Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T06:00:21.883Z Has data issue: false hasContentIssue false

Castrating parasites and colonial hosts

Published online by Cambridge University Press:  06 February 2012

H. HARTIKAINEN
Affiliation:
School of Biological Sciences, University of Reading, Whiteknights, Reading, Berkshire RG6 6BX, UK
B. OKAMURA*
Affiliation:
School of Biological Sciences, University of Reading, Whiteknights, Reading, Berkshire RG6 6BX, UK
*
*Corresponding author: Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK. Tel: +44 (0)2079 426631. Fax: +44 (0)2079 425054. E-mail: b.okamura@nhm.ac.uk

Summary

Trajectories of life-history traits such as growth and reproduction generally level off with age and increasing size. However, colonial animals may exhibit indefinite, exponential growth via modular iteration thus providing a long-lived host source for parasite exploitation. In addition, modular iteration entails a lack of germ line sequestration. Castration of such hosts by parasites may therefore be impermanent or precluded, unlike the general case for unitary animal hosts. Despite these intriguing correlates of coloniality, patterns of colonial host exploitation have not been well studied. We examined these patterns by characterizing the responses of a myxozoan endoparasite, Tetracapsuloides bryosalmonae, and its colonial bryozoan host, Fredericella sultana, to 3 different resource levels. We show that (1) the development of infectious stages nearly always castrates colonies regardless of host condition, (2) castration reduces partial mortality and (3) development of transmission stages is resource-mediated. Unlike familiar castrator-host systems, this system appears to be characterized by periodic rather than permanent castration. Periodic castration may be permitted by 2 key life history traits: developmental cycling of the parasite between quiescent (covert infections) and virulent infectious stages (overt infections) and the absence of germ line sequestration which allows host reproduction in between bouts of castration.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Alekseev, V. R., de Stasio, B. T. and Gilbert, J. J. (2007). Diapause in aquatic invertebrates: theory and human use. In Monographiae Biologicae, Vol. 84. Springer, Dordrecht, The Netherlands.Google Scholar
Anderson, C. L., Canning, E. U. and Okamura, B. (1999). Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 119, 555561.CrossRefGoogle ScholarPubMed
Baayen, R. H., Davidson, D. J. and Bates, D. M. (2008). Mixed-effects modelling with crossed random effects for subjects and items. Journal of Memory and Language 59, 390412.CrossRefGoogle Scholar
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335352.CrossRefGoogle ScholarPubMed
Blecha, F. (2000). Immune system response to stress. In The Biology of Animal Stress. Basic Principles and Implications for Animal Welfare (ed. Moberg, G. D. and Mench, J. A.), pp. 111119. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Bonds, M. H. (2006). Host life-history strategy explains pathogen-induced sterility. The American Naturalist 168, 281293.CrossRefGoogle ScholarPubMed
Canning, E. U., Curry, A., Feist, S. W., Longshaw, M. and Okamura, B. (2000). A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). Journal of Eukaryotic Microbiology 47, 456468.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 Diseases 25, 477482.CrossRefGoogle Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Diseases of Aquatic Organisms 45, 6168.CrossRefGoogle ScholarPubMed
Gay, M., Okamura, B. and de Kinkelin, P. (2001). Evidence that infectious stages of Tetracapsula bryosalmonae for rainbow trout Oncorhynchus mykiss are present throughout the year. Diseases of Aquatic Organisms 46, 3140.CrossRefGoogle ScholarPubMed
Grabner, D. S. and El-Matbouli, M. (2008). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Diseases of Aquatic Organisms 79, 133139.CrossRefGoogle ScholarPubMed
Hall, S. R., Knight, C. J., Becker, C. R., Duffy, M. A., Tessier, A. J. and Cáceres, C. E. (2009). Quality matters: resource quality for hosts and the timing of epidemics. Ecology Letters 12, 118128.CrossRefGoogle ScholarPubMed
Hartikainen, H., Johnes, P., Moncrieff, C. and Okamura, B. (2009). Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers. Freshwater Biology 54, 23202334.CrossRefGoogle Scholar
Hechinger, R. F., Lafferty, K. D., Mancini, F. T. III, Warner, R. R. and Kuris, A. M. (2009). How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology 23, 651667.CrossRefGoogle Scholar
Hill, S. L. L. and Okamura, B. (2007). Endoparasitism in colonial hosts: patterns and processes. Parasitology 134, 841852.CrossRefGoogle ScholarPubMed
Holland, J. W., Okamura, B., Hartikainen, H. and Secombes, C. J. (2010). A novel minicollagen gene links cnidarians and myxozoans. Proceedings of the Royal Society of London, B 278, 546553.Google ScholarPubMed
Hughes, T. P. and Jackson, J. B. C. (1980). Do corals lie about their age? Some demographic consequences of partial mortality, fission, and fusion. Science 209, 713715.CrossRefGoogle ScholarPubMed
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.CrossRefGoogle ScholarPubMed
Jimenez-Guri, E., Philippe, H., Okamura, B. and Holland, P. W. H. (2007). Buddenbrockia is a cnidarian worm. Science 317, 116118.CrossRefGoogle ScholarPubMed
Johnes, P. J. and Heathwaite, A. L. (1992). A procedure for the simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulphate microwave digestion. Water Research 26, 12811287.CrossRefGoogle Scholar
Jokela, J., Taskinen, J., Mutikainen, P. and Kopp, K. (2005). Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 108, 156164.CrossRefGoogle Scholar
Karlson, R. H. (1994). Recruitment and catastrophic mortality in Plumatella emarginata Allman. In Biology and Palaebiology of Bryozoans. Proceedings of the 9th International Bryozoology Association Conference (ed. Hayward, P. J., Ryland, J. S. and Taylor, P. P.), pp. 9396. Olsen and Olsen, Fredensborg, Swansea, Wales.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology & Evolution 17, 507513.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564572.CrossRefGoogle ScholarPubMed
Lom, J. and Dykova, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 136.CrossRefGoogle ScholarPubMed
Mano, R. (1964). The coelomic corpuscules and their origin in the freshwater bryozoan, Lophopodella carteri. Science Reports Tokyo Kyoiku Daigaku Section B 11, 211235.Google Scholar
Marker, A. F. H. (1994). Chlorophyll a, SCA Method Revision. PR395/3/A.Google Scholar
Morris, D. C., Morris, D. J. and Adams, A. (2002). Development of improved PCR to prevent false positives and false negatives in the detection of Tetracapsula bryosalmonae, the causative agent of proliferative kidney disease. Journal of Fish Diseases 25, 483490.CrossRefGoogle Scholar
Morris, D. and Adams, A. (2006 a). Proliferatice, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). Journal of Parasitology 92, 984989.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2006 b). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease, to the freshwater bryozoan Fredericella sultana. Parasitology 133, 701709.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2006 c). Trasmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371377.CrossRefGoogle Scholar
O'Keefe, K. and Antonovics, J. (2002). Paying by different rules: the evolution of virulence in strerilising pathogens. The American Naturalist 159, 597605.CrossRefGoogle Scholar
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. and Wahli, T. (2011). Proliferative kidney disease as an emerging disease: the importance of life cycle complexity and environmental change. Freshwater Biology 56, 735753.CrossRefGoogle Scholar
Poulin, R. (2010). Parasite manipulation of host behavior: An update and frequently asked questions. Advances in the Study of Behavior 41, 151186.CrossRefGoogle Scholar
Seppälä, O., Liljeroos, K., Karvonen, A. and Jokela, J. (2008). Host condition as a contraint for parasite reproduction. Oikos 117, 749753.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.CrossRefGoogle ScholarPubMed
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, 109121.CrossRefGoogle ScholarPubMed
Tops, S., Hartikainen, H. and Okamura, B. (2009). The effects of myxozoan infection and temperature on fitness of colonial hosts. International Journal for Parasitology 39, 10031010.CrossRefGoogle Scholar
Winnepenninckx, B., Backeljau, T. and De Wachter, R. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9, 407.Google ScholarPubMed
Wood, T. S. (1973). Colony development in species of Plumatella and Fredericella (Ectoprocta: Phylactolaemata). In Animal Colonies, Development and Function through Time (ed. Boardman, R. S., Cheetham, A. H. and Oliver, W. A. J.), pp. 395432. Dowden, Hutchinson and Ross, Stroudsburg, PA, USA.Google Scholar
Wood, T. S. and Okamura, B. (2005). A Key to the British and European freshwater Bryozoans with Ecological Notes. Freshwater Biological Association, Ambleside, UK.Google Scholar