Hostname: page-component-745bb68f8f-kw2vx Total loading time: 0 Render date: 2025-01-23T20:43:34.578Z Has data issue: false hasContentIssue false
  • English
  • Français

Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus ? — an experimental analysis of behavioural resistance

Published online by Cambridge University Press:  06 April 2009

C. Wedekind  and
M. Milinski
C. Wedekind
Affiliation:
Abteilung Verhaltensökologie, Zoologisches Institut, Universität Bern, CH-3032 Hinterkappelen, Switzerland
M. Milinski
Affiliation:
Abteilung Verhaltensökologie, Zoologisches Institut, Universität Bern, CH-3032 Hinterkappelen, Switzerland
Get access Rights & Permissions [Opens in a new window]

Summary

Many parasites that use intermediate hosts are transmitted to the next host through predation. If the next host's fitness is strongly reduced by the parasite, it is under selection either to recognize and avoid infected intermediate hosts or to exclude that prey species from its diet when alternative prey are available. We investigated the predator-prey interaction between laboratory bred three-spined sticklebacks (Gasterosteus aculeatus), the second intermediate host of the cestode Schistocephalus solidus, from 2 parasitized and 1 unparasitized population, and different prey types: infected and uninfected copepods and size-matched Daphnia as alternative prey. Copepods with infective procercoids were more active, had a lower swimming ability and were easier to catch than uninfected controls. The sticklebacks preferred moving copepods. Therefore parasitized copepods were preferentially attacked and consumed. There was no effect of the sticklebacks' parent population being parasitized or not. The sticklebacks switched from Daphnia to (uninfected) copepods in the course of a hunting sequence; this switch occurred earlier in smaller fish. With this strategy the fish maximized their feeding rate: Daphnia were easier to catch than copepods but increasingly difficult to swallow when the stomach was filling up especially for smaller fish. However, there was no indication that sticklebacks from infected populations either consumed Daphnia rather than copepods or switched later in the hunting sequence to consuming copepods than fish from an uninfected population. Thus, sticklebacks did not avoid parasitized prey although S. solidus usually has a high prevalence and causes a strong fitness reduction in its stickleback host.

Keywords

Schistocephalus soliduscopepodGasterosteus aculeatusbehavioural changespredation riskoptimal dietpopulation
Type
Research Article
Information
Parasitology , Volume 112 , Issue 4 , April 1996 , pp. 371 - 383
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arme, C. & 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, 301–14.CrossRefGoogle ScholarPubMed
Bakker, T. C. M. (1986). Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study. Behaviour 98, 1–143.CrossRefGoogle Scholar
Berenbaum, M. R. & Zangerl, A. R. (1992). Genetics of physiological and behavioral resistance to host furanocoumarins in the parsnip webworm. Evolution 46, 1373–84.CrossRefGoogle ScholarPubMed
Chappell, L. H. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775–8.CrossRefGoogle Scholar
Chevassus, B. & Dorson, M. (1990). Genetics of resistance to disease in fishes. Aquaculture 85, 83–107.CrossRefGoogle Scholar
Combes, C. (1991). Ethological aspects of parasite transmission. The American Naturalist 138, 866–80.CrossRefGoogle Scholar
Cunningham, E. J., Tierney, J. F. & Huntingford, F. A. (1994). Effects of the cestode Schistocephalus solidus on food intake and foraging decisions in the three-spined stickleback, Gasterosteus aculeatus. Ethology 97, 65–75.CrossRefGoogle Scholar
Dawkins, R. (1990). Parasites, desiderata lists and the paradox of the organism. Parasitology 100, 63–73.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1988). The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology 63, 139–65.CrossRefGoogle ScholarPubMed
Emlen, J. M. (1966). The role of time and energy in food preference. The American Naturalist 100, 611–17.CrossRefGoogle Scholar
Giles, N. (1983). Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Animal Behaviour 31, 1192–4.CrossRefGoogle Scholar
Giles, N. (1987). Predation risk and reduced foraging activity in fish: experiments with parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L. Journal of Fish Biology 31, 37–44.CrossRefGoogle Scholar
Gill, A. B. & Hart, P. J. B. (1994). Feeding behaviour and prey choice of the three-spine stickleback: the interaction effects of prey size, fish size and stomach fullness. Animal Behaviour 47, 921–32.CrossRefGoogle Scholar
Hart, B. L. (1994). Behavioural defense against parasites: interaction with parasite invasiveness. Parasitology 109 (Suppl.), S139–S151.CrossRefGoogle ScholarPubMed
Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. & Wright, C. A.). Zoological Journal of the Linnean Society 51, 123–49.Google Scholar
Holmes, J. C. & Zohar, S. (1990). Pathology and host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 34–94. London: Taylor & Francis.Google Scholar
Hopkins, C. A. & Smyth, J. D. (1951). Notes on the morphology and life history of Schistocephalus solidus (Cestoda: Diphyllobothridae). Parasitology 41, 283–91.CrossRefGoogle Scholar
Hulscher, J. B. (1973). Burying-depth and trematode infection in Macoma balthica. Netherlands Journal of Sea Research 6, 141–56.CrossRefGoogle Scholar
Keymer, A. D., Crompton, D. W. T. & Sahakian, B. J. (1983). Parasite-induced learned taste aversion involving Nippostrongylus in rats. Parasitology 86, 455–60.CrossRefGoogle ScholarPubMed
Keymer, A. D. & Read, A. F. (1991). Behavioural ecology: the impact of parasitism. In Parasite-Host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschliman, A. & Bolis, L.), pp. 37–61. Oxford: Oxford University Press.CrossRefGoogle Scholar
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. The American Naturalist 140, 854–67.CrossRefGoogle Scholar
Lozano, G. A. (1991). Optimal foraging theory – a possible role for parasites. Oikos 60, 391–5.CrossRefGoogle Scholar
Macarthur, R. H. & Pianka, E. R. (1966). On optimal use of a patchy environment. The American Naturalist 100, 603–9.CrossRefGoogle Scholar
May, R. M. & Anderson, R. M. (1990). Parasite-host coevolution. Parasitology 100, 271–318.CrossRefGoogle ScholarPubMed
McPhail, J. D. & 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, 901–14.CrossRefGoogle Scholar
Meakins, R. H. (1974). A quantitative approach to the effects of the plerocercoid of Schistocephalus solidus Müller 1776 on the ovarian maturation of the three-spined stickleback Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 44, 73–9.CrossRefGoogle Scholar
Meakins, R. H. & Walkey, M. (1973). Aspects of in vivo growth of the plerocercoid stage of Schistocephalus solidus. Parasitology 67, 133–41.CrossRefGoogle ScholarPubMed
Milinski, M. (1984). Parasites determine a predator's optimal feeding strategy. Behavioral Ecology and Sociobiology 15, 35–7.CrossRefGoogle Scholar
Milinski, M. (1985). Risk of redation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93, 203–16.CrossRefGoogle Scholar
Milinski, M. (1990). Parasites and host decision-making. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 95–116. London: Taylor & Francis.Google Scholar
Milinski, M. & Barker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, London 344, 330–3.CrossRefGoogle Scholar
Milinski, M. & Heller, R. (1978). Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.). Nature, London 275, 642–4.CrossRefGoogle Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–16.CrossRefGoogle Scholar
Minchella, D. J. & Loverde, P. T. (1983). Laboratory comparison of the relative success of Biomphalaria glabrata stocks which are susceptible and insusceptible to infection with Schistosoma mansoni. Parasitology 86, 335–44.CrossRefGoogle ScholarPubMed
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000–15.CrossRefGoogle Scholar
Moore, J. (1984). Parasites that change the behavior of their host. Scientific American 250, 82–9.CrossRefGoogle Scholar
Moore, J. (1995). The behavior of parasitized animals. BioScience 45, 89–96.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1990). Phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 193–229. London: Taylor & Francis.Google Scholar
Orr, T. S. C. & Hopkins, C. A. (1969). Maintenance of Schistocephaltis solidus in the laboratory with observations on rate of growth of, and proglottid formation in, the plerocercoid. Journal of the Fisheries Research Board Canada 26, 741–52.CrossRefGoogle Scholar
Pascoe, D. & Mattey, D. (1977). Dietary stress in parasitized and non-parasitized Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 51, 179–86.CrossRefGoogle Scholar
Pasternak, A. F., Huntingford, F. A. & Crompton, D. W. T. (1995). Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110, 395–9.CrossRefGoogle ScholarPubMed
Pennycuick, L. (1971 a). Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus. Journal of Zoology 165, 143–62.CrossRefGoogle Scholar
Pennycuick, L. (1971 b). Differences in the parasite infections in three-spined sticklebacks (Gasterosteus aculeatus L.) of different sex, age and size. Parasitology 63, 407–18.CrossRefGoogle ScholarPubMed
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109 (Suppl.), S109–S118.CrossRefGoogle ScholarPubMed
Poulin, R., Curtis, M. A. & Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–71.CrossRefGoogle Scholar
Price, D. J. (1985). Genetics and susceptibility and resistance to disease in fishes. Journal of Fish Biology 26, 509–19.CrossRefGoogle Scholar
Ranta, E. (1995). Schistocephalus infestation improves prey-size selection by three-spined sticklebacks. Journal of Fish Biology 46, 156–8.CrossRefGoogle Scholar
Smyth, J. D. (1954). Studies on tapeworm physiology. VII. Fertilization of Schistocephalus solidus in vitro. Experimental Parasitology 3, 64–71.CrossRefGoogle ScholarPubMed
Smyth, J. D. (1985). Introduction to Animal Parasitology. London: Hodder and Stoughton.Google Scholar
Stephens, D. W. & Krebs, J. R. (1987). Foraging Theory. Princeton: University Press.CrossRefGoogle Scholar
Thompson, S. N. & Kavaliers, M. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109 (Suppl.), S119–S138.CrossRefGoogle ScholarPubMed
Threlfall, W. (1968). A mass die-off of three-spined sticklebacks (Gasterosteus aculeatus L.) caused by parasites. Canadian Journal of Zoology 46, 105–6.CrossRefGoogle ScholarPubMed
Tierney, J. F., Huntingford, F. A. & Crompton, D. W. T. (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–5.CrossRefGoogle Scholar
Toscanelli, B. (1992). Die Beutewahl von juvenilen Stichlingen (Gasterosteus aculeatus) unter dem Einfluss des Parasitierungsrisikos. Thesis, Universität Bern.Google Scholar
Urdal, K., Tierney, J. F. & Jakobsen, P. J. (1995). The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. Journal of Parasitology 81, 330–3.CrossRefGoogle Scholar
Walkey, M. & Meakins, R. H. (1970). An attempt to balance the energy budget of a host-parasite system. Journal of Fish Biology 2, 361–2.CrossRefGoogle Scholar
Yan, G., Stevens, L. & Schall, J. J. (1994). Behavioral changes in Tribolium beetles infected with a tapeworm, variation in effects between beetle species and among genetic strains. The American Naturalist 143, 830–47.CrossRefGoogle Scholar