr i c Ma la r i a M orb id i t y ac ross t he Va r ied T ransm iss ion

S e t ti n gs o f A f ri ca . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

5. The R isks o f Mo r ta l i t y du r ing C h i l dhoo d w i t h I nc reas ing I n tens i t y o f

M a l ar ia T r a n sm i s s io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 43

6. L i m it a ti o ns o f t h e x - A x is . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 45

7 . Re -exa m in ing t he Mor ta l i t y and Transm iss ion I n tens i t y Ev idence . . . . . . . . . . . 247

8. R econc i l ing the R o le o f D i rec t and Ind i rec t Ef fec ts o f P. f lcip rum on

Ch i ld Su rv i va l w i t h t he Sa tu ra t i on o f A l l -Cause Mor ta l i t y w i t h

I nc re a si ng T r a ns m i s si o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 50

9 . I n se c ti c id e - Tr e a te d B e d N e ts i n A f r ic a . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251

10 . Wh o Wi l l Bene f i t Mos t f r om Reduc t i ons i n Pa rasi te Exposu re? . . . . . . . . . . . . . 255

11. C o n c lu s i on s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 56

A c k n o w l e d g e m e n ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257

R e fe re n ce s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 58

BSTR CT

Ma la r i a t r ans mis s ion in tens i ty in Af r i ca va r i e s ove r s eve ra l log o rde rs f ro m

les s than one in f ec ted b i t e pe r yea r to more than one thous and . In thi s rev iew

A D V A N C E S I N P A R A S I T O L O G Y V O L 5 2

Copyright ©

2002 Elsevier Science Ltd

0 0 6 5 3 0 8 X

ll rights of reproduction in any form reserved



236 R W SNOW AND K MARSH

w e e x a m i n e t h e c o n s e q u e n c e s i n t e r m s o f a g e p a t t e r n , c l i n i c a l s p e c t r u m a n d

overa l l bu rde n o f d i s ease and d i s cus s t he pos s ib l e imp l i ca t i ons fo r i n t e rven t i ons

tha t r educe e xposu re t o i n fec t ed b i te s . W i th ve ry l ow t r an sm i s s ion i n tens i ty , al l

age g rou ps a re suscep t i b l e to s evere m al a r ia . W i th i nc reas ing t r ansm i s s ion in t en -

s i ti e s, o l d e r c h i l d r e n a n d a d u l t s s u f f e r l e s s s e v e r e d i s e a s e a n d w i t h h i g h

t r a n s m i s s io n r a te s t h e m a j o r i t y o f s e v e re c a s e s o c c u r i n i n f a n ts u n d e r o n e y e a r o f

age . Th i s pa t t e rn r e f l ec t s t he i nc reas ing ly r ap id acqu i s i t ion o f im m un e responses

tha t l im i t t he f i f e - t h rea t en ing e f fec t s o f ma l a r i a w i th i nc reas ing exp osu re t o t he

paras i te . The c l i n i ca l spec t rum o f s evere mal a r i a va ri e s wi th t r ansmi s s ion : wi th

h i g h t r a n s m i s s io n , s e v e r e m a l a r i a l a n a e m i a d o m i n a t e s a n d c e r e b ra l m a l a r i a i s

r a re . A s o n e m o v e s t o w a r d s l o w e r t ra n s m i s s io n r a te s , c e re b r a l m a l a r i a a c c o u n t s

f o r a n i n c r e a s i n g l y l a rg e p r o p o r t i o n o f c a s es . A l t h o u g h t h e p o p u l a t i o n r i sk o f

severe d i s ease f a ll s w i th age , t he r i sk o f de a th a t an i nd iv idua l l eve l m ay r i s e wi th

a g e a f t e r a n i n i t ia l f a ll f r o m v e r y h i g h c a s e f a t a li ty ra t e s i n c h i l d r e n a g e d u n d e r

6 m o n t h s . O f c e n t r a l i n te r e s t t o m a l a r ia c o n t r o l is h o w t h e o v e r a ll a m o u n t o f d i s-

e a s e i n c h i l d h o o d v a r i e s w i t h t r a n s m i s s i o n . D a t a f r o m a n u m b e r o f s o u r c e s

s u g g e s t th a t , w i t h l o w t r a n s m i s s i o n , th e a m o u n t o f m a l a r ia l d i s e a s e r is e s w i t h

inc reas ing exp osu re bu t t ha t t h is s a tu ra t es r e la t i ve ly ea r ly . A key i s sue i s wh e the r

t h e s a m e p a t t e r n o b t a i n s f o r d e a th s , b o t h t h o s e d i r e c t ly d u e t o m a l a r i a a n d t h o s e

f r o m a l l c a u s e s . T h e m e t h o d o l o g i c a l l i m i t a t i o n s o f e c o l o g i c a l c o m p a r i s o n s

b e t w e e n d i f f e r e n t a r e a s a r e d i s c u s s e d b e f o r e p r e s e n t i n g a r e v i e w o f a t t e m p t s t o

use t h i s app roach i n Af r i ca . Th i s sugges t s t ha t ch i l d ren l i v ing i n a reas o f l ow

m a l a r i a l e n d e m i c i ty h a v e a l l- c a u s e m o r t a l i t y r a te s a b o u t h a l f o f t h o s e o f c h i ld r e n

l iv i n g i n a r e a s o f m o d e r a t e t o h i g h t r a n s m i s s io n . D e a t h s i n t h e f ir s t y e a r o f l if e

r i se l i n e a r l y w i t h i n c r e a s in g e x p o s u r e t o m a l a r i a o v e r a w i d e r a n g e o f t r a n s m i s -

s i o n in t e n s it ie s ; b y c o n t r a s t a l l- c a u s e m o r t a l it y in c h i l d r e n a g e d 0 - 4 y e a r s

appear s t o s a tu ra t e a t r e l a t i ve ly l ow t r ansm i s s ion i n tens i t ie s . Th ese da t a su gges t

t ha t in t e rven t i ons t ha t r edu ce ex posu re t o m a l a r i a pa ras it e s , such as i n sec t i c i de -

t r e a te d b e d n e t s I T N s ) , w i l l h a v e t h e g r e a t e s t c h a n c e o f a s u s ta i n e d e f fe c t w h e n

u s e d i n a r e a s w h e r e d i s e a s e b u r d e n s a r e h i g h b u t t h e f r e q u e n c y o f p a ra s i te e x p o -

su re i s l ow- to -m odera t e . In co nd i t i ons o f h igh t r ansm i s s ion , in i t ia l r educ t i ons i n

m o r t a l it y m a y p r o v e d i f f ic u l t t o s u s t a i n a s t h e r e d u c e d l e ve l o f t r a n s m i s s i o n

m ay s t il l l ie on t he pa r t o f the cu rv e wh ere m or t a l i t y has s a tu ra ted . How ever , a t

a l l le v e ls o f t r a n s m i s s i o n t h e o v e r a l l b a l a n c e o f b e n e f i ts , i n c l u d i n g r e d u c e d l o a d

o n f a m i l i e s a n d h e a l t h s e r v ic e s f r o m n o n - l i f e - th r e a t e n i n g m a l a ri a , f a v o u r s t h e

w i d e s p r e a d i n t r o d u c t io n o f I T N s i n e n d e m i c a r e a s o f A f r i c a .


O v e r t h e l a s t d e c a d e t h e r e h a s b e e n a b r o a d e n i n g o f th e e p i d e m i o l o g i c a l

a p p r o a c h e s t o m a l a r ia , f r o m a n e m p h a s i s o n v e c t o r - p a r a s i te d y n a m i c s to a n



TRANSMISSION OF

P L S M O D I U M F L C lP R U M

IN AFRICA 37

approach tha t i s beg inn ing to cap tu re the impac t on morb id i ty and mor ta l i ty .

Co inc iden ta l ly , s evera l con ten t iou s i s sues have r e -em erged f ro m a deba te tha t

b e g a n o v e r 5 0 y e a r s a g o . T h e s e d e b a t e s h a v e s w u n g b e t w e e n e m o t i v e c l a i m s

t o i n f o r m e d o p i n i o n b a s e d u p o n l i m i t e d e v i d e n c e . T h e d e b a t e c e n t r e s o n

w h e t h e r r e d u c i n g t h e r is k o f i n f e c ti o n w i t h

P l a s m o d i u m f a l c i p a r u m

wil l

a lwa ys l ead to reduc t ion in the l i f e - time r i sks o f dea th f rom mala r ia .

A charac te ri s ti c o f ma la r i a in m os t pa r ts o f sub -Saharan Af r i ca i s tha t in fec -

t ion w i th P .

f a l c i p a r u m

i s c o m m o n a n d t h a t d e a t h f r o m m a l a r i a , w h i l s t

num er ica l ly cons ide rab le , i s r e l a t ive ly r a re com pared to the l if e - t im e r isk and

f r e q u e n c y o f i n f e c ti o n . M o s t s e v e r e o u t c o m e s a n d d e a t h f o l l o w i n g i n fe c t io n

occur in ch i ld ren . I t has the re fo re been w ide ly he ld tha t the acqu i s i t ion o f

i m m u n i t y d u r i n g c h i l d h o o d i s an i m p o r t a n t s u r v iv a l m e c h a n i s m f o r p o p u l a -

t ions l iv ing under cond i t ions o f s t ab le , endemic mala r i a t r ansmis s ion . The

cos t , in t e rms o f ch i ld m or tal i ty , i s h igh , su f f i c i en t ly h igh to hav e s e lec ted fo r

s e v e ra l in n a t e s u r v i va l m e c h a n i s m s s u c h a s t h e g e n e t i c p o l y m o r p h i s m s a s s o -

c ia ted w i th r ed b loo d ce l l s t ruc tu re and func t ion (H i l l, 1992).

I n t e rf e r in g w i t h n a t u r e s b a l a n c e u n d e r s ta b l e , e n d e m i c c o n d i t io n s o f

t r a n s m i s s i o n l e d s o m e to q u e s t i o n t h e v i r t u e o f i n d o o r r e s i d u a l h o u s e - s p r a y -

i n g a s a m e a n s o f m a l a r i a c o n t r o l i n A f r i c a d u r i n g t h e o p t i m i s t i c e r a d i c a t i o n

e r a o f t h e la t e 1 9 4 0 s a n d e a r ly 1 9 5 0 s ( G a r n h a m , 1 9 4 9 ; W i l so n , 1 9 4 9 ; W H O ,

1 9 5 0 ; W i l s o n

et a l .

1 9 50 ; D o b s o n

et a l .

2 0 0 0 ) . O v e r 5 y e a r s a g o t h is d e b a t e

w a s r e o p e n e d i n th e l ig h t o f e c o l o g i c a l c o m p a r i s o n s o f m e a s u r e s o f m o r ta l -

i t y f r o m m a l a r ia a n d m e a s u r e s o f p a r a s i te c h a l l e n g e ( S n o w a n d M a r s h ,

1 9 9 5 ) . T h e r e f o l l o w e d a s e r i e s o f a n a l y s e s o f t h e s a m e a n d d i f f e r e n t d a t a

(Mo l ineaux , 1996 ; Trape and Rog ie r , 1996 ; An ony m ous , 1997 ; Bro wn , 1997;

D A l e s s a n d r o a n d C o o s e m a n s , 1 99 7 ; G r e e n w o o d , 1 99 7; L e n g e l e r e t a l .

1997 ; Trape , 1997 ; Smi th , T .A . et a l . 2 0 0 1 ) . I n t e rp r e t a ti o n s o f t h e s e c o m -

p a r a t i v e s t u d i e s c a n b e b r o a d l y d i v i d e d i n t o t h o s e w h i c h c o n c l u d e d t h a t

m a l a r i a m o r t a l it y a m o n g s t c h i l d re n a g e d l e s s th a n 5 y e a r s ri s es l i n e a r ly w i t h

i n c r e a s i n g t r a n s m i s s i o n i n t e n s i ty a n d t h o s e w h i c h s h o w e d th a t i n it ia l l i n e ar

r i s e s in m o r t a l i ty r i s k s s a t u r at e u n d e r c o n d i t i o n s o f m o d e r a t e - t o - h i g h t ra n s -

m i s s i o n .

There a re s evera l i s sues nes ted w i th in the p r imary de ba te tha t dem and ca re -

fu l in te rp re ta t ion . F i r st , under cond i t ions o f s tab le , endem ic t r ansmis s ion , ju s t

how qu ick ly do the r i sks o f a poo r c lin ica l ou tco m e fo l lowing in fec t ion dec l ine

wi th ag e? Seco nd , i s the hos t s ab i l ity to deve lo p func t iona l im m uni ty inde-

pend en t o f age ? Th i rd , and a log ica l ex tens ion , do the cum ula t ive r isks o f a

p o o r c l in i c al o u t c o m e t o w a r d s th e e n d o f c h i ld h o o d v a r y b e t w e e n c o m m u n i t ie s

wi th d i f f e ren t fo rces o f tr ansm is s ion? Four th , and pe rhaps o f g rea te r impo r -

t ance to the pu b l i c hea l th deba te , do es P . f a l c i p a r u m in fec t ion p e r s e in f luence

the r i sks o f d i s ease o r dea th no t neces sa r i ly d i r ec t ly due to ma la r i a? F ina lly , i s

the re a po in t a t wh ich a l inea r a s soc ia t ion be tw een m or ta l i ty and t r ansm is s ion

in tens i ty s a tu ra tes , and , i f so , wha t i s th i s endemic i ty r ange , wha t i s i t s



2 3 8 R W S N O W A N D K M A R S H

g e o g r a p h i c a l e x t e n t i n A f r i c a , a n d h o w s u c c e s s f u l c a n i n t e r v e n t i o n s b e i n

reduc ing in fec t ion r isks to p lace pop u la t ions be lo w th is r ange?

2 T H E A G E P A T T ER N S O F S E V E R E M A L A R I A M O R B ID I TY :

D E V E LO P IN G F U N C T I O N A L IM M U N I T Y

The re have be en severa l descr ip t ions o f the re la tive , age-specif ic risks of severe

paedia t r ic m orbid i ty a t t r ibuted to P . f lcip rum infect ion across Afr ica . F igure

1 p rov ides a summ ary o f the da ta ava i l ab le f rom hosp i ta l s e t tings loca ted w i th in

tw o crudely def ined t ransmiss ion set tings . T he hosp i ta l data have bee n extracted

f rom e igh t a reas wh ere l e s s than 50 o f the ch i ldhood comm uni t i e s us ing the

hosp i ta l w ere l ike ly to be in fec ted w i th P .

f lcip rum

w h e n s u r v e y e d a t c r o s s

sec t ion ( low- to -mod era te in tens i ty t r ansmis sion ). The r emain ing fou r hosp i tal s

s e r v e d p o p u l a t io n s w h e r e t h e p re v a l e n c e o f in f e c t io n a m o n g c h i l d r e n w a s

greater than 75 (h igh- in tens ity t ransmiss ion) . Character is t ic of severe d isease

under cond i t ions o f h igh - in tens ity t r ansmis s ion i s the overw he lm ing burden

am ong in fan ts (55 -66 o f a l l ch i ldhood mala r ia adm is s ions ) w i th f a r f ew er

cases amon gs t ch ild ren aged 4 yea r s ( le s s than 4 ) . Conver se ly , under cond i -

70

60

~ 5o

~ 4

g 30

.co

E 2 0

< 10

A B C D E F G H I J K L

H o s p i t a l

F i g u r e 1 Percen tage of paediatr ic (0- 4 y ears) malar ia adm iss ions ag ed less than 1

yea r (black) or aged 4 y ears (grey) f rom eigh t areas o f low -to-mod erate intensi ty transmis-

s ion (A: Bakau , The G am bia (Snow e t a l . 1997); B: Kericho, K eny a (Shanks and Snow,

unpublished data), C : Hu m era, Ethiop ia (Seb ox a and Snow, 1997), D: Kil if i Township,

Ke nya (Snow and Marsh, unpublished data); E: Kinshasa, D R C (Greenberg

e t a l .

1989); F:

Brazzavil le, C on go (Trape e t a l . 1987); G Sukuta, Th e Garnbia (Snow e t a l . 1997); F:

Kil if i rural , north, Kenya (Snow e t a l . 1997)) and fou r areas of intense transmission (I :

Kil if i rural, south, K eny a (Snow e t a l . 1997); J : Ncheleng e, Za m bia (Gernaat e t a l . 1998);

K: S iaya, Ken ya (Snow e t a l . 1997); L: Idete and L um eno,Ta nzania (T . Teuscher, unpu b-

lished data)).



TRANSMISSION OF

PL SMODIUM F LCIP RUM

N AFRICA 39

t ions of low -to-m ode rate in tens i ty t ransmiss ion the age-s t ructured , propor t ional

burden appear s to be sp read mo re even ly ac ros s ch i ldhood . A cons i s ten t find ing

in a l l such s tud ies i s tha t the c l in ica l p resen ta t ions o f com pl ica ted f a lc ipa rum

mala r ia a l so va ry accord ing to the in tens i ty o f t r ansmis s ion . The f r equenc y o f

cerebra l m alar ia decl ines wi th increas ing in tens i ty o f t ransmiss ion w hi ls t severe

mala r ia anaemia inc reas ing ly domina tes the c l in ica l bu rden (S lu t ske r e t a l .

1994 ; Snow e t a l . 1994, 1997; Modiano e t a L 1998) . One fur ther impor tant

obse rvat ion i l lus t ra ted in F igu re 1 is that, a t a ll in tens i t ies o f t ransmiss ion , the

r i sks o f s evere d i s ease a re a lway s h igher in in fancy com pared to the f if th yea r

o f l i fe , imp ly ing tha t a deg ree o f im mu ni ty occur s ve ry ea r ly in l i fe .

T o e x a m i n e t h e s p e e d w i t h w h i c h t h i s f u n c t i o n a l i m m u n e r e s p o n s e i s

a c q u i r e d w e s t u d i e d t h e r i sk s o f d e v e l o p i n g s e v e r e m a l a r ia i n i n f a n t s p r e -

s e n t in g t o h o s p i t a l i n f o u r d i s t in c t t r a n s m i s s i o n s e tt i n g s ( S n o w e t a l . 1997) .

D u r i n g t h e f i r st 3 m o n t h s o f l if e th e i n c i d e n c e o f s e v e r e m a l a r ia w a s l o w i n

a ll s e t ti n g s , p r e s u m a b l y a s a re s u l t o f th e p r o t e c t i o n a f f o r d e d b y p a s s i v e l y

a c q u i r e d m a t e r n a l im m u n o g l o b u l i n G ( M c G r e g o r , 1 9 6 5 ) , t h e p h y s i o l o g i c a l

p r o t e c t i o n o f f e r e d th r o u g h t h e c o n t i n u e d p r e s e n c e o f fe t a l h a e m o g l o b i n

( P a s v o l e t a l . 1 9 7 7 ) a n d p o s s i b l y ri b o f l a v i n d e f i c i e n c y ( B a t e s e t a l . 1982) .

T h e r e a f t e r, u n d e r c o n d i t i o n s o f h i g h t r a n sm i s s io n , p e a k i n c i d e n c e i n s e v e r e

d i s e a s e w a s r e a c h e d b y t h e f i f th t o s e v e n t h m o n t h s o f li fe , a f t e r w h i c h i t

s i g n i f ic a n t l y d e c l i n e d b e f o r e t h e f ir s t b i rt h d a y . I n t h e t w o a r e a s o f l o w - t o -

m o d e r a t e t r a n sm i s s i o n , t h e i n c i d e n c e o f s e v e r e d i s e a s e c o n t i n u e d t o r is e p a s t

t h e f i r s t b i r t h d a y . T h e i n c i d e n c e d a t a i n i n f a n c y w e r e m o d e l l e d a g a i n s t t h e

f o r c e o f in f e c t io n , a s m e a s u r e d t h r o u g h t h e i n fa n t p a r a s i to l o g i c a l c o n v e r s i o n

r a te a m o n g s t a s y m p t o m a t i c in f a n ts l iv i n g in th e s a m e c o m m u n i t i e s ( G u p t a e t

a l . 1 9 9 9 ). T h e b e s t - f i t m o d e l s s u g g e s t e d t h a t a s i g n if i c a n t d e g r e e o f fu n c -

t i o n a l i m m u n i t y a g a i n s t s e v e r e d i s e a s e o c c u r r e d f o l l o w i n g e x p o s u r e t o

r e l a t iv e l y f e w n e w i n f e c ti o n s . I t i s im p o r t a n t t o r e c o g n i z e t h a t th e s a m e m a y

n o t b e t r u e f o r a c h i l d s a b i l it y t o m o u n t a n e f f e c t i v e i m m u n e r e s p o n s e t o

in fec t ion

p e r s e

n o r o n e t h a t p r e v e n t s m i l d c l i n ic a l e p i s o d e s . T h e p r e v a l e n c e

o f b o t h th e s e s t a t e s c o n t i n u e s t o r e m a i n h i g h t h r o u g h o u t c h i l d h o o d i n a l m o s t

e v e r y tr a n s m i s s i o n s e tt in g . P r e v e n t i n g t h e s e s t a te s m a y r e q u i r e e x p o s u r e t o

a w i d e r a n g e o f p ar a si te p o l y m o r p h i s m s w h i l s t th e e p i d e m i o l o g i c a l d a t a o n

s e v e r e m a l a r i a o u t c o m e s l e n d s u p p o r t to a d e g r e e o f s t r a i n - t r a n s c e n d i n g

i m m u n i t y ( G u p t a e t a l . 1999) .

T h e r e a p p e a r s t o b e a g e n e r a l c o n s e n s u s t h a t t h e i n t e n s i t y o f P . f a l c i -

p a r u m t r a n s m i s s io n p r o v i d e s a u s e f u l i n d ic a t i o n o f t h e l ik e l y a g e - s t r u c t u r e d

r i sk o f s e v e r e c li n i c a l d i s e a s e i n a g i v e n p o p u l a t io n . I t a l s o s e e m s r e a s o n a b l e

t o a s s u m e t h a t t h e d e c l i n i n g i n c i d e n c e o f s e v e r e o u t c o m e s f o l l o w i n g i n f e c -

t io n i s in s o m e w a y a f u n c t i o n o f t h e d e g r e e o f p a r a s i te e x p o s u r e f r o m b i r th .

W h e t h e r t h e o u t c o m e s o f a c l in i c a l e p i s o d e o f m a l a r i a a r e b e t t e r o r w o r s e a s

c h i l d r e n p r o g r e s s t h r o u g h i n f a n c y a n d c h i l d h o o d i s t h e r e f o r e i m p o r t a n t t o

def ine .



24 R W S N O W A N D K M A R S H

3 T H E EF FE C TS O F A G E O N T H E R IS K O F D I S E A S E O U T C O M E S

With several infectious diseases, notably measles and rubella, primary expo-

sure to the pathogen later in life results in a poorer clinical outcome compared

to an exposure in early life (Anderson and May, 1991). With malaria, several

authors have argued that the opposite may be true when an older child is better

able to recover from primary infections than younger children or to respond to

treatment (D Alessandro and Coosemans, 1997; Greenwood, 1997). There

are probably good behavioural reasons to imagine this would be the case when

an older child can draw attention to symptoms more quickly than young chil-

dren. However empirical descriptions of this age-effect or any biological basis

for its existence have until recently not been well addressed.

Baird and colleagues have described the relationship between age, infection

and severity of outcome through a series of studies amongst both immune

and na fve populations in Irian Jaya, Indonesia (Baird e t a l . 1993, 1998; Baird,

1998). Whilst it appears that, among non-immune migrants to falciparum

endemic areas, adults develop a stronger and faster immune response to infec-

tion than children, the clinical outcomes of infection are worse in adulthood

than those in childhood. This suggests some increasing constitutional ability of

the immune system to mount a response to infection as patients get older.

This response however may not provide any additional advantage in dealing

with the primary infection. Two further analyses of risks and outcomes of fal-

ciparum malaria among non-immune migrants support the findings from Irian

Jaya. The risk of clinical malaria among non-immune Israeli travellers was

highest amongst the group below 40 years of age but the risks of developing

severe, complicated malaria were four times higher among those aged over 40

years (Schwartz e t a L 2001). Similarly, in the United States of America P f a l -

c i p a r u m malaria case-fatality rates among non-immune travellers aged over 20

years were 10 times higher than those among travellers aged less than 20

years (Greenberg and Lobel, 1990).

When studying the effects of age upon disease risks in highly endemic areas

such as Africa, there is a problem differentiating the coincidental effects of

cumulative parasite exposure with time from those of a g e p e r s e. One useful and

available source of information is the survival chances of those who have devel-

oped disease. We have previously compiled case-fatalities amongst severe and/or

complicated malaria admissions from several clinical settings across Africa

where hospitals are located in a wide range of endemicities (Figure 2; Marsh and

Snow, 2000). One striking feature is that very young children (1-5 months of

age) have a particularly poor prognosis following admission with complicated

malaria. Between 6 and 23 months, case-fatalities decline but thereafter show,

despite wide confidence intervals, a consistent rise with increasing age of the

child. This is consistent with the findings from non-immune travellers and



TRANSMISSION OF PL SMODIUM F LCIP RUM N AFRICA 24

~ 6

o~

v 5

'~ 3

1- 6- 12- 24- 36- 48-

Age months)

Figure 2

Age-specific case-fatalities (percentage; 95 confidence interval) among

paediatric admissions from 10 locations representing the transmission intensity range

common to Africa (Marsh and Snow, 2000).

supports a general principle that, whilst incidence o f severe disease ma y decline

throughout childhood, the risks of a fatal outcom e increase.

4 . RATES OF PAEDIATRIC MA LAR IA MOR BID ITY ACROSS THE

V A R IE D T R A N S M I S S I O N S E T T I N GS OF A F R I C A

There have been several attempts to examine differences in m orbidity betwee n

communities living under different intensities of transmission. Ellman et al.

(1998) recorded the monthly per iod prevalence of fever associa ted wi th a

peripheral

P. f a l c ipa rum

parasitaemia > 400 0 parasites per microlitre ( 'malaria

cases ') am ong children aged 6-7 1 months in f ive clusters of vil lages located at

different altitudes in M uhe za district, Tanzania. As altitude increased the fre-

quency of 'malaria cases' decreased, although the only significant reduction in

risk was in the two clusters where the prevalence of 'asym ptom atic ' infection

was lowe st (46 and 33 ) . Conversely, in two similar rural populations of

Senegal subjected to challenges of around 20 and 200 infected bites per person

per year, respectively, the total l ifet ime experience of cl inical episodes of

malaria was h igher in the population receiving the lower challenge (Trape and

Rogier, 1996). How ever, there is circularity in the definition o f morbid ca ses of

malar ia dur ing fever surveys under varying in tensit ies of t ransmiss ion.

Etiological fraction estimates of the num bers of fevers attributed to a given par-

asit ic infection will differ between areas where infection is rare and those

where infection is frequent (Smith, T.A. et al. 1994).



2 4 2 R .W. S NOW A ND K . MA RS H

100 q

.~ 90 1

--~

o 8

o

~ - ~ 6 0

5O

• 30

o

< o

i i i i r i

0 10 20 30 40 50 60 70

Prevalence of infection ( )

Figure 3 The annual incidence of hospitalization with severe malaria per 1000 infants

aged 1-11 months (with 95 confidence nterval) from five communities ocated within

easy access of the hospital site against the prevalence of P l a s m o d i u m f a l c i p a r u m infection

among asymptomatic nfants aged 3-11 months from these communities (Snowe t a l .

1998a).

A clearer distinction can be made with the definition of severe, complicated

malaria. Trape and colleagues (1987) reviewed the hospital records in

Brazzaville, where populations living in close proximity and using the same

health services were exposed to a wide range of challenges. The incidence of

cases of severe, life-threatening, malaria was similar at all levels of transmis-

sion but maximum values were observed in areas of moderate transmission.

More recently, we used a standardized protocol to examine prospectively the

incidence of severe malaria in five different populations across Africa having

similar access to, and utilization of, hospital services but living with a wide

range of malaria transmission levels (Snow e t a l . 1997, 1998a). For infants, the

risks of hospitalization with a severe malaria event rose with increasing preva-

lence of 'asymptomatic' infection defined amongst infants in these

communities (Figure 3). The combined risks throughout childhood (1-59

months) were lowest among populations exposed to very low intensity parasite

transmission (childhood infection prevalence in the community less than 5 ).

However, as with the previous studies amongst older children, the highest risk

occurred in communities exposed to moderate intensity transmission (infection

prevalence 40-50 ) and risk declined in populations exposed to high trans-

mission (infection prevalence > 75 ) (Figure 4).

Thus, with severe clinical outcomes examined using a range of methodolo-

gies, a consistent pattern seemed to emerge. Nevertheless, reliance upon

hospital data in the comparison of community risk has been much criticized. It

has been argued that communities vary enormously in their utilization of hos-

pitals, one determinant being a community's perception of disease severity.

The latter is particularly important owing to reported differences in the clinical

presentations of life-threatening disease with age and endemicity (Greenwood,



T R A N S M I S S I O N O F PL SMO DIUM F LCIP RUM IN A FRICA 24 3

50

B

L

~o 40

o o

o

< 0

I

i i i i i i i i

0 10 20 30 40 50 60 70 80 90

Preva lence of p arasitaem ia in childhood

F i g u r e 4 T h e

annual incidence of severe malaria admissions per 1000 children aged

1-59 months (with 95 confidence nterval) from five communitieswith differentmalaria

transmission intensities (Snow

e t a l .

1997).

1997; Smith, T. A.

e t a l .

2001). Furthermore, one feature of hospitalized cases

of severe disease, whilst serving as a clinical proxy for mortality, is character-

ized by survival at discharge. Hospital case-fatalities can be high but invariably

90 of admissions do survive and are returned to the communityl

5 T H E R I S K S O F M O R T A L I T Y D U R I N G C H I L D H O O D W I T H

I N C R E A S I N G I N T E N S I T Y O F M A L A R I A T R A N S M I S S I O N

The critical issue to arise is whether one can conclude that the patterns

described from studies of hospitalized malaria morbidity would remain true for

deaths from malaria in the community. During an early examination of this we

reviewed available data on malaria-specific mortality at different levels of

transmission (Snow and Marsh, 1995). The limited data covered a range of

endemicities, mortality measurement techniques and time periods. The data

were consistent with any number of interpretations: malaria mortality rising,

reaching a plateau, or declining as transmission intensity increased.

We concluded that the data were not sufficiently robust to draw definitive

conclusions. Important reservations were raised about the ecological compar-

isons made between different communities separated sometimes by over 50

years, when changing access to treatment and other child survival initiatives

would have confounded any comparison. Furthermore, the measurements of

mortality risks ranged from civil registration systems to more contemporary

systems of active demographic surveillance. Finally, the clinical presentation

of malaria often shares symptoms with other infectious diseases, notably fever,

diarrhoea and respiratory abnormalities and the attribution of malaria as the



2 4 4 R W S N O W A N D K M A RS H

primary cause of a paediatric death through interviews with bereaved relatives

lacks both sensitivity and specificity (Anker e t a l . 1999).

Two more recent analyses of mortality data amongst infants and children in

Africa against a range of transmission conditions have tried to redress some of

the deficiencies in our earlier comparative studies. First, Chandromohan e t a l .

(2001) analysed contemporary data from a collaborative programme of demo-

graphic surveillance in two of the three sentinel demographic surveillance

system (DSS) districts of a single country, Tanzania. The authors described one

mesohyperendemic district and three transects of a low malaria risk district,

according to whether communities are located at 1001-1250 m, 1251-1500 m

or above 1500 m. The analysis considered the age-structured acute febrile

mortality risks, rather than all-cause mortality, and showed that these risks

were low in areas above 1251 m, at intermediate levels between 1001 and

1250 m, and highest where stable endemic transmission had been recorded, in

Morogoro district. Interpretation of these data at the lower altitude transects

was hampered by the lack of any empirical knowledge of either infection

prevalence or sporozoite inoculation rates. The most persuasive conclusion to

be drawn was that, where transmission is restricted by low ambient tempera-

ture, mortality from malaria is rare amongst all age groups from infancy

through to the tenth birthday.

T.A. Smith and colleagues (2001) have provided the second more recent

extension of the debate. They revisited the ecological comparisons of the rela-

tionship between entomological inoculation rates (EIR) and childhood

mortality outcomes, and argued in favour of a comparison of all-cause mor-

tality rather than malaria-specific mortality. This is an important extension for

several reasons beyond the technical difficulties in defining malaria-specific

mortality. First, cause-specific mortality implies that a single cause is respon-

sible for each death, when in reality malaria may be a secondary, coincidental

or co-primary cause of death. Second, the effects of a single malaria infection

may go beyond the direct consequences of surviving that infection, when the

parasitized host may not experience any direct clinical effect of the infection

but susceptibility to the pathological consequences of other infectious agents

may be amplified, leading to indirect mortality .

Smith, T.A.

e t a l .

(2001) therefore first considered the rates of all-cause

infant mortality from 20 DSS studies undertaken since 1980 plotted against an

estimate of the intensity of transmission as judged by the EIR (Figure 5). The

spread of infant mortality risk was considerable but there was a significant pos-

itive association between all-cause infant mortality and increasing intensity of

transmission. To examine whether this association was maintained throughout

childhood, the authors extended their analysis to consider mortality risks

between the first and fifth birthdays. Two striking observations were: (i) all-

cause mortality among older children varied less than infant mortality across

the transmission intensity range; and (ii) it did not support the notion that




T

200

180

160

140

120

100

80

60

40

20

0

O

•

• [ ]

e

D D

[]

[ ] [ ] ~ ]

10 100 1000

EIR infect ive bi tes pe r person pe r year)

Figure 5 Distribution o f all-cause mortality 0-11 mo nths (O) and 12-59 mo nths ([~)

from 20 sites in Africa by the a nnual P. f a l c iparum entom ological inoculation rate (EIR)

(Sm ith, T.A. et al. 2001).

m o r t a l it y i n th i s a g e r a n g e r o s e w i t h in c r e a s in g E I R ( F i g u r e 5) . T h e c o m b i n e d

m o r t a l it y ri sk s f r o m b i r th t h r o u g h t o t h e f i ft h b i r th d a y d i d s u g g e s t a t e n d e n c y

t o w a r d s h i g h e r m o r t a l i t y w i t h i n c r e a s i n g E I R , d r i v e n p r i n c i p a l l y b y t h e e f f e c t s

d u r i n g i n f a n c y , b u t t h is a s s o c i a t i o n w a s n o t s i g n i f ic a n t . T h i s o b s e r v a t i o n s u g -

g e s ts t h a t a d e l a y i n t h e r i sk o f d e a t h e a r l y in l i f e m a y i n c r e a se t h e n u m b e r s o f

y e a r s o f l if e s a v e d b u t m a y n o t a l te r th e n u m b e r o f d e a t h s i f d e a th w e r e s i m p l y

d e l a y e d u n t i l la t e r in c h i l d h o o d . G i v e n t h e e p i d e m i o l o g i c a l c o n c e r n s r a i se d

t h r o u g h e a r li e r s t u d ie s o n th e p o s s ib l e d e l a y e d r is k s o f s e v e re m a l a r i a m o r -

b i d i ty , t h is o b s e r v a t i o n d e s e r v e s f u r t h e r r e v ie w .

6 . L I M I T A T I O N S O F T H E x A X I S

E c o l o g i c a l c o m p a r i s o n s a r e o p e n t o m u c h c r i ti c is m . E v e r y d e m o g r a p h i c s it e

h a s i ts o w n i d i o s y n c r a s i e s i n t e r m s o f s o c i o e c o n o m i c v a ri a b le s , a c c e s s t o a n d

e f f e c ti v e n e s s o f h e a l t h s e rv i ce s , p r e v a le n c e o f h u m a n i m m u n o d e f i c i e n c y v ir u s

o r t h e g e n e t i c m a k e - u p o f t h e p o p u l a t io n . A l l t h in g s a r e n o t e q u a l a n d e p i-

d e m i o l o g i s ts c o m p a r i n g r i sk s b e t w e e n g e o g r a p h i c a l a r e as c a n a t b e s t s u p p o r t

o r c a s t d o u b t o n a g e n e r a l p ri n c i p le . N e v e r t h e l e s s , d a t a o n m o r t a l i t y o u t c o m e s

p l o t t e d a g a i n s t e s t im a t e s o f th e f r e q u e n c y o f p a r a s i te c h a l l e n g e r e m a i n o u r o n l y

p r i m a r y s o u r c e o f e v i d e n c e t o e x a m i n e t h e r e l a t i o n s h i p b e t w e e n e x p o s u r e




intensity and disease outcome. The one area where it is possible to insist upon

a degree of comparability is in the methodologies used to define the parame-

ters of interest.

The EIR is the product of the human biting rate (the number of vectors

biting an individual over a fixed period of time, usually expressed per year)

and the sporozoite rate (the proportion of vectors with sporozoites in the

salivary glands). Estimates of sporozoite challenge across broad geograph-

ical areas are fraught with methodological problems. First, the frequency of

parasite exposure varies considerably within small geographical areas and

even between households (Cattanni

e t a l .

1985; Mbogo

e t a l .

1995).

Previous comparisons of the risks of parasite challenge from birth and dis-

ease outcomes have often selected one point estimate of EIR from a single

household or a collection of households to represent the wide areas from

which mortality has been documented. Second, whilst the EIR defines the

frequency of contact between hosts and infected vectors, methods used to

measure it in the field vary (Githeko

e t a l .

1996). Whether sampling of vec-

tors is undertaken indoors or outdoors with light-traps placed close to the

bed, with pyrethrum spray catches, or by human bait catches, affects the cal-

culation of the EIR. The overall consequence is that EIR data are hard to

reconcile as standard measures between sites and may convey a degree of

precision in the estimation of parasite challenge that simply does not exist.

A final comment for the purposes of ecological comparisons is that a focus

on estimates of sporozoite inoculation excludes the use of considerable

additional mortality data for which other proxies of transmission intensity

exist.

A more readily available, and widely used, index of transmission intensity

is the parasite rate (Metselaar and Van Theil, 1959). This is often presented as

the prevalence of

P . f a l c i p a r u m

infection among children and has the advan-

tage over entomological measures of endemicity in that surveys often cover

more comprehensively the geographical areas used to define mortality.

Prevalence of infection crudely corresponds to the frequency and duration of

parasite exposure but does not provide a precise estimate of the number of

new infections received by a child each year. The non-linear relationship

between challenge and infection prevalence has long been recognized

(MacDondald, 1957). Given the long persistence of parasitaemia after a single

infection (Eyles and Young, 1951), it might be expected that parasite preva-

lence would become an increasingly blunt instrument at higher levels of

transmission.

Beier and colleagues (1999) have recently reviewed coincidental measures

of the parasite prevalence in childhood and standardized estimates of EIR.

Their analysis showed that over 70 of the variance in parasite prevalence

could be explained by logarithmic classification of the EIR, overall and when

analysed by region - East and West Africa - or 'ecological zone'. Broadly, no




t h e p r e v a le n c e o f in f e c t i o n a m o n g c h i l d r e n a g e d b e t w e e n 0 a n d 1 5 y e a r s o f a g e

( T a b le 1 , p p . 2 5 2 - 3 ) . T h e 2 6 m o r t a l i t y e s t i m a t e s h a v e b e e n g r o u p e d a c c o r d i n g

t o w h e t h e r t h e p r e v a l e n c e o f i n f e c t io n w a s l e ss t h a n 2 5 ( lo w t ra n s m i s s i o n

i n te n s i ty ) , 2 5 - 5 0 ( l o w - t o - m o d e r a t e t r a n s m i s s io n i n te n s it y ) , 5 1 - 7 4 ( m o d -

e r a t e - t o - h i g h t r a n s m i s s i o n i n t e n s i t y ) o r g r e a t e r t h a n 7 4 ( h i g h t r a n s m i s s i o n

in t ens i t y ) (F igu re 6 ) .

O n e i m p o r t a n t o b s e r v a t i o n i s t h a t a n A f r i c a n c h i l d s t a n d s a s i g n i f i c a n t l y

g r e a t e r c h a n c e o f s u r v i v in g c h i l d h o o d i f h e o r s h e l i v es i n a n a r e a o f l o w

m a l a r i a r is k . C h i l d r e n l i v i n g in l o w t r a n s m i s s i o n a r e a s o f A f r i c a e x p e r i e n c e

a l m o s t h a l f th e m o r t a l it y ri sk s c o m p a r e d t o t h o s e w h o l iv e u n d e r c o n d i ti o n s o f

m o d e r a t e - t o - h i g h t r a n s m i s s i o n i n t e n s i t y . T h i s i s e n t i r e l y c o n s i s t e n t w i t h t h e

o b s e r v a t io n s d e r i v e d f r o m t h e s t u d y o f s e v e r e d i se a s e ( F i g u r e s 3 a n d 4 ) a n d

a c u t e f e b r il e m o r t a li t y r i sk ( C h a n d r a m o h a n

e t a l .

2 0 0 1 ). T h e r i s k o f a p o o r

m a l a r i a o u t c o m e u n d e r s u c h c o n d i t i o n s o f t r a n s m i s si o n is l i k e l y to b e d i r e c tl y

r e l a t e d t o t h e c h a n c e o f e n c o u n t e r s w i t h in f e c t i o n . F o r a l l- c a u s e m o r t a l i t y t h i s

o b s e r v a t i o n h a s g r e a t e r s i g n i f i c a n c e a s i t d e m o n s t r a t e s c l e a r l y t h e c o n t r i b u t i o n

m a l a r i a m a k e s t o t h e o v e r a l l c h a n c e s o f s u r v i v a l . N e v e r t h e l e s s , i t c o u l d b e

a r g u e d t h a t a re a s o f l o w m a l a r i a r is k a r e t h o s e o f g r e a t er e c o n o m i c g r o w t h a n d

s t a b i l i t y . I n d e e d , t h e a r e a s w e h a v e c l a s s i f i e d a s l o w m a l a r i a r i s k a r e h i g h

i n t e n s i t y a g r i c u l t u r a l r e g i o n s o f e a s t a n d s o u t h e r n A f r i c a ( T r a n s v a a l , S o u t h

80

Q

o 60

¢

4 0

E

2 0

<

3

In tens i ty o f P f a l c ip a r u m r a n s mi s s i o n

Figure 6

Box plot show ing m edian (central lines), 25 , 75 quartile ranges around the

me dian (box dep th) and upp er and lower limits (T-bars) of all-cause childhood mortality per

1000 children aged 0--4 years per annum recorded during the surveillance of c om mu nities

located in (1) areas o f low, (2) low -to-mode rate, (3) m oderate-to-high or (4) high intensity

transmission as defined in T able 1.




Africa, Mu ranga and Kericho in Ken ya and Hai in Tanzania). By extension ou r

analysis ma y simply b e an eco logical fallacy, reflecting m ore a poverty divide

with malaria m aintaining som e comm unities in the vicious trap o f poor health.

On a global scale, this has bee n well articulated by Sachs and Ma laney (2002);

at a continental level, it has be en less w ell defined. It wo uld be hard to distin-

guish the t rue cause or ef fec t of the ro le p layed by malar ia but whatever

explanation one favou rs it rem ains true that within the series of data presented

in Figure 6, living under cond itions of low malaria risk imp roves the chance o f

surviving childhood.

The second str iking observation, consistent with the analysis provided by

Smith, T.A.

e t a l

(2001), is that across a broad range of malaria transmission

intensities all-cause mortality under 5 years of age appears to vary very little.

This pattern o f all-cause childhood m ortality is strikingly similar to the pattern

described for severe morbidity presenting to hospital (Figure 4). The notion of

a mortality 'plateau' is most evident from the comparison o f median estimates

of mortali ty under 5 years within the moderate-to-high and high transmission

categor ies . These t ransmiss ion condi t ions cover a wide range of se t t ings

encom passing childhood infection prevalence rates from 50 to 90 . The mor-

tality ranges within areas of low-to -mo derate intensity transmission are harder

to interpret. W hat is clear is that mo rtality risk proba bly rises sharply und er rel-

at ively small changes in the frequency o f parasite challenge. At the low er end

of this transmission category, mortali ty rates were comparable to those in

endemic sites in the low intensity transmission range. Within this range, a

small increase in the prevalence of infection w as associated w ith a much larger

rise in mortality risk (Table 1). At some ill-defined point within this range of

transmission conditions mortality, as with severe disease risk, prob ably reaches

its point of saturation. This nadir is probably higher than prev iously propose d

for malaria-specific mortality by Trape and Ro gier (1996), wh o argued that sat-

uration occurs at conditions supporting one infective bite every 8 years.

As one would expect with any ecological comparison, the ranges of mor-

ta l i ty wi thin any given t ransmiss ion ca tegory vary considerably and are

probab ly the result of differences betw een com mun ities in factors other than

the frequency of infection. Nevertheless, for the same reasons we feel com-

fortable with the proposit ion that al l-cause mortali ty below 5 years of age is

considerably lower under condit ions of low intensity transmission because

w e feel that there is little eviden ce that mortality in this age gro up rises ov er a

broad range of low-to-m oderate , mo dera te- to-high and high t ransmiss ion

intensities.



250 R.W. SNO W AND K. MARSH

8 . R E C O N C I L I N G T H E R O L E O F D IR E C T A N D I N D IR E C T E F F E C TS O F

P F A L C l P A R U M O N C H IL D S U R V I V A L W I T H T H E S A T U R A T I O N

O F A L L C A U S E M O R T A L I T Y W I T H I N C R E A S I N G T R A N S M I S S I O N

Several au thors have argued that indi rect mor ta l i ty i s a s ignif icant fea ture of

mala r i a in fec t ion and tha t in tense t r ansmis s ion w i l l l ead to a s t a te o f ch ron ic

paras it i za t ion tha t p rov ides a gen era l i zed enha ncem en t o f r isk o f ea r ly mor ta l -

i ty (Gree nw ood , 1997 ; Mol ineau x , 1997). D a ta used in suppor t o f ind i r ec t

mala r i a m or ta l i ty w ere de r ived f rom resu l t s ob ta ined du r ing t ri a ls o f chem o-

p r o p h y l a x i s ( G r e e n w o o d

e t a l .

1988) and insec t i c ide - t r ea ted bed ne t s ( ITNs )

( A l o n s o

e t a l .

1993b) pe r fo rm ed in The Gam bia . These t r ia l s show ed tha t the

e f f ec t s upon a l l - cause mor ta l i ty were l a rge r than wou ld have been expec ted

g i v e n t h e b a s e l i n e e s t im a t e s o f m a l a r i a -s p e c i f ic m o r t a li t y d e f i n e d t h r o u g h

verba l au topsy , a l though i t m us t a l so be t rue tha t th is cou ld be in te rp re ted as

fu r the r ev idence o f the inadequacy o f the ve rba l au topsy t echn ique . The s econd

and w ide ly c i ted sources o f ev idence in suppor t o f ind i rec t ma la r ia mor ta l i ty a r e

the h i s to r i ca l and p rec ip i tous dec l ines in a l l - cause mor ta l i ty a s soc ia ted w i th

aggres s ive vec to r con t ro l p rogramm es in S r i Lanka , Gu a tem ala and the Pare

region of Tanzania (M olinea ux, 1985; 1996; Brad ley, 1991, 1992). Ho w eve r, as

mos t au tho r s comment ing on these da ta h igh l igh t , vec to r con t ro l was imple -

m e n t e d c o i n c i d e n t a l l y w i t h g e n e r a l i z e d i m p r o v e m e n t s i n t h e p r o v i s i o n o f

cu ra t ive s e rv ices ( ac tua l ly in s t iga ted in the Pare r eg ion because o f f ea r s o f

' r eboun d ' m or ta l i ty ' ; Smi th , A . and P r ing le , 1967) o r bec ause o f eco nom ic

dev elop m ent (Lan gford , 1996) . This ge nera l pr incip le w e wi l l re turn to later .

T h e r e i s p e r s u a s i v e e v i d e n c e o f t h e i n d i r e c t ro l e p l a y e d b y m a l a r i a i n

inc reas ing the r i sks o f low b i rth w e igh t bab ies fo r wo m en l iv ing under inc reas -

i n g i n te n s i t ie s o f m a l a r ia t r a n s m i s s io n . L o w b i r th w e i g h t is a m a j o r

de te rminan t o f neona ta l and pos t -neona ta l mor ta l i ty to the ex ten t tha t i t has

been sugge s ted tha t 25 o f a l l neona ta l dea ths can be a t tr ibu ted to ma la r i a

d u r i n g p r e g n a n c y ( G o o d m a n e t a l . 1999). In fancy a l so m arks a pe r iod o f pa r -

t i cu la r r i sk fo r invas ive bac te r i a l in fec t ions . Paed ia t r i c bac te raem ias a re m os t

c o m m o n a m o n g c h i l d r e n a g e d 0 - 6 m o n t h s a n d r e c e n t m o r e d e t a i l e d c l i n i c a l

desc r ip t ions o f the ir pa tho log y and p rogn os i s sug ges t tha t ma la r i a l in fec t ions

m ay inc rease the r i sk o f a f a t a l ou tc om e in hosp i t a l s e t t ings . F ina lly , ch ron ic

and r epea ted in fec t ions du r ing ea r ly ch i ldhood l ead to a s ta t e o f anaem ia and

o the r s t a te s o f undernu t r i t ion so tha t the com bine d e f f ec t s m ay enh ance the

suscep t ib i l i ty to genera l i zed m orb id i ty and mor ta l ity . Ana em ia , mic ronu t r i en t

de f i c ienc ies and w as t ing a re pa r t i cu la r ly m arked dur ing the f i rs t yea r o f li f e in

m o s t m a l ar ia e n d e m i c c o m m u n i t i e s . T h e s e ' in d i r e c t' m o r t a li ty r is k s m a y w e l l

exer t the i r g rea tes t in f luence du r ing a pe r iod o f an in fan t ' s l i f e wh en h e o r she

i s a t low es t ri sk o f a d i r ec t f a ta l ou tc om e fo l lowing in fec tion . As the in tens i ty

o f t r ansmis s ion inc reases , the r isks o f ind ir ec t , ea r ly in fan t m or ta l i ty m ay



T R A N S M I S S I O N O F P L S M O D I U M F L C l P R U M IN AFRICA 25

i n c r e a se b u t t h is w o u l d b e b a l a n c e d a g a i n st s u r v iv o r s m o r e r a p i d l y b e c o m i n g

i m m u n e t o t h e d i r e c t e ff e c t s o f s e v e r e m a l ar ia . F u r t h e rm o r e , i t w o u l d a p p e a r

f rom the ana lys i s o f a ll - cause m or ta l ity th roughou t ch i ldhoo d (F igures 5 and 6 )

t h a t u n d e r c o n d i t i o n s o f f r e q u e n t p a r a s i t e c h a l l e n g e i n A f r i c a t h e i n d i r e c t

e f f e c t s o f i n f e c ti o n o n c h i ld h e a l t h a r e o u t w e i g h e d b y t h e d i re c t c o n s e q u e n c e s

o f in fec tion .

9 . I N S E C T I C I D E T R E A T E D B E D N E T S I N A F R I C A

On e o f the m os t s ign i f i can t advance s in ma la r i a con t ro l in Af r i ca ov er the l a s t

1 5 y e a r s h a s b e e n t h e r e s u lt s o f c a r e f u l l y d e s i g n e d c l in i c a l t ri a ls o f I T N s

( insec ti c ide - tr ea ted be d ne t s ) and cu r ta ins. The com bine d r esu l ts o f these t r ia l s

s u g g e s t th a t t h e u s e o f I T N s c a n r e d u c e a l l- c a u s e c h i ld h o o d m o r t a l i ty b y 1 7

( L e n g e l e r , 1 9 9 8 ). T h e t r ia l s w e r e u n d e r t a k e n a c r o s s a r a n g e o f b a s e l i n e

endemic i t i e s in Af r i ca and one ea r ly obse rva t ion was tha t p ro tec t ive e f f i cacy

appea red to dec l ine w i th inc reas ing in tensi ty o f tr ansmis s ion (Tab le 2, p . 254) .

Nev er the les s , i t has bee n sugg es ted tha t com par i sons o f r e su l ts ob ta ined f rom

randomized con t ro l l ed t r i a l s (RCTs ) shou ld focus on a t t r ibu tab le r i sks (num-

ber s o f l ives s aved) r a the r than r a te r a t io s (p ro tec t ive e f f i cacy ) (Lenge le r

e t a l .

1998) . W hen r eana lysed , the t r i al da ta sh ow ed tha t the re w as l i tt le d i f f e rence

i n t h e n u m b e r o f l i v e s s a v e d ( 1 o r 6 - 5 9 m o n t h s o f a g e ) w h e t h e r t h e t r i a l s

were under taken in h igh o r low in tens i ty t r ansmis s ion loca t ions (Lenge le r

e t

a l .

1998) . Th i s may sugges t tha t ITNs a re l ike ly to be o f sus ta ined pub l i c

hea l th va lue ac ros s the en t i r e t r ansmis s ion spec t rum, bu t such an as se r t ion

requ i r es a t leas t tw o bas ic a s sump t ions . F i r s t, t he r esu lt s o f the RC Ts c an be

sus ta ined fo r more than 1 o r 2 yea r s and a r ea l ignmen t o f mor ta l i ty r i sk fo l -

lowing ch anges in in fec tion r i sk f rom b i rth m us t no t a f f ec t long- te rm ch i ldhood

surv iva l . Second , i f the t r end in p ro tec t ive e f f i cac ies in f avour o f a r eas o f

l o w e r i n t e n s i ty t r a n s m i s s i o n i n d e e d e x i s t s, th e n c h i l d h o o d m o r t a l i ty ( 0 - 4

year s ) w ou ld need to b e cons i s t en t ly h igher a t inc reas ing in tensi t ie s o f t rans -

m is s ion to ba lanc e any dec l in ing p ro tec t ive e f f icacy . As d i s cus sed ab ove , the re

is l it t le e v id enc e in supp or t o f th is .

O n l y t w o p u b l i s h e d R C T s h a v e b e e n u n d e r t a k e n i n a r e a s o f h i g h i n t e n si ty

t r ansmis s ion (Tab le 2 ) . Bo th s tud ies , in no r the rn Ghana (B inka

e t a l .

1996)

and Burk ina Faso (Hab lue tze l

e t a l .

1997), show ed r educe d p ro tec t ive e f fi cacy

dur ing the s econ d yea r o f the t ri a ls co m pared to the f ir s t yea r. The u nad jus ted

ra te ra t io s o f the in te rven t ion to con t ro l mor ta l i ty amo ngs t ch i ld ren age d 6 -5 9

mo nths w as 0 .72 du r ing yea r 1 com pared w i th 1 .01 du r ing y ea r 2 in Ghana and

0 .84 du r ing ye a r 1 and 1 .04 du r ing y ea r 2 in Burk ina Faso . On e fu r the r RCT ,

in an a rea o f in tense , pe renn ia l t r ansmis s ion a t Asembo Bay , wes te rn Kenya ,

w h e r e s t r i c t r a n d o m i z a t i o n w a s m a i n t a i n e d f o r 2 y e a r s , h a s r e c e n t l y b e e n




Table A l l -c a u s e c h i ld h o o d m o r ta l i ty 0 --4 y e a r s ) a t 2 6 s i t e s in A f r i c a a c c o rd in g to

c a te g o r i c a l e s t ima te s o f th e in t e n s i ty o f P la smod ium fa l c i p a r um t r a n s mis s io na

Si te Chi ldho od D ate s f P e rs o n - Al l-cause Mortal ity

in fe ct io n mortality years mortality rate

preva lence ,a survei llance expo sure e v e n ts un de r

to risk 0- 4 years) 5 years)

0--4 years)

L o w e n d e m i c i ty a r ea s e

1. Agincourt , South Africa 6 [0-9] 1 99 2 -9 5 2,880,00 0 216 0.075

2. Hai district, Tanzania 4 [0-9] 199 2-9 5 74,4 94 1,233 16.55

3. Kericho , Keny a 12 [0-9] 19 97 -9 8 30,623 325 10.61

4. M barara, Uganda 18 [0-3] 19 88- 89 4,320 104 24.07

5. M uranga, Kenya 24 [0-15] 19 85- 88 1,952 251 21.0

L o w t o m o d e r a t e e n d e m i c i ty a r e as

6. Dar es Salaam, Tanzania 28 [0-9] 199 2-9 5 34,023 883 25.95

7. Band im II, Gu inea Bissau 35 [1-5] 19 87 -9 0 2,753 153 55.58

8. Katana, Dem ocratic Repu blic

of Congo DH C) 35 [1-9] 198 6-8 7 5,187 358 69.02

9. Farafenni, North Bank, The

Gam bia 39 [0.5-6] 19 82 -8 3 2,505 171 68.3

10. Mlom p, Senegal 46 [2-9] 19 85- 95 7,886 194 24.6

11. Kilifi, Kenya 49 [0-9] 19 91- 93 20,679 455 22.0

12. Niakar, Senegal 50 [2-9] 19 84- 95 58,9 82 3,24 2 54.97

M o d e r a t e t o h i g h e n d e m i c i t y a r e a s 8

13. Morogoro district, Tanzania 52 [0-2] 199 2-9 5 50,071 1,795 35.85

14. Kan gondjan, Burkina Faso 54 [0.5-9] 1982-86 1,271 43 36.20

15. Farafenni South Ban k

hamlets, The Gam bia 55 [1-5] 19 88 -90 3,130 150 47.92

16. Bo, Sierra Leone 59 [0-7] 19 90 776 35 45.1

17. Farafenni South Bank PH C

villages, The Gam bia 66 [1-5] 19 88 -89 2,263 146 64.52

18. Upper River Division,

T h e G a mb ia 71 [1 --4 ] 1 9 8 9 -9 3 1 1 3 ,3 1 9 3 ,7 76 3 3.3 2

H i g h e n d e m i c i ty a r e as h

19. Imb o Sud, Lac Nyanz a,

Burundi 76 [2-9] 199 0-91 3,815 160 41.94

20. Bagamoyo, Tanzania 82 [0.5-3.5] 19 92 -94 5,850 192 32.82

21. Pahou and environs, Benin 83 [0-15] 19 89 1,037 29 27.97

22. Asembo Bay, Kenya 83 [1-4] 199 7 NA NA 59.9

23. Nav rongo, Gha na 87 [0-7] 19 90 1,065 35 32.86

24. Tanga, Tanzania 88 [1-4] 19 92- 93 2,072 90 43.44

25. Kilom bero, Tanzan ia 90 [1-9] 1996--97 8,761 279 31.85

26. Bandafassi, Senegal 95 [2-9] 198 4-9 5 16,975 1,167 68.75




Table 2 M ortality reductions recorded during random ized controlled trials o f

insecticide-treated bed nets in Africa and prevalence o f

P l a s m o d i u m f a l c i p a r u m

infection

in children not using treated netsa

Unadjusted Duration

rate ratio ( 6 ~ ) b o f trial

(years)

Baseline or control estimates of

infection prevalence amo ngst

children aged 0- 9 years ( )

The G ambiaC 23

Kilifi, Keny ad 29

Oub ritenga, Burkina Fasor 14

Navrongo, Ghanah 17

1 39c

2 49 e

2 858

2 87

a S e e a ls o L e n g e l e r et al ( 1 9 9 8 ) .

b 1 - - ( i n t e r v e n t i o n m o r t a l i t y r a t e ) / ( c o n t r o l m o r t a l i t y r a t e ) x 1 0 0 .

c D A l e s s an d r o

etal

( 1 9 9 5 ) .

d N e v i l l

et al

( 1 9 9 6 ) .

e S n o w

etal

( 1 9 9 7 ) .

f H a b l u e t z e l etal ( 1 9 9 7 ) .

g H a b l u e t z e l

etal

( 1 9 9 9 ) .

h B i n k a et al ( 1 9 9 6 ) .

i B i n k a

et al

( 1 9 9 4 ) .

c o m p l e t e d . P r e l i m i n a r y e x a m i n a t i o n o f t h e s e r e s u lt s i n d i c a te d a n i m p o r t a n t

r e d u c t i o n i n m o r t a l it y a l th o u g h t h e d a t a a ls o c o n f i r m e d r e d u c e d p r o t e c t i v e

e f f i c a c y a g a i n s t a l l -c a u s e m o r t a l it y a m o n g c h i l d r e n a g e d l es s t h a n 5 y e a r s

d u r i n g t h e s e c o n d , c o m p a r e d t o t h e f i rs t , y e a r o f t h e t ri a l (P . P h i l i p s - H o w a r d ,

p e r s o n a l c o m m u n i c a t i o n ). C o n v e r s e ly , th e o n l y R C T m a i n t a i n e d o v e r 2 y e a r s

i n a n a r e a o f l o w - t o - m o d e r a t e t r a n s m i s s i o n i n t e n s it y ( K i l if i, K e n y a ; N e v i l l

e t

a l . 1 9 9 6 ) s h o w e d l i t t l e v a r i a t i o n b e t w e e n t r i a l y e a r s i n t h e u n a d j u s t e d r a t e

r a t io s f o r a l l -c a u s e m o r t a l i t y a m o n g c h i l d r e n a g e d 6 - 5 9 m o n t h s ( 0 .7 0 i n y e a r

1 a n d 0 . 7 4 i n y e a r 2 ; u n p u b l i s h e d d a t a ).

I t i s i m p o r t a n t t o r e c o g n i z e t h a t , o v e r a l l, m o s t o f th e t r ia l s c a r r i e d o u t i n a

b r o a d s p e c t r u m o f t r a n s m i s s i o n c o n d i t i o n s , w i t h t h e e x c e p t i o n o f th a t in

B u r k i n a F a s o , a c h i e v e d a s i g n i f ic a n t e f f e c t o n c h i l d s u r v i v a l o v e r t h e c o m -

b i n e d s u r v e i l l a n c e p e r i o d a n d t h e y w e r e n o t d e s i g n e d t o u n d e r t a k e a n y

s u b - g r o u p a n a l y si s . N e v e r t h e l e s s , t h e r e r e m a i n s a s t r o n g s u g g e s t i o n t h a t t h e

i n it ia l g a in s a f f o r d e d b y I T N s m a y i n s o m e s e t t in g s d e c l i n e w i t h d u r a t i o n o f

u s e b y t h e c h i l d h o o d p o p u l a t io n . T h e r e c o u l d b e a v a r i et y o f r ea s o n s w h y t hi s

m a y o c c u r . A m o n g s t t h e s e m u s t b e i n c l u d e d t h e p o s s i b i l i t y t h a t , a s c h i l d r e n

a g e w i t h c h a n g i n g c o n d i t i o n s o f p a r a si t e c h a l l e n g e , m o r t a l i t y ri s k re a d j u s ts .

T h i s w o u l d b e c o n s i s t e n t w i t h t h e e c o l o g i c a l a n d c l in i c a l e v i d e n c e c u r r e n t l y

a va i l a b l e .

S u c h a r e a l ig n m e n t o f m o r t a l i ty ri s k u n d e r c o n d i t i o n s o f h i g h t r a n s m i s s i o n

w o u l d n o t b e i m p o r t a n t i f t h e r i s k w e r e b a l a n c e d a g a i n st t h e s a m e l e v e l o f



TRANSMISSION OF P L S M O D I U M F L C lP R U M IN AFRICA 55

p r o t e c t iv e e f f i c a c y a g a in s t c h i l d h o o d m o r t a l i t y a t 0 - 4 y e a r s a s h as b e e n

r e p o r t e d i n a r e a s o f l o w e r i n t e n s i t y t r a n s m i s s i o n o r i f c h i l d h o o d m o r t a l i t y

we re cons i s ten t ly h igher und er cond i t ions o f h igh t r ansmis s ion . N e i the r pos i -

t ion appear s to be suppor ted by the ava i l ab le ev idence . The r esu l t s f rom the

RC Ts sugges t tha t the p ro tec t ion i s h igher under cond i t ions tha t f avour low- to -

m ode rate in tens i ty t ransm iss ion (T able 2). Nei ther Sm ith , T.A. e t a l . (2001) no r

the da ta in F igure 6 f avours the no t ion tha t a l l - cause mor ta l i ty th roughou t

ch i ldho od i s any h igher und er cond i t ions o f m odera te - to -h igh t r ansmis s ion .

1 0 W H O W IL L B E N E F IT M O S T F R O M R E D U C T I O N S IN P A R A S IT E

E X P O S U R E ?

The pos i t ive l inea r a s soc ia t ion be tween severe , l i f e - th rea ten ing mala r ia mor -

b id i ty , dea th f rom mala r ia o r dea th f rom o the r causes du r ing the f i r s t yea r o f

l i fe and inc reasing in tensi ty o f t r ansmis s ion i s suppor ted b y a va r ie ty o f empi r -

i ca l da ta sou rces r ev iewed in Sec t ions 5 and 7 above . However , the idea tha t

th is a s soc ia t ion i s ma in ta ined th roug hou t ch i ldhoo d i s no t suppo r ted by s imi -

l a r a n a l y s e s o f a l l - c a u s e m o r t a l i t y o r s e v e r e m a l a r i a m o r b i d i t y . T h i s i s

impor tan t fo r long- te rm pub l ic hea l th ques t ions su r round ing the implemen ta -

t ion o f in te rven t ions a im ed a t r educ ing p a ras it e cha l l enge .

On e c lea r and unam biguo us pos i t ion i s tha t a ll - cause mor ta l i ty am ong ch i l-

d ren l e s s than 5 yea r s o f age is lowe s t a s one approac hes the

x - y

in te rcep t w i th

t r ansmis s ion in tens ity . An a rea on the e x t r em e le f t o f the x t r ansmis s ion ax i s

p ro bab ly enco m passe s a sha rp in f lec t ion in the ri sks o f s evere o r f a tal d i s ease

o u t c o m e s . O f in t e re s t, t h e r e f o r e , i s h o w l i k e l y I T N s , o r a n y o t h e r c o n t r o l

m e t h o d , w o u l d b e t o r e d u c e t h e p r e v a l e n c e o f in f e c ti o n b e l o w t h is p o i n t ( s e e

F i g u r e 6 ) a n d h o w m a n y p e o p l e l i ve w i t h in a r a n g e o f e n d e m i c i t i e s l ik e l y t o

benef i t m os t f rom th is p ropor t iona l r educ t ion in in fec tion r i sk .

D u r i n g t h e R C T s o f I T N s t h e p r ev a l e n ce o f P. f a l c i p a r u m infect ion in ch i ld-

h o o d w a s re d u c e d b y a s l it tl e a s 7 i n B u r k i n a F a s o ( H a b l u e t z e l e t a l . 1999) ,

and as m uch as 30 in K i l if i, Ke nya (unpub l i shed da ta ). In The Gam bia , a

r a n g e o f r e d u c t i o n s i n i n f e c t i o n p r e v a l e n c e w a s o b s e r v e d b e t w e e n t h e f i v e

m a t c h e d c o m m u n i t i e s f r o m n il t o o v e r 5 0 ( D ' A l e s s a n d r o

e t a l .

1995). In

m any com m uni t i e s loca ted in a reas o f low- to -m odera te t r ansmis s ion in tens ity ,

a 30 -50 r educ t ion in in fec t ion p reva lence w ou ld be su f f i c ien t to p lace ch i ld -

h o o d c o m m u n i t i e s i n t h e c a t e g o r y o f l o w m o r t a l i t y r i s k a n d a r g u a b l y t h e

s u s t a i n e d i m p a c t s o f I T N s a r e l i k e l y to b e l a r g e s t u n d e r s u c h c o n d i t io n s .

Ho we ver , in a reas o f h igh (o r h igher ) t r ansmis s ion such a reduc t ion w ou ld

resu l t in pa ras i t e p reva lences s ti ll abo ve th is th resho ld . In such c i r cum s tances ,

p o t e n t i a l l o n g - t e r m r e a l i g n m e n t o f d i s e a s e r i s k c o u l d l im i t t h e n u m b e r o f

severe d i s ease ep i sod es avo id ed o r lives s aved .




Africa includes an enormous range of transmission conditions from one

infectious bite every 5-10 years to several infectious bites every night (Hay e t

a l .

2000). Preliminary maps of infection risks suggest that relatively few

people live under high transmission conditions. Only 9 of the population of

west Africa and 14 of that of Kenya live in areas with a prevalence of infec-

tion in excess of 70 (Snow

e t a l .

1998b; Kleinschmidt

e t a l .

2001). New

developments in mapping malaria infection risks in Africa should allow better

definition of the location and numbers of people living in areas likely to

achieve maximum gains from different control activities (Rogers

e t a l .

2002).

1 1 C O N C L U S I O N S

The African continent exhibits enormous heterogeneity in both the risks of

infection with P. a l c i p a r u m and death within the first 5 years of life. Variation

in the risks of exposure to infectious agents and mortality forms the rationale

for mathematical approaches to the epidemiology of many disease systems.

However, in contrast to diseases like measles, rubella or several veterinary dis-

eases, where it has been possible to estimate age-structured risks against the

force of transmission, the malaria community's efforts have been hampered by

the lack of reliable quantification of either exposure or disease outcome risks.

Yet, we must begin to draw together the most plausible epidemiological evi-

dence in order to define a public health framework for the likely successes of

existing and new interventions.

This review has provided a digest of some of the issues that have re-

emerged over the last 5 years in relation to the question of how malaria

transmission intensity relates to the pattern, spectrum and magnitude of disease

outcomes in childhood. There are several areas where a level of general agree-

ment can be defined. First, under all conditions of stable transmission the

incidence of a severe clinical outcome following malaria infection declines

rapidly in childhood. However, clinical outcome for the individual may worsen

with increasing age. These two features of clinical malaria are consistent with

the basic principle of endemic stability proposed for other infectious diseases

(Coleman

e t a l .

2001). Second, at a community level the decline in the risk of

a severe disease outcome occurs earlier in life when the frequency of parasite

exposure from birth is greatest (highest transmission intensity). Third, severe

life-threatening malaria morbidity and all-cause mortality during infancy rise

consistently with increasing intensity of transmission and it seems reasonable

to assume that immunologically na'fve infants would benefit from any reduc-

tion in the risk of parasite challenge from any starting point.

What will continue to be contentious is whether or not malaria-specific

and all-cause mortality throughout childhood reach a point of saturation with



TRANSMISSION OF PL SMODIUM F LClP RUM N AFRICA 57

inc reas ing in tens i ty o f tr ansmis s ion . W e be l i eve tha t the da ta p resen ted f rom a

se r i e s o f independen t eco log ica l compar i sons s t rong ly sugges t tha t they do .

F u r t h e rm o r e , e x a m i n a t i o n o f th e d a t a f r o m t ri al s w h i c h h a v e r e d u c e d t h e f re -

q u e n c y o f p a ra s it e e x p o s u r e a m o n g c o h o r t s o f c h il d re n u s i n g I T N s s u g g e s t s

tha t und er cond i t ions o f h igh t r ansm is s ion ea r ly succe s ses o f the in te rven t ion

m a y b e d i l u t e d w i t h d u r a ti o n o f u s e . R e a l i g n m e n t o f t h e s p e e d w i t h w h i c h

ch i ld ren deve lo p func t iona l imm uni ty in the f ace o f new co nd i t ions o f pa rasi t e

cha l l enge f rom b i r th p rov ide s a p laus ib le exp lana t ion .

E a r l y s u c c e s s e s a c h i e v e d b y I T N s u n d e r a l l t r a n s m i s s i o n c o n d i t i o n s a r e

l i k e l y t o b e c o n c e n t r a t e d a m o n g s t y o u n g , i m m u n o l o g i c a l l y n a i v e i n f a n t s , a

g r o u p a t t h e h i g h e st r i sk o f d e a th f r o m b o t h m a l a ri a a n d a w i d e r a n g e o f o th e r

causes , and these e f f ec t s shou ld be sus ta ined . The long - te rm succes s o f ITN s ,

in t e rms o f overa l l reduc t ion in ch i ldhood mor ta li ty , w i l l be g rea tes t w here d i s-

e a s e b u r d e n s a r e h i gh b u t t h e f r e q u e n c y o f p a r a si te e x p o s u r e i s

l o w - t o - m o d e r a t e . F o r t u n a t e l y , n o t w i t h s t a n d i n g t h e n e e d f o r m o r e a c c u r a t e

m app ing o f tr ansmis s ion in tensi t ie s , i t s eem s l ike ly tha t la rge pa r t s o f Af r i ca

fa l l in to th is ca tegory . In a r eas o f h igh t r ansmis s ion , in te rven t ions m ay ha ve

l e s s c h a n c e o f re d u c i n g e x p o s u r e t o th e p o i n t w h e r e o n e w o u l d e x p e c t s u s -

t a ined r educ t ion in overa l l m or ta l i ty th rough ch i ldhood . How ever , th is shou ld

no t l imi t the w idesca le use o f ITNs under a l l t r ansmis s ion cond i t ions fo r a

num ber o f r easons . F i r st , under a l l t r ansmis s ion cond i t ions , the majo r ea r ly

r e d u c t io n i n c h i ld h o o d m o r t a l it y w i ll b e e n o r m o u s l y i m p o r t a n t a n d w i ll g i v e

im petu s to a ll o ther par ts of the m alar ia con tro l s trategy. Seco nd, a l thoug h th is

r ev iew has conce n t r a ted on r e la tionsh ips be twe en t r ansmis s ion and l i fe - th rea t -

en ing m ala ri a , r educ t ion in the m ass ive load o f l e s s s evere d i s ease w i l l have a

m ajo r im pac t o n hea l th s e rv ices in t e rm s o f bo th the co s t s o f t r eat ing m ala r ia

and the deve lopm en t o f d rug r es i s t ance , and i t i s l ike ly tha t th is e f f ec t w i l l be

sus ta ined under a l l t r ansmis s ion cond i t ions . F ina l ly , a l l p r ed ic t ions o f wh a t

m a y h a p p e n w h e n t r a n s m i s s i o n i s r e d u c e d h a v e t o b e q u a l i f i e d b y c a u t i o n

c o n c e r n i n g t h e l i m i ta t io n s o f e c o l o g i c a l c o m p a r i s o n s o n w h i c h s u c h p r e d i c-

t ions a re based . In the end , i t w i l l be the w idesp re ad in t roduc t ion o f succes s fu l

con t ro l measu res tha t w i l l th row m os t l igh t on the r e la t ionsh ip be tw een m ala ri a

t ra n s m i s s io n a n d o u t c o m e .

C K NOWL EDG EMEN T S

T h i s w o r k w a s s u p p o r te d b y t h e W e l l c o m e T r u st U K ) a n d th e K e n y a n M e d i c a l

R e s e a r c h I n s t it u te K E M R I ) . W e a r e g r at e fu l t o a v a r i e ty o f i n d iv i d u a ls w h o

have supp l i ed add i t iona l in fo rmat ion in o rde r to p rov ide more r e l i ab le age -

s t ruc tu red mor ta l i ty and in fec t ion r i sk da ta a s p resen ted in th i s paper . They

i n c lu d e G i l ly M a u d e a n d N i c o la D o l li m o r e N a v r o n g o , G h a n a V A S T




p r o g r a m m e ) , Y u s u f H e m e d A d u l t M o r b i d i t y a n d M o r t a l i ty P r o g r a m m e ,

M i n i s t r y o f H e a l th , T a n za n ia ) , D o n d e S a v i g n y M A R A d a t a c o - o r d i n a ti o n in

T a n z a n ia ) , D e n n i s S h a n k s W a l te r R e e d R e s e a r c h P r o g r a m a t K e r i c h o , K e n y a )

a n d J e a n - F r a n c o i s T r a p e I n s ti tu t d e R e c h e r c h e p o u r le D r v e l o p p e m e n t ,

S e n e g a l ) . T h e a u t h o r s a r e a l s o g r a t e f u l t o J e a n - F r a n c o i s T r a p e a n d E l e n o r

G o u w s f o r th e i r c o m m e n t s o n e a r l ie r p r e s e n ta t io n s o f th e s e d at a. R W S a n d K M

a r e s u p p o r t e d a s W e l l c o m e T r u s t S e n i o r R e s e a r c h F e l lo w s n o s . 0 3 3 3 4 0 a n d

6 3 1 3 4 2 ) . T h i s p a p e r is p u b l i s h e d w i t h t h e p e r m i s s i o n o f th e D i r e c to r , K E M R I .

R E F E R E N E S

Akog beto, M., Modiano, D. and Bosman , A. 1992). M alaria transmission in the lagoon area

of Cotonou, Benin. Parassitologia 34, 147-154.

Atonso, P.L., Lindsay, S.W ., Arm strong-Schellenberg, J.R.M., G omez, P., Hill, A.G., D avid,

P.H., Fegan, G., Cham, K. and Greenw ood, B .M . 1993a). A m alaria control trial using

insecticide-treated bed nets and targeted chemop rophylaxis in a rural area o f The G amb ia,

W est Africa. 2: Mortality and m orbidity from m alaria in the study area. Transactions o f

the Royal Society o f Tropical M edicine a nd Hygiene 87, supplement 2, 13-18.

Alonso, P.L., Lindsay, S.W ., Arm strong-Schellenberg, J.R.M., G om ez, P., Hill, A.G., D avid,

P.H., Fegan, G., Cham, K . and Greenwo od, B .M. 1993b). A malaria control trial using

insecticide-treated bed nets and targeted chem opro phy laxis in a rural area of Th e

Gam bia, West Africa. 6: The impact o f the interventions on m ortality and m orbidity fro m

malaria. Transactions of the Royal Society o f Tropical M edicine a nd Hygiene 87, sup-

plement 2, 37--44.

Anderson, R.M. and May , R.M. 1991). Infectious Diseases of Hum ans: Dynam ics and

Control. Oxford: O xford U niversity Press.

Anker, M., Black, R .E., Coldham, C ., Kalter, H.D., Qu igley, M .A., Ross, D. an d S now , R.W.

1999). A Standard Verbal Autopsy Method fo r Investigating Causes o f Deaths in Infants

and Childhood. Geneva: World Heal th Organization, m imeo graph ed docu men t

WHO/CDS/CSR/ISR/99.4.

Anonym ous 1997). Plagued by cures. The Econom ist 22 Novem ber, 1997 .

Arm strong-Schellenberg, J.R.M., Abdu lla S., Minja H., Nathan, R ., M ukasa, O ., M archant,

T., M ponda, H., Kikum bih, N., Lyimo, E., M anchester, T., Tanner, M. and Len geler, C.

1999). KINE T: a social marketing pro gra m m e of treated nets and net treatmen t for

malaria control in Tanzania, with evaluation o f child health and long-term survival.

Transactions of the Royal Society o f Tropical M edicine a nd Hygiene 93, 225-231.

Baird, J.K. 1998). A ge- dep end en t characteristics o f pro tectio n v. susceptibility to

Plasmodium falciparum. Annals o f Tropical M edicine a nd Parasitology 92, 367-390.

Baird, J.K ., Basri, H .P ., Ba ng s, M .J., Andersen, E.M., Jon es, T.R., Masbar, S.,

Harjosuwarno, S., Subianto, B. and Arbani, P.R. 1993). Age-specific prevalence of

Plasmodium falciparum

among six populations with limited histories of exposure to

endemic malaria. American Journal o f Tropical Medicine and Hygiene 49, 707-719.

Baird, J.K., Masbar, S., Basri, H, Tirtokusumo, S., Subianto, B. and Hoffman, S.L. 1998).

Age-dependent susceptibility to severe disease with primary exposure to Plasmodium

falciparum. Journal o f Infectious D iseases 178, 592-595.

Barnish, G., Mau de, G.H., Bockarie, M.J., Eggelte, T.A. and Greenwo od, B.M . 1993). The

epidemiology o f malaria in southern Sierra Leone. Parassitologia 35 , 14 .



TRANSMISSION OF PL SMODIUM F LClP RUM N AFRICA 59

Bates, C.J., Prentice, A.M ., Paul, A.A . , Prentice, A . , Sutcl iffe, B .A. an d W hitehea d, R.G .

(1982) . Ribof lavin s tatus in infants born in rural Gam bia , and ef fect of a weaning fo od

supplement. Transactions o f the Roy al Socie ty o f Tropical M edicine a nd H ygiene 76,

2 5 3 - 2 5 8

Beier , J .C. , Ki l leen, G .E an d Gi thure , J .I . (1999). En tom olo gic inocu lat ion ra tes and

P l a s m o d i u m f a l c i p a r u m m alaria prevalence in Africa. Am er ican Journal o f T rop ica l

M e d i c in e a n d H y g i e n e 61 , 109-113

Bink a, EN ., Morris, S.S. , Ross, D.A., Arthur, P. and Arye etey, M .E. (1994). Pat terns o f

malar ia morbidi ty and mor ta l i ty in chi ldren in nor thern Ghana. Transactions o f the

Royal Soc i e ty o f Tropica l M edic ine and Hygiene 88 , 381-385 .

Bink a, EN ., Ku jabe, A. , Ad uik, M., W ill iams, L.A . , Lengeler, C . , M aud e, G.H., Arm ah,

G.E. , Kajihara, B. , Ad iam ah, J .H. an d Smith, P.G. (1996). Im pa ct o f permethrin imp reg-

nated bed nets on chi ld mor ta l i ty in Kassena-Nakana dis t r ic t , Ghana: a randomised

con trol led tr ial . Tropical Medicine a nd Internat ional H eal th 1, 147-154.

Bloland, P.B. , Bo riga, D.A., Rue bus h, T.K. , McC orm ick, J .B. , Rob erts, J .M., Olo o, A.J.,

Hawley, W. , Lal , A. , Nahlen, B. and C am pbel l , C.C. (1999). Lon gi tudinal cohor t s tudy

of the epidem iology o f ma lar ia transmiss ion I I . Descriptive epide m iology of malar ia

infect ion and disease am on g yo un g chi ldren. Am er ican Journal o f T ropica l M edic ine

a n d H y g i e n e 60 , 641-648 .

Brad ley , D . J . (1991) . Morb id i ty and mor t a l i t y a t Pa re -Tave ta , Kenya and Tanzan ia ,

195 4-66 ; the ef fects of a per iod o f ma lar ia cont rol . In Disease and Mortal i ty in Sub-

Sah aran Africa. (T .C.G.A. Feacham and D.T. Jamison, eds) , pp. 248-261. Oxford:

Oxford U nivers i ty P ress fo r the W or d Bank .

Bradley, D.J. (1992). Malaria: old infections, cha ng ing epide m iology . Health Transi t ion

R e v i e w 2, supplem entary issue, 137-1 53.

Brink, C.J.H. (1958). Malaria control in the northern Transvaal .

South A f r i can M edica l

Journal 32 , 800-808 .

Brown, E (1997). Picking holes in the net . N ew Scientist, 16-1 7 Au gust , 1997.

Carm e, B. , Gui l lo du Boda n, H. and Lal lenat, M . (1992) . In fant and chi ld mor ta l i ty and

mala r i a i n the Co ngo . The t r end in t he suburbs o f Brazzav i ll e be tween 1981-1988 .

Tropical M edic ine a nd Parasi tology 43 , 177-180 .

Cattanni , J .A. , Moir , J .S. , Gibson, ED ., Ginny, M., Pain t , J . , Davidson, W . and Alpers, M .E

(1985). Smal l - a r ea va r ia t ions i n t he ep ide mio logy of mala r i a i n Mad ang P rov ince .

Papua New Guinea M edica l Journal 29, 11-17.

Chan dram ohan , D. , Green wo od, B.M . and Cox, J. (2001). Relationship betwee n malar ia

end em icity and ac ute febri le i llness m ortal i ty in children. Bul le t in o f the World He al th

Organization 79 , 375-376 .

Co lem an, EG ., Perry, B.D . and W oolh ouse , M.E.J. (2001). End em ic stabil ity - a veterinary

idea applied to hum an pub lic heal th. L a n c e t 357 , 1284-1286 .

Co osem ans, M. (1987) . Rech erche ~pid~miologique sur le palud isme dan s la plaine de la

Rusizi et dans l Imbo Su d (R~publique du Burundi) . Evaluation des m oyen s de lut te. P h D

thesis, Universi t6 Catholique de Louvain, Belgium.

D A lessandro , U . and Coosem ans , M. (1997). Concerns on long- te rm e f f icacy of an i nsec -

ticide treated bed net. Parasitology Today 13, 124.

D A less an dro , U. , Olaleye, B.O. , Mc Gu ire, W ., La nge rock , E, B ennett, S. , Aikins, M.K.,

Tho mso n, M.C. , Cham , M.K., Cham , B.A. and Greenw ood, B.M. (1995) . Mor ta l i ty and

mo rbidi ty f rom malar ia in Gam bian chi ldren af ter int roduct ion of an impregnated bed

ne t p rogramme. L a n c e t 345 , 479-483 .

Delacollette, C. and Barutw ana yo , M . (1993). M ortal it6 et morbidi t6 aux jeu nes a ges dans

une r t g ion h pa lud i sme hyp erendtm ique s t ab le , com m une de Nya nza Lac , Im bo Sud ,

Burundi. Bullet in de la Soci~t~ de Pathologie E xotiqu e 86, 1-7.




D e la c o l l e t t e , C . , V a n d e r S tu y f t , P., M o l ima , K . , D e la c o l l e t te -K e b ru n , C . a n d W 6 ry , W.

(19 8 9) . I~tud e d e l a mo r ta l i t6 g lo b a le e t d e l a mo r ta l i t6 au p a lu d i s m e d a n s l e K iv u mo n -

tagneux , Za i re .

Revue Epid~miologique et Santd-Publique

37 , 161-166 .

De laco l le t te , C . , Van de r S tuyf t , P ., M ul im na , K . , Hendr ix , L . a nd W6ry , W. (1990) . Ind ic ies

p a lu d o m e t r iq u e s s e lo n a g e e t s e lo n l e s s a i s o n s d a n s l a z o n e d e s a nt6 d e K a ta n a , a u

K i v u , M o n t a g n u e x , Z a i r e .

Annales de la Soci~t~ Belge de M~dicine Tropicale

70

2 6 3 - 2 6 8 .

Do bson , M .J . , M alowan y , M . and Snow, R.W. (2000) . M ala r ia con tro l in Eas t Afr ica : the

K a m p a l a co n f e r en c e a n d t h e P a r e- T a v et a S c h e m e - a m e e t i n g o f c o m m o n a n d h i g h

ground .

Parassitologia

4 2 , 1 4 9 -1 6 7 .

E l lma n , R . , M a x w e l l , C . , F in c h , R . a n d S h a y o , D . (19 98 ). M a la r i a a n d a n a e mia a t d i f f e re n t

a l t i t u d e s in Mu h e z a d i s t r i c t o f T a n z a n ia : c h i ld h o o d mo r ta l i ty in r e l a t io n to l e v e l o f

e x p o s u re to in fe c tio n .

Annals of Tropical Medicine and Parasitology

9 2 , 7 4 1 -7 5 3 .

E y le s , D .E . a n d Y o un g, M .D . (1 9 5 1 ) . T h e d u ra t io n o f u n t re a te d o r in a d e q u a te ly t r e a te d


in fec t ions in the hum an hos t .

Journal of the National Malaria

Society

10 , 327-336 .

G a m h a m , P .C .C . (1 9 4 9 ). M a la r i a l imm u n i ty in A f r i c a n s : e f f e c ts in in fa n c y a n d e a r ly c h i ld -

hood .

Annals of Tropical Medicine and Parasitology

4 3 , 4 7 -6 1 .

Gazin, P. (1990). Le

paludisme au Burkina Faso: dtude ~pid~miologique de la transmission

des indicies parasitologiques de la morbiditY de la l~talit~.

PhD thes is , Univers i t6 de

M o n tp e l l i e r 1 , F ra n c e .

G em aa t , H.B.P .E . , D echer ing , W .H.J .C. and Voorhoeve , H.W .A. (1998) . Cl in ica l ep id em i-

o l o g y o f p a e d i a t r i c d i s e a s e s a t N c h e l e n g e , n o r t h - e a s t Z a m b i a .

Annals of Tropical

Paediatrics

18 , 129-138 .

G i th e k o , A .K . , M b o g o , C .N .M. , C u r t i s , C .F . , L in e s , J . a n d L e n g e le r , C . (1 9 9 6 ).

E n t o m o l o g i c a l m o n i t o r i n g o f l a r g e - s c a l e v e c t o r c o n t r o l i n t e r v en t io n s .

Parasitology

Today

12, 127-128.

G o o d ma n , C .A . , C o le ma n , P .G . a n d M i l l s , A . J . (1 99 9) . C o s t -e f fe c t iv e n e s s o f m a la r i a c o n -

t ro l i n s u b -S a h a ra n A f r i c a .

Lancet

3 5 4 , 3 7 8 -3 8 5 .

Greenb erg , A.E . and L obe l , H.O. (1990). M orta l i ty f rom

Plasmodiumfalciparum

m a la r i a in

t r a v e l l er s fr o m t h e U n i t e d S t a t es , 1 9 5 9 - 1 9 8 7 .

Annals of Internal Medicine

113,

3 2 6 - 3 2 7 .

G re e n b e rg , A .E . , N tu mb a n z o n d o , M. , N tu la , N . , Ma w a , L . , H o w e l l , J . a n d D a v a c h i , F .

(19 8 9) . H o s p i t a l -b a s e d s u rv e i l l a n c e o f ma la r i a - re l a t e d p a e d ia t r i c mo rb id i ty a n d m o r ta l -

i ty in Kinshasa , Za i re .

Bulletin of the World Health Organization

67 , 189-196 .

G re e n w o o d , B .M . (19 97 ). M a la r i a t r a n s mis s io n a n d v e c to r c o n t ro l . Parasitology Today13,

9 0 - 9 2 .

G re e n w o o d , B .M. , B ra d le y , A .K . , G re e n w o o d , A .M. , B y a s s , P ., J a mm e h , K . , Ma rs h , K . ,

T u l lo c k , S . , O ld f i e ld , F .S . J . a n d H a y e s , R . J . (1 9 8 7 ) . Mo r ta l i ty a n d mo rb id i ty f ro m

ma la r i a a mo n g c h i ld re n in a ru ra l a re a o f T h e G a m b ia , W e s t A f r i c a .

Transactions of the

Royal Society of Tropical Medicine and Hygiene

8 1 , 4 7 8 - 4 8 6 .

G re e n w o o d , B .M . , G re e n w o o d , A .M. , B ra d le y , A .K . , S n o w , R .W. , B y a s s , P ., H a y e s , R . a n d

N j i e , A .B .H . (19 88 ). A c o m p a r i s o n o f tw o d ru g s t r a te g ie s fo r th e c o n t ro l o f m a la r i a

w i t h i n a P r i m a r y H e a l t h C a r e P r o g r a m m e i n T h e G a m b i a , W e s t A f r i c a .

Lancet

i i ,

1121-1127.

G u p ta , S . , S n o w , R .W. , D o n n e l ly , C . , Ma rs h , K . a n d N e w b o ld , C . (1 9 9 9 ) . Immu n i ty to

s e v e re ma la r i a i s a c q u i re d a f t e r o n e o r tw o e x p o s u re s .

Nature Medicine

5 , 3 4 0 -3 4 3 .

H a b lu e tz e l , A . , D ia l lo , D .A . , E s p o s i to , E , L a m iz a n a , L . , P a g n o n i , F . , L e n g e le r, C . , T ra o re ,

C . a n d C o u s e n s , S .N . (1 9 9 7 ) . D o in s e c t i c id e - t r e a te d c u r t a in s r e d u c e a l l - c a u s e c h i ld

mo r ta l i ty in B u rk in a F a s o ?

Tropical Medicine and International Health

2 , 8 5 5 -8 6 2 .

H a b lu e tz e l , A . , C u rz in , N . , D ia l lo , D .A . , N e b ie , I . , B e le m, S . , C o u s e n s , S .N . a n d E s p o s i to ,



TRANSMISSION OF P L S M O D I U M F L C l P R U M IN AFRICA 26

E (1 9 9 9) . In s e c t i c id e - t r e a te d c u r t a in s r e d u c e th e p re v a le n c e a n d in t e n s i ty o f ma la r i a

in fe c t io n in B u rk in a F a s o .


4 , 5 5 7 -5 6 4 .

H a y , S . I . , T o ome r , J .F ., R o g e rs , D . J . a n d S n ow , R .W. (2 0 0 0 ). A n n u a l e n to mo lo g ic a l in o c u -

l a t io n r a t e s (E IR ) a c ro s s A f r i c a : l i t e ra tu re s u rv e y , in t e rn e t a c c e s s a n d re v ie w .

Transactions of the Royal Society of Tropical Medicine and Hygiene

94 , 113-127 .

Hi l l , A.V.S . (1992) . M ala r ia res is tance genes : a na tu ra l se lec t ion .

Transactions of the Royal

Society of Tropical Medicine and Hygiene

86 2 2 5 - 2 2 6 .

Ib ra h im , M.M . , O m a r , H .M. , P e r s o n , L .A . a n d W a l l , S . (1 99 6) . C h i ld mo r ta l i ty in a c o l -

l a p s in g A f r i c a n S o c ie ty .

Bulletin of the World Health Organization

7 4 , 5 4 7 -5 5 2 .

J a ffa r, S . , L e a c h , A . , G re e n w o o d , A .M. , J e p s o n , A . , Mu l l e r , O . , O ta , M.O .C . , B o ja n g , K . ,

O b a ro , S . a n d G re e n w o o d , B .M. (1 9 9 7 ). C h a n g e s in th e p a t te rn o f in fa n t a n d c h i ld h o o d

mo r ta l i ty in U p p e r R iv e r D iv i s io n , T h e G a m b ia , f ro m 1 98 9 to 1 99 3 .

Tropical Medicine

and International Health

2 , 2 8 -3 7 .

Je l l i f fe , E .ED. and Je l l i f fe , D.B. (1963) .

Plasmodium malariae

i n U g a n d a n c h i ld re n . I :

p r e v a l e n c e i n y o u n g c h i l d r e n i n r u r a l c o m m u n i t i e s .

American Journal of Tropical

Medicine and Hygiene

12 , 296-297 .

K h a n , K . , T o l lma n , S .M. , G a re n n e , M. a n d G e a r , J .S .S . (1 9 9 9 ) . Wh o d ie s f ro m w h a t?

D e te rm in in g c a u s e o f d e a th in S o u th A f r i c a s ru ra l n o r th -e a s t.

Tropical Medicine and

International Health

4 , 4 3 3 - 4 4 1 .

K id a n e , G . a n d Mo r ro w , R .H . (2 0 0 0 ) . T e a c h in g mo th e r s to p ro v id e h o me t r e a tme n t o f

ma la r i a in T ig ra y , E th io p ia : a r a n d o m is e d t r i a l.

Lancet

3 5 6 , 5 5 0 -5 5 5 .

K le in s c h mid t , I . , O mu mb o , J . , B r i e t , O . , v a n d e G ie s e n , N . , S o g o b a , N . , Me n s a h , N .K . ,

W inderm ei je r , P ., M oussa , M . and Teuscher, T . (2001) . A n em pir ica l ma la r ia d is t r ibu t ion

ma p fo r W e s t A f r i c a .


6 , 7 7 9 -7 8 6 .

L a n g fo rd , C .M. (1 9 9 6 ) . R e a s o n s fo r th e d e c l in e in mo r ta l i ty in S r i L a n k a imm e d ia te ly

a f t e r th e S e c o n d W o r ld Wa r : a r e -e x a min a t io n o f th e e v id e n c e .

Health Transition Review

6 , 3 -2 3 .

L e n g e le r , C . (1 9 9 8 ) .

Insecticide Treated Bednets and Curtains for Malaria Control

Cochrane Review).

O x fo rd : U p d a te S o f tw a re , T h e C o c h ra n e L ib ra ry , i s s u e 3 .

Lenge le r , C . , Smith , T .A. and Armstron g-Sche l lenb erg , J . (1997). Focu s on the e f fec t o f bed-

n e t s o n m a la r i a mo rb id i ty a n d m o r ta l ity .

Parasitology Today

13, 123.

L e n g e le r , C ., A rms t ro n g -S c h e l l e n b e rg , J .R .M. , D A le s s a n d ro , U . , B in k a , E a n d C a t t a n i , J .

(1 9 9 8 ). R e la t iv e v e r s u s a b s o lu te r i s k o f d y in g re d u c t io n a f t e r u s in g in s e c t i c id e - t r e a te d

n e t s f o r m a l a r i a c o n t r o l i n A f r i c a .


3 ,

2 8 6 - 2 9 0 .

L in d s k o g , U . , L in d s k o g , E , C a r s t e n s e n , J ., L a r s s o n , Y . a n d G e b re -M e d h in , M. (1 9 8 8 ).

C h i ld h o o d m o r ta l i ty in r e l a t io n to n u t r i t io n a l s ta tu s a n d w a te r s u p p ly - a p ro s p e c t iv e

s tu d y f ro m ru ra l Ma la w i .

Acta Paedatrica Scandinavica

7 7 , 2 6 0 -2 6 8 .

L y im o , E .O . , Ms u y u , E H .M . , R w e g o s h o ra , R .T . , N ic h o l s o n , E .A . , M n z a v a , A .E .E , L in e s ,

J .D . a n d C u r t i s , C .E (1 9 9 1) . T r i a l o f p y re th ro id imp re g n a te d b e d n e t s in a n a re a o f

T a n z a n ia h o lo e n d e m ic fo r ma la r i a . P a r t 3: e f f e c ts o n th e p re v a le n c e o f m a la r i a p a ra -

s i taem ia and fever.

Acta Tropica

49 , 157-163 .

M a c D o n a l d , G . ( 1 9 5 7 ) .

The Epidemiology and Control of Malaria.

L o n d o n : O x f o r d

U n iv e r s i ty P re s s .

M arsh , K. and Snow, R.W. (2000) . Ma la r ia t ransm iss ion and m orb id i ty .

Parassitologia

41 ,

2 4 1 - 2 4 6 .

M b o g o , C .N .M . , S n ow , R .W. , K h a m a la , C .E M . , K a b i ru , E.W., O u ma , J .H . , G i th u re , J . I. ,

M arsh , K. and Be ie r , J .C . (1995) . R e la t ionsh ips be tw een

Plasmodiumfalciparum

t rans -

mis s io n b y v e c to r p o p u la t io n s a n d th e in c id e n c e o f s e v e re d i s e a s e a t n in e s i t e s o n th e

K e n y a n c o a s t .

American Journal of Tropical Medicine and Hygiene

5 2 , 2 0 1 -2 0 6 .

Mc G re g o r , I .A . (1 9 6 5 ) . T h e p a s s iv e t r a n s fe r o f h u ma n immu n i ty .

American Journal of




Tropical M edicine a nd Hyg iene 1 3 , 2 3 7 -2 3 9 .

M e ts e la a r , D . a n d V a n T h e i l , P .M. (1 9 5 9 ) . C la s s i f i c a t io n o f m a la r i a .

Tropical and

Geographical Medicine

11, 157-161.

Mi rz a , N .M. , Ma c h a r i a , W.M. , Wa fu la , E .M. , A g w a n d a , R . a n d O n y a n g o , F .E . (1 9 9 0 ) .

M o r t a l i t y p a tt e r n s i n a r u r a l K e n y a c o m m u n i t y . East Afr ican M edical Journal 67 ,

8 2 3 - 8 2 9 .

M o d ia n o , D . , S i r ima , B .S . , S a w a d o g o , A . , S a n o u , I ., P a re , J . , K o n a te , A . a n d P a g n o n i , F .

(19 98 ). S e v e re ma la r i a in B u rk in a F a s t : i n f lu e n c e o f a g e a n d t r a n s mis s io n l e v e l o n

c l in ica l p resen ta t ion .

American Journal o f Tropical Med icine an d Hygiene

5 9 , 5 3 9 -5 4 2 .

M o lb a k , K . , A a b y , P ., In g h u lt , L . , H o j iy n g , N . , G o t t sc h a u , A . , A n d e rs e n , H . , B r in k , L . ,

Gans ted , U. , Pe rm in , A. , Vol lmer , A. and da S i lva , A.P . (1992). Pe rs is ten t and acu te d ia r -

rh o e a a s th e l e a d in g c a u s e s o f c h i ld mo r ta l i ty in u rb a n G u in e a -B is s a u . Transactions of

the Royal Society o f Tropical M edicine a nd Hygiene

8 6 , 2 1 6 -2 2 0 .

M o l in e a u x , L . (1 98 5) . T h e imp a c t o f p a ra s i t i c d i s e a s e s a n d th e i r c o n t ro l , w i th a n e mp h a s i s

o n ma la r i a a n d A f r i c a . In :

Health Policy Social Policy and Mortality Prospects

(J.

V a l l in an d A .D . L o p e z , e d s ) , p p . 1 3 -4 4 . L ie g e : O rd in a E d i t io n s .

Mol ineaux , L . (1997) .


m a l a r i a : s o m e e p i d e m i o l o g i c a l i m p l i c a -

t io n s o f p a ra s i t e a n d h o s t d iv e r s i ty .

Annals of Tropical Medicine and Parasitology 90

3 7 9 - 3 9 3 .

M tango , ED .E. and Neu vians , D. (1986). A cu te resp i ra to ry in fec t ions in ch i ld ren under f ive

y e a r s. C o n t ro l p ro je c t in B a g a m o y o d i s t ri c t , T a n z a n ia . Transactions of the Royal Society

of Tropical Medicine and H ygiene

8 0 , 8 5 1 -8 5 8 .

Nevi l l , C .G . , Som e, E .S . , Mu ng a l a , V.O. , M utemi , W. , New, L . , M arsh , K. , Lenge le r , C . and

S n ow , R .W. (1 9 9 6 ) . In s e c t i c id e t r e a te d b e d n e t s r e d u c e m o r ta l i ty a n d s e v e re mo rb id i ty

f ro m m a la r i a a mo n g c h i ld re n o n th e K e n y a n c o a s t.

Tropical Med icine and International

Health

1 , 139-146 .

Nj oro ge, E.P. (1987).

Com munity parasite survey mo nthly report.

N a i ro b i , K e n y a : D iv i s io n

o f V e c to r B o rn e D is e a s e s , M in i s t ry o f H e a l th .

Pasvo l , G. , W ea thera l l , D.J . and W ilson , R .J .M. (1977). Effec ts o f foe ta l hemo glob in on sus -

c e p t ib i l i t y o f r e d c e l l s to

Plasmodiumfalciparum. Nature

2 7 0 , 1 7 1 -1 7 3 .

P re mj i , Z . , N d a y a n g a , P . , S h i f t , C . , Min ja s , J . , L u b e g a , P . a n d Ma c L e o d , J . (1 9 9 7 ) .

C o m mu n i ty b a s e d s tu d ie s o n c h i ld h o o d mo r ta l i ty in a ma la r i a h o lo e n d e mic a re a o n th e

Tanzan ian coas t . Acta Tropica 63 , 101-109 .

Rog ers , D.J . , Randolp h , S .E . , Snow, R.W . and H ay , S . I . (2002) . Sa te l l i te im age ry in the

s tu d y a n d fo re c a s t o f m a la r i a .

Nature

4 1 5 , 7 1 0 -7 1 5 .

S a c h s , J. a n d M a la n e y , P . (2 0 0 2 ). T h e e c o n o m ic a n d s o c ia l b u rd e n o f ma la r i a . Nature 415,

6 8 0 -6 8 5 .

S a lu m, E M . , W i lk e s , T .J ., K iv u mb i , K . a n d C u r t i s , C .E (19 94 ). M o r ta l i ty o f u n d e r f iv e s in

a ru ra l a re a o f h o lo e n d e m ic ma la r i a t r an s mis s io n . Acta Tropica 5 8 , 2 9 -3 4 .

S c h w a r tz , E . , S a d e tz k i , S ., Mu ra d , H . a n d R a v e h , D . (2 0 0 1 ) . A g e a s a r i s k f a c to r fo r s e v e re

Plasmodium fa lc iparum m a l a r i a a m o n g n o n - i m m u n e p a t ie n t s. Clinical Infectious

Diseases

3 3 , 1 7 7 4 -1 7 7 7 .

Sebox a , T . and Snow, R.W. (1997). Ep idem io log ica l fea tu res o f severe paed ia t r ic m a la r ia in

H u m e ra d i s t r i c t , n o r th w e s te rn E th io p ia .

Ea st African M edical Journal

7 4 , 7 8 0 -7 8 3 .

S h a n k s , G . D . , B i o m o n d o , K . , S no w , R . W . a n d t h e H i g h l a n d M a l a r i a G r o u p ( 1 9 9 9 ) .

E p i d e m i o l o g y o f m a l a r i a i n a h i g h l a n d t e a p l a n t a t io n i n w e s t e r n K e n y a .

Amer ican

Journal o f Tropical Medicine and Hygiene

61 , supp lem ent , 364 [abs t rac t ] .

S h a n k s , G .D . , B io mo n d o , K . , H a y , S T a n d S n ow , R .W. (2 0 0 0 ). C h a n g in g p a t t e rn s o f c l in -

i c a l ma la r i a s in c e 1 96 5 a m o n g a t e a e s t a t e p o p u la t io n lo c a te d in th e K e n y a n h ig h la n d s .

Transactions of the Royal So ciety o f Tropical Med icine an d Hygiene 9 4 2 5 3 - 2 5 5 .

Sh if t , C .J . , Min jas , J .N. , Ha l l , T . , Hunt , R .H. and Lyimo, E .S . (1995) . Measurement o f



TRANSMISSION OF

PL SMODIUM F LClP RUM

N AFRICA 63

malaria infection potential of anopheline mosq uitoes sam pled by light trapping indoo rs

at Bag am oyo , Tanzania. Medical and Veterinary Entomology 9, 256-262.

Slutsker, L., Taylor, T.E., Wirima, J. and Steketee, R. (1994). I n hospital morbid ity and mo r-

tality due to malaria-associated severe anaem ia in two areas o f Malaw i with different

patterns of mala ria infection. Transactions of the Royal Society o f Tropical Medicine and

Hygiene 88 548-551.

Sm edm an, L., Lindeberg, A., Jeppesso n, O. and Zetterstrom, R. (1983). Nutritional status

and measles: a community study in Guinea Bissau. Annals of Tropical Paediatrics 3

169 176.

Smith, A. and Pringle, G. (1967). Malaria in the Taveta area of Kenya and Tanzania. V:

Transmission eight years after the spraying period. East African Medical Journal 44,

469-473.

Sm ith, T.A., Charlw ood, J.D., Kihonda, J., M wa nkusye, S., Billingsley, P., Meuwissen, J.,

Lyim o, E., Takken, W ., Teuscher, T. and Tanner, M. (1993). A bsen ce o f seasonal varia-

tion in malari a parasitaemia in an area of intense seasonal transmission. Acta Tropica

54,

55-72.

Sm ith, T.A., Schellenberg, J.R.M.A. and Hayes, R. (1994). Attributable frac tion estimates

and case-definitions for malaria endem ic areas. Statistics in Medicine 13, 2345-2358

Sm ith T.A., Leuenberger, R. and Lengeler, C. (2001). Child mo rtalit y and ma laria trans-

mission in Africa. Trends in Parasitology 17, 145-149.

Snow, R.W. and Marsh, K. (1995). Will reducing Plasmodium falciparum transmission

alter mortality am ong African children? Parasitology Today 11, 188-190.

Snow, R.W., Bastos de Azeved o, I., Low e, B.S., Kabiru, E.W., Nevill, C.G., Mw ankus ye, S.,

Kassiga, G., Marsh, K. and Teuscher, T. (1994a). Severe childhood malaria in two areas

of marked ly different falciparum m alaria transmission in East Africa.

Acta Tropica

57,

289-300.

Snow, R.W., Mu ng a ta, V.O., Forster, D. and M arsh, K. (1994b). The role o f the district hos-

pital in child survival at the Kenyan coast. African Journal o f Health Sciences 1, 71-7 5.

Snow, R.W., Omumbo, J.A., Lowe, B., Molyneux, S.M., Obiero, J.O., Palmer, A., Weber,

M.W., Pinder, M., Nahlen, B., Obonyo, C., Newbold, C., Gupta, S. and Marsh, K.

(1997). R elation between severe malaria morbid ity in children and level of Plasmodium

falciparum transmission in Afri ca. Lancet 349, 1650-1654.

Snow, R.W., Nahlen, B., Palmer, A., Donnelly, C.A., Gupta, S. and Marsh, K. (1998a). Risks

of severe malaria among African infants: direct evidence of clinical protection during

early infancy. Journal o f lnfectious Diseases 177, 819-822.

Snow, R.W., Gouw s, E., Om um bo, J., Rapuoda, B., Craig, M.H., Tanser, EC., le Sueur, D.

and Oum a, J. (1998b). Mo dels to predict the intensity of Plasmodiumfalciparum trans-

mission: applications to the burden of disease in Kenya. Transactions of the Royal

Society o f Tropical Medicine and Hygiene 92, 601-606.

Spencer, H.C., Kaseje, D.C.O., M osley, W.H., Sempebwa, E.K.N., Houng , A.Y. and Roberts,

J.M. (1987). Im pact on mortality and fertility o f a commu nity-bas ed malaria control pro-

gram me in Saradidi, Kenya. Annals of Tropical Medicine and Parasitolology 81, 36--45.

Tanzan ia (1997). Policy implications o f adult morbidity and mortality: end o f phase 1. Dar

es Salaam, Repu blic o f Tanzania: Ministry o f Health.

Tho mso n, M.C., D Ale ssa ndr o, U., Bennett, S., Connor, S.J., Langer ock, P., Jawara, M.,

Todd., J. and Greenwood, B.M. (1994). Malaria prevalence is inversely related to vector

density in the Gambia, West Africa. Transactions of the Royal Society of Tropical

Medicine and Hygiene 88, 638-643.

Trape J.E (1997). Which strategy for malaria control in Africa? Parasitology Today 13,

t.25-126.

Trape, J.F. and Rogier, C. (1996). Com batin g malaria morbidi ty and mortalit y by reduc ing




transmission. Parasitology Today 12 , 236-240 .

Trape, J .E, Q uinet, M.C. , N zing oula, S. , Sen ga, P., Tchichelle, E , C arm e, B. , Candito, D . ,

M aya nda , H. and Zoulani, A . 1987). Malaria and urbanisat ion in Central A frica: the

exam ple o f Brazzavil le. Part V. Pern icious at tacks and m ortal ity. Transactions of the

Royal Society o f Tropical Med icine an d Hygiene 81, supplement 2, 34--42.

Trape, J .E, P ison, G. , Preziosi , M .E, En el , C. , D esg rres d u Lou , A. , Del Au nay , V. , Samb,

B. , Laga rde, E . , M olez, J .E and S imo ndon , E 1998). Im pac t of chloroqu ine resi stance

on malaria mortal i ty. Com ptes Rendus de l Acadgm ie des Sciences, P aris, S~rie III,

321, 689-69 7 .

Van den B roec k, J . , Eeckels, R. and Vuylsteke, J . 1993). Influ enc e o f nutri tional status on

child m ortal i ty in rural Zaire. Lancet 341, 1491-1495.

Van den Ho m berg , J . 1994) . M alarial Anaem ia in Infants and Y oung Children from

M orogoro Region in Tanzania. Epidemiology and Clinical Aspects. MSc thes is , London

Scho ol of Hyg iene and Tropical M edicine , UK .

VA ST Gh ana vi tamin A supplementat ion t reatment s tudy team ) 1993). Vi tamin A sup-

plementation in north ern Gh ana: effects on cl inic at tendance, hospital adm issions and

child mo rtality. Lancet 342, 7-12.

Velema, J .E, Alihonou, E.M., Chippaux, J .E, van Boxel , Y. , Gbedji , E. and Adegbini , R.

1991a). M alar ia m orbidi ty and m or ta l i ty in chi ldren under three years of age on the

coas t o f Benin , W es t Af r ica . Transactions of the Royal Society o f Tropical Med icine an d

Hygiene 85, 430--435.

Velema, J .E , Al ihonou, E .M., Ga ndaho , T . and Hou nye, E 1991b). C hi ldho od mo r ta l ity

am on g users and non-users o f pr imary heal th care in a rural W est Afr ican com mu ni ty.

International Journa l o f Epidemiology

20 , 474 -479 .

Vella, V. , Tomk ins, A. , Nid ku, J . and Marshall , T . 1992). D eterminants o f chi ld mo rtal i ty

in south west Uganda. Journal o f Biosocial Science 24, 103-112.

WHO 1950) . Re po rt o f the M alaria C onference in Equatorial Africa. Geneva: Wor ld

He alth Organizat ion, Technical R epo rt Series, no. 38.

W ilson, D.B. 1949). O n the presen t and future m alaria outlook in East Africa. Ea st African

Medical Journal 26 , 378-385 .

Wilson, D.B., Ga rnham , EC .C. and Swellengrebel, N.H. 1950). A review o f hyp eren-

dem ic malaria. Tropical Diseases Bulletin 47 , 677-698 .

Yam agata, Y. 1996 ). Final Report: Malaria Control in the United Republic of Tanzania

(1993-1996). Re por t by Japanese International Co -operat ion Ag enc y to M inis t ry of

Health, Dar-es-Salaam, Tanzania.



Cytokine Mediated Host Responses during

Schistosome Infections; Walking the Fine Line

between Immunological Control and

Immunopathology

Karl F. Ho f fm ann 1 Th om as A . Wy nn 2 and Dav id W. Dun ne 1

~Department o f Pathology University o f Cambridge Tennis Court Road

Cambridge CB2 1QP UK

2Laboratory o f Parasitic Diseases lmmunobiology Section Schistosomiasis

Immunology and Pathology Unit 50 South Drive Rm 6154 M SC 8003

Bethesda M D 20892 USA

A b s tr ac t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 66

1. I n tr o d uc t io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 66

2. S c h i st o s o m ia s i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 68

2.1. B a c k g ro u n d . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 68

2.2. T h e e g g a n d t h e g r a n u l o m a . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 69

2.3 . C o n c e p t o f T h l / T h 2 d i c h o t o m y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271

3 . I nduc t i on Regu la t i on and Consequ ences o f Hos t -M ed ia ted Type -2 Imm une

Responses du r ing I n fec ti on w i t h

ch i s tosom a m anso n i

. . . . . . . . . . . . . . . . . . . 2 7 2

3 .1 . Type -2 imm uno log i ca l r esponses dom ina te du r ing he lm in th i n fec t i ons . . 272

3 .2 . I nduc t i on o f t ype -2 -assoc ia ted imm une responses du r ing S . m a n s o n i

i nf e ct io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 76

4. D i s ti n ct F o rm s o f S c h i s t o s o m e - M e d i a t e d I m m u n o p a t h o l o y c a n b e I n d u ce d

d u r in g I nf ec ti on . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 83

4.1. L i fe - t hr e a te n i n g e g g - i n d u c e d i m m u n o p a t h o l o g y d o e s n o t d e v e l o p i n m o s t

I n fe c te d h u m a n s o r e x p e r i m e n t a l a n i m a l m o d e l s . . . . . . . . . . . . . . . . . . . . . 2 83

4 .2 . D e v e l o p m e n t o f s e v e re i m m u n o p a t h o l o g y d u r i n g s c h i s to s o m i a s i s is

l i nked to IL -10 and assoc ia ted w i t h i napp rop r ia te h igh l y skewed o r

u n c o n tr o ll a b le i m m u n e r e sp o n se s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 85

5. C o n c lu s io n s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 96

A c k n o w l e d g e m e n ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 96

R e fe re n ce s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 96

A D V A N C E S I N P A R A S I T O L O G Y V O L 5 2

Copyright ©

2002 Elsevier Science Ltd

0 0 6 5 3 0 8 X ll rights of reproduction in any form reserved



2 6 6 K F H O F F M A N N E T A L

A B S T R A C T

M o s t h e lm i n t h i n f e ct i o n s o f h u m a n s a n d a n im a l s i n d u c e s i m i la r i m m u n e

r e s p o n s e s , w h i c h a r e c h a r a c te r i se d b y t h e p r o d u c t i o n o f T h 2 - a s s o c i a t e d

cyto kine s ( in ter leukin ( IL)-4 , IL-5 , IL-9 , IL-10, IL-1 3) and a nt ibod ies ( IgG 1 -

m o u s e , I g G 4 - m a n , I g E - b o t h ). T h i s t y p e - 2 - b i a s e d i m m u n e p h e n o t y p e g e n -

e r a l ly p e r s i s ts f o r t h e d u r a t i o n o f t h e i n f e c ti o n . A l t h o u g h s i m i l a r t y p e s o f

immune r esponses a re a l so t r iggered du r ing a l l e rgy , a topy and anaphy lax i s ,

c h r o n i c h e l m i n t h - i n d u c e d t y p e - 2 - a s s o c i a t e d re s p o n s e s a r e u s u a l l y h e l d i n

check b y appropr ia te ly r egu la ted con t ro l mecha n i sms tha t limi t the des t ruc t ive

p o t e n t i a l o f p r o l o n g e d c y t o k i n e b i a s . A m o n g n u m e r o u s r e p o r t e d a c t i v i t i e s ,

h e l m i n t h - i n d u c e d t y p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s h a v e b e e n l i n k e d t o

the expu l s ion o f gas t ro in tes tina l nem atodes and the fo rma t ion o f c i r cum ova l

g ranu lomas du r ing s ch i s tosomias i s . However , wha t happens when th i s h igh ly

r e g u l a t e d , a n d o f t e n b e n e f i c i a l , t y p e - 2 i m m u n e r e s p o n s e b e c o m e s c h r o n i c ,

improp er ly con t ro ll ed , o r exagg era ted du r ing he lmin th in fec tions? U s ing s ch i s -

t o s o m i a s i s a s a m o d e l d i s e a s e , w e d e s c r i b e t h e l e t h a l c o n s e q u e n c e s o f

inappropr ia te imm une r esponse induc t ion b y r ev iewing the l it e ra tu re genera ted

f rom exper imen ta l an imal s tud ies and human ep idemio log ica l inves t iga t ions .

D e v e l o p m e n t o f s e v e r e a n d n o n - o v e r la p p i n g i m m u n o p a t h o l o g i c a l p h e n o t y p e s

wi l l be d i s cus sed in the con tex t o f imm une dev ia t ion and in the s e t ting o f

ch ron ic and /o r hyper -po la r i s ed cy tok ine env i ronmen ts .


P a r a si ti c w o r m i n f ec t io n s c a u s e d m a i n l y b y o r g a n i s m s c o n t a i n e d w i t h in t h e

P h y l a P l a t y h e l m i n t h e s a n d N e m a t o d a r e m a i n o n e o f t h e m a j o r c a u s e s o f

hum an m orb id i ty and mor ta l i ty in the deve lop ing wor ld today . These in fec t ions

a r e s o c o m m o n t h at r e c e n t s u m m a r ie s o f t he w o r l d w i d e p r e v a l en c e o f al l

m a j o r h u m a n h e l m i n th d i s e a s e s h a v e s h o w n t h at th e r e a r e m o r e t h a n e n o u g h

ex i s t ing in fec t ions fo r eve ry l iv ing pe r son to ha rbour a t l eas t one pa ras i t e i f

w o r m i n f e ct i o n s w e r e s p r e a d e v e n l y a c r o s s th e p o p u l a t i o n o f t h e w o r l d ( L e

Riche , 1967) How ever , the vas t m a jo r i ty o f a l l s evere ly deb i l i ta t ing hum an

in fec t ions occur in the t rop ics and sub- t rop ics . Here , they accoun t fo r s evere

malnutr i t ion , b l indness , haem orrhaging, fever , d iar rhoea, and a var ie ty of o ther

c l in ica l ma lad ies . De sp i t e the ex i s t ence o f an t i -he lmin th chem otherap ies , the

a c c u m u l a t i o n o f c r i p p l in g a n d c h r o n i c d i s o r d e r s s u c h as t h o s e m e n t i o n e d

above no t on ly can l ead to an inc rease in ind iv idua l morb id i ty and mor ta l i ty

ra tes bu t a l so can induce a sp ir al ling co l l apse o f the soc ioec onom ic s ta tus o f an

a f f ec ted v i ll age , comm uni ty , o r even a who le coun t ry . Wh y? On e r eason i s tha t



HOST RESPONSES DURING SCHISTOSOME INFECTIONS 67

h e l m i n th i n f e c ti o n s i n d u c e c o m m o n s y m p t o m s o f o t h e r il ln e s se s . B e c a u s e o f

t hi s t h e y a r e o f t e n m i s d i a g n o s e d a n d s u b s e q u e n t l y tr e a te d i n c o r r e c tl y b y m e d -

ical pract i tioners . E ven i f these infect ions are prope r ly d iagno sed and iden t i f ied

in a t ime ly f ash ion , many peop le f a i l to ge t the appropr ia te t r ea tmen t due to

po l i ti ca l , econo m ic , o r soc ia l r easons . In add i tion , the cu r ren t ly av a i l ab le and

m o s t w i d e l y u s e d c h e m o t h e r a p i e s t o d a y ( a l b e n d a z o le , m e b e n d a z o l e , d i e t h y l-

c a r b a m a z i n e , i v e r m e c t i n , a n d p r a z i q u a n t e l ) c a n f a i l t o i n d u c e l i f e - l o n g

pro tec t ion and , the re fo re a l l ev ia te in fec t ion and morb id i ty on ly t empora r i ly .

Taken toge the r, these f ac to r s can po ten t i a l ly l ead to a pop u la t ion o f ch ron ica l ly

i l l ind iv idua l s no t con t r ibu t ing to the p roduc t ive deve lopmen t o f the i r com-

m u n i t y . U l t i m a t e l y , t h i s s t a te o f m e d i c a l e m e r g e n c y l e a d s t o c o u n t r i e s

su f fe r ing ( in som e ins tances s t agger ing ) f inanc ia l lo s ses tha t ma y be un reco v-

e r a b le . C o n c e r n s o v e r t h e m e d i c a l a n d e c o n o m i c h e a lt h o f d e v e l o p i n g

coun t r i e s have fue l l ed r esea rch r e la ted to (1 ) the s ea rch fo r new chemothera -

p ies th rough nove l d rug des ign , (2 ) the accura te iden t i f i ca t ion o f a t r i sk

popu la t ions th rough ep idemio log ica l approaches , (3 ) the de l ive ry and admin-

i s t ra t ion o f d rugs th rough hum an i ta r i an e f fo r t s , (4 ) the charac te r i s a t ion o f

chemotherapue t ic and immunoprophy lac t i c t a rge t s , and (5 ) the under s tand ing

of he lm in th /hos t in te rac t ions th rough im m uno b io log ica l inves tiga t ions .

Th is r ev iew wi l l focus on one pa r t i cu la r a spec t o f he lmin th /hos t in te rac -

t ions - the hos t s inappropria te deve lopm en t o f h igh ly skewe d , imb a lanced and

d e l e t e r io u s i m m u n o p a t h o l o g i c a l i n f l a m m a t o r y r e a c t i o n s th a t e v o l v e d u r in g

sch i s tosome in fec t ion . These r eac t ions , un l ike those p roper ly r egu la ted and

b a l a n c e d o n e s c o m m o n l y a s s o c i a t e d w i t h n o n - l e t h a l c h r o n i c p e r s i s t e n c e o f

sch i s toso m e parasi t e s, l ead to e leva ted morb id i ty and mor ta l i ty r a tes . Bec ause

d i s tinc t types o f a typ ica l im mu nopa tho log ies a re inc reas ing ly be ing r epor ted in

s c h i s t o s o m e i n f e c ti o n s o f e x p e r i m e n t a l a n i m a l m o d e l s a n d h u m a n p o p u l a -

t ions , inves t iga to r s have ques t ioned whe the r these pa tho log ies a re , in f ac t ,

u n c o m m o n . T h e c o n s e n s u s a m o n g s t m o s t s c h i s t o s o m e i n v e s t i g a t o r s , t h e r e -

fo re , i s tha t i t i s impor tan t to iden t i fy the immune co r re la tes , pa thways and

m olec u les tha t a s soc ia te w i th s evere pa tho log ica l r eac t ions du r ing s ch i s toso -

mias i s . Onc e iden ti f ied , they need to be p roper ly charac te r i s ed and und er s tood

in o rde r fo r s t r a teg ies o f in te rven t ion o r p reven t ion to be implemen ted suc -

cess fu l ly .

T h e p u r p o s e o f t h is r e v i e w is to s u m m a r i se h o w a b a l a n c e d i m m u n e

respo nse dev e lops and i s m a in ta ined in the hos t du r ing s ch i s tosomias i s and to

d i s c u s s t h e d e l e t e r i o u s c o n s e q u e n c e s o f s k e w e d , a t y p i c a l a n d e x a g g e r a t e d

im m une r esponse induc tion . Spec i fi ca lly , a focus w i l l be p resen ted tha t de f ines

the d i f f e ren t pa tho log ica l s t a te s induced by inappropr ia te immune r esponses ,

desc r ibes how these d i s t inc t s t a te s may deve lop dur ing s ch i s tosomias i s , and

d iscus ses wh e the r s imi la r pa tho log ica l r eac t ions occu r in o the r he lmin th in fec -

t io n s u s i n g e x a m p l e s f r o m b o t h h u m a n a n d a n i m a l s t u d ie s .




2 S C H I S T O S O M I A S I S

2 1 B a c k g r o u n d

H u m a n s c h i s to s o m i a s i s , c a u s e d b y t h r ee m a j o r s p e c i e s o f tr e m a t o d e s

S c h i s to s o m a m a n s o n i , S . j a p o n i c u m and S . h a e m a t o b i u m ) , i s t r ansmi t t ed by

cerca r i ae r e leased f rom wate r -dwel l ing sna i l s . S c h i s t o s o m a m a n s o n i and S.

j a p o n i c u m cause in tes t ina l and hepa t i c s ch i s tosomias i s whereas S . haemato-

b i u m cau ses u r ina ry s ch i s tosomias i s . In tes t ina l and h epa t i c s ch i s tosomias i s i s

found m ain ly in sub -Saharan Af r i ca S. mansoni ) , S o u t h A m e r i c a S. mansoni ) ,

t h e M i d d l e E a s t

S . manson i )

a n d A s i a

S . j a p o n i c u m )

wh ereas u r ina ry s ch i s -

to somias i s S . h a e m a t o b i u m ) i s g e n e ra l ly e n d e m i c t o N o r t h a n d s u b - S a h a ra n

Af r ica . Cur ren tly , s ch i s tosom es a re e s tima ted to in fec t more than 200 m i l lion

p e o p l e w o r l d w i d e w i t h a s m a n y a s 6 0 0 m i ll io n m o r e i n d iv i d u a ls i n d a n g e r o f

acqu i r ing s ch i s tosomias i s due to mass immigra t ions , emig ra t ions and newly

created i rr igation pro jects Be rgquis t and Col ley , 1998). Th ese par t icu lar m eta-

z o a n o r g a n i s m s a r e l a r g e , e x t r a c e l l u l a r , m a c r o - e n d o p a r a s i t e s t h a t u n d e r g o

la rval to adu l t me tam orpho s i s w i th in va r ious t i s sues o f an in fec ted hos t .

He lmin ths , a s a g roup , a r e sup reme su rv iva l s t r a t eg i s t s , hav ing evo lved

s t ruc tu res, behav iou r s and m echan i sms tha t a l low fo r the succ es s fu l con t inu -

a t ion o f l i f e in ha r sh hos t env i ronmen ts such as b lood , the gas t ro in tes t ina l

t r ac t and the lymph a t i c s amo ng m any o the rs ) . Sch i s tosom es a re no excep t ion ;

S . ma nson i , S . j apo n icum , and S . haem atob ium all l ive the m ajor i ty o f thei r l i fe

spans in the b loo d o f the i r de f in i tive hos t s ve r t eb ra te m am m als ) and have

evo lved va r ious su rv iva l s t ra t eg ies Pea rce and Sher, 1987) . Reach ing s exua l

m a t u r i t y in th e b l o o d s tr e a m , m a l e a n d f e m a l e s c h i s t o s o m e s u n l ik e o t h e r

t r ematodes , wh ich a re he rmaphrod i t i c , s ch i s tosomes a re d ioec ious ) ma te and

each pa i r p roduces hundreds S . ma nson i and S . haem atob ium ) to thousan ds S .

j a p o n i c u m )

o f e g g s e v e r y d a y . M a n y o f t h e s e e g g s w i ll u l t i m a t e l y b e t r a ns -

m i t t e d t o t h e o u t s i d e e n v i r o n m e n t e i t h e r b y p a s s i n g w i t h t h e fa e c e s S .

j a p o n i c u m a n d S . manson i ) or in the u r ine S . haematob ium) . In a su i tab le

w ater environm ent , the eggs wi l l ha tch v iab le larval paras i te s tages m iracid ia)

and the s ea rch fo r an in te rme d ia te sna il hos t ensues . Fo ur to f ive wee ks fo l -

l o w i n g m i r a c id i a l p e n e t r a t i o n a n d a s e x u a l r e p r o d u c t i o n o f i n t r a m o l l u s c a n

sch i s tosom e paras it e l i f e - st ages , sna i ls w i l l beg in to shed a s e cond l a rva l s t age

ce rca r i ae ) , wh ich i s in fec t ious to humans and o the r mammal ian de f in i t ive

h o s t s . A l t h o u g h s o m e p a t h o l o g i c a l c o n s e q u e n c e s d e v e l o p w h e n a h o s t i s

in fec ted by ce rca r i ae M ulv ih i ll and Burne t t , 1990) , these a re usua l ly minor

and i l l -de f ined in compar i son to those changes tha t evo lve in r e sponse to the

eggs tha t become t r apped in hos t t i s sues du r ing a pa ten t in fec t ion . In f ac t ,

ex t r apo la t ions t aken f rom mu r ine s tud ies sugge s t it i s the s ch i s tosom e egg tha t

induces the majo r i ty o f a l l pa tho log ica l r eac t ions in an in fec ted ind iv idua l .



270 K F H O F F M A N N E T A L

nude mice (Cheever e t a l . 1989). In each of these examples, the host fails to

form a well-organised, circumoval granuloma and ult imately dies. Although

the exact cause of death is not entirely known, Dunne and Doenhoff have pro-

vided evidence which demonstrates that certain S . m a n s o n i (not observed in S.

j a p o n i c u m or S . h a e m a t o b i u m infections) egg molecules are highly toxic to

liver parenchyma cells (Doenhoff e t a l . 1981; Dunne e t a l . 1981; Dunne and

Doenhoff, 1983). Therefore, if the host fails to form a mature circumoval

granuloma during S . m a n s o n i infections, these hepatotoxic egg antigens can

leach out into the surrounding parenchyma and induce extensive liver damage.

Although some of these egg molecules have been biochemically characterised

(Dunne e t a l . 1991), their molecular identities are currently unknown.

From these early and elegant studies, it was apparent that T cells were

important for granuloma formation and host survival. However, some of these

studies also demonstrated that host T cell populations were paramount to the

schistosome s survival as well (e.g. Doenhoff e t a l . 1986; Cheever e t a l .

1999). Specifically, it was illustrated that the absence of host T cells led to a

state in which schistosome eggs could not efficiently traverse the intestinal

lumen, which ultimately interrupted the continuation of the parasite s life

cycle. Therefore, the survival of both host and parasite are intimately related

to the generation of a stable and activated T cell population during infection.

At the time o f these initial experiments, it was unclear which population of T

cell was responsible for the observed effects on granuloma inflammation,

host survival and parasite egg transmission, although CD4 ÷ and CD8 + T cell

populations (either expressing ~ T cell receptors or 7/8 T cell receptors)

were the most likely candidates. Therefore, a series of seminal studies were

undertaken to demonstrate firmly which cell population positively influenced

the development of circumoval granulomas as well as host and parasite sur-

vival.

Infection of mice deficient for MHC II (Abeta (o)) (Hernandez e t a l . 1997;

Angyalosi

e t a l .

1998), c~/~ T cell receptors (Iacomini

e t a l .

1995) or CD4 +

T cells (Fallon e t a l . 2000a) led to a similar pathological outcome as infected

thymectomised, SCID, nude or T cell-depleted mice. This common pathology

was characterised by abrogated granuloma inflammation, liver damage and

increased mortality rates. A study of CD4 ÷ T cell-deficient humans (HIV co-

infected) also revealed the importance of this cell population in mediating S.

m a n s o n i egg excretion (Karanja e t a l . 1997). In this study, HIV and schisto-

some co-infected individuals (in comparison to HIV-, schistosome+

individuals) had a significant defect in egg excretion. This requirement of

CD4 ÷ T cells to mediate egg passage across the gut lumen is quite similar to

the phenomenon observed in infected SCID mice (Cheever e t a l . 1999).

The contribution of other T cell populations to granuloma formation was

further examined in subsequent studies. Infection of mice deficient for MHC

I (TAP knockout mice or ~-2 microglobulin knockout mice) (Hernandez e t a l .




1997; Yap

e t a l .

1997) , ? /8 T cel l recepto rs ( Iacom ini

e t a l .

1 9 9 5) o r C D 8 ÷ T

cel ls (Yap e t a l . 1997) r esu l t ed in the fo rmat ion o f c i rcum ova l g ranu lom as

s imi la r to in fec ted gene- su f f i c i en t o r w i ld - type m ice . The r esu lt s o f these s tud -

ies and o thers (ar t i f ic ia l i n v i t r o g r a n u l o m a f o r m a t i o n ; D o u g h t y e t a l . 1987)

c o n c l u s i v e l y d e m o n s t r a te d t h a t ~ C D 4 ÷ T c e ll s i n te r a ct in g w i t h M H C c l a s s

I I m o lecu les on an t igen -p resen t ing ce l l s a r e abso lu te ly r equ i r ed fo r the deve l -

opm en t o f hos t -p ro tec t ive g ranu lom as and succes s fu l , long- te rm hos t /pa ras i t e

survival. Fur therm ore , these s tudies ad di t ional ly dem ons tra ted that ? /8 CD 4 + or

C D 8 + T c e l ls , a s w e l l a s M H C c l a s s I m o l e c u l e s , c o n t r i b u t e m i n i m a l l y t o

g r a n u l o m a t o u s i n f la m m a t i o n d u r i n g s c h i s t o s o m e i n f ec t io n .

2 3 Concept o f Th l /Th 2 D ichotomy

T y p i c a l l y , h e l m i n t h i n f e c t i o n s o f d e f i n i t i v e h o s t s a r e a s s o c i a t e d w i t h h i g h

leve l s o f c i r cu la t ing an d t i s sue eos inoph i l ia , en hanced m as t ce l l and baso ph i l

f u n c t i o n a l a c t iv i ty , a n d e l e v a t e d a n t i g e n - s p e c i f i c a n d p o l y c l o n a l I g E / I g G 4

( h u m a n ) o r I g E / I g G 1 ( m o u s e ) a n t i b o d y p r o d u c t i o n ( B e l l , 1 9 9 6 ).

S c h i s t o s o m i a s i s i s n o e x c e p t i o n a n d w a s t h e f ir s t h e l m i n th d i s e a s e to b e u s e d

a s a n e f f e c t i v e m o d e l t o s t u d y t h e se c o m m o n i m m u n o l o g i c a l c h a ra c t er is ti c s.

Ho wev er , i t wa s no t un t i l the mid -19 80s tha t the true mechan i s t ic c om plex i ty

o f the hos t s im m une r esponses to he lmin th in fec t ions w as s ta rt ing to be appre -

c i a te d a n d u n r a v e ll e d . D u r i n g t h i s ti m e , M o s m a n a n d c o l l e a g u e s d i s c o v e r e d

func t iona l d ive r se subse t s o f mu r ine C D4 ÷ T he lpe r ce l l c lones , the m os t eas i ly

i d e n ti f ia b l e p o p u l a t i o n s o f w h i c h w e r e c a l le d T h l a n d T h 2 ( M o s m a n n a n d

C o f f m a n , 1 9 8 9 a , b ) . T h e s e c l o n e s w e r e d i s t in g u i s h e d o n t h e b a s i s o f t h e

c y t o k i n e p r o f il e s t h e y p r o d u c e d u p o n a c ti v at io n : T h l c l o n e s p r o d u c e d i n te r -

f e ron ( IFN ) -? , tum our nec ros i s f ac to r (TN F) - l] and in te rl euk in ( IL) -2 ; w hereas

T h 2 c l o n e s p r o d u c e d I L - 4 , I L - 5 , I L - 6 , IL - 1 3 a n d I L - 1 0. H u m a n e q u i v a l e n ts o f

m u r i n e T h l a n d T h 2 c l o n e s w e r e i d e n t i f i e d s h o r t l y t h e r e a f t e r ( R o m a g n a n i ,

1991a). T he su bse qu en t f inding that

i n v i v o

p o p u la t io n s o f h u m a n T h l / T h 2

ce l l s were genera ted du r ing he lmin th in fec t ion and in f luenced the s ever i ty

and m agn i tude o f d i s ease suscep t ib i l i ty and r es i st ance s t rong ly sugges ted tha t

these ce l l s we re no t ju s t the r esu lt o f i n v i t r o cu l tu ring cond i t ions (Rom agnan i ,

1991b) . In f ac t, these impo r tan t s tud ies r ep resen ted a wa te r shed in how m os t

h o s t / p a r a s i t e i n t e r a c t i o n s a n d i m m u n o l o g i c a l i n v e s t i g a t i o n s w o u l d s u b s e -

q u e n t l y b e in t e r p r e te d . F o r e x a m p l e , a l l h e l m i n t h i n f e c t i o n s ( i n c l u d i n g

s c h i s t o s o m i a s i s ) a r e n o w c u r r e n t l y t h o u g h t o f a s T h 2 - d o m i n a t e d d i s e a s e s ,

b e c a u s e o f t h e i n d u c ti o n o f h i g h I g E / Ig G 4 / I g G 1 a n t i b o d y l e v e l s a n d e l e v a t e d

e o s i n o p h i l p o p u l a t io n s , w h i c h a r e th e r e s u lt o f c h r o n ic , h o s t T h 2 c y t o k i n e

produc t ion (main ly IL-13 , IL-4 and IL-5 ) . Subsequen t ly , a l l cu r r en t ly pub-

l i shed work s inves tiga t ing the in te rac tion o f a hos t s im m une sys tem w i th a

p a r a s i t e w i l l u n d o u b t e d l y b e d o m i n a t e d b y d i s c u s s i o n s c o n c e r n i n g t h e




ThlFF h2 d icho tom y. C D 4 ÷ T- regu la to ry -ce l ls (p rodu c ing e i the r IL-10 , t r ans -

f o r m i n g g r o w t h f a c t o r b e t a ( T G F - ~ ) o r a c o m b i n a t i o n o f b o t h I L - 1 0 a n d

T G F -[3 ) h a v e r e c e n t l y b e e n i d e n t i fi e d a n d m a y b e i m p o r ta n t i n d o w n - m o d u -

l a t i n g o r c o n t r o l l i n g c h r o n i c i m m u n e r e s p o n s e s o n b o t h p o l e s ( P a p i e r n i k ,

2 0 0 1 ; R e a d a n d P o w r i e , 2 0 0 1 ; R o n c a r o l o

e t a l .

2 0 0 1 ; T o m s a n d P o w r i e ,

2001) . A l though i t i s genera l ly ag reed tha t Th l ce l l s p lay a c r i t ica l ro le in ce ll -

m ed ia ted im m uni ty aga inst in t race l lu la r pa thogens such as p ro tozoan pa rasi te s ,

and tha t Th2 ce l l s he lp in humora l immune r esponses aga ins t ex t r ace l lu la r

pa thog ens such as he lmin th pa ras i te s , these c ros s -r egu la t ing and s e l f - ampl i fy -

ing ce l l popu la t ions c lea r ly have add i t iona l func t iona l ac t iv i ti e s. M any o f these

act iv i t ies are s t i l l be ing d iscovered .

A p le tho ra o f work has been pub l i shed desc r ib ing the in i t i a t ion , deve lop-

men t , c ros s - r egu la t ion , s t ab i l i ty and func t ions o f Th ce l l popu la t ions an d the

in te res ted r eade r i s d i r ec ted to these fo r fu r the r in fo rmat ion ( e .g . A bb as

e t a l .

1 9 9 6 ) . T h e t y p i c a l T h 2 i m m u n o l o g i c a l c a s c a d e i n d u c e d a f t e r s c h i s t o s o m e

in fec t ion has a l so been the sub jec t o f in tens ive r esea rch e f fo r t s and yea r s o f

inves t iga t ion have l ed to many ins igh t s and advances wh ich a re a l so tho r -

oug h ly r ev iew ed e l s ew here ( e.g . Pea rce and Re ine r , 1995; W ynn and C heever ,

1995). Ho we ver , a s th is r ev iew d i s cus ses the de le te r ious pa tho log ica l con se -

q u e n c e s o f d e v e l o p i n g a h i g h ly s k e w e d i m m u n o l o g i c a l o r i m b a l a n c e d T h

response , so m e t ime m us t be spen t r e - ana lys ing the even t s tha t induce , con t ro l

a n d r e g u l a te t h e T h 2 - d o m i n a t e d i m m u n o l o g i c a l r e a c t i o n s th a t t y p i c a l ly o c c u r

in mo s t s ch i s toso m e- in fec ted de f in i tive hos ts .

I N D U C T I O N R E G U LA T IO N A N D C O N S E Q U E N C E S O F H O S T-

M E D IA T E D T Y P E -2 I M M U N E R E S P O N S E S D U R I N G I N FE C T IO N

W I T H

S C H I S T O S O M A M A N S O N I

3 .1 . Type-2 Imm uno log ica l Responses Dom inate During He lm in th

Infections

H e l m i n t h i n f e c ti o n s g e n e r a l l y i n d u c e t h e p r o d u c t i o n o f T h 2 c e l l p o p u la t i o n s

wi th in the in fec ted hos t . The deve lopm en ta l even t s l ead ing to Th2 ce l l d i ff e r -

e n t i a t i o n a r e e x t r a o r d i n a r i l y c o m p l e x a n d s t i l l i n c o m p l e t e l y u n d e r s t o o d .

H o w e v e r , t w o m a j o r t h e o ri e s ( i n st ru c t io n a n d s e l e c t io n ) h a v e e m e r g e d f r o m

ex is ting da ta tha t cou ld exp la in ho w Th ce l l s d i ff e ren ti a t e, r em ain s t ab le and

i n f lu e n c e t h e e v o l v in g i m m u n e r e s p o n s e s ( r e v i e w e d in M u r p h y

e t a l .

2000) .

Ac cord ing to the in s t ruc tion m ode l o f Th ce l l d if f e ren ti a t ion , na ive C D 4 ÷ Th0

c e l ls ( c a p a b le o f p r o d u c i n g b o t h T h l / T h 2 c y t o k i n e s ) a r e i n s tr u c t e d t o d i ff e r-

en t i a te in to a po pu la t ion o f C D 4 ÷ Th2 ce l l s upon p r ima ry ac t iva tion in the

p resenc e o f IL-4 ( r ev iew ed in Seder and Pau l , 1994). T hese s e l f - ampl i fy ing ,




IL-4 - ins t ruc ted , CD 4 ÷ Th2 ce l l s , p roduc ing cy tok ines tha t co un te r - r egu la te

Th l ce l l s , w i l l even tua l ly p redomina te du r ing the in fec t ion . In con t r as t , t he

s e l e c ti o n m o d e l p r o p o s e s t h at n a i v e C D 4 ÷ T h 0 c e l ls d e v e l o p i n to a p o p u l a t i o n

o f C D 4 ÷ T h 2 c e l ls b e c a u s e o f th e s e l e c t i v e o u t g r o w t h o f p r e c o m m i t te d p r e -

c u r s o r s . E v i d e n c e e x i s t s th a t t h e n u m b e r o f c e l l d i v i s i o n s i n f l u e n c e s t h e

g e n e r a t io n o f C D 4 ÷ T h 2 c e l ls f r o m t h e s e p r e c u r s o r s ( B i r d e t a l . 1998) .

C u r r e n t l y , t h e r e i s n o t e n o u g h e v i d e n c e a s y e t t o a r g u e w h i c h m o d e l ( o r

ano the r ) p redom ina tes du r ing he lmin th in fec t ions o r even i f these mo de l s a r e

m utua l ly exc lus ive . In f ac t , i t i s h igh ly l ike ly tha t bo th m ode l s ( and pos s ib ly

o t h e r s) i n f lu e n c e t h e d e v e l o p m e n t a n d s ta b i li s at io n o f C D 4 ÷ T h 2 c e l l p o p u l a -

t ions f rom na ive C D 4 ÷ Th0 ce l l s du r ing he lmin th in fec t ions , a lbe i t p rob ab ly

opera t ing a t d i f fe ren t t imes a nd loca t ions .

H e l m i n t h i n f e c t io n s d r i v e th e d i f f e r e n ti a t io n o f n a i v e, t h y m u s - s e l e c t e d ,

C D4 ÷ p recu r so r T h ce l l s (C D4 + Th p ce l l s ) in to t r ans ito ry , in te rmed ia te CD 4 +

T h 0 c e ll s. C D 4 ÷ T h 0 c e ll s, c a p a b l e o f p r o d u c i n g I L - 2 , I L - 1 0 , I F N - y a n d I L - 4

( m i x e d T h l / T h 2 e n v i ro n m e n t ) , a r e n o w s u b j e c t e d t o o n e o r b o t h o f th e T h d i f -

f e re n t ia t io n m e c h a n i s m s d e s c r i b e d a b o v e . A c c o r d i n g t o t h e i n s tr u c ti o n t h e o r y

of Th ce l l d i f fe ren t ia t ion , IL-4 i s the es sen t ia l cy tok ine need ed to com m i t p re -

cu r so r s dow n the Th2 pa th wa y dur ing he lmin th in fec tion . Th i s cy tok ine exert s

i ts func t iona l ac t iv i ty v ia b ind ing to the IL-4 r ece p to r ( IL-4R ) on t a rge t ce l l s

a n d s i g n a l l i n g t h r o u g h s i g n a l tr a n s d u c e r a n d a c t i v a t o r o f t r a n s c r ip t i o n 6

(STAT6) (Takeda e t a l . 1996) . Al tho ugh th is in teract ion is cri t ica l for the m at-

u ra t ion , m em ory , and s t ab i l is a t ion o f type -2 imm une r esp onses , s tud ies in

I L - 4 R - o r S T A T 6 - d e f l c i e n t m i c e i n f e c t e d w i t h e i t h e r N i p p o s t r o n g y l u s

b r a s i l i e n s i s o r S . m a n s o n i h a v e q u e s t i o n e d t h e r e q u i re m e n t o f IL - 4 R / S T A T 6

s ig n a ll in g i n th e i n d u c t io n o f s o m e t y p e - 2 i m m u n e r e s p o n s e s ( J a n k o v i c e t a l .

1999 , 2000 ; Urban e t a l . 2001) . In these s tud ies, in fec ted IL -4R- o r STAT6-

d e f i c i e n t m i c e a r e s ti ll c a p a b l e o f p r o d u c i n g s o m e p a r a s it e - sp e c i f ic t y p e - 2

c y t o k i n e a n d a n t i b o d y r e s p o n s e s ; h o w e v e r , t h e s e r e s p o n s e s a r e m u c h l o w e r

than in in fec ted w i ld - typ e mice . Fu r the rmore , in a s epara te s tudy , STAT6 was

show n to be neces sa ry and su f f i c ien t fo r IL-4 s ro le in Th2 d i f f e ren t i a t ion and

e x p a n s i o n ( Z h u e t a l . 2001) . Taken toge the r , these obse rva t ions imply tha t

t y p e - 2 i m m u n e r e s p o n s e i n d u c t io n p r o c e e d s o p t i m a l l y i n t h e p r e se n c e o f I L - 4

s igna l ling th rough the IL-4 r ecep to r and STAT6 pa thway . Nev er the les s , o the r

m e c h a n i s m s o f t y p e - 2 r e s p o n s e i n d u c ti o n , n o t y e t i de n t if ie d , m a y a l s o w o r k

d u r in g h e l m i n t h i n fe c t io n s . T h e s e a l te r n at iv e p a t h w a y s m a y b e i n f l u e n c e d b y

co- s t imula to ry molecu les (K ing e t a l . 1996b ; Subraman ian e t a l . 1997; Padrid

e t a l . 1 9 9 8 ; M a c D o n a l d e t a l . 2 0 0 2 b ) , d e n d r i t i c c e l l s ( M a c D o n a l d e t a l .

2 0 0 1 ; d e J o n g e t a l . 2 0 0 2 ) p a r a s it e m o l e c u l e s ( F a l c o n e e t a l . 1996 ; Okano e t

a l . 1 9 9 9 ; H o l l a n d e t a l . 2 0 0 0 ; W h e l a n e t a l . 2 0 0 0 ; C u e l l a r e t a l . 2001 ;

H a i s c h e t a l . 2 0 0 1 ) o r p r o c e e d v i a a d e f a u l t p a t h w a y n o t o b s e r v e d d u r i n g

i n f e c ti o n s w i t h t y p e -1 i m m u n e r e s p o n s e -s t im u l a ti n g p a t h o g e n s ( s u g g e s t e d b y

A b b a s e t a l . 1996).



274 K F HOFFMAN N ET AL

i ~

j

i i~ o

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t

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~




ac t iv i ti e s. The p resen ce and ro le o f IL-25 For t e t a l . 2001) in he lmin th in fec -

t ions has ye t to be es tab l ished . IL-10 seem s to no t on ly be s ec re ted by T h2 ce l ls ,

bu t a l so by Th l ce l ls and o the r ce l ls ) So rnas se

e t a l .

1996); therefore, i ts ofte n

c i t ed t ex tbook as soc ia tion w i th po la r i s ed Th2 responses i s no t com ple te ly accu-

ra te and needs fu r the r r ev i s ion M ura i ll e and Leo , 1998). These cy tok ines can

c a u s e n u m e r o u s p h y s i o l o g i c a l e f f e c t s b y d i r e c t l y a c t i n g u p o n t a r g e t c e l l s

e x p r e ss i n g c o m p l e m e n t a r y r ec e p to r s. S o m e o f th e m o s t c o m m o n m e a s u r a b le

ef fects of cy tokine s obse rved dur ing helminth infect ions are increases in mature

popu la t ions and func t iona l ac t iv i t i e s o f acces so ry ce l l s such as eos inoph i l s ,

ma s t ce l l s and basoph i l s . Add i t ional ly , these type-2 cy tok ines can ind uce the

c las s sw i tch ing o f B ce l l s to p roduc e an t ibod ies o f the IgG 4 human) , IgG 1

m o u s e ) o r I g E b o t h ) i s o ty p e s . T y p e - 2 - a s s o c i a te d i m m u n e r e s p o n s e s a r e

induced to con t ro l the pa thogen ic i ty o f he lmin th in fec tions and depe nd upon

appropr ia te hos t r egu la to ry mechan isms to l imi t the i r po ten t i a l ly des t ruc t ive

na tu re . Fa i lu re to su f f i c ien t ly induce and con t ro l type-2 -as soc ia ted immune

responses du r ing he lmin th in fec t ions o f ten l eads to the s evere ly de tr imen ta l

pa tho log ica l r eac t ions d i s cus sed in fu r the r de ta i l be low. F ina l ly , i t mus t be

apprec ia ted tha t i t i s no t on ly the Th2 ce l l popu la t ion tha t mak es up the type-2

po la r i s ed r esponse du r ing he lmin th in fec t ion . The con t r ibu t ion o f Tc2 CD 8 ÷ T

ce l ls ) , Be 2 B ce l l s ), Eo s2 eos inoph i l s ), M as t2 m as t ce l ls ) , N K2 na tu ra l

k i l le r ce l ls ) , M ac2 a l te rna tive ly ac t iva ted m acrophag es ) and Bas2 basoph i l s )

a re o f ten over lo oked bu t a re equa l ly impor tan t e .g . He sse e t a l . 2001) .

3 .2 . I n d u c t i o n o f T y p e 2 a s s o c i a t e d I m m u n e R e s p o n s e s D u r in g S .

m n s o n i I n fec t ion

H o w s o o n a f t e r i n f e c t i o n c a n t h e s e t y p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s b e

m easured , w ha t a re the pa rasi t e mo lecu le s tha t d r ive these r esponses , w ha t a re

t h e c e l l u l a r c o m p o n e n t s o f t h e s e r e s p o n s e s , w h a t a c t i v i t i e s d o t h e t y p e - 2 -

a s s o c i a t e d c y t o k i n e s m e d i a t e a n d h o w i s t h i s t y p e - 2 i m m u n e r e s p o n s e

r e g u l a te d a n d c o n t r o l le d a r e s o m e o f th e q u e s t i o n s t h at s c h i s t o s o m e i m m u n o -

b i o l o g i st s h a v e a t t e m p t e d t o a n s w e r o v e r t h e p a s t f e w d e c a d e s . M o s t a n s w e r s

to these ques t ions have come abou t th rough inves t iga t ing s ch i s tosome in fec -

t ions in an imal m ode ls w here hou s ing cond i t ions , in fec tious dose and nu t ri tion

c a n b e c a r e f u l l y m o n i t o r e d a n d c o n t r o l l e d . T h e m o u s e r e p r e s e n t s t h e m o s t

ex tens ive ly s tud ied exper imen ta l an imal mode l owing to i t s f a s t r ep roduc t ive

na tu re, the w ide ava i l ab i l ity o f t r ansgen ic an d kno cko u t s t ra ins and the sus -

cep t ib le na tu re o f th i s an imal to s ch i s tosom e in fec t ion . In f ac t , deve lopm en ta l

m a t u r a t i o n o f S . m a n s o n i p r o c e e d s q u i t e s i m i l a r l y i n m o u s e a n d m a n

A r m s t r o n g , 1 9 6 5 ) , a l t h o u g h d i f f e r e n c e s i n t h e k i n e t i c s a n d f e a t u r e s o f

i m m u n o p a t h o l o g y c l e a r ly d o e x i st b e t w e e n th e s e tw o h o s ts C h e e v e r

e t a l .

2000 ; Fa l lon , 20 00) .



HOS T RE S P ONS E S DUR I NG S CH I S TOS OM E INFE CTIONS 77

In com par i son to exper im enta l m ur ine invest iga t ions , imm uno logica l s tud-

i e s o f s ch i s to s omi as is i n h um an popu l a ti ons a r e e x t r em e l y li m i t ed in b o t h

s t udy des ign and ou t com e meas u r emen t s . T h i s i s ma i n l y ow i ng t o e t h i ca l con -

s t raints , as i t i s not acceptable to perform longi tudinal or invas ive s tudies in

infec ted ind iv idua l s and , therefore , no t perm iss ib le to fo l low the deve lopm ent

of chronic morb id i ty . An addi t iona l compl ica t ion involves se t t ing up f i e ld-

bas ed l abo ra t o ri e s in r em o t e a r eas o f the w or l d , and even w h en t h is can be

achieved , s evera l f ac tor s m ay po ten t i a l ly con foun d any re la t ionsh ip be twee n

infec t ion s ta tus and im m un e response . S om e of these f ac tor s inc lude co- infec-

t ions by o ther paras i tes , d i f f e rences in in fec t ion in tens i ty , d i f f e rences in age

and sex , he te rog eneo us gene t i c back ground s and v ar ia tion in the nu t r i t iona l

s tatus o f the s tudy popula t ion . How ever , as s ch i s tosomias i s is a m ajor burden

on w or l dw i de hum an popu l a t ions , i t rema i ns i mper a t ive t o ov e r com e t hes e

obs tac les and f ind new w ays to m ake sense of the l imi ted , bu t very impor tan t ,

i n f o r ma t i on comi ng f r om hu m an i m mu noep i dem i o l og i ca l i nvest iga t ions i n

t he f ie l d. B y com bi n i ng t hes e da t a w i t h t hos e f r om m uf i ne expe r i men t a l st ud -

i es ( and o t he r expe r i men t a l mode l s ), a m or e t ho r ough unde r s t and i ng o f t he

i mm uno l og i ca l even ts i nduced b y s ch i st o s ome i n f ec t ion w i l l be ach i eved .

3 .2 .1 . S c h i s t o s o m e e g g s d r i v e t y p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s

Sho r t ly a f t e r M osm an ' s d i scove ry of func t iona l ly d iver se subse t s o f Th ce l l s ,

G r zych , Pea r ce and co l l eagues demons t r a t ed tha t T h2 cy t ok i nes w er e i nduced

dur ing sch i s tosomias i s a t a t ime cons i s t en t w i th the product ion of paras i t e

eggs an d the i r depos i t ion in to hos t ti s sues (G rzych e t a l . 1991; Pearce e t a l .

1991) . A l though the hos t r esponded to the deve lop ing paras i t e p r io r to egg

lay ing , these r esponses we re l imi ted to typ e- 1 -as soc ia ted IFN-y and IL-2 pro-

d u c t io n . I t w a s o n l y w h e n e g g p r o d u c t io n c o m m e n c e d (~ 5 w e e k s

pos t - in fec t ion) tha t the au thors mea sured a ma jor boos t in the product ion o f

type-2-as soc ia ted cy tok ines ( IL-4 and IL-5) in sp leen ce l ls cu l tu red e x v i v o ;

impor tan t ly , IFN-7 and IL-2 prod uct ion r em ained , a lbe i t a t low er leve l s. Even

m ore impor tan tly , h igh l eve ls o f IL-5 and IL-4 ( and low leve l s o f IL-2 and IFN -

~) w er e s ubs equen t l y f ound i n w ho l e l ive r and g r anu l om a ce l l cu l t u r e s o f

in fec ted an imals a l so . Thi s f ind ing was subsequ ent ly con f i rme d in addi t iona l

inves tiga tions and m os t r ecen t ly by Hay ash i e t a l . (1999). Tog ether, thes e s tud-

i e s f o r m a l l y d e m o n s t r a t e d t h a t c i r c u m o v a l g r a n u l o m a f o r m a t i o n d u r i n g

sch i s tosomias i s is as soc ia ted wi th the product ion o f type-2 cy tok ine r esponses

( type - 2 g r anu l oma) and i s no t d r i ven by t ype - l - m ed i a t ed de l ayed - t ype hype r -

s ens it iv i ty r eac t i ons ( t y pe - l - o r t ube r cu l o id - g r anu l oma) , a s w as p r ev i ous l y

sugges ted (Boros and Warren, 1970) . In addi t ion, these resul ts f i rmly es tab-

l i s hed t ha t t he egg w as t he ma j o r s t i mu l us beh i nd t hes e r e s pons es , bo t h

sys tem ical ly (spleen) and local ly ( l iver and granu lom a) dur ing schis tosomias is.




T h i s a l s o a p p e a r s t o a p p l y t o h u m a n i n f e c t i o n s e . g . P a r r a e t a l . 1992 ;

W i l l i a m s e t a l . 1994; E1 Ridi e t a l . 1997) , a l though m ixed ty pe- I / typ e-2 an ti -

e g g c y t o k i n e r e s p o n s e s c a n b e o b s e r v e d i n c h r o n i c a l l y i n f e c t e d i n d i v i d u a l s

M o n t e n e g r o e t a l . 1999).

Add i t iona l ev ide nce tha t conf i rme d the ro le o f IL-4 in g ranu loma fo rmat ion

and hos t type-2 cy tok ine r esponse induc t ion w as p resen ted in the ea r ly 1990s

wh en a s e r i e s o f s tud ies inves tiga t ing the e f f ec t o f IL-4 dep le t ion in s ch i s to -

som e- in fec ted m ice o r i .v . egg- in jec ted mice l eads to pu lm onary g ranu lomas -

p u l m o n a r y m o d e l ) w e r e p e r f o r m e d Y a m a s h i ta a n d B o r o s , 1 99 2; W y n n

e t a l .

1 9 9 3; C h e e v e r

e t a l .

1994). T hese r e la ted s tud ies a l l dem ons t r a ted tha t IL-4

dep le t ion had a d ramat ic e f f ec t in r educ ing e gg- ind uced g ranu loma in f lam-

m at ion and the p rodu c t ion o f the type-2 cy tok ine s IL-5 and IL-13 . In a r e l a ted

s tu d y , a d m i n i s tr a t io n o f re c o m b i n a n t I L - 4 t o c h r o n i c a l l y i n f e c t e d a n i m a l s

r e v e r s e d t h e d o w n - r e g u l a t e d g r a n u l o m a t o u s r e s p o n s e t y p i c a l l y o b s e r v e d i n

la t te r s tages o f in fec t ion Yam ash i ta and Bo ros , 1992). M oreover , s tud ies in

i n f e c t e d I L - 4 - d e f i c i e n t a n i m a l s c o n f i r m e d s e v e ra l o f t h e a b o v e f in d i n g s,

a l t h o u g h v a r i a t i o n s a m o n g I L - 4 - d e f i c i e n t m o u s e g e n e t i c b a c k g r o u n d s a n d

exper imen ta l p rocedures p rodu ced som e d ive rgen t r e su lt s Pea rce

e t a l .

1996).

F ina l ly , a ca re fu l examina t ion in to the k ine t ic s o f cy tok ine p roduc t ion du r ing

p r i m a r y g r a n u l o m a f o r m a t i o n i n t h e p u l m o n a r y m o d e l t h o r o u g h l y d e s c r i b e d

the qua l ity and magn i tude o f the ensu ing type -2 dom inan t r e sponse induced by

s c h i s t o s o m e e g g s W y n n e t a l . 1993) . Together , these f indings demons tra ted

tha t eggs a re the s timu lus beh ind the genera t ion o f IL-4 , hos t type-2 -m ed ia ted

i m m u n e r e s p o n s e s a n d g r a n u l o m a t o u s i n f l a m m a t i o n d u r i n g i n f e c t i o n .

Whatever add i t iona l ro les IL-4 pa r t i c ipa tes in du r ing s ch i s tosomias i s , i t i s

c lea r f rom the abo ve s em ina l s tud ies tha t thi s cy tok ine i s, in pa r t, r e spon s ib le

fo r the genera tion and m ain tenance o f the type-2 imm une r esponses . Imp or tan t

ques t ions a r i s ing f rom th is conc lus ion a re how i s IL-4 f i rs t induced and f rom

wh ich ce l l popu la t ion doe s th i s cy tok ine f ir s t o r ig ina te?

3 . 2 . 2 . P o s s i b le c e l l s o u r c e s o f e a r ly I L - 4 d u r i n g s c h i s t o s o m i a s i s

B e c a u s e s c h i s t o s o m e e g g s i n d u c e t y p e - 2 i m m u n e r e s p o n s e s d u r in g i n fe c t io n ,

h o s t c e ll s o f th e i n n a te i m m u n e s y s t e m t h a t p r o b a b l y i n te r a c t w i t h e g g s a n d

t h ei r c o m p o n e n t s w e r e e x a m i n e d a s p o s s i b l e ea r ly s o u r c e s o f IL - 4 . W i l l ia m s

e t

a l . 1 9 9 3 ) d e m o n s t r a t e d t h a t o n e s u c h c e l l p o p u l a t i o n , n o n - B , n o n - T c e l l s

N B N T c e l l s ) e x p r e s s i n g a n F c e p s i l o n r e c e p t o r , w e r e a m a j o r s o u r c e o f

sp leen -der ived , egg- spec i f i c IL-4 du r ing mur ine s ch i s tosome in fec t ion . The

e x a c t i d e n t it y o f t h e s e N B N T c e l ls w a s n o t c e r ta i n i n t h i s s t u d y b u t b a s o p h i l s

o r m a s t ce l ls w e r e t h e m o s t li k e l y c a n d i d a te s m o u s e e o s i n o p h il s d o n o t

expres s Fc eps i lon r ecep to r s ; de Andres e t a l . 1997) . NBNT ce l l s p roduc ing

I L - 4 w e r e a l s o m e a s u r e d i n a n i m a l s i n f e c t e d w i t h t h e h e l m i n t h s




Nippos t rongy lus bras i l i e ns i s

and

Trichine l la spiral i s

Conrad

et al .

1990;

Carman et al. 1992). T hese studies led investigators to ex am ine carefully the

role of N BN T cell populations in providing an early source o f antigen-specific

IL-4 du ring schistosome infection. It was postulated that egg/wo rm antigens

could activate NBN T cells to produ ce IL-4 via cross-linking of IgE molecu les

and signalling throu gh the Fc epsilon receptor. Indeed, in 1996, Falcone et al.

demo nstrated that egg-stimulated hum an basophils collected from naive indi-

viduals were capable of producing IL-4 Falcone

et al .

1996). This IL-4

response was depend ent upon IgE and Fc epsilon interactions, although IgE-

independ ent histamine release from basophils has recently been o bserved for

a recombin antly expressed S . m anson i translationally controlled tumour pro-

tein ortholog Rao

et al .

2002). Since IL-4 was produced by basophils from

non-exposed donors, Falcone et al. 1996) con cluded that basophils m ight be

responsible for the early source o f this cytokine during schistosomiasis. Also

during this same year, Sabin

et al.

1996) identified a pa thway o f early IL-4

production from eosinophils that was d epende nt upon mast cell-produced IL-

5 in a murine model . However , la ter s tudies f rom these same authors

demo nstrated that IL-5-deficient and mast cell-deficient mice were stil l capa-

ble o f generating a type-2 im mu ne response against schistosome eggs during

infection, confound ing the role o f eosinophils in providing an early source o f

IL-4 Brunet

et al .

1999b; E.A. Sabin and E.J. Pearce, unpublished data).

Neverthe less, a subsequ ent study confir me d that mou se eosinophils are a sig-

nificant source of IL-4 and type-2-associated cytokines at later time points

during infection Rum bley et al . 1999). Current and future work in both

hum an studies and animal models will undoubted ly provide addit ional clues

concerning the importance of NBNT cells in the generation of type-2 imm un e

responses.

An interest ing recent s tudy provided evidence that Kupffer cel ls , i .e .

macrop hages resident in the fiver of schistosome-infected mice, co uld also pro-

vide an early source of IL-4 and IL-13 Hayashi

et al .

1999). The authors

dem onstrated that this Kupffer cell-derived IL-4 and IL-13) was stimulated by

wo rm antigen, was present 3 weeks after infection prior to egg deposition) and

dram atically increase d after egg deposition. How parasite m olecu les stimulate

these hepatic macrophages to produce IL-4 remains uncertain, but clearly

these cel ls have the capaci ty to manipulate the development of type-2-

associated im mu ne responses during schistosomiasis Hesse et al . 2001).

Finally, it must be ap preciated that naive T cells, themselves, cou ld contribute

to this pool of antigen-specific IL-4 production Coffman and vo nd er Weid,

1997, Co ffm an and Reiner, 1999) and, in fact, m ay be para mo unt to egg-spe-

cific type-2 im mu ne responses occurring in the l iver. Com plem entary to these

investigations will be those that define and characterise the components of

schistosome eggs that induce the production of IL-4 and type-2-associated

imm une responses.




3 .2 .3 . E g g c a r b o h y d r a t e s d r i v e I L - 4 p r o d u c t i o n a n d g e n e r a t i o n o f t y p e- 2 -

a s s o c i a t e d i m m u n e r e s p o n s e s d u r i n g s c h i s t o s o m i a s i s

F r o m s o m e o f t h e s t u di e s s u m m a r i se d a b o v e , it w a s c l e a r th a t s t a b l e t y p e - 2

i m m u n e r e s p o n s e d e v e l o p m e n t d u r i n g s c h i s t o s o m i a s i s p r o c e e d e d a t a t i m e

c o n c o m i t a n t w i t h e g g d e p o s i t i o n . T h i s l e d i n v e s t i g a t o r s t o t r y a n d

iden t i fy /de f ine those egg molecu les r e spons ib le , w i th the f i r s t c lues demon-

s t ra t in g t h a t e g g g l y c o p r o t e i n s w e r e e f f e c t i v e st i m u l a t o r s o f g r a n u l o m a

fo rmat ion in exper imen ta l mode l s (Weis s e t a l . , 1987 ; J acob s e t a l . , 1999a, b).

M o r e r e c e n t l y i t w a s r e p o r te d t h a t c a r b o h y d r a te s , t h e m s e l v e s , o n s c h i s t o s o m e

e g g s , p l a y a c r it i c a l ro l e i n t h e i n d u c t i o n o f e g g - s p e c i f i c t y p e - 2 i m m u n e

r e s p o n s e s ( O k a n o

e t a l . ,

1999). H a i sch and co l l eagues have de f ined one g ly -

c o c o n j u g a t e o f s c h i s t o s o m e e g g s t h a t d r i v e s I L - 4 p r o d u c t i o n f r o m h u m a n

b a s o p h i l s ( H a i s c h e t a l . , 2 0 0 1 ) . T h i s a n t i g e n c o n t a i n s m a n n o s e r e s i d u e s

a t t ached to a pep t ide backbone and ac t iva tes basoph i l s th rough IgE c ros s -

l ink ing and Fc eps i lon r ecep to r s igna l ling . T he ex ac t s t ruc tu re o f the m anno se

modi f i ca t ion o r iden t i ty o f the p ro te in s equence has ye t to be charac te r i s ed .

O k a n o

e t a l .

(2001) have a l so iden t i f i ed a po ly lac tosamine sugar , l ac to -N-

f u c o p e n t a o s e I II ( L N F P I I I ) d e ri v e d f r o m s c h i s t o s o m e e g g s t h a t c a n a c t a s a

t y p e - 2 i m m u n e r e s p o n s e a d j u v a n t, w h e n c o u p l e d t o h u m a n s e r u m a l b u m i n. I t

a l s o a p p e a rs t h a t L N F P I I I a l o n e c a n i n d u c e B c e l ls f r o m s c h i s t o so m e - i n f e c te d

m i c e t o p r o d u c e t h e a n t i -i n f la m m a t o r y p r o d u c t s I L - 1 0 a n d p r o s ta g l a n d in E 2

(Velupil la i and Ham , 1994). Th ese ant i - inf lam m atory me dia tors pro bab ly con -

t ri b u te i n d i r e c tl y t o t h e g e n e r a ti o n o f t y p e - 2 i m m u n e r e s p o n s e s b y e f f e c t iv e l y

c ros s - regu la t ing hepa t i c CD 4 ÷ Th 1 ce l ls . Add i t iona l egg-der ived ca rboh ydra te

s t ruc tu res tha t d r ive type-2 -as soc ia ted immune r esponses ( e i the r d i r ec t ly o r

ind i r ec t ly ) a r e cu r r en t ly be ing iden t i f i ed and s tud ied (Van de r K le i j

e t a l . ,

2002) .

3 . 2 .4 . A n t i g e n - p r e s e n t i n g c e l ls a n d c o - s t i m u l a t o r y m o l e c u l e s p a r t i c i p a t e i n

t h e in d u c t i o n o f e g g - s p ec i fi c t y p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s

M a c r o p h a g e s a n d d e n d r i t i c c e l l s e x p r e s s i n g c o - s t i m u l a t o r y m o l e c u l e s h a v e

the capac i ty to po ten t ly ac tiva te T ce l l s du r ing s ch i s tosom ias i s (Hernan dez e t

a l . ,

1 9 9 7 ; H a y a s h i

e t a l . ,

1 9 9 9 ; M a c D o n a l d

e t a l . ,

2 0 0 2 b ) . K u p f f e r c e l l s ,

s t im u l a t e d b y w o r m a n t ig e n s , c a n i n f l u e n c e t h e d i f fe r e n t ia t i o n o f t y p e - 2

i m m u n e r e s p o n s e s b y s e c r e t i n g I L - 4 ( H a y a s h i e t a l . , 1999) . Dendr i t i c ce l l s

have a l so been a t t r ac t ing a g rea t dea l o f a t ten t ion , spe c i f i ca l ly r egard ing the i r

ro le in T ce l l d i f f e ren t i a t ion (Banchereau e t a l . , 2 0 0 0 ; M o s e r a n d M u r p h y ,

2 0 0 0 ; R e i d e t a l . , 2 0 0 0 ) . I n t h e c a s e o f i n fe c t i o u s a g e n t s t h a t in d u c e t y p e - I -

a s s o c i a t e d i m m u n e r e s p o n s e s T o x o p l a s m a g o n d i i a n d L e i s h m a n i a sp , for

exam ple ) , the func t iona l ro le o f dendr i t i c ce l l s (DC1 ce l l s ) has bee n ca re fu l ly




i n v e s t ig a t e d R e i s e S o u s a e t a l . , 1999) . H ow dendr i t i c ce l l s in f luence Th d i f -

f e r e n t i a t i o n d u r i n g s c h i s t o s o m i a s i s i s n o t a s cl e a r, b u t i s s l o w l y b e i n g

u n r a v e l l e d . C u r r e n t e v i d e n c e s u g g e s t s t h a t O X 4 0 L , u p - r e g u l a t e d o n h u m a n

p e r i p h e r al b l o o d m o n o n u c l e a r c e ll s P B M C ) - d e r i v e d d e n d r i ti c c e l ls p r i m e d

w i t h s c h i s t o s o m e e g g a n t i ge n s , m a y p l a y a n i m p o r t a n t r o l e i n th e d i f f e re n t i -

a t i o n o f T h 2 c e l l s d u r in g h u m a n s c h i s to s o m i a s i s d e J o n g

e t a l . ,

2002) . In the

m u r i n e m o d e l , C D 4 0 e x p r e s s i o n o n s c h i s t o s o m e e g g a n t i g e n - p u l s e d b o n e

m a r r o w d e n d r i ti c c e l ls C D 8 - ) a n d l ig a t io n o f t h is c o - s t im u l a t o r y m o l e c u l e t o

C D 1 5 4 o n T c e ll s i s r e q u i r e d f o r T h 2 d i f f e re n t ia t io n M a c D o n a l d e t a l . ,

2 0 0 1 ) . I n a d d it io n , t h e s ig n a l li n g p a t h w a y f a c il i ta t e d b y C D 8 0 , C D 2 8 a n d B 7

c o - s t i m u l a t o r y m o l e c u l e s a l s o a p p e a r s t o b e i m p o r t a n t f o r o p t i m a l T h 2 c e l l

d i f f e ren t i a t ion K ing

e t a l . ,

1 9 9 6 b ; S u b r a m a n i a n

e t a l . ,

1 9 9 7 ; H e r n a n d e z

e t

a l . ,

1999) . Toge the r , these s tud ies demons t r a te tha t an t igen -p resen t ing ce l l s

a n d t h e c o - s t i m u l a t o r y m o l e c u l e s t h e y e x p r e s s i n f l u e n c e t h e d i f f e r e n t i a t i o n

a n d d e v e l o p m e n t o f T h 2 c e l ls in r e s p o n s e t o s ti m u l a t io n b y s c h i s t o s o m e e g g

an t igens . The r e la t ive impor tance o f th is p roces s du r ing s ch i s tosom e in fec t ion

in human s and the exac t pa ras it e m olecu les tha t ac t iva te these ce ll s r ema ins to

b e e l u c i d a te d .

3 . 2 .5 . C D 4 T c e ll s a n d e o s i n o p h i l s s u s ta i n e g g - s t im u l a t e d t y p e -2 i m m u n e

r e s p o n s e s d u r i n g s c h i s t o s o m i a s i s

M ast cells , basoph ils , m acroph ages, eo sinoph ils and naive T c ells al l contr ibute to

the induc tion o f type-2 -as soc ia ted im mu ne r esponses du r ing s ch i s tosom e in fec -

t ion . How ever , Vel la and Pearce 1992) dem ons tra ted that the maintenance o f

these responses i s h ighly d epende nt upon the C D4 ÷ T cel l arm. This po pula t ion of

T cel ls i s a lso cr i t ica l for the format ion of c i rcumoval granulomas . Vel la and

Pearce used a m ode l o f Th2 r esponse induc t ion in w h ich they in jec ted s ch i s to -

some eggs in to the foo tpads o f mice and subsequen t ly measu red the

i n v i t r o

parasite-specif ic cyto kine respo nses of popli teal lym ph nod e cell cultures at 3 and

10 days pos t- immunisa tion . B y s e lect ive ly r emoving CD 4 ÷ T ce l ls o r CD 8 ÷ T

cel ls f rom the popl i tea l lymp h node p opula t ions pr ior to cultur ing , they con -

c luded that the type-2 cy tok ine r esponse in th is m ode l ) was a lmo s t com ple te ly

abrogated by C IM ÷ T c el l deple tion Vella and Pearce , 1992) . Infected SCID - and

CD 4 ÷ T cel l -deple ted mice a lso fa i l to g enera te s t rong typ e-2 cy tokine responses .

These da ta toge the r w i th those o f Rum bley

e t a l .

1998) support the important role

o f C D 4 ÷ T ce l ls in the m ain tenance o f egg- induced type-2 im mu ne r esponses

prim ed b y acc essory cells . Re cen t evide nce has also demonstrated that eosinophils

a r e m a j o r c o n t r i b u to r s o f t y p e - 2 c y t o k i n e s i n th e e g g - i n d u c e d g r a n u l o m a

R u m b l e y

e t a l . ,

1999) . I t seem s l ikely that these two c el l popula t ions as w el l as

o thers a ll contr ibute to the cont inued m aintenance of a type-2 cytok ine environ-

m ent in response to egg deposit ion in the l iver and other t issues) o f infected mice.



28 2 K F HOFFMA NN ET AL

=0

I=

\ °



HOST RESPONSES DURING SCHISTOSOM E INFECTIONS 83

I n s u m m a r y F i g u r e 2 ), e x i s t in g e v i d e n c e s t r o n g l y s u p p o r t s t h e a s s o c i a t i o n

o f a ty p e - 2 i m m u n o l o g i c a l r e s p o n s e w i t h t h e d e v e l o p m e n t o f s c h i st o s o m e

g r a n u l o m a s . G l y c o c o n j u g a t e d e g g a n t i g e n s h a v e th e c a p a c i t y to i n d u c e g r a n -

u l o m a f o r m a t i o n a n d d r i v e T h c e l l d i f f e r e n t i a t i o n . V a r i o u s c e l l p o p u l a t i o n s

p r o b a b l y in t e r a c t w i th t h e s e g l y c o c o n j u g a t e s a n d t h e ir a c ti v a ti o n , r e c r u i t m e n t

a n d t u r n o v e r u l t im a t e l y a l te r s th e d e v e l o p m e n t a n d d e g r e e o f g r a n u l o m a t o u s

i m m u n o p a t h o l o g y . T h e s e d i f f er e n t t y p e s o f i m m u n o p a t h o l o g y a r e d e s c r i b e d

b e l o w w i t h a t t e n t i o n g i v e n t o t h o s e s e v e r e f o r m s i n d u c e d b y i n a p p r o p r i a t e

c y t o k i n e a n d i m m u n e r e s p o n s e s .

4 . D IS T IN C T F O R M S O F S C H I S T O S O M E - M E D I A T E D I M M U N O -

P A T H O L O G Y C A N B E I N D U C E D D U R I N G IN F E C T IO N

4 .1 . L i fe - th r e a t e n in g E g g - in d u c e d I m m u n o p a t h o l o g y d o e s n o t

D e v e l o p i n m o s t In f e c te d H u m a n s o r E x p e r i m e n t a l A n i m a l M o d e l s

I n m o s t c h r o n i c s c h i s t o s o m e i n f e c ti o n s , w h e r e t h e h o s t is n o t i m m u n o l o g i c a l l y

c o m p r o m i s e d , t h e p r o g r e s s i o n o f s e v e re , l i f e- t h re a t en i n g m o r b i d i t y d o e s n o t

Figure

Th e development o f tightly regulated circumoval granulom as and tissue fibro-

sis during S c h i s to s o me ma n s o n i infection is linked to the development of balanced Th 2 cell

popula tions . Many of the eggs l a id by sexua lly m a ture female s ch is tosomes becom e

depo sited in hepatic pho tom icrograph illustrated in this figure), intestinal or bladder tissue.

Here, the eggs secrete bioactive glycoconjugates that are released into the surrounding

milieu a nd induce a very pow erful inflam m atory response. Th is ensuing delay ed-typ e

inflammation leads to the formation o f circumov al granulomas characterised by the recruit-

ment, maturation and turnover o f N BN T cells basophils, m ast cells and eosinophils), B and

T lymphocy tes, macrophages and dendritic cells. Eg g glycoconjugates pro bab ly interact

with surface IgE receptors on N BN T cells where this receptor/ligand interaction initiates the

cellular release o f IL- 4 and IL-5. Hepatic m acrophages and dendritic cells act as powerful

antigen egg glycoconjugate) presenting cells during granuloma formation w here they serve

as additional reservoirs for IL-4 and IL -10 as well as provide co-stimu lation. B lymphocy tes

are also stimu lated by egg glycoconjugates by an unknow n mechanism possibly involving

Ig receptor engagem ent) and this leads to the re lease of ant i - inf lamm atory IL-10 and

prostaglandin E 2 PGE 2). Th e additive contribution o f imm unological m ediators provided

by these cell populations and others mentioned in the text) ultimately leads to an environ-

m ent rich in Th 2 cy tokines an d favours the preferential expansion of Th2 CD 4 ÷ T cells.

Fibrotic lesions begin to develop in these tissues as the result of increased pro-fibrotic IL-

l 3 and IL-4 transcription. The inhibition of CD 4÷ Th 1 cell expansion and the prevention o f

imbalanced CD4÷ Th2 cellular responses are, in part, actively tempered by IL -10. Top pho -

tomicrograph: haem atoxylin- and eosin-stained liver granuloma original mag nification, x

40). Botto m photom icrograph: picrosirius red-stained liver granuloma original magn ifica-

tion, x 40).




us ua l l y occu r. H ow eve r, t ype - 2 - as s oc ia t ed in f l amm at i on i nduced by t he egg

does in i t i a te c lear h i s to log ica l change s wi th in an in fec ted hos t. O ne o f these

eas i ly m easurab le h is to log ica l changes is the deve lopm ent and accum ula t ion of

hepa t ic , per ipor tal and intes t inal fibros is . The de velo pm ent o f f ibrot ic les ions

and t he i m mu no l og i ca l m echan i s ms r e spons i b le have been mo s t ex t ens ive l y

s tud i ed in t he m ur i ne mod e l o f S . m a n s o n i in fec tion . Here , i t has b een hypo th-

es i sed tha t these l es ions (of ten foun d wi th in or ne ar g ranuloma s ; s ee F igure 2)

are r espons ib le for m ain ta in ing a hos t -pro tec tive bar r ie r tha t p revent s po ten-

t i a l l y hepa t o t ox i c egg an t i gens f r om be i ng r e l ea s ed ( ev i dence f r om SC I D

m ice , e tc .) . Thi s c an t be the wh ole s to ry as

S . ja p o n i c u m - i n f e c t e d

SC I D m i ce ,

wh ich cann ot fo rm f ib ro t ic c i r cum oval les ions l ive jus t as long as in fec ted

wild- typ e animals that do fo rm f ibrot ic lesions (Che ever

e t a l .

1999) . Al tho ugh

th is m odel im pl ies tha t hepa to tox ic egg an t igens a re n o t expres sed by S . j a p o n -

i c u m i t a l s o r a i s e s t he ques t i on : w hy do f i b r o t i c l e s i ons deve l op du r i ng

infec t ion i f there i s no th ing to pro tec t the ho s t f rom? M ice in fec ted wi th S .

m a n s o n i by vacc ina t ion wi th S . m a n s o n i eggs / IL-12 also fai l to d evelop f ibrot ic

les ions a roun d hepa t i c eggs , ye t l ive desp i t e the presence and re lease of hepa-

to tox ic an tigens (Wyn n e t a l . 1995). I t is argue d in both o f the abo ve s tudies

( and o t he r s no t m en t i oned he r e ) t ha t the de ve l opme n t o f co l lagen - con t a i n ing

f ibro t i c les ions a round depos i t ed eggs prob ably oc curs as an inev i t ab le conse-

quen ce of the type-2 granulom atous response . Thi s func t ion requi res the ac t ion

of prof ibro t i c cy tok ines induced du r ing the r esponse . I t cou ld a l so be deb a ted

tha t the ba lanced , in f l am m atory type-2 im m un e response ( l ead ing to f ib ro t ic

les ions ) m ight be an ev olu t ionary adapta tion , mu tua l ly indu ced by bo th hos t

and paras i te to ensu re tha t min ima l hos t m or ta l ity co inc ides w i th m axim al egg

t ransmiss ion . F ina lly , the f ib ro t ic l es ions m ay serve a secon dary func t ion in

prevent ing the escape o f hepa to tox ic egg an t igens ( a lthough hos t an t ibodies a re

a l so capable of p ro tec t ing f rom hepatoce l lu la r dam age; Du nne e t a l . 1991) that

i s no t nece ssary for the surv iva l o f a ll s c h i s tosom e- infec ted hos ts .

Th e deve lopm ent o f f ib ro t i c les ions dur ing sch i s tosomias i s has , thus f a r ,

bee n di rect ly att ributable to the act ivit ies o f the pro-f ibrot ic me diators IL-4, IL-

13 and TGF-~ . S tud ies publ i shed dur ing the l a te 1990s an d shor t ly a f t e r the

t u rn o f t he m i l lenn i um con c l us ive l y dem ons t r a ted t hat I L - 13 w as t he mo s t

impo r tan t cy tok in e d i rec t ly respons ib le for th i s t i ssue f ib rosi s dur ing m ur ine

s ch i s t o s omi as i s ( C h i a r amon t e e t a l . 1999 ; M cK enz i e e t a l . 1999).

C h i a r amon t e e t a l . ( 1999 ) f u r t he r p r ov i ded ev i dence f o r IL - 13 s m echan i s m o f

act ion by show ing that this cyto kine di rect ly s timulates

i n v i t r o

cul tured f ibrob-

las ts to pr od uc e the bui lding bloc ks o f fibros is , i .e . col lage n. The refore , i t is

l ike ly tha t IL-13 , ac t ing th rough the IL -4 r ecep tor (Jankovic

e t a l .

1999) and

STAT6 (Kaplan e t a l . 1998) s igna ll ing pa thw ay d i rec t ly s t imu la tes hepa t i c -

r e s i den t f ib r ob la s ts ( deve l opm en t a l l y ma t u r e I T O ce l l s /my of i b r ob l a s ts ) o r

recrui ted via chem otaxis (W yler and P os t le thwai te , 1983) ci rculat ing fibrocytes

( B uca l a e t a l . 1 9 9 4 ) t o p r o d u c e c o l l a g e n . T h e m e c h a n i s m o f c o l l a g e n



HOST RESPONSES DURING SCHISTOSOM E INFECTIONS 85

p r o d u c t i o n i n t h e s e c el ls m a y i n v o l v e t h e T GF -[~ p a t h w a y C z a j a et a l . 1989;

Farah et al . 2 0 0 0 ; L e e e t a l . 2 0 0 1 ) a n d r e l y u p o n t h e p r o d u c t i o n o f p ro l i n e

m o l e c u l e s s u p p l ie d b y a lt e rn a t i v el y a c t i v a te d m a c r o p h a g e s H e s s e

e t a l .

2001) . A l tho ugh i t i s d i f f icu l t to mea su re the m echan i sm s l ead ing to f ib rob las t

ac t iva t ion du r ing hum an sch i s tosom ias i s , a s imi la r pa thw ay o f co l l agen p ro -

duc t ion l ead ing to pe r ipo r ta l and hepa t i c f ib ros i s p resu m ab ly occur s .

I n s u m m a r y , t h e d e v e l o p m e n t o f f ib r o t ic l e s io n s i n c o m b i n a t i o n w i t h

c i r cum ova l g ranu lom as i s l ike ly to be an inev i tab le conseq uen ce o f genera t ing

t y p e - 2 i m m u n e r e s p o n s e s a g a i n s t t i ss u e - tr a p p e d s c h i s t o s o m e e g g s . T h i s h o s t

r espon se u l t ima te ly l eads to a d i s ease s ta t e cha rac te r i s ed by ch ron ic m orb id i ty

bu t , mos t impor tan t ly , s e ldom ind uces the de t r im en ta l ca scade o f even t s l ead -

ing to dea th . Inves t iga t ing the immuno log ica l pa r t i c ipan t s and inappropr ia te

m e c h a n i s m s a s s o c i a t e d w i t h e n h a n c e d m o r b i d i t y a n d m o r t a l i t y r a t e s d u r i n g

sch i s tosom ias i s w i l l he lp ou r under s tand ing o f appropr ia te s t r a teg ies induce d

b y t h e h o s t to c o n t r o l c h r o n ic t y p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s.

4 .2 . D e v e l o p m e n t o f S e v e r e Im m u n o p a t h o l o g y D u r in g

S c h i s t o s o m i a s i s i s L i n k e d to IL - 1 0 a n d A s s o c i a te d w i t h

I n a p p r o p ria t e H i g h ly S k e w e d o r U n c o n t ro l la b l e Im m u n e R e s p o n s es

4 . 2. 1 . U n r e g ul a te d p o l a r i s e d t y p e - l - a s s o c i a t e d i m m u n e r e s p o n s e s d u r i n g

s c h i s t o s o m i a s i s l e a d t o in c r e a s e d m o r t a l it y

T h e h o s t r e s p o n s e t o s c h i s t o s o m e e g g s s h o u l d b e o n e t h a t r e c o g n i s e s t h e

des t ruc t ive na tu re o f these agen t s and r esponds appropr ia te ly in a con t ro l l ed

m anner to l imi t s eve re pa tho logy . Indeed , m os t exper imen ta l in fec t ions o f an i -

m a l s a n d n a t ur a l i n f e c ti o n s o f h u m a n s a r e a s s o c i a te d w i t h t h e d e v e l o p m e n t o f

t ig h t l y r e g u l a te d t y p e - 2 i m m u n e r e s p o n s e s d i r e c t e d a g a i n st t h e e g g . A s m e n -

t ioned ab ove , these r espon ses can l ead to f ib ro ti c t is sue l e s ions , bu t genera l ly

do no t con t r ibu te to o r r e su l t in mor ta li ty . D ev ia t ion aw ay f rom th is t igh t ly r eg -

u la ted , egg-as soc ia ted , type-2 immune r esponse l eads to pa tho log ies tha t a r e

severe and o f t en l i fe - th rea ten ing .

O n e o f t h e f ir s t r e p o r ts o f a ty p i c a l i m m u n o p a t h o l o g y l e a d in g t o s c h i st o -

s o m e - i n d u c e d d e a t h w a s m a d e i n t h e m i d - 1 9 9 0 s w h e n s c h i s t o s o m e i n f e c ti o n

s t u d ie s w e r e b e i n g p e r f o r m e d in I L - 4 - d e f i c ie n t m i c e B r u n e t et a l . 1997).

B r u n e t

et a l .

s h o w e d t h at I L - 4 - d e f i c ie n t m i c e r e s p o n d e d t o s c h i s t o s o m e i n f e c -

t io n b y g e n e r a t i n g s t ro n g l y p o l a r i se d t y p e - l , a s o p p o s e d t o ty p e - 2

in f l amm ato ry r eac t ions . Th i s type-1 in f lam ma to ry r esponse r epor ted by Brune t

et al . w a s o b s e r v e d s h o r tl y a f t er e g g d e p o s i t i o n a n d w a s d e f i n e d b y e g g - s p e -

c i f i c IFN - 7 , TN F-c t , and induc ib le n i t r ic ox ide iNO ) p roduc t ion as we l l a s a

r a p id r a te o f w e i g h t l o ss B r u n e t et a l . 1 9 9 7 ) . T h e g r a n u l o m a s t h a t f o r m e d

around t i s sue -dep os i t ed eggs in IL-4 -def lc ien t an imals w ere o f a s imi la r s i ze to




c o n t r o l , i n f e c t e d w i l d - t y p e m i c e b u t h e p a t i c f i b r o s i s w a s d i m i n i s h e d . T h e

a u t h o r s c o n c l u d e d f r o m t h e s e s t u d i e s t h a t t h e p r o n o u n c e d t y p e - l - m e d i a t e d

i n f la m m a t o r y r e a c t i o n s th a t d e v e l o p e d in t h e a b s e n c e o f I L - 4 i n c o m b i n a t i o n

wi th inc reased sys tem ic endo tox in l eve l s induced a s t a te o f cachex ia tha t l ed to

rap id mor ta l i ty (Brune t

e t a l .

1997). S ubseque n t ly , w ork f rom the s am e labo-

r a t o ry d e m o n s t r a t e d t h a t th i s r a p id m o r t a l it y ( i n t h e a b s e n c e o f I L - 4 ) w a s

I L - 1 2 a n d I F N - 7 in d e p e n d e n t ( L a F l a m m e

e t a l .

2001b ; Pa t ton

e t a l .

2001) ,

as soc ia ted w i th induc ib le n i t r i c ox ide syn thase ( iNOS) dys regu la t ion (Brune t

e t a l .

1 9 9 9 a ) an d l i n k e d to d a m a g i n g p e r o x y n i tr i te p r o d u c t i o n ( L a F l a m m e

e t

a l . 2 0 0 1 a ) . H o w e v e r , I L - 4 - d e f i c i e n t m o u s e i n f e c t i o n s t u d i e s p e r f o r m e d i n

o the r l abora to r ies (Metwal i

e t a l .

1996) o r on a d i f fe ren t gene t i c backgro und

(Pearce

e t a l .

1996) d id not resul t in a s t rong d efaul t towa rds the type-1 d i rec-

t ion o r enhan ced mor ta l ity .

I t i s impor tan t to no te tha t cachex ia and e leva ted dea th r a tes obse rved in IL-

4 -def ic ien t mice a re d i r ec t ly r e la ted to in fec t ion in tens i ty . Decreas ing the

in fec t ious dose w i l l induce f luc tua t ing we igh t lo s s in IL-4 -de f ic ien t mice bu t

w i l l n o t in c r e a s e m o r t a l it y i n c o m p a r i s o n t o i n f e c te d W T a n i m a ls ( M e t w a l i

e t

a l . 1996; Brunet e t a l . 1997 ; Hof fmann e t a l . 2000) . Toge the r, these im por -

t a n t i n v e s t i g a t i o n s i n i n f e c t e d I L - 4 - d e f i c i e n t m i c e p r o v i d e d t h e f i r s t r e a l

e v i d e n c e t h a t d e v i a t i o n a w a y f r o m p r o p e r l y r e g u l a t e d t y p e - 2 i m m u n e

responses du r ing s ch i s tosomias i s cou ld be l e tha l . Immunolog ica l f ac to r s , in

add i t ion to IL-4 , a r e now be ing inves t iga ted in o rde r to a sce r ta in the i r p ro tec -

t ive ro le du r ing s ch i s tosomias i s .

An in te res ting f ind ing revea led du r ing B rune t and co l l eague s s tud ies in

i n f e c t e d I L - 4 - d e f i c i e n t m i c e w a s i n t h e l e v e l o f I L - 1 0 p r o d u c e d f r o m r e -

s t imula ted sp leen ce l l s e x v i v o (Brune t e t a l . 1997). In fec ted IL-4 -de f ic ien t

an imals , su f fe r ing f rom inc reased m or ta l i ty r a tes , had s ign i fi can t ly l e s s an t i-

g e n - s p e c i f i c I L - 1 0 p r o d u c t i o n i n c o m p a r i s o n t o c o n t r o l i n f e c t e d a n i m a l s .

C o u l d a d e c r e a s e i n I L - 1 0 p r o d u c t i o n b e r e s p o n s i b l e f o r t h e i n c r e a s e d

i m m u n o p a t h o l o g y o b s e r v e d i n I L - 4 - d e f i c i e n t a n i m a l s ? S h o r t l y a f t e r I L - 1 0

w a s i d e n ti f ie d ( M o s m a n n e t a l . 1990) as a so lub le f ac to r r e spons ib le fo r inh i -

b i ti o n o f c y t o k i n e s y n t h e s is b y T h l c e ll s, S h e r

e t a l .

(1991) inves t iga ted the

k ine t i c s o f sp leen -der ived IL-10 p rod uc t ion du r ing s ch i s tosomias i s .

S h e r

e t a l .

( 1 9 9 1 ) d e m o n s t r a t e d t h a t I L - 1 0 p r o d u c t i o n w a s r a p i d l y p r o -

duced a t a t ime concomi tan t w i th egg depos i t ion and , fu r the rmore , tha t th i s

cy tok ine r emained e leva ted in to the ch ron ic s t ages o f d i s ease . A conc lus ion

f r o m t h i s s t u d y a n d o f o t h e r s ( F l o r e s - V i l l a n u e v a

e t a l .

1 9 9 6 ; R e i s e r a n d

S tadecker , 1996) w as tha t IL-10 co un te r - r egu la ted , o r m ade anerg ic , in f l am-

m a t o r y T h l c e l l p o p u l a t i o n s a n d a l l o w e d f o r th e d e v e l o p m e n t o f st a b le ,

egg- induced , type-2 immune r esponses . Th i s f ind ing , in add i t ion to de fec t ive

I L - 1 0 p r o d u c t i o n d u r i n g t h e s t u d y b y B r u n e t

e t a l .

( 1 9 9 7 ) o f I L - 4 - d e f i c ie n t

m ice , l ed inves t iga to r s to be l i eve tha t IL-10 w as induc ed as a hos t -p ro tec t ive

c y t o k i n e d u r i n g s c h i s t o s o m i a s i s . D e f e c t s i n I L - 1 0 p r o d u c t i o n d u r i n g




s c h i s t o s o m i a s i s w e r e , t h e r e f o r e , h y p o t h e s i s e d t o c o r r e l a t e w i t h a h o s t ' s

inc reased r i sk o f deve lop ing s evere d i s ease . A se r ie s o f impor tan t s tud ies, in

b o t h m o u s e a n d m a n , c o n f i r m e d t h is h y p o t h e s i s a n d c o n c l u s i v e ly d e m o n -

s t r a ted the impor tan t r eg u la to ry ro le o f IL-1 0 dur ing s ch i s tosom ias i s .

B o s s h a r d t

e t a l .

(1997) inves t iga ted

S . m a n s o n i

i n f e c ti o n i n C B A / J m i c e .

Th is m ous e m ode l i s ac tua l ly qu i t e un ique in tha t 80 o f in fec ted an imals

deve lop a modera te d i s ease s t a te a f t e r in fec t ion (modera te sp lenomega ly o r

M SS) whereas the r emain ing 20 go on to deve lop s evere hepa tosp lenom ega ly

(HSS) . Th ese pe rcen tages o f mod era te to s evere d i s ease s ta tes s een in in fec ted

C B A / J m i c e a r e r e m i n i s c e n t o f t h e h u m a n s i tu a t io n ( l a r g er p e r c e n t a g e o f

in fec ted humans su f fe r ing f rom modera te d i s ease than s evere d i s ease s t a tes ) .

T h e i m p o r t a n t f i n d in g f r o m t h e s t u d ie s o f B o s s h a r d t

e t a l .

(1997) w as tha t the

M S S m i c e p r o d u c e d s i g n i f i c a n t l y m o r e a n t i g e n - s p e c i f i c I L - 1 0 t h a n t h e H S S

m ice espec ia l ly du r ing ch ron ic s t ages o f d i s ease . Sch i s tosom e-spec i f i c c ros s -

r eac t ive id io types ( Id ) appear to pa r ti c ipa te in the m odu la t ion o f these m ur ine

p a t h o l o g i e s , a l t h o u g h t h e t i m i n g o f I d e x p o s u r e s e e m s t o b e c r i t i c a l

( M o n t e s a n o

e t a l .

1999, 200 2) . Together, these data su ppor t the con tent ion that

de f ic ienc ies in IL-10 p rodu c t ion and Id r egu la t ion du r ing s ch i s tosom ias i s a re

i n d e e d r e l at e d t o i n c r e a se s i n t h e s e v e r i ty o f h o s t i m m u n o p a t h o l o g y .

M e c h a n i s m s t h a t r e g u l a t e I L - 1 0 p r o d u c t i o n , s u c h a s c o - s t i m u l a t i o n d u r i n g

an t igen p resen ta t ion , a r e be ing inves t iga ted in o rde r to a sce r ta in the i r ro le in

t h e d e v e l o p m e n t o f l et h al i m m u n o p a t h o l o g y ( K i n g

e t a l .

1996b ; Hernandez

e t

a l .

1 99 9 ; M a c D o n a l d

e t a l .

2002a) .

A n o t h e r r o le o f IL - 1 0 i n p re v e n t in g s e v e r e d i s e a s e w a s s u b s e q u e n t l y c o n -

f i r m e d i n a m u r i n e s t u d y w h e r e I L - 1 0 a d m i n i s t r a t i o n t o i n f e c t e d a n i m a l s

d r a m a t i c a l l y d e c r e a s e d t h e s i z e o f c i r c u m o v a l g r a n u l o m a s d u r i n g t h e a c u t e

s tages o f d i s ease (F lo res -Vi l l anueva

e t a l .

1996) . Later , Wynn

e t a l .

(1998)

dem ons t r a ted tha t in fec ted IL-10 -def ic ien t mice d i sp la yed s ign i f ican t ly la rge r

c i r cum ova l g ranu lomas than con t ro l - in fec ted W T an imals , the reby conf irming

t h e a n t i -i n f l a m m a t o r y r o l e o f t h i s c y t o k i n e d u r in g a c u t e s c h i s t o s o m i a s i s .

F ina lly , a de ta i l ed exam ina t ion o f the imm uno log ica l cha rac te r is t ic s in these

in fec ted IL-10-def ic ien t mice dem ons t r a ted tha t they deve lop inc reases in bo th

t y p e - 1 a n d t y p e - 2 i m m u n e r e s p o n s e s a n d d o i n d e e d s u f f e r e n h a n c e d m o r t a l i ty

( W y n n

e t a l .

1998) . Toge the r , these s tud ies p rov ided conv inc ing ev idence

t h a t in c r e a s e d d i s e a s e s t a t es d e v e l o p i n t h e a b s e n c e o f I L - 1 0 d u r i n g m u r i n e

in fec t ions , and sugge s t tha t IL-10 induc t ion i s e ssen t ia l fo r the deve lopm en t o f

con t ro l l ed and r egu la ted type-2 immune r esponses du r ing s ch i s tosomias i s . I s

th is the case fo r hum an sch i s tosom ias i s ?

A recen t s tudy has e legan t ly conf i rmed the ro le o f IL-10 in u r ina ry t rac t mor -

b id i ty dur ing

S . h a e m a t o b i u m

infect ion (King

e t a l .

200 1). In this investigation,

t h e a u th o r s m e a s u r e d I L - 1 0 ( a n d T N F - o 0 r e l e a se f r o m e g g - s t im u l a t e d P B M C

cul tu res ob ta ined f rom in fec ted ch i ld ren and ad o lescen t s su f fe r ing f rom m od-

e ra te to s evere b ladder wa l l pa tho logy . In a com par i son w i th age- and in fec t ion




in tens i ty -m atched contro l s, the a u thors r epor ted a s ign i f ican t ly lowe r r a tio o f

egg-spec i f i c IL-10/TNF- tx product ion f rom PB M C cul tures ob ta ined f rom the

pa t ien t s w i th severe b ladd er wal l pa tho logy . Thi s d a ta sugges t s tha t low IL-10

and h igh TNF- tx cor re la tes w i th an increased r i sk o f deve lop ing severe d i sease

dur ing sch i s tosomias i s ( see a l so Brunet

e t a l .

1997; Hof fmann

e t a l .

2000;

Bosshard t e t a l 1997). Fur therm ore , a r ece n t s tudy , exam ining the cor re la tes

of deve lop ing severe f ib ros is in adul t male popula t ions l iv ing in U gan da w ho

w er e ch r on i ca l ly i n f ec t ed w i t h S . m a n s o n i dem ons t ra ted tha t a d ef ic ienc y in

IL-10 was par t ly r espons ib le (M. Booth an d D . W. Dunne , per sona l co m m u-

n i ca t i on ) . T he r e f o r e , t he s e s t ud i e s , i n bo t h mous e and man , have now

dem ons t ra ted tha t IL-10 regula tes the deve lop me nt o f s evere pa tho logy dur ing

sch i s tosomias i s . Thi s c y tok ine presum ably exer t s i ts ac t iv ity by inducing a

s ta te o f t em porary hyporesp ons iveness or r ever sib le anergy dur ing in fec t ion

and , t he r e f o r e , p r even t s t he deve l opmen t o f s eve r e pa t ho l og i ca l r eac t i ons

caus ed by exagge r a t ed o r uncon t r o l lab l e i mm une hype r ac t i v it y (K i ng e t a l .

1996a; Malaquias e t a l . 1997; Montenegro e t a l . 1998). H yporespo ns iveness

as soc ia ted wi th IL-10 has a l so been observed for o ther he lmin th in fec t ions

( M ahan t y e t a l . 1997) sugges t ing a com m only em ploy ed hos t r egula tory str at-

egy induced dur ing chronic he lmin th in fec t ions . In te res t ing ly , a benef ic ia l

s ide e f fec t o f p ro longed , he lmin th- induced , IL-10 product ion in chronica l ly

infec ted ind iv idua ls (no t norm al ly observed in people f rom d evelop ed coun-

t r ies ) is the ab i li ty o f th i s cy tok ine to suppress a topy (van den Bigge laar e t a l .

2000). T he r o l e o f o t he r I L - 10 f am i l y me m ber s ( F i ckens che r e t a l . 2002)

dur ing sch i s tosomias i s rem ains to be de te rm ined

The re has been ex tens ive deba te con cern ing the pro tec t ive ver sus pa tho-

l og i ca l r o l e o f type - 2 i mm uno l og i ca l r e s pons es du r ing he l m i n t h in f ec t ion

(e.g . Ab bas e t a l . 1996; F inke lm an and Urban , 2001). Thi s deba te s t ems f rom

s e v e r a l f i n d i n g s i n w h i c h s e v e r e i m m u n o p a t h o l o g y i s i n d u c e d w h e n t h e

infec ted hos t inappropr ia te ly r esponds to in fec t ion wi th a type-1 po lar i sed

i m m une r e spons e . H i gh - dos e i n f ec ti on o f I L - 4 - de fi c ien t m i ce ( B r une t

e t a l .

1997), in fec t ion of IL-10/ IL-4 dou bly def ic ien t m ice (Ho f fma nn e t a l . 2000),

in fec t ion of mice made to le ran t to egg an t igens (Fa l lon and Dunne , 1999) ,

i m m u n i s a ti o n o f m i c e w i t h e g g a n t i g e n s a n d c o m p l e t e F r e u n d s a d j u v an t

(Rut i t zky e t a l . 2001), in fec t ion of C D4 ÷ T ce l l -dep le ted mice (Fa l lon e t a l .

2000a ) and co - i n f ec t ion o f

S . m a n s o n i - i n f e c t e d

m i ce w i th

T o x o p l a s m a g o n d i i

(Marshal l e t a l . 1999) a l l l ead to increased m or ta l i ty and p o lar i sed type-1

im m un e responses aga ins t the sch i s tosom e and i ts egg . In each of these exper -

i m e n t a l m o d e l s , t h e h o s t d e v i a t e s a w a y f r o m c o n t r o l l e d a n d r e g u l a t e d

T h2 - as s oc i a t ed i m m une r e s ponses . T he pa t ho l og i e s tha t deve l op unde r t he s e

condi t ions a re qu i t e severe and range f rom ex tens ive liver dam age ow ing to

impai red c i r cum oval g ranulom a format ion , cachexia , exaggera ted iNO S ac tiv -

i ty , detectab le seru m IFN - 7 and TNF-t~, to e ventua l death. In crease s in hepa t ic

neu t r oph i l and mac r ophage r ec r u i t men t and ac t i va t i on a l s o co r r e l a t e w i t h




s eve re pa t ho l ogy H of f m ann e t a l . 2001) . Interes t ingly, w he n me asure d, a l l of

the above-descr ibed a typ ica l pa tho log ies were a l so as soc ia ted wi th a defec t

n

IL-10 produ ct ion . There fore , i t i s no t jus t th e deve lopm ent o f po lar i sed

t ype - 1 a s s oc i a t ed i mmune r e s pons es t ha t p r ed i s pos es an i n f ec t ed hos t t o

e n h a n c e d m o r b i d it y a n d m o r ta li ty . T h e s e i m m u n e r e s p o n s e s m u s t a l so b e

a s s o c ia t e d w i t h a d e f i c i e n c y in I L - 1 0 p r o d u c t i o n . T h is m a y e x p l a i n w h y

e g g / IL - 1 2 - im m u n i s ed m i c e W y n n e t a l . 1995) or so m e IL-4-def ic ien t m ice

C h i a r amon t e

e t a l .

1999), w hich dev e lop type-1 im m un e responses a f t e r S.

m a n s o n i

in fec t ion , do no t d ie . In bo th o f the m odel s desc r ibed above , an t igen-

spec i fi c IL-10 i s con t inuous ly produ ced dur ing in fec t ion , wh ich coun terac t s

t he po t en t ia l ly l e tha l pa t ho l ogy o f an o ve r w he l mi ng t ype - 1 domi nan t i m m une

r e sp o n s e . E g g / I L - 1 2 - i m m u n i s e d I L - 1 0 - d e fi c ie n t m i c e q u i c k l y s u c c u m b t o

lethal pathological react ions af ter infect ion T.A. W ynn and M . Hesse, personal

com mu nica t ions ) . However , it is imp or tan t to no te tha t none o f these a typ ica l

m ur ine pa tho log ies, as soc ia ted wi th type-1 im m un e po lar isa tion , a re hom olo-

gous to mor b i d i t y m eas u r em en t s des c r ibed fo r i n f ec ted hum ans C heeve r

e t

a l .

2000).

Never the les s , there i s ev idence f rom a t l eas t one s tudy of hepa tosp len ic

pa t i en t s tha t ind ica tes increases in type-1 im m un e responses d o co r re la te w i th

a un ique f o r m o f seve r e hepa t o s p len i c d is eas e i n hum an popu l a ti ons M w at ha

e t a l .

1998). In th is s tudy , the au thors descr ibed im m uno logica l responses in

g r oups o f S . m a n s o n i - i n f e c t e d ch i l d r en and ado l e s cen t s , w i t h and w i t hou t

hepa tosp lenom egaly . Impor tan t ly , there w as l i tt le o r n o apparen t pe r ipor ta l o r

hepa t i c fib rosi s c l in ica l and u l t rasound m easure m ents , unpu bl i shed observa-

t ions ) in e i ther s tudy group . B oth o f these groups of ind iv idua l s were carefu l ly

m a t ched f o r age , p r eva lence and i n tens i ty o f i n f ec ti on and o r i g ina t ed f r om t he

s ame e t hn i c t ri be A k am ba peop le ) . T he r e f o r e , t he pu r pos e o f th is ca r e f u l l y

control led s tudy w as to iden t i fy the imm uno logical di f ferences betw een pat ients

d i sp lay ing severe hepa tosp lenom egaly min im al ly r e la ted to f ib rosi s) and those

w ho d id not . A s t r iking f inding unc ove red in this inves t igat ion was that those

ch i l d r en / ado l e s cen t s w ho s u f f e r ed s eve r e en l a r gemen t o f l i ve r and s p l een

asses sed by pa lpa t ion) had s ign i f i can t ly more type- l - as soc ia ted IFN-c t and

TNF product ion f rom an t igen-s t imula ted PBMCs in compar i son to cont ro l s .

Addi t iona lly , h igh p lasma leve l s o f sTNFR-I , sTN FR-I I and ICAM -1 were a l l

s ign i f ican t ly as soc ia ted wi th hepa tosp len om egaly . In te res ting ly , the typ e-2-

as soc ia ted cy tok ine IL-5 was nega t ive ly as soc ia ted w i th hepa tosp lenomegaly .

IL-10 p roduct ion w as n ot assay ed in this s tudy. These o bservat ions indicate that

hepatosplenomegaly, in the ab sence o f severe f ibrosis, c an be associated with ele-

va t ed t ype - l - a s s oc i a t ed i mmune r e s pons es unde r ce r t a i n cond i t i ons . O t he r

poss ib le ex plana t ions for these d i f f e rences in hepa tosp lenom egaly , such as

envi ron m enta l f ac tors and co- infec t ions wi th o ther pa thogen s Ful ford e t a l .

1991), a re cur ren t ly be ing exam ined .

An othe r r ecen t study of acu te sch i s tosom ias is a l so r epor ted the as soc ia t ion




of e leva ted type- 1 cy tok ine p rodu c t ion to s evere d i s ease (de J esu s

e t a l .

2002) .

In th is s tudy , the au thor s s tud ied PBM C cy tok ine r esponses f rom 31 Braz i l ians

w h o h a d r e c e n t l y a c q u i r e d

a S . m a n s o n i

i n f e c t i o n . B l o o d w a s d r a w n f r o m

these ind iv idua l s sho r t ly a f t e r in fec t ion and p r io r to egg depo s i t ion so tha t the

i m m u n e c o r r el a te s o f t o x a e m i c ( G a z z i n e ll i

e t a l .

1985 ; Lamber tucc i

e t a l .

2 0 0 0 ) , a c u t e s c h i s t o s o m i a s i s c o u l d b e c o m p a r e d t o t h o s e i m m u n e r e s p o n s e s

a s s o c i a t e d w i t h c h r o n i c s c h i s t o s o m i a s i s ( d e J e s u s e t a l . 2 0 0 2 ) . W h e r e a s

ch ron ic s ch i s tosomias i s was charac te r i s ed by worm-spec i f i c IL-5 p roduc t ion ,

a c u t e d i s e a s e w a s a s s o c i a t e d w i t h w o r m - s p e c i f i c I F N - 7 re s p o n s e s .

Add i t ional ly , s ignificant e levat ions in the pro- inf lam m atory c ytok ines IL-6 , IL-

l a n d T N F - t x w e r e o n l y o b s e r v e d in P B M C c u l t u r es s t i m u l a te d w i t h w o r m

an t igens co l l ec ted f rom acu te s ch i s tosome- in fec ted pa t ien t s. In a s imi la r inves -

t i g a t i o n , M o n t e n e g r o e t a l . ( 1 9 9 9 ) a l s o f o u n d d o m i n a n t T h l r e s p o n s e s i n

pa t i en ts w i th acu te s ch i s tosom ias i s .

E v i d e n c e i s m o u n t i n g f r o m s t u d i e s l i k e t h e s e t h a t s h o w s i n a p p r o p r i a t e

i n d u c t i o n o f p o l a r i s e d t y p e -1 i m m u n e r e s p o n s e s ( in t h e a b s e n c e o f I L - 1 0 ) a t

a n y s t a g e d u r in g s c h i s t o s o m i a s i s c a n l e a d to s e v e r e p a t h o l o g i c a l c o n s e -

q u e n c e s . T h e e f f e c t o f ty p e - 1 c y t o k i n e a n d a n t i b o d y r e s p o n s e s o n t h e

d e v e l o p m e n t o f im m u n o p a t h o l o g y d u r in g o t h e r h e l m i n th i n f ec t io n s h a s a l s o

recen t ly s t a r ted to a t t rac t a t t en tion . F o r exam ple , T r i c h u r i s m u r i s i n f e c t io n o f

I L - 1 0 - d e f i c ie n t o r I L - 1 0 / I L - 4 - d e fi c i e n t m i c e , w h e r e p o l a r i se d t y p e - l - a s s o -

c i a t e d i m m u n e r e s p o n s e s d e v e l o p , l e a d s to d e v a s ta t i n g p a t h o l o g i c a l c h a n g e s

a n d 1 0 0 m o r t a l it y ( S c h o p f

e t a l .

2 0 0 2 ) . W h i l e t h e a b o v e e x a m p l e i l l u s -

t ra t e s t h at t y p e - l - m e d i a t e d i m m u n o p a t h o l o g y c a n o c c u r d u r in g i n f e c ti o n

w i t h h e lm i n t h s o t h e r t h an s c h i s to s o m e s , t h e m e c h a n i s m b y w h i c h i n f e c t e d

h o s t s d e v i a t e a w a y f r o m a c o n t r o l l e d T h 2 r e s p o n s e t o w a r d s T h l - d o m i n a n t

r e a c t i o n s r e m a i n s a n i m p o r t a n t a r e a o f re s e a r c h . A s d e m o n s t r a t e d b y s e v e r a l

s t u d i e s , c o - i n f e c t i o n w i t h o t h e r p a t h o g e n s c l e a r l y m a n i p u l a t e s t h e h o s t

i m m u n e r e s p o n s e s t o h e l m i n t h s ( F u l f o r d e t a l . 1991 ; Cur ry e t a l . 1995;

M a r s h a l l

e t a l .

1 9 9 9; M w i n z i

e t a l .

2 0 0 1 ) a n d m a y b e p a r t l y r e s p o n s i b l e f o r

t h is i m m u n e i m b a l a n c e . A r e a s o f t h e w o r l d w h e r e s c h i s t o s o m e in f e c t i o n i s

e n d e m i c a r e a l s o h o t - s p o t s f o r t h e tr a n s m i s s i o n o f g e o h e l m i n t h s a n d t h e r e i s

a c l e a r p o t e n t i a l f o r i n t e r a c t i o n s a m o n g p a r a s i t e s o c c u p y i n g o v e r l a p p i n g

n i c h e s ( B o o t h

e t a l .

1998) . Add i t iona l ly , v i r a l , bac te r i a l and p ro tozoan co -

i n f e c ti o n s m a y a f f e c t m a i n t e n a n c e o f ty p e - 2 - a s s o c i a t e d i m m u n e r e s p o n s e s t o

h e l m i n th s a n d th e d e v e l o p m e n t o f i m m u n o p a t h o l o g y . E n v i r o n m e n t a l a n d

s o c i a l f a c t o r s m a y a l s o a l t er t h e d e v e l o p m e n t , m a i n t e n a n c e a n d s t a b i l i t y o f

h e l m i n t h - i n d u c e d t y p e - 2 im m u n e r e s p o n s e s . H o s t f a c t o r s s u c h as a g e ( S m i t h

e t a l .

2 0 0 1 ) a n d g e n e t i c s m a y a l s o p l a y i n f l u e n ti a l r o l e s . I n v e s ti g a t i o n s i n t o

t h e s e t o p i c s s h o u l d p r o v i d e a d d i t i o n a l i n s i g h t i n t o t h e m e c h a n i s m s r e s p o n -

s i b l e f o r i n a p p r o p r i a t e t y p e - 1 i m m u n e r e s p o n s e d e v e l o p m e n t d u r i n g

s c h i s t o s o m i a s i s .



292 K F HOFFMAN N ET AL

pro-/anti-fibrotic mediators resulted in the deposition of significantly more

hepatic collagen in the livers of infected IL-10/IL-12 doubly deficient mice and

ultimately death, in a h igh proportion o f animals. Th e type-2-asso ciated death,

during the chronic stages of infection, was presum ably due to rupturing o f gut

varices caused by fibrosis-induced hypertension and increased portal vein

pressure as evidenced by pools o f blood found in the cae cum and intestinal

cavities at autopsy Hoffm ann et al . 2000, 2001). A definitive link betw een the

developm ent of unregulated type-2 im mu ne responses and severe, f ibrosis-

related imm unop athology contr ibut ing to en hanced mortal i ty rates dur ing

schistosomiasis was there by established in this investigation.

A more recent study using cDNA microarray expression profil ing pro-

vided addit ional evidence that type-2-associated imm une responses actively

induce d the transcription of several genes involved in the fibrotic m achin ery

Hoffmann et al . 2001). The contribution o f these genes in hepatic f ibrosis-

related imm unopatho logy seems probable, as they w ere preferential ly induced

only in the infected IL-10/IL-12 animals. The type-1 polarised, IL-10/IL-4

doub ly deficient animals minimal developm ent of f ibrosis) displayed mini-

mal indu ction of these genes. Interestingly, the IL-10/IL-12 d oubly deficient

animals a lso had high detectable levels of systemic TNF-t~ as wel l as

increased recruitm ent of hepatic neutrophils also observed in infected type-

1 skewed, IL-10/IL-4 doubly deficient mice). Both TNF-t~ and activated

neutrophi ls probably affected the development of severe f ibrosis-related

imm unop atholog y Hernan dez-Pand o and Rook, 1994; Louis et al . 1998).

Therefore, the studies by H offmann

et al .

2000, 2001) su ggest that while bal-

anced Th2 responses are clearly host protective, when uncontrolled, these

responses can also cause significant dam age to the host. In fact , these reports

forma lly dem onstrate that generation of highly sk ewed or uncon trolled type-

2 polarised responses are as pathogenic as the generation of type-1 im mu ne

responses.

Additional evidence that supports the pathogenic role of uncontrollable

type-2 immune responses dur ing murine schis tosomiasis was recent ly

reported Fallon et a l . 2000b). Here, the authors infected a transgenic mo use

strain that constitutively expresses IL-9 w ith S . manson i . Althoug h no differ-

ences in parasitological burdens or fecundity were m easured in this study, the

infected t ransgenic m ice developed enhanced type-2 im mu ne responses and

suffered higher mo rtali ty rates in comparison to control infected WT mice.

Unlike the fibrosis-related patho logy obse rved in infected IL-10/IL-12 doub ly

deficient animals, the infected IL-9 transgenic mice produ ced normal equiv-

alent to controls) levels of hepatic f ibrosis. Here, the cause of death was

attr ibutable to enteropathy. Therefo re, in the m urine m odel o f schistosomia-

sis, unregulated type-2 immune responses can lead to severe pathological

consequences related to overexpression and action of profibrotic cytokines

and/or factors that induce intest inal dysfunct ion. Is there evidence that




unregula ted type-2-associa ted imm une responses induce severe pathology in

infected human popula t ions?

In the setting of chronic typ e-2 imm unological responses, the vast majori ty

of al l schistosome-infected humans do no t develop severe hepatic morbidity,

but a minor i ty (2 .5-5 ) of individuals wi l l evolve qui te severe

hepatosplenomegaly and immunopathology related to f ibrosis . Specifically,

these hepatosplenic , f ibrot ic individuals develop disease s ta tes tha t can

include hepatic and periportal f ibrosis , which leads to portal hypertension,

por ta l -sy s tem ic shunt ing of b lood vesse ls around the l iver, oesopha geal

varices, abdominal ascites and haematemesis. Hepatosplenomegaly, associ-

ated with this t issue f ibrosis , develops as a result of increased hepatic portal

and splenic vein pressures, reticuloendothelial hyp erplasia and hepatic inflam-

mation d ue to circumov al granulomas. These severely il l individuals are not

necessari ly the most heavily infected (peak levels of infection occur around

puberty), but have usually harboured the disease for the longest period of

t ime . Ul t rasound measurements have conf i rmed tha t the p rogress ion o f

hepatic and periportal f ibrosis develops with age. This has been well docu-

mented in S . japon icum- in fec ted patients where more severe f ibrosis (Grade

3) was obs erved in older individuals as com pared to you ng individuals (Grade

1) (Old s et al . 1996). Ou r cross-sectional studies in Ug anda and other inves-

t igators ' s tudies in

S . manson i

endemic areas conf i rm th is age/f ibros is

relat ionship. These f indings seem to suggest that the individuals w ho g o on to

develop severe f ibrotic-related hepatosplenomegaly later in l ife are a sub-

group of the infected population that fai l to resolve their init ial low-grade

hepatic lesions. Why?

It is possible that these people have defects in their abil i ty to counter-

regulate the detrimental effects of prolonged production of IL-4, IL-13 and

other type-2-associated imm une responses. This wou ld certainly increase the

risk of developing health complications due to f ibrosis . Exist ing evidence

from hu man genetic segregation analyses conducted in Sudan sugg ests that this

is a very l ikely hypothesis . Dessein and colleagues have elegantly demon-

strated a link betw een a major gene map ped to human chrom osom e 6q22--q23

and to those individuals w ho suffer from hepatosplenomegaly related to severe

hepatic and periportal fibrosis (Dessein et al. 1999). A candidate gene m apped

close to this chro mo som al location is one that code s for the IF N-y receptor

alpha chain. From this study, it is easy to construct a hypothesis that links

defects in IFN-y signall ing to the people suffering from severe f ibrosis . As

IFN-y is a potent anti-f ibrotic cytokine (Czaja et al . 1993), segregation of

6q22-q23 among severely f ibrotic individuals suggests that these infected

peop le cannot counter-regulate the pro-fibrotic activit ies of IL-4 and IL-13.

A more recent s tudy examining immune corre la tes re la ted to

immunopathology in chronically infected Ugandan populations has provided

firm evidence l inking high IL-4 and IL-13 levels with those adult male and



294 K F HOFFMA NN ET AL

t -I

o

r~ •M

o~ ~

=1




f e m a l e i n d i v id u a l s , r e s p e c t iv e l y , s u f fe r i n g f r o m s e v e r e fi b r o s is ( M . B o o t h a n d

D . W . D u n n e , p e r s o n a l c o m m u n i c a t io n ) . D a t a f r o m m u r i n e m o d e l s a ls o d e m o n -

s t r a t e t h a t w i t h o u t p r o p e r c o u n t e r - r e g u l a t i o n m e d i a t e d b y I F N - ~ / , a l t e r n a t i v e l y

a c t i v a t e d m a c r o p h a g e s ( s t i m u l a t e d b y I L - 4 a n d I L - 1 3 ) p r o d u c i n g c o l l a g e n

p r e c u r s o r s ( p r o l i n e ) c a n c o n t r i b u t e t o t h e p r o c e s s o f f ib r o s i s ( H e s s e

e t a l .

2 0 0 1 ) . T h e c o u n t e r - r e g u l a t o r y r o l e o f I F N - ) , h a s m o s t r e c e n t l y b e e n a l l u d e d t o

i n t h e h u m a n s e t t i n g ( H e n r i e t a l . 2 0 0 2 ) . T h e s e d a t a , t h e r e f o r e , s u g g e s t a

p r o b a b l e m e c h a n i s m b y w h i c h s e v e r e f i b r o s i s c a n o c c u r i n c h r o n i c a l l y

i n f e c t e d h u m a n p o p u l a t io n s . T h e c o m b i n a t i o n o f d e f e c t i v e IF N -~ t s i g n al l i n g

w i t h i m p r o p e r l y b a l a n c e d t y p e - 2 c y t o k i n e r e g u la t io n l e a d s t o a n e n v i r o n m e n t

s u i t a b l e f o r c o l l a g e n s y n t h e s i s, h e p a t i c a n d p e r i p o r t a l f i b r o s is , a n d e l e v a t e d

m o r b i d i t y a n d m o r t a l i ty r a te s . F r o m e x i s t i n g e v i d e n c e , t h is t y p e o f

i m m u n o p a t h o l o g y b e c o m e s m a n i f e s te d f u l ly o n l y a f t er y e a r s o f e x p o s u re t o

s c h i s t o s o m e p a r a s i t es a n d / o r a b n o r m a l h o s t r e s p o n s e s , w h i c h m a y b e m o r e

o f t e n o b s e r v e d d u r i n g t h e c h r o n i c s t a g e s o f d i s e a se . I t i s e n v i s a g e d t h a t a d d i -

t io n a l i n v e s ti g a t i o n s i n t o t h e i m m u n o p a t h o l o g y o f c h r o n i c a l l y i n f e c t e d

i n d i v i d u a l s l i v i n g i n e n d e m i c a r e a s w i l l p r o v i d e n o v e l g e n e t i c a n d e n v i r o n -

m e n t a l li n k s a s s o c ia t e d w i t h t h e d e v e l o p m e n t o f se v e r e h e p a t o s p l e n o m e g a l y

r e l a t e d t o f i b r o s i s . E x p e r i m e n t a l a n i m a l m o d e l s w i l l a l s o c o n t i n u e t o b e

i n v a l u a b l e in o u r u n d e r s t a n d i n g o f t h e p r o c e s s e s l e a d i n g t o d y s f u n c t i o n a l

i m m u n e r e s p o n s e r e g u l a t io n r e s u l ti n g i n t h e a c c u m u l a t i o n o f f i b r o si s -r e l a te d

p a t h o l o g y .

F i g u r e 3 Successful, long -term host/schistosome interexistence d epends upo n the

induction and maintenance of controlled/balanced typ e-2 imm une responses: increased

morbidity and enhanced mortality strongly associate with immune polarised/exaggerated

states. As described in this review, the va st majority o f schistosome-infected individuals

living in endem ic areas generally harbour disease states that are mildly sym ptomatic and are

often not associated with life-threatening conditions (safe zone: 90-9 5% of all infected indi-

viduals). Although these individuals present w ith som e morbidity, they are able to control

properly chronic type-2-associated immune responses and, therefore, seldom succumb to

infection-induced d eath. Studies in both animal m odels and m an have demo nstrated that the

induction and m aintenance of IL-1 0 during schistosomiasis is critical for suppressing the

developmen t of severe egg-associated pathologies, although o ther immu nological factors are

certain to participate. Current evidence suggests that individuals presenting with severely

symptom atic fo rm s of schistosomiasis fall into two ma jor subgroups: those that fail to con -

trol the dow nstream effects of chronic type-2-associated imm une responses (danger zone 2:

approximately 2.5 -5% of infected individuals) or those that develop egg-associated imm une

responses that are type-1 in nature (danger zone 1: percentage uncertain). Infection-associ-

ated characteristics and factors that prob ably contribute to severe morbidity in diverse

mou se mo dels and m an are summ arised here (photomicrograph of liver granuloma: picrosir-

ius red stain, x 40), ^, observations obtained in S . h a e m a t o b i u m - i n f e c t e d humans; *,

observations obtained in S . h a e m a t o b i u m - or S . m a n s o n i - i n f e c t e d hum ans; , observations

obtained in S . m a n s o n i - i n f e c t e d hum ans (M . Booth and D.W . Dun ne, unpublished data and

Henri e t a L 2002).



296 K F HOFFMA NN ET AL

5 C O N C L U S I O N S

In the vas t m a jo r i ty o f in fec ted ind iv idua l s, s ch i s tosom es and the i r eggs gen-

e ra l ly induce a t igh t ly r egu la ted and con t ro l l ed hos t in f l ammato ry r esponse

c h a r a c te r i se d b y t h e p r o d u c t i o n o f t y p e - 2 - a s s o c i a te d c y t o k i n e s a n d a n t i b o d ie s

d i r e c t e d a g a i n s t p a r a s i te a n t i g e n s . I n d i v i d u a l s w h o d e v e l o p th i s t y p e o f

i m m u n e r e s p o n s e m a i n t a i n c h r o n i c i n f e c t i o n s t h a t o f t e n p r e s e n t w i t h m i l d

s y m p t o m s a n d m o r b i d i t y b u t d o n o t c o r r e l a t e w i t h l i f e - t h r e a t e n i n g

i m m u n o p a t h o l o g i e s . I m p r o p e r h o s t r e g u l a t o r y o r c o n t r o l m e c h a n i s m s m a y

induce a sh i f t in th i s r e sponse tha t in s t iga tes inc reased m orb id i ty and mor ta l -

i ty r a te s a m o n g i n f e c t e d i n d iv i d u a ls . T h e m a j o r i ty o f th e s e i m p r o p e r l y

c o n t r o l l e d h o s t m e c h a n i s m s a r e c a u s e d b y i n a p p r o p r i a t e r e g u l a t i o n o f

c y t o k i n e s a n d t he i r e f fe c t o r m e c h a n i s m s . E v i d e n c e p o i n t s t o e x tr e m e i m m u n e

respon se po la r i s a tion as a ma jo r con t r ibu t ing f ac to r to som e o f the m os t l e tha l

s c h i s t o s o m e - a s s o c i a t e d i m m u n o p a t h o l o g i e s . A s i l l u s t r a t e d h e r e , u n c h e c k e d

T h l - a n d T h 2 - m e d i a t e d i m m u n e r e s p o n s e s a g a in s t s c h i st o s o m e p a r a si te s c a n

l e a d t o d e v a s t a t i n g c o n s e q u e n c e s ( F i g u r e 3 ) . T h e r e f o r e , a s e l e g a n t l y s u m -

m a r i s e d a n d p e r h a p s e v e n u n d e r s t a t e d b y R h o d e s a n d G r a h a m , w h e n

d i scus s ing

Onchocerca

in fec t ion o f ca t tl e , a p ro long ed cy tok in e b ias , ind i-

ca t ing a l ack o f imm uno lo g ica l con t ro l, is no t des i r ab le (Rh odes and Graham ,

2002) . In t e rms o f s ch i s tosomias i s , ou r r ev iew has expanded upon th i s top ic

a n d o f f e r e d e v i d e n c e t h a t s u g g e s t s p r o l o n g e d c y t o k i n e b i a s e s a r e n o t o n l y

undes i r ab le , bu t a r e , in f ac t , a l so l e tha l . S tudy ing the deve lopmen t o f s evere

imm unop a tho log y in o the r he lmin th in fec t ions w i l l de te rm ine i f th is i s a w id e-

s p re a d a n d c o m m o n p h e n o m e n o n .

A C K N O W L E D G E M E N T S

W e t h a n k t h e m a n y p e o p l e w h o h a v e c o l l a b o r a t e d w i t h o u r g r o u p s o v e r t h e

year s . W e a re e spec ia l ly g ra te fu l to those ind iv idua l s w ho have co n t r ibu ted to

t h e s u c c e s s f u l d e s i g n a n d c o m p l e t i o n o f t h e h u m a n i m m u n o e p i d e m i o l o g i c a l

f i e ld -based inves t iga t ions pe r fo rmed in Braz i l , Kenya and Uganda as we l l a s

t h o s e p e o p l e w h o w e r e i n s t ru m e n t a l i n m a n y o f th e l a b o r a t o r y - b a s e d e x p e ri -

m e n t a l s t u d i e s p e r f o r m e d b y t h e a u t h o rs a n d o u r c o - w o r k e r s .

R E F E R E N C E S

Abbas, A.K., Murphy, K.M. and Sher, A. (1996). Functional diversity of helper T lympho-

cytes.

ature

383, 787-793.




A m id , E, L ock sley, R.M., Parslow, T.G., Sadick, M., Rector, E. , Rit ter , D. an d McKerrow,

J .H. 1992). T um our necrosis factor a lpha res tores granulom as and induces paras ite

egg- l ay ing in sch i s tosome- infec ted S CID mice . Nature 356 , 604 -607 .

An gyalo s i , G. , Pancre , V. , Herno , J. and Aur iault , C. 1998). Imm uno logical response o f

ma jor h i s tocom pat ib il it y comp lex c l ass I I -de f ic i en t Abe ta o )) m ice i n fec ted by the

parasite Schistosoma man soni. Scandinavian Journal o f Immu nolology 48 , 159-169 .

Arm s t rong , J. 1965). Mat ing behav ior and deve lopm ent o f sch i s tosomes in the mou se .

Journal o f Parasitology 51 , 605-616 .

Ban chere au, J . , Briere, E , C aux , C. , Da vou st , J . , Leb ecq ue, S. , Liu, Y.J., Pulendran, B. and

Palucka, K. 2000). Imm un ob iolo gy o f dendri tic cel ls . Annual Review of lmmunology

18 , 767 -811 .

Bell, R.G. 1996). IgE , al lergies and helminth parasi tes: a new perspective on an old con un -

drum. Immunology and Cell Biology 74 , 337-3 45 .

Bergquist, N .R. and Colley, D.G . 1998). Schistosomiasis vacc ines: research to dev elop -

ment . Parasitology Today 14 , 99-1 04 .

Bird, J .J . , Brown, D.R. , Mullen, A.C. , Moskowitz, N.H., Mahowald, M.A., Sider, J .R. ,

Gajewski , T.E , W ang , C.R. and Reiner, S.L. 1998). H elper T cell differentiat ion is

cont rol led by the cel l cycle . Immunity 9 , 229-237 .

Boo th, M. , Mayo m ban a, C. and Ki lima, E 1998). The populat ion biolog y and epidemiol -

ogy of sch i s tosome and geohe lmin th i n fec t i ons among schoolch i ld ren in Tanzan ia .

Transactions of the Royal Society o f Tropical Med icine a nd Hygiene 92 , 491-4 95 .

Boros , D.L. and Warren, K.S . 1970). D elayed hypersensi t ivi ty- type granu lom a form at ion

and d ermal react ion induced a nd e l ic ited by a soluble factor isola ted f rom Schistosoma

mansoni eggs . Journal o f Experimental M edicine 132 , 488-5 07 .

Bosshardt, S.C., Freem an, G.L. , Jr ., Secor, W .E. and Colley, D.G . 1997). IL -10 defici t cor-

r el at es wi th chron ic , hyper sp l enomega ly syndrom e in male C BA /J mice i n fec ted w ith

Schistosoma mansoni. Parasite Immunology 19 , 347-35 3 .

Brunet , L.R. , Finkelman, ED ., Cheever, A.W., Kopf, M.A. and Pearce, E.J. 1997). IL-4 pro-

t ec t s aga ins t TNF-a lpha-media t ed cachex ia and dea th dur ing acu t e sch i s tosomias i s .

Journal o f Immunology 159 , 777 -785 .

Brunet , L.R. , Beall, M., Dun ne, D.W. and Pearce, E.J. 1999a). Nitr ic oxid e and the Th 2

response co m bine to prevent severe hepatic d am age dur ing Schistosoma mansoni infec-

tion. Journal o f Immunology 163, 4976--4984.

Brunet, L .R., Sabin, E.A ., Cheev er, A.W ., K op f, M .A. and Pearce, E.J. 1999b ). Interleukin

5 IL-5) i s not requi red fo r expression of a Th2 respo nse or host resi stance me chanism s

dur ing mur ine schistosomiasis man soni but does play a role in development of IL-4-pro-

duc ing non-T, non -B cel ls . Infection and Immu nity 67 , 3014-3018 .

Bu cala, R. , Spiegel, L .A. , Chesney, J ., Hog an, M. and Cerami, A. 1994). Circulat ing f ibro-

cytes def ine a new leukocyte subpopulat ion that mediates t i ssue repai r . Molecular

Medicine 1 , 71-81 .

Carm an, J.A., Pond , L . , Nasho ld, E , Wassom, D.L. and Hay es , C.E. 1992). Im m un i ty to

Trichinella spiralis i n f ec t ion i n v i t amin A-def i c i en t mice . Journal of Experimental

Medicine 175, 111-120.

Cheever, A.W. 1968). A quantitative p ost-m orte m study o f Schistosomiasis mansoni in

man. American Journal o f Tropical Medicine a nd Hygiene 17 , 38-64 .

C h e e v e r, A .W . , B y r a m , J. E . a n d v o n L i c h t e n b e r g , F . 1 9 8 5 ). I m m u n o p a t h o l o g y o f

Schistosomajaponicum infect ion in a thym ic mice. Parasite Immunology 7 , 387-398 .

Cheever, A.W. , Deb , S . and Duvall , R.H. 1989). Gran ulom a form at ion in Schistosoma

japonicum infected nud e mice: the effects o f reconsti tut ion with L3 T4 ÷ o r L y t 2+ splenic

cells. American Journal o f Tropical Med icine an d Hygiene 40 , 66-71 .

Cheever, A.W. , El toum , I .A. , And rade, Z .A. and Co x, T .M. 1993). Bio logy and patholo gy




o f Schistosoma mansoni and Schistosoma japonicum infect ions in several strains of

nude m ice . American Journal of Tropical Medicine and Hygiene 48 , 496-503 .

Cbeever , A.W. , Wil l iams, M.E. , Wynn, T .A. , F inkelman, ED. , Seder , R.A. , Hieny, S . ,

Caspar , P. and Sher, A . 1994) . An t i - IL -4 t r ea tme nt o f Schistosoma mansoni infected

m i c e i n h i b i ts d e v e l o p m e n t o f T c e l ls a n d n o n - B , n o n - T c e l ls e x p r e s s i n g T h 2

cytok ines whi l e dec reas ing egg- induced hepa t i c f i b ros i s . Journal of Immunology

153 , 753-754 .

Cheever, A.W., Jank ovic , D. , Yap, G.S., K ullberg, M .C. , Sher, A. and W ynn , T.A. 1998).

Role o f cytokines in the form at ion and down regulat ion of hepatic c i rcumo val granulo-

m as and hepatic f ibrosis in

Schistosoma mansoni infected

mice.

Memorias do Instituto

Oswaldo Cruz 93, 25-32.

Cheever, A.W. , Poindexter , R.W. and Wynn, T .A. 1999). Eg g laying i s delaye d but wo rm

fecundi ty i s normal in SC ID m ice infected wi th Schistosomajaponicum and S. mansoni

wi th o r wi thout r ecombinan t t umor nec ros i s f ac to r a lpha t r ea tment .

Infection and

Immunity 67 , 2201-2208 .

Cheever, A .W. , Hof fmann , K .E and Wynn, T .A. 2000) . Imm unop a tho logy of sch i s tosomi -

as is m ansoni in mice and men. Immunology Today21 , 465-466 .

Chiaramonte, M .G. , Donaldson, D.D., Cheever, A.W. and W ynn, T .A. 1999). An IL-13

inhibi tor bloc ks the develo pm ent o f hepatic f ibrosis d uring a T-helper typ e 2-dom inated

inf lamm atory response. Journal of Clinical Investigation 104 , 777-7 85 .

Co ffm an, R.L. and Reiner, S.L. 1999). Instruct ion, select ion, or tam pering with the odds ?

Science

284 , 1283-1285 .

Coffm an, R.L. and v on de r Weid, T. 1997). M ul tiple pathw ays for the ini tiat ion o f T helper

2 Th2) responses. Journal of Experimental Medicine 185, 373-3 75 .

Con rad, D.H. , Ben -Sasson, S .Z ., Le Gros , G. , F inkelman , ED . and Paul , W.E. 1990).

Infect ion wi th Nippostrongylus brasiliensis or injection o f ant i-IgD antibodies m arked ly

enhances Fc-receptor-med iated inter leukin 4 p roduct ion by no n-B, no n-T cell s. Journal

of Experimental Medicine 171, 1497-1508.

Cuellar , C. , Perteguer, M .J. and Ro dero , M . 2001). Presen ce of IL-4-1ike m olecu les in

l a rva l excre to ry- sec re to ry p roduc t s and c rude ex t r ac t s f rom Anisakis simplex.

Scandinavian Journal o f Immunology

53 , 483-488 .

Curry, A.J., Else, K.J., Jones, E, B anc roft , A. , Grencis, R.K . and Du nne , D.W. 1995).

Ev iden ce that cytokine-mediated imm une interact ions indu ced by Schistosoma mansoni

al ter disease outcome in mice concurrent ly infected wi th Trichuris muris. Journal of

Experimental Medicine 181, 769-77 4 .

Czaja, M.J. , Weiner, ER., Flanders, K.C. , Giambrone, M.A., Wind, R. , Biempica, L. and

Zeru, M .A. 1989).

In vitro and in vivo

associa tion of t ransforming grow th factor -beta 1

with hep atic f ibrosis.

Journal of Cell Biology

108 , 2477 -2482 .

Cza j a , M. J . , Weiner , ER. , Takahash i , S . , G iambrone , M.A. , van de r Meide , EH. ,

Schellekens, H. , Biem pica, L . and Zern, M .A. 1993). G am ma -inter feron t reatment

inhibi ts col lag en dep osi t ion in m urine schistosomiasis. Hepatology 10 , 795 -800 .

de Andres, B . , Rakasz, E. , Hage n, M., Mc Co rm ik, M.L. , M ueller , A.L. , Elliot, D . , Metwali ,

A. , Sandor, M ., Bri tigan, B.E. , Weinstock, J .V . and Ly nch , R.G. 1997). L ac k o f Fc-

epsi lo n receptors on murin e eosinophils: implicat ions fo r the func tional signif ican ce o f

elevated Ig E and eo sinop hils in parasi tic infect ions. Blood 89 , 3826-3836 .

de Jesus, A.R. , Si lva, A. , Santana, L.B . , Magalhaes, A. , de Jesus, A.A ., de Alme ida, R.E ,

Re go, M .A. , Buratt ini , M.N . , Pearce , E .J . and Carvalho, E .M. 2002). Cl inical and

im m un olog ic evaluation o f 31 patients with acute schistosomiasis m anso ni .

Journal of

Infectious Diseases 185, 98-105.

de Jon g, E.C., Vieira, E L., K alinski, E, Sc huitemaker, J.H., Tanaka, Y., W ierenga, E.A.,

Yazdanbakhsh, M . and Kapsenb erg, M.L. 2002). M icrobial com po und s selectively




Farah, I .O. , Mo la, P.W., Kariuki, T.M., Nyin do , M., Blanton , R.E. and K ing, C.L. 2000).

Repeated exposure induces periportal fibrosis in Schistosoma mansoni infected baboons :

ro l e o f TGF-be t a and IL -4 . Journal o f Immunology 164 , 5337 -5343 .

Fickenscher, H. , Hot, S., Kupers, H. , Knappe, A . , W ittmann, S. and Sticht , H. 2002). Th e

interleukin-10 fam ily o f cytokines. Trends in Imm unology 23, 89-96.

Finkelman, E D . and Urban, J .E, Jr . 2001). The other side of the coin: the protect ive role o f

the TH 2 cytokines. Journal o f Allergy an d Clinical Imm unology 107 , 772-7 80 .

Flores-Villanueva, E O ., Zheng, X.X., Strom, T.B. and Stadecker, M.J. 1996). Recom binan t

IL - l 0 and IL-1 0/Fc t reatment down-regu late egg antigen-specif ic delaye d hype rsensi -

t ivi ty react ions and eg g gran ulom a form ation in schistosomiasis. Journal o f Immunology

156, 3315-33 20 .

Fort, M.M., Cheung, J. , Yen, D., Li, J. , Zurawski, S.M., Lo, S., Menon, S., Clifford, T.,

Hunte, B . , Lesley, R. , M uch am uel, T., Hurst , S.D. , Zurawski , G. , Leach , M.W ., Gorm an,

D.M. and Ren nick, D.M. 2001). IL -25 induce s IL-4, IL-5, and IL-13 and Th2 -associ -

a ted pathologies in vivo. Immunity 15 , 985-9 95 .

Fulford, A.J. , Mbugua, G.G., Ouma, J.H. , Kariuki , H.C. , Sturrock, R.E and Butterworth,

A.E. 1991). Di f ferences in the ra te o f hepatospleno me galy due to Schistosoma mansoni

infect ion between tw o areas in Macha kos D ist rict , Kenya. Transactions of the Royal

Society o f Tropical Med icine an d Hygiene 85, 481--488.

Gazzinell i, G. , Lam bertu cci , J .R. , Katz, N. , Roch a, R.S., Lim a, M.S. an d Colley, D.G .

1985). Im m un e responses dur ing hum an schistosomiasis ma nsoni . XI . Im m uno logic

status o f pat ients with ac ute infect ion s and a fter treatment. Journal o f Immunology 135,

2 1 2 1 - 2 t 2 7 .

G rzy ch, J.M., Pearce, E. , Cheever, A. , Caulada, Z.A . , Caspar, E , Heiny, S. , Lew is, E and

Sher, A. 1991). Egg deposit ion is the m ajor st imulus fo r the production o fT h 2 cytok ines

in m urine schistosomiasis mansoni . Journal o f Immunology 146, 1322-1327.

Haisch, K. , Schramm , G. , Falcone, EH . , Alexander, C. , Schlaak, M . and Haas , H. 2001).

A g l y c o p r o t e i n f r o m Schistosoma mansoni eggs b inds non-an t igen- spec i f i c

immunoglobul in E and r e l eases i n t e r l euk in-4 f rom human basophi l s . Parasite

Immunology 23 , 427 -434 .

Hayashi, N., Matsui, K., Tsutsui, H., Osada, Y., Mohamed, R.T., Nakano, H., Kashiwamura,

S. , Hy od o, Y. , Takeda, K . , Ak ira, S. , Hada, T. , Hig ashino , K. , Kojima, S. and Nakanishi,

K. 1999). Ku pffer cel ls fro m Schistosoma mansoni infected m ice part icipate in the

pro m pt type 2 differentiation o f hepatic T cel ls in respon se to w orm antigens. Journal of

Immunology 163, 6702-67 11 .

Henri , S. , Chevil lard, C. , Mergani , A. , Paris, E, Gaudart , J . , Camilla, C. , Dessein, H. ,

M ontero, E , Elwali , N.M .A. , Saeed, O.K., M agzo ub, M . and Dessein, A.J . 2002).

Cy tokine regulat ion of peripor ta l f ibrosis in hum an Schistosoma mansoni: I F N - g a m m a

is associated w ith protection ag ainst fibrosis and TN F-a lph a w ith aggravation o f disease.

Journal o f Immunology 169 2) , 929-936.

H em an dez , H.J. , W ang, Y. , Tzellas, N . and Stadecker, M .J. 1997). Ex press ion of class II ,

but not c lass I , m ajor histocom pat ibi l ity comp lex molecules i s required for granulo ma

format ion in infect ion wi th Schistosoma mansoni. European Journal o f Immunology 27,

1 1 7 0 1 1 7 6 .

H em an dez , H.J., Sharpe, A.H . and Stadecker, M.J. 1999). Experimental m urine schisto-

somias i s i n t he absence of B7 cos t imula tory molecu les : r ever sa l o f e l i c i t ed T ce l l

cy tok ine p rof i le and pa r t ia l i nh ib i ti on o f egg g ranu lo m a format ion . Journal o f

Immunology 162, 2884-28 89 .

Hem ande z-Pand o, R. and Ro ok, G.A. 1994). T he role of TN F-alpha in T-cel l-mediated

inf lamm at ion depends on the TH 1/TH2 cy tok ine bal ance. Immunology 82 , 591-595 .

Hesse, M., Modolel l , M., La Flamme, A.C. , Schito, M., Fuentes, J .M., Cheever, A.W.,



HOST RESPONSES DURING SCHISTOSOME INFECTIONS 3 1

Pearce, E.J. and Wynn , T.A. 2001). Differential regulation o f nitric oxide synthase-2 a nd

arginase-1 b y type 1/ type 2 cytokine s in vivo: granulomatous pa tho logy is shaped by the

pattern of L-arginine metabol i sm.

Journal o f Immunology

167 , 6533 -6544 .

Hof fm ann , K .E , Cheever, A .W. and W ynn, T .A. 2000) . IL -10 and the danger s o f imm une

polar izat ion: excess ive type 1 and type 2 cytokine responses induce dis t inct forms of

l e th a l i m m u n o p a t h o l o g y i n m u r i n e s c h i st o s o m i a si s . Journal o f Immunology 164,

6 4 0 6 - 6 4 1 6 .

H offm ann , K.F. , M cCa rty, T.C. , Segal , D.H., C hiaramonte, M., Hesse, M ., Davis, E.M.,

Cheever, A.W., Meltzer , P.S. , M orse, H.C. , 3rd and W ynn , T.A. 2001). D isease f inger-

print ing w ith cD N A micro array s reveals dist inct gen e expression profi les in lethal typ e

1 and typ e 2 cytokine-mediated inflam m atory react ions.

FASEB Journal

15 , 2545-2547 .

Holland, M .J., Harcus, Y.M ., Riches, P.L. and Maizels, R.M . 2000). Proteins secreted by the

parasi t ic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses .

European Journal o f Immunology

30 , 1977-1987 .

Iaco m ini , J ., Ricklan, D.E. and Stadecker, M.J. 1995). T cel ls expre ssing the gam m a delta

T ce l l r ecep tor a r e no t r equ i r ed fo r egg granu loma format ion in sch i s tosomias i s .

European Journal of Immunology 25 , 884-888 .

Jacobs, W., Deelder, A. and Van Marck, E. 1999a). Schistosomal gran ulom a modulat ion. II .

Spec i fi c imm unogen ic ca rbohydra t es can m odula t e sch i s tosome-egg-an t igen- induced

hepa t ic g ranu lom a format ion . Parasitology Research 85, 14-18.

Jacobs , W. , van Dam , G. , Bog ers , J ., Deelder , A. and Van M arck, E . 1999b). Schis tosom al

granulom a mod ula ti on . I . Schistosoma mansoni w o r m a n tig en s C A A a n d C C A p r im e

egg-ant igen- induced hepat ic granuloma format ion. Parasitology Research 85 , 7 -13 .

Jank ov ic, D. , Cheever, A.W., Kullberg, M .C. , W ynn , T.A. , Yap, G. , Caspar, E, L ew is, E A .,

Clynes , R. , Ravetch, J .V. and Sher , A. 1998). CD 4 ÷ T cel l-mediated granulom atous

path olog y in schistosomiasis is downregulated by a B cel l-dependent m ech anism requir-

ing Fc rece ptor signaling. Journal o f Experimental M edicine 187, 619-62 9 .

Jankovic, D. , Kullberg, M.C. , Noben-Tranth, N. , Caspar, E, Ward, J .M., Cheever, A.W.,

Paul, W.E. and Sher, A. 1999). Sc his tosom e- infected IL-4 recepto r kno cko ut KO )

mice, in cont ras t to 1L-4 KO mice, fa il to develop gran uloma tous patholo gy whi le ma in-

ta ining the sam e lym pho kine express ion profi le . Journal o f Immunology 163 , 337-3 42 .

Jank ov ic, D. , Kullberg, M .C. , Noben-Trauth, N. , Caspar, E, Paul , W .E. and Sher, A. 2000).

Sing le cell ana lysis reveals that IL-4 receptor/Stat6 signaling is not required for the in

vivo o r in vitro deve lopment o f C D4 + lym phocy tes wi th a T h2 cy tok ine p rof il e. Journal

of Immunology 164 , 3047-3055 .

Kaplan, M .H., W hitf ield, J .R. , Bo ros, D.L. and Grusby, M.J. 1998). Th 2 cells are required

for t he Schistosoma mansoni e g g - i n d u c e d g r a n u l o m a t o u s r e s p o n s e . Journal of

Immunology 160, 1850-1856.

Karanja, D.M ., Colley, D.G., Nahlen , B.L. , Oum a, J.H. and Secor, W.E. 1997). Studies on

schistosomiasis in western Kenya: I . Ev iden ce for imm une-faci li tated excretion o f schis-

tosome eggs f rom pat ients wi th Schistosoma mansoni a n d h u m a n i m m u n o d e f ic i en c y

vi rus co infect ions . American Journal o f Tropical Medicine and H ygiene 56 , 515 -521 .

King, C .L. , Medhat , A . , Malhotra, I . , N afeh, M ., Helmy, A. , Khaudary, J . , Ibrah im, S. , E1-

Sherbiny, M ., Za ky , S., Stupi, R.J., Brustoski, K., Shehata, M . and Shata, M.T. 1996a).

Cy tokine cont rol of paras ite-specif ic anerg y in hum an ur inary schis tosomiasis . IL-1 0

mo dulates lym pho cyte reactivity.

Journal o f Immunology

156 , 4715 -4721 .

King, C.L. , Xianli, J . , June, C.H. , Ab e, R. and Lee, K.P. 1996b). C D2 8-de ficient m ice gen-

erate an impai red Th 2 response to Schistosoma mansoni infection. European Journal o f

Immunology 26 , 2448-2455 .

King, C .L. , Malhotra, I . , M ung ai , P., W amachi, A . , Kioko , J ., Muchiri , E. an d Ou m a, J.H.

2001) . Schistosoma haema tobium induced ur ina ry t r ac t morb id i ty cor r e l a t es wi th




increased tum or necrosis factor-alpha a nd diminished interleukin-10 production. Journal

o f Infectious Diseases 184, 1176-1182.

Kovacs, E.J. (1991). Fibrogenic cytokines: the role of im m une m ediators in the development

o f sc ar t issue. Immunology Today 12, 17-23.

La F lamm e, A.C. , Patton, E .A. , Baum an, B. and Pearce , E .J. (2001a) . IL-4 plays a crucia l

role in regulat ing oxidat ive damage in the l iver dur ing schis tosomiasis . Journal of

Immunology 166, 1903-1911.

La Flam m e, A.C. , Patton, E.A . and Pearce, E.J. (2001b). R ole of ga m m a interferon in the

patho gen esis o f severe schistosomiasis in intede uk in-4-d eficien t mice.

Infection and

Immunity 69 , 7445-7452 .

Lam bertuc ci , J.R. , Serufo , J .C., G erspacher-Lara, R. , Raye s, A.A ., Teixeira, R. , Nob re, V.

and Antunes, C .M. (2000). Schistosoma mansoni: assessment of morbidi ty before and

after c ontrol. Acta Tropica 77, 101-109.

Le Riche, W.H. (1967) . Wo rld incidence and prevalence of the m ajor comm unicab le dis-

eases. In: Health o f Mankind pp. 1-42. Bo ston: Li tt le , Brow n Co.

Lee, C.G. , Homer, R.J. , Zhu, Z. , Lanone, S. , Wang, X. , Kotel iansky, V. , Shipley, J .M.,

Gotwals, P., Noble, P., Chen, Q., Senior, R.M. and Elias, J.A. (2001). Interleukin-13

indu ces tissue f ibrosis b y select ively st imulat ing and activating transfo rm ing grow th

factor beta( I ) . Journal o f Experimental M edicine 194 , 809-82 1 .

Lo uis, H. , Van Laethem , J.L. , Wu, W., Quert inmont, E. , Degraef, C. , Van den B erg, K. ,

De m ols, A. , Go ldm an, M ., Le Moine, O. , Geerts, A. and D eviere, J . (1998). Interleukin-

10 co ntro ls neutrophilic infiltration, he pa toc yte proliferation, an d liver fibrosis indu ce d

by ca rbo n tetrachloride in mice. Hepatology 28 , 1607-1615 .

Lund y , S .K . , Lerman , S .P . and B oros , D .L . (2001). So lub le egg an t igen- st imula t ed T

he lpe r l ymph ocy te apoptos i s and ev idence fo r ce l l dea th m edia ted b y FasL(+) T and B

ce l l s dur ing mur ine Schistosoma mansoni i n f ec t i on . Infect ion and Immuni ty 69,

2 7 1 - 2 8 0 .

M acD on ald , A.S., Straw, A.D., Bau ma n, B . and Pearce, E.J. (2001). C D8-den dritic cell acti-

vat ion status plays an integral role in influencin g Th 2 resp ons e development. Journal of

Immunology 167, 1982-1988.

MacDonald, A.S. , Pat ton, E.A. , La Flamme, A.C. , Araujo, M.I . , Huxtable, C.R. , Bauman,

B. and Pearce , E .J . (2002a) . Im pai red Th2 dev elopm ent and increased mor ta l i ty dur ing

Schistosoma mansoni infect ion in the absence o f CD 40/C D1 54 interaction. Journal of

Immunology 168 , 4643 -4649 .

MacDonald, A.S. , Straw, A.D., Dalton, N.M. and Pearce, E.J. (2002b). Cutt ing edge: Th2

response ind uct ion by dendr it ic cell s: a role fo r CD40. Journal of Immunology 168

5 3 7 - 5 4 0 .

M a h a n t y , S . , R a v i c h a n d r a n , M . , R a m a n , U . , J a y a r a m a n , K . , K u m a r a s w a m i , V . a n d

Nutm an, T .B . (1997) . Regu la t ion o f pa ras i te an t igen-dr iven imm une r espo nses by

in t e r leuk in-10 ( IL -10) and IL -1 2 in l ym pha t i c f i la r ia s i s. Infection and Imm unity 65,

1 7 4 2 - 1 7 4 7 .

Malaquias, L.C. , Falcao , P.L. , Si lveira, A .M ., Gazzinel li , G. , Prata, A. , Coffm an, R.L. ,

Pizziolo , V. , Sou za, C.P., Colley, D.G . and Correa-Oliveira, R. (1997). C ytok ine regula-

t ion of human imm une r esponse t o Schistosoma mansoni: analys is of the role o f IL-4,

IL-5 and IL-1 0 on per ipheral bloo d m ono nuc lear cel l responses. Scandinavian Journal

o f lmmunolo logy

46 , 393-398 .

Marshall , A.J. , Brunet , L.R. , van Gessel , Y. , Alcaraz, A. , Bliss, S.K. , Pearce, E.J. and

Denk ers, E .Y. (1999). Toxoplasma gondii and Schistosoma mansoni synergize to pro-

mo te hepatocyte dysfunct ion associa ted wi th high levels o f plasm a TNF -alpha and ear ly

death in C57B L/6 mice. Journal of lmm unolog y 163, 2089-209 7 .

Mathew, R.C. and Boro s, D.L . (1986). A nti-L 3T 4 antib od y treatm ent suppresses hepatic



HO ST RESPONSES DURING S HISTOSOME INFE TIONS 3 3

g r a n u l o m a f o r m a t i o n a n d a b r o g a t e s a n t i g e n - i n d u c e d i n t e r l e u k i n - 2 p r o d u c t i o n i n

Schistosoma mansoni infection. Infection and Immunity 54 , 820-826 .

McK enzie, G.J. , Fallon, P.G. , Em son , C.L. , Grencis, R.K . and M cK enz ie, A .N. (1999).

Sim ultaneo us disruption o f interleukin (IL)-4 and IL-13 defines individual roles in T

he lpe r ce l l t ype 2 -media t ed r esponses . Journal of Experimental Medicine 189,

1565-1572 .

Metwali , A . , Eltiott , D . , Blum , A.M ., Li , J . , Sandor, M ., Lync h, R. , Noben-Trauth, N. and

W einstock, J .V. (1996). Th e granulomatous response in mu rine

Schistosomiasis mansoni

does no t swit ch t o Thl i n IL -4-def i c ien t C57B L/6 m ice . Journal oflmmunology 157,

4546--4553.

M ontenegro , S .M. , Miranda, E , Ab ath, EG . , Teixeira , K.M. , Cout inho, E .M. , Dom ingues ,

A.L . , Do m ingu es, L. , Brinkman, J . , Goncalves, I ., Mahanty, S. , Sher, A. an d W ynn , T.A.

(1998). P re l iminary r esu lt s on t he r egu la to ry ro l e o f IFN-g am m a and IL -10 hum an

schistosomiasis mansoni.

Memorias do Instituto Oswaldo Cruz

93, 173.

M on tene gro, S.M., Miranda, P., Mahanty, S. , Ab ath, EG ., Teixeira, K.M ., Cou tinho , E.M.,

Br inkman, J . , Goncalves , I . , Domingues , L .A. , Domingues , A.L. , Sher , A. and Wynn,

T.A. (1999). C ytokine prod uct ion in acute versus ch ronic hum an schis tosomiasis m an-

soni : the cro ss- regulatory role of inter feron-gam m a and inter leukin-10 in the responses

o f peripheral blo od mo no nu clea r cel ls a nd splen ocy tes to parasi te ant igens. Journal of

Infectious Diseases 179, 1502-1514.

M ontes ano , M.A ., Colley, D.G., Eloi-Santos, S. , Freem an, G.L. , Jr . and Secor, W.E. (1999).

Ne on atal idio typ ic exposure alters subsequent cytokine, pathology, an d survival patterns

in experimental Schistosoma mansoni infections. Journal of Experimental Medicine

1 8 9 , 6 3 7 ~ 4 5 .

M on tesano , M.A ., Colley, D.G., Willard, M .T., Freem an, G.L. , Jr. and Secor, W.E. (2002).

Idioty pes expressed early in experimental Schistosoma mansoni infect ions predic t c l in-

ical outco m es o f chronic disease.

Journal of Experimental Medicine

195, 1223-1228.

Moser , M . and M urphy, K.M. (2000) . D endr i t ic cel l regulat ion o f TH 1-TH 2 development .

Nature Immunology 1, 199-205.

M osm ann, T .R. and Coffm an, R.L. (1989a) . Heterog enei ty of cytokine secretion patterns

and funct ions o f helper T cel ls .

dvances in Immunology

46, 111-147.

M osm ann, T .R. and Coffma n, R.L. (1989b). TH1 and TH 2 cell s: d i f ferent patterns of lym -

pho kine secret ion lead to different func tional properties.

nnual Review of Immunology

7 , 145-173 .

M osm ann , T.R. , Sch um ache r, J .H. , Fiorentino, D .E, Leverah, J ., M oore , K.W. and Bon d,

M.W. (1990) . I sola t ion of mo noclon al antibodies speci fic fo r IL-4, IL-5, IL-6, and a new

Th2-speci f ic cytokine ( IL-10) , cytokine synthes is inhibi tory factor , by us ing a sol id

phase radioimmunoadsorbent assay. Journal oflmmunology 145, 2938-29 45 .

Mulvihi ll , C.A . and Bu m ett , J .W. (1990). S w im m er s i tch: a cercarial dermatit is .

Cutis

46,

2 1 1 - 2 1 3 .

Murail le, E. and Leo, O. (1998). Revisi t ing the Thl/Th2 paradigm. Scandinavian Journal

oflmmunolology

47, 1-9.

M urph y, K.M., O uy ang , W., Farrar , J .D. , Yang, J ., Ran gan ath, S. , As nag li , H., Afkarian, M .

and M urph y, T.L. (2000). S ignaling an d transcription in T helpe r development.

nnual

Review of Immunology 18, 451--494.

M wa tha, J .K. , Kimani, G. , Kam au, T., M bug ua, G.G., Ou m a, J.H. , Mu m o, J., Fulford, A.J.,

Jones, EM., Butterworth, A.E. , Roberts, M.B. and Dunne, D.W. (1998). High levels of

TNF, soluble TN F receptors , soluble ICA M -1, and IFN -gam m a, but low levels o f IL-5,

are associated with hepatosplenic disease in hu m an schistosomiasis mansoni . Journal of

Immunology

160, 1992-1999.

M winz i , EN ., Karanja, D.M., Colley, D.G., O rago , A.S. and Secor, W .E. (2001). Cellular




imm une responses of schis tosomiasis patients are a ltered by hum an imm uno def ic ienc y

vi rus type 1 coinfect ion. Journal oflnfectious Diseases 184, 488--496.

Ok ano , M., Satoskar, A.R . , Nishizaki , K. , Ab e, M . and H am , D.A ., Jr . 1999). Ind uctio n o f

Th2 responses and IgE i s largely due to carbohydrates funct ioning as adjuvants on

Schistosoma mansoni

egg antigens.

Journal of lmmunology

163, 6712--6717.

Ok ano , M., Satoskar, A.R. , Nishizaki , K . and Ham , D.A ., Jr . 2001). Lacto-N -fuco pen taose

I I I fo u n d o n

Schistosoma mansoni

egg ant igens funct ions as adjuvant for proteins by

inducing Th2 - type response.

Journal of Immunology

167 , 442-4 50 .

Olds, G .R., Olveda, R., W u, G., W iest, P., M cGarvey , S., Aligui, G ., Zh an g, S., Ramirez, B.,

Dan iel, B ., Peters, P., R om ulo , R., Fevidal, P., Tiu, W., Yua n, J. , D om ing o, E. an d Bias,

B. 1996). Im m un ity and m orb idi ty in schistosomiasis j apo nicu m infect ion. American

Journal of Tropical Medicine and Hygiene 55, 121-126.

Padrid, P.A. , Mathur, M., Li , X. , Herrmann, K. , Qin, Y. , Cattamanchi , A. , Weinstock, J . ,

E l l io t t , D . , Sper li ng , A . I . and B lues tone , J .A . 1998) . C TL A 4Ig inh ib i ts a i rway

eosinophil ia and hyperresponsiveness by regulat ing the development of T hl /T h2 subsets

in a mur ine model of as thma. American Journal of Respiratory Cell and Molecular

Biology 18 , 453-4 62 .

Papiernik, M. 2001). Na tural CD 4 ÷ CD 25 ÷ regulatory T cell s. Thei r role in the c ont rol o f

superantigen responses. Immunological Review 182, 180-189.

Park, M.K., Hoffmann, K.F. , Cheever, A.W., Amichay, D. , Wynn, T.A. and Farber, J .M.

2001). Pat terns of chem okine express ion in mo dels of Schistosoma mansoni inf lam-

m at ion and infect ion reveal re la tionships betw een typ e 1 and typ e 2 response s and

chemokines in vivo Infection and Immunity 69 , 6755-6768 .

Parra, J .C. , Dou ghty , B. , Colley, D.G . and Gazzinell i, G. 1992). H um an schistosomiasis

mansoni : s tudies on

in vitro

granu lom a modulation.

Memorias do Instituto Oswaldo

Cruz 87 Suppl 5 ), 79-81 .

Patton, E .A. , Brunet, L.R. , La Flam m e, A.C. , Pedras-Vasconcelos, J . , Kopf, M . and Pearce,

E.J. 2001). Severe schistosomiasis in the abse nce of interleukin-4 IL-4 ) is IL- 12 inde-

pendent. Infection and Immunity 69 , 589-5 92 .

Pearce, E.J. and Reiner, S.L. 1995). In du ction of Th 2 respon ses in infect iou s diseases.

Current Opinion in Immunology

7 , 497 -504 .

Pearce , E . J . and Sher, A . 1987) . M echani sm s o f imm une evas ion in sch i s tosom ias is .

Contributions to Microbiology and Immunology

8 , 219-23 2 .

Pearce, E.J., Caspar, P., G rzyc h, J .M., Lewis, F.A. and Sher, A . 1991). Do w nreg ulat ion of

T h l c y t o k i n e p ro d u c t i o n a c c o m p a n i e s i n d u c t io n o f T h 2 r e s p o n s e s b y a p a r a si ti c

helminth, Schistosoma mansoni Journal of Experimental Medicine 173, 159-166.

Pearce, E.J. , Cheev er, A., Le on ard , S., Cov alesky, M., Fernandez-B otran, R., Kohler, G . and

Kop f , M. 1996) . Schistosoma mansoni i n IL -4-def i c i en t mice . International

Immunology

8 , 435 -444 .

Rao , K.V. , Chen, L . , Gnanasekar, M . and Ram aswa m y, K. in press). Cloning and cha rac-

terization o f a calcium-binding, histamine-releasing protein fro m Schistosoma mansoni

Journal of Biological Chemistry

Re ad, S. and Powrie, E 2001). CD4 +) regulatory T cells . Current Opinion in Immunology

13 , 644-64 9 .

Reid, S.D. , Penna, G. and Adorini, L. 2000). Th e control of T cel l respo nses by dendrit ic

cell subsets.

Current Opinion in Immunology

12, 114-121.

Reis e Sousa, C. , Sher, A. and K ay e, P. 1999). Th e role of dendrit ic cel ls in the inductio n

and regulat ion o f im m un ity to m icrobia l infect ion. Current Opinion in Immunology 11,

3 9 2 - 3 9 9 .

Reiser , H. and S tadecker , M.J . 1996). C ost imulatory B7 molecu les in the pathogenesis of

in fec t ious and au to immune d i seases .

New England Journal of Medicine

335 ,



HOST RESPONSES DURING SCHISTOSOME INFECTIONS 3 5

1369-1377 .

Rhod es , S .G. and Graham , S .E (2002) . I s t im ing impo r tant for cytok ine polar izat ion?

Trends in Imm unology 23 , 246-249 .

Ri tter , D.M . and M cKerrow, J .H. (1996). Intercel lular adhesion m olecule 1 i s the m ajor

adhes ion mo lecu le expressed dur ing sch i s tosome granu loma format ion . Infection and

Immunity 64, 4706--4713.

Ro ma gnan i , S . (1991a). Hu m an TH1 and TH 2 subsets : d oub t no more. Immunology Today

12 , 256 -257 .

Ro m agn ani , S. (1991b). T ype 1 T helpe r and type 2 T helpe r cel ls: functions, regulat ion and

ro l e i n p ro t ec t i on and d i sease . International Journ al o f Clinical and Laboratory

Research 21 , 152-158 .

Roncarolo, M.G. , Bacchet ta , R. , Bordignon, C. , Narula , S . and Levings , M.K. (2001) .

Ty pe 1 T reg ulatory cel ls. Immunological Review 182, 68-79.

Ru m bley, C.A . , Zekavat , S.A. , Sug aya , H. , Perrin, EJ. , Ra m ada n, M.A . and Phill ips, S.M.

(1998). Th e sch istosom e gran ulom a: characterizat ion of lym ph oc yte migration, act iva-

t ion, an d cytok ine product ion. Journal o f Immunology 161 , 4129 -4137 .

Ru m bley, C.A. , Sug aya , H. , Zekavat, S.A. , E1 Refaei, M., Perrin, E J. and Phil lips, S.M.

(1999) . Ac t ivated eosinophi l s are the m ajor source o f Th2 -associa ted cytokine s in the

sch i s tosome granuloma. Journal o f Immunology 162, 1003-1009.

Rumbley , C .A. , Sugaya , H . , Zekava t , S .A . , Pe r r in , P . J . and Ph i l l i ps , S .M. (2001) .

E l i m i n a t i o n o f l y m p h o c y t e s , b u t n o t e o s i n o p h i l s , b y F a s - m e d i a t e d a p o p t o s i s i n

mur ine sch i s tosomias i s . American Journal of Tropical Medicine and Hygiene 65,

4 4 2 - 4 4 9 .

Rut itzky, L . I . , Hern andez, H.J . and S tadecker, M.J . (2001) . Th l -po lar iz ing imm unizat ion

with egg antigens correlates w ith severe exacerbation o f im m un op atho log y and death in

sch i s tosome in fec t ion .

Proceedings of the Nat ional Aca dem y o f Science USA

98,

13243-13248 .

Sabin, E.A. , Kopf, M.A. and Pearce, E.J. (1996). Schistosoma mansoni egg- induced ea r ly

IL-4 produc t ion i s dependent upon IL -5 and eos inophi l s . Journal of Experimental

Medicine 184, 1871-1878.

Sch opf, L.R. , H offm ann , K.F. , Cheever, A.W., Urban, J .E, Jr . and W ynn , T.A. (2002). IL -10

is critical fo r ho st resistance an d survival during gastrointestinal he lm inth infection.

Journal o f Immunology 168, 2383-239 2 .

Seder, R.A. and Paul , W.E. (1994) . Acquis i t ion of lym pho kine-pro duc ing phen otype by

C D 4 ÷ T cells. Annual Review of Immunology 12 , 635-67 3 .

Sher, A. , Fiorentino, D. , Caspar, E , Pearce, E. and Mo sm ann , T. (1991). Prod uctio n of IL -

l 0 b y C D 4 ÷ T lym pho cytes corre la tes wi th do wn -regulat ion of Th 1 cytokine synthes is

in helm inth infect ion. Journal o f Immunology 147 , 2713 -2716 .

Smith, E , Dun ne, D.W. and Fal lon, E G . (2001). D efect ive in vivo induct ion o f funct ional

type 2 cy tok ine r esponses i n aged mice . European Journal o f Immunology 31,

1495-1502 .

Sornasse, T., La ren as, EV., Davis, K.A., de Vries, J.E. and Yssel, H . (1996). Differentiation

and s tabil ity o fT helper l and 2 cel ls der ived f rom naive hum an neonatal CD 4 ÷ T cells,

ana lyze d at the single-cell level. Journal o f Experimental M edicine 184, 473--483.

Subram anian, G ., K azu ra, J.W., Pearlman, E., Jia, X ., M alhotra, I. an d King, C.L. (1997).

B7-2 r equir ement fo r he lmin th- induced granu lom a format ion and C D4 type 2 T he lpe r

cel l cy tokin e expression. Journal o f Immunology 158 , 5914 -5920 .

Takeda, K. , Tanaka, T. , Shi , W ., M atsum oto, M ., M inam i, M., Kashiwamura, S. , Nakanishi,

K. , Yoshida, N. , K ishim oto, T. and Akira, S. (1996). Essential role o f Stat6 in IL- 4 sig-

nalling. Nature 380 , 627-630 .

Tom s, C. and Pow rie, F. (2001). Co ntrol of intest inal inflam m ation by regu latory T cel ls .




Microbes and Infection

3 , 929-93 5 .

Urban, J .E , Jr ., Noben-Trauth, N. , Schop f, L. , Madden, K.B. and Fink elm an, ED . 2001).

Cut t ing edge: IL -4 receptor expression by no n-bo ne marrow -der ived cell s i s required to

exp el gastrointest inal nem atod e parasi tes. Journal oflmmunology 167 , 6078 -6081 .

van den B iggelaar, A .H. , van Ree, R. , Rod rigues , L.C . , Lell , B. , Deelder, A.M ., Kremsner,

P .G . and Yazdan bakhsh , M. 2000). De creased a topy in ch i ld ren i n fec ted wi th

Schistosoma haematobium: a role for paras i te- induced inter leukin-10. Lancet 356 ,

1723-1727 .

Van der Kleij , D. , Van Rem oortere , A. , Schuitemaker, J .H., K apsenberg, M .L. , Deelder,

A.M ., Tielens, A.G., Ho kke , C.H . and Yazdanbakhsh, M . 2002). Trigg ering of innate

i m m u n e r e s p o n s e s b y s c h i s to s o m e e g g g l y c o l i p id s a n d t h e i r c a r b o h y d r a t e e p it o p e

GalN Ac beta 1-4 Fuc a lpha 1-2Fuc a lpha 1-3)GlcNAc. Journal oflnfectious Diseases

185 , 531-5 39 .

Vel la , A.T. and Pearce , E .J. 1992). CD 4 ÷ Th2 response indu ced by

Schistosoma mansoni

eggs develops rapidly, through an ear ly , t rans ient , Th0-1ike s tage. Journal of

Immunology

148 , 2283-2 288 .

Velupil la i, P . and Ha m , D.A. 1994). Ol igosa cchar ide-sp eci f ic induct ion of inter leukin 10

produc t ion b y B2 20 ÷ ce l ls f ro m sch i s tosome- infec t ed m ice : a mech ani sm for r egu la -

t ion o fC D 4 ÷ T-cel l subsets . Proceedings of the National Academy of Science USA 91,

18-22 .

Weiss, J.B. , Aro nstein, W .S. and Strand, M. 1987). Schistosoma mansoni: st imulat ion of

art if ic ia l gran ulom a form at ion

in vivo

by ca rbohydra t e de t e rminan t s .

Experimental

Parasitology 64 , 228-236 .

W helan , M., Harnett , M .M., H ousto n, K.M., Patel , V. , Ha m ett , W . and Rigley, K.P. 2000).

A fi larial nem atod e-secre ted prod uct signals dendrit ic cel ls to acquire a phe no typ e that

dr ives develop m ent of Th2 cell s. Journal of Immunology 164 , 6453 -6460 .

W illiams, M.E., K ullberg, M .C., Barbieri, S., Caspar, P., Be rzo fsk y, J.A., Seder, R.A . an d

Sher, A. 1993). Fc epsilon receptor-posi tive cel ls are a m ajor sou rce o f ant ige n-ind uce d

intedeuk in-4 in spleens o f m ice infected wi th

Schistosoma mansoni European Journal

of Immunology 23 , 1910-1916 .

Will iams, M.E. , M onte neg ro, S. , Do m ingu es, A.L. , W ynn , T.A. , Teixeira, K. , Mahanty, S. ,

Cou t inho, A. and Sher, A. 1994). L euko cytes of patients wi th Schistosoma mansoni

r espond w i th a Th 2 pa t t em of cy tok ine p roduc t ion to mi togen or egg an tigens bu t wi th

a Th0 pat tern to wo rm antigens. Journal of Infectious Diseases 170 , 946-9 54 .

W yler, D.J. an d Postlethwaite, A .E. 1983). Fibroblast stimulation in schistosomiasis. IV.

I so l a t ed egg granu lomas e l abora t e a f i b rob las t chemoat t r ac t an t in vitro Journal of

Immunology

130, 1371-1375.

W ynn, T .A. and Cheever , A.W. 1995). C ytokine regulat ion of granulom a form at ion in

schistosomiasis. Current Opinion in Immunology 7 , 505-5 11 .

W ynn , T.A. , Eltou m , I. , Cheever, A.W., Lew is, EA ., Gau se, W .C. and Sher, A. 1993).

Analys is of cytokine m RN A expression dur ing pr imary granulom a formation induced b y

e g g s o f

Schistosoma mansoni Journal of Immunology

151, 1430-1440.

Wynn, T.A. , Cheever, A.W., Jankovic, D. , Poindexter , R.W., Caspar, E, Lewis, EA. and

Sher, A. 1995). An IL -12-ba sed vaccinat ion m ethod for prevent ing f ibrosis indu ced by

schisto som e infect ion. Nature 376 , 594-596 .

W yn n, T.A., Cheever, A.W., W illiams, M .E., Hieny, S., Caspar, P., Kuh n, R., Muller, W. and

Sher, A. 1998). IL-1 0 regulates l iver pa tho log y in acu te m urine Schistosomiasis m an-

soni but is no t required for imm une dow n-m odu lat ion of chron ic disease .

Journal of

Immunology 160, 4473-448 0 .

Yamashita, T . and Bo ros , D.L. 1992). IL-4 inf luences IL-2 product ion and granulom atous

inf l ammat ion in mur ine sch i s tosomias i s mansoni .

Journal of Immunology

149,



HOST RESPONSES DURING SCHISTOSOM E INFECTIONS 3 7

3 6 5 9 - 3 6 6 4 .

Yap, G. , Cheever , A. , Caspar , E , Jankovic , D. and Sher , A. (1997) . Unimpai red down-

m o d u l a t io n o f th e h e p a t ic g r a n u l o m a t o u s r e s p o n s e i n C D 8 T - c e l l- a n d g a m m a

interferon-deficient m ice chro nica l ly infected with Schistosoma mansoni Infection and

Immunity 65 , 2583-2586 .

Zh u, J . , Gu o, L. , Watson, C .J., H u-L i, J . and Paul , W .E. (2001). Stat6 is nec essary an d suf-

f icient for 1L-4 s role in Th2 differentiation and cel l expansion. Journal o f Immunology

166 , 7276 -7281 .



IN EX

Page numbers in

italic

indicate figures and tables.

Abramis ballerus 38

Abramis brama 18, 22

Acanthocephalus anguiUae

56, 57, 120,

130

adipose index 61- 9

Agama

80, 86

Allocraedium isoporum 39

Anas 212

Ancylus

96

Ancyrocephalus vanbenedeni

127

Anguilla anguiUa

41, 52, 71

Anguilla japonicum 7

Anguilla rostrata

43, 117

AnguiUicola crassus 7

Anisakis simplex

275

Anolis

87

Apatemon

130

Apium inundatum 4

Apodemus sylvaticus

87

Archigetes iowensis

41

Ascaridia galli

21

Asellus

110

Asellus aquaticus

99

Asellus meridianus

99

Asymphylodora tincae

38

Austrobilharzia

163, 192

Austrobilharzia terrigalensis

189, 191

Austrobilharzia variglandis 183, 201

average score per taxon (ASPT) 116, 117

Aythya 2 2

Bacillus thuringiensis israelensis 2 3

Baetis rhodani

33

Barbus barbus 38

Berg er-Pa rker index 43, 92, 97

Bilharziella 163, 192

BilharzieUa polonica

206

Biological moni tor ing w orking party

(BMWP) 4, 115, 116, 117


160

Bivitellobilharzia 163

Bothriocephalus acheilognathi

72

Bothriocephalus claviceps

12, 18, 33

Bril louin s index 1 l , 43, 92, 97

Bunodera 80, 87

Bunodera lucioperca

18, 38, 39, 80

Bunodera sacculata

38

Calicotyle kroyeri 80

Callitriche hamulata 5

Callitriche obtusangula 4

Callitriche stagnalis 7

Camallanus lacustris 39

Camallanus oxycephalus

41

Capillaria

18-19, 22, 33, 38, 60, 61, 92

Carex acuta 4

Caryophaeides fennica

80

Caryophyllaeus laticeps

22, 41, 53, 55, 80,

118

Catastomus m acrocheilus

130

Cercaria ocellata 161,166

Cerc aria parocella ta 191

cercarial dermatitis 203-6

control 213-1 4

distribution 209

epidemiology 208-15

potential transmission si tes 211 -13

prophylaxis 214-15

Cichlasoma synspilum 127

Clavella devastatrix

126-7

concom itant immu nity 119

condi t ion factor 61-9

Coregonus albula

126

Coregonus laveratus

71, 80



3 1 I N D E X

Crangonyx 109

Crango nyx pseudogracilis 99, 109

Crepidostomum 11, 13, 45 , 101

Crepidostomum cooperi 39

Crepidostomum cornutum 14

Crepidostomumfarionis 10, 22, 24, 26, 28,

32, 92

changing abundance 97 , 98

hos t age/s ize and 45, 47, 52

host wel lbeing and 60, 61, 64

life cyc le strategy 14, 18

as pol lut ion indicator 115

species interact ions 120, 12 1,1 22 , 123,

125, 126, 131

temperature and 37, 38, 39, 40, 42

water f low and 33, 34

Crepidostomum isostonum 14

Crepidostomum metoecus 10, 22, 24, 26,

28, 32, 92

chan ging abund ance 96, 97, 98, 99

hos t age/s ize and 45, 47, 50

hos t sex and 7 5, 86, 89

host wel lbeing an d 62, 64, 65, 66, 67, 68

life cyc le strategy 14, 18

as pol lut ion indicator 115

species interact ions 120, 12 1,1 22 , 123,

125, 126, 127, 130-1

temperature and 37, 38, 39, 40, 42

water f low and 33

Crepidula fornicata 183

Cu cullanu s Truttaed acnitis ) truttae 12,

22, 28, 32, 92, 96

changing abundance 103

host age/s ize and 51

host sex and 86

host wel lbeing and 59, 60, 61, 68

life cyc le strategy 19

species interact ions 120, 121,122, 123,

125, 126 , 130-1

temperature and 37, 38, 41

water f low and 33, 34

Cucullanus heterochrous 131

Cucullanus minutus 131

Cyanthocephalus truncatus

80, 87, 95

Cyprinus carpio 41

Cystidicola 95

Cystidicoloides ephem eridarum 12, 18-19,

33, 34, 60, 92

Cystidicoloides tenuissima 4 0

Dactylogurus vastator 37, 41, 53, 57, 130

Daphnia 107

Dendritobilharzia 163 , 198 , 201

Deschampsia caespitosa 4

Diphyllobothrium 38, 60, 71

Diphyllobothrium ditremum 12, 18, 22, 33,

47, 54, 92

changing abundance 101

host sex and 80

host wel lbeing an d 59, 60, 61, 71

Diphyllobothrium sagittata 22, 24, 26, 28,

31, 32, 33

host age/s ize and 45, 47, 53

host sex 84, 85, 86

host wel lbeing and 60, 61, 62, 67, 68

life history strategy 12

species interact ions 12 0, 12 3, 12 5, 126

temperature and 37

in t rout and salm on parr 92, 93, 96

Diplostomum 38, 60, 71

Diplostomum spathaceum 53, 56, 80, 108

Diplozoon paradoxum 118

Discotyle sagittata 80

Dreissena polymorpha

18

Drosera rotundifolia 8

Ecdyonurus torrentis 33

Echinoparyphium recurvatum 107, 109

Echinorhynchus gadi 39

Echinorhynchus salmonis 41

Echinorhynchus truttae 40 , 99-101

Echinostoma audyi 214

entom ological inoculat ion ra tes EIR)

2 4 4 - 5 , 2 4 6 - 7

Equisitum 4

Equitability index 92, 97

Ergasilus nannus 127

Erimyzon oblongatus 80

Eso x lucius 41, 53, 80, 130

Eubothrium crassum 56, 80, 1 22, 127, 132

Eubothrium salvelini 7 2

Eustrongylides sp. 80

fibrinogen-related proteins FR EP s) 184

Fontinalis antipyretica 7, 8

Fundu lus heteroclitus 8 0

Gadus merlangi 127

Galba 171



I N D E X 3

Galium palustre 4

Gammarus

9 6

Gamm arus pseudolimnaeus

109

Gammaruspulex

18 , 33 , 99 , 101 ,103 ,

109, 110


18, 21, 38, 41, 80

Gigantobilharzia 163 , 171 ,205

Glyceria fluitans 4

Gobiomorphus breviceps

69

Griphobilharzia

157, 163

Gymnocephalus cernuus 38

Gyrocotyle

127, 129

Gyrodactylus rarus 53

Gyrodactylus salaris

56, 58, 71

Gyrodactylus salmonis

58, 71

H a m i l t o n - Z u k h y p o t h e s i s 4 , 7 4 , 7 5 - 8 9

h e lmin th p a ra s i t e s in s a lmo n id f is h h o s t s

a b u n d a n c e , d e c l in e in 9 6 -1 0 3 , 98-102

c h a n g e s b e twe e n 1 95 0 a n d 1 9 98 9 6 -1 1 8

c o mmu n i ty s t ru c tu re 44 1 2 7 - 8

d i s p e r s io n p a t t e rn s 1 9 -2 2

e n v i ro n me n ta l f a c to r s a f fe c t in g

in te rme d ia te h o s t s 1 0 3 -1 3

e v o lu t io n a ry as p e c t s 1 3 2 -4

fe ma le s e x b ia s 8 4

h a b i t a t s e g re g a tio n 1 2 0 -2

h o s t a g e / s i z e a n d a b u n d a n c e o f 4 5 -5 8 ,

49 50 51

h o s t s e x b ia s 7 4 -9 2 ,

76-9

h o s t w e l l b e i n g a nd a b u n d an c e o f 5 9 - 7 4

in f ra c o mmu n i t i e s 1 2 2 -7

in te r s p e c ie s c o m p e t i t io n 1 1 8 -3 4

in t ra s p e c i f i c in t e ra ct io n s 1 3 1 -2

le n t i c wa te r b o d ie s 3 4

l i fe h is to ry s t ra teg ies 12 -19 ,

15- 17

m a l e v u l n e r a b il i ty 7 5 - 8 7

a s p o l lu t io n b io in d ic a to r s 1 1 3 -1 8

q u a n t i ta t iv e d a ta 2 2 -3 2

s t u d y m e t h o d s 1 0 - 1 2

s tu d y s i t e s 6 - 9

te mp o ra l d iv e r s i f i c a t io n 1 31

i n t r o u t c f s a l m o n p a r r 9 2 - 6 ,

93- 5

wa te r c h e mis t ry 9 , 4 3 -5

wa te r f lo ws a n d w a te r ty p e s 3 2 -5

wa te r t e mp e ra tu re a n d p h o to p e r io d

3 5 - 4 3

Heterobilharzia 163

Heterobilharzia americana

208

Hi l l s n u m b e r 1 17

Homoproteus 81

Hymenolepis

129

Hymenolepis diminuta

119

IL ( in te r l e u k in ) -4 2 91

ro le in g ra n u lo ma fo rma t io n 2 7 8

s o u rc e o f 2 75 , 2 7 7 , 2 7 8 -8 3

IL -4 r e c e p to r p a th wa y 2 7 3

IL-5 277

I L - 9 2 9 2 - 3

I L - 1 0 2 8 6 - 9 0 , 2 9 1 - 2

I L - 1 2 2 9 1 - 2

IL -1 3 2 84 , 2 9 3 -5

imm u n o c o m p e te n c e h y p o th e s i s 4 , 7 4 ,

7 5 - 8 9

in d u c ib le n it r i c o x id e s y n th a s e ( iNO S )

d y s re g u la t io n 2 8 6

in s e c t i c id e - t r e a te d b e d n e t s ( IT N s ) 2 3 6 ,

2 5 1 - 6

in t r a e p i th e l ia l t y mp h o c y te s ( IE L ) 5 6

Jilinobilharzia 162, 163

Juncus effusus 6

Juncus quarrosus 8

K fac to r ana lyses 3 , 54

1 1 k e t o t e s t o s t e r o n e

85

la c to -N- fu c o p e n ta o s e I I I (L N F P I I I ) 2 8 0

l a m i n a p r o p i a l y m p h o c y t e s ( L P L ) 5 6

Lampetra 41

Leishmania sp . 280

Lepomis cyanellus

60, 122


122, 132

Leuciscus leuciscus 41 , 80

Leuctra

spp. 33

Ligula 44

6 0 , 6 9 , 7 1 ,1 1 8

Luronium natans 4

Lymnaea

96, 109

Lymnaea acuminata

110

Lymnaea auricularia

212

Lymnaea natalensis

187

Lymnaeaperegra

18, 68, 86, 98

Lymnaea rubiginosa

2 1 4

Lymnaea stagnalis

69, 159-62, 168, 173,

1 8 1 - 6

Macrobilharzia

163



3 2 INDEX

malaria see Plasmodium falciparum

Mann W hitney test 75

Maximum Bri l louin Indices 92

Mazocraes alosae

41

Mesocoelium monodi 80, 86


34, 72, 80, 132

miracidia-attracting glycoproteins MA Gs)

278, 180

Molinia caerula 8

Moniliformis moniliformis =dubius)

119,

129

Monobothrium ulmeri

80

Morone chrysops

41

Mugil saliens

127

Myriophyllum 4, 5

nasal schistosomes 195 -6

Neoechinorhynchus cristatus 18

Neoechinorhynchus cylindratus

80

Neoechinorhynchus cylindricus

18, 72

Neoechinorhynchus golvani

127

Neoechinorhynchus rutili

18, 22, 24, 26,

27, 28, 31, 32

changing abundance 97, 101

host age /size and 46, 47, 50, 51

host sex bias and 75, 86, 89

host w ellbein g and 59, 60, 62, 64, 65,

67, 68

species interactions 120, 121,122 , 123,

123, 126, 131

temp erature and 37, 38, 40

in trout and salmon parr 92, 93, 96

water flow and 33

Neoechinorhynchus saginatus 18

nestedness 127-8

Nippostrongylus brasiliensis

273, 279

non-B, non-T cells NBNT cells) 278 -9

Notocotylus attenuatus 107, 109

Nuphar lutea 4

Octobothrium merlangi 126

Odneriotrema incommodum 80

oestradiol- 7beta levels 84

Onchorhynchus mykiss

80, 131

Onchorhynchus nerka

41, 88

Onchorhynchus tshawytscha 41

Orientobilharzia

163

Ornithobilharzia

163, 192, 205,206, 207

Ornithobilharzia canaliculata

199

OX40L 281

Paraleptophlebia submarginata

33

Paraquimperia tenerrima

12, 17, 19, 33

parasitic castration 183

Perca flavescen s

39

Peromyscus californicus

82

Phalaris arundacea 6

Philonema agubernaculum 41

Philonema onchorhynchi

41, 88

Phyllodistomum 14, 22, 38

Phyllodistomum dogieli 18

Phyllodistomumfolium 14, 38, 40, 130

Phyllodistomum lysteri

60

Phyllodistomum simile 11, 14, 22, 26, 27,

28, 32

changing abundance 96, 97, 98

host age /size and 47

host sex bias and 75, 86, 89

host w ellbeing and 60, 68

species interactions 120, 121

temp erature and 37, 38, 41

in trout and salmon parr 92

water flow and 33

Physa acuta 187

Pisidium

18, 45, 68, 86, 98, 101,109

Planorbarius corneus 162, 186

Planorbis rotundatus

162

Plasmodium chaubaudi

82


235-57

age patterns of morb idity 238-9, 238

age, risk of disease outcomes and

240-1 ,241

benefits of reductions in parasite

exposure 255~5

child morbidity, African settings 24 1-3,

242-3

child survival and direct and indirect

effects 250 -1

childhoo d m ortality, transmission

intens i ty and 243-5,2 45, 247-9,

248, 252-3

incidence of infection 235

limitation of the x-axis 245- 7

Platichthyes fle sus

131

Podocotyle

sp. 40

pollution bioindicators 113-1 7

Polystoma integerrimum

43


38, 56, 57, 89,



INDEX 3 3

120, 130, 131

Potamopyrgus jenkinsi

109

Potomogeton natans 4, 5

Proteocephalus

41

Prote oceph alus amploplitis 34

Proteocephalusfilicollis

21, 41, 122

Protopolystoma fissilis 127

Proto polystom a simplicis

127

Pseudobilharziella 162

Pseudodiplorchis americanus

87

Radix

171,175

Ra dix auricularia 159, 168, 170, 171,175,

176, 181

Radix labiata 171

Radix ovata

159, 161,170, 171,175, 176,

181

Radixperegra

159, 168, 170, 171,175

Rai dx lagotis

171

Ramellogammarus vancouverensis 18

Ranunculus acris 4

Ranunculus penicillatus 7

Ranunculus penicillatus Dumart) var.

penicillatus 4

Raphidascaris acus 19

decline in abundance 103

host ag e/size and 51

host wellbeing and 60, 61

temp erature and 38, 41

in trout and salmon parr 92, 96

water flow and 33

River invertebrate prediction and

classification system RIVPACS) 4,

115, 116, 117

Rutilus rutilus

18, 80

Salmo salar 5, 41, 58, 80

Salmo trutta

5, 19

Salvelinus alpinus

34, 52

Salvelinus fontinalis

52

Sanguinicola

60, 71

Sap rob ien Index 115, 116

Scaphiopus conchii

86

Schistocephalus 71

Schistocephalus solidus 80, 87

Schistosoma 157, 163, 190, 193, 202

Schistosoma haematobium 211,268, 270,

287

Schistosoma japonicum 208, 268, 270,

284, 293

Schistosoma mansoni

88, 108, 158, 191,

282 3

antibodies 206

anti-inflammatory factor in 204

attachment 189

control 214

distribution 268

eggs in 269, 270

host finding 187

immu nopatho logy 284, 287, 288, 289,

290, 291,292, 293

in vitro

larval development 160

monitoring me thod 211

in skin lesions 199

skin tests 208

type-2 imm unolog ical responses 273,

276

Schistosoma nasale

195

Schistosomatium

163

schistosome infections, host imm une

responses during 265-96

chemotherapies for 266 -7

egg and granuloma 269-71

incidence 268

life cy cle 268

socioeconom ic impact 266

Th 1/Th2 dichotom y 271- 2

types 268

type-2 immunological response 272-6

antigen-presenting cells and 28 0-1

CD4+ T cells and eosinop hils and 281

co-stimulatory molecules and 28 0-1

eggs and 277-8 , 280

induction of 276-83

forms of imm unopathology induced

during 283-95

failure to develop imm unop athology

283-5

link to IL-10 285-9 5

unregulated, po larised type-1-

ssoci ted immune responses

285-90

unregulated, polarised type-2-

associated immu ne responses

291-5

schistosomin 69

Semisulcospira libertina 170

Shan non- Wie ner index 11, 43, 92, 117



3 4 INDEX

Sialis

52, 68, 86

Sialis lutaria

18, 101

signal transducer and activator of

transcription 6 STAT6) 273, 284

Siluris glanis 41

Simp son diversity index 11, 92, 97

Simulium

96

Sphaerium

18, 96

Sphaerium corneum 11, 18, 19, 68, 86, 97,

98, 103

Sphagnum 6

Spirocamallanus rebecae

127

Spirometra mansonoides

69

Stagnicola

159, 172

Stagnicola palustris

162, 173, 181

STAT6 273, 284

testosterone levels, host , reduction in 88- 9

Toxoplasma gonodii 280, 288

Trent Biotic index 116

Triaenophorus crassus 41, 71

Triaenophorus nodulosus

80

Tribolium 132

Trichinella spiralis

279

Trichob ilharzia

155-216

intermediate hos ts 170 -1,17 8-8 6

cellular and humoral immunity 185~i

effects on sna il host 182-3

host-finding and p enetration by

miracid ia 178-81 ,179-80

intramolluscan developm ent 181-2

internal defenc e reactions 183--6

snail immuno biology 183-5

life cycles

174 5

experimental 159-60

general 157-9,

158

systematics 160-77

adults 168-70,

169

bird hosts 172

cercariae 166-8,

167

cytogenetical and m olecular analyses

172-5

diagnosis 163-75

eggs 164-5,

164

historical overview 161-2

intermediate hosts 170-1

mir acid ia 165~5,

165

species overview 176-7

sporocysts 166

vertebrate hosts 187-96

cercaria-schistosomulum

transformation and immu ne

evasion 190

compatible 196-202

egg dissemination 194

host-finding 187

immune response and pathology

196-208, 200

incompat ible 203 -8

skin penetration 187-9,

188

migration 190-6

Trichobilharzia anatina

169

Trichobilharzia arcuata

158, 164, 167,

172, 196

Trichobilharzia aureliani

172

Trichobilharzia australis

166, 167, 169,

172

Trichobilharzia brantae 162


169, 172, 192, 198,

206, 214

Trichobilharzia cameroni

178, 191

Trichobilharzia ceryleri 172

Trichobilharzia corvi

164, 165, 166, 167,

169, 170, 172

Trichobilharzia elvae

159, 162, 164, 169,

172, 198

Trichobilharzia filiformis

164

Trichobilharzia fra nk i

162

bird hosts 172

cerca riae 168

cytogenetic and m olecular analysis 173,

175

eggs 164, 165

host-finding and penetration by

miracid ia 180

intermediate hosts 170

life cycle 159

systematics 176

Trichobilharzia indica 166

Trichobilharzia jequitibaensis

176

Trichobilharzia jianensis

176

Trichobilharzia kegonsensis 172

Trichobilharzia kossarewi

161,162

Trichobilharzia maegraithi 172, 176


215

cercariae 168

cytogenetical and molec ular analysis

173, 175



INDEX 3 5

effects on snail host 182 183 184 185

186

eggs 164 165

host finding 181 187

immune evasion 190

intermediate hosts 170 171

life cycle 160

migration 191 192 193 194

miracid ia 166 178 181

parasite stages 181 182

systematics 161 162 176

vertebrate host 187 189 190 191 192

193 194

vertebrate im mu ne respon se 197 198

199 204 206

richobilharzia oregonensis 191 198

richobilharzia paoi 176

richobilharziaparocellata 164 191 194

richobilharzia physeUae 172 192 194

198 206

richobilharzia querquedulae 172

richobilharzia regenti 157

bird hosts 172

cercariae 167

cytogenetical and molecular analyses

173 175

deve lopm ent in vertebrate hosts 195

196

eggs 164

host-finding and penetration b y

miracidia 178

incompatible hosts 207

intermediate hosts 170 171

life cycle 158

miracidia 166

penetration o f vertebrate skin 189

systematics 161 162 176

vertebrate immune response and

pathology 197 198 201 202

richobilharzia rodhaini 172

richobilharzia salmanticensis

162 164

166 167 176

richobilharzia stagnicolae 172 173 191

192 206

richobilharzia szidati

adults 169

bird hosts 172 206

cellular and humoral immu nity and 185

cercariae 167 168

control 214

cytogenetical and m olecular analysis

173

host penetration 178 187 189

life cycl e 158 159

migra tion 192 193

sporocysts 166

systematics 162

vertebrate pathology 198

richobilharzia tatianae 162

richobilharzia yokogawai 162

richostrongylus tenuis 72

richuris muris

290

ropisterus columbianus 129

ubifex 107

Uvulifer ambloplitis 70 71

Verger-Parker index 11

visceral schistosomes

in liver phase 193 -4

in lung phase 19 1-2

in skin phase 191

Xenopus wittei 127

Zonothrix columbianus 129



onten ts of Vo lum es in This Series

Volume 4

T h e S o u t h e r n C o n e I n it i at i ve A g a i n s t C h a g a s D i s e a se . . . . . . . . . . . . . . . . 1

C. J. SCHOFIELD AND J.C .P. DIAS

Phytomonas a n d O t h e r T r y p a n o s o m a t i d P a r as i te s o f P l a n ts a n d F r u it . . . . . . . . 3 1

E.P. CAMARGO

Pa r a gon imia s i s a nd t he Ge nus Paragonimus . . . . . . . . . . . . . . . . . . . . . 1 1 3

D. BLAIR Z. -B . XU AND T. AGATSUMA

I m m u n o l o g y a n d B i o c h e m i s t r y o f Hymenolepis diminuta 223

J. ANREASSEN E.M. BENNET-JENKINS AND C. BRYANT

C o n t r o l S t ra t e gi e s f o r H u m a n I n t e st i n al N e m a t o d e I n f e ct i o n s . . . . . . . . . . . . 2 7 7

M . ALBONICO D.W .T. CROMPTON AND L. SAVIOLI

DN A V a c c ines : Te c hno logy a nd App l i c a t i ons a s An t i - pa r a s i t e a nd An t i - m ic r ob i a l

A g e nt s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 43

J.B . ALARCON G.Wo WAINE AND D.P. MCMANUS

Volume 43

G e n e t i c E x c h a n g e i n t he Trypanosomatidae

l

W . GIBSO N AND J. STEVENS

T h e H o s t - Pa r a s it e R e l at io n s hi p i n N e o s po r o si s . . . . . . . . . . . . . . . . . . . 47

A. HEMPHILL

P r ot ea s es o f P r o to z o an P a ra s it es . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 5

P.J. ROSENTHAL

P r o t e in a s e s a n d A s s o c i a te d G e n e s o f P a r a si ti c H e l m i n t h s . . . . . . . . . . . . . .

161

J. TORT P.J. BRINDLEY D. KNOX K. H. WOLFE AND J.P. DALTON

P a r as i ti c F u n g i a n d t h e i r I n t er a c ti o n s w i t h t h e I n s e c t I m m u n e S y s t e m . . . . . . . 2 6 7

A. VILCINSKAS AND P. GOTZ

Volume 44

Ce l l B io logy o f Leishmania

E. HANDMAN

I m m u n i t y a n d V a c c in e D e v e l o p m e n t i n t h e B o v i n e T h e il e ri o s e s . . . . . . . . . . .

41

N. BOULTER AND R. HALL

The D i s t r i bu t i on o f Schistosoma bovis Sons ino , 1876 in Re l a t i on t o I n t e r me d ia t e

H o s t M o l l u s c -P a r a s it e R e l at io n s h ip s . . . . . . . . . . . . . . . . . . . . . . . 98

H. MONI~ G . MOUAHID AND S. MORAND

T h e L a r v ae o f M o n o g e n e a P l a ty h e lm i n th e s ) . . . . . . . . . . . . . . . . . . . . 138

I.D.

WHITYINGTON

L.A .

CHISHOLM AND

K.

ROHDE



3 8 CONTENTS OF VOLUMES IN THIS SERIES

Sea l ice on Sa lmonids : The i r B io logy and Cont ro l . . . . . . . . . . . . . . . . . . 233

A.W . PiKE AND S.L . WADSWORTH

Volume 5

The Biolog y of som e Int raerythrocyt ic Paras i tes of F ishes , Amph ibia and

R e p t i l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

A.J. DAVIES AND M. R.L . JOHNSTON

The R ange and Biological Act ivi ty of FMRFam ide-re la ted Pept ides and Class ical

N e u ro tr a ns m it te r s i n N e m a t o de s . . . . . . . . . . . . . . . . . . . . . . . . . 1 09

D. BROWNLEE, L. HOLDEN-DYE ANDR WALKER

The Imm unob iology of Gast rointes t inal Nem atode Infect ions in Ruminants . . . . 181

A. BALIC, V.M. BOWELS AND E.N.T . MEEUSEN

Volume 6

Host -Paras i te Interactions in Acanthocephala : a Morpholog ical

A p pr oa ch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

H. TARASCHEWSKI

Eicosanoids i n Pa ras it es and Paras it ic In fec t ions . . . . . . . . . . . . . . . . . . . 181

m. DAUGSCHIESAND A. JOACHIM

Volume 7

An Overv i ew of Remote Sens ing and G eodesy fo r Epidemio logy and Publ i c Hea l th

A p pl ic at io n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

S.I. HAY

L i nk i ng R e m o t e S e ns in g , L a n d C o v e r a n d D i se a se . . . . . . . . . . . . . . . . . 3 7

P.J. CURRAN, P.M. ATKINSON, G .M . FOODY AND E.J . MILTON

Spat ia l S ta ti s tics and Geograp hic Informat ion Systems in Epidem iology and Publ ic

H ea lth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83

T.P. ROBINSON

Sate l li te s , Space, T ime and the Af r i can T rypanosomiases . . . . . . . . . . . . . . 133

D.J. ROGERS

Ear th Observat ion, Geographic Informat ion Systems and P lasmodium fa lc iparum

M a l ar ia i n S u b -S a ha r an A f r ic a . . . . . . . . . . . . . . . . . . . . . . . . . . 175

S.I. HAY, J. OMUMBO, M. CRAIG AND R.W. SNOW

Ticks and T ick-borne Di sease Sys t ems in Space and f rom Space . . . . . . . . . . 219

S.E. RANDOLPH

The Potentia l of Geographical Informat ion Systems GIS) and Remo te Sensing in

the Epidemio logy and Cont ro l o f Human He lmin th In fec t ions . . . . . . . . . . 247

S. BROOKER AND E. MICHAEL

Advan ces in Sate l l i te Remote Sensing of Envi ronm ental Variables for

E p i d em i o l og i c al A p p li c at io n s . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 93

S.J. GOETZ, S.D . PRINCE AND J. SMALL

Forecas t ing Disease Risk for Increased Epidem ic Preparedness in Publ ic Heal th . . 313

M .E MYERS, D.J. ROGERS, J. C o x, A. FLAUHALT AND S.I. HAY

Educat ion, Out reach and the Future of Rem ote Sensing in Hum an Heal th . . . . . 335

B.L. Wo oDs , L.R . BECK, B.M . LOBITZ AND M.R . BOBO

Advances in Parasit Ology

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