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Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: host response to infection

Published online by Cambridge University Press:  11 May 2005

A. KOSTADINOVA
Affiliation:
Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, PO Box 22 085, 46071 Valencia, Spain
R. S. MAVRODIEVA
Affiliation:
Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria

Abstract

We examined the patterns of parasite melanization in Gammarus insensibilis using data on microphallids from Pomorie Lagoon (Black Sea) in the light of 3 predictions associated with host survival: (i) hosts invest more in defence in an environment where the likelihood for infection is higher; (ii) multiple immune challenges exhaust host reserves and result in decreased melanization rates in older hosts; (iii) host immune response is directed against the cerebral metacercariae of Microphallus papillorobustus that alter amphipod behaviour and are most detrimental to the host. G. insensibilis was capable of melanizing the metacercariae of all four species of trematodes found to be hosted by the amphipods. The frequency of melanization and mean abundance of melanized metacercariae were substantially higher than those observed in the same amphipod-gammarid system on the French Mediterranean coast. However, the rate of melanization was low and showed a significant decrease with amphipod size. Although the 4 species were differentially melanized, the host response was largely directed against Microphallus hoffmanni and M. subdolum. We suggest that (i) the lower melanization efficiency with age is due to the mode of infection, probably leading to loss of haemolymph and monopolization of the defence resources for wound healing and (ii) in the French system, host response focuses on the most prevalent and abundant species.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Bush, A. O., Laferty, K. D., Lotz, J. M. and Shostack, A. W. ( 1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cerenius, L. and Söderhäll, K. ( 2004). The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116126.CrossRefGoogle Scholar
Edgerton, B. F., Evans, L. H., Stephens, F. J. and Overstreet, R. M. ( 2002). Synopsis of freshwater crayfish diseases and commensal organisms. Aquaculture 206, 57135.CrossRefGoogle Scholar
Eslin, P. and Prévost, G. ( 2000). Racing against host's immunity defences: a likely strategy for passive evasion of encapsulation in Asobara tabida parasitoids. Journal of Insect Physiology 46, 11611167.CrossRefGoogle Scholar
Fredensborg, B. L., Mouritsen, K. N. and 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, 253265.CrossRefGoogle Scholar
Ginetsinskaya, T. A. ( 1988). Trematodes, their Life Cycles, Biology and Evolution. Amerind Publishing Co., New Delhi.
Helluy, S. ( 1983). Relations hôtes-parasite du trématode Microphallus papillorobustus (Rankin, 1940). II-Modifications du comportement des Gammarus hôtes intermédiaires et localisation des métacercaires. Annales de Parasitologie Humaine et Comparée 58, 117.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 tests de prédation. Annales de Parasitologie Humaine et Comparée 59, 4156.CrossRefGoogle Scholar
Jensen, T., Jensen, K. T. and Mouritsen, K. N. ( 1998). The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival. Journal of Experimental Marine Biology and Ecology 227, 3548.CrossRefGoogle Scholar
Kostadinova, A. and Gibson, D. I. ( 1994). Microphallid trematodes in the amphipod Gammarus subtypicus Stock, 1966 from a Black Sea lagoon. Journal of Natural History 28, 3745.CrossRefGoogle Scholar
Kostadinova, A. and Mavrodieva, R. S. ( 2005). Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: manipulation hypothesis going East? Parasitology 131, (this issue).Google Scholar
König, C. and Schmid-Hempel, P. ( 1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society of London, B 260, 225227.CrossRefGoogle Scholar
Moret, Y. and Schmid-Hempel, P. ( 2000). Survival for immunity: the price of immune system activation for bumble bee workers. Science 290, 11661168.CrossRefGoogle Scholar
Mouritsen, K. N. and Jensen, K. T. ( 1997). Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123134.CrossRefGoogle Scholar
Norušis, M. J. ( 2002). SPSS®11.0 Guide to Data Analysis. Prentice Hall Inc., New Jersey.
Plaistow, S. J., Outreman, Y., Moret, Y. and Rigaud, T. ( 2003). Variation in the risk of being wounded: and overlooked factor in studies of invertebrate immune function? Ecology Letters 6 489494.Google Scholar
Rigaud, T. and Moret, Y. ( 2003). Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127, 571577.Google Scholar
Rigby, M. C. and Moret, Y. ( 2000). Life-history trade-offs with immune defenses. In Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. & Skorping, A.) Elsevier, Amsterdam.
Rolff, J. and Siva-Jothy, M. T. ( 2002). Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences, USA 99, 99169918.CrossRefGoogle Scholar
Rózsa, L., Reiczigel, J. and Majoros, G. ( 2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 226232.Google Scholar
Schmid-Hempel, P. and Ebert, D. ( 2003). On the evolutionary ecology of specific immune defence. Trends in Ecology and Evolution 18, 2732.CrossRefGoogle Scholar
Siva-Jothy, M. T., Tsubaki, Y., Hooper, R. E. and Plaistow, S. J. ( 2001). Investment in immune function under chronic and acute immune challenge in an insect. Physiological Entomology 26, 15.Google Scholar
Thomas, F., Renaud, F., Rousset, F., Cézilly, F. and De Meeûs, T. ( 1995). Differential mortality of two closely related species induced by one parasite. Proceedings of the Royal Society of London, B 260, 349352.CrossRefGoogle Scholar
Thomas, F., Poulin, R. and Renaud, F. ( 1998 a). Nonmanipulative parasites in manipulated hosts: ‘Hitch-hikers’ or simply ‘lucky passengers’? Journal of Parasitology 84, 10591061.Google Scholar
Thomas, F., Villa, M., Montoliu, I., Santalla, F., Cézilly, F. and Renaud, F. ( 1998 b). Analyses of a debilitating parasite (Microphallus papilorobustus, Trematoda) and its “hitch-hiker” parasite (Maritrema subdolum, Trematoda) on survival of their intermediate host (Gammarus insensibilis, Amphipoda). Journal of the Helminthological Society of Washington 65, 15.Google Scholar
Thomas, F., Guldner, E. and Renaud, F. ( 2000). Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). Journal of Parasitology 86, 650654.CrossRefGoogle Scholar
Thörnqvist, P.-O. and Söderhäll, K. ( 1997). Crustacean immune reactions, a short review. In Diseases in Asian Aquaculture III. Fish Health Section, Asian Fisheries Society, Philippines.
Zander, C. D., Koçoglu, Ö., Skroblies, M. and Strohbach, U. ( 2002). Parasite populations and communities from the shallow littoral of the Orther Bight (Fehmarn, SW Baltic Sea). Parasitology Research 88, 734744.CrossRefGoogle Scholar