Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators

Parasitology

Volumn 135, Issue 5, 2008, Pages 627-632

  Kaldonski, N ^a   Perrot Minnot, M J ^a   Motreuil, S ^a   Cezilly F ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Host manipulation; Polymorphus minutus; Pomphorhynchus laevis; Pomphorhynchus tereticollis; Trophic transmission

Indexed keywords

ACANTHOCEPHALUS; AMPHIPODA; ARTICLE; CRAYFISH; GAMMARUS; GAMMARUS PULEX; HELMINTHIASIS; HOST PARASITE INTERACTION; MICROCOSM; NONHUMAN; POLYMORPHUS MINUTUS; POMPHORHYNCHUS LAEVIS; POMPHORHYNCHUS TERETICOLLIS; PREDATOR; PRIORITY JOURNAL; ANIMAL; CLASSIFICATION; FOOD CHAIN; PARASITOLOGY; PHYSIOLOGY; PREDATION; SPECIES DIFFERENCE;

ACANTHOCEPHALA (WORMS); AMPHIPODA; ASTACOIDEA; CRUSTACEA; GAMMARIDAE; GAMMARUS PULEX; INVERTEBRATA; NEPA CINEREA; NEPIDAE; ORCONECTES LIMOSUS; POLYMORPHUS MINUTUS; POMPHORHYNCHUS LAEVIS; POMPHORHYNCHUS TERETICOLLIS;

ACANTHOCEPHALA; AMPHIPODA; ANIMALS; ASTACOIDEA; FOOD CHAIN; HOST-PARASITE INTERACTIONS; PREDATORY BEHAVIOR; SPECIES SPECIFICITY;

EID: 42449117953     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S003118200800423X     Document Type: Article

References (48)

1. Åbjörnsson, K., Dahl, J., Nyström, P. and Brönmark, C. (2000). Influence of predator and dietary chemical cues on the behaviour and shredding efficiency of Gammarus pulex. Aquatic Ecology 34, 379-387.
2. Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098-1104.
3. Baldauf, S. A., Thünken, T., Frommen, J. G., Bakker, T. C. M., Heupzl, O. and Kullmann, H. (2007). Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odour. International Journal for Parasitology 37, 61-65.
4. Bethel, W. M. and 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.
5. Cézilly, F., Grégoire, A. and 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.
6. 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, 223-228.
7. Chesson, J. (1978). Measuring preference in selective predation. Ecology 59, 211-215.
8. Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: Why add intermediate hosts? American Naturalist 162, 172-181.
9. Corona, A., Soto, L. A. and Sanchez, A. J. (2000). Epibenthic amphipod abundance and predation efficiency of the pink shrimp Farfantepenaeus duorarum (Burkenroad, 1939) in habitats with different physical complexity in a tropical estuarine system. Journal of Experimental Marine Biology and Ecology 253, 33-48.
10. Crawford, L., Yeomans, W. E. and Adams, C. E. (2006). The impact of introduced signal crayfish Pacifastacus leniusculus on stream invertebrate communities. Aquatic Conservation: Marine and Freshwater Ecosystems 16, 611-621.
11. Dawkins, R. (1982). The Extended Phenotype, Oxford University Press, Oxford.
12. Dezfuli, B. S., Maynard, B. J. and Wellnitz, T. A. (2003). Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitologica 50, 129-134.
13. Dick, J. T. A. and Platvoet, D. (1996). Intraguild predation and species exclusions in amphipods: The interaction of behaviour, physiology and environment. Freshwater Biology 36, 375-383.
14. Duffy, M. A., Hall, S. R., Tessier, A. J. and Huebner, M. (2005). Selective predators and their parasitized prey: Are epidemics in zooplankton under top-down control? Limnology and Oceanography 50, 412-420.
15. Elliott, J. M. (2005). Day-night changes in the spatial distribution and habitat preferences of freshwater shrimps, Gammarus pulex, in a stony stream. Freshwater Biology 50, 552-566.
16. Fenton, A. and Rands, S. A. (2006). The impact of parasite manipulation and predator foraging behavior on predator-prey communities. Ecology 87, 2832-2841.
17. Fullick, T. G. and Greenwood, J. J. D. (1979). Frequency-dependent food selection in relation to 2 models. American Naturalist 113, 762-765.
18. Griffen, B. D. and Byers, J. E. (2006). Intraguild predation reduces redundancy of predator species in multiple predator assemblage. Journal of Animal Ecology 75, 959-966.
19. Holmlund, M. B., Peterson, C. H. and Hay, M. E. (1990). Does algal morphology affect amphipod susceptibility to fish predation. Journal of Experimental Marine Biology and Ecology 139, 65-83.
20. Hynes, H. B. N. (1954). The ecology of Gammarus duebeni lilljeborg and its occurence in fresh water in western Britain. Journal of Animal Ecology 23, 38-84.
21. Kaldonski, N., Perrot-Minnot, M. J. and Cézilly, F. (2007). Differential influence of two acanthocephalan parasites on the anti-predator behaviour of their common intermediate host. Animal Behaviour 74, 1311-1317.
22. Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854-867.
23. Lafferty, K. D. and Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390-1397.
24. Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839-2847.
25. MacNeil, C., Dick, J. T. A. and Elwood, R. W. (1999). The dynamics of predation on Gammarus spp. (Crustacea: Amphipoda). Biological Reviews 74, 375-395.
26. Maltby, L., Clayton, S. A., Wood, R. M. and McLoughlin, N. (2002). Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: Robustness, responsiveness, and relevance. Environmental Toxicology and Chemistry 21, 361-368.
27. Manly, B. F. J. (1974). A model for certain types of selection experiments. Biometrics 30, 281-294.
28. Marriott, D. R., Collins, M. L., Paris, R. M., Gudgin, D. R., Barnard, C. J., Mcgregor, P. K., Gilbert, F. S., Hartley, J. C. and Behnke, J. M. (1989). Behavioral modifications and increased predation risk of Gammarus pulex infected with Polymorphus minutus. Journal of Biological Education 23, 135-141.
29. McCafferty, W. (1981). Aquatic Entomology. Science Books International, Boston.
30. Moore, J. (2002). Parasites and the Behavior of Animals, Oxford University Press, New York.
31. Mouritsen, K. N. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043-1050.
32. Ness, J. H. and Foster, S. A. (1999). Parasite-associated phenotype modifications in threespine stickleback. Oikos 85, 127-134.
33. Nickol, B. B., Fuller, C. A. and Rock, P. (2006). Cystacanths of Oncicola venezuelensis (Acanthocephala: Oligacanthorhynchidae) in Caribbean termites and various paratenic hosts in the US Virgin Islands. Journal of Parasitology 92, 539-542.
34. Nilsson, P. A., Nilsson, K. and Nystrom, P. (2000). Does risk of intraspecific interactions induce shifts in prey-size preference in aquatic predators? Behavioral Ecology and Sociobiology 48, 268-275.
35. Ohba, S. and Nakasuji, F. (2006). Dietary items of predacious aquatic bugs (Nepoidea: Heteroptera) in Japanese wetlands. Limnology 7, 41-43.
36. Perrot-Minnot, M.-J., Kaldonski, N. and Cézilly, F. (2007). Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected host. International Journal for Parasitology 37, 645-651.
37. Poulin, R. (1995). "'Adaptive" changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 1371-1383.
38. Poulin, R., Fredensborg, B. L., Hansen, E. and Leung, T. L. F. (2005). The true cost of host manipulation by parasites. Behavioural Processes 68, 241-244.
39. Redmond, M. S. and Scott, K. J. (1989). Amphipod predation by the infaunal polychaete, Nephtys incisa. Estuaries 12, 205-207.
40. Runck, C. and Blinn, D. W. (1994). Role of Belostoma bakeri (Heteroptera) in the trophic ecology of a fishless desert spring. Limnology and Oceanography 39, 1800-1812.
41. Seppälä, O., Karvonen, A. and Valtonen, E. T. (2006a). Host manipulation by parasites and risk of non-host predation: is manipulation costly in an eye fluke-fish interaction? Evolutionary Ecology Research 8, 871-879.
42. Seppälä, O., Karvonen, A. and Valtonen, E. T. (2006b). Susceptibility of eye fluke-infected fish to predation by bird hosts. Parasitology 132, 575-579.
43. Sokal, E. R. and Rohlf, F. J. (1995). Biometry, 3rd Edn. W.H. Freeman, New-York.
44. Stewart, T. W., Miner, J. G. and Lowe, R. L. (1998). An experimental analysis of crayfish (Orconectes rusticus) effects on a Dreissena-dominated benthic macroinvertebrate community in western Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 55, 1043-1050.
45. Tain, L., Perrot-Minnot, M.-J. and Cézilly, F. (2006). Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society of London, B 273, 3039-3045.
46. Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185-199.
47. Vance, S. A. and Peckarsky, B. L. (1997). The effect of mermithid parasitism on predation of nymphal Baetis bicaudatus (Ephemeroptera) by invertebrates. Oecologia 110, 147-152.
48. Wilhelm, F. M., Hamann, J. and Burns, C. W. (2002). Mysid predation on amphipods and Daphnia in a shallow coastal lake: prey selection and effects of macrophytes. Canadian Journal of Fisheries and Aquatic Sciences 59, 1901-1907.