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Solo Schistocephalus solidus tapeworms are nasty

Published online by Cambridge University Press:  25 May 2016

JARLE TRYTI NORDEIDE  and
FELIPE MATOS
JARLE TRYTI NORDEIDE*
Affiliation:
Faculty of Biosciences and Aquaculture, Nord University, NO-8026 Bodø, Norway
FELIPE MATOS
Affiliation:
Faculty of Biosciences and Aquaculture, Nord University, NO-8026 Bodø, Norway
*
*Corresponding author. Nord University, Universitetsalléen 1, NO-8026 Bodø, Norway. E-mail: [email protected]
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Summary

Trophically transmitted parasites must trade-off own growth on one hand and energy drain from the intermediate host on the other hand, since killing the host before transmission to the next host is a dead end for both parasites and hosts. This challenge becomes especially intriguing when multiple parasites find themselves within the same individual host. The tapeworm Schistocephalus solidus may gain more than 98% of its final body mass within few months infecting its three-spined stickleback (Gasterosteus aculeatus) intermediate host. During these months the tapeworms may achieve a mass even larger than its host. We studied virulence of single and multiple infections of S. solidus, by comparing body condition of wild stickleback hosts in two perennial stickleback populations located at high latitudes, and each population was studied in two different years. Our results demonstrated multiple compared with single infections to be a highly significant predictor of the condition of stickleback hosts, with multiple-infected hosts having relatively higher body condition. However, this applied only after adjusting for parasite mass, which was another significant predictor for host condition. Thus, our results suggested that, at a given parasite mass, S. solidus was more harmful towards their host's body condition in single compared with multiple infections.

Keywords

Schistocephalus solidusGasterosteus aculeatussticklebackmultiple infectionsparasite–host interactionsparasite cooperationvirulence
Type
Research Article
Information
Parasitology , Volume 143 , Issue 10 , September 2016 , pp. 1301 - 1309
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Arme, C. and Owen, R. W. (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects. Parasitology 57, 301–314.CrossRefGoogle ScholarPubMed
Axelrod, R. and Hamilton, W. D. (1981). The evolution of cooperation. Science 211, 1390–1396.CrossRefGoogle ScholarPubMed
Barber, I. and Scharsack, J. P. (2010). The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137, 411–424.CrossRefGoogle ScholarPubMed
Bråten, T. (1966). Host specificity in Schistocephalus solidus . Parasitology 56, 657–664.Google Scholar
Christen, M. and Milinski, M. (2003). The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126, 369–378.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, 979–996.Google Scholar
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–77.Google Scholar
Grafen, A. and Hails, R. (2002). Modern Statistics for the Life Sciences. Oxford University Press, Oxford, UK.Google Scholar
Hafer, N. and Milinski, M. (2015). When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69, 611–620.Google Scholar
Hafer, N. and Milinski, M. (2016). An experimental conflict of interest between parasites reveals the mechanism of host manipulation. Behavioral Ecology 27, 617–627.Google Scholar
Hammerschmidt, K. and Kurtz, J. (2005). Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proceedings of the Royal Society B, Biological Sciences 272, 2511–2518.Google Scholar
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.Google Scholar
Hardin, G. (1968). Tragedy of the common. Science 162, 1243–1248.CrossRefGoogle 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.Google Scholar
Hopkins, C. A. and McCaig, M. L. O. (1963). Studies on Schistocephalus solidus. I. The correlation of development in the plerocercoid with infectivity to the definite host. Experimental Parasitology 13, 235–243.CrossRefGoogle Scholar
Jäger, I. and Schjørring, S. (2006). Multiple infections: relatedness and time between infections affect the establishment and growth of the cestoda Schistocephalus solidus in its stickleback host. Evolution 60, 616–622.Google Scholar
Jakob, E. M., Marshall, S. D. and Uetz, G. W. (1996). Estimating fitness: a comparison of body condition indices. Oikos 77, 61–67.CrossRefGoogle Scholar
Jakobsen, P. J., Johnsen, G. H. and Larsson, P. (1988). Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine threespine stickleback (Gasterosteus aculeatus). Canadian Journal of Fisheries and Aquatic Sciences 45, 426–431.Google Scholar
Koella, J. C., Rieu, L. and Paul, R. E. L. (2002). Stage-specific manipulation of a mosquito's host-seeking behavior by the malaria parasite Plasmodium gallinaceum . Behavioral Ecology 13, 816–820.CrossRefGoogle Scholar
Levri, E. P. (1998). The influence of non-host predators on parasite-induced behavioral changes in a freshwater snail. Oikos 81, 531–537.Google Scholar
Love, R. M. (1980). The Chemical Biology of Fishes, Vol. 2. Advances 1968–1977. Academic Press, London, UK.Google Scholar
McPhail, J. D. and Peacock, S. D. (1983). Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): evolutionary aspects of a host-parasite interaction. Canadian Journal of Zoology 61, 901–908.Google Scholar
Meakins, R. H. (1974). A quantitative approach to the effects of the plerocercoid of Schistocephalus solidus Muller 1776 on the ovarian maturation of the three-spined stickleback Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 44, 73–79.Google Scholar
Meakins, R. H. and Walkey, M. (1973). Aspects of in vivo growth of the plerocercoid stage of Schistocephalus solidus . Parasitology 67, 133–141.Google Scholar
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus . Evolutionary Ecology 20, 39–57.Google Scholar
Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 9, 203–216.Google Scholar
Orr, T. S. C. and Hopkins, C. A. (1969). Maintenance of Schistocephalus solidus in the laboratory with observations on rate of growth of, and proglottid formation in the plerocercoid. Journal of the Fisheries Research Board of Canada 26, 741–752.Google Scholar
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 47–54.Google Scholar
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448–458.Google Scholar
Pennycuick, L. (1971). Seasonal variations in parasite infections in a population of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 63, 373–388.Google Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites – From Individuals to Communities. Chapman & Hall, London, UK.Google Scholar
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.Google Scholar
Poulin, R. and Thomas, F. (1999). Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15, 28–32.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Scharer, L. and Wedekind, C. (1999). Lifetime reproductive output in a hermaphrodite cestode when reproducing alone or in pairs: a time cost of pairing. Evolutionary Ecology 13, 381–394.Google Scholar
Scharsack, J. P., Koch, K. and Hammerschmidt, K. (2007). Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society B, Biological Sciences 274, 3151–3158.Google Scholar
Smyth, J. D. (1946). Studies on tapeworm physiology I. The cultivation of Schistocephalus solidus in vitro . Journal of Experimental Biology 23, 47–70.Google Scholar
Smyth, J. D. (1994). Introduction to Animal Parasitology. Cambridge University Press, Cambridge, UK.Google Scholar
Tierney, J. F. and Crompton, D. W. T. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definite host, Gallus gallus . Journal of Parasitology 78, 1049–1054.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 Schistocphalus solidus infection. Journal of Fish Biology 49, 483–493.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.Google Scholar
Wedekind, C. and Milinski, M. (1996). Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? – An experimental analysis of behavioural resistance. Parasitology 112, 371–383.CrossRefGoogle Scholar
Wootton, R. J. (1976). The Biology of Sticklebacks. Academic Press, London, UK.Google Scholar
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