Chinese Journal of Oceanology and Limnology Vol.18, No.l, P .54-60 , 2000

MICROHABITAT DISTRIBUTION OF METAZOAN PARASITES ON GIIJS OF SILURUS ASOTUS IN JIANGKOU RESERVOIR,

JIANGXI PROVINCE, CHINA*

NIE Pin ( laboratory of Fish Diseases, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Ch/na)

Received Apr. 16,1998;revision accepted July 6,1999

Abstract 1his paper deals with the l~oportional di~Sbution, niche brea&h and niche ov~lap d two metazoan parasites (copepods species, Ergas//us anchorams Markewitsch, 1946 and Pseudargas//us pams//ur/ Vamagu~, 1936) a n d ~ (in the gems ~ ~ , 1976) found on gills ffthe fish, asotus L. from Jiangkou Reservoir in Jiangxi Province, (lfina. E. ~ was the c~m,m and &n/nant ~ parasite on gills of the fish in this locality as indicated by the higher infection levds, arm di~ikaed al- most evenly on gill arches without any ~ e d gill-arch p r d ~ , as shown by the wide proix~onal distribu- tion and broad niche breadth. P. parasthr ~ in S/]tuodsm/des ~ere found also wifl't~ any fig- nitlcara gill-arch preference although they had a rather narrow niche lxeadth, rIhe observed significant overlap be- t~,een P. paras//ur/and ~ spp. may be simply dnc to the lower infection levels of the parasites. The ~bserved pattem d m.~stricted ds d the para~c e~1x~s on t~dls ~f the ~sh rmy he ~ f~r~ at least in part, by the moving alfility of the copepods, and may also indicate that the parasite does not exlfibit any fe~a-e ti" gill-arch p r e f ~ . However, ~ e x ~ research is needed to verify the tnicrdaahitat ~ - hdion d the parasites.

Key words: parasite ecology, microhabitat distribution, fish parasite, gill-areh preference

INTRODUCTION

Intestinal parasite communities in fish are found normally to be poor in terms of species compo- sitions when compared with those in birds and some other higher vertebrates (Kennedy et a l . , 1986; Esch et a l . , 1990). However, ectoparasite compositions on gills of fish are considered as species rich (Koskivaara et a l . , 1991 ) . The ectoparasite communities on gills of fish have thus formed an interesting subject in ecological studies (Koskivaara et a l . , 1992; Janovy et a l . , 1997).

Microhabitat distribution and niche preference of parasites on frsh ~lis were studied by various re- seachers(Anne and Halton, 1972; Wootten, 1974; Adams, 1986; Buchmann, 1989; Nie, 1996). For monogeneans on gills, intmspecific relationships were considered more important than interspecific inter- actions as niche-restricting factors (Rohde, 1991). In a detailed study on cotmmnities of monogenean parasites on roach Rut//us rut//us, Koskivaara and Valtonen (1992) found that multispecies infection may exist without competition between monogenean species due to the possible low resistance of the host to the parasites and the ample resource and space on the host. The gill-arch preference by the monogeneans was to some extent seasonal and thus a simple reflection of seasonality, although some species of the rmnoge- neans studied exhibited some niche restriction (Koskivaam et a l . , 1992; Nie, 1996).

* Project 39370122 supported by NSFC.

NIE et al. : PARASrI'ES ON S. ASOTUS 55

During an investigation into the population biology of a parasitic copepod, Ergasilus andugmaz Marke- witsch, 1946 (Nie, 1998), other metazoan parasites, i . e . another species of copepod, Pseudergas//us paras//ur/Yarmguti, 1936 and moncgeneans in the genus of S/huod/a~/des Gtrss~, 1976 were recorded also on gills of S//urus asotus L. fix~ Jiangkon Reservoir in Jiangxi Province of China. rlhe present study is on the r n i ~ i t a t distributiom of the m e ~ parasites on gills of S. asam.

MATERIALS AND METHODS

In total, 176 fish from Jiangkou Reservoir(114~176 situated in Jiangxi Province were examined for the presence and number of metazoan parasites on the gills.

Two species of copepods, i . e . E , anchoratus and P. parasiluri, and monogeneans in the ge- nus Silurodiscordes were found on the gills of S. asotus. The monogeneans found were not identified into species as their numbers were few and the species in the genus Silurodiscordes parasitic on gills of the fish are several (Pan et a l . , 1990) and examinations of individual specimens which are nec- essary for the species identification are considered not feasible. Species identification of the monoge- neans was thus not done and they were analysed as a group as done by many others (Hanek and Fer- nando, 1978; Adams, 1986).

The parasite number of the two copepods and the number of monogeneans on gill arches of the same order on the left and right sides were added together, that is, the respective parasite number on the left and right sides of gill arch 1 ,2 ,3 ,4 were added respectively. Gill-arch preferences of the parasites were then compared, according to Koskivaara et al. (1992), using the proportions of specimens of each of the two copepods and the monogeneans on the 4 arches, and the monthly dif- ferences in the proportions among gill arches were tested using ANOVA. The niche breadth of the metazoan parasites on the gills was calculated from the 4 gill arches of each individual fish using the method of Koskivaara et al. (1992). For the overlap between species, a proportional similarity measure (Schoener, 1968) was used: 1-1/2 ( P/a- Pja) , where P/a is the proportion of the speci- mens of species i in a sample and Pya is the proportion of species j . Differences in this measure were tested by the Mann-Whitney U-test. All terms used were defined either by Margolis et al. (1982) or Esch et al. (1990).

RESULTS

3he infection levels of the metazoan parasites found on ~11~ ofS. asotus were different, qlae prevalence and abundance of E. anchoratus were significantly higher than those of P. paras//ur/ and S/hu'M/.wo/des spp. (P <0.01, G-test of heten~neity for prevalence and t-test for parasite number) (Table 1). qhis in- dicated that in Jiangkon Reservoir, E. anchoratus was the most conanm and dcnfin~t metazoan parasite on ~11~ of S. asotus. No statistical difference was found between infection levels of P. paras//ur/and S//uro- d/scoMes spp. (san'~e test as above, but P>0.05).

Table 1 The prevalence and abundance of E . anchoratus , P . parasiluri a n d S ~ o i d e s spp. on gills of S//urus asoms in J'mngkou R~servoir in Y ~ g ~ Province, China

E. anchoratus P . paras//ur/ S//urod/sco/des spp.

Pr~alenee (%) 69.46 13.17 7.78

Abundanee(x • S. D) 28.95 +41.38 0.31 • 1.50 0.22 + 0.98

56 CHIN. J. OCEANOL. LIMNOL., 18(1), 2000

Monthly changes in the proportion of the metazoan parasites on the 4 gill arches are given in Fig. 1. E. anchoratus was found throughout the study period, while P. parasiluri and Silurodis- coides spp. were observed in 7 and 5 out of a total of 8 samples, respectively (Fig. l : a - c ) . Re- stricted distribution of E. anchoratus was not observed, and as indicated by the proportional distri- bution, a pattern of gill arch preference by the parasite was not observed. The parasite was distribut- ed almost equally on the 4 gills arches (Fig. l a ) , although in some months such as in May and June the parasite was distributed slightly more on gill arches 2 and 3. An analysis of variance indicated that changes in the proportions were not significantly seasonal on gill arches 1 - 4, nor significantly different among the4 gill arches (for gill arches, F = 0 . 8 0 , P = 0 . 5 1 ; for months, F = 0 . 8 8 , P =0.54).

0.50 V a

0.75~ b 0'50~,,, x

0'25 V] 1

0.50 V c

M A M J J A S 0 N D

Months

Fig.1 Monthly proportional distribution of E. anchoratus (above), P. paras//ur/(middle) and Silurodiscoides spp. on gills of S. asotus in Jiangkou Reservoir in Jiangxi Province, China

The proportional distributions of P. parasiluri on the 4 gill arches were found also without any selective distribution on any particular gill arches, although in some samples all parasites were found on a single gill arch as indicated by the higher proportions observed in May, September and Decem- ber. This may be due to the lower infection levels of the parasite in these samples. Indeed, only 4,

NIE et al. : PARASITES ON S. ASOTUS 57

1 and 1 specimens were recorded in the three samples, respectively. Statistical analyses revealed that changes in the proportion were not significantly different seasonally or among the 4 gill arches (for gill arches, F = 0 .77, P = 0.53 ; for months, F = 0.26, P = 0 .96) . Again, no obvious gill arch preference was found for Silurodiscoides app. (for gill arches, F = 2 . 7 6 , P = 0 .07 ; for months, F = 0 . 0 8 8 , P = 0 . 0 9 ) .

M i ~ i t a t niche breadths (~ the rmtazoan Imrasites were studied rrtmthly for the whole period (Table 2). As indicated by the greater values of the parameter, E. anchomats had broader niches during the whole period of the study, and in general P . paros/had and S / / ~ / d e s spp. had rather narrow distributions on the gill arches. The Mann-Whitney U-test revealed that the parameter value for E. anchoratus was signifi- cantly higher than that for both P.paras//ur/ ( P =0.(1014) and S//urod/sco/des spp. ( P =0.(I152). This indicated that E. anchoratus had a boarder distribution on the gills. However, cmoarision showed that the values of the pm-arneter for P . paras//ur/and S/hu'MZ~/des slap. were not significantly different(sam test,

but P =0.83). Changes in the niche breadths of the copepods and the rnonogcmem~ were not significantly seasonal(ANOVA, P >0.05).

Table 2 The monthly mean niche breadths of the metazoan parasites, E. anchora/us, P. paras//ur/ and SUurodiscoides spp. on ~ of S. asotus in J'mngkou Reservoir in Jiangxi Province, China

Month Parasite

III V VI VII IX X XI XII

0.3453• 0.4167• 0.6668• 0.4961• 0.2753• 0.2094• 0.3790+ 0.1904• E. anchoratus

0.2866 0.3500 0.2204 0.3592 0.2536 0.1963 0.3142 0.2507

0.1161• 0.0464• 0.0580• 0.1926• 0.0348• 0.0631• 0.0145• P. paras//nr/ 0.2476 0.1512 0.1606 0.3789 0.1101 0 0.1706 0.0711

S//ur~sco/des 0.0240• 0.0240• 0.2500• 0.2000• 0.2400• 0 0 0

spp. 0.0910 0.0910 0.3700 0.2800 0.2900

Note: Data are expressed as mean + standard deviation.

Table 3 The overlap between pairs of the nmtazoan parasites, E. anchorams, P . pams//ur/ and Sibarodiscoides spp. on gills of S. asoms hi Jiangkou Reservoir in J'mng~d Province,

China, calculated frmn monthly data Month

Overlap III V VI VII IX X XI XII

EA + PP 0.5287 0.5337 0.5030 0.6039 0.5325 0.6212 0.5298 0.5086

EA + SP 0.5144 0.5337 0.5023 0.5773 0.5599 0.7424 0.5149 0.5043

PP + SP 0.9857 0.0000 0.9993 0.9734 0.9726 0.8788 0.9851 0.9951

EA: Ergasilus anchoratus ; PP: P. paras//ur/; SP: S//urod/sco/de~ spp. ; EA + PP: the overlap between E. anchorams and P.

paras//ud, and so on.

The niche overlap for pairs of the parasites was examined for the entire study period (Table 3). In general, the overlap between P. parasiluri and Silurodiscoides spp. was greater than that between E. anchoratus and P. parasiluri or S//urod/sco/des spp. (Mann-Whitney U-test,P =0.014, same for each comparison), indicating that P . paras//ur/and S / / ~ / d e s spp. were rnom overlap-distributed on the gills. The overlap between E. anchoratus and the others had no statistical differences at all (same te~t, but P = 0.92). The overlap between P . paras//ur/and S//urod/sco/des spp. was further demonstrated by the overlap calculated from the pooled data(Table 4).

58 CHIN. J. OCEANOL. LIMNOL., 18(1), 2000

Table 4 'I'ne overlap between pairs of the metazoan parasites, E. anchoratus, P. paras/h~ and SUurodiscoides spp. on gills of S. asotus in J'mngkou Reservoir in Jiangxi

Province, China, calculated from the Imoled data

E. anchoratus P. parasiluri Silurodiscoides spp.

E. anchoratus 0.5198 0.5177

P . paras//ur/ 0.9979 S//urod/sco/des spp.

DISCUSSION

In general, species which coexist exhibit features of resource partitioning (Werner, 1986). Koskivaara et al. (1992) found that dactylogyrids on roach partition their common resources both spatially and temporally by segregation of microhabitat utilization. In their system, nine species of dactylogyrids were found with two most abundant species being considered as core species, and the niche breadths and species overlaps of some of the Dactylogyrus species were characterized by abun- dance, which led them to conclude that competition does not restrict the distribution of all species, although there were some indications of possible competitive restrictions when the effect of absence or presence of other species on niche breadths was examined. The finding of higher infection levels of E. anchoratus and relatively low infection levels of P. parasiluri and Silurodiscoides spp. may in- dicate the dominance of E. anchoratus in the metazoan parasite communities, wherein E. anchora- tus can well be considered as the core species.

In the present system, E. anchoratus was distributed almost evenly on the four gill arches without any gill-areh preference observed. However, gill-arch preferences were reported as common in systems where parasites are usually the monogeneans, and the preferences as indicated by propor- tional distribution and niche breadth are normally related to abundance and seasonality of the mono- geneans although some species of monogeneans have restricted distributions on some gill arches (Buchmann, 1989; Koskivaara et a l . , 1992; Nie, 1996). Although E. anchoratus exhibited sea- sonal changes in infection levels and in reproduction (Nie, 1998), the observed pattern of unre- stricted distribution of the copepod on gill arches may reflect simply that E. anchoratus does not ex- hibit any feature of gill arch preference.

Ergasilus anchoratus, like the monogeneans on freshwater fish gills, also has a direct life cycle and uses its specialized antennae for attachment which differ from haptors of monogeneans. Never- theless, the copepods and monogeneans are to some extent very similar in life cycle and ways of at- tachment. But their movements may differ considerably. E. anchoratus may simply move itself us- ing either its antennae or swimming limbs, while monogeneans move by way of looping. Parasitic copepods may thus be capable of moving frequently on fish gills and this may account for the ob- served pattern of um~stricted distribution of E. anchoratus. On the other hand, the almost even distribution of the copepod may also indicate the possible occurrence of intraspecifice competition, as proposed by Rohde (1991) and Koskivaam and Valtonen(1992) for parasites on fish gills. How- ever, the influence of the moving ability of E. anchoratus and intraspecific relationship on its dis- tribution on gill arches requires experimetal investigation.

Gill-arch preferences were also not observed in P. parasiluri and Silurodiscoides spp. The in-

NIE et al. : PARASITES ON S. ASOTUS 59

fection levels of the copepod and the monogeneans were extremely low and in some samples only sev- eral specimens of the parasites were found. In a study on the seasonal occurrence of monogeneans in the genus Silurodiscoides on silurid fish in a reservoir, Huang (1964) found that the species compo- sition and their numbers were subject to seasonal changes and were higher than those in the present system. The lower infection levels of P. parasiluri and Silurodiscoides spp. in the present study may thus obscure the gill-arch preferences by the parasites, and this may also indicate the dominance of E. anchoratus on gills of S. asotus in the reservoir. However, P. parasiluri and Silurodiscoides spp. may also use other species of fish as the major hosts where they may have a higher infection rate,as reported for other species offish (Pan et a l . , 1990; Kuang and Qian, 1991).

Koskivaara et al. (1992) found that the overlap between monogeneans on fish gills were clearly affected by abundance during the period of greatest species diversity. Adams (1986) examined the interspecific interactions and community structure of six parasites on fish gills, and found that the second and third gill arches had the greatest species diversity and that, when niche breadths and overlap of the species were considered, they were capable of evenly distributing on the arches. The distribution of the metazoan parasites on gills of S. asotus agree well with the findings of Adams (1986). The overlap observed between P. parasiluriand Silurodisoides spp. might have resulted from the distribution of the parasites on the same gill arches. But due to the low infection levels of the parasites and rich resources on fish gills, it seems unlikely that the overlap observed between P . parasiluri and Silurodiscoides spp. indicates any occurrence of interspecific competitions.

Many other influencing factors were suggested for the gill-arch preference. Host immunore- sponses (Arme and Halton 1972; Koskivaara et a l . , 1991) and physical conditions (Gelnar, 1987) may have some impact on the population size of the parasites but the effects tend to be equal on each gill arch (Koskivaara et al. 1992). Several authors suggested the importance of water current over the gill arches (Hanek and Fernando, 1978) and surface areas of different gill arches (Wootten, 1974; Nie, 1996). But as suggested by Koskivaara et al. (1992), water current is probably similar in all seasons and it seems improbable that the reactions of parasites to the current may vary season- ally. The unrestricted distributions observed in the present study also support the view as proposed above by Koskivaara et al. (1992). The gill filaments on the four gill arches of fish may be different and indeed such difference exists in S. asotus (Anonymous, 1976). Why gill arches with more frla- ments or bigger surface areas do not harbour more parasites is at present difficult to explain although further experimental research may provide explanations. Indeed, laboratory experiments are required to clarify the gill-arch preferences and the relationship among the parasites on gills of the fish, S. o~ott/~.

ACKNOWLEDGEMENTS

The field work was partially supported by Mr. Liu Jianxiong, to whom many thanks are due.

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