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Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal

Published online by Cambridge University Press:  03 August 2007

E. AFONSO*
Affiliation:
Université de Lyon; Université Lyon 1; CNRS; UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, 43 boulevard du 11 novembre 1918, Villeurbanne F-69622, France 2C2A – CERFE, 08240 Boult-aux-Bois, France Laboratoire de Parasitologie – Mycologie, EA 3800, UFR Médecine, Université de Reims Champagne-Ardenne, 51 rue Cognacq Jay, Hôpital Maison Blanche, 51096 Reims cedex, France
P. THULLIEZ
Affiliation:
Laboratoire de la Toxoplasmose, Institut de Puériculture et de Périnatalogie, 26 boulevard Brune, 75014 Paris, France
D. PONTIER
Affiliation:
Université de Lyon; Université Lyon 1; CNRS; UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, 43 boulevard du 11 novembre 1918, Villeurbanne F-69622, France
E. GILOT-FROMONT
Affiliation:
Université de Lyon; Université Lyon 1; CNRS; UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, 43 boulevard du 11 novembre 1918, Villeurbanne F-69622, France
*
*Corresponding author: Université de Lyon; Université Lyon 1; CNRS; UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, 43 boulevard du 11 novembre 1918, Villeurbanne F-69622, France. Tel: +33 4 72 43 35 84. E-mail: afonso@biomserv.univ-lyon1.fr

Summary

Toxoplasma gondii is largely transmitted to definitive felid hosts through predation. Not all prey species represent identical risks of infection for cats because of differences in prey susceptibility, exposure and/or lifespan. Previously published studies have shown that prevalence in rodent and lagomorph species is positively correlated with body mass. We tested the hypothesis that different prey species have different infection risks by comparing infection dynamics of feral cats at 4 sites in the sub-Antarctic Kerguelen archipelago which differed in prey availability. Cats were trapped from 1994 to 2004 and anti-T. gondii IgG antibodies were detected using the modified agglutination test (⩾1:40). Overall seroprevalence was 51·09%. Antibody prevalence differed between sites, depending on diet and also on sex, after taking into account the effect of age. Males were more often infected than females and the difference between the sexes tended to be more pronounced in the site where more prey species were available. A difference in predation efficiency between male and female cats may explain this result. Overall, our results suggest that the composition of prey items in cat diet influences the risk of T. gondii infection. Prey compositon should therefore be considered important in any understanding of infection dynamics of T. gondii.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

AFSSA (2005). Toxoplasmose: état des Connaissances et Evaluation du Risque Lié à l'Alimentation. AFSSA Ed., Maisons-Alfort, France.Google Scholar
Afonso, E., Thulliez, P. and Gilot-Fromont, E. (2006). Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). International Journal for Parasitology 36, 13731382.CrossRefGoogle Scholar
Almeria, S., Calvete, C., Pagés, A., Gauss, C. B. L. and Dubey, J. P. (2004). Factors affecting the seroprevalence of Toxoplasma gondii infection in wild rabbits (Oryctolagus cuniculus) from Spain. Veterinary Parasitology 123, 265270.CrossRefGoogle ScholarPubMed
Arnaudov, D., Arnaudov, A. and Kirin, D. (2003). Study on the toxoplasmosis among wild animals. Experimental Pathology and Parasitology 6/11, 5154.Google Scholar
Bollo, E., Pregel, P., Gennero, S., Pizzoni, E., Rosati, S., Nebbia, P. and Biolatti, B. (2003). Health status of a population of nutria (Myocastor coypus) living in a protected area in Italy. Research in Veterinary Science 75, 2125.CrossRefGoogle Scholar
Brillhart, D. B., Fox, L. B., Dubey, J. P. and Upton, S. J. (1994). Seroprevalence of Toxoplasma gondii in wild mammals in Kansas. Journal of the Helminthological Society of Washington 61, 117121.Google Scholar
Burnham, K. P. and Anderson, D. R. (1992). Data-based selection of an appropriate model: the key to modern data analysis. In Wildlife Populations (ed. McCullough, D. R. and Barrett, R. H.), pp. 1630. Elsevier Applied Science, London.Google Scholar
Burridge, M. J., Bigler, W. J., Forrester, D. J. and Hennemann, J. M. (1979). Serologic survey for Toxoplasma gondii in wild animals in Florida. Journal of the American Veterinary Medical Association 175, 964–947.Google ScholarPubMed
Cañon-Franco, W. A., Yai, L. E. O., Joppert, A. M., Souza, C. E., D'Auria, S. R. N., Dubey, J. P. and Gennari, S. M. (2003). Seroprevalence of Toxoplasma gondii antibodies in the rodent Capybara (Hidrochoeris hidrochoeris) from Brazil. The Journal of Parasitology 89, 850.CrossRefGoogle ScholarPubMed
Carme, B., Aznar, C., Motard, A., Demar, M. and de Thoisy, B. (2002). Serologic survey of Toxoplasma gondii in noncarnivorous free-ranging neotropical mammals in French Guyana. Vector Borne and Zoonotic Diseases 2, 1117.CrossRefGoogle Scholar
Chalupsky, J., Vavra, J., Gaudin, J. C., Vandewalle, P., Arthur, C. P., Guenezan, M. and Launey, H. (1990). Mise en évidence sérologique de la présence d'encephalitozoonose et de toxoplasmose chez le lapin de Garenne (Oryctolagus cuniculus) en France. Bulletin de la Société Française de Parasitologie 8, 9195.Google Scholar
Chinchilla, M., Guerrero, O. M., Reyes, L. and Abrahams, E. (1996). Susceptibility of Sigmodon hispidus (Rodentia: Cricetidae) to Toxoplasma gondii (Eucoccidia: Sarcocystidae). Revista de Biologia Tropical 44, 265268. (In Spanish.)Google ScholarPubMed
Conroy, C. J. and Cook, J. A. (2000). Molecular systematics of holarctic rodent (Microtus: Muridae). Journal of Mammalogy 81, 344359.2.0.CO;2>CrossRefGoogle Scholar
Cox, J. C., Edmonds, J. W. and Shepherd, R. C. (1981). Toxoplasmosis and the wild rabbit Oryctolagus cuniculus in Victoria, Australia with suggested mechanisms for dissemination of oocysts. Journal of Hygiene (London) 87, 331337.CrossRefGoogle ScholarPubMed
Degen, A. A., Kam, M., Khokhlova, I. S., Krasnov, B. R. and Barraclough, T. G. (1998). Average daily metabolic rate of rodents: habitat and dietary comparisons. Functional Ecology 12, 6373.CrossRefGoogle Scholar
Doby, J. M., Desmonts, G., Beaucournu, J. C. and Akinchina, G. T. (1974). Systematic immunologic study of toxoplasmosis in small wild mammals of France. Folia Parasitologica (Praha) 21, 289300.Google ScholarPubMed
Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, USA.Google Scholar
Dubey, J. P. and Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337339.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Hoover, E. A. (1977). Attempted transmission of Toxoplasma gondii infection from pregnant cats to their kittens. Journal of American Veterinary Medicine Association 170, 538540.Google ScholarPubMed
Dubey, J. P., Weigel, R. M., Siegel, A. M., Thuilliez, P., Kitron, U. D., Mitchell, M. A., Mannelli, A., Mateus-Pinilla, N. E., Shen, S. K., Kwok, O. C. H. and Todd, K. S. (1995). Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. The Journal of Parasitology 81, 723729.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2006). Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Veterinary Parasitology 140, 6975.CrossRefGoogle ScholarPubMed
Durish, N. D., Halcomb, K. E., Kilpatrick, C. W. and Bradley, R. D. (2004). Molecular systematics of the Peromyscus truei species group. Journal of Mammalogy 85, 11601169.CrossRefGoogle Scholar
El Nahal, H. S., Morsy, T. A., Bassili, W. R., El Missiry, A. G. and Saleh, M. S. (1982). Antibodies against three parasites of medical importance in Rattus sp. collected in Giza Governorate, Egypt. Journal of the Egyptian Society of Parasitology 12, 287293.Google ScholarPubMed
Ernest, S. K. M. (2003). Life history characteristics of placental non-volant mammals. Ecology 84, 3402.CrossRefGoogle Scholar
Felsenstein, J. (1985). Phylogenies and the comparative methods. The American Naturalist 125, 115.CrossRefGoogle Scholar
Franti, C. E., Riemann, H. P., Behymer, D. E., Suther, D., Howarth, J. A. and Ruppanner, R. (1976). Prevalence of Toxoplasma gondii antibodies in wild and domestic animals in northern California. Journal of the American Veterinary Medical Association 169, 901906.Google ScholarPubMed
Frölich, K., Wisser, J., Schmuser, H., Fehlberg, U., Neubauer, H., Grunow, R., Nikolaou, K., Priemer, J., Thiede, S., Streich, W. and Speck, S. (2003). Epizootiologic and ecologic investigations of European brown hares (Lepus europaeus) in selected populations from Schleswig-Holstein, Germany. Journal of Wildlife Diseases 39, 751761.CrossRefGoogle ScholarPubMed
Gustafsson, K. and Uggla, A. (1994). Serologic survey for Toxoplasma gondii infection in the brown hare (Lepus europaeus P.) in Sweden. Journal of Wildlife Diseases 30, 201204.CrossRefGoogle ScholarPubMed
Gustafsson, K., Uggla, A. and Jarplid, B. (1997). Toxoplasma gondii infection in the mountain hare (Lepus timidus) and domestic rabbit (Oryctolagus cuniculus). I. Pathology. Journal of Comparative Pathology 117, 351360.CrossRefGoogle ScholarPubMed
Hejlicek, K. and Literak, I. (1994). Prevalence of toxoplasmosis in rabbits in South Bohemia. Acta Veterinaria 63, 145150.CrossRefGoogle Scholar
Holmes, R. G., Illman, O. and Beverley, J. K. (1977). Toxoplasmosis in coypu. The Veterinary Record 101, 7475.CrossRefGoogle ScholarPubMed
Hosmer, D. W., Hosmer, T., Le Cessie, S. and Lemeshow, S. (1997) A comparison of goodness of fit tests for the logistic regression model. Statistics in Medicine 16, 965980.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Huchon, D. and Douzery, E. J. P. (2001). From the old to the new world: a molecular chronicle of the phylogeny and biogeography of hystricognath rodents. Molecular Phylogenetics and Evolution 20, 238251.CrossRefGoogle Scholar
Jackson, M. H., Hutchison, W. M. and Siim, J. C. (1986). Toxoplasmosis in a wild rodent population of central Scotland and a possible explanation of the mode of transmission. Journal of Zoology, London, Series A 209, 549557.CrossRefGoogle Scholar
Jeon, S.-H. and Yong, T. S. (2000). Serological observation of Toxoplasma gondii prevalence in Apodemus agrarius, a dominant species in field rodents in Korea. Yonsei Medical Journal 41, 491496.CrossRefGoogle ScholarPubMed
Jones, E. and Coman, B. J. (1981). Ecology of the feral cat Felis catus (L.), in southern Australia. 1. Diet. Australian Wildlife Research 8, 249262.CrossRefGoogle Scholar
Kapperud, G. (1978). Survey for toxoplasmosis in wild and domestic animals from Norway and Sweden. Journal of Wildlife Diseases 14, 157162.CrossRefGoogle ScholarPubMed
Karatepe, M., Babür, C., Karatepe, B., Kiliç, S. and Cakir, M. (2004). Prevalence of Toxoplasma gondii antibodies in anatolian ground squirrels, Spermophilus xanthophrymnus (Rodentia: Sciuridae) from Nigde, Turkey. Revue de Médecine Vétérinaire 155, 530532.Google Scholar
Liberg, O. (1982). Hunting efficiency and prey impact by a free-roaming house cat population. Transactions of the International Congress of Game Biology 14, 269275.Google Scholar
Michaux, J. R., Chevet, P., Filippucci, M.-G. and Macholan, M. (2002). Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Molecular Phylogenetics and Evolution 23, 123136.CrossRefGoogle Scholar
Mir, N. A., Chhabra, M. B., Bhardwaj, R. M. and Gautam, O. P. (1982). Toxoplasma infection and some other protozoan parasites of the wild rat in India. The Indian Veterinary Journal 59, 6063.Google Scholar
Niewold, F. J. J. (1986). Voedselkeuze, terreingebruik en aantalsregulatie van in het veld operende huiskatten Felis catus L., 1758. Lutra 29, 145187. In The Domestic Cat. The Biology of its Behaviour (ed. Turner, D. C. and Bateson, P. B.), pp. 145187. Cambridge University Press, Cambridge, UK.Google Scholar
Ottaviani, D., Cairns, S. C., Oliverio, M. and Boitani, L. (2006). Body mass as a predictive variable of home-range size among Italian mammals and birds. Journal of Zoology 269, 317330.CrossRefGoogle Scholar
Pascal, M. and Castanet, J. (1978). Méthode de détermination de l’âge chez le chat haret des îles Kerguelen. La Terre et la Vie 4, 529555.Google Scholar
Pontier, D., Say, L., Debias, F., Bried, J. and Thioulouse, J. (2002) The diet of feral cats (Felis catus L.) at five sites on the Grande Terre, Kerguelen archipelago. Polar Biology 25, 833837.CrossRefGoogle Scholar
Pontier, D., Say, L., Devillard, S. and Bonhomme, F. (2005). Genetic structure of the feral cat (Felis catus L.) introduced 50 years ago to a sub-Antarctic island. Polar Biology 28, 268275.CrossRefGoogle Scholar
R Development Core Team (2005). R: A Language and Environment for Statistical Computing. Vienna, Austria. http://www.R-project.org.Google Scholar
Robinson, T. J. and Matthee, C. A. (2005). Phylogeny and evolutionary origins of the Leporidae: a review of cytogenetics, molecular analyses and supermatrix analysis. Mammals Review 35, 231247.CrossRefGoogle Scholar
Sedlak, K., Literak, I., Pavlasek, I. and Benak, J. (2001). Susceptibility of common voles to experimental toxoplasmosis. Journal of Wildlife Diseases 37, 640642.CrossRefGoogle ScholarPubMed
Say, L., Gaillard, J.-M. and Pontier, D. (2002 a). Spatio-temporal variation in cat population density in a sub-Antarctic environment. Polar Biology 25, 9095.CrossRefGoogle Scholar
Say, L., Devillard, S., Natoli, E. and Pontier, D. (2002 b). The mating system of feral cats (Felis catus L.) in a sub-Antarctic environment. Polar Biology 25, 838842.CrossRefGoogle Scholar
Smith, D. D. and Frenkel, J. K. (1995). Prevalence of antibodies to Toxoplama gondii in wild mammals of Missouri and east central Kansas: biologic and ecologic considerations of transmission. Journal of Wildlife Diseases 31, 1521.CrossRefGoogle Scholar
Sokal, R. R. and Rohlf, F. S. (1981). Biometry. W. H. Freeman, New York.Google Scholar
Speakman, J. R. (2005). Body size, energy metabolism and lifespan. The Journal of Experimental Biology 208, 17171730.CrossRefGoogle ScholarPubMed
Steppan, S. J., Adkins, R. M. and Anderson, J. (2004). Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53, 533553.CrossRefGoogle ScholarPubMed
Stewart, R. L., Humphreys, J. G. and Dubey, J. P. (1995). Toxoplasma gondii antibodies in woodchucks (Marmota monax) from Pennsylvania. Journal of Parasitology 81, 126127.CrossRefGoogle ScholarPubMed
Stutzin, M., Contreras, M. C. and Schenone, H. (1989). Epidemiology of toxoplasmosis in Chile. V. Prevalence of the infection in humans and domestic and wild animals, studied by indirect hemagglutination reaction, in the Juan Fernandez Archipelago. V Region. Boletín Chileno de Parasitología 44, 3740. (In Spanish.)Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Turner, D. C. and Bateson, P. B. (2000). The Domestic Cat. The Biology of its Behaviour. Cambridge University Press, Cambridge, UK.Google Scholar
Zhang, S.-Y., Jiang, S. F., He, Y. Y., Pan, C. E., Zhu, M. and Wei, M.-X. (2004). Serologic prevalence of Toxoplasma gondii in field mice, Microtus fortis, from Yuanjiang, Hunan Province, People's Republic of China. Journal of Parasitology 90, 437438.Google Scholar