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Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex

Published online by Cambridge University Press:  19 July 2007

N. FRANCESCHI ,
T. RIGAUD ,
Y. MORET ,
F. HERVANT  and
L. BOLLACHE
N. FRANCESCHI*
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS Biogéosciences 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
T. RIGAUD
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS Biogéosciences 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
Y. MORET
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS Biogéosciences 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
F. HERVANT
Affiliation:
Ecologie des Hydrosystèmes Fluviaux, UMR CNRS 5023, Université Claude Bernard Lyon1, 69622 Villeurbanne cedex, France
L. BOLLACHE
Affiliation:
Equipe Ecologie Evolutive, UMR CNRS Biogéosciences 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France
*
*Corresponding author: Equipe Ecologie Evolutive, UMR CNRS 5561, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France. Tel: +33 380 39 62 28. Fax: +33 380 39 62 31. E-mail: [email protected]
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Summary

Some parasites with complex life-cycles are able to manipulate the behaviour of their intermediate hosts in a way that increases their transmission to the next host. Gammarids infected by the tapeworm Cyathocephalus truncatus (Cestoda: Spathebothriidea) are known to be more predated by fish than uninfected ones, but potential behavioural manipulation by the parasite has never been investigated. In this study, we tested the hypothesis that C. truncatus is able to manipulate the behaviour of one of its intermediate hosts, Gammarus pulex (Crustacea: Amphipoda). To assess if any behavioural change was linked to other phenotypic alterations, we also measured the immunity of infected and uninfected individuals and investigated the pathogenic effects of the parasite. Infected gammarids were significantly less photophobic than uninfected ones, but no effect of infection on the level of immune defence was found. The results on survival, swimming activity and oxygen consumption suggest that the parasite also has various pathogenic effects. However, the alteration in host phototaxis was not correlated to some of these pathogenic effects. Therefore, we propose that the modification in host reaction to light is a behavioural manipulation, explaining the previously observed increase of gammarid predation rate.

Keywords

cestodeGammaridaebehavioural manipulationimmunitypathogenic effects
Type
Research Article
Information
Parasitology , Volume 134 , Issue 12 , November 2007 , pp. 1839 - 1847
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Arme, C. and Owen, R. W. (1967). Infections of the three-spined stickleback, Gastrosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects. Parasitology 57, 310–314.CrossRefGoogle ScholarPubMed
Awachie, J. B. E. (1966). Observations on Cyathocephalus truncatus Pallas 1781 (Cestoda: Spathebothriidea) in its intermediate and definitive hosts in a trout stream, North Wales. Journal of Helminthology 40, 1–10.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Barber, I. and Svensson, P. A. (2003). Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126, 359–367.CrossRefGoogle ScholarPubMed
Bauer, A., Haine, E. R., Perrot-Minnot, M. J. and Rigaud, T. (2005). The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric hosts Gammarus pulex (native host) and Gammarus roeseli (invasive host). Journal of Zoology 267, 39–43.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1973). Altered evasive behaviour and response to light in amphipods harbouring acanthocephalan cystacanths. Journal of Parasitology 59, 945–956.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–116.CrossRefGoogle Scholar
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle ScholarPubMed
Bollache, L., Kaldonski, N., Troussard, J. P., Lagrue, C. and Rigaud, T. (2006). Spines and behaviour as defences against fish predators in an invasive freshwater amphipod. Animal Behaviour 72, 627–633.CrossRefGoogle Scholar
Cézilly, F., Grégoire, A. and Bertin, A. (2000). Conflict between co-occuring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago and London.Google Scholar
Damian, R. T. (1964). Molecular mimicry: antigen sharing by parasite and host and its consequences. The American Naturalist 98, 129–149.CrossRefGoogle Scholar
Franz, K. and Kurtz, J. (2002). Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods? Parasitology 125, 187–196.CrossRefGoogle ScholarPubMed
Hervant, F., Mathieu, J., Barré, H., Simon, K. and Pinon, C. (1997). Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comparative Biochemistry and Physiology 118A, 1277–1283.CrossRefGoogle Scholar
Hoogenboom, I. and Dijkstra, C. (1987). Sarcocystis cernae: a parasite increasing the risk of predation of its intermediate host, Microtus arvalis. Oecologia 74, 86–92.CrossRefGoogle ScholarPubMed
Knudsen, R., Gabler, H. M., Kuris, A. M. and Amundsen, P. A. (2001). Selective predation on parasitized prey. A comparison between two helminth species with different life-history strategies. Journal of Parasitology 87, 941–945.Google Scholar
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.CrossRefGoogle Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Altered drift behaviour and increased vulnerability to predation in intermediate hosts infected by an acanthocephalan parasite: field evidence for adaptive manipulation. Ecology (in the Press).CrossRefGoogle Scholar
Levri, E. P. (1999). Parasite-induced change in host behaviour of a freshwater snail: parasitic manipulation or byproduct of infection? Behavioral Ecology 10, 234–241.CrossRefGoogle Scholar
Levri, E. P. and Fisher, L. M. (2000). The effect of a trematode parasite (Microphallus sp.) on the response of the freshwater snail Potamopyrgus antipodarum to light and gravity. Behaviour 137, 1141–1151.CrossRefGoogle Scholar
Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93, 203–215.CrossRefGoogle Scholar
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–1015.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Moore, J. and Lasswell, J. (1986). Altered behaviour in isopods (Armadillidium vulgare) infected with the nematode Dispharynx nasuta. Journal of Parasitology 72, 186–189.CrossRefGoogle Scholar
Moret, Y., Bollache, L., Wattier, R. and Rigaud, T. (2007). Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context. International Journal for Parasitology 37, 637–644.CrossRefGoogle ScholarPubMed
Moret, Y. and Schmid-Hempel, P. (2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
Nigam, Y., Maudlin, I., Welburn, S. and Ratcliffe, N. A. (1997). Detection of phenoloxidase activity in the hemolymph of tsetse flies, refractory and susceptible to infection with Trypanosoma brucei rhodesiense. Journal of Invertebrate Pathology 69, 279–281.CrossRefGoogle ScholarPubMed
Okaka, C. E. (1984). Studies on the biology of Cyathocephalus truncatus (Pallas, 1781) (Cestoda: Spathebothriidea) in the fish and crustacean host. Unpublished Ph.D. thesis, University of Leeds, UK.Google Scholar
Pasternak, A. F., Huntingford, F. A. and Crompton, D. W. T. (1995). Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110, 395–399.CrossRefGoogle ScholarPubMed
Perrot-Minnot, M. J. (2004). Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). International Journal for Parasitology 34, 45–54.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Poulin, R. (1995). “Adaptive” changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 1371–1383.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall, London, UK.Google Scholar
Poulin, R., Curtis, M. A. and Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–271.CrossRefGoogle Scholar
Pulkkinen, K., Pasternak, A. F., Hasu, T. and Valtonen, E. T. (2000). Effect of Triaenophorus crassus (Cestoda) infection on behaviour and susceptibility to predation of the first intermediate host Cyclops strenuus (Copepoda). Journal of Parasitology 86, 664–670.CrossRefGoogle ScholarPubMed
Quinn, G. P. and Keough, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Rigaud, T. and Moret, Y. (2003). Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosupression? Parasitology 127, 571–577.CrossRefGoogle Scholar
Rumpus, A. E. and Kennedy, C. R. (1974). The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology 68, 271–284.CrossRefGoogle ScholarPubMed
Söderhäll, K. and Cerenius, L. (1998). Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 23–28.CrossRefGoogle ScholarPubMed
Sugumaran, M., Nellaiappan, K. and Valivittan, K. (2000). A new mechanism for the control of phenoloxidase activity: inhibition and complex formation with quinone isomerase. Archives of Biochemistry and Biophysics 379, 252–260.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Thomas, F. and Poulin, R. (1998). Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431–436.CrossRefGoogle ScholarPubMed
Urdal, K., Tierney, J. F. and Jakobsen, P. J. (1995). The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. Journal of Parasitology 81, 330–333.CrossRefGoogle Scholar
Walkey, M. and Meakins, R. H. (1970). An attempt to balance the energy budget of a host-parasite system. Journal of Fish Biology 2, 361–372.CrossRefGoogle Scholar
Webb, T. J. and Hurd, H. (1999). Direct manipulation of insect reproduction by agents of parasite origin. Proceedings of the Royal Society of London, B 266, 1537–1541.CrossRefGoogle Scholar