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Effects of the trematode Maritrema novaezealandensis on the behaviour of its amphipod host: adaptive or not?

Published online by Cambridge University Press:  12 April 2024

T.L.F. Leung  and
R. Poulin
T.L.F. Leung
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
R. Poulin*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
*
*Author of correspondence Fax: +64 3 479 7584 Email: robert.poulin@stonebow.otago.ac.nz
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Abstract

There are many recorded cases of parasites that are capable of altering the behaviour of their host to enhance their transmission efficiency. However, not all of these cases are necessarily the results of the parasites actively manipulating host behaviour; they may rather be the ‘by-products’ of pathology caused by the parasite's presence. This study investigates the effect of the microphallid trematode Maritrema novaezealandensis on the behaviour of one of its crustacean intermediate hosts, the amphipod Paracalliope novizealandiae. Uninfected amphipods were experimentally infected by exposure to M. novaezealandensis cercariae. The activity level and vertical position of experimentally infected amphipods were compared with uninfected amphipods at 2 weeks and 6 weeks post-infection, i.e. both before and after the parasite achieved infectivity to its definitive host. Infected amphipods were found to exhibit significantly lower levels of activity and to occur significantly lower in the water column than uninfected controls during both periods. Based on the timing of the change in behaviour exhibited by infected amphipods, the results suggest that the altered behaviour exhibited by P. novizealandiae infected with M. novaezealandensis is most likely due to pathology caused by the parasite rather than a case of active, and adaptive, behavioural manipulation.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 3 , September 2006 , pp. 271 - 275
Copyright
Copyright © Cambridge University Press 2006

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References

Bakker, T.C.M., Mazzi, D. & Zala, S. (1997) Parasite-induced changes in behaviour and colour make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle Scholar
Bauer, A. Trouvé, S, Grégoire, A., Bollache, L. & Cézilly, F. (2000) Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology 30, 1453–1457.CrossRefGoogle ScholarPubMed
Franz, K. & Kurtz, J. (2002) Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods?. Parasitology 125, 187–196.CrossRefGoogle ScholarPubMed
Fredensborg, B.L., Mouritsen, K.N. & Poulin, R. (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.10.1016/j.jembe.2004.05.011CrossRefGoogle Scholar
Helluy, S. (1983) Relations hôtes-parasites du trématode Microphallus papillorobustus (Rankin 1940). II Modifications du comportement des Gammarus hôtes intermédiaires et localization des métacercaires. Annales de Parasitologie Humaine et Comparée 58, 1–17.CrossRefGoogle Scholar
Helluy, S. (1984) Relations hôtes-parasites du trématode Microphallus papillorobustus (Rankin 1940). III Facteurs impliqués dans les modifications du comportement des Gammarus hôtes intermédiaires et test de prédation. Annales de Parasitologie Humaine et Comparée 59, 41–56.10.1051/parasite/1984591041CrossRefGoogle Scholar
Helluy, S. & Thomas, F. (2003) Effects of Microphallus papillorobustus (Platyhelminthes, Trematoda) on serotonergic immunoreactivity and neuronal architecture of the brain of Gammarus insensibilis (Crustacea, Amphipoda). Proceedings of the Royal Society of London B 270, 563–568.CrossRefGoogle ScholarPubMed
Kunz, A.K. & Pung, O.J. (2004) Effects of Microphallus turgidus (Trematoda: Microphallidae) on the predation, behaviour, and swimming stamina of the grass shrimp Palaemonetes pugio. Journal of Parasitology 90, 441–445.10.1645/GE-183RCrossRefGoogle ScholarPubMed
Lafferty, K.D. (1999) The evolution of trophic transmission. Parasitology Today 15, 111–115.10.1016/S0169-4758(99)01397-6CrossRefGoogle ScholarPubMed
Martorelli, S.R., Fredensborg, B.L., Mouritsen, K.N. & Poulin, R. (2004) Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbour, South Island, New Zealand. Journal of Parasitology 90, 272–277.10.1645/GE-3254CrossRefGoogle Scholar
Moore, J. (2002) Parasites and the behaviour of animals.pp 315.Oxford Oxford University Press.10.1093/oso/9780195084412.001.0001CrossRefGoogle Scholar
Poulin, R. (1995) “Adaptive”changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 1371–1383.10.1016/0020-7519(95)00100-XCrossRefGoogle ScholarPubMed
Poulin, R. (2000) Manipulation of host ehaviour by parasites: a weakening paradigm?. Proceedings of the Royal Society of London B 267, 787–792.10.1098/rspb.2000.1072CrossRefGoogle Scholar
Poulin, R., Curtis, M.A. & Rau, M.E. (1992) Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–271.10.1017/S0031182000074199CrossRefGoogle Scholar
Poulin, R., Nichol, K. & Latham, A.D.M. (2003) Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict?. International Journal for Parasitology 33, 425–433.10.1016/S0020-7519(03)00002-XCrossRefGoogle ScholarPubMed
Shirakashi, S. & Goater, C.P. (2005) Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology 130, 177–183.10.1017/S0031182004006432CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., Rousset, F., Cézilly, F. & de Meeûs, T. (1995) Differential mortality of two closely related host species induced by one parasite. Proceedings of the Royal Society of London B 260, 349–352.Google Scholar
Tompkins, D.M., Mouritsen, K.N. & Poulin, R. (2004) Parasite-induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?. Journal of Evolutionary Biology 17, 247–256.10.1111/j.1420-9101.2003.00688.xCrossRefGoogle ScholarPubMed
Urdal, K., Tierney, J.F. & 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, 330–333.10.2307/3283949CrossRefGoogle Scholar
Webster, J.P., Gowtage-Sequeira, S., Berdoy, M. & Hurd, H. (2000) Predation of beetles (Tenebrio molitor) infected with tapeworms (Hymenolepis diminuta): a note of caution for the Manipulation Hypothesis. Parasitology 120, 313–318.10.1017/S003118209900548XCrossRefGoogle ScholarPubMed