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An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators

Published online by Cambridge University Press:  14 May 2008

V. MEDOC  and
J.-N. BEISEL
V. MEDOC
Affiliation:
Université Paul Verlaine-Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosystèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, rue du général Delestraint, F-57070 Metz, France
J.-N. BEISEL*
Affiliation:
Université Paul Verlaine-Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosystèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, rue du général Delestraint, F-57070 Metz, France
*
*Corresponding author: Tel: +(0)3 87 37 84 29. Fax: +(0)3 87 37 84 23. E-mail: [email protected]
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Summary

Among the potential effects of parasitism on host condition, the ‘increased host abilities’ hypothesis is a counterintuitive pattern which might be predicted in complex-life-cycle parasites. In the case of trophic transmission, a parasite increasing its intermediate host's performance facing non-host predators improves its probability of transmission to an adequate, definitive host. In the present study, we investigated the cost of infection with the acanthocephalan Polymorphus minutus on the locomotor/escape performance of its intermediate host, the crustacean Gammarus roeseli. This parasite alters the behaviour of its intermediate host making it more vulnerable to predation by avian definitive hosts. We assessed the swimming speeds of gammarids using a stressful treatment and their escape abilities under predation pressure. Despite the encystment of P. minutus in the abdomen of its intermediate host, infected amphipods had significantly higher swimming speeds than uninfected ones (increases of up to 35%). Furthermore, when interacting with the non-host crustacean predator Dikerogammarus villosus, the highest escape speeds and greatest distances covered by invertebrates were observed for parasitized animals. The altered behaviour observed among the manipulated invertebrates supported the ‘increased host abilities’ hypothesis, which has until now remained untested experimentally. The tactic of increasing the ability of infected intermediate hosts to evade potential predation attempts by non-host species is discussed.

Keywords

escape responseGammarus roeselilocomotor performancenon-host predatorsparasite-induced behaviourPolymorphus minutus
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 8 , July 2008 , pp. 977 - 984
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Alibert, P., Bollache, L., Corberant, D., Guesdon, V. and Cézilly, F. (2002). Parasitic infection and developmental stability: fluctuating asymmetry in Gammarus pulex infected with two acanthocephalan species. The Journal of Parasitology 88, 47–54.CrossRefGoogle ScholarPubMed
Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle Scholar
Baldauf, S. A., Thünken, T., Frommen, J. G., Bakker, T. C. M., Heupel, O. and Kullmann, H. (2007). Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours. International Journal for Parasitology 37, 61–65.CrossRefGoogle ScholarPubMed
Bauer, A., Haine, E. R., Perrot-Minnot, M.-J. and Rigaud, T. (2005). The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli. Journal of the Zoological Society of London 267, 39–43.CrossRefGoogle Scholar
Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. and Cézilly, F. (2000). Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native invader gammarid species. International Journal for Parasitology 30, 1453–1457.CrossRefGoogle ScholarPubMed
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 65, 667–669.Google Scholar
Bollache, L., Devin, S., Wattier, R., Chovet, M., Beisel, J.-N., Moreteau, J.-C. and Rigaud, T. (2004). Rapid extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: potential consequences. Archiv für Hydrobiologie 160, 57–66.CrossRefGoogle 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., Grégoire, A. and Bertin, A. (2000). Conflict between co-occuring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630.CrossRefGoogle Scholar
Charniaux-Cotton, H. and Payen, G. (1985). Sexual differentiation. In The Biology of the Crustacea, vol.9. Integument, Pigments, and Hormonal Processes (ed. Bliss, D. E. and Manter, L. H.), pp. 217–300. Academic Press, New York.CrossRefGoogle Scholar
Devin, S., Piscart, C., Beisel, J.-N. and Moreteau, J.-C. (2004). Life history traits of the invader Dikerogammarus villosus (Crustacea: Amphipoda) in the Moselle River, France. International Review of Hydrobiology 89, 21–34.CrossRefGoogle Scholar
Dezfuli, B. S. & Giari, L. (1999). Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host-parasite interface. Folia Parasitologica 46, 117–122.Google Scholar
Dezfuli, B. S., Maynard, B. J. and Wellnitz, T. A. (2003). Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitologica 50, 129–134.CrossRefGoogle ScholarPubMed
Dick, J. T. A. and Platvoet, D. (2000). Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proceedings of the Royal Society of London 267, 977–983.CrossRefGoogle ScholarPubMed
Dick, J. T. A., Platvoet, D. and Kelly, D. W. (2002). Predatory impact of the freshwater invader Dikerogammarus villosus (Crustacea: Amphipoda). Canadian Journal of Fisheries and Aquatic Sciences 59, 1078–1084.CrossRefGoogle Scholar
Jazdzewski, K. (1980). Range extensions of some gammaridean species in European inland waters caused by human activity. Crustaceana 6, 84–107.Google Scholar
Kaldonski, N., Perrot-Minnot, M.-J. and Cézilly, F. (2007). Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Animal Behaviour 74, 1311–1317.CrossRefGoogle Scholar
Karaman, G. S. and Pinkster, S. (1977). Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda) Part II. Gammarus roeseli-group and related species. Bijdragen tot de Dierkunde 47, 165–196.CrossRefGoogle Scholar
Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. and Bollache, L. (2007). Modification of host's behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.CrossRefGoogle ScholarPubMed
Levri, E. P. (1998). The influence of non-host predators on parasite-induced behavioural changes in a freshwater snail. Oikos 81, 531–537.CrossRefGoogle Scholar
Maynard, B. J., Wellnitz, T. A., Zanini, N., Wright, W. G. and Dezfuli, B. S. (1998). Parasite-altered behavior in a crustacean intermediate host: field and laboratory studies. Journal of Parasitology 84, 1102–1106.CrossRefGoogle Scholar
McCahon, C. P., Maund, S. J. and Poulton, M. J. (1991). The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex). Freshwater Biology 25, 507–513.CrossRefGoogle Scholar
Médoc, V., Bollache, L. and Beisel, J.-N. (2006). Host manipulation of a freshwater crustacean (Gammarus roeseli) by an acanthocephalan parasite (Polymorphus minutus) in a biological invasion context. International Journal for Parasitology 36, 1351–1358.CrossRefGoogle Scholar
Moore, J. K. (1984). Altered behavioural responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist 123, 572–577.CrossRefGoogle Scholar
Moore, J. K. and Gotelli, N. J. (1990). Phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. and Behnke, J. M.), pp. 193–229. Taylor & Francis, London.Google Scholar
Mouritsen, K. M. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.CrossRefGoogle ScholarPubMed
Pascoe, D., Kedwards, T. J., Blockwell, S. J. and Taylor, E. J. (1995). Gammarus pulex (L.) feeding bioassay – effects of parasitism. Bulletin of Environmental Contamination and Toxicology 55, 629–632.CrossRefGoogle ScholarPubMed
Perrot-Minnot, M. J. (2004). Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis. International Journal for Parasitology 34, 45–54.CrossRefGoogle ScholarPubMed
Perrot-Minnot, M. J., Kaldonski, N. and Cézilly, F. (2007). Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. International Journal for Parasitology 37, 645–651.CrossRefGoogle Scholar
Piscart, C., Webb, D. and Beisel, J. N. (2007). An acanthocephalan parasite increases the salinity tolerance of the freshwater amphipod Gammarus roeseli (Crustacea: Gammaridae). Naturwissenschaften 94, 741–747.CrossRefGoogle ScholarPubMed
Pöckl, M., Webb, B. W. and Sutcliffe, D. W. (2003). Life history and reproduction capacity of Gammarus fossarum and G. roeseli (Crustacea: Amphipoda) under naturally fluctuating water temperatures: a simulation study. Freshwater Biology 48, 53–66.CrossRefGoogle Scholar
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasited animals: a critical review. International Journal for Parasitology 25, 1371–1383.Google ScholarPubMed
Poulin, R. (2000). Manipulation of host behaviour by parasites: a weakening paradigm? Proceedings of the Royal Society of London 267, 787–792.Google ScholarPubMed
Rumpus, A. E. and Kennedy, C. R. (1974). The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host Gammarus pulex. Parasitology 68, 271–284.Google ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Ward, P. (1986). A comparative field study of the breeding behaviour of a stream and pond population of Gammarus pulex (Amphipoda). Oikos 46, 29–36.CrossRefGoogle Scholar
Wisenden, B. D., Cline, A. and Sparkes, S. T. C. (1999). Survival benefit to antipredator behavior in the amphipod Gammarus minus (crustacea: Amphipoda) in response to injury-released chemical cues from conspecifics and heterospecifics. Ethology 105, 407–414.CrossRefGoogle Scholar
Zohar, S. and Holmes, J. C. (1998). Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study. Behavioral Ecology 9, 206–211.CrossRefGoogle Scholar