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The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves?

  • Population Ecology
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An Erratum to this article was published on 09 December 2004

Abstract

The role of parasites in influencing the trophic dynamics of hosts is becoming increasingly recognized in the ecological literature. Echinococcus granulosus is a tapeworm that relies on the predator-prey relationship between the definitive host (wolf, Canis lupus) and the intermediate host, (moose, Alces alces) to complete its life cycle. Heavy infection by E. granulosus may predispose moose to increased risk of predation by wolves. Theory predicts that parasite-induced vulnerability to predation will reduce the degree of aggregation of parasites in a host population. We tested for different levels of aggregation of E. granulosus in moose in areas of low, moderate, and high levels of wolf predation using Green’s coefficient of dispersion. Parasite aggregation was lower in an area with high predation rate, thus we hypothesize that heavy infection by E. granulosus predisposes moose to predation by wolves. This increase in predation rate due to parasite infection may influence the role of wolves in regulating moose populations. We discuss alternative explanations for the negative correlation between predation rate and parasite aggregation.

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References

  • Adjei EL, Barnes A, Lester RJG (1986) A method for estimating possible parasite-related host mortality illustrated using data from Callitetrarhynchus gracilis (Cestoda: Trypanorhyncha) in lizardfish (Saurida spp.). Parasitology 92:227–243

    Google Scholar 

  • Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398

    PubMed  Google Scholar 

  • Boutin S (1992) Predation and moose population dynamics: a critique. J Wildl Manage 56:116–127

    Google Scholar 

  • Crête M, Rivest L-P, Jolicoeur H, Brassard J-M, Messier F (1986) Predicting and correcting helicopter counts of moose with observations made from fixed-wing aircraft in southern Québec. J Appl Ecol 23:751–761

    Google Scholar 

  • Gasaway WC, Boertje RD, Grangaard DV, Kelleyhouse DG, Stephenson RO, Larsen DG (1992) The role of predation in limiting moose at low densities in Alaska and Yukon and implications for conservation. Wildl Monogr 120

  • Gordon DM, Rau ME (1982) Possible evidence for mortality induced by the parasite Apatemon gracilis in a population of brook sticklebacks (Culaea inconstans). Parasitology 84:41–47

    Google Scholar 

  • Gray DR (1993) The use of muskox kill sites as temporary rendezvous sites by arctic wolves with pups in early winter. Arctic 46:324–330

    Google Scholar 

  • Green RH (1966) Measurement of non-randomness in spatial distributions. Res Popul Ecol 8:1–7

    Google Scholar 

  • Hadeler KP, Freedman HI (1989) Predator-prey populations with parasitic infection. J Math Biol 27:609–631

    CAS  PubMed  Google Scholar 

  • Hayes RD, Harestad AS (2000) Wolf functional response and regulation of moose in the Yukon. Can J Zool 78:60–66

    Article  Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61:681–692

    Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Google Scholar 

  • Ives AR, Murray DL (1997) Can sublethal parasitism destabilize predator-prey population dynamics? A model of snowshoe hares, predators and parasites. J Anim Ecol 66:265–278

    Google Scholar 

  • Janovy J Jr, Kutish GW (1998) A model of encounters between host and parasite populations. J Theor Biol 134:391–401

    Google Scholar 

  • Joly DO, Patterson BR (2003) Use of selection indices to model the functional response of predators. Ecology 84:1635–1639

    Google Scholar 

  • Keymer AE, Anderson RM (1979) The dynamics of infection of Trilobium confusum by Hymenolepis diminuta: the influence of infective-stage density and spatial distribution. Parasitology 79:195–207

    CAS  PubMed  Google Scholar 

  • Krebs CJ (1999) Ecological methodology, 2nd edn. Harper Collins, New York

  • Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115

    Article  CAS  PubMed  Google Scholar 

  • McNeill MA, Rau ME (1987) Echinococcus granulosus (Cestoda: Taeniidae) infections in moose (Alces alces) from southwestern Québec. J Wildl Dis 23:418–421

    CAS  PubMed  Google Scholar 

  • Mech LD (1970) The wolf: the ecology and behavior of an endangered species. Natural History Press, New York

    Google Scholar 

  • Messier F (1985a) Social organization, spatial distribution, and population density of wolves in relation to moose density. Can J Zool 63:1068–1077

    Google Scholar 

  • Messier F (1985b) Solitary living and extraterritorial movements of wolves in relation to social status and prey abundance. Can J Zool 63:239–245

    Google Scholar 

  • Messier F (1994) Ungulate population models with predation: a case study with the North American moose. Ecology 75:478–488

    Google Scholar 

  • Messier F (1996) On the functional and numerical responses of wolves to changing prey density. In: Carbyn LN, Fritts SH, Seip DR (eds) Ecology and conservation of wolves in a changing world. University of Alberta Press, Edmonton, pp 187–197

  • Messier F, Crête M (1985) Moose-wolf dynamics and the natural regulation of moose populations. Oecologia 65:503–312

    Google Scholar 

  • Messier F, Joly DO (2000) Comment: the regulation of moose density by wolf predation. Can J Zool 78:506–510

    Article  Google Scholar 

  • Messier F, Rau ME, McNeill MA (1989) Echinococcus granulosus (Cestoda: Taeniidae) infections and moose-wolf population dynamics in southwestern Québec. Can J Zool 67:216–219

    Google Scholar 

  • Murray DL, Cary JR, Keith LB (1997) Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. J Anim Ecol 66:250–264

    Google Scholar 

  • Myers JH (1978) Selecting a measure of dispersion. Environ Entomol 7:619–621

    Google Scholar 

  • Pennycuick L (1971) Frequency distributions of parasites in a population of three-spined sticklebacks, Gasterosteus aculeatus L., with particular reference to the negative binomial distribution. Parasitology 63:389–406

    CAS  PubMed  Google Scholar 

  • Peterson RO (1977) Wolf ecology and prey relationships on Isle Royale. National Park Service Science Monograph no. 11, Washington, D.C.

  • Post E, Peterson RO, Stenseth NC, McLaren BE (1999) Ecosystem consequences of wolf behavioural response to climate. Nature 410:905–907

    Article  Google Scholar 

  • Rau ME, Caron FR (1979) Parasite-induced susceptibility of moose to hunting. Can J Zool 57:2466–2468

    Google Scholar 

  • Rausch RL (1995) Life cycle patterns and geographic distribution of Echinococcus species. In: Thompson RCA , Lymbery AJ (eds) Echinococcus and hydatid disease. CAB International, Wallingford, pp 90–134

  • Rousset F, Thomas F, De Meeûs T, Renaud F (1996) Inference of parasite-induced host mortality from distributions of parasite loads. Ecology 77:2203–2211

    Google Scholar 

  • Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111(Suppl):S111–S133

    PubMed  Google Scholar 

  • Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597–610

    Article  PubMed  Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill, New York

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York

  • Thompson RCA (1995) Biology and systematics of Echinococcus. In: Thompson RCA , Lymbery AJ (eds) Echinococcus and hydatid disease. CAB International, Wallingford, pp 1–37

  • Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313

    Article  CAS  PubMed  Google Scholar 

  • Van Ballenberghe V, Ballard WB (1994) Limitation and regulation of moose populations: the role of predation. Can J Zool 72:2071–2077

    Google Scholar 

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Acknowledgements

This manuscript was improved by comments from C. Osenberg, K. Lafferty, S. Ferguson, D. Gummer, T. Armstrong and B. Patterson and an anonymous reviewer. We are grateful to A. Plante for technical support. Financial support for the original study was provided by the Canadian National Sportmen’s Shows, the Natural Sciences and Engineering Research Council of Canada (NSERC), and the Ministère du Loisir, de la Chasse et de la Pêche du Québec. Damien O. Joly was supported by the University of Saskatchewan and Natural Sciences and Engineering Research Council of Canada and subsequently the USGS-National Wildlife Health Center.

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  1. Damien O. Joly

    Present address: Department of Wildlife Ecology, University of Wisconsin-Madison, 207 Russell Laboratory, 1630 Linden Drive, Madison, WI, 53711, USA

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  1. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, Canada, S7N 5E2

    Damien O. Joly & François Messier

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  1. Damien O. Joly
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  2. François Messier
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Correspondence to Damien O. Joly.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00442-004-1802-1

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Joly, D.O., Messier, F. The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves?. Oecologia 140, 586–590 (2004). https://doi.org/10.1007/s00442-004-1633-0

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