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

Parasitology

Volumn 141, Issue 2, 2014, Pages 254-258

  Bacela Spychalska, K ^a,b   Rigaud, T ^a   Wattier, R A ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITY OF LODZ   (Poland)

Author keywords

activity; biological invasion; microsporidia; parasite induced behavioural changes; predation

Indexed keywords

AMPHIPODA; ARTICLE; BEHAVIOR CHANGE; DECAPODA (CRUSTACEA); DIKEROGAMMARUS VILLOSUS; HABITAT; HOST PARASITE INTERACTION; MACROINVERTEBRATE; MICROSPORIDIA; NONHUMAN; POLAND; PREDATION; SPECIES INVASION; ANIMAL; FEMALE; INTRODUCED SPECIES; MALE; PARASITOLOGY; PHYSIOLOGY; RIVER;

AMPHIPODA; CRUSTACEA; DIKEROGAMMARUS VILLOSUS; MICROSPORIDIA;

AMPHIPODA; ANIMALS; FEMALE; HOST-PARASITE INTERACTIONS; INTRODUCED SPECIES; MALE; MICROSPORIDIA; POLAND; PREDATORY BEHAVIOR; RIVERS;

EID: 84893923060     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182013001510     Document Type: Article

References (42)

1. 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, 1831-1842.
2. 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, 322-329.
3. 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, 133-139.
4. 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 fr Hydrobiologie 147, 547-558.
5. 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 fr Hydrobiologie 160, 57-66.
6. 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, 166-169.
7. Bulnheim, H. P. (1975). Microsporidian infections of amphipods with special reference to host-parasite relationships: a review. Marine Fisheries Review 37, 39-45.
8. 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, 817-823.
9. 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, 977-983.
10. 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, 636-638.
11. Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161-184.
12. Dunn, A. M. and Perkins, S. E. (2012). Invasions and infections. Functional Ecology 26, 1234-1237.
13. 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, 321-325.
14. 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, 331-336.
15. 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, 895-912.
16. Grabowski, M., Jazdzewski, K. and Konopacka, A. (2007). Alien Crustacea in Polish waters - Amphipoda. Aquatic Invasions 2, 25-38.
17. Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters 9, 1253-1271.
18. Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2008). A keystone effect for parasites in intraguild predation? Biology Letters 4, 534-537.
19. 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, 113-122.
20. Krisp, H. and Maier, G. (2005). Consumption of macroinvertebrates by invasive and native gammarids: a comparison. Journal of Limnology 64, 55-59.
21. 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, 265-274.
22. 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, 516-527.
23. 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, 247-256.
24. 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, 2085-2093.
25. 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, 441-444.
26. Mdoc, 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, 537-546.
27. Naug, D. and Gibbs, A. (2009). Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40, 595-599.
28. 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, 191-204.
29. Piscart, C., Bergerot, B., Laffaille, P. and Marmonier, P. (2010). Are amphipod invaders a threat to regional biodiversity? Biological Invasions 12, 853-863.
30. 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, 2085-2093.
31. Pckl, M. (2009). Success of the invasive Ponto-Caspian amphipod Dikerogammarus villosus by life history traits and reproductive capacity. Biological Invasions 11, 2021-2041.
32. Poulin, R. (1999). The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology 29, 903-914.
33. 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, 385-390.
34. Preston, D. and Johnson, P. (2012). Ecological consequences of parasitism. Nature Education Knowledge 3, 47.
35. Price, P.W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.
36. 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, 266-273.
37. Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185-199.
38. 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, 189-196.
39. Torchin, M. E. and Mitchell, C. E. (2004). Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and Environment 2, 183-190.
40. 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, 2043-2054.
41. 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, 39-58.
42. 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, 1941-1953.