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Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: no apparent environmental effect

Published online by Cambridge University Press:  29 July 2008

C. LAGRUE  and
R. POULIN
C. LAGRUE*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Tel: +64 3 479 7964. Fax: +64 3 479 7584. E-mail: lagcl981@student.otago.ac.nz
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Summary

Parasites with complex life cycles have developed numerous and very diverse adaptations to increase the likelihood of completing this cycle. For example, some parasites can abbreviate their life cycles by skipping the definitive host and reproducing inside their intermediate host. The resulting shorter life cycle is clearly advantageous when definitive hosts are absent or rare. In species where life-cycle abbreviation is facultative, this strategy should be adopted in response to seasonally variable environmental conditions. The hermaphroditic trematode Coitocaecum parvum is able to mature precociously (progenesis), and produce eggs by selfing while still inside its amphipod second intermediate host. Several environmental factors such as fish definitive host density and water temperature are known to influence the life-history strategy adopted by laboratory raised C. parvum. Here we document the seasonal variation of environmental parameters and its association with the proportion of progenetic individuals in a parasite population in its natural environment. We found obvious seasonal patterns in both water temperature and C. parvum host densities. However, despite being temporally variable, the proportion of progenetic C. parvum individuals was not correlated with any single parameter. The results show that C. parvum life-history strategy is not as flexible as previously thought. It is possible that the parasite's natural environment contains so many layers of heterogeneity that C. parvum does not possess the ability to adjust its life-history strategy to accurately match the current conditions.

Keywords

abbreviated life cycleCoitocaecum parvumlife-history strategiescomplex life cycle
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 10 , September 2008 , pp. 1243 - 1251
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Barger, M. A. and Esch, G. W. (2000). Plagioporus sinitsini (Digenea: Opecoelidae): a one-host life cycle. Journal of Parasitology 86, 150–153.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Brown, S. P., Renaud, F., Guegan, J. F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.CrossRefGoogle 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, 172–181.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, USA.Google Scholar
Davies, S. J. and McKerrow, J. H. (2003). Developmental plasticity in schistosomes and other helminths. International Journal for Parasitology 33, 1277–1284.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483–489.CrossRefGoogle ScholarPubMed
Font, W. F. (1980). The effect of progenesis on the evolution of Alloglossidium (Trematoda, Plagiochiida, Macroderoididae). Acta Parasitologica Polonica 27, 173–183.Google Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2005). Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series 290, 109–117.CrossRefGoogle Scholar
Hansen, E. K. and Poulin, R. (2006). Spatial covariation between infection levels and intermediate host densities in two trematode species. Journal of Helminthology 80, 255–259.Google ScholarPubMed
Hay, K. B., Fredensborg, B. L. and Poulin, R. (2005). Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association, UK 85, 989–992.CrossRefGoogle Scholar
Holton, A. L. (1984 a). A redescription of Coitocaecum parvum Crowcroft, 1945 (Digenea: Allocreadiidae) from crustacean and fish hosts in Canterbury. New Zealand Journal of Zoology 11, 1–8.CrossRefGoogle Scholar
Holton, A. L. (1984 b). Progenesis as a mean of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowfton, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 63–70.Google Scholar
Kattel, G. R. and Closs, G. P. (2007). Spatial and seasonal variation in the fish community of a South Island, New Zealand coastal lake. New Zealand Journal of Marine and Freshwater Research 41, 1–11.CrossRefGoogle Scholar
Krist, A. C., Lively, C. M., Levri, E. P. and Jokela, J. (2000). Spatial variation in susceptibility to infection in a snail-trematode interaction. Parasitology 121, 395–401.CrossRefGoogle 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, 1189–1195.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 (in the Press), doi: 10.1016/j.ijpara.2008.04.006CrossRefGoogle ScholarPubMed
Lefebvre, F. and Poulin, R. (2005 a). Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes. Journal of Helminthology 79, 47–53.CrossRefGoogle ScholarPubMed
Lefebvre, F. and Poulin, R. (2005 b). Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 130, 587–605.CrossRefGoogle ScholarPubMed
Lefebvre, F. and Poulin, R. (2005 c). Alternative reproductive strategies in the progenetic trematode Coitocaecum parvum: comparison of selfing and mating worms. Journal of Parasitology 91, 93–98.CrossRefGoogle ScholarPubMed
Levri, E. P., Dillard, J. and Martin, T. (2005). Trematode infection correlates with shell shape and defence morphology in a freshwater snail. Parasitology 130, 699–708.CrossRefGoogle Scholar
MacFarlane, W. V. (1939). Life cycle of Coitocaecum anaspidis Hickman, a New Zealand digenetic trematode. Parasitology 31, 172–184.CrossRefGoogle Scholar
Marcogliese, D. J., Compagna, S., Bergeron, E. and McLaughlin, J. D. (2001). Population biology of eyeflukes in fish from a large fluvial ecosystem: the importance of gulls and habitat characteristics. Canadian Journal of Zoology 79, 1102–1113.CrossRefGoogle Scholar
McDowall, R. M. (1990). New Zealand Freshwater Fishes: a Natural History and Guide. Heinemann Reed MAF Publishing Group, Auckland, New Zealand.Google Scholar
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, 480–484.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623–630.CrossRefGoogle Scholar
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R. (2007). Evolutionnary Ecology of Parasites. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Poulin, R. and Cribb, T. H. (2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.CrossRefGoogle ScholarPubMed
Poulin, R. and Lefebvre, F. (2006). Alternative life-history and transmission strategies in a parasite: first come, first served? Parasitology 132, 135–141.CrossRefGoogle Scholar
Quinn, J. M., Steele, G. L., Hickey, C. W. and Vickers, M. L. (1994). Upper thermal tolerances of twelve New Zealand stream invertebrate species. New Zealand Journal of Marine and Freshwater Research 28, 391–397.CrossRefGoogle Scholar
Richardson, J., Toubée, J. A. T. and West, D. W. (1994). Thermal tolerance and preference of some native New Zealand freshwater fish. New Zealand Journal of Marine and Freshwater Research 28, 399–407.CrossRefGoogle Scholar
Rowe, D. K. (1994). Vertical segregation and seasonal changes in fish depth distributions between lakes of contrasting trophic status. Journal of Fish Biology 45, 787–800.CrossRefGoogle Scholar
Schallenberg, M. and Burns, C. W. (2003). A temperate, tidal lake-wetland complex-II. Water quality and implications for zooplankton community structure. New Zealand Journal of Marine and Freshwater Research 37, 429–447.CrossRefGoogle Scholar
Skirnisson, K., Galaktionov, K. V. and Kozminsky, E. V. (2004). Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. Journal of Parasitology 90, 50–59.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, 259–270.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390.CrossRefGoogle ScholarPubMed
Wang, C. L. and Thomas, F. (2002). Egg production by metacercariae of Microphallus papillorobustus: a reproductive insurance? Journal of Helminthology 76, 279–281.CrossRefGoogle ScholarPubMed
Wilhelm, F. M., Closs, G. P. and Burns, C. W. (2007). Seasonal diet and amphipod size selection of juvenile common bully, Gobiomorphus cotidianus, in a coastal New Zealand lake. Hydrobiologia 586, 303–312.CrossRefGoogle Scholar