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

Parasitology

Volumn 140, Issue 2, 2013, Pages 258-265

  Lagrue, C ^a,b   Guvenatam A ^b   Bollache, L ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Echinorhynchus truttae; host distribution; intermediate host manipulation; Polymorphus minutus; trophic transmission

Indexed keywords

ARTICLE; ECHINORHYNCHUS TRUTTAE; GAMMARUS PULEX; NONHUMAN; PARASITE; PARASITE PREVALENCE; PARASITE TRANSMISSION; PARASITOSIS; POLYMORPHUS MINUTUS; PREDATOR; PRIORITY JOURNAL;

ACANTHOCEPHALA; AMPHIPODA; ANIMALS; BEHAVIOR, ANIMAL; DIET; ESCAPE REACTION; FISHES; FOOD CHAIN; HELMINTHIASIS, ANIMAL; HOST-PARASITE INTERACTIONS; LINEAR MODELS; POPULATION DENSITY;

EID: 84873384099     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012001552     Document Type: Article

References (50)

1. 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, 379-387.
2. Awachie, J. B. E. (1966). The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology 40, 11-32.
3. 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, 481-484.
4. 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, 61-65.
5. 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, 219-230.
6. Benesh, D. P., Kitchen, J., Pulkkinen, K., Hakala, I. and Valtonen, E. T. (2008a). The effects of Echinorhynchus borealis (Acanthocephala) infection on the anti-predator behaviour of a benthic amphipod. Journal of Parasitology 94, 542-545.
7. Benesh, D. P., Valtonen, E. T. and Seppälä, O. (2008b). Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan. Parasitology 135, 617-626.
8. 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, 131-137.
9. Cézilly, F., Gregoire, A. and Bertin, A. (2000). Conflict between cooccurring manipulative parasites? An experimental study of the joint influences of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625-630.
10. 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.
11. Cézilly, F. and Perrot-Minnot, M.-J. (2010). Interpreting multidimensionality in parasite-induced phenotypic alterations: Panselectionism versus parsimony. Oikos 119, 1224-1229.
12. Crompton, D.W. T. and Nickol, B. B. (1985). Biology of the Acanthocephala. Cambridge University Press, Cambridge, UK.
13. 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, 1339-1344.
14. 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, 2692-2698.
15. 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, 8-15.
16. 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.
17. Holmes, J. C. and Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. Zoological Journal of the Linnean Society 51, 123-149.
18. 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, 110-115.
19. 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, 1311-1317.
20. 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, 627-632.
21. 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, 1-59.
22. Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111-115.
23. 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, 318-322.
24. 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, 2839-2847.
25. Levri, E. P. (1998). Perceived predation risk, parasitism, and the foraging behaviour of a freshwater snail (Potamopyrgus antipodarum). Canadian Journal of Zoology 76, 1878-1884.
26. Lima, S. L. (1998). Nonlethal effects in the ecology of predator-prey interactions - What are the ecological effects of anti-predator decisionmaking? Bioscience 48, 25-34.
27. 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, 686-697.
28. 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, 1401-1404.
29. 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, 57-64.
30. 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, 135-141.
31. Mathis, A. and Hoback, W.W. (1997). The influence of chemical stimuli from predators on precopulatory pairing by the amphipod, Gammarus pseudolimnaeus. Ethology 103, 33-40.
32. Médoc, V. and Beisel, J.-N. (2008). An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators. Parasitology 135, 977-984.
33. Médoc, V. and Beisel, J.-N. (2009). Field evidence for non-host predator avoidance in a manipulated amphipod. Naturwissenschaften 96, 513-523.
34. Médoc, V. and Beisel, J.-N. (2011). When trophically-transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos 120, 1452-1458.
35. 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, 1351-1358.
36. 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, 1235-1241.
37. Moore, J. (2002). Parasites and the behaviour of animals. Oxford Series in Ecology and Evolution. Oxford University Press, NY, USA.
38. 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, 1043-1050.
39. 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, 41-45.
40. 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, 47-54.
41. 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, 645-651.
42. Poulin, R. (1995). "Adaptive" changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology 25, 1371-1383.
43. Rousset, F., Thomas, F., de Meeüs, T. and Renaud, F. (1996). Inference of parasite-induced mortality from distributions of parasite loads. Ecology 77, 2203-2211.
44. Seppälä, O. and Jokela, J. (2008). Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663-666.
45. 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, 1611-1615.
46. 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, 349-352.
47. Thomas, F., Adamo, S. A. and Moore, J. (2005). Parasitic manipulation: Where are we and where should we go? Behavioural Processes 68, 185-199.
48. Thomas, F., Poulin, R. and Brodeur, J. (2010). Host manipulation by parasites: A multidimensional phenomenon. Oikos 119, 1217-1223.
49. Wellnitz, T., Giari, L., Maynard, B. and Dezfuli, B. S. (2003). A parasite spatially structures its host population. Oikos 100, 263-268.
50. 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, 1163-1173.