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A co-invasive microsporidian parasite that reduces the predatory behaviour of its host Dikerogammarus villosus (Crustacea, Amphipoda)

Published online by Cambridge University Press:  18 October 2013

K. BACELA-SPYCHALSKA*
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 6282, Équipe Écologie Évolutive, Université de Bourgogne, 21000 Dijon, France Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Poland
T. RIGAUD
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 6282, Équipe Écologie Évolutive, Université de Bourgogne, 21000 Dijon, France
R. A. WATTIER
Affiliation:
Laboratoire Biogéosciences, UMR CNRS 6282, Équipe Écologie Évolutive, Université de Bourgogne, 21000 Dijon, France
*
* Corresponding author: Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Banacha 12/16, 90-237 Lodz, Poland. E-mail: karolina@biol.uni.lodz.pl

Summary

Parasites are known to affect the predatory behaviour or diet of their hosts. In relation to biological invasions, parasites may significantly influence the invasiveness of the host population and/or mediate the relationships between the invader and the invaded community. Dikerogammarus villosus, a recently introduced species, has had a major impact in European rivers. Notably, its high position in trophic web and high predatory behaviour, have both facilitated its invasive success, and affected other macroinvertebrate taxa in colonized habitats. The intracellular parasite Cucumispora dikerogammari, specific to D. villosus, has successfully dispersed together with this amphipod. Data presented here have shown that D. villosus infected by this parasite have a reduced predatory behaviour compared with healthy individuals, and are much more active suggesting that the co-invasive parasite may diminish the predatory pressure of D. villosus on newly colonized communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Bacela-Spychalska, K., Wattier, R. A., Genton, C. and Rigaud, T. (2012). Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna. Biological Invasions 14, 18311842.CrossRefGoogle Scholar
Bernot, R. J. and Lamberti, G. A. (2008). Indirect effects of a parasite on a benthic community: an experiment with trematodes, snails and periphyton. Freshwater Biology 53, 322329.CrossRefGoogle Scholar
Boets, P., Lock, K., Marjolein Messiaen, M. and Goethals, P. L. M. (2010). Combining data-driven methods and lab studies to analyse the ecology of Dikerogammarus villosus . Ecological Informatics 5, 133139.CrossRefGoogle Scholar
Bollache, L., Gambade, G. and Cezilly, F. (2000). The influence of micro-habitat segregation on size assortative pairing in Gammarus pulex (L.) (Crustacea, Amphipoda). Archive für Hydrobiologie 147, 547558.CrossRefGoogle Scholar
Bollache, L., Devin, S., Wattier, R. A., Chovet, M., Beisel, J. N., Moreteau, J. C. and Rigaud, T. (2004). Rapid range extension of the pontocaspian amphipod D. villosus (Crustacea, Amphipoda) in France: potential consequences. Archiv für Hydrobiologie 160, 5766.CrossRefGoogle Scholar
Bollache, L., Dick, J. T. A., Farnsworth, K. D. and Montgomery, W. I. (2008). Comparison of the functional responses of invasive and native amphipods. Biology Letters 4, 166169.CrossRefGoogle ScholarPubMed
Bulnheim, H. P. (1975). Microsporidian infections of amphipods with special reference to host–parasite relationships: a review. Marine Fisheries Review 37, 3945.Google Scholar
Crane, A. L., Fritts, A. K., Mathis, A., Lisek, J. C. and Barnhart, M. C. (2011). Do gill parasites influence the foraging and antipredator behaviour of rainbow darters, Ethestoma caeruleum . Animal Behaviour 82, 817823.CrossRefGoogle Scholar
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, Series B 267, 977983.CrossRefGoogle ScholarPubMed
Dick, J. T. A., Armstrong, M., Clarke, H. C., Farnsworth, K. D., Hatcher, M. J., Ennis, M., Kelly, A. and Dunn, A. M. (2010). Parasitism may enhance rather than reduce the predatory impact of an invader. Biology Letters 6, 636638.CrossRefGoogle ScholarPubMed
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161184.CrossRefGoogle ScholarPubMed
Dunn, A. M. and Perkins, S. E. (2012). Invasions and infections. Functional Ecology 26, 12341237.CrossRefGoogle Scholar
Fielding, N. J., MacNeil, C., Dick, J. T. A., Elwood, R. W., Riddell, G. E. and Dunn, A. M. (2003). Effects of the acanthocephalan parasite Echinorhynchus truttae on the feeding ecology of Gammarus pulex (Crustacea: Amphipoda). Journal of Zoology 261, 321325.CrossRefGoogle Scholar
Fielding, N. J., MacNeil, C., Robinson, N., Dick, J. T. A., Elwood, R. W., Terry, R. S., Ruiz, Z. and Dunn, A. M. (2005). Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus . Parasitology 131, 331336.CrossRefGoogle ScholarPubMed
Goddard, J. H. R., Torchin, M. E., Kuris, A. M. and Lafferty, K. D. (2005). Host specificity of Sacculina carcini, a potential biological control agent of introduced European green crab Carcinus maenas in California. Biological Invasions 7, 895912.CrossRefGoogle Scholar
Grabowski, M., Jazdzewski, K. and Konopacka, A. (2007). Alien Crustacea in Polish waters – Amphipoda. Aquatic Invasions 2, 2538.CrossRefGoogle Scholar
Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters 9, 12531271.CrossRefGoogle ScholarPubMed
Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2008). A keystone effect for parasites in intraguild predation? Biology Letters 4, 534537.CrossRefGoogle ScholarPubMed
Kooi, B. W., van Voorn, G. A. K. and Das, K. P. (2011). Stabilization and complex dynamics in a predatory–prey model with predator suffering from an infectious disease. Ecological Complexity 8, 113122.CrossRefGoogle Scholar
Krisp, H. and Maier, G. (2005). Consumption of macroinvertebrates by invasive and native gammarids: a comparison. Journal of Limnology 64, 5559.CrossRefGoogle Scholar
Kyriazakis, I., Tolkamp, B. J. and Hutchings, M. R. (1998). Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour 56, 265274.CrossRefGoogle ScholarPubMed
MacLeod, C. J., Paterson, A. M., Tompkins, D. M. and Duncan, R. P. (2010). Parasites lost – do invaders miss the boat or drown on arrival? Ecology Letters 13, 516527.CrossRefGoogle ScholarPubMed
MacNeil, C. and Dick, J. T. A. (2011). Parasite-mediated intraguild predation as one of the drivers of coexistence and exclusion among invasive and native amphipods (Crustacea). Hydrobiologia 665, 247256.CrossRefGoogle Scholar
MacNeil, C., Fielding, N. J., Dick, J. T. A., Briffa, M., Prenter, J., Hatcher, M. J. and Dunn, A. M. (2003). An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea). Freshwater Biology 48, 20852093.CrossRefGoogle Scholar
MacNeil, C., Platvoet, D., Dick, J. T. A., Fielding, N., Constable, A., Hall, N., Aldridge, D., Renals, T. and Diamond, M. (2010). The Ponto-Caspian “killer shrimp”, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles. Aquatic Invasions 5, 441444.CrossRefGoogle Scholar
Médoc, V., Piscart, C., Maazouzi, C., Simon, L. and Beisel, J. N. (2011). Parasite-induced changes in the diet of a freshwater amphipod: field and laboratory evidence. Parasitology 138, 537546.CrossRefGoogle ScholarPubMed
Naug, D. and Gibbs, A. (2009). Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae . Apidologie 40, 595599.CrossRefGoogle Scholar
Ovcharenko, M., Bacela, K., Wilkinson, T., Ironside, J., Rigaud, T. and Wattier, R. A. (2010). Cucumispora dikerogammari n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers. Parasitology 137, 191204.CrossRefGoogle ScholarPubMed
Piscart, C., Bergerot, B., Laffaille, P. and Marmonier, P. (2010). Are amphipod invaders a threat to regional biodiversity? Biological Invasions 12, 853863.CrossRefGoogle Scholar
Platvoet, D., Dick, J. T. A., MacNeil, C., Van Riel, M. and Van der Velde, G. (2009). Invader–invader interactions in relation to environmental heterogeneity leads to zonation of two invasive amphipods, Dikerogammarus villosus (Sowinsky) and Gammarus tigrinus (Sexton). Biological Invasions 11, 20852093.CrossRefGoogle Scholar
Pöckl, M. (2009). Success of the invasive Ponto-Caspian amphipod Dikerogammarus villosus by life history traits and reproductive capacity. Biological Invasions 11, 20212041.CrossRefGoogle Scholar
Poulin, R. (1999). The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology 29, 903914.CrossRefGoogle ScholarPubMed
Prenter, J., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385390.CrossRefGoogle ScholarPubMed
Preston, D. and Johnson, P. (2012). Ecological consequences of parasitism. Nature Education Knowledge 3, 47.Google Scholar
Price, P. W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Terry, R. S., MacNeil, C., Dick, J. T. A., Simth, J. E. and Dunn, A. M. (2003). Resolution of a taxonomic conundrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895). Journal of Eukaryotic Microbiology 50, 266273.CrossRefGoogle ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.CrossRefGoogle ScholarPubMed
Tompkins, D. M., White, A. R. and Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters 6, 189196.CrossRefGoogle Scholar
Torchin, M. E. and Mitchell, C. E. (2004). Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and Environment 2, 183190.CrossRefGoogle Scholar
Van der Velde, G., Leuven, R. S. E. W., Platvoet, D., Bacela, K., Huijbregts, M. A. J., Hendriks, H. W. M. and Kruijt, D. (2009). Environmental and morphological factors influencing predatory behaviour by invasive non-indigenous gammaridean species. Biological Invasions 11, 20432054.CrossRefGoogle Scholar
Van Riel, M. C., Van der Velde, G., Rajagopal, S., Marguiller, S., Dehairs, F. and Bij de Vaate, A. (2006). Trophic relationships in the Rhine food web during invasion and after establishment of the Ponto-Caspian invader Dikerogammarus villosus . Hydrobiologia 565, 3958.CrossRefGoogle Scholar
Wattier, R. A., Haine, E. R., Beguet, J., Martin, G., Bollache, L., Musko, I. B., Platvoet, D. and Rigaud, T. (2007). No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos 116, 19411953.CrossRefGoogle Scholar