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Manipulative parasites may not alter intermediate host distribution but still enhance their transmission: field evidence for increased vulnerability to definitive hosts and non-host predator avoidance

Published online by Cambridge University Press:  15 October 2012

C. LAGRUE*
Affiliation:
University of Otago, Department of Zoology, Dunedin, New Zealand Université de Bourgogne, UMR CNRS 6282 Biogéosciences, Dijon, France
A. GÜVENATAM
Affiliation:
Université de Bourgogne, UMR CNRS 6282 Biogéosciences, Dijon, France
L. BOLLACHE
Affiliation:
Université de Bourgogne, UMR CNRS 6282 Biogéosciences, Dijon, France
*
*Corresponding author: Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin 9054, New Zealand. Tel: +64 3479 7986. Fax: +64 3479 7584. E-mail: clement.lagrue@gmail.com

Summary

Behavioural alterations induced by parasites in their intermediate hosts can spatially structure host populations, possibly resulting in enhanced trophic transmission to definitive hosts. However, such alterations may also increase intermediate host vulnerability to non-host predators. Parasite-induced behavioural alterations may thus vary between parasite species and depend on each parasite definitive host species. We studied the influence of infection with 2 acanthocephalan parasites (Echinorhynchus truttae and Polymorphus minutus) on the distribution of the amphipod Gammarus pulex in the field. Predator presence or absence and predator species, whether suitable definitive host or dead-end predator, had no effect on the micro-distribution of infected or uninfected G. pulex amphipods. Although neither parasite species seem to influence intermediate host distribution, E. truttae infected G. pulex were still significantly more vulnerable to predation by fish (Cottus gobio), the parasite's definitive hosts. In contrast, G. pulex infected with P. minutus, a bird acanthocephalan, did not suffer from increased predation by C. gobio, a predator unsuitable as host for P. minutus. These results suggest that effects of behavioural changes associated with parasite infections might not be detectable until intermediate hosts actually come in contact with predators. However, parasite-induced changes in host spatial distribution may still be adaptive if they drive hosts into areas of high transmission probabilities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

Åbjörnsson, K., Dahl, J., Nyström, P. and Brönmark, C. (2000). Influence of predator and sietary chemical cues on the behaviour and shredding efficiency of Gammarus pulex. Aquatic Ecology 34, 379387.CrossRefGoogle Scholar
Awachie, J. B. E. (1966). The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology 40, 1132.CrossRefGoogle Scholar
Awachie, J. B. E. (1973). The status of the infection of the bullhead, Cottus gobio L., by Echinorhynchus truttae Schrank, 1788 (Acanthocephala) in Mon Terrig. Acta Parasitologica Polonica 21, 481484.Google Scholar
Baldauf, S. A., Thünken, T., Frommen, J. G., Bakker, T. C. M., Heuprl, 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, 6165.CrossRefGoogle ScholarPubMed
Benesh, D. P., Hasu, T., Seppälä, O. and Valtonen, E. T. (2009). Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted? Parasitology 136, 219230.CrossRefGoogle ScholarPubMed
Benesh, D. P., Kitchen, J., Pulkkinen, K., Hakala, I. and Valtonen, E. T. (2008 a). The effects of Echinorhynchus borealis (Acanthocephala) infection on the anti-predator behaviour of a benthic amphipod. Journal of Parasitology 94, 542545.CrossRefGoogle Scholar
Benesh, D. P., Valtonen, E. T. and Seppälä, O. (2008 b). Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan. Parasitology 135, 617626.CrossRefGoogle ScholarPubMed
Bollache, L. and Cézilly, F. (2004). State-dependent pairing behaviour in male Gammarus pulex (L.) (Crustacea, Amphipoda): effects of time left to moult and prior pairing status. Behavioural Processes 66, 131137.CrossRefGoogle ScholarPubMed
Cézilly, F., Gregoire, A. and Bertin, A. (2000). Conflict between co-occurring manipulative parasites? An experimental study of the joint influences of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625630.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. and Perrot-Minnot, M.-J. (2010). Interpreting multidimensionality in parasite-induced phenotypic alterations: panselectionism versus parsimony. Oikos 119, 12241229.CrossRefGoogle Scholar
Crompton, D. W. T. and Nickol, B. B. (1985). Biology of the Acanthocephala. Cambridge University Press, Cambridge, UK.Google Scholar
Dahl, J., Anders Nilsson, P. and Pettersson, L. B. (1998). Against the flow: chemical detection of downstream predators in running waters. Proceedings of the Royal Society of London, B 265, 13391344.CrossRefGoogle Scholar
Dianne, L., Perrot-Minnot, M. J., Bauer, A., Gaillard, M., Leger, E. and Rigaud, T. (2011). Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 26922698.CrossRefGoogle ScholarPubMed
Gaudin, P., Martin, E. and Caillere, L. (1981). Le tubage gastrique chez les poissons: mise an point d'un équipement et test chez le chabot Cottus gobio (L.). Bulletin Français de la Pêche et de la Pisciculture 282, 815.CrossRefGoogle Scholar
Haddaway, N. R., Wilcox, R. H., Heptonstall, R. E. A., Griffiths, H. M., Mortimer, R. J. G., Christmas, M. and Dunn, A. M. (2012). Predators functional response and prey choices identify predation differences between native/invasive and parasitized/unparasitised crayfish. Plos One 7, e32229. doi:10.1371/journal.pone.0032229.CrossRefGoogle ScholarPubMed
Holmes, J. C. and Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. Zoological Journal of the Linnean Society 51, 123149.Google Scholar
Holmes, J. C. and Bethel, W. M. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110115.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, 13111317.CrossRefGoogle Scholar
Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. and Cézilly, F. (2008). Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host predators. Parasitology 135, 627632.CrossRefGoogle Scholar
Klemetsen, A., Amundsen, P.-A., Dempson, J. B., Jonsson, B., Jonsson, N., O'Connell, M. F. and Mortensen, E. (2003). Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12, 159.CrossRefGoogle Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111115.CrossRefGoogle ScholarPubMed
Lagrue, C. and Bollache, L. (2006). Effects of temperature on persistence times of native and invasive gammarid species in the stomachs of bullhead, Cottus gobio. Journal of Fish Biology 68, 318322.CrossRefGoogle Scholar
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
Levri, E. P. (1998). Perceived predation risk, parasitism, and the foraging behaviour of a freshwater snail (Potamopyrgus antipodarum). Canadian Journal of Zoology 76, 18781884.CrossRefGoogle Scholar
Lima, S. L. (1998). Nonlethal effects in the ecology of predator-prey interactions – What are the ecological effects of anti-predator decision-making? Bioscience 48, 2534.CrossRefGoogle Scholar
MacNeil, C., Elwood, R. W. and Dick, J. T. A. (1999). Brown trout predation on native and introduced amphipods in N. Ireland, a behavioural study. Ecography 22, 686697.Google Scholar
MacNeil, C., Elwood, R. W. and Dick, J. T. A. (2001). Persistence times of four amphipod species in the stomachs of brown trout. Journal of Fish Biology 59, 14011404.Google Scholar
MacNeil, C., Fielding, N. J., Hume, K. D., Dick, J. T. A., Elwood, R. W., Hatcher, M. J. and Dunn, A. M. (2003). Parasite altered micro-distribution of Gammarus pulex (Crustacea: Amphipoda). International Journal for Parasitology 33, 5764.CrossRefGoogle Scholar
Marriott, D. R., Collins, M. L., Paris, R. M., Gudgin, D. R., Barnard, C. J., McGregor, F. S., Gilbert, F. S., Hartley, J. C. and Behnke, J. M. (1989). Behavioural modifications and increased predation risk of Gammarus pulex infected with Polymorphus minutus. Journal of Biological Education 23, 135141.CrossRefGoogle Scholar
Mathis, A. and Hoback, W. W. (1997). The influence of chemical stimuli from predators on precopulatory pairing by the amphipod, Gammarus pseudolimnaeus. Ethology 103, 3340.CrossRefGoogle Scholar
Médoc, V. and Beisel, J.-N. (2008). An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators. Parasitology 135, 977984.CrossRefGoogle ScholarPubMed
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. and Beisel, J.-N. (2011). When trophically-transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos 120, 14521458.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 antipredator response decreases its vulnerability to a nonhost predator. Animal Behaviour 77, 12351241.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the behaviour of animals. Oxford Series in Ecology and Evolution. Oxford University Press, NY, USA.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, 10431050.CrossRefGoogle ScholarPubMed
Okada, C. E. and Koura, E. A. (2000). The ecology of endohelminth parasites of fish in the Driffield trout stream, Yorkshire, England. Journal of Aquatic Sciences 15, 4145.Google Scholar
Parker, G. A., Chubb, J. C., Michaud, M. and Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionnary Biology 16, 4754.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, 645651.CrossRefGoogle Scholar
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology 25, 13711383.CrossRefGoogle ScholarPubMed
Rousset, F., Thomas, F., de Meeüs, T. and Renaud, F. (1996). Inference of parasite-induced mortality from distributions of parasite loads. Ecology 77, 22032211.CrossRefGoogle Scholar
Seppälä, O. and Jokela, J. (2008). Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663666.CrossRefGoogle ScholarPubMed
Seppälä, O., Valtonen, P. and Benesh, D. P. (2008). Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society of London, B 275, 16111615.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., Rousset, F., Cézilly, F. and de Meeüs, T. (1995). Differential mortality of two closely related host species induced by one parasite. Proceedings of the Zoological Society of London 260, 349352.CrossRefGoogle Scholar
Thomas, F., Adamo, S. A. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.CrossRefGoogle Scholar
Thomas, F., Poulin, R. and Brodeur, J. (2010). Host manipulation by parasites: a multidimensional phenomenon. Oikos 119, 12171223.CrossRefGoogle Scholar
Wellnitz, T., Giari, L., Maynard, B. and Dezfuli, B. S. (2003). A parasite spatially structures its host population. Oikos 100, 263268.CrossRefGoogle Scholar
Wudkevich, K., Wisenden, B. D., Chivers, D. P. and Smith, R. J. F. (1997). Reactions of Gammarus lacustris to chemical stimuli from natural predators and injured conspecifics. Journal of Chemical Ecology 23, 11631173.CrossRefGoogle Scholar
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Manipulative parasites may not alter intermediate host distribution but still enhance their transmission: field evidence for increased vulnerability to definitive hosts and non-host predator avoidance
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