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Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis

Published online by Cambridge University Press:  15 July 2011

C. A. RAUQUE ,
R. A. PATERSON ,
R. POULIN  and
D. M. TOMPKINS
C. A. RAUQUE*
Affiliation:
Laboratorio de Parasitología, INIBIOMA (CONICET-Universidad Nacional del Comahue), 1250 Quintral, San Carlos de Bariloche 8400, Argentina
R. A. PATERSON
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
D. M. TOMPKINS
Affiliation:
Landcare Research, Private Bag 1930, Dunedin 9054, New Zealand
*
*Corresponding author: Laboratorio de Parasitología, INIBIOMA (CONICET-Universidad Nacional del Comahue), 1250 Quintral, San Carlos de Bariloche 8400, Argentina. Tel: +54 2944 423374. Fax: +54 2944 422111. E-mail: [email protected]
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Summary

There is a gap in our understanding of the relative and interactive effects of different parasite species on the same host population. Here we examine the effects of the acanthocephalan Acanthocephalus galaxii, an unidentified cyclophyllidean cestode, and the trematodes Coitocaecum parvum and Microphallus sp. on several fitness components of the amphipod Paracalliope fluviatilis, using a combination of infection surveys and both survival and behavioural trials. In addition to significant relationships between specific parasites and measures of amphipod survival, maturity, mating success and behaviour, interactions between parasite species with respect to amphipod photophilia were also significant. While infection by either A. galaxii or C. parvum was associated with increased photophilia, such increases were negated by co-infection with Microphallus sp. We hypothesize that this is due to the more subtle manipulative effect of A. galaxii and C. parvum being impaired by Microphallus sp. We conclude that the low frequency at which such double infections occur in our sampled population means that such interactions are unlikely to be important beyond the scale of the host individual. Whether or not this is generally true, implying that parasitological models and theory based on single parasite species studies do generally hold, requires cross-species meta-analytical studies.

Keywords

Paracalliope fluviatilishost fitnessparasiteshost behaviourreproductionsurvivalMicrophallus sp.Acanthocephalus galaxiiCoitocaecum parvumCyclophyllidea sp
Type
Research Article
Information
Parasitology , Volume 138 , Issue 9 , August 2011 , pp. 1176 - 1182
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Babirat, C., Mouritsen, K. N. and Poulin, R. (2004). Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. Journal of Helminthology 78, 195–199.CrossRefGoogle Scholar
Behnke, J. M., Eira, C., Rogan, M., Gilbert, F. S., Torres, J., Miquel, J. and Lewis, J. W. (2009). Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus. Parasitology 136, 793–804.CrossRefGoogle Scholar
Beldomenico, P. M. and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious cycles? Trends in Ecology & Evolution 25, 21–27.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1973). Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59, 945–956.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.Google Scholar
Bollache, L., Gambade, G. and Cézilly, F. (2001). The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda). Behavioral Ecology and Sociobiology 49, 296–303.CrossRefGoogle Scholar
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle ScholarPubMed
Cézilly, F., Gregoire, A. and Bertin, A. (2000). Conflict between co-occurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Cothran, R. D. (2004). Precopulatory mate guarding affects predation risk in two freshwater amphipod species. Animal Behaviour 68, 1133–1138.Google Scholar
Ebert, D. (2011). A genome for the environment. Science 331, 539–540.CrossRefGoogle ScholarPubMed
Fredensborg, B. L. and Poulin, R. (2006). Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology 75, 44–53.Google Scholar
Graham, A. L., Lamb, T. J., Read, A. F. and Allen, J. E. (2005). Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases 191, 410–421.CrossRefGoogle ScholarPubMed
Hine, P. M. (1977). Acanthocephalus galaxii n. sp. parasitic in Galaxias maculatus (Jenyns, 1842) in the Lema Stream, New Zealand. Journal of the Royal Society of New Zealand 7, 51–57.CrossRefGoogle Scholar
Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. (2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Jolles, A. E., Ezenwa, V. O., Etienne, R. S., Turner, W. C. and Olff, H. (2008). Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 2239–2250.CrossRefGoogle ScholarPubMed
Keeling, M. J. and Rohani, P. (2007). Modelling Infectious Diseases in Humans and Animals. Princeton University Press, Princeton, NJ, USA.Google Scholar
Kruschwitz, L. G. (1978). Environmental factors controlling reproduction of the amphipod Hyalella azteca. Proceedings of the Oklahoma Academy of Science 58, 16–21.Google Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.CrossRefGoogle ScholarPubMed
Lefebvre, F., Fredensborg, B., Armstrong, A., Hansen, E. and Poulin, R. (2005). Assortative pairing in the amphipod Paracalliope fluviatilis: a role for parasites? Hydrobiologia 545, 65–73.CrossRefGoogle Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London 428, 840–844.CrossRefGoogle ScholarPubMed
Macfarlane, W. V. (1939). Life cycle of Coitocaecum anaspidis Hickman, a New Zealand digenetic trematode. Parasitology 31, 172–184.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Plaistow, S. J., Bollache, L. and Cézilly, F. (2003). Energetically costly precopulatory mate guarding in the amphipod Gammarus pulex: causes and consequences. Animal Behaviour 65, 683–691.Google Scholar
Poulin, R. (2001 a). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.), S3–S11.CrossRefGoogle ScholarPubMed
Poulin, R. (2001 b). Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623–630.Google Scholar
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.Google Scholar
Poulin, R., Nichol, K. and Latham, A. D. M. (2003). Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425–433.CrossRefGoogle ScholarPubMed
Rauque, C. (2007). Life cycle of acanthocephalans of aquatic Andean Patagonic environments. Ph. D. thesis, National University of Comahue, Argentina.Google Scholar
Rauque, C. and Semenas, L. 2007. Infection pattern of two simpatric acanthocephalan species in Hyalella patagonica (Amphipoda: Hyalellidae) from Lake Mascardi (Argentina). Parasitology Research 100, 1271–1276.CrossRefGoogle Scholar
Rauque, C. and Semenas, L. (2009). Effects of two acanthocephalan species on the reproduction of Hyalella patagonica (Amphipoda, Hyalellidae) in an Andean Patagonian lake. Journal of Invertebrate Pathology 100, 35–39.Google Scholar
Rousset, F., Thomas, F., De Meeus, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distributions of parasite loads. Ecology 77, 2203–2211.Google Scholar
Smith, K. F., Acevedo-Whitehouse, K. and Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.CrossRefGoogle Scholar
Sparkes, T. C., Wright, V. M., Renwick, D. T., Weil, K. A., Talkington, J. A. and Milhalyov, M. (2004). Intra-specific host sharing in the manipulative parasite Acanthocephalus dirus: does conflict occur over host modification? Parasitology 129, 335–340.CrossRefGoogle ScholarPubMed
Sutherland, D. L., Hogg, I. D. and Waas, J. R. (2007). Is size assortative mating in Paracalliope fluviatilis (Crustacea: Amphipoda) explained by male–male competition or female choice? Biological Journal of the Linnean Society 92, 173–181.Google Scholar
Thomas, F., Fauchier, J. and Lafferty, K. D. (2002). Conflict of interest between a nematode and a trematode in an amphipod host: test of the “sabotage” hypothesis. Behavioral Ecology and Sociobiology 51, 296–301.CrossRefGoogle Scholar
Thomas, F., Renaud, F. and Poulin, R. (1998). Exploitation of manipulators: hitch-hiking as a parasite transmission strategy. Animal Behaviour 56, 199–206.Google Scholar
Tompkins, D. M. and Begon, M. (1999). Parasites can regulate wildlife populations. Parasitology Today 15, 311–313.Google Scholar
Tompkins, D. M., Dunn, A. M., Smith, M. J. and Telfer, S. (2011). Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38.CrossRefGoogle ScholarPubMed
Williams, C. M., Poulin, R. and Sinclair, B. J. (2004). Increased haemolymph osmolality suggests a new route for behavioural manipulation of Talorchestia quoyana (Amphipoda: Talitidae) by its mermithid parasite. Functional Ecology 18, 685–691.Google Scholar