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Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus

Published online by Cambridge University Press:  10 June 2005

N. J. FIELDING ,
C. MacNEIL ,
N. ROBINSON ,
J. T. A. DICK ,
R. W. ELWOOD ,
R. S. TERRY ,
Z. RUIZ  and
A. M. DUNN
N. J. FIELDING
Affiliation:
School of Biology and Biochemistry, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, N. Ireland, UK
C. MacNEIL
Affiliation:
School of Biology and Biochemistry, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, N. Ireland, UK
N. ROBINSON
Affiliation:
School of Biology and Biochemistry, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, N. Ireland, UK
J. T. A. DICK
Affiliation:
School of Biology and Biochemistry, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, N. Ireland, UK
R. W. ELWOOD
Affiliation:
School of Biology and Biochemistry, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, N. Ireland, UK
R. S. TERRY
Affiliation:
Centre for Biodiversity and Conservation, School of Biology, University of Leeds, Leeds LS2 9JT, UK
Z. RUIZ
Affiliation:
Department of Geography, University of Exeter, Amory Building, Rennes Drive, Exeter EX4 4RJ, UK
A. M. DUNN
Affiliation:
Centre for Biodiversity and Conservation, School of Biology, University of Leeds, Leeds LS2 9JT, UK
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Abstract

The microsporidian parasite, Pleistophora mulleri, infects the abdominal muscle of the freshwater amphipod Gammarus duebeni celticus. We recently showed that P. mulleri infection was associated with G. d. celticus hosts being more vulnerable to predation by the invasive amphipod Gammarus pulex. Parasitized G. d. celticus also had a reduced ability to prey upon other co-occurring amphipods. We suggested the parasite may have pervasive influences on host ecology and behaviour. Here, we examine the association between P. mulleri parasitism and parameters influencing individual host fitness, behaviour and interspecific interactions. We also investigate the relationship between parasite prevalence and host population structure in the field. In our G. d. celticus study population, P. mulleri prevalence was strongly seasonal, ranging from 8·5% in summer to 44·9% in winter. The relative abundance of hosts with the heaviest parasite burden increased during summer, which coincided with high host mortality, suggesting that parasitism may regulate host abundance to some degree. Females were more likely to be parasitized than males and parasitized males were paired with smaller females than unparasitized males. Parasitism was associated with reduction in the host's activity level and reduced both its predation on the isopod Asellus aquaticus and aggression towards precopula pairs of the invasive G. pulex. We discuss the pervasive influence of this parasite on the ecology of its host.

Keywords

AmphipodGammarusisopodmicrosporidianPleistophora mulleritrophic
Type
Research Article
Information
Parasitology , Volume 131 , Issue 3 , September 2005 , pp. 331 - 336
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Andreadis, T. G. ( 2002). Epizootiology of Hyalinocysta chapmani (Microsporidia: Thelohaniidae) infections in field populations of Culiseta melanura (Diptera: Culicidae) and Orthocyclops modestus (Copepoda: Cyclopidae): a three-year investigation. Journal of Invertebrate Pathology 81, 114–121.CrossRefGoogle Scholar
Anonymous ( 1995). The Observer. Noldus Information Technology. Base Package for Windows, Version 3.0. Wageningen, The Netherlands.
Bjornson, S. and Keddie, B. A. ( 1999). Effects of Microsporidium phytoseiuli (Microsporidia) on the performance of the predatory mite, Phytoseiulus persimils (Acari: Phtytoseiidae). Biological Control 15, 153–161.CrossRefGoogle Scholar
Breed, G. M. and Olson, R. E. ( 1977). Biology of the microsporidian parasite Pleistophora crangoni n. sp. in three species of crangonid sand shrimps. Journal of Invertebrate Pathology 30, 387–405.Google Scholar
Cali, A. and Takvorian, P. M. ( 1991). The incidence of Glugea stephani (Protozoa: Microsporidia) in winter flounder, Pseudopleuronectes americanus, from the New York-New Jersey lower bay complex and factors influencing it. Canadian Journal of Zoology 69, 317–321.CrossRefGoogle Scholar
Chen, M. and Power, G. ( 1972). Infection of American smelt in Lake Ontario and Lake Erie with the microsporidian parasite Glugea hertwigi (Weissenberg). Canadian Journal of Zoology 50, 1183–1188.CrossRefGoogle Scholar
Dick, J. T. A., Elwood, R. W. and Montgomery, W. I. ( 1995). The behavioural basis of a species replacement: differential aggression and predation between the introduced Gammarus pulex and the native G. duebeni celticus (Amphipoda). Behavioural Ecology and Sociobiology 37, 393–398.CrossRefGoogle Scholar
Dick, J. T. A., Montgomery, W. I. and Elwood, R. W. ( 1993). Replacement of the indigenous amphipod Gammarus duebeni celticus by the introduced G. pulex: differential cannibalism and mutual predation. Journal of Animal Ecology 62, 79–88.Google Scholar
Dunn, A. M. and Smith, J. E. ( 2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381–388.CrossRefGoogle Scholar
Elwood, R. W., Gibson, J. and Neil, S. ( 1987). The amorous Gammarus: size assortative mating in G. pulex. Animal Behaviour 35, 1–6.CrossRefGoogle Scholar
Hanley, K. A., Vollmer, D. M. and Case, T. J. ( 1995). The distribution and prevalence of helminths, coccidian and blood parasites in 2 competing species of gecko – implications for apparent competition. Oecologia 102, 220–229.CrossRefGoogle Scholar
Keeling, P. J. and Fast, N. M. ( 2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56, 93–116.CrossRefGoogle Scholar
Kelly, D., Dick, J. T. A., Montgomery, W. I. and MacNeil, C. ( 2003). Differences in composition of macroinvertebrate communities with invasive and native Gammarus spp. (Crustacea: Amphipoda). Freshwater Biology 48, 306–315.Google Scholar
MacNeil, C., Dick, J. T. A. and Elwood, R. W. ( 1997). The trophic ecology of freshwater Gammarus (Crustacea: Amphipoda). Biological Reviews of the Cambridge Philosophical Society 74, 375–395.Google Scholar
MacNeil, C., Dick, J. T. A., Hatcher, M. J., Fielding, N. J., Hume, K. D. and Dunn, A. M. ( 2003 b). Parasite transmission and cannibalism in an amphipod (Crustacea). International Journal for Parasitology 33, 795–798.Google Scholar
MacNeil, C., Dick, J. T. A., Hatcher, M. J., Terry, R. S., Smith, J. E. and Dunn, A. M. ( 2003 a). Parasites mediate mutual predation between native and invasive species. Proceedings of the Royal Society of London, B 270, 1309–1314.Google Scholar
Minchella, D. J. and Scott, M. E. ( 1991). Parasitism: a cryptic determinant of animal community structure. Trends in Ecology and Evolution 6, 250–254.CrossRefGoogle Scholar
Prenter, J., MacNeil, C., Dick, J. T. A. and Dunn, A. M. ( 2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385–390.CrossRefGoogle Scholar
Price, P. W., Westloy, M. and Rice, B. ( 1988). Parasite-mediated competition: some predictions and tests. American Naturalist 131, 544–555.CrossRefGoogle Scholar
Ramasamy, P., Jaykumar, R. and Brennan, G. P. ( 2000). Muscle degeneration associated with cotton shrimp disease of Penaeus indicus. Journal of Fish Disease 23, 77–81.CrossRefGoogle Scholar
Schrag, S. J. and Rollinson, D. ( 1994). Effects of Schistosoma haematobium infection on reproductive success and male out-crossing ability in the simultaneous hermaphrodite Bulinus truncatus (Gastropoda: Planorbidae). Parasitology 108, 27–34.CrossRefGoogle Scholar
Terry, R. S., MacNeil, C., Dick, J. T. A., Smith, J. E. and Dunn, A. M. ( 2003). Resolution of a taxonomic conundrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895; Georgevitch 1929). Journal of Eukaryotic Microbiology 50, 266–274.CrossRefGoogle Scholar
Tompkins, D. M., White, A. R. and Boots, M. ( 2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters 6, 189–196.CrossRefGoogle Scholar
Weiss, L. M. ( 2001). Microsporidia: emerging pathogenic protists. Acta Tropica 78, 89–102.CrossRefGoogle Scholar