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Does the carotenoid-based colouration of Polymorphus minutus facilitate its trophic transmission to definitive hosts?

Published online by Cambridge University Press:  18 July 2013

L. JACQUIN*
Affiliation:
Université Pierre et Marie Curie, Sorbonne Universités, CNRS UMR Ecologie & Evolution, Paris, France INRA, USC Écologie des populations et communautés, Paris, France Redpath Museum and Department of Biology, McGill University, Montréal, Québec, Canada
Q. MORI
Affiliation:
Université Pierre et Marie Curie, Sorbonne Universités, CNRS UMR Ecologie & Evolution, Paris, France INRA, USC Écologie des populations et communautés, Paris, France
V. MÉDOC
Affiliation:
Université Pierre et Marie Curie, Sorbonne Universités, CNRS UMR Ecologie & Evolution, Paris, France INRA, USC Écologie des populations et communautés, Paris, France
*
*Corresponding author: Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke Street West, QC H3A 0C4, Montréal, Québec, Canada. E-mail: [email protected]

Summary

Freshwater gammarids infected with the acanthocephalan parasite Polymorphus minutus show behavioural alterations but also differ from uninfected individuals in their appearance because of the carotenoid-based colouration of the parasite visible through the cuticle. However, it's not clear whether this phenotypic alteration is an adaptation favouring parasite transmission to the definitive host. To test this hypothesis, we investigated the selective preference of mallard towards two prey types: uninfected gammarids on which we applied a dot of inconspicuous brown paint, and uninfected gammarids on which we applied a dot of bright orange paint to mimic the change in appearance due to P. minutus without changes in host behaviour. Mallards showed a significant preference for orange-painted gammarids regardless of how gammarids were distributed (isolated or aggregated). This suggests that parasite's colouration may play a role in enhanced transmission to definitive avian hosts. The role of P. minutus’ colouration in the conspicuousness of gammarids has however to be balanced by the extent to which mallards use visual cues to forage in the field. From the perspective of a multidimensional manipulation, this study suggests that the change in appearance may act synergistically with the changes in behaviour to promote transmission to waterbirds.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alisauskas, R. and Ankney, C. (1992). Ecology and Management of Breeding Waterfowl, 1st Edn. University of Minnesota Press, Minneapolis, MN, USA.Google Scholar
Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behaviour and colour make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.CrossRefGoogle Scholar
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 55, 110115.CrossRefGoogle Scholar
Cézilly, F. and Perrot-Minnot, M.-J. (2005). Studying adaptive changes in the behaviour of infected hosts: a long and winding road. Behavioural Processes 68, 223228.CrossRefGoogle ScholarPubMed
Cézilly, F., Thomas, F., Médoc, V. and Perrot-Minnot, M.-J. (2010). Host manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311317.CrossRefGoogle ScholarPubMed
Chesson, J. (1978). Measuring preference in selective predation. Ecology 59, 211215.CrossRefGoogle Scholar
Chesson, J. (1983). The estimation and analysis of preference and its relationship to foraging models. Ecology 64, 12971304.CrossRefGoogle Scholar
Crompton, D. W. T. (1985). Reproduction. In Biology of the Acanthocephala (ed. Crompton, D. W. T. and Nickol, B. B.), pp. 213271. Cambridge University Press, Cambridge, UK.Google Scholar
Crompton, D. W. T. and Harrison, J. (1965). Observations on Polymorphus minutus (Goeze, 1782) (Acanthocephala) from a wildfowl reserve in Kent. Parasitology 55, 345355.CrossRefGoogle ScholarPubMed
Dessborn, L., Brochet, A., Elmberg, J., Legagneux, P., Gauthier-Clerc, M. and Guillemain, M. (2011). Geographical and temporal patterns in the diet of pintail Anas acuta, wigeon Anas penelope, mallard Anas platyrhynchos and teal Anas crecca in the Western Palearctic. European Journal of Wildlife Research 57, 11191129.CrossRefGoogle Scholar
Dezfuli, B. S. and Giari, L. (1999). Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host–parasite interface. Follia Parasitologica 46, 117122.Google Scholar
Franceschi, N., Rigaud, T., Moret, Y., Hervant, F. and Bollache, L. (2007). Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex. Parasitology 134, 18391847.CrossRefGoogle ScholarPubMed
Gaillard, M., Juillet, C., Cézilly, F. and Perrot-Minnot, M.-J. (2004). Carotenoids of two freshwater amphipod species (Gammarus pulex and G. roeseli) and their common acanthocephalan parasite Polymorphus minutus. Comparative Biochemistry and Physiology B 139, 129136.CrossRefGoogle Scholar
Guillemain, M. and Martin, G. (2002). Feeding methods, visual fields and vigilance in dabbling ducks (Anatidae). Functional Ecology 16, 522529.CrossRefGoogle Scholar
Guillemain, M., Fritz, H. and Blais, S. (2000). Foraging methods can affect patch choice: an experimental study in Mallard (Anas platyrhynchos). Behavioural Processes 50, 123129.CrossRefGoogle ScholarPubMed
Hart, N. (2001). The visual ecology of avian photoreceptors. Progress in Retinal and Eye Research 20, 675703.CrossRefGoogle ScholarPubMed
Hinsbo, O. (1972). Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris. Nature 238, 333.CrossRefGoogle Scholar
Holmes, J. C. and Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. and Wright, C. A.), pp. 123149. Academic Press, London, UK.Google Scholar
Hynes, H. (1954). The ecology of Gammarus duebeni Lilljeborg and its occurence in fresh water in western Britain. Journal of Animal Ecology 23, 3884.CrossRefGoogle Scholar
Itämies, J., Valtonen, E. and Fagerholm, H. P. (1980). Polymorphus minutus (Acanthocephala) infestation in eiders and its role as a possible cause of death. Annales Zoologici Fennici 17, 285289.Google Scholar
Kaldonski, N., Perrot-Minnot, M.-J., Dodet, R., Martinaud, G. and Cézilly, F. (2009). Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proceedings of the Royal Society of London Series B Biological Sciences 276, 169176.Google ScholarPubMed
Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Kolluru, G. R., Green, Z. S., Vredevoe, L. K., Kuzma, M. R., Ramadan, S. N. and Zosky, M. R. (2011). Parasite infection and sand coarseness increase sand crab (Emerita analoga) burrowing time. Behavioural Processes 88, 184191.CrossRefGoogle Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111115.CrossRefGoogle ScholarPubMed
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts’ behaviour by a parasite: field evidence for adaptive manipulation. Ecology 88, 28392847.CrossRefGoogle ScholarPubMed
Manly, B., Miller, P. and Cook, L. (1972). Analysis of a selective predation experiment. American Naturalist 106, 719736.CrossRefGoogle Scholar
Médoc, V. and Beisel, J.-N. (2009). Field evidence for non-host predator avoidance in a manipulated amphipod. Naturwissenschaften 96, 513523.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, 13511358.CrossRefGoogle Scholar
Médoc, V., Rigaud, T., Bollache, L. and Beisel, J.-N. (2009). A manipulative parasite increasing an antipredatory response decreases its vulnerability to a nonhost predator. Animal Behaviour 77, 12351241.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behaviour of Animals. Oxford University Press, New York, USA.CrossRefGoogle 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, 10431050.CrossRefGoogle ScholarPubMed
Nickol, B. (1985). Epizootiology. In Biology of the Acanthocephala (ed. Crompton, D. W. T. and Nickol, B. B.), pp. 307346. Cambridge University Press, Cambridge, UK.Google Scholar
Perrot-Minnot, M.-J., Gaillard, M., Dodet, R. and Cézilly, F. (2011). Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate host. International Journal for Parasitology 41, 173181.CrossRefGoogle ScholarPubMed
Thomas, F., Poulin, R. and Brodeur, J. (2010). Host manipulation by parasites: a multidimensional phenomenom. Oikos 119, 12171223.CrossRefGoogle Scholar
Thünken, T., Baldauf, S. A., Bersau, N., Bakker, T. C. M., Kullmann, H. and Frommen, J. G. (2010). Impact of olfactory non-host predator cues on aggregation behaviour and activity in Polymorphus minutus infected Gammarus pulex. Hydrobiologia 654, 137145.CrossRefGoogle Scholar
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. Springer Science, New York, USA.CrossRefGoogle Scholar