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Implications of increased susceptibility to predation for managing the sylvatic cycle of Echinococcus multilocularis

Published online by Cambridge University Press:  03 February 2006

M. VERVAEKE ,
S. DAVIS ,
H. LEIRS  and
R. VERHAGEN
M. VERVAEKE
Affiliation:
University of Antwerp, Department of Biology, Evolutionary Biology Group, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
S. DAVIS
Affiliation:
University of Antwerp, Department of Biology, Evolutionary Biology Group, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
H. LEIRS
Affiliation:
University of Antwerp, Department of Biology, Evolutionary Biology Group, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
R. VERHAGEN
Affiliation:
University of Antwerp, Department of Biology, Evolutionary Biology Group, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
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Abstract

The ability to increase the chances that infectious prey are taken by predators is an observed feature of many parasites that rely on one or more predator-prey relationships to complete their life-cycle. In the sylvatic life-cycle of Echinococcus multilocularis – the causative agent of human alveolar echinococcosis – foxes are the final host, with voles acting as intermediate hosts. Here we review the evidence that E. multilocularis causes increased susceptibility to predation and present a general mathematical model for the sylvatic life-cycle. The ability to increase susceptibility to predation in the intermediate host reduces the sensitivity of the parasite population to adverse conditions. For example, there is no critical density of foxes below which the parasite is expected to die out, even if the effect of the parasite on infected prey is very small. We suggest that increased susceptibility to predation is a plausible explanation for the observed resilience of E. multilocularis during and following field trials of praziquantel baiting.

Keywords

Echinococcosismathematical modelwildlife managementpredator-prey relationship
Type
Research Article
Information
Parasitology , Volume 132 , Issue 6 , June 2006 , pp. 893 - 901
Copyright
2006 Cambridge University Press

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References

REFERENCES

Artois, M. ( 1997). Managing problem wildlife in the ‘Old World’: a veterinary perspective. Reproduction and Fertility Development 9, 17–25.CrossRefGoogle Scholar
Begon, M., Bennett, M., Bowers, R. G., French, N. P., Hazel, S. M. and Turner, J. ( 2002). A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiology and Infection 129, 147–153.CrossRefGoogle Scholar
Crowden, A. E. and Broom, D. M. ( 1980). Effects of the eyefluke, Diplostomum spathaceum, on the behavior of dace (Leuciscus leuciscus). Animal Behaviour 28, 287–294.CrossRefGoogle Scholar
Delattre, P., Pascal, M., Lepesteur, M. H., Giraudoux, P. and Damange, J. P. ( 1988). Ecological and epidemiological characteristics of Echinococcus multilocularis during a complete population cycle in a secondary host (Microtus arvalis). Canadian Journal of Zoology-Revue Canadienne de Zoologie 66, 2740–2750.CrossRefGoogle Scholar
Deplazes, P. and Eckert, J. ( 2001). Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. Veterinary Parasitology 98, 65–87.CrossRefGoogle Scholar
Dobson, A. P. ( 1988). The population biology of parasite-induced changes in host behaviour. Quarterly Review of Mammalogy 63, 139–165.Google Scholar
Eckert, J., Gemmell, M. A., Meslin, F. X. and Pawlowski, Z. S. ( 2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. World Organization for Animal Health.
Giraudoux, P., Raoul, F., Bardonnet, K., Vuillaume, P., Tourneux, F., Cliquet, F., Delattre, P. and Vuitton, D. A. ( 2001). Alveolar echinococcosis: characteristics of a possible emergence and new perspectives in epidemiosurveillance. Medecine et Maladies Infectieuses 31, 247S–256S.CrossRefGoogle Scholar
Gloor, S., Bontadina, F., Hegglin, D., Deplazes, P. and Breitenmoser, U. ( 2001). The rise of urban fox populations in Switzerland. Mammalian Biology 66, 155–164.Google Scholar
Hadeler, K. P. and Freedman, H. I. ( 1989). Predator-prey populations with parasitic infection. Journal of Mathematical Biology 27, 609–631.CrossRefGoogle Scholar
Hansen, F., Tackmann, K., Jeltsch, F., Staubach, C. and Thulke, H. ( 2002). If space changes all, the small-scale epidemiology of the fox tapeworm. In Proceedings of the Society for Veterinary Epidemiology and Preventative Medicine ( ed. Menzies, F. D. and Reid, S. W. J.), pp. 73–85. Society for Veterinary Epidemiology and Preventative Medicine, The Netherlands.
Hansen, F., Tackmann, K., Jeltsch, F., Wissel, C. and Thulke, H. H. ( 2003). Controlling Echinococcus multilocularis – ecological implications of field trials. Preventive Veterinary Medicine 60, 91–105.CrossRefGoogle Scholar
Hegglin, D., Ward, P. I. and Deplazes, P. ( 2003). Anthelmintic baiting of foxes against urban contamination with Echinococcus multilocularis. Emerging Infectious Diseases 9, 1266–1272.CrossRefGoogle Scholar
Hofer, S., Gloor, S., Muller, U., Mathis, A., Hegglin, D. and Deplazes, P. ( 2000). High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135–142.CrossRefGoogle Scholar
Holmes, J. C. and Bethel, W. M. ( 1972). Modification of intermediate host behaviour by parasites. Zoological Journal of the Linnean Society 51, 123–149.Google Scholar
Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. ( 2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford.
Joly, D. O. and Messier, F. ( 2004). The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves? Oecologia 140, 586–590.Google Scholar
Kapel, C. M. O., Torgerson, P. R., Thompson, R. C. A. and Deplazes, P. ( 2006). Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. International Journal for Parasitology 36, 79–86.CrossRefGoogle Scholar
Kern, P., Bardonnet, K., Renner, E., Auer, H., Pawlowski, Z., Ammann, R. W., Vuitton, D. A. and Kern, P. ( 2003). European echinococcosis registry: human alveolar echinococcosis, Europe, 1982–2000. Emerging Infectious Diseases 9, 343–349.CrossRefGoogle Scholar
Lloyd, H. G., Jensen, B., Vanhaaften, J. L., Niewold, F. J. J., Wandeler, A., Bogel, K. and Arata, A. A. ( 1976). Annual turnover of fox populations in Europe. Zentralblatt für Veterinärmedizin Reihe B-Journal of Veterinary Medicine Series B-Infectious Diseases Immunology Food Hygiene Veterinary Public Health 23, 580–589.CrossRefGoogle Scholar
Macdonald, D. W., Mathews, F. and Berdoy, M. ( 1999). The behaviour and ecology of Rattus norvegicus: from opportunism to kamikaze tendencies. In Ecologically Based Management of Rodent Pests ( ed. Singleton, G. R., Hinds, L., Leirs, H. and Zhang, Z.), pp. 49–80. ACIAR, Canberra.
Moore, J. ( 2002). Parasites and the Behaviour of Animals. Oxford University Press, Oxford.
Petavy, A. F. and Deblock, S. ( 1983). Connaissance du foyer auvérgnat d' échinococcose alvéolaire – Recherche de l'hôte intémedaire, description des lésions. Annales de Parasitologie Humaine et Comparée 58, 439–453.CrossRefGoogle Scholar
Poulin, R. ( 2002). Parasite manipulation of host behaviour. In The Behavioural Ecology of Parasites ( ed. Lewis, E. E., Campbell, J. F. and Sukhdeo, M. V. K.), pp. 243–257. CAB International, Wallingford, Oxon, UK.CrossRef
Raoul, F., Deplazes, P., Nonaka, N., Piarroux, R., Vuitton, D. A. and Giraudoux, P. ( 2001). Assessment of the epidemiological status of Echinococcus multilocularis in foxes in France using ELISA coprotests on fox faeces collected in the field. International Journal for Parasitology 31, 1579–1588.CrossRefGoogle Scholar
Raoul, F., Michelat, D., Ordinaire, M., Decote, Y., Aubert, M., Delattre, P., Deplazes, P. and Giraudoux, P. ( 2003). Echinococcus multilocularis: secondary poisoning of fox population during a vole outbreak reduces environmental contamination in a high endemicity area. International Journal for Parasitology 33, 945–954.CrossRefGoogle Scholar
Roberts, M. G. and Aubert, M. F. A. ( 1995). A model for the control of Echinococcus multilocularis in France. Veterinary Parasitology 56, 67–74.CrossRefGoogle Scholar
Romig, T. ( 2002). Spread of Echinococcus multilocularis in Europe? In Cestode Zoonoses: Echinococcosis and Cysticercosis ( ed. Craig, P. and Pawlowski, Z.), pp. 65–80. IOS Press, Oxford, UK.
Romig, T., Bilger, B., Dinkel, A., Merli, M. and Mackenstedt, U. ( 1999). Echinococcus multilocularis in animal hosts: new data from western Europe. Helminthologia 36, 185–191.Google Scholar
Schelling, U., Frank, W., Will, R., Romig, T. and Lucius, R. ( 1997). Chemotherapy with praziquantel has the potential to reduce the prevalence of Echinococcus multilocularis in wild foxes (Vulpes vulpes). Annals of Tropical Medicine and Parasitology 91, 179–186.CrossRefGoogle Scholar
Schmitt, M., Saucy, F., Wyborn, S. and Gottstein, B. ( 1997). Infestation of water voles (Arvicola terrestris) with metacestodes of Echinococcus multilocularis in the canton of Freiburg (Switzerland). Schweizer Zeitschrift für Obst- und Weinbau 139, 84–93.Google Scholar
Tackmann, K., Loschner, U., Mix, H., Staubach, C., Thulke, H. H. and Conraths, F. J. ( 1998). Spatial distribution patterns of Echinococcus multilocularis (Leuckart 1863) (Cestoda: Cyclophyllidea: Taeniidae) among red foxes in an endemic focus in Brandenburg, Germany. Epidemiology and Infection 120, 101–109.CrossRefGoogle Scholar
Tackmann, K., Loschner, U., Mix, H., Staubach, C., Thulke, H. H., Ziller, M. and Conraths, F. J. ( 2001). A field study to control Echinococcus multilocularis infections of the red fox (Vulpes vulpes) in an endemic focus. Epidemiology and Infection 127, 577–587.CrossRefGoogle Scholar
Veit, P., Bilger, B., Schad, V., Schafer, J., Frank, W. and Lucius, R. ( 1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 79–86.CrossRefGoogle Scholar
Vervaeke, M., Dorny, P., Vercammen, F., Geerts, S., Brandt, J., Van Den Berge, K. and Verhagen, R. ( 2003). Echinococcus multilocularis (Cestoda, Taeniidae) in red foxes (Vulpes vulpes) in northern Belgium. Veterinary Parasitology 115, 257–263.CrossRefGoogle Scholar