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The cestode parasite Schistocephalus pungitii: castrator or nutrient thief of ninespine stickleback fish?

Published online by Cambridge University Press:  11 January 2017

DAVID C. HEINS*
Affiliation:
Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, LA 70118, USA
*
*Corresponding author: Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, LA 70118, USA. E-mail: heins@tulane.edu

Summary

In this investigation, the host–parasite relationship of ninespine stickleback fish Pungitius pungitius and the cestode parasite Schistocephalus pungitii was studied using samples from Dog Bone Lake, Kenai Peninsula, Alaska, to test the hypothesis that S. pungitii is a castrator of ninespine stickleback. Infected, adult females of all sizes (ages) were capable of producing clutches of eggs. S. pungitii had a negative effect on the ability of host females to produce a clutch, which was related to increasing parasite:host mass ratio (parasite index, PI). Among infected females with egg clutches, both clutch size and egg size were reduced; and the reduction increased with greater PI. The results of this study are consistent with the hypothesis that S. pungitii causes host sterility as a result of simple nutrient theft and is not a true castrator as hypothesized in earlier reports. The degree of parasite-induced sterility appears to vary among populations of the ninespine stickleback, perhaps reflecting differences in resource availability. Populations of ninespine stickleback appear to show a greater reduction in host reproductive capacity with PI than populations of the threespine stickleback infected by Schistocephalus solidus, possibly owing, in part, to the length-adjusted somatic mass of the threespine stickleback being greater.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Arme, C. and Owen, R. W. (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoids larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects. Parasitology 57, 301314.Google Scholar
Barber, I., Berkhout, B. W. and Ismail, Z. (2016). Thermal change and the dynamics of multi-host parasite life cycles in aquatic ecosystems. Integrative and Comparative Biology 56, 561572.Google Scholar
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335352.Google Scholar
Bråten, T. (1966). Host specificity in Schistocephalus solidus . Parasitology 56, 657664.Google Scholar
Christen, M. and Milinski, M. (2005). The optimal foraging strategy of its stickleback host constrains a parasite's complex life cycle. Behaviour 142, 979996.Google Scholar
Hacker, C. S. and Kilama, W. L. (1974). The relationship between Plasmodium gallinaceum density and the fecundity of Aedes aegypti . Journal of Invertebrate Pathology 23, 101105.Google Scholar
Hall, S. R., Becker, C. and Cáceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295309.Google Scholar
Heins, D. C. and Baker, J. A. (1993). Clutch production in the darter Etheostoma lynceum Hay and its implications for life-history study. Journal of Fish Biology 42, 819829.Google Scholar
Heins, D. C. and Baker, J. A. (2008). The stickleback-Schistocephalus host–parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625645.Google Scholar
Heins, D. C. and Baker, J. A. (2010). Castration of female ninespine stickleback by the pseudophyllidean cestode Schistocephalus pungitii: evolutionary significance and underlying mechanism. Journal of Parasitology 96, 206208.Google Scholar
Heins, D. C. and Ecke, J. K. (2012). The rise and fall of an epizootic of the diphyllobothriidean cestode Schistocephalus pungitii infecting the ninespine stickleback. Journal of Parasitology 98, 15.Google Scholar
Heins, D. C., Singer, S. S. and Baker, J. A. (1999). Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus . Canadian Journal of Zoology 77, 19671974.Google Scholar
Heins, D. C., Johnson, J. M. and Baker, J. A. (2003). Reproductive ecology of the ninespine stickleback from south-central Alaska. Journal of Fish Biology 63, 11311143.Google Scholar
Heins, D. C., Ulinski, B., Johnson, J. M. and Baker, J. A. (2004). Effect of the cestode macroparasite Schistocephalus pungitii on the reproductive success of ninespine stickleback, Pungitius pungitius . Canadian Journal of Zoology 82, 17311737.Google Scholar
Heins, D. C., Baker, J. A., Toups, M. A. and Birden, E. L. (2010). Evolutionary significance of fecundity reduction in threespine stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus . Biological Journal of the Linnean Society 100, 835846.Google Scholar
Heins, D. C., Baker, J. A. and Green, D. M. (2011). Processes influencing the duration and decline of an epizootic cycle in Schistocephalus solidus . Journal of Parasitology 97, 371376.Google Scholar
Heins, D. C., Eidam, D. M. and Baker, J. A. (2016). Timing of infections in the threespine stickleback (Gasterosteus aculeatus) by Schistocephalus solidus in Alaska. Journal of Parasitology 102, 286289.Google Scholar
Henrich, T. and Kalbe, M. (2016). The role of prezygotic isolation mechanisms in the divergence of two parasite species. BMC Evolutionary Biology 16, 245.Google Scholar
Hogg, J. C. and Hurd, H. (1995). Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111, 555562.Google Scholar
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.Google Scholar
Javadian, E. and MacDonald, W. W. (1974). The effect of infection with Brugia pahangi and Dirofilaria repens on the egg-production of Aedes aegypti . Annals of Tropical Medicine and Parasitology 68, 477481.Google Scholar
Kuris, A. M. (2003). Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89(Suppl.), S96S100.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507513.Google Scholar
Marcogliese, D. J. (2016). The distribution and abundance of parasites in aquatic ecosystems in a changing climate: more than just temperature. Integrative and Comparative Biology 56, 611619.Google Scholar
Newcombe, R. G. (1998). Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 17, 857872.Google Scholar
Nishimura, N., Heins, D. C., Andersen, R. O., Barber, I. and Cresko, W. A. (2011). Distinct lineages of Schistocephalus parasites in three-spined and ninespine stickleback hosts revealed by DNA sequence analysis. PLoS ONE 6, e22505.Google Scholar
Orr, T. S. C., Hopkins, C. A. and Charles, G. H. (1969). Host specificity and rejection of Schistocephalus solidus . Parasitology 59, 683690.Google Scholar
Renshaw, M. and Hurd, H. (1994). The effects of Onchocerca lienalis infection on vitellogenesis in the British blackfly, Simulium ornatum . Parasitology 109, 337343.Google Scholar
Schultz, E. T., Topper, M. and Heins, D. C. (2006). Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect? Oikos 114, 303310.Google Scholar
Smyth, J. D. (1962). Introduction to Animal Parasitology. C. C. Thomas, Springfield, Illinois, 470 p.Google Scholar
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1996). Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483493.Google Scholar
Wilson, E. B. (1927). Probable inference, the law of succession, and statistical inference. Journal of the American Statistical Association 22, 209212.Google Scholar
Woods, P. F. (1985). Limnology of Nine Small Lakes, Matanuska–Susitna Borough, Alaska, and the Survival and Growth Rates of Rainbow Trout. United States Geological Survey Water-Resources Investigations Report 85–4292. Geological Survey, United States Department of the Interior, Anchorage, Alaska, USA.Google Scholar
Wootton, R. J. (1994). Energy allocation in the threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback (ed. Bell, M. A. and Foster, S. A.), pp. 114143. Oxford University Press, Oxford, UK.Google Scholar