Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-20T05:30:14.817Z Has data issue: false hasContentIssue false
  • English
  • Français

Endoparasitism in colonial hosts: patterns and processes

Published online by Cambridge University Press:  09 February 2007

S. L. L. HILL  and
B. OKAMURA
B. OKAMURA*
Affiliation:
School of Biological Sciences, University of Reading, Whiteknights, Reading RG6 6BX, UK
*
*Corresponding author. Tel: +44 (0)118 378 7059. Fax: +44 (0)118 931 0180. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study begins to redress our lack of knowledge of the interactions between colonial hosts and their parasites by focusing on a novel host-parasite system. Investigations of freshwater bryozoan populations revealed that infection by myxozoan parasites is widespread. Covert infections were detected in all 5 populations studied and were often at high prevalence while overt infections were observed in only 1. Infections were persistent in populations subject to temporal sampling. Negative effects of infection were identified but virulence was low. Infection did not induce mortality in the environmental conditions studied. However, the production of statoblasts (dormant propagules) was greatly reduced in bryozoans with overt infections in comparison to uninfected bryozoans. Overtly-infected bryozoans also grew more slowly and had low fission rates relative to colonies lacking overt infection. Bryozoans with covert infections were smaller than uninfected bryozoans. High levels of vertical transmission were achieved through colony fission and the infection of statoblasts. Increased fission rates may be a strategy for hosts to escape from parasites but the parasite can also exploit the fragmentation of colonial hosts to gain vertical transmission and dispersal. Our study provides evidence that opportunities and constraints for host-parasite co-evolution can be highly dependent on organismal body plans and that low virulence may be associated with exploitation of colonial hosts by endoparasites.

Keywords

bryozoansmyxozoansvertical transmissioncovert infectionovert infectionvirulence
Type
Research Article
Information
Parasitology , Volume 134 , Issue 6 , June 2007 , pp. 841 - 852
Copyright
Copyright © Cambridge University Press 2007

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

Ahmed, A. M. and Hurd, H. (2006). Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes and Infection 8, 308–315.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–426.CrossRefGoogle ScholarPubMed
Bedhomme, S., Agnew, P., Sidobre, C. and Michalakis, Y. (2004). Virulence reaction norms across a food gradient. Proceedings of the Royal Society of London, B 271, 739–744.CrossRefGoogle ScholarPubMed
Bradley, C. A. and Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8, 290–300.CrossRefGoogle Scholar
Bratton, J. H. (1991). Volume 3 – Invertebrates other than Insects. British Red Data Books. Joint Nature Conservation Committee.Google Scholar
Brown, M. J. F., Schmid-Hempel, R. and Schmid-Hempel, P. (2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72, 994–1002.CrossRefGoogle Scholar
Burden, J. P., Nixon, C. P., Hodgkinson, A. E., Possee, R. D., Sait, S. M., King, L. A. and Hails, R. S. (2003). Covert infections as a mechanism for long-term persistence of baculoviruses. Ecology Letters 6, 524–531. doi:10.1046/j.1461-0248.2003.00459.x.CrossRefGoogle Scholar
Canning, E. U., Tops, S. A., Curry, A., Wood, T. S. and Okamura, B. (2002). Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. Journal of Eukaryotic Microbiology 49, 280–295.CrossRefGoogle ScholarPubMed
Canning, E. U. and Okamura, B. (2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131.CrossRefGoogle ScholarPubMed
de Kinkelin, P., Gay, M. and Forman, S. (2002). The persistence of infectivity of Tetracapsula bryosalmonae-infected water for rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Disease 25, 477–482.CrossRefGoogle Scholar
Decaestecker, E., De Meester, L. and Ebert, D. (2002). In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proceedings of the National Academy of Sciences, USA 99, 5481–5485.CrossRefGoogle ScholarPubMed
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of Proliferative Kidney Disease (PKD) in rainbow trout (Oncorhynchus mykiss Richardson) via the bryozoan Fredericella sultana (Blumenbach, 1779), infected with Tetracapsula bryosalmonae Canning, Curry, Feist, Longshaw & Okamura, 1999. Diseases of Aquatic Organisms 45, 61–68.CrossRefGoogle Scholar
Fellowes, M. D. E., Kraaijeveld, A. R. and Godfray, H. C. J. (1998). Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society of London, B 265, 1553–1558.CrossRefGoogle ScholarPubMed
Figuerola, J., Green, A. J., Black, K. and Okamura, B. (2003 a). Influence of gut morphology on passive transport of freshwater bryozoans by waterfowl in Doñana (southwestern Spain). Canadian Journal of Zoology 82, 835–840.CrossRefGoogle Scholar
Figuerola, J., Green, A. J. and Santamaría, L. (2003 b). Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Global Ecology and Biogeography 12, 427–436.CrossRefGoogle Scholar
Fox, A. and Hudson, P. J. (2001). Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus). Ecology Letters 4, 139–143.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2006). Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology 75, 44–53.CrossRefGoogle Scholar
Freeland, J. R., Noble, L. R. and Okamura, B. (2000). Genetic consequences of the metapopulation biology of a facultatively sexual freshwater invertebrate. Journal of Evolutionary Biology 13, 383–395.CrossRefGoogle Scholar
Furla, P., Allemand, D., Schick, M. J., Ferrier-Pagès, C., Richier, S., Plantivaux, A., Merle, P.-L. and Tambutté, S. (2005). The symbiotic anthozoan: a physiological chimera between alga and animal. Integrative and Comparative Biology 45, 595–604.CrossRefGoogle ScholarPubMed
Herre, E. A. (1995). Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111 (Suppl.), S179–S191.CrossRefGoogle Scholar
Herre, E. A., Knowlton, N., Mueller, U. G. and Rehner, S. A. (1999). The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends in Ecology and Evolution 14, 49–53.CrossRefGoogle ScholarPubMed
Hirose, E., Maruyama, T., Cheng, L. and Lewin, R. A. (1996). Intracellular symbiosis of a photosynthetic prokaryote, Prochloron, in a colonial ascidian. Invertebrate Biology 115, 343–348.CrossRefGoogle Scholar
Jackson, J. B. C. and Coates, A. G. (1986). Life cycles and evolution of clonal (modular) animals. Philosophical Transactions of the Royal Society of London, B 313, 7–22.Google Scholar
Jacot, A., Scheuber, H., Kurtz, J. and Brinkhof, M. W. G. (2005). Juvenile immune system activation induces a costly upregulation of adult immunity in field crickets Gryllus campestris. Proceedings of the Royal Society of London, B 272, 63–69.Google ScholarPubMed
Kim, K. and Harvell, C. D. (2004). The rise and fall of a six-year coral-fungal epizootic. The American Naturalist 164 (Suppl.), S52–S63.CrossRefGoogle ScholarPubMed
Lion, S., van Baalen, M. and Wilson, W. G. (2006). The evolution of parasite manipulation of host dispersal. Proceedings of the Royal Society of London, B 273, 1063–1071.Google ScholarPubMed
Maldonaldo, M., Cortadellas, N., Trillas, M. I. and Rützler, K. (2005). Endosymbiotic yeast maternally transmitted in a marine sponge. Biological Bulletin 209, 94–106.CrossRefGoogle Scholar
Mano, R. (1964). The coelomic corpuscles and their origin in the freshwater bryozoan, Lophopodella carteri. Science Reports. Tokyo Kyoiku Daigaku. Section B 11, 211–235.Google Scholar
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London, B 219, 281–313.Google ScholarPubMed
McGovern, T. M. and Hellberg, M. E. (2003). Cryptic species, cryptic endosymbionts, and geographical variation in chemical defenses in the bryozoan Bugula neritina. Molecular Ecology 12, 1207–1215.CrossRefGoogle ScholarPubMed
McGurk, C., Morris, D. J., Auchinachie, N. A. and Adams, A. (2006). Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss). Veterinary Parasitology 135, 249–257.CrossRefGoogle ScholarPubMed
Moret, Y. and Schmid-Hempel, P. (2001). Immune defence in bumble-bee offspring. Nature, London 414, 506.CrossRefGoogle ScholarPubMed
Morris, D. J. and Adams, A. (2006). Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371–377.CrossRefGoogle ScholarPubMed
Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behavioural Ecology 11, 19–26.CrossRefGoogle Scholar
Okamura, B. and Canning, E. U. (2003). Orphan worms and homeless parasites: Biodiversity and evolution of the obscure. Trends in Ecology and Evolution 18, 633–639.CrossRefGoogle Scholar
Okamura, B. and Hatton-Ellis, T. (1995). Population biology of freshwater bryozoans: correlates of sessile, colonial life histories in freshwater habitats. In Population Biology of Freshwater Invertebrates. Experientia 51, 510–525.Google Scholar
Sachs, J. L. and Wilcox, T. P. (2006). A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proceedings of the Royal Society of London, B 273, 425–429.Google ScholarPubMed
Tops, S. (2004). Ecology, life history and diversity of malacosporeans. Ph.D. dissertation, The University of Reading, Reading, UK.Google Scholar
Tops, S., Baxa, D. V., McDowell, T. S., Hedrick, R. P. and Okamura, B. (2004). Evaluation of malacosporean life cycles through transmission studies. Diseases of Aquatic Organisms 60, 109–121.CrossRefGoogle ScholarPubMed
Tops, S., Curry, A. and Okamura, B. (2005). Diversity and systematics of the Malacosporea (Myxozoa). Invertebrate Biology 124, 285–295.CrossRefGoogle Scholar
Tops, S., Lockwood, W. and Okamura, B. (2006). Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Diseases of Aquatic Organisms 70, 227–236.CrossRefGoogle ScholarPubMed
Tops, S. and Okamura, B. (2003). Infection of bryozoans by Tetracapsuloides bryosalmonae in sites endemic for salmonid proliferative kidney disease. Diseases of Aquatic Organisms 31, 221–226.CrossRefGoogle Scholar
Vizoso, D. B. and Ebert, D. (2005). Phenotypic plasticity of host-parasite interactions in response to the route of infection. Journal of Evolutionary Biology 18, 911–921.CrossRefGoogle Scholar
Vizoso, D. B., Lass, S. and Ebert, D. (2005). Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 130, 501–509.CrossRefGoogle ScholarPubMed
Webster, J. P. and Woolhouse, M. E. J. (1999). Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proceedings of the Royal Society of London, B 266, 391–396.CrossRefGoogle Scholar
Wood, T. S. (1996). Aquarium culture of freshwater invertebrates. The American Biology Teacher 58, 46–50.CrossRefGoogle Scholar
Wood, T. S. and Okamura, B. (2005). A new key to the freshwater bryozoans of Britain, Ireland and Continental Europe, with notes on their ecology. Freshwater Biological Association, The Ferry House, Far Sawrey, Ambleside, Cumbria, UK.Google Scholar