Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation

Ecology

Volumn 78, Issue 4, 1997, Pages 1098-1104

  Bakker, Theo C M ^a   Mazzi, Dominique ^a   Zala, Sarah ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Behavioral changes; Coloration; Gammarus pulex; Gasterosteus aculeatus; Intermediate host; Parasite transmission; Pomphorhynchus laevis; Predation risk

Indexed keywords

CRUSTACEA; GAMMARIDAE; GAMMARUS PULEX; GASTEROSTEUS ACULEATUS; POMPHORHYNCHUS LAEVIS; PULEX; ACANTHOCEPHALA; AMPHIPODA;

BODY COLOUR; PARASITE TRANSMISSION; PREDATION RISK;

EID: 0030614118     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(1997)078[1098:piciba]2.0.co;2     Document Type: Article

References (48)

1. Bakker, T. C. M. 1993. Positive genetic correlation between female preference and preferred male ornament in stickle- backs. Nature 363:255-257.
2. Bakker, T. C. M., and B. Mundwiler. 1994. Female mate choice and male red coloration in a natural stickleback population. Behavioral Ecology 5:74-80.
3. Bakker, T. C. M., and P. Sevenster. 1983 Determinants of dominance in male sticklebacks (Gasterosteus aculeatus L.). Behaviour 86:55-71.
4. Barrett, J., and P. E. Butterworth. 1968. The carotenoids of Polymorphic minutus (Acanthocephala) and its intermediate host, Gammarus pulex. Comparative Biochemistry and Physiology 27:575-581.
5. Barrett, J., and P. E. Butterworth. 1973. The carotenoid pigments of six species of adult Acanthocephala. Experientia 29:651-653.
6. Bentley, C. R., and H. Hurd. 1993. Pomphorhynchus laevis (Acanthocephala): elevation of haemolymph protein concentration in the intermediate host. Gammarus pulex (Crustacea: Amphipoda). Parasitology 107:193-198.
7. Bethel, W. M., and J. C. Holmes. 1973. Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59:945-956.
8. Bethel, W. M., and J. C. Holmes. 1974. Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradox (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60:272-274.
9. Bethel, W. M., and J. C. Holmes. 1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Canadian Journal of Zoology 55:110-115.
10. Bolger, T. and P. L. Connolly 1989. The selection of suitable indices for the measurement and analysis of fish condition. Journal of Fish Biology 34:171-182.
11. Boonyaratpalin, M., and N. Unprasert. 1989. Effects of pigments from different sources on colour changes and growth of red Oreochromis niloticus. Aquaculture 79:375-380.
12. Brush, A. H., and H. M. Reisman. 1965. The carotenoid pigments in the three-spined stickleback, Gasterosteus aculeatus. Comparative Biochemistry and Physiology 14:121- 125.
13. Byron, E. A. 1982. The adaptive significance of calanoid copepod pigmentation: a comparative and experimental analysis. Ecology 63:1871-1886.
14. Camp, J. W., and H. W. Huizinga. 1979. Altered color, behavior and predation susceptibility of the isopod, Asellus intermedius, infected with Acanthocephalus dirus. Journal of Parasitology 65:667-669.
15. Chubb, J. C. 1965. Mass occurrence of Pomphorhynchus laevis (Müller, 1776) Monticelli 1905 (Acanthocephala) in the chub Squalius cephalus L. from the River Avon, Hampshire. Parasitology 55:1-5.
16. Curio, E. 1976. The ethology of predation. Springer-Verlag, Berlin, Germany.
17. Czeczuga, B. 1980. Carotenoids in fish. XXVI. Pungitius pungitius (L.) and Gasterosteus aculealus L. (Gasterosteidac). Hydrobiologia 74:7-10.
18. Goodwin, T. W. 1986. Metabolism, nutrition, and function of carotenoids. Annual Review of Nutrition 6:273-297.
19. Hairston, N. G., Jr. 1976. Photoprotection by carotenoid pigments in the copepod Diaptomus nevadensis. Proceedings of the National Academy of Sciences USA 73:971-974.
20. _. 1979. The relationship between pigmentation and reproduction in two species of Diaptomus (Copepoda). Limnology and Oceanography 24:38-44.
21. _. 1980. The vertical distribution of diaptomid copepods in relation to body pigmentation. Pages 98-110 in W. C. Kerfoot, editor. Evolution and ecology of zooplankton communities. University Press of New England, Hanover, New Hampshire, USA.
22. Harris-Warrick, R. M., R. E. Flamm, B. R. Johnson, and P. S. Katz. 1989. Modulation of neural circuits in Crustacea. American Zoologist 29:1305-1320.
23. Helluy, S., and J. C. Holmes. 1990. Serotonin, octapamine, and the clinging behavior induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Canadian Journal of Zoology 68:1214- 1220.
24. Hindsbo, O. 1972. Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris. Nature 238:333.
25. Hine, P. M., and C. R. Kennedy. 1974. Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller). Journal of Fish Biology 6:521-535.
26. Holmes, J. C., and W. M. Bethel. 1972. Modification of intermediate host behaviour by parasites. Zoological Journal of the Linnean Society, Supplement 1 51:123-149.
27. Ibrahim, A. A., and F. A. Huntingford. 1992. Experience of natural prey and feeding efficiency in three-spined stickle- backs (Gasterosteus aculeatus L.). Journal of Fish Biology 41:619-625.
28. Kennedy, C. R., P. F. Broughton, and P. M. Hine. 1978. The status of brown and rainbow trout, Salmo trutta and S. gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis. Journal of Fish Biology 13:265-275.
29. Latferty, K. D. 1992. Foraging on prey that are modified by parasites. The American Naturalist 140:854-867.
30. Luecke, C., and W. J. O'Brien. 1981. Phototoxicity and fish predation: selective factors in color morphs in Heterocope. Limnology and Oceanography 26:454-460.
31. Luecke, C., and W. J. O'Brien. 1983. Photoprotective pigmentation in a pond morph of Daphnia middendorffiana. Arctic 36:365-368.
32. Mackney, P. A., and R. N. Hughes. 1995. Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241- 1253.
33. Milinski, M., and T. C. M. Bakker. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330-333.
34. Moore, J. 1984. Altered behavioral responses in intermediate hosts - an acanthocephalan parasite strategy. American Naturalist 123:572-577.
35. _. 1995. The behavior of parasitized animals. Bio- Science 45:89-96.
36. Moore, J., and N. J. Gotelli. 1990. A phylogenetic perspec- tive on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. Pages 193-233 in C. J. Barnard and J. M. Behnke, editors. Parasite and host behaviour. Taylor and Francis, London, UK.
37. Nickol, B. B. 1985. Epizootiology. Pages 307-346 in D. W. T. Crompton and B. B. Nickol, editors. Biology of the Acanthocephala. Cambridge University Press, Cambridge, UK.
38. Poulin, R. 1994. Meta-analysis of parasite-induced behavioral changes. Animal Behaviour 48:137-146.
39. Poulin, R., M. A. Curtis, and M. E. Rau. 1992. Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105:265-271.
40. Ringelberg, J. 1980. Aspects of red pigmentation in zooplankton, especially copepods. Pages 91-97 in W. C. Kerfoot, editor. Evolution and ecology of Zooplankton communities. University Press of New England, Hanover, New Hampshire, USA.
41. Ringelberg, J., A. L. Keyser, and B. J. G. Flik. 1984. The mortality effect of ultraviolet radiation in a translucent and in a red morph of Acanthodiaptomus denticornis (Crustacea, Copepoda) and its possible ecological relevance. Hydrobiologia 112:217-222.
42. Rumpus, A. E., and C. R. Kennedy. 1974. The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology 68:271-284.
43. Segner, H., P. Arend, K. von Pocppinghausen, and H. Schmidt. 1989. The effect of feeding astaxanthin to Oreochromis niloticus and Colisa labiosa on the histology of the liver. Aquaculture 79:381-390.
44. Simpson, K. L., T. Katayama, and C. O. Chichester. 1981. Carotenoids in fish feeds. Pages 463-538 in J. C. Bauernfeind, editor. Carotenoids as colorants and vitamin A precursors. Technological and Nutritional Applications. Academic Press, New York, New York, USA.
45. Thompson, S. N., and M. Kavaliers. 1994. Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109:S119-S138.
46. Urdal, K., J. F. Tierney, and P. J. Jakobsen. 1995. The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. Journal of Parasitology 81:330-333.
47. Wedekind, C., and M. Milinski. 1996. Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus - an experimental analysis of behavioural resistance. Parasitology 112:371- 383.
48. Williamson, C. E. 1995. What role does UV-B radiation play in freshwater ecosystems? Limnology and Oceanography 40:386-392.