Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-05-20T14:30:35.380Z Has data issue: false hasContentIssue false
  • English
  • Français

Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: manipulation hypothesis going East?

Published online by Cambridge University Press:  21 April 2005

A. KOSTADINOVA  and
R. S. MAVRODIEVA
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
Get access Rights & Permissions [Opens in a new window]

Abstract

Patterns of parasite site selection, variation in infection parameters and interspecific associations are examined in the light of new field data on larval microphallids in Gammarus insensibilis from a Black Sea lagoon. These patterns are discussed in relation to the predictions for the manipulative effect of Microphallus papillorobustus and its relationships with the other microphallid species based on studies on the French Mediterranean coast. Four species were recovered: Maritrema subdolum, Microphallus hoffmanni, M. papillorobustus and Levinseniella propinqua. The latter two were located in both corporal and cephalic segments, but the selection of brain appeared stronger for L. propinqua. M. subdolum was the first colonizer of amphipod population recruits, and unequivocally the dominant species in the lagoon. There was a significant positive relationship between the parasite load of all 4 species. Concurrent infections were exceedingly frequent, and no departures from random association were detected. We found no evidence that the cerebral metacercariae of M. papillorobustus consistently predict the parasite load of any of the other species in the system and identify sources for heterogeneity that may account for the differences between the Black Sea and the Mediterranean system: habitat heterogeneity, bird diversity and host-parasite systems used to infer relationships between microphallids.

Keywords

Microphallid metacercariaeamphipodsGammarus insensibilisinterspecific associationsBlack Sea
Type
Research Article
Information
Parasitology , Volume 131 , Issue 3 , September 2005 , pp. 337 - 346
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bartoli, P. and Holmes, J. C. ( 1997). A transmission study of two sympatric digeneans: spatial constraints and solutions. Journal of the Helminthological Society of Washington 64, 169–175.Google Scholar
Belopol'skaya, M. M. ( 1957). [Larval trematode fauna of Gammarus locusta L. from the Baltic Sea.] Trudy Leningradskogo Obshchestva Estestvoispytateley 73, 164–170. (In Russian.)Google Scholar
Bush, A. O., Lafferty, 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, 575–583.CrossRefGoogle Scholar
Combes, C. ( 2001). Parasitism. The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago-London.
Deblock, S., Capron, A. and Rosé, F. ( 1961). Contribution à la connaissance des Microphallidae Travassos, 1920 (Trematoda). V. Le genre Maritrema Nicoll, 1907; cycle évolutif de M. subdolum Jägerskiöld, 1909. Parasitologia 3, 105–119.Google Scholar
Deslous-Paoli, J-M., Souchu, P., Mazouni, N., Juge, K. and Dagault, F. ( 1998). Relationship between environment and resources: impact of shellfish farming on a Mediterranean lagoon (Thau, France). Oceanologica Acta 21, 831–843.CrossRefGoogle Scholar
Georgiev, B. B., Biserkov, V. Y. and Genov, T. ( 1986). In toto staining method for cestodes in iron acetocarmine. Helminthologia 23, 279–281.Google 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, 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 tests de prédation. Annales de Parasitologie Humaine et Comparée 59, 41–56.CrossRefGoogle Scholar
Hust, J., Frydenberg, J., Sauriau, P.-G., Le Gall, P., Mouritsen, K. N. and Thomas Jensen, K. ( 2004). Use of ITS rDNA for discriminating of larval stages of two microphallid (Digenea) species using Hydrobia ulvae (Pennant, 1777) and Corophium volutator (Pallas, 1766) as intermediate hosts. Parasitology Research 93, 304–310.CrossRefGoogle Scholar
Janssen, H., Scheepmaker, M., van Couwelaar, M. and Pinkster, S. ( 1979). Biology and distribution of Gammarus aequicauda and G. insensibilis (Crustacea, Amphipoda) in the lagoon system of Bages-Sigean (France). Bijdragen tot de Dierkunde 48, 42–70.Google Scholar
Kesting, V., Gollasch, S. and Zander, C. D. ( 1996). Parasite communities of the Schlei Fjord (Baltic coast of northern Germany). Helgoländer Meeresuntersuchungen 50, 477–496.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, 37–45.CrossRefGoogle Scholar
Kuris, A. ( 1990). Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In Parasite communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. & Aho, J. M.). Chapman and Hall, London-New York.
Lafferty, K. D. ( 1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle Scholar
Lafferty, K. D., Thomas, F. and Poulin, R. ( 2000). Evolution of host phenotype manipulation by parasites and its consequences. In Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. & Scorping, A.). Elsevier Science, Amsterdam.
Latham, A. D. M. and Poulin, R. ( 2002). Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Marine Biology 141, 1131–1139.Google Scholar
Meissner, K. and Bick, A. ( 1997). Population dynamics and ecoparasitological surveys of Corophium volutator in coastal waters in the Bay of Mecklenburg (southern Baltic Sea). Diseases of Aquatic Organisms 29, 169–179.CrossRefGoogle Scholar
Meissner, K. and Bick, A. ( 1999). Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae) – laboratory studies. Diseases of Aquatic Organisms 35, 47–52.CrossRefGoogle Scholar
Michev, T. and Profirov, L. ( 2003). Mid-winter numbers of waterbirds in Bulgaria (1977–2001). Pensoft. Sofia-Moscow.Google Scholar
Mordvinova, T. N. ( 1978). [Microphallid metacercariae parasitising Black Sea crustaceans.] Biologiya Morya 45, 34–40. (In Russian.)Google Scholar
Mordvinova, T. N. ( 1985). [Helminth fauna of some crustaceans from the Black Sea.] Ekologiya Morya 20, 50–57. (In Russian.)Google Scholar
Mouritsen, K. N. ( 1997). Crawling behaviour in the bivalve Macoma balthica: the parasite-manipulation hypothesis revisited. Oikos 79, 513–520.CrossRefGoogle Scholar
Mouritsen, K. N. ( 2001). Hitch-hiking parasite: a dark horse may be the real rider. International Journal for Parasitology 31, 1417–1420.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, 123–134.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. ( 2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.CrossRefGoogle Scholar
Naidenova, N. N. and Mordvinova, T. N. ( 1985). The helminths and comensals of crustaceans of the Black Sea. In Parasitology and Pathology of Marine Organisms of the World Ocean (ed. Hargis, W. J., Jr). NOAA Technical Reports. NMFS, 25, pp. 123–127.
Norušis, M. J. ( 2002). SPSS® 11.0 Guide to Data Analysis. Prentice Hall Inc., New Jersey.
Outreman, Y., Bollache, L., Plaistow, S. and Cézilly, F. ( 2002). Patterns of intermediate host use and levels of association between two conflicting manipulative parasites. International Journal for Parasitology 32, 15–20.CrossRefGoogle Scholar
Poulin, R. ( 2002). Parasite manipulation of host behaviour. In The Behavioural Ecology of Parasites (ed. Lewis, E. E., Campbell, J. F. & Sukhdeo, M. V. K.). CAB International, Wallingford.CrossRef
Poulin, R., Steeper, M. J. and Miller, A. A. ( 2000). Non-random patterns of host use by the different parasite species exploiting a cockle population. Parasitology 121, 289–295.CrossRefGoogle Scholar
Rousset, F., Thomas, F., De Meeûs, T. and Renaud, F. ( 1996). Inference of parasite-induced host mortality from distributions of parasite load. Ecology 77, 2203–2211.CrossRefGoogle Scholar
Rózsa, L., Reiczigel, J. and Majoros, G. ( 2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 226–232.Google Scholar
Sokal, R. R. and Rohlf, F. J. ( 1981). Biometry. 2nd Edn. Freeman, NY.
Thomas, F., De Meeûs, T. and Renaud, F. ( 1996 a). Pattern of infection of Gammarus aequicauda (Amphipoda) with metacercariae of Levinseniella tridigitata (Trematoda: Microphallidae). Journal of the Helminthological Society of Washington 63, 8–11.Google Scholar
Thomas, F., Guldner, E. and Renaud, F. ( 2000). Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). Journal of Parasitology 86, 650–654.CrossRefGoogle Scholar
Thomas, F., Lambert, A., De Meeûs, T., Cézilly, F. and Renaud, F. ( 1995 a). Influence of Microphallus hoffmanni (Trematoda, Microphallidae) on the survival, sexual selection, and fecundity of Gammarus aequicauda (Amphipoda). Canadian Journal of Zoology 73, 1634–1639.Google Scholar
Thomas, F., Meté, K., Helluy, S., Santalla, F., Verneau, O., De Meeûs, T., Cézilly, F. and Renaud, F. ( 1997). Hitch-hiker parasites or how to benefit from the strategy of another parasite. Evolution 51, 1316–1318.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, 1059–1061.Google Scholar
Thomas, F. and Renaud, F. ( 2001). Microphallus papillorobustus (Trematoda): a review of its effects in lagoon ecosystems. Revue Écologie (Terre Vie) 56, 147–156.Google Scholar
Thomas, F., Renaud, F. and Cézilly, F. ( 1996 b). Assortative pairing by parasitic prevalence in Gammarus insensibilis (Amphipoda): patterns and processes. Animal Behaviour 52, 683–690.Google Scholar
Thomas, F., Renaud, F., Derothe, J. M., Lambert, A., De Meeûs, T. and Cézilly, F. ( 1995 c). Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite. Oecologia 104, 259–264.Google Scholar
Thomas, F., Renaud, F., Rousset, F., Cézilly, F. and De Meeûs, T. ( 1995 b). Differential mortality of two closely related species induced by one parasite. Proceedings of the Royal Society, B 260, 349–352.Google Scholar
Thomas, F., Verneau, O., Santalla, F., Cézilly, F. and Renaud, F. ( 1996 c). The influence of intensity of infection by a trematode parasite on the reproductive biology of Gammarus insensibilis (Amphipoda). International Journal for Parasitology 26, 1205–1209.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, 1–5.Google Scholar
Vasilev, V. P. and Mitrofanova, G. P. ( 1998). [Hydrology and hydrochemistry of the Pomorie lake.] Trudove na Instituta po Okeanologiya 2, 186–194. [In Bulgarian.]Google Scholar
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, 734–744.CrossRefGoogle Scholar