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International Journal for Parasitology 29 (1999) 1793±1801

Factors aecting abundance of Triaenophorus infection in Cyclops strenuus, and parasite-induced changes in host ®tness A.F. Pasternak 1, K. Pulkkinen *, V.N. Mikheev 2, T. Hasu, E.T. Valtonen Department of Environmental and Biological Science, University of JyvaÈskylaÈ, P.O. Box 35, 40351 JyvaÈskylaÈ Finland Received 4 May 1999; received in revised form 22 June 1999; accepted 22 June 1999

Abstract Factors aecting the abundance of Triaenophorus crassus and Triaenophorus nodulosus procercoids in their copepod ®rst intermediate host, Cyclops strenuus, and eects of infection on feeding behaviour, reproduction and survival of the host were studied experimentally. When exposed to the same number of coracidia, copepods harboured considerably less procercoids in the trials where ciliates or Artemia salina nauplii were given as alternative food items. The prevalence of infection was higher in adult copepods as compared with copepodite stage IV and stage V, and higher in stage V than in stage IV. The prevalences in adult females and males did not dier signi®cantly from each other. The frequency of females carrying egg sacs was lower among infected than among exposed uninfected and unexposed copepods. The rate of feeding on Artemia nauplii remained at the same level in uninfected copepods, but decreased strongly in infected copepods during 7 days p.i. The survival of unexposed, exposed uninfected and infected copepods did not dier signi®cantly from each other for the ®rst 11 days postexposure, but the mortality of infected copepods increased signi®cantly after 3 weeks post-exposure. However, the rate of development and mortality of copepods might have been aected by the apparently arrested development of stage IV copepodites found in the experiment. Some of the contradictions between these results and earlier observations are suggested to be caused by the dierences in the duration of exposure, intensity of infection and duration of observation post-exposure in the present study as compared with other experiments. # 1999 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. Keywords: Cestode; Copepod; Fecundity; Infectivity; Survival; Triaenophorus

* Corresponding author. Tel.: +358-14-260-2332; fax: +358-14-260 2321. E-mail address: [email protected].® (K. Pulkkinen) 1 Present address: Institute of Oceanology, Russian Academy of Science, 36 Nakhimov Avenue, Moscow 117 853, Russia. 2 Present address: A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Science, 33 Leninskii Prospekt, Moscow 117071, Russia.

1. Introduction Copepods often serve as ®rst intermediate hosts for tapeworms of ®shes. Copepods acquire the free-living coracidia larvae through feeding [1]. The host ®nding of coracidia is passive, as they do not respond actively to signals from the environment or the host [2].

0020-7519/99/$20.00 # 1999 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 0 - 7 5 1 9 ( 9 9 ) 0 0 1 0 8 - 3

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A.F. Pasternak et al. / International Journal for Parasitology 29 (1999) 1793±1801

Transmission is thus determined by environmental factors, the abundance of both parasites and hosts, and the feeding behaviour of the hosts [1]. Cyclopoid copepods are omnivorous crustacean predators that feed raptorially and select for soft-bodied prey items [3]. Pseudophyllidean coracidia resemble in appearance ciliate protozoans, which are preyed upon by many cyclopoids [3±5]. Whether cyclopoids can distinguish between coracidia and ciliates and how the presence of ciliates or other alternative food items aects parasite uptake have not been examined so far. Size, developmental stage [6±8] and sex [9±11] of the copepod have been shown to aect its probability of acquiring cestode infection. However, the eects of these factors have been found to vary in dierent copepod±parasite systems. Parasites have been shown to modify feeding patterns of their intermediate hosts [12, 13]. Both decreases [14, 15] and increases [16] in foraging eciency of parasitised animals have been described. Hosts may try to compensate for the increased nutritional demands caused by the parasite with increased foraging [15, 17]. However, few studies have examined the eect of larval cestodes on the food intake of their ®rst intermediate copepod hosts [18, 19]. Parasites can adversely aect on the ®tness of their hosts by decreasing host fecundity and/ or survival (e.g. [20±22]). Cestode infections have been observed to aect copepod fecundity [10, 19, 23] and survival [8, 9], but contradictory results also exist [10, 18, 19, 23]. The present work aimed to experimentally study the interactions of larval stages of Triaenophorus with the ®rst intermediate host, Cyclops strenuus, by examining factors aecting the acquisition of Triaenophorus coracidia by C. strenuus and the eect of Triaenophorus infection on factors aecting the ®tness of C. strenuus. 2. Materials and methods 2.1. Obtaining coracidia and infecting cyclopoids Spawning pike, Esox lucius L., were obtained

from Lake Saimaa in southeast Finland after the spring ice melt in 1994 and 1997. Fish were caught by netting, killed, and stored at 58C for up to 48 h. In the laboratory, mature Triaenophorus were removed from the intestine, and identi®ed as Triaenophorus crassus or Triaenophorus nodulosus according to the scolex hooks. Eggs were obtained from gravid worms and stored in the dark at 2±58C for up to 2 months each year according to the method described by Rosen and Dick [9]. Coracidia were used for experimental infections within 24 h of hatching. A culture of C. strenuus originating from lakes near JyvaÈskylaÈ, in central Finland, was maintained in aerated water at 178C and fed with ciliates. Part of the stock culture was ®ltered through a 250 mm sieve and copepodites stage IV and stage V, as well as adult males and females, retained in the sieve were used for experimental infections. Copepods were exposed to freshly hatched T. crassus coracidia for 30 min (eect of developmental stage, egg clutch production) or to a mixture of T. crassus and T. nodulosus coracidia for 1 h (alternative food, feeding rate experiments). The copepods were separated from uneaten coracidia with a 90 mm sieve, placed in 1 L jars, and fed with ciliates. The control copepods were treated similarly at each step of the procedure, except for exposure to coracidia. Exposures were conducted at 19±228C, after which the experimental animals were transferred to 178C, with the exception of the alternative food and feeding rate experiments, which were carried out at 19±228C and 19±258C, respectively, at the ®eld station where conditioned temperature was not available. 2.2. Eect of alternative food on abundance of Triaenophorus infection Ciliates and 1-day-old Artemia salina nauplii were used as alternative food items for copepods exposed simultaneously to coracidia. Individual Artemia nauplii were measured and counted under a dissecting microscope and the abundances and sizes of the ciliates and coracidia were evaluated in a plankton counting chamber


under a light microscope. The diameters of the ciliates and coracidia were approx. 40 mm and the body length of Artemia nauplii approx. 400 mm. Volumes of each of the food items were calculated by assuming coracidia as spherical, ciliates as oval and Artemia as cone-shaped objects. Concentrations (by volume) of each type of food were evaluated to approx. 20 mm3 l ÿ 1. Copepods pre-starved for a day were placed in three plastic jars, 50±60 individuals per jar. The copepods were exposed either to coracidia only (treatment 1), coracidia and ciliates (treatment 2) or coracidia and A. salina nauplii (treatment 3), so that the concentration of the food particles in the treatments 2 and 3 was twice as high as in treatment 1. At 8±10 days post-exposure (p.e.), the intensity of infection was examined by placing living copepods individually with a ®ne pipette in a thin layer of water on a glass slide under a compound microscope using 125±500 magni®cation. Dierences in mean abundance [24] among the three treatments were analysed with ANCOVA, using length of the copepod as a covariate. Pairwise comparisons were made with single degree of freedom hypotheses (SYSTAT 6.0 for Windows: Statistics. SPSS, 1996) without the eect of the covariate. 2.3. Infectivity in relation to developmental stage of the host and eect of infection on egg clutch production in females A subsample of around 200 copepods was thoroughly stirred and divided into two 1 L plastic jars. One of the jars was randomly chosen for exposure and the other acted as an unexposed control. Copepods were exposed to freshly hatched coracidia as described above. At days 8± 10 p.e., all copepods in both jars were counted, and their developmental stage and infection status examined as described above. The trial was repeated eight times within a month. For each trial, the percentage of infected and uninfected adults and stage IVs and stage Vs in the exposure jars was recorded. The percentage of females carrying egg sacs was recorded both among uninfected and infected exposed copepods and the unexposed control copepods. Dierences between

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the prevalence of infection in dierent developmental stages of host, as well as dierences between the percentage of females carrying egg sacs, were analysed with repeated measures ANOVA, since the parameters were dependent on each other within each trial. The pairwise comparisons between the prevalences in dierent developmental stages and females carrying egg sacs in dierent exposure groups were performed with non-orthogonal contrasts using the Bonferroni correction and with orthogonal contrasts, respectively. 2.4. Eect of infection on the feeding rate of copepods Copepods exposed to coracidia, as well as unexposed copepods, were placed individually into 40 ml beakers containing 10 1-day-old nauplii of A. salina. Copepods were allowed to feed on nauplii for 5 h, after which the copepods were transferred to fresh ®ltered water, and the remaining nauplii were counted. Damaged nauplii were assumed to comprise one-half of an intact specimen. The exposed copepods were screened on day 2 p.e. and those with established procercoids were included in the experiment. Daily observations for 7 consecutive days were made on 13 uninfected and 10 infected copepods. The data were analysed using linear regressions, on both uninfected and infected copepods. 2.5. Eect of infection on the survival of the host Copepods of the copepodite stage IV were removed individually from the stock culture and placed in groups of 10 into 20 100-ml jars. Ten of the jars were randomly chosen for exposure. Five-hundred microlitres of water containing freshly hatched coracidia (880 2110; mean 2 S.D.) were added to each exposure jar, and the same amount of aged charcoal-®ltered tap water to each control jar. The copepods were allowed to feed on coracidia for 24 h, after which they were removed individually with a pipette and transferred into fresh water. The jars were stored at 178C. Animals were fed with ciliates ad libitum and their survival was checked on alter-

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Fig. 1. Mean abundance (2S.E.M.) of Triaenophorus infection in Cyclops strenuus fed with coracidia only, with a mixture of coracidia and ciliates, and with a mixture of coracidia and Artemia salina nauplii.

nate days, starting from day 1 p.i. Dead copepods were checked for procercoid infection and their developmental stage was recorded. The experiment was terminated on day 49 p.i. The surviving copepods were anaesthetised with carbon dioxide and examined for infection as described above.

3. Results Mean abundances of Triaenophorus procercoids in copepods diered signi®cantly among the three treatments in the experiment where the eect of oering an alternative food on acquisition of Triaenophorus infection was examined (Fig. 1; ANCOVA F = 6.126, P = 0.003). Copepod length did not signi®cantly aect the mean abundance of infection (ANCOVA

Fig. 2. Mean percentage (2S.E.M.) of infected individuals in dierent developmental stages of Cyclops strenuus.

Fig. 3. Feeding rate of (a) uninfected and (b) infected Cyclops strenuus. Lines represent linear regressions.

F = 0.002, P = 0.967). The mean abundance in the ®rst treatment was not statistically dierent from the sum of the mean abundances in the other two treatments (ANOVA, single degree of freedom design F = 1.235, P = 0.269) and treatments 2 and 3 did not dier signi®cantly from each other (ANOVA, single degree of freedom design F = 0.043, P = 0.836). The percentage of infected copepods diered signi®cantly between the dierent developmental stages (Fig. 2) (repeated measures ANOVA F3,21 = 71.025, P < 0.001). Copepodite stage Vs were infected around four times more frequently than stage IVs (Fig. 2; repeated measures ANOVA, non-orthogonal within-subjects contrasts F1,7 = 18.970, P = 0.009), and the prevalence of infection in adult specimens was signi®cantly higher than in copepodite stages (F1,7 = 191.097, P < 0.001). The prevalences of infection in the adult males and females did not dier signi®cantly (F1,7 = 5.231, P = 0.168). The feeding rate of uninfected copepods remained stable over the 7-day experiment (Fig. 3a; regression coecient B =ÿ 0.059,


Fig. 4. Mean (2S.E.M.) percentage of unexposed, exposed uninfected and infected female Cyclops strenuus carrying egg sacs.

S.E.M. = 0.467, P = 0.573). Infected copepods ingested the same amount of nauplii on day 1 p.i. as uninfected copepods (Fig. 3b), but then gradually decreased their food intake to almost zero at day 7 (Fig. 3b; B =ÿ 0.375, S.E.M. = 0.068, P < 0.001). Females carrying egg sacs were approximately eight times less frequent among the exposed infected copepods than among exposed uninfected or unexposed females (Fig. 4; repeated measures ANOVA, within-subjects contrasts F1,7 = 11.445, P = 0.012). The unexposed and exposed uninfected females produced egg sacs at almost equal frequencies (repeated measures ANOVA, within-subjects contrasts F1,7 = 0.052, P = 0.826). Survival curves for the unexposed, exposed uninfected and exposed infected copepods differed signi®cantly from each other during the 49day observation period (Fig. 5; non-parametric log-rank test w 2 = 16.134, P < 0.001). All three survival curves overlapped for the ®rst 20 days of observation, after which the mortality of infected copepods increased more than that of unexposed and exposed uninfected copepods, while the curves for the latter two groups continued to overlap for the rest of the observation period (Fig. 5). The mean abundance of procercoids was 0.9 (S.D. = 1.32, range 0±5) in exposed copepods that died during the experiment and 0.2 (S.D. = 0.71, range 0±3) in exposed copepods that were alive at the end of the experiment 49 days p.e. Exposed copepodite IV stages (21 of

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Fig. 5. Survival (mean2S.E.M.) for unexposed (open circles), exposed uninfected (solid squares) and exposed infected (open squares) copepods during 49 days post-exposure.

100) developed into higher developmental stages (copepodite stage Vs, males or females) during the experiment signi®cantly more often than unexposed copepodite IVs (11 of 101) (Pearson chi-square w 2 = 3.836, P = 0.050).

4. Discussion 4.1. Factors aecting acquisition of coracidia by Cyclops strenuus In experiments where copepods were oered only larval parasites on which to feed, the resulting infection level in copepods has been found to follow a functional response curve reaching a plateau, a response typical of predator±prey interactions [8, 25]. In the natural environment coracidia comprise only a fraction of available prey items for cyclopoid copepods, and the probability of coracidia being eaten may be diminished by the dilution eect and/or selective consumption. In the present work, copepods exposed to the same number of coracidia harboured considerably fewer procercoids when simultaneously oered alternative prey items. The mean abundances in the three treatments seemed to be directly proportional to the density of coracidia, i.e. the mean abundance in treatment 1, where only coracidia were oered, was two times higher than in treatments 2 and 3, where alternative food items were oered. This kind of result could be expected if the copepods ate the food

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items unselectively. Therefore, the copepods appeared to prey on ciliates and coracidia as encountered, and could not distinguish between them. Cyclopoids have been shown to select larger zooplankton over ciliates [3], and therefore could have been expected to prefer Artemia over ciliates. However, interpretation of the result of treatment 3 is complicated due to the size dierence, and hence dierences in handling times between Artemia and coracidia, and the selective consumption could not be proven. Nevertheless, our results indicate that the success of cestode transmission to ®rst intermediate hosts depends not only on the densities of infective stages and hosts, and their spatial distributions [26], but also on availability and size range of alternative prey. The probability of acquiring procercoid infection in copepods has been shown to increase with the increasing number of coracidia ingested [8, 10]. This, in turn, depends on encounter and ingestion rates, and larger copepods would therefore be exposed to coracidia more frequently than smaller individuals due to their greater swimming and foraging activity. When exposure time is short, adult copepods would be infected more frequently than younger stages. However, if the exposure time is long, even a small copepodite is able to encounter and ingest several coracidia. It has been suggested that coracidia might penetrate the intestine of young copepods more easily than that of adults [8], and the probability of becoming infected in young copepods might therefore increase to a relatively greater extent than in adults when the duration of the exposure increases. Allowing for diering interactions between dierent host and parasite species, the results obtained from several studies on copepod±cestode interactions could be attributed to the duration of experimental exposures. In studies where exposure time was short (30± 60 min), the prevalence of infection in adult individuals exceeded that in stage Vs and stage IVs ([23]; the present study). However, in studies where the exposure times were much longer, young copepodites were found to harbour a higher parasite burden than gravid females [8], or the copepod±procercoid relationship was found to be unaected by the copepod developmental

stage [7]. On the basis of their smaller size and slower swimming speed [27], male cyclopoids could therefore be expected to be exposed to coracidia less frequently than females. However, their level of infection did not dier from that in females in the present study. This is probably due to the higher susceptibility to parasitic infection in males than females [10, 11]. 4.2. Eects of procercoids on their copepod hosts In the present work the feeding rate of C. strenuus infected with Triaenophorus procercoids decreased to almost zero during the ®rst week p.i., while in uninfected copepods it remained stable. The result is similar to that observed by Pasternak et al. [19] in Cyclops infected with Diphyllobothrium spp., although in their experiments the adverse eect on feeding became apparent only after 3 weeks. The relatively high temperature (19±258C) in the present experiment may have accelerated the development of the procercoid [28] and enhanced its possible pathogenic eect on the copepod. However, the results of Shostak and Dick [18] implied that T. crassus infection did not aect the feeding of copepods on Paramecium during 10 days p.i. These three studies, including the present one, are the only cases where the food intake in infected copepods has been studied. These results might indicate that procercoid infection aects the copepod's encounter rate with, or its ability to catch and handle, large prey such as Artemia rather than its ability to ingest and digest food, but more systematic studies are needed to verify this. Triaenophorus crassus infection was also found to aect adversely both the fecundity and survival of C. strenuus. The eect on fecundity was detected 8±10 days p.i., while that on survival became apparent after 3 weeks p.i. However, the exposure to coracidia as such did not aect either fecundity or survival. Shostak and Dick [18] did not observe any eect of T. crassus infection on fecundity or timing of egg clutch release in Cyclops bicuspidatus thomasi, provided that the copepods received as much food as uninfected ones, nor did they detect any parasite-induced mortality. However, in the experiments of Rosen


and Dick [9] with the same copepod±cestode system, two mortality peaks were found, at days 1± 4 and 13±20 p.i. One factor explaining the contradictory results on the eect of cestodes on copepod fecundity may be dierences in the feeding regimens of copepods in the experiments, which would aect the energy available for both the copepod and the parasite. One factor contributing to contradictory results on eect on survival might be the dierences in the number of parasites harboured and the duration of the observation period p.e. in these experiments, which is also discernible in the studies with other copepod±cestode systems. A pronounced increase in mortality of infected copepod hosts was observed in studies where the mean number of procercoids was high (three to ®ve parasites per copepod) or the duration of infection was long (more than 20 days) ([8, 9]; the present study), but no eect on the survival of infected hosts was detected in experiments where infection intensity was lower or duration of infection shorter [10, 18, 19]. In the survival experiment, the development of both exposed and unexposed stage IV copepodites was unexpectedly delayed, so that only a small proportion of them developed into subsequent stages (stage Vs and adults). The duration of the experiment (49 days) was long enough for the stage IVs to have developed into adults at the temperature of 178C used [29, 30]. It is possible that, for an unknown reason, some of the stage IV copepodites were in active diapause, during which their development and growth is arrested [31]. During this phase the copepodites are able to feed, however, although at a lower rate than active individuals [32]. Kuperman and Kireev [23] found the development time of stage IVs and stage Vs to be prolonged due to T. nodulosus infection in C. strenuus. In the present work exposed copepods (including both infected and uninfected) had developed into next developmental stages more often than unexposed ones, which is contradictory to Kuperman and Kireev's [23] results. The present result on the survival of infected copepods is consistent with our earlier experience from the same copepod±cestode system in cases when no delayed development was observed (K Pulkkinen, T Hasu, ET Valtonen,

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unpublished observations). However, the possibility of an active diapause complicates the situation, and could be an additional factor when considering the dynamics of parasite±host interaction. The transmission of a parasite with a complex life-cycle depends on the eciency of the intermediate host functioning, i.e. whether the host can acquire the parasite, support its growth and development, and transfer it to the next host. We have demonstrated that besides the well-known dependence on concentrations of both hosts and parasites, acquisition of coracidia by copepod hosts also depends on the presence of alternative prey and host population structure. We also demonstrated adverse eects of Triaenophorus infection on feeding behaviour, fecundity and survival of infected copepods. The usage of a mixture of T. crassus and T. nodulosus coracidia in the alternative food and feeding rate experiments may have resulted in dierent results than would have been obtained from experiments with single-species infections. However, no evidence of interaction between the two species in simultaneous infections exists, and two such closely related species with very similar life-cycles [23] are likely to produce similar responses in the same host. For T. crassus, we have shown also that it increases the vulnerability of C. strenuus to predation by the second intermediate host, white®sh Coregonus lavaretus, after procercoids have reached infectivity to white®sh at around 12 days p.i. (K. Pulkkinen, A.F. Pasternak, T. Hasu, E.T. Valtonen, unpublished observations), while the eect on survival was apparent only after 3 weeks p.i. in the present work. Therefore, the ®tness costs of T. crassus infection in natural populations of C. strenuus are likely to be manifested primarily by decreased fecundity and increased mortality through predation, rather than through a direct decrease in survival. Acknowledgements The authors are grateful to A. Niemi and K. Poikola for co-operation, M. Julkunen for help with the statistics, Dr J. Taskinen for comments

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on the manuscript and Dr R. Siddall for checking the English. The research was funded by the Finnish Graduate School for Fish Biology and Fisheries, Employment and Economic Development Centre of Kymi and a grant for the exchange of scientists between Finland and Russia from the Academy of Finland.

References [1] Mackiewicz JS. Cestode transmission patterns. J Parasitol 1988;74:60±71. [2] MacInnis AJ. How parasites ®nd hosts. Some thoughts on the inception of host±parasite integration. In: Kennedy CA, editor. Ecological aspects of parasitology. Amsterdam: North Holland, 1976;3±20. [3] Wickham SA. Trophic relations between cyclopoid copepods and ciliated protists: complex interactions link the microbial and classic food webs. Limnol Oceanogr 1995;40:1173±81. [4] Monakov AV. Feeding and food relationships in freshwater copepods. Leningrad: Nauka, 1976 [in Russian]. [5] Wickham SA. Cyclops predation on ciliates: species± speci®c dierences and functional responses. J Plankt Res 1995;17:1633±46. [6] Halvorsen O. Studies on the helminth fauna of Norway: VIII: an experimental investigation of copepods as ®rst intermediate hosts for Diphyllobothrium norvegicum Vik (Cestoda). Nytt Mag Zool 1966;13:83±117. [7] Dupont F, Gabrion C. The concept of speci®city in the procercoid±copepod system: Bothriocephalus claviceps (Cestoda) a parasite of the eel (Anguilla anguilla). Parasitol Res 1987;73:151±8. [8] Nie P, Kennedy CR. Infection dynamics of larval Bothriocephalus claviceps in Cyclops vicinus. Parasitology 1993;106:503±9. [9] Rosen R, Dick TA. Development of the procercoid of Triaenophorus crassus Forel and mortality of the ®rst intermediate host. Can J Zool 1983;61:2120±8. [10] Wedekind C. The infectivity, growth and virulence of the cestode Schistocephalus solidus in its ®rst intermediate host, the copepod Macrocyclops albidus. Parasitology 1997;115:317±24. [11] Wedekind C, Jakobsen PJ. Male-biased susceptibility to helminth infection: an experimental test with a copepod. Oikos 1998;81:458±62. [12] Milinski M. Parasites and host decision-making. In: Barnard CJ, Behnke JM., editors. Parasitism and host behaviour. London: Taylor & Francis, 1990;95±116. [13] Moore J, Gotelli NJ. A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In: Barnard CJ, Behnke

[14]

[15]

[16]

[17]

[18]

[19]

[20]

[21]

[22]

[23]

[24]

[25]

[26]

[27]

[28]

[29]

JM, editors. Parasitism and host behaviour. London: Taylor & Francis, 1990;193±233. Crowden AE, Broom DM. Eects of the eye¯uke, Diplostomum spathaceum on the behaviour of dace (Leuciscus). Anim Behav 1980;28:287±94. Milinski M. Risk of predation of parasitized sticklebacks, Gasterosteus aculeatus L. under competition for food. Behaviour 1985;93:203±16. Williams CL, Gilberston DE. Altered feeding response as a cause for the altered heartbeat rate and locomotor activity of Schistosoma mansoni-infected Biomphalaria glabrata. J Parasitol 1983;69:671±6. Holmes JC, Zohar S. Pathology and host behaviour. In: Barnard CJ, Behnke JM, editors. Parasitism and host behaviour. London: Taylor & Francis, 1990;34±63. Shostak AW, Dick TA. Eect of food intake by Cyclops bicuspidatus thomasi (Copepoda) on growth of procercoids of Triaenophorus crassus (Pseudophyllidea) and on host fecundity. Am Midl Nat 1986;115:225±33. Pasternak AF, Huntingford FA, Crompton DWT. Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 1995;110:395±9. Dobson AP. The population biology of parasiteinduced changes in host behavior. Q Rev Biol 1988;63: 139±65. Barnard CJ. Parasitic relationships. In: Barnard CJ, Behnke JM., editors. Parasitism and host behaviour. London: Taylor & Francis, 1990;1±33. Hurd H. Physiological and behavioural interactions between parasites and invertebrate hosts. Adv Parasitol 1990;29:272±318. Kuperman BI, Kireev VK. The eect of procercoids of Triaenophorus nodulosus on the biology of their ®rst intermediate hosts, Cyclops strenuus [in Russian with English summary]. Parazitologiya (Leningr.) 1976;10:434±8. Bush AO, Laerty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997;83:575±83. Ashworth ST, Kennedy CR, Blanc G. Density-dependent eects of Anguillicola crassus (Nematoda) within and on its copepod intermediate hosts. Parasitology 1996;113:303±9. Keymer AE, Anderson RM. The dynamics of infection of Tribolium confusum by Hymenolepis diminuta: the in¯uence of infective-stage density and spatial distribution. Parasitology 1979;79:195±207. Gerritsen J. Instar-speci®c swimming patterns and predation of planktonic copepods. Verh Int Ver Limnol 1978;20:2531±6. Kuperman BI. Tapeworms of the genus Triaenophorus, parasites of ®shes. Leningrad: Nauka, 1973 [English translation, New Delhi: Amerind Publishing, 1981]. Elgmork K. Seasonal occurrence of Cyclops strenuus strenuus. Folia Limnol Scand 1959;11:1±196.

A.F. Pasternak et al. / International Journal for Parasitology 29 (1999) 1793±1801 [30] Maier G. The eect of temperature on the development, reproduction, and longevity of two common cyclopoid copepodsÐEucyclops serrulatus (Fischer) and Cyclops strenuus (Fischer). Hydrobiologia 1990;203:165± 75. [31] Elgmork K. Evolutionary aspects of diapause in fresh-

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water copepods. In: Kerfoot WC, editor. Evolution and ecology of zooplankton communities. Hanover, NH: University Press of New England, 1980;411±17. [32] Krylov PI, Alekseev VR, Frenkel OA. Feeding and digestive activity of cyclopoid copepods in active diapause. Hydrobiologia 1996;320:71±9.