Jones & Reynolds RFBF 97

Effects of pollution on reproductive behaviourof ®shes

JACKIE C. JONES and JOHN D. REYNOLDS�

School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, United Kingdom

Contents

Abstract page 463

Introduction 464

Fish behaviour in pollution research 465

Case study 1: mosquito®sh and paper mill ef¯uent

Case study 2: sun®sh and herbicide

Comparisons between case studies

Review of studies 480

Motivation for research

Selection of study species and pollutant

Laboratory or wild

Emphasis on reproductive behaviour

Effects on reproductive success

Experimental designs

Secondary effects of pollution 483

Prospects for the future: integrating pollution and reproductive behaviour 483

From individual behaviour to populations

Effects on future reproductive success

Population size

Genetic changes

Adaptation

Uses of reproductive behaviour studies

Behavioural assays for protecting other species and habitats

Conservation

Conclusion 488

Acknowledgements 488

References 488

Abstract

This review attempts to integrate pollution research with behavioural ecology by focusingon reproductive behaviour of ®shes. A search of Aquatic Sciences and FisheriesAbstracts and other sources showed that only 0.1% of 19 199 studies of aquatic pollution

Reviews in Fish Biology and Fisheries 7, 463±491 (1997)

0960±3166 # 1997 Chapman & Hall

�Author to whom correspondence should be addressed (e-mail: [email protected]).

and ®shes during the past 20 years have made this link. Effects on parental care andcourtship have been investigated using a variety of pollutants (e.g. acidi®cation,herbicide, thermal ef¯uent) in several ®sh families (e.g. Cichlidae, Poeciliidae,Gasterosteidae, Cyprinidae).

Eleven of the 19 studies found a change in behaviour from the norm. Effects oncourtship included decreases or increases in frequency of displays, increased courtshipduration, or performance of male-like behaviour by masculinized females. Studies ofparental care have found decreased nest-building activity, decreased offspring defence,or changes in division of parental care between the sexes. Few studies have measuredreproductive success or extrapolated their results to effects on populations.

We develop a framework for exploring links between pollution and behavioural ecologywhich suggests potential impacts on life history trade-offs in reproduction, genetic changesin populations, and population sizes. Many reproductive behaviours of ®sh species arereadily quanti®able and behaviours such as courtship by male guppies and other membersof the Poeciliidae show some promise for pollution monitoring and behavioural toxicitytests. Choice of such assays would have to compete with the sensitivity and practicality ofmore traditional methods but may serve as useful complements. There is considerablescope for further research into conservation. A synthesis between behavioural ecologyand toxicology should thus provide useful insights for both ®elds.

Introduction

Evidence of the state of many major British rivers during the reign of George III (1760±1820) was made apparent by a letter reportedly written by a member of Parliament to thePrime Minister. The letter complained about the odour and appearance of the RiverThames. It was written not in ink, but with water from the Thames itself (Strandberg,1971). Historically, the Thames had been a major salmon river but towards the end of the18th century, ®sh species had declined dramatically and large areas of the river becamedevoid of ®sh altogether (Wood, 1982). This was typical of many rivers in heavilypopulated areas of Europe.

Fish populations are vulnerable because the aquatic environment is the recipient ofvirtually every form of human waste (Moyle and Leidy, 1992). The IUCN (InternationalUnion for Conservation of Nature) Red List (1996) records 734 ®sh species asthreatened and 92 species as extinct worldwide. Water pollution is one of severalcontributors to such declines in ®sh populations (Clark, 1992; Moyle and Leidy, 1992;Lawton and May, 1995; Maitland, 1995).

Pollution can be de®ned as `̀ the presence in the environment, or the introduction intoit, of products of human activity which have harmful or objectionable effects'' (OxfordEnglish Dictionary, CD-ROM). Studies of ®shes have ®gured prominently in pollutionresearch, particularly in sublethal physiological effects (review: Kime, 1995). Manystudies focus on reproduction because this is one of the most vulnerable periods in thelife cycle of ®shes (Gerking, 1980; Little et al., 1985).

Recently there has been development towards the use of behaviour in toxicologicalresearch (Little et al., 1985; Dùving, 1991; Smith and Logan, 1997). This represents afusion of the ®elds of behaviour, ecology, toxicology and conservation biology. In thisarticle, we present what might be termed a `prospective review'. The `review' elementconcerns studies that have examined impacts of pollutants on reproductive behaviour of

464 Jones and Reynolds

®shes. The `prospects' that we are interested in concern the value of integratingpollution research into the ®eld of behavioural ecology for gaining insights into waterquality management and conservation of ®shes.

Fish behaviour in pollution research

Before focusing on reproductive behaviour speci®cally, it is instructive to consider theoverall role of ®sh behaviour in pollution research. We searched Aquatic Sciences andFisheries Abstracts (ASFA) on CD-ROM from 1978 to 1997 for references containingvarious combinations of truncated search terms such as `behav�', to include variousspellings and forms of the key words (e.g. `behave', `behaviour', `behavioral'). The result(Fig. 1) shows that only 13.8% of studies involving ®sh and pollution included behaviourand of these, only 1% involved reproductive behaviour as opposed to other behaviourssuch as attraction and avoidance. Thus, of the original 19 199 studies of aquatic pollutionand ®shes, only 0.14% involve reproductive behaviour. This con®rms the impressionfrom previous reviews of the paucity of such studies (Atchison et al., 1987; Beitinger,1990; Dùving, 1991; Scherer, 1992).

The lack of studies of reproductive behaviour in pollution research can be attributedin part to a perception that behaviour is dif®cult to measure and interpret. This makesbehavioural assays less appealing than lethal toxicity tests; death is a rather de®nitiveendpoint! However, behavioural responses may provide more sensitive early warningsthan standard test methods (Smith and Logan, 1997), and ethologists have been makingaccurate measurements and analyses of many forms of animal behaviour for over 50

Reproduc*Behav*

Feed*Behav*

Predat*or Prey

Avoid* orAttract*

Behav*

(No Extras)

0.1 1 10 100% References With Pollut*, Fish* and...

26

152

576

366

2641

19199

Fig. 1. Results of a search of the Aquatic Sciences and Fisheries Abstracts CD-ROM from 1978 to

1997 for references on pollution and various types of ®sh behaviour. Numbers beside each bar show

the number of studies found for that category.

Effects of pollution on reproductive behaviour 465

years. Furthermore, during the past 20±30 years there has been a vigorous developmentof the ®eld of behavioural ecology, which is concerned with how behaviour affects lifehistories, reproductive success of individuals and their interactions with the surroundingenvironment (Krebs and Davies, 1997). In linking the reproductive behaviour ofindividuals to their environment, one can explore how stressful conditions such as thosecaused by pollution will affect offspring production, survival, and population dynamics.

We begin by reviewing the studies that have integrated the ®elds of reproductivebehaviour and pollution research. The behaviours considered include courtship,spawning interactions and parental care. Studies that investigated effects of pollutionon fecundity or reproductive success, or presence±absence of spawning only, withoutmeasuring associated reproductive behaviours, are not included in this review.

Based on the above ASFA search and an additional literature survey, 19 studies werefound that investigated the effects of pollution on reproductive behaviour (Table 1).This total excludes a few studies revealed by the initial ASFA keywords that proved notto be relevant to this review. Courtship was studied most often, followed by parentalcare. The studies varied widely in selection of ®sh species and pollutant, and in therelative contribution that reproductive behaviour made to the research.

Eleven of the 19 studies found a change in reproductive behaviour from the norm. Itshould be borne in mind that there may be a publication bias towards signi®cant effectsof pollutants. Studies investigating parental care have found either no effect, decreasednest-building or egg-directed activity, decreased protection of the young, disruption tocare or changes in division of parental care between the sexes. Effects on courtshipranged from no effect to either decreases or increases in display frequency, increasedduration of courtship and performance of male-like display behaviour by masculinizedfemales. Additional effects reported, but without strong supporting evidence, aredescribed in Table 1. Two contrasting cases from Table 1 illustrate the range ofapproaches used.

CASE STUDY 1: MOSQUITOFISH AND PAPER MILL EFFLUENT

Howell et al. (1980) investigated the impact of paper mill ef¯uent on a local populationof mosquito®sh (Gambusia af®nis holbrooki, Poeciliidae), in Elevenmile Creek,Escambia County, Florida, USA. This research was precipitated by observations thatsome females in the study area exhibited morphological signs of masculinization. Manyfemales had developed a gonopodium, the modi®ed anal ®n used by males for internalfertilization in this family of ®shes (Figs 2 and 3). Fish from above and below theef¯uent out¯ow were compared using histological examinations of gamete abnormalitiesand karyotypes. Comparisons of reproductive behaviour between the two ®sh groupswere also made in the laboratory. Fish were observed in each of the followingcombinations: (1) three pregnant masculinized females and three normal females, (2) twomasculinized females, (3) a precociously masculinized male and a normal female, (4) aprecociously masculinized male, a normal male and three normal females, and (5) anormal male and a normal female. No quantitative data were recorded, but descriptionsof morphology and reproductive behaviour were provided.

Howell et al. (1980) showed that ®sh from above the ef¯uent discharge exhibitednormal sexual expression. However, all females 13±45 mm standard length, collectedfrom below the ef¯uent out¯ow, showed some degree of gonopodial development. Therewas no evidence of testicular tissue, and heteromorphic sex chromosomes were absent.


Table 1. Summary of effects of pollution on ®sh reproductive behaviour

Behavioural

category

Species Pollutant and

sublethal level

used

Effect on reproductive

behaviour

Effect on reproductive output Comments Reference

Shown Extrapolated

Courtship Guppy

Poecilia

reticulata

Phenol.

10 mg lÿ1 for 10

days.

Decreased male court-

ship, e.g. approaches

to females and sigmoid

displays.

Not

determined.

Probably

disruptive

because sexual

selection and

elaborate

courtship are

prominent in

this species.

Unclear if phenol expo-

sure affects females and

their reproductive out-

put.

Colgan et

al. (1982)

Courtship Guppy

Poecilia

reticulata

Wastewater,

lindane.

10% sewage

plant water at

stage of release

to river, or

1 ìg lÿ1 lindane.

Both exposures

over observation

period only (2±

3 days).

Authors state that a

difference between two

laboratory strains in

male courtship displays

decreases. A difference

in gonopodial thrusting

increases under both

pollutants.

Not

determined.

A reduction of

®tness by one

laboratory

strain relative

to the other

due to the

pollutants

would be

expected.

Only 3 pairs of males

were tested with lindane,

and 9 pairs with waste-

water. Statistics erro-

neously used multiple

observations of same

®sh as independent data

points (hence sample

sizes of 49 and 153

respectively). Time was

confounded with treat-

ments. Interesting results

inconclusive.

SchroÈder

and Peters

(1988a)

continued overleaf

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

467

Table 1. (continued)

Behavioural

category


sublethal level

used


behaviour


Shown Extrapolated

Courtship Guppy

Poecilia

reticulata

Wastewater.

10% sewage

plant water at

stage of release

to river. Expo-

sure was for

observation

period only

(3 days).

Authors state that

males of the `Macula-

tus' strain increased

gonopodial thrusting

and `closed' courtship

display, but had

decreased `open'

displays. Males of

`Blue Iridescence'

strain increased

thrusting.

`Maculatus'

males sired a

larger propor-

tion of young

when in com-

petition with

`Blue Irides-

cence' males

in wastewater

than in tap-

water.

None

suggested.

Only 2 pairs of males

used (one of each strain

in a pair) in each treat-

ment (wastewater or

tapwater). Multiple ob-

servations of the same

®sh arti®cially in¯ated

sample sizes on beha-

viour to 16 for each

treatment. Findings

inconclusive.

SchroÈder

and Peters

(1988b)

Courtship Fathead

minnow

Pimephales

promelas

Selenium.

20 mg lÿ1 and

30 mg lÿ1 for 24

hours.

No signi®cant differ-

ence in frequencies of

behaviours (approach,

leading, lateral display,

tail beating, vibrating

and butting) between

exposed males and

control males.

None due to

behaviour, but

many larvae

were born

deformed and

died.

None

suggested.

Fish died at higher con-

centrations (60 mg lÿ1).

Sample sizes unclear,

apparently 5 pairs of

exposed ®sh per treat-

ment. Uncontaminated

water used for breeding

tests.

Pyron and

Beitinger

(1989)

468

Jones

and

Reyn

old

s

Courtship Orange

chromide

Etroplus

maculatus

Monochloramine

Either 0.025 or

0.05 mg lÿ1 from

within 24 hours

of pair being

placed together

until spawning.

Little courtship and no

spawning occurred at

0.05 mg lÿ1, with ®sh

dying or becoming ill.

Comparisons between

0.025 mg lÿ1 and con-

trol showed: 64% in-

crease in length of

courtship period, 34%

reduction in clutch

size, increased ®n-

¯icker by males,

reduced quivering

and ®n-¯icker by

females.

No spawning

at higher

concentration.

Hatching data

not given.

Increased

courtship

length may

increase preda-

tion risk. An

additional be-

haviour which

increased was

gill-purging.

This might be

misinterpreted

by conspeci®es

as aggression

and hamper

pair formation.

A comprehensive study,

primarily aimed at

determining suitability

of behavioural toxicity

for pollution monitoring.

Stafford

and Ward

(1983)

Courtship Mosquito®sh

Gambusia

af®nis

holbrooki

Paper mill

ef¯uent.

Fish collected

6.5 km down-

stream of the

ef¯uent output.

Exposed females

became masculinized.

Masculinized pregnant

females displayed only

typical male reproduc-

tive behaviour (chasing

normal and masculi-

nized females with

gonopodial swings and

thrust attempts). Ex-

posed males matured

precociously and

exhibited typical but

more aggressive court-

ship. A masculinized

male was dominant

over a normal male.

Not

determined.

None

suggested.

No data or analyses

presented. One replicate

for each combination

involving 1±3 masculi-

nized or normal ®sh.

Interesting ®ndings from

wild-exposed ®sh merit

further investigation.

Howell

et al. (1980)

continued overleaf

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

469


Behavioural

category


sublethal level

used


behaviour


Shown Extrapolated

Courtship

and

aggression

Mosquito®sh

Gambusia

af®nis

Kraft mill

ef¯uent.

Exposure in

wild 1±5 km

downstream of

discharge.

No signi®cant differ-

ence for either sex in

any behaviour (ap-

proach, chase, display,

thrust and penetrate)

between exposed and

control ®sh. Exposed

females had become

masculinized morpho-

logically.

Not

determined.

None

suggested.

Further work

was recom-

mended.

Fish had been in clean

water in captivity for 2±

4 weeks before testing.

Results might have been

different if ®sh had been

held in water from con-

taminated site. Good

number of replicates

used (20 per ®sh com-

bination).

Bortone et

al. (1989)

Courtship

and

aggression

Mosquito-

®sh

Gambusia

af®nis

af®nis

Simulated mas-

culinizing effect

of kraft mill

ef¯uent.

Degraded pro-

ducts of 65%

stigmastanol and

30% B-sitosterol

for one month.

Exposed females

became masculinized

and showed more

male-like courtship

than control females in

the presence of a

female. These beha-

viours were less fre-

quent than in normal

males. When two

masculinized females

were placed together,

the smaller one acted

as a male, and the

larger as a female.

Masculinized females

did not have increased

aggression.

Not

determined.

Detrimental

effects prob-

ably minimal

in an exposed

population be-

cause masculi-

nized females

reverted to

normal female

behaviour in

the presence of

a normal male,

and could still

reproduce.

It would be interesting

to examine longer-term

effects on both sexes.

Krotzer

(1990)

470

Jones

and

Reyn

old

s

Male

courtship

Cichlid

Sarothero-

don

mossambi-

cus

Endosulfan

insecticide.

Three treat-

ments: (A)

adults exposed

to 0.5 ìg lÿ1 for

4 weeks;

(B) juveniles

exposed to

0.6 ìg lÿ1 for 9

weeks (with

1.5 ìg lÿ1 for

®rst 3 days);

(C) juveniles

exposed to

either 0.6 or

0.2 ìg lÿ1 for 6

weeks.

(A) No effect on adult

male sexual behaviour

of female clutch

production or mouth-

brooding time.

(B) Onset of juvenile

male sexual behaviour

and female clutch

production delayed.

Females had higher

clutch production rates

but lower retention

times than controls,

suggesting that clutch

abortion was

occurring.

(C) More control

males showed normal

breeding behaviour

between days 36 and

42 than exposed males.

Many fry died

at low expo-

sure concentra-

tion (24 hour

LC50 was

0.5 ìg lÿ1).

Delayed breed-

ing displays in

newly matur-

ing males may

explain a

reduction of

approximately

75% in nests

of related

Tilapia ren-

dalli in the

Okavango

Delta,

Botswana.

Concentrations were

similar to those found in

the wild soon after

spraying. Additional

direct physiological

effects noted on ®sh.

Matthiessen

and Logan

(1984)

continued overleaf

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

471


Behavioural

category


sublethal level

used


behaviour


Shown Extrapolated

Nest

building

Cichlid

Tilapia

rendalli

Endosulfan.

Application of

9.5 g haÿ1

sprayed onto the

river by aircraft.

The density of Tilapia

nests was about 75%

less in sprayed areas

than in unsprayed

areas.

Juveniles were

less numerous

in a sprayed

lagoon com-

pared with

control.

The 1977 year-

class ®sh were

less abundant

in the areas

sprayed in that

year than in

those areas not

sprayed,

implying fewer

®sh were pro-

duced. As long

as the same

sites are not

sprayed an-

nually, then

®sh population

should not be

reduced per-

manently.

Although effects on the

reproductive success

were only inferred from

the ®ndings, this was a

thorough study investi-

gating all aspects of

effects on ®sh, from

mortality to behaviour

and populations.

Douthwaite

et al.

(1981)

Parental

care

Threespine

stickleback

Gasterosteus

aculeatus

Thermal ef¯uent.

28±30 8C.

Disruption of parental

behaviour occurred.

May cause males to

eat own eggs or aban-

don nest.

Eggs died,

apparently due

to disruption

of parental

behaviour.

None

suggested.

This paper is an abstract

from a meeting. Insuf®-

cient detail to evaluate

it.

Ryabov

(1985)

472

Jones

and

Reyn

old

s

Parental

care

Naked goby

Gobiosoma

bosc

Episodic

hypoxia.

Field; down to

,0.5 mg lÿ1

Laboratory;

down to

0.15 mg lÿ1

Males guarded their

eggs and nests until

the dissolved oxygen

level reached almost

lethal levels (0.15±

0.6 mg lÿ1), when they

abandoned.

The eggs died

if males left

the nest. If the

male does not

leave the nest

when lethal

limits are

being reached

he will die.

Even if there

are no eggs in

the nest, the

male will lose

mating oppor-

tunities if he

abandons

unnecessarily.

Thorough study, unusual

in incorporating both

®eld observations and

laboratory experiments.

Breitburg

(1992)

Parental

care

Bluegill

sun®sh

Lepomis

macrochirus

Redear

sun®sh

Lepomis

microlophus

Herbicides

2,4-dichlorophe-

noxyacetic acid

and Aquathol-K

sprayed on sur-

face of lake to

obtain a con-

centration of

4 mg lÿ1.

Sprayed water

was used as a

control.

Although some males

abandoned nests tem-

porarily in each treat-

ment, there was no

signi®cant difference

between them. Conge-

ners usually intruded

during male absence

and some egg preda-

tion was observed in

all treatments. There

was no signi®cant ef-

fect on male parental

care (e.g. displays to-

wards intruding males,

egg fanning).

Not

determined.

None expected

from herbicide

exposure.

Sample sizes were low

(5±9 males per treat-

ment). A possible trend

towards higher rates of

temporary desertion in

both species and conse-

quently effects on egg

predation might prove

signi®cant with larger

sample sizes.

Bettoli and

Clark

(1992)

Parental

care

Fathead

minnow

Pimephales

promelas

Waterborne lead.

0.5 mg lÿ1 lead

for 30 days

while ®sh

spawned.

Males exposed to lead

spent signi®cantly less

time in activities

directed towards ceil-

ing of nest, including

preparation of sub-

strate for eggs, and

touching ceiling with

dorsal pad.

Drastic

decrease in

egg production

by exposed fe-

males. Role of

reduced paren-

tal behaviour

in reproductive

output unclear.

Reproductive

success may

be reduced

due to less

cleaning of

nest ceiling

and egg mass

surface.

Dif®cult to interpret the

cause of reduced nest

maintenance behaviours,

i.e. an effect of lead

exposure versus fewer

eggs received.

Weber

(1993)

continued overleaf

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

473


Behavioural

category


sublethal level

used


behaviour


Shown Extrapolated

Parental

care and

aggression

Convict

cichlid

Cichlasoma

nigrofascia-

tum

Acid stress

pH 5±5.5 versus

control pH 7.

Administered to

pair-bonded ®sh

24 hours after

introduction to

breeding tank.

Continued expo-

sure.

Experiments were car-

ried out in the pre-

sence of conspeci®cs.

Egg fanning time was

reduced by 25% due to

a decrease in female

fanning activity, which

was only partly

compensated by an

increase in male fan-

ning. Females

increased their guard-

ing time, while this

decreased in males.

Males increased their

aggressive behaviours.

Not

determined.

Acidication in

the natural

environment

could reduce

survival of fry

due to changes

in parental

behaviour.

Experiments capitalize

effectively on the rich

repertoire of behaviours

by both sexes in this

species.

Lorenz and

Taylor

(1992a)

Parental

care

Convict

cichlid

Cichlasoma

nigrofascia-

tum

Acid stress.

pH 5±5.5 versus

control pH 7.

Administered to

pair-bonded ®sh

24 hours after

introduction to

breeding tank.

Continued expo-

sure until fry 5

days old.

Survival of fry unaf-

fected by pH alone.

However, conspeci®cs

preyed upon more fry

at low pH compared

with control pH. Total

number of displays by

both parents towards

predators increased at

low pH, and there was

a trend towards fewer

attacks.

Decreased per

cent fry survi-

val after day 5

of free-swim-

ming stage

under acid

stress when in

the presence of

predators.

Switching

from attacks to

displays may

conserve

energy of

parents, but

this is not

effective

against

predators.

Shows the importance of

ecological context (i.e.

predation risk) for

understanding sublethal

effects of pollution on

®tness.

Lorenz and

Taylor

(1992b)

474

Jones

and

Reyn

old

s

Parental

care

Bluegill

sun®sh

Lepomis

macro-

chirus

Di¯ubenzuron; a

pesticide

2.5 ìg lÿ1 and

30 ìg lÿ1

applied twice,

®rst application

into the desig-

nated ®sh enclo-

sures 2 months

after ®sh intro-

duced and sec-

ond application

1 month later.

No effects on male

reproductive behaviour

observed.

None due to

behaviour.

Only one

spawning event

was observed

in all exposure

treatments

(30 ìg lÿ1) but

most spawning

events (86%)

took place

prior to expo-

sure. Spawning

appeared to be

more in¯u-

enced by water

temperature

than di¯uben-

zuron expo-

sure. Reduced

juvenile

growth rates.

Reduced juve-

nile growth

could have

major impoli-

cations for ®sh

survival during

winter through

starvation and

increased pre-

dation risk.

No statistical analysis

was performed and only

2 replicates per treat-

ment used. Reproductive

behaviour effects not

quanti®ed and hatching

success based on one

spawning event at

30 ìg lÿ1. Most spawn-

ing events took place

before exposure. How-

ever, focused on ecolo-

gical context of effect of

pesticide exposure on

natural food supply, and

effects on reproductive

behaviour were not in-

tended as a main focus.

Tanner and

Hoffett

(1995)

continued overleaf

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

475


Behavioural

category


sublethal level

used


behaviour


Shown Extrapolated

Parental

care

Bluegill

sun®sh

Lepomis

macro-

chirus

Azinphos-

methyl: a

pesticide.

1 ìg lÿ1 and

4 ìg lÿ1 7 weeks

after ®sh

introduced.


behaviour unclear be-

cause most spawning

took place prior to

exposure.

None due to

behaviour.

Although

spawning

caused in three

of the four

ìg lÿ1 repli-

cates after

exposure, it

also ceased in

three of the

four control

replicates.

None

suggested.

Statistical analyses used

for larval growth and

biomass data. Most

spawning events took

place prior to exposure.

Reproductive behaviour

effects not quanti®ed but

played a minor part.

Data from before and

after pesticide applica-

tion were used to calcu-

late each average

hatching success. The

study took place in lit-

toral enclosures and in-

vestigated effects on

reproductive success

from spawning to juve-

nile production.

Tanner and

Knuth

(1995)

476

Jones

and

Reyn

old

s

Parental

care

Bluegill

sun®sh

Lepomis

macro-

chirus

Esfenvalerate: a

pesticide

0.01, 0.08, 0.2,

1.0 and 5 ìg lÿ1

applied twice,

®rst application

1 month after

®sh introduced

and second ap-

plication another

month later.

At 1 ìg lÿ1, one male

guarding a nest with

embryos rim-circled

rapidly. In all enclo-

sures except 5 ìg lÿ1,

where the adults died,

rim-circling occurred

both before and after

exposure.

None due to

behaviour.

Adults died at

5 ìg lÿ1.

Spawning

ceased for 15

days in

1 ìg lÿ1 enclo-

sure following

both applica-

tions and lar-

val mortality

was observed

following the

second appli-

cation. A

reduction in

juvenile

growth rate

was measured

at 1.0, 0.2 and

0.08 ìg lÿ1.

If esfenvalerate

were to be ap-

plied repeat-

edly biweekly

at concentra-

tions greater

than

0.44 ìg lÿ1,

spawning and

hence juvenile

production

would cease.

Reduced juve-

nile growth

could have

major implica-

tions for ®sh

survival over

winter through

starvation and

increased

predation risk.

No statistical analysis

was performed and 1

replicate per treatment

was used. Reproductive

behaviour effects not

quanti®ed but played a

minor role. The rapid

rim-circling that oc-

curred in the 1 ìg lÿ1

treatment was observed

in only one male. Com-

bined data from before

and after pesticide apli-

cation were used to

calculate average hatch-

ing success.

Tanner and

Knuth

(1996)

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

477

Masculinized females exhibited some male reproductive behaviour and males exhibitedprecocious development of secondary sex characters and reproductive behaviour. Aphysiologically normal male and female when placed together exhibited normalbehaviour (see Table 1 for detailed behavioural ®ndings).

CASE STUDY 2: SUNFISH AND HERBICIDE

Bettoli and Clark (1992) investigated the effects of herbicide exposure on nestingbehaviour in bluegill sun®sh, Lepomis macrochirus and redear sun®sh, L. microlophus(Centrarchidae) in Old Monterey Lake, Monterey, Tennessee, USA. Underwater videocameras were set up near nests in the wild and ®sh were ®lmed prior to, during and afterherbicide application (Aquathol-K or 2,4-dichlorophenoxyacetic acid). Some of theredear sun®sh observations were also made from the lakeside using binoculars. Speci®cbehaviours such as display, spawning and egg fanning were recorded, along withincidence and timing of nest abandonment. Statistical comparisons were made betweenmales with nests in test plots sprayed with Aquathol-K, 2,4-D or with water (control).

There was no difference in the number of nests abandoned nor in the actual time ofabandonment between treatments (herbicide or water sprayed). When abandonment didoccur, congeners usually entered the nest to feed on eggs or fry until the male returned.Finally, frequencies of rim circling, egg fanning and agonistic behaviours of theguarding males did not differ between treatments. Bettoli and Clark (1992) concludedthat these herbicides, if applied properly, cause no pronounced shift in sun®shreproductive behaviour.

Fig. 2. Normal specimens of Gambusia af®nis holbrooki collected above paper-mill ef¯uent in

Elevenmile Creek, Escambia County, Florida (Howell et al., 1980; reproduced by permission of

Copeia). The top ®sh is a pregnant female (31 mm standard length). The bottom ®sh is a male

(25 mm standard length) showing gonopodial differentiation of the anal ®n.


COMPARISONS BETWEEN CASE STUDIES

These studies show the diversity of approaches to the study of effects of pollution on ®shreproductive behaviour. Whereas the mosquito®sh study focused primarily on morph-ology, with some unquanti®ed behavioural observations, the sun®sh study was restrictedentirely to reproductive behaviour. Many mosquito®sh were put into each observationtank and only one replicate of each ®sh combination was used. The sun®sh study usedbetween ®ve and nine individually sprayed areas per treatment to study effects ofherbicide exposure on ®sh in the wild. Owing to the nature of the data collected in the®rst study, no analysis could be undertaken, while in the second study a rigorous analysisof the data was performed. However, the mosquito®sh study was concerned primarilywith morphological effects, with behavioural observations comprising a small part of theresearch. Although the behavioural data were non-quantitative, they provide a startingpoint for further work.

Fig. 3. Masculinized specimens of Gambusia af®nis holbrooki collected below a paper-mill ef¯uent in

Elevenmile Creek, Escambia County, Florida (Howell et al., 1980; reproduced by permission of

Copeia). (A) Immature male (15 mm SL) showing precocious anal ray elongation. (B) Mature male

(17 mm SL) showing precocious gonopodium. (C) Pregnant female (23 mm SL) with a gonopodium.

(D) Pregnant female (28 mm SL) with a gonopodium. (E) Pregnant female (34 mm SL) with a

gonopodium. (F) pregnant female (36 mm SL) with a gonopodium.


To obtain a clearer picture of effects of pollution on reproductive behaviour, weassess various aspects of the studies carried out so far.

Review of studies

MOTIVATION FOR RESEARCH

Some studies were aimed towards development of a behavioural assay for toxicity testing,based on changes in behaviour such as courtship (Stafford and Ward, 1983; SchroÈder andPeters, 1988a; Bortone et al., 1989). This information could be used in a similar vein tolethal toxicity tests, but with behavioural responses as an end point (Stafford and Ward,1983; Little et al., 1985; Bortone et al., 1989). SchroÈder and Peters (1988a) contendedthat as a behavioural assay, courtship by guppies (Poecilia reticulata, Poeciliidae) isextremely sensitive to very low concentrations of aquatic contaminants. Stafford andWard (1983) found orange chromides (Etroplus maculatus, Cichlidae) also to be asuitable test organism and proposed that behavioural assays are liable to be moresensitive measures of effects of toxicants than previous methods.

The aims of the other studies were less clear, but many were concerned with effectson reproductive behaviour and reproductive success (Howell et al., 1980; Matthiessenand Logan, 1984; Ryabov, 1985; SchroÈder and Peters, 1988b; Pyron and Beitinger,1989; Bettoli and Clark, 1992; Lorenz and Taylor, 1992a,b; Weber, 1993; Tanner andKnuth 1995, 1996; Tanner and Moffett, 1995). For example, Lorenz and Taylor (1992b)tested the hypothesis that if offspring survival is reduced in an unfavourableenvironment (in this case due to acid stress), then parents may reduce their care toconserve energy for future reproduction (Carlisle, 1982). This was supported by testswith convict cichlids (Cichlasoma nigrofasciatum, Cichlidae), which suffered a decreasein reproductive success. Some studies went further in hypothesizing that reducedreproductive output owing to changes in behaviour may have a detrimental effect onpopulation numbers (Douthwaite et al., 1981; Colgan et al., 1982; Krotzer, 1990;Breitburg, 1992). Krotzer (1990) studied the effect of masculinization on the behaviourof female mosquito®sh (Gambusia af®nis af®nis, Poeciliidae). It was suggested that iffemales became more aggressive and less receptive to males, exposed populations inthe wild could suffer. The primary aim of three studies of bluegill sun®sh by oneresearch group was to measure effects of pesticides on reproductive success fromspawning to juvenile production, with reproductive behaviour playing a very minor role(Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995). Although some studieswent into greater depth on the consequences of changes in behaviour than others, theinformation provided by most studies could be used as a starting point towards furtherresearch.

SELECTION OF STUDY SPECIES AND POLLUTANT

Studies varied widely in species and pollutant investigated. Most of those that focused oneffects on the reproductive behaviour of the ®sh chose a ®sh±pollutant combinationoccurring in the wild at a site of speci®c concern. Examples include ®sh±pollutantcombinations such as mosquito®sh exposed to paper mill or kraft mill ef¯uent (Howell etal., 1980; Bortone et al., 1989), cichlids (Tilapia rendalli, Cichlidae) exposed toendosulfan insecticide (Douthwaite et al., 1981), threespine sticklebacks (Gasterosteus


aculeatus, Gasterosteidae) exposed to power station thermal ef¯uent (Ryabov, 1985),naked gobies (Gobiosoma bosc, Gobiidae) exposed to hypoxic water conditions(Breitburg, 1992) and bluegill sun®sh exposed to herbicide contamination (Bettoli andClark, 1992). Although not all of these studies were carried out in the ®eld, suchcombinations were known to occur in the wild. This gives the ®ndings direct relevance tosuch affected areas.

Other criteria may affect selection of ®sh species. For example, Weber (1993) usedfathead minnows (Pimephales promelas, Cyprinidae) because this species is a standardtest species for use in aquatic toxicity studies (Denny, 1987). Fathead minnows werealso used by Pyron and Beitinger (1989) to investigate the in¯uence of seleniumexposure.

Other ®sh may be readily available, have well-documented reproductive behaviour,survive well in the laboratory, or breed readily. These were used speci®cally in thebehavioural toxicity tests. For example, the suitability of orange chromide cichlids fortoxicity tests was investigated under exposure to monochloramine (Stafford and Ward,1983) and guppies were exposed to treatment-plant wastewater (SchroÈder and Peters,1988a). However, these ®sh species may not encounter such pollutants in the wild.Researchers have thus sacri®ced direct relevance of the environmental situationnormally faced by the ®sh for the sake of practicality and standardization.

LABORATORY OR WILD

Studies have differed greatly in the origin of the ®sh used and the type of exposurereceived. Nine of the 19 studies in Table 1 used laboratory-bred and laboratory-exposed®sh (Colgan et al., 1982; Stafford and Ward, 1983; Matthiessen and Logan, 1984;SchroÈder and Peters, 1988a,b; Pyron and Beitinger, 1989; Lorenz and Taylor, 1992a,b;Weber, 1993). One study used wild mosquito®sh, exposed and observed in the laboratory(Krotzer, 1990) while three used hatchery-reared bluegill sun®sh and exposed them inoutdoor littoral enclosures (Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995).Five studies used wild ®sh that were exposed to the pollutant in the ®eld. Of these, threeobserved the ®sh in the wild: sun®sh, Lepomis macrochirus and L. microlophus (Bettoliand Clark, 1992), Tilapia rendalli (Douthwaite et al., 1981), and threespine stickleback(Ryabov, 1985). The other two observed mosquito®sh under non-polluted conditions inthe laboratory (Howell et al., 1980; Bortone et al., 1989) after exposure in the ®eld. Onlyone study used wild ®sh (naked gobies) in both wild and laboratory exposureobservations (Breitburg, 1992). Differences in the results of these studies could, in part,have arisen because of the varied background and exposure conditions of experimental®sh.

Although results may be less directly relevant to the wild, there is a bene®t in usinglaboratory ®sh strains compared with wild ®sh because one can eliminate the potentialeffects of tolerance through genetic adaptation or physiological acclimation. Toleranceto pollutants has been shown in several ®sh species, including mosquito®sh, Gambusiaholbrooki (Poeciliidae) (Benton et al., 1994), rainbow trout, Oncorhynchus mykiss(Salmonidae) (Pascoe and Beattie, 1979) and central mudminnow, Umbra limi(Umbridae) (Kopp et al., 1992), as well as in other taxa (Bryan and Langston, 1992;Gustavson and Wangberg, 1995). There is considerable scope for further research intodifferences among wild populations in pollution tolerance.


EMPHASIS ON REPRODUCTIVE BEHAVIOUR

Some studies were purely behavioural (e.g. SchroÈder and Peters, 1988a; Pyron andBeitinger, 1989; Lorenz and Taylor, 1992a). Others contained combinations ofreproductive physiology, morphology and behaviour (e.g. Howell et al., 1980; Weber,1993) while others dedicated little to effects on reproductive behaviour (Tanner andKnuth, 1995, 1996; Tanner and Moffett, 1995). Usually, only a small part of thereproductive behaviour repertoire was studied, such as courtship, spawning behaviour,nest building, parental care of eggs, or defence of newly hatched fry. Ideally, the entirereproductive behaviour repertoire should be investigated (from mate choice and courtshipto egg or larval independence) to see at what stages pollution exerts an effect. Time andexpense will hinder such an approach, but if the purpose is to develop a toxicity test forwater quality management, full reproductive cycle studies could serve as an important®rst step, to be re®ned by simpler, focused behavioural assays.

EFFECTS ON REPRODUCTIVE SUCCESS

Eleven of the studies in Table 1 considered the possible effects of a change in reproductivebehaviour on reproductive success. Only three studies actually measured this directly: twofound a negative effect (Breitburg, 1992; Lorenz and Taylor, 1992b) and one reported anincrease in reproductive success (SchroÈder and Peters, 1988b). The latter result should betreated with caution owing to a small sample size and inappropriate experimental design(see Table 1 and general comments under `Experimental designs', below). A possibledecrease in reproductive success was inferred by Douthwaite et al. (1981), who measuredthe age distribution of juvenile Tilapia rendalli in the Okavango Delta, Botswana,comparing sites that had been sprayed with insecticide 2 years previously with controlsites. Although few studies have measured impacts on reproductive output via behaviouralchanges, in some cases it was likely that any such effects would have been overshadowedby physiological problems. For example, Weber (1993) found reduced egg production infemale fathead minnows upon exposure to lead. Stafford and Ward (1983) investigated theeffect of monochloramine on orange chromide. At levels of 0.05 mg lÿ1, some ®sh becameill and courtship and spawning stopped, while at levels of 0.025 mg lÿ1, female eggproduction was reduced. Finally, some studies estimated effects on reproductive successwithout trying to establish a causal link to changes in reproductive behaviour (Tanner andKnuth, 1995, 1996; Tanner and Moffett, 1995).

EXPERIMENTAL DESIGNS

In Table 1 most of our comments concerning experimental designs are rather critical. Infairness to the authors, we wish to emphasize two points strongly. First, many of thestudies were done before biologists were fully aware of the problems of non-independence of samples within treatments (`pseudoreplication', Hurlbert, 1984). Second,as noted earlier, a combination of physiological and behavioural effects of pollutants wasinvestigated in some studies, sometimes with effects on reproductive behaviour appearingas a secondary objective (e.g. Howell et al., 1980).

Nevertheless, to evaluate our current state of knowledge in this ®eld, it must be bornein mind that many of the studies lacked adequate controls, replication, or statisticalanalyses. Multiple observations of the same ®sh under the same treatment cannot becounted as separate statistical data points. One ®sh may be watched 10 times whenexposed to a pollutant and another ®sh may be watched 10 times in a control situation,


but effectively this still leaves one data point (e.g. mean behaviour per ®sh) under eachtreatment (Hurlbert, 1984). Furthermore, 10 ®sh in one aquarium exposed to a pollutantshould not be compared as 10 independent samples to ®sh in a control tank. Fishwithin aquaria are not independent because individuals may affect each other bothbehaviourally and physiologically. For example, there may be in¯uences from eachother's activity levels, dominance, pheromones, or metabolic wastes. These problemsapply to more traditional non-behavioural tests as well. Furthermore, aquaria are boundto differ by more than the presence or absence of the pollutant concerned. For example,levels of nutrients, light intensities, or other uncontrolled and unknown factors mayconfound treatments. This necessitates the use of multiple aquaria per treatment inrandomized or alternating spatial patterns. If multiple ®sh or observations are used peraquarium, each aquarium should yield a single mean data point in a t-test or standardANOVA design, or observations from individual ®sh within tanks can be used in a nestedANOVA-type design.

Our general impression from the information summarized in Table 1 is that many ofthese early studies report tantalizing results, but the use of ®sh reproductive behaviourin pollution research is still very much in its infancy.

Secondary effects of pollution

Additional studies are available in the literature which measure secondary effects ofpollutants on reproductive behaviour. For example, silting arises from high sedimentloading, and lowered oxygen levels often result from bacterial degradation under highorganic pollution (Clark, 1992; Mason, 1996). Although such studies were not includedin Table 1 because they did not use pollutants directly, their results could still be usefulin water quality management and conservation.

Silting was found to affect parental care in the ®fteenspine stickleback (Spinachiaspinachia, Gasterosteidae) (Potts et al., 1988). During parental care, males use their ®nsto fan water over their egg mass. Silting increased the number of times males fannedtheir eggs. Nest inspection and nest pushing also became more frequent. Loweredoxygen has also been found to affect paternal care in the threespine stickleback (Reebset al., 1984), with an increase in the length of egg-fanning bouts. When oxygen levelsfell below 2.8 mg lÿ1, males spent more time swimming outside the nest but still fannedat intervals. In the guppy, lowered oxygen levels increased the frequency of breathing atthe surface by males at a cost of decreased courtship (Kramer and Mehegan, 1981). Todate, such studies have not examined consequences for reproductive success.

Prospects for the future: integrating pollution and reproductive behaviour

There is now a growing interest in understanding sublethal effects of pollutants onaquatic organisms (Alabaster and Lloyd, 1982; MuÈller and Lloyd, 1994). To evaluate theusefulness of developing this ®eld further, it is helpful to integrate general theory frombehavioural ecology to clarify the biological links between behavioural responses ofindividuals and population changes. We can then use this information to help decide theprospects for using behavioural studies to help protect populations of the ®shesthemselves, as well as developing assays for protecting other species in the habitat.


FROM INDIVIDUAL BEHAVIOUR TO POPULATIONS

Figure 4 is a schematic diagram of behavioural testing procedures, responses of theanimals, and potential uses for this information. Nearly all of the studies reviewed areconcerned with step 1, which links reproductive behaviour of ®shes and their exposure tosublethal doses of the contaminant in question. As we have seen, few of the studies havegone on to step 2, from reproductive behaviour to reproductive success, and these havebeen concerned only with current broods rather than impacts on subsequent reproductivebouts. We have not found any studies that take the `®nal' step (step 3) of testing forpopulation responses, although there was circumstantial evidence of a decrease in thenumbers of Tilapia rendalli in the Okavango Delta in two areas sprayed with endosulfaninsecticide (Douthwaite et al., 1981). Below, we discuss the logic and potential of theseunder-developed steps.

Effects on future reproductive success

Life history theory, supported by a large body of empirical research on a variety of taxa,suggests that commitment of resources to a given reproductive bout should have costs forsurvival, growth, or reproduction in subsequent bouts (Williams, 1966; Roff, 1992;Stearns, 1992; Sargent and Gross, 1993). If this were not true, animals could make hugeinvestments in reproduction forever (Partridge and Harvey, 1985). An example from®shes concerns male bluegill sun®sh, which have been induced to ventilate their eggs byfanning water across them more frequently when given larger broods experimentally(Coleman et al., 1985). Increased fanning reduces the time available to males forcourting new females, and it reduces energy reserves through the loss of non-polar lipids(Coleman and Fischer, 1991). This may impair survival and future reproduction. Suchreproductive trade-offs may be most evident under conditions of stress (Roff, 1992). Forexample, in the sand goby (Pomatoschistus minutus, Gobiidae), females that initiallyproduced large clutches before receiving a low food ration produced smaller clutches inthe next bout (Kvarnemo, 1997). This trade-off did not occur with high food. Thus,environmental stressors such as pollutants could have delayed effects on reproductionwhich would be overlooked if only a single reproductive cycle were studied.

Population size

Links between individual behaviour and population biology have been much sought-afterby ecologists (Sibly and Smith, 1985; Sutherland, 1996). In theory, any external force thatalters behaviour of individuals from the optimum under natural and sexual selectioncould lead to reduced population sizes. But this effect may be far from straightforward,depending on the nature of density dependence in the population. For example, Lorenzand Taylor (1992b) showed that under conditions of low pH, convict cichlids were lessable to rear their young in the presence of conspeci®cs. But if population densities ofthese ®sh were restricted by food or predation at a different stage of life, reduced survivalof young being guarded by parents may have no impact on population size. The dif®cultyof showing relationships between reproduction and population size is well known to®sheries biologists who rarely ®nd clear patterns between stock size and recruitment(Hilborn and Walters, 1992; King, 1995). Thus, if one is concerned with conservation, amajor challenge is to demonstrate clear effects of sublethal doses of pollutants onpopulation size.


EXPOSURE

ORGANISMRESPONSE

POPULATIONRESPONSE

Fish exposed to sublethal dose

Effect on reproductive behaviour?

Effect on current and futurereproductive success?

Effect on population?

Number of individualsGenetic changes

Adaptation

1

2

3

TESTS

Monitoring water quality

USES

4

5

6

7

Protection ofother speciesand habitat

Conservation ofthe test fish

species

Fig. 4. Schematic diagram showing hierarchy of pollution effects on reproductive behaviour and the potential uses for such information. Circled

numbers are reference points for discussion in the text.

Effects

of

pollu

tion

on

repro

ductive

beh

avio

ur

485

Genetic changes

Environmental impacts that change the reproductive behaviour of individuals (e.g. choiceof mate or oviposition site) could alter the genetic composition of populations. Anexample from a natural environmental parameter concerns the effects of light levels onbehaviour of Trinidadian guppies (Reynolds, 1993). Under low light levels, large-bodiedmales have higher mating success than smaller ones, because of female choice. Thispattern is reversed under higher light levels, when males may be hampered by greaterrisk of predation. Because male body size has a genetic basis (Reynolds and Gross,1992), such changes in mating behaviour in response to an environmental change mayhave genetic consequences for the population. Genetic changes such as these have yet tobe shown in the context of pollution, but given the numerous demonstrations ofheritability of traits under natural selection (Falconer, 1989) and sexual selection(Pomiankowski and Mùller, 1995; cf. Alatalo et al., 1997), researchers would be welladvised to bear these possibilities in mind.

Adaptation

Long-term selection may lead to the evolution of resistance. This depends on theintensity of selection, additive genetic variance in resistance and the population size.Benton et al. (1994) provided an example in a comparison of populations of freshwatersnails (Helisoma trivolvis, Planorbidae) and mosquito®sh from a relatively clean site anda site contaminated with a variety of heavy metals and other elements. They found that inthe populations exposed to the pollutants, both species may have evolved increasedtolerance. In mosquito®sh, this tolerant genotype seems to be linked to small body size.

Particularly relevant here is the possibility that altered mate choice, courtship orparental care could be adaptive, leading to a buffering against environmental change.This could occur either through short-term, facultative changes in behaviour or throughgenetic responses to selection. This is a risky proposition, because changes in behaviourcould be non-adaptive, and genetic adaptations may not evolve quickly enough.Furthermore, genetic bottlenecks and inbreeding are risks when the effective populationsize is reduced owing to fewer individuals reproducing (Meffe, 1986).

USES OF REPRODUCTIVE BEHAVIOUR STUDIES

Aside from gaining a better understanding of pollution in an ecological context, whatdirect practical uses can be made from the framework in Fig. 4? We believe the answersdepend on whether one is concerned with development of general assays for protectingwater quality for other species and the habitat, or with conservation of the particularspecies under study.

Behavioural assays for protecting other species and habitats

Toxicity tests may be used to screen new chemicals, and to formulate water qualitycriteria and standards (Council of the European Communities, 1978; Alabaster and Lloyd,1982; Abel, 1989; Lloyd, 1992; Howells, 1994). Standardized protocols for toxicity tests,for example LC50 tests using guppies or Daphnia magna (Daphniidae), or life-cycle testsusing salmonids, are often used (Alabaster and Lloyd, 1982; Lloyd, 1992; Howells, 1994;Mason, 1996). Toxicity tests are also used to assess hazards presented by ef¯uents, forexample from industry or sewage treatment works. Such monitoring of ef¯uent is


especially useful when substances are dif®cult to analyse or where a concoction ofsubstances is present (Alabaster and Lloyd, 1982).

Whether the objective is to monitor ef¯uent water quality (arrow 4 in Fig. 4) orformulate water quality criteria or standards (arrow 5), the ideal protocol involves aspecies that can be reared quickly and easily, with a minimum of equipment and space,and which responds quickly to the testing procedure, in a highly repeatable manner(Alabaster and Lloyd, 1982; Smith and Logan, 1997). Given these requirements, itseems unlikely that many of the ®sh species and reproductive behaviours reviewed inTable 1 will be practical for general use. We suggest that the species that come closestmight be poeciliids such as the guppy (already a standard test species for traditionaltoxicity tests) and mosquito®sh (Gambusia spp.). They are small and breed readily incaptivity, and male courtship is easily quanti®able and occurs under a wide variety ofcircumstances (Farr, 1980; SchroÈder and Peters, 1988a; Reynolds et al., 1993; Houde,1997). Rice®sh (Oryzias latipes, Cyprnodonitidae) and killi®sh (Fundulus, Cyprnodo-nitidae) are also worth exploring, although their courtship behaviour is less elaboratethan in guppies. Female poeciliids have already been shown to undergo physical, and toa less extent behavioural, masculinization as a result of exposure to paper mill ef¯uent(Howell et al., 1980). It would be interesting to see whether the opposite effect ±feminization ± occurs during exposure of males to oestrogenic compounds, and whetherchanges in courtship could yield an early warning system for such pollutants (Purdomet al., 1994; Sumpter et al., 1996).

Overall, it remains to be seen whether courtship by ®shes yields an improvement insensitivity, practicality, and cost over existing methods. This is well worth exploring,particularly as automated behavioural monitoring techniques using videos andcomputers become increasingly advanced.

Conservation

Studies of impacts of pollutants on reproductive behaviour may be more important forunderstanding conservation of the test ®sh themselves (arrows 6 and 7 in Fig. 4) than asgeneral assays for monitoring water quality and recommending criteria on behalf of otherspecies. Such studies could complement, rather than replace traditional studies of effectson physiology and survival.

The ecological framework presented (Fig. 4) suggests several reasons for focusing onreproductive behaviour. For example, behavioural studies of the impacts of oestrogeniccompounds might yield insights into reproductive output in species where males provideparental care. Indeed, parental care itself, including egg guarding and ventilation, placeshigh energetic demands on ®shes, which often lose weight during parental cycles(Sargent and Gross, 1993; Smith and Wootton, 1995). Pollutants may exacerbate thesecosts, as well as costs from sexual selection, including predation, courtship,territoriality, mating competition, and mate choice (Magnhagen, 1991; Andersson,1994; Reynolds and CoÃteÂ, 1995). One or more forms of such mating competition arewidespread in ®shes. Although there are numerous routes towards reduced offspringproduction in current and future breeding attempts (Fig. 4), we need more research onthese to explore properly their links to conservation.

Empirical justi®cation for focusing on reproductive behaviour comes from a recentsurvey of conservation of ®shes (Bruton, 1995). Cross-species comparisons suggestedthat ®sh with more complex reproductive behaviours are particularly at risk. Parental


care is found in 21% of teleost ®sh families (Gross and Sargent, 1985), and isparticularly common in species breeding in fresh water, estuaries, and coastal marineenvironments. These are also the habitats that receive the greatest inputs of pollutants(Clark, 1992; Mason, 1996).

Conclusion

The study of effects of pollution on reproductive behaviour of ®shes has yielded someclear effects on courtship and partental care for several species, but few studies havegone far enough to draw clear inferences for effects on populations. As a tool forbiomonitoring or use in water quality criteria, such studies are unlikely to be able tocompete with standard toxicity tests, although they may complement them effectively,especially since there is evidence of strong sensitivity to pollutants. From the standpointof conservation of populations of the ®shes themselves, it would be useful to explorefurther the links between alterations in reproductive behaviour, reproductive output, andthe mechanisms that govern population dynamics. Such an integration of behaviouralecology with pollution research may provide useful insights for both ®elds.

Acknowledgements

We wish to thank W. Mike Howell for the photographs used for Figs 2 and 3 and forcomments on the manuscript. We also thank Mike Elliott, Alastair Grant and PeterMatthiessen for helpful discussions and Nick Dulvy, Paul Hart, David Kime, Carl Smithand two anonymous referees for comments on the manuscript.

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Accepted 3 July 1997


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