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Influence of the pseudophyllidean cestode Schistocephalus solidus on oocyte development in the threespine stickleback Gasterosteus aculeatus

Published online by Cambridge University Press:  04 February 2010

D. C. HEINS  and
N. J. BROWN-PETERSON
D. C. HEINS*
Affiliation:
Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, LA70118, USA
N. J. BROWN-PETERSON
Affiliation:
Department of Coastal Science, The University of Southern Mississippi, 703 East Beach Dr., Ocean Springs, MS39564, USA
*
*Corresponding author: Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, LA70118, USA. Tel: +504 865 5563. Fax: +504 862 8706. E-mail: [email protected]
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Summary

The objective of this study was to investigate the means by which Schistocephalus solidus might reduce annual fecundity in female threespine stickleback fish (Gasterosteus aculeatus) through processes of oocyte development. Histological examinations of specimens from one lake in Alaska in 2000 and 2001 were used to analyse the effects of S. solidus on recruitment of primary growth oocytes into vitellogenesis, atresia of vitellogenic oocytes, and the interspawning interval. The ratio of primary growth to late secondary growth (late vitellogenic) oocytes was significantly greater (P<0·01) among infected fish than uninfected ones in early-season samples from 2000 and 2001, revealing a decrease in recruitment of oocytes from primary growth into vitellogenic oocytes among infected females. The difference was marginally non-significant (P=0·087) in a mid-season sample from 2001 due to reductions in the entire pool of vitellogenic (early and late secondary growth) oocytes recruited prior to the spawning season in this determinate-fecundity species. Atresia among all vitellogenic oocytes was low and did not differ between infected and uninfected females. Histological estimations of the interspawning interval using post-ovulatory follicles showed no significant differences between infected and uninfected fish, suggesting that the number of spawnings in stickleback females each spawning season is unaffected by S. solidus infection. Thus, annual fecundity appears to be reduced only through recruitment of oocytes into vitellogenesis.

Keywords

threespine sticklebackSchistocephalus solidusoocyte recruitmentoocyte atresiaspawning frequencyinterspawning intervaldeterminate fecundityfecundity reduction
Type
Research Article
Information
Parasitology , Volume 137 , Issue 7 , June 2010 , pp. 1151 - 1158
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Ali, M. and Wootton, R. J. (1999). Effect of variable food levels on reproductive performance of breeding female three-spined sticklebacks. Journal of Fish Biology 55, 1040–1053. doi:10.1111/j.1095-8649.1999.tb00739.xGoogle Scholar
Arme, C. and Owen, R. W. (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology 57, 301–314.CrossRefGoogle ScholarPubMed
Bagamian, K. H., Heins, D. C. and Baker, J. A. (2004). Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64, 1568–1576. doi:10.1111/j.1095-8649.2004.44411.xCrossRefGoogle Scholar
Baker, J. A., Foster, S. A., Heins, D. C., Bell, M. A. and King, R. W. (1998). Variation in female life-history traits among Alaskan populations of the threespine stickleback, Gasterosteus aculeatus L. (Pisces: Gasterosteidae). Biological Journal of the Linnean Society 63, 141–159. doi:10.1111/j.1095-8312.1998.tb01643.xGoogle ScholarPubMed
Baker, J. A., Heins, D. C., Foster, S. A., and King, R. W. (2008). An overview of life-history variation in female threespine stickleback. Behaviour 145, 579–602.Google Scholar
Brown-Peterson, N. J., Lowerre-Barbieri, S. K., Macewicz, B. J., Saborido-Rey, F., Tomkiewicz, J. and Wyanski, D. M. (2007). An improved and simplified terminology for reproductive classification in fishes. Pre-print doc. doi: http://hdl.handle.net/10261/11844.Google Scholar
Brown-Peterson, N. J. and Heins, D. C. (2009). Interspawning interval of wild female three-spined stickleback Gasterosteus aculeatus in Alaska. Journal of Fish Biology 74, 2299–2312. doi:10.1111/j.1095-8649.2009.02237.xCrossRefGoogle ScholarPubMed
Field, A. (2005). Discovering Statistics Using SPSS, 2nd Edn.Sage Publications, London, UK.Google Scholar
Fletcher, D. A. (1984). Effects of food supply on egg quality and quantity in fishes. Ph.D. thesis. University of Wales, Aberystwyth, Wales, UK.Google Scholar
Fletcher, D. A. and Wootton, R. J. (1995). A hierarchical response to differences in ration size in the reproductive performance of female three-spined sticklebacks. Journal of Fish Biology 46, 657–668. doi:10.1111/j.1095-8649.1995.tb01102.xGoogle Scholar
Grier, H. J., Uribe-Aranzábel, M. C. and Patiño, R. (2009). The ovary, folliculogenesis, and oogenesis in teleosts. In Reproductive Biology and Phylogeny of Fishes (Agnathans and Bony Fishes) Vol. 8A (ed. Jamieson, B. G. M.), pp. 25–84. Science Publishers, Enfield, NH, USA.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, 295–309. doi:10.1093/icb/icm057CrossRefGoogle Scholar
Heins, D. C. and Baker, J. A. (2003). Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite. Journal of Parasitology 89, 1–6.CrossRefGoogle ScholarPubMed
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, 625–645.CrossRefGoogle Scholar
Heins, D. C. and Rabito, F. G. Jr. (1986). Spawning performance in North American minnows: direct evidence of the occurrence of multiple clutches in the genus Notropis. Journal of Fish Biology 28, 343–357. doi:10.1111/j.1095-8649.1986.tb05171.xCrossRefGoogle 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, 1967–1974.CrossRefGoogle Scholar
Hunter, J. R. and Macewicz, B. J. (1985). Measurement of spawning frequency in multiple spawning fishes. In An Egg Production Method for Estimating Spawning Biomass of Pelagic Fish: Application to the Northern Anchovy (Engraulis mordax) (ed. Lasker, R.), pp. 79–94. US Department of Commerce, NOAA Technical Report NMFS 36.Google Scholar
Hunter, J. R., Macewicz, B. J., Lo, C. H. and Kimbrell, C. A. (1992). Fecundity, spawning and maturity of female Dover sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fishery Bulletin 90, 101–128.Google Scholar
Jönsson, K. I. (1997). Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78, 57–66.CrossRefGoogle Scholar
Kuris, A. M. (2003). Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89, S96–S100.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507–513.CrossRefGoogle Scholar
Lester, R. J. G. (1971). The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. Canadian Journal of Zoology 49, 361–366.CrossRefGoogle Scholar
Meakins, R. H. and Walkey, M. (1975). The effects of parasitism by the plerocercoid of Schistocephalus solidus Muller 1776 (Pseudophyllidea) on the respiration of the three-spined stickleback Gasterosteus aculeatus L. Journal of Fish Biology 7, 817–824.CrossRefGoogle Scholar
Murua, H. and Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the north Atlantic. Journal of Northwest Atlantic Fisheries Science 33, 23–31.CrossRefGoogle Scholar
Pascoe, D. and Mattey, D. (1977). Dietary stress in parasitized and non-parasitized Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 51, 179–186.CrossRefGoogle Scholar
Patiño, R. and Sullivan, C. V. (2002). Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiology and Biochemistry 26, 57–70.CrossRefGoogle Scholar
Patiño, R. and Thomas, P. (1990). Effects of gonadotropin on ovarian intrafollicular processes during the development of oocyte maturational competence in a teleost, the Atlantic croaker: Evidence for two distinct stages of gonadogropic control of final oocyte maturation. Biology of Reproduction 43, 204–217.CrossRefGoogle Scholar
Poizat, G., Rosecchi, E. and Crivelli, A. (1999). Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks. Proceedings of the Royal Society of London, B 266, 1543–1548.CrossRefGoogle Scholar
Reger, R. D. and Updike, R. G. (1983). Upper Cook Inlet region and the Matanuska Valley. In Guidebook to Permafrost and Quaternary Geology along the Richardson and Glenn Highways between Fairbanks and Anchorage, Alaska. Proceedings of the Fourth International Conference on Permafrost, Fairbanks, Alaska, 18–22 July 1983 (ed. Pewe, T. L. and Reger, R. D.), pp. 185–263. Division of Geology and Geophysical Surveys, Department of Natural Resources, State of Alaska, Fairbanks, USA.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, 303–310.CrossRefGoogle Scholar
Sokal, R. R. and Rohlf, F. J. (1995). Biometry, 3rd Edn.W.H. Freeman and Co, New York, USA.Google Scholar
Sokolowska, E. and Kulczykowska, E. (2006). Annual reproductive cycle in two free living populations of three-spined stickleback (Gasterosteus aculeatus L.): patterns of ovarian and testicular development. Oceanologia 48, 103–124.Google Scholar
Walkey, M. and Meakins, R. H. (1970). An attempt to balance the energy budget of a host–parasite system. Journal of Fish Biology 2, 361–372.CrossRefGoogle Scholar
Wallace, R. A. and Selman, K. (1979). Physiological aspects of oogenesis in two species of sticklebacks, Gasterosteus aculeatus L. and Apeltes quadracus (Mitchill). Fisheries Biology 14, 551–564. doi: 10.1111/j.1095–8649.1979.tb03555.xCrossRefGoogle Scholar
Woods, P. F. (1985). Limnology of nine small lakes, Matanuska–Susitna Borough, Alaska, and the survival and growth rates of rainbow trout. US Geological Survey Water-Research Investigation Rep. 85-4292. US Department of the Interior, Anchorage, Alaska, USA.Google Scholar
Wootton, R. J. (1977). Effect of food limitation during the breeding season on the size, body components and egg production of female sticklebacks (Gasterosteus aculeatus). Journal of Animal Ecology 46, 823–834.CrossRefGoogle Scholar
Wootton, R. J. (1994). Energy allocation of the three-spined stickleback. In The Evolutionary Biology of the Threespine Stickleback (ed. Bell, M. A. and Foster, S. A.), pp. 133–143. Oxford University Press, Oxford, UK.Google Scholar