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Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs?

Published online by Cambridge University Press:  18 July 2011

KRISTIN K. HERRMANN*
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
*
*Corresponding author: Tel: +64 3 479 5848. Fax: +64 3 479 7584. E-mail: [email protected]

Summary

Each transmission event in complex, multi-host life cycles create obstacles selecting for adaptations by trematodes. One such adaptation is life cycle abbreviation through progenesis, in which the trematode precociously matures and reproduces within the second intermediate host. Progenesis eliminates the need for the definitive host and increases the chance of life cycle completion. However, progenetic individuals face egg-dispersal challenges associated with reproducing within metacercarial cysts in the tissues or body cavity of the second intermediate host. Most progenetic species await host death for their eggs to be released into the environment. The present study investigated temporal variation of progenesis in Stegodexamene anguillae in one of its second intermediate fish hosts and the effect of the fish's reproductive cycle on progenesis. The study involved monthly sampling over 13 months at one locality. A greater proportion of individuals became progenetic in the gonads of female fish hosts. Additionally, progenesis of worms in the gonads was correlated with seasonal daylight and temperature changes, major factors controlling fish reproduction. Host spawning events are likely to be an avenue of egg dispersal for this progenetic species, with the adoption of progenesis being conditional on whether or not the parasite can benefit from fish spawning.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Bartoñ, K. (2009). MuMIn: multi-model inference. Available at http://r-forge.r-project.org/projects/mumin/.Google Scholar
Bates, D. and Maechler, M. (2009). lme4: Linear mixed-effects models using S4 classes. Available at http://CRAN.R-project.org/package=lme4.Google Scholar
Billard, R. and Breton, B. (1978). Rhythms of reproduction in teleost fish. In Rhythmic Activity of Fishes (ed. Thorpe, J. E.), pp. 3153. Academic Press, London, UK.Google Scholar
Bolger, T. and Connolly, P. L. (1989). The selection of suitable indices for the measurement and analysis of fish condition. Journal of Fish Biology 34, 171182.CrossRefGoogle Scholar
Bullough, W. S. (1939). A study of the reproductive cycle of the minnow in relation to the environment. Proceedings of the Zoological Society of London Series a-General and Experimental 109, 79102.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd Edn. Springer-Verlag, New York, USA.Google Scholar
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: Why add intermediate hosts? American Naturalist 162(2), 172181.CrossRefGoogle ScholarPubMed
Combes, C. (1991). Ethological aspects of parasite transmission. American Naturalist 138, 866880.CrossRefGoogle Scholar
Corkum, K. C. and Beckerdite, F. W. (1975). Observations on the life history of Alloglossidium macrobdellensis (Trematoda: Macroderoididae) from Macrobdella ditetra. (Hirudinea: Hirudinidae). American Midland Naturalist 93, 484491.CrossRefGoogle Scholar
Davies, B. and Bromage, N. (2002). The effects of fluctuating seasonal and constant water temperatures on the photoperiodic advancement of reproduction in female rainbow trout Oncorhynchus mykiss. Aquaculture 205, 183200.CrossRefGoogle Scholar
Escobedo, G., Roberts, C. W., Carrero, J. C. and Morales-Montor, J. (2005). Parasite regulation by host hormones: an old mechanism of host exploitation? Trends in Parasitology 21, 588593. doi: 10.1016/j.pt.2005.09.013.CrossRefGoogle ScholarPubMed
Herrmann, K. K. and Poulin, R. (2011). Life cycle truncation in a trematode: does higher temperature indicate shorter host longevity? International Journal for Parasitology 41, 697704.CrossRefGoogle Scholar
Hickman, V. V. (1934). On Coitocaecum anaspidis sp. nov., a trematode exhibiting progenesis in the fresh-water crustacean Anaspides tasmaniae Thomson. Parasitology 26, 121128.CrossRefGoogle Scholar
Holton, A. L. (1984). Progenesis as a means of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowcroft, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 6370.Google Scholar
Huber, M. and Bengtson, D. A. (1999). Effects of photoperiod and temperature on the regulation of the onset of maturation in the estuarine fish Menidia beryllina (Cope) (Atherinidae). Journal of Experimental Marine Biology and Ecology 240, 285302.CrossRefGoogle Scholar
Jeppesen, E., Lauridsen, T. L., Mitchell, S. F., Christoffersen, K. and Burns, C. W. (2000). Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients. Journal of Plankton Research 22, 951968.CrossRefGoogle Scholar
Kattel, G. R. (1999). Seasonal and diel dynamics of pelagic fish and zooplankton populations in a shallow lowland South Island coastal lake, New Zealand. MSc University of Otago, New Zealand.Google Scholar
Kearn, G. C. (1998). Parasitism and the Platyhelminths, 1st Edn. Chapman & Hall, London, UK and New York, USA.Google Scholar
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 11891195. doi: 10.1111/j.1420-9101.2006.01277.x.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2008). Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 14351444. doi: 10.1016/j.ijpara.2008.04.006.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2009). Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking? Journal of Evolutionary Biology 22(8), 17271738. doi: 10.1111/j.1420-9101.2009.01787.x.CrossRefGoogle ScholarPubMed
Lagrue, C., Poulin, R. and Keeney, D. B. (2009). Effects of clonality in multiple infections on the life-history strategy of the trematode Coitocaecum parvum in its amphipod intermediate host. Evolution 63, 14171426. doi: 10.1111/j.1558-5646.2009.00619.x.Google Scholar
Lefebvre, F. and Poulin, R. (2005). Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 130, 587605. doi: 10.1017/s0031182004007103.CrossRefGoogle ScholarPubMed
Macfarlane, W. V. (1951). The life cycle of Stegodexamene anguillae n. g., n. sp., an allocreadiid trematode from New Zealand. Parasitology 41, 110.CrossRefGoogle Scholar
Macfarlane, W. V. (1952). Bionomics of two trematode parasites of New Zealand eels. Journal of Parasitology 38, 391397.CrossRefGoogle ScholarPubMed
Macy, R. W. and Basch, P. F. (1972). Orthetrotrema monostomum gen. et sp. n., a progenetic trematode (Dicrocoeliidae) from dragonflies in Malaysia. Journal of Parasitology 58, 515518.CrossRefGoogle Scholar
McLaughlin, J. D., Marcogliese, D. J. and Kelly, J. (2006). Morphological, developmental and ecological evidence for a progenetic life cycle in Neochasmus (Digenea). Folia Parasitologica 53, 4452.CrossRefGoogle ScholarPubMed
Moore, J. (2002). Parasites and the Behavior of Animals, Oxford Press, Oxford, UK.CrossRefGoogle Scholar
Pampoulie, C., Lambert, A., Rosecchi, E., Crivelli, A. J., Bouchereau, J. L. and Morand, S. (2000). Host death: A necessary condition for the transmission of Aphalloides coelomicola Dollfus, Chabaud, and Golvan, 1957 (Digenea, Cryptogonimidae)? Journal of Parasitology 86, 416417.CrossRefGoogle Scholar
Pampoulie, C., Morand, S., Lambert, A., Rosecchi, E., Bouchereau, J. L. and Crivelli, A. J. (1999). Influence of the trematode Aphalloides coelomicola Dollfus, Chabaud and Golvan, 1957 on the fecundity and survival of Pomatoschistus microps (Kroyer, 1838) (Teleostei: Gobiidae). Parasitology 119, 6167.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480484. doi: 10.1038/nature02012.Google Scholar
Poulin, R. (1995). ‘‘Adaptive'’ changes in the behaviour of parasitized animals: A critical review. International Journal for Parasitology 25, 13711383.CrossRefGoogle ScholarPubMed
Poulin, R. (1997). Egg production in adult trematodes: adaptation or constraint? Parasitology 114, 195204.Google Scholar
Poulin, R. (2001). Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623630.CrossRefGoogle Scholar
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 28992903.Google Scholar
Poulin, R. (2007). Evolutionay Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R. and Cribb, T. H. (2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176183.CrossRefGoogle ScholarPubMed
Poulin, R. and Hamilton, W. J. (2000). Egg size variation as a function of environmental variability in parasitic trematodes. Canadian Journal of Zoology-Revue Canadienne De Zoologie 78, 564569.CrossRefGoogle Scholar
Poulin, R. and Lefebvre, F. (2006). Alternative life-history and transmission strategies in a parasite: first come, first served? Parasitology 132, 135141. doi: 10.1017/s003118200500870x.CrossRefGoogle Scholar
Prairie, Y. T. and Bird, D. F. (1989). Some misconceptions about the spurious correlation problem in the ecological literature. Oecologia 81, 285288.CrossRefGoogle ScholarPubMed
R Development Core Team. (2009). R: A language and environment for statistical computing. Version 2.11.2. Availiable at http://www.r-project.org. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Schallenberg, M. and Burns, C. W. (2003). A temperate, tidal lake-wetland complex-2. Water quality and implications for zooplankton community structure. New Zealand Journal of Marine and Freshwater Research 37, 429447.CrossRefGoogle Scholar
Siefert, R. E. (1968). Reproductive behavior, incubation, and mortality of eggs, and postlarval food selection in the white crappie. Transactions of the American Fisheries Society 97, 252259.CrossRefGoogle Scholar
Stephens, R. T. T. (1982). Reproduction, growth and mortality of the common bully, Gobiomorphus cotidianus McDowall, in a eutrophic New Zealand lake. Journal of Fish Biology 20, 259270.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