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Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence

Published online by Cambridge University Press:  06 January 2005

D. B. VIZOSO ,
S. LASS  and
D. EBERT
D. B. VIZOSO
Affiliation:
Département de Biologie, Unité d'Ecologie and Evolution, Université de Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland Present address: Institut für Zoologie und Limnologie, Abteilung Ultrastrukturforschung und Evolutionsbiologie, Universität Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria. E-mail: dita.vizoso@uibk.ac.at
S. LASS
Affiliation:
Département de Biologie, Unité d'Ecologie and Evolution, Université de Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland
D. EBERT
Affiliation:
Département de Biologie, Unité d'Ecologie and Evolution, Université de Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland
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Abstract

Periods of low host density impose a constraint on parasites with direct transmission, challenging their permanence in the system. The microsporidium Octosporea bayeri faces such constraint in a metapopulation of its host, the cladoceran Daphnia magna, where ponds frequently lose their host population due to ponds drying out in summer and freezing in winter. We conducted experiments aimed to investigate the mechanisms of transmission of O. bayeri, and discuss how these mechanisms could contribute to the parasite's permanence in the system. Spores accumulate in the fat cells and the ovaries of the host, and vary in morphology, possibly corresponding to 3 different spore types. Horizontal transmission occurred through the release of spores from dead hosts, with the proportion of infected hosts depending on the spore dose. Further, spores are able to persist outside the host both in dry and wet conditions. Vertical transmission occurred to both parthenogenetic and sexual offspring. The former were invariably infected, while the sexually produced resting eggs (=ephippia) had a less efficient transmission. The parasite may be carried by the ephippia, and thus disperse to new ponds together with the host. Together, these mechanisms may allow the parasite to endure periods of harsh environmental conditions both outside and inside the host.

Keywords

vertical and horizontal transmissionparasite permanencespore survivalmetapopulationOctosporea bayeriDaphnia magna
Type
Research Article
Information
Parasitology , Volume 130 , Issue 5 , May 2005 , pp. 501 - 509
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

AGNEW, P., BECNEL, J. J., EBERT, D. & MICHALAKIS, Y. ( 2002). Symbiosis of microsporidia and insects. In Insect Symbiosis (ed. Bourtzis, K.), pp. 145–163. CRC Press LLC, Florida.
ANDERSON, R. M. & MAY, R. M. ( 1978). Regulation and stability of host-parasite population interactions.1. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
ANDERSON, R. M. & MAY, R. M. ( 1981). The population dynamics of micro-parasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London, Series B 291, 451–524.CrossRefGoogle Scholar
ANDERSON, R. M. & MAY, R. M. ( 1986). The invasion, persistence and spread of infectious-diseases within animal and plant-communities. Philosophical Transactions of the Royal Society of London, Series B 314, 533–570.CrossRefGoogle Scholar
BECNEL, J. J. & ANDREADIS, T. G. ( 1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis (ed. Wittner, M. & Weiss, L. M.), pp. 447–501. American Society for Microbiology, Washington, D.C.CrossRef
BIGLIARDI, E. & SACCHI, L. ( 2001). Cell biology and invasion of the Microsporidia. Microbes and Infection 3, 373–379.CrossRefGoogle Scholar
BONHOEFFER, S., LENSKI, R. E. & EBERT, D. ( 1996). The curse of the pharaoh: The evolution of virulence in pathogens with long living propagules. Proceedings of the Royal Society of London, Series B 263, 715–721.CrossRefGoogle Scholar
BROOKS, W. M. ( 1988). Entomogenous protozoa. In CRC Handbook of Natural Pesticides. Microbial Insecticides, Part A: Entomogenous Protozoa and Fungi (ed. Ignoffo, C. M.), pp. 1–150. CRC Press, Boca Raton, Florida.
BULL, J. J., MOLINEUX, I. J. & RICE, W. R. ( 1991). Selection of benevolence in a host-parasite system. Evolution 45, 875–882.CrossRefGoogle Scholar
CANNING, E. ( 1982). An evaluation of protozoal characteristics in relation to biological control of pests. Parasitology 84, 119–149.CrossRefGoogle Scholar
CANNING, E. U., REFARDT, D., VOSSBRINCK, C. R., OKAMURA, B. & CURRY, A. ( 2002). New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). European Journal of Protistology 38, 247–265.CrossRefGoogle Scholar
DUNN, A. M. & SMITH, J. E. ( 2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381–388.CrossRefGoogle Scholar
EBERT, D. ( 1995). The ecological interactions between a microsporidian parasite and its host Daphnia magna. Journal of Animal Ecology 64, 361–369.CrossRefGoogle Scholar
EBERT, D., HOTTINGER, J. W. & PAJUNEN, V. I. ( 2001). Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82, 3417–3434.CrossRefGoogle Scholar
EBERT, D., ZSCHOKKE-ROHRINGER, C. D. & CARIUS, H. J. ( 1998). Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society of London, Series B 265, 2127–2134.CrossRefGoogle Scholar
FRANK, S. A. ( 1991). Ecological and genetic models of host-pathogen coevolution. Heredity 67, 73–83.CrossRefGoogle Scholar
FRANK, S. A. ( 1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.CrossRefGoogle Scholar
GATEHOUSE, H. S. & MALONE, L. A. ( 1998). The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. Journal of Invertebrate Pathology 71, 97–105.CrossRefGoogle Scholar
GREEN, J. ( 1957). Parasites and epibionts of Cladocera in rock pools of Tvärminne archipelago. Archivum Societatis Zoologicae Botanicae Fennicae “Vanamo” 12, 5–12.Google Scholar
GREEN, J. ( 1974). Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London 32, 417–515.CrossRefGoogle Scholar
HAAG, C. R., HOTTINGER, J. W., RIEK, M. & EBERT, D. ( 2002). Strong inbreeding depression in a Daphnia metapopulation. Evolution 56, 518–526.CrossRefGoogle Scholar
JÍROVEC, O. ( 1936). Über einige in Daphnia magna parasitierende Mikrosporidien. Zoologischer Anzeiger 116, 136–142.Google Scholar
KLEINBAUM, D. G., KUPPER, L. L., MULLER, K. E. & NIZAM, A. ( 1998). Applied regression Analysis and Other Multivariate Methods. Duxbury Press, Pacific Grove, CA.
KLÜTTGEN, B., DÜLMER, U., ENGELS, M. & RATTE, H. T. ( 1994). ADaM, an artificial freshwater for the culture of zooplankton. Water Research 28, 743–746.CrossRefGoogle Scholar
LUCAROTTI, C. J. & ANDREADIS, T. G. ( 1995). Reproductive strategies and adaptations for survival among obligatory microsporidian and fungal parasites of mosquitoes: a comparative analysis of Amblyospora and Coelomyces. Journal of the American Mosquito Control Association 11, 111–121.Google Scholar
MADDOX, J. V. ( 2002). Environmental persistence of Microsporidia. In Factors Affecting the Survival of Entomopathogens (ed. Baur, M. E. & Fuxa, J. R.). Southern Cooperative Series Bulletin 400. Available at: http://www.agctr.lsu.edu/s265/default.htm
ONSTAD, D. W., MADDOX, J. V., COX, D. J. & KORNKVEN, E. A. ( 1990). Spatial and temporal dynamics of animals and the host-density threshold in epizootiology. Journal of Invertebrate Pathology 55, 76–84.CrossRefGoogle Scholar
PAJUNEN, V. I. ( 1986). Distributional dynamics of Daphnia species in a rock-pool environment. Annales Zoologici Fennici 23, 131–140.Google Scholar
RANTA, E. ( 1979). Niche of Daphnia species in rock pools. Archiv für Hydrobiologie 87, 205–223.Google Scholar
REGOES, R. R., HOTTINGER, J. W., SYGNARSKI, L. & EBERT, D. ( 2003). The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiology and Infection 131, 957–966.CrossRefGoogle Scholar
SAUVAGE, F., LANGLAIS, M., YOCCOZ, N. G. & PONTIER, D. ( 2003). Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. Journal of Animal Ecology 72, 1–13.CrossRefGoogle Scholar
SMITH, J. E. & DUNN, A. M. ( 1991). Transovarial transmission. Parasitology Today 7, 146–148.CrossRefGoogle Scholar
VAN BAALEN, M. ( 2000). Parent-to-offspring infection and the struggle for transmission. In Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Moran, S. & Skorping, A.), pp. 97–116. Elsevier, Amsterdam.
VIZOSO, D. B. & EBERT, D. ( 2004). Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128, 31–38.CrossRefGoogle Scholar
ZHU, X., WITTNER, M., TANOWITZ, H. B., CALI, A. & WEISS, L. M. ( 1993). Nucleotide sequence of the small ribosomal RNA of Encephalitozoon cuniculi. Nucleic Acids Research 21, 1315.Google Scholar