Intra-specific host sharing in the manipulative parasite Acanthocephalus dirus: does conflict occur over host modification? | Parasitology | Cambridge Core (original) (raw)

Abstract

The acanthocephalan parasite Acanthocephalus dirus induces a colour change in the intermediate host, the aquatic isopod Caecidotea intermedius, which increases transmission to definitive hosts (creek chub, sunfish). We examined the potential for conflict to occur between infective (cystacanth) and non-infective (acanthor, acanthella) stages of A. dirus over the level of colour modification that should be induced when these stages share a host. Using a field survey, we showed that host sharing by infective and non-infective stages was relatively common and that infective and non-infective stages differed in their effects on colour modification. Non-infective stages induced a colour change over 40% of the body, whereas infective stages induced a colour change over 80%. Thus, conflict could occur between stages over the level of modification that should be induced. We then showed that mixed-stage infections induced a colour change in the host that was consistent with the level of modification induced by the infective stage. We discuss the potential significance of these results to patterns of host modification and their effects on stage-related survival in nature.

References

AMIN, O. M. (1984).Variability and redescription of Acanthocephalus dirus (Acanthocephala: Echinorhynchidae) from freshwater fishes in North America.Proceedings of the Helminthological Society of Washington 51,225–237.Google Scholar

BAKKER, T. C. M.,MAZZI, D. &ZALA, S. (1997).Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation.Ecology 78,1098–1104.CrossRefGoogle Scholar

BETHEL, W. M. &HOLMES, J. C. (1974).Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host.Journal of Parasitology 60,272–274.CrossRefGoogle Scholar

BETHEL, W. M. &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.CrossRefGoogle Scholar

BRATTEY, J. (1983).The effects of larval Acanthocephalus lucii on the pigmentation, reproduction, and susceptibility to predation of the isopod Asellus aquaticus.Journal of Parasitology 69,1172–1173.CrossRefGoogle Scholar

BROWN, S. P. (1999).Cooperation and conflict in host-manipulating parasites.Proceedings of the Royal Society, B 266,1899–1904.CrossRefGoogle Scholar

BUSH, A. O.,LAFFERTY, K. D.,LOTZ, J. M. &SHOSTAK, A. W. (1997).Parasitology meets ecology on its own terms: Margolis et al. revisited.Journal of Parasitology 83,575–583.CrossRefGoogle Scholar

CAMP, J. W. &HUIZINGA, H. W. (1979).Altered color, behavior and predation susceptibility of the isopod Asellus intermedius infected with Acanthocephalus dirus.Journal of Parasitology 65,667–669.CrossRefGoogle Scholar

CAMP, J. W. &HUIZINGA, H. W. (1980).Seasonal population interactions of Acanthocephalus dirus (Van Cleave 1931) in the creek chub, Semotilus atromaculatus, and the isopod, Asellus intermedius.Journal of Parasitology 66,299–304.CrossRefGoogle Scholar

CEZILLY, F.,GREGOIRE, A. &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 Scholar

DEZFULI, B. S.,GIARI, L. &POULIN, R. (2001).Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths.Parasitology 122,483–489.CrossRefGoogle Scholar

HARGEBY, A.,JOHANSSON, J. &AHNESJÖ, J. (2004).Habitat-specific pigmentation in a freshwater isopod: adaptive evolution over a small spatiotemporal scale.Evolution 58,81–94.CrossRefGoogle Scholar

HECHTEL, L. J.,JOHNSON, C. L. &JULIANO, S. A. (1993).Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus.Ecology 74,710–713.CrossRefGoogle Scholar

HOLMES, J. C. (1962).Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). II. Effects on growth.Journal of Parasitology 48,87–96.Google Scholar

JOHNSON, C. L. (1994).Modification of antipredator behavior in a parasitized isopod: energy demand or host manipulation? M.S. thesis,Illinois State University.

LAFFERTY, K. D. (1999).The evolution of trophic transmission.Parasitology Today 15,111–115.CrossRefGoogle Scholar

LAFFERTY, K. D.,THOMAS, F. &POULIN, R. (2000).Evolution of host phenotype manipulation by parasites and its consequences. In_Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality_ (ed. Poulin, R., Morand, S. & Skorping, A.), pp.117–127.Elsevier Science Publishers,New York.

MOORE, J. (2002).Parasites and the Behavior of Animals.Oxford University Press,Oxford.

OETINGER, D. F. &NICKOL, B. B. (1981).Effects of acanthocephalans on pigmentation of freshwater isopods.Journal of Parasitology 67,672–684.CrossRefGoogle Scholar

OETINGER, D. F. &NICKOL, B. B. (1982 a).Developmental relationships between acanthocephalans and altered pigmentation in freshwater isopods.Journal of Parasitology 68,463–469.Google Scholar

OETINGER, D. F. &NICKOL, B. B. (1982 b).Spectrophotometric characterization of integumental pigments from uninfected and _Acanthocephalus dirus_-infected Asellus intermedius.Journal of Parasitology 68,270–275.Google Scholar

POULIN, R. (2002).Parasite manipulation of host behaviour. In_The Behavioural Ecology of Parasites_ ( ed. Lewis, E. E., Campbell, J. F. & Sukhdeo, M. V. K.), pp.243–257.CABI Publishing,New York.CrossRef

POULIN, R. &THOMAS, F. (1999).Phenotypic variability induced by parasites: extent and evolutionary implications.Parasitology Today 15,28–32.CrossRefGoogle Scholar

POULIN, R.,NICHOL, K. &LATHAM, D. M. (2003).Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33,425–433.Google Scholar

SEIDENBERG, A. J. (1973).Ecology of the acanthocephalan, Acanthocephalus dirus (Van Cleave, 1931), in its intermediate host, Asellus intermedius Forbes (Crustacea: Isopoda).Journal of Parasitology 59,957–962.CrossRefGoogle Scholar

STEINAUER, M. L. &NICKOL, B. B. (2003).Effect of cystacanth body size on adult success.Journal of Parasitology 89,251–254.CrossRefGoogle Scholar

THOMAS, F.,RENAUD, F. &POULIN, R. (1998).Exploitation of manipulators: ‘hitch-hiking’ as a parasite transmission strategy.Animal Behaviour 56,199–206.CrossRefGoogle Scholar

WEIL, K. A. (2002).Effects of an acanthocephalan parasite (Acanthocephalus dirus) on reproduction and sexual conflict dynamics in a freshwater isopod (Caecidotea intermedius). M.S. thesis,DePaul University.

ZAR, J. H. (1999).Biostatistical Analysis, 4th Edn.Prentice Hall,New Jersey.