Advertisement

Parasitology Research

, Volume 101, Issue 3, pp 605–611 | Cite as

Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland

  • Leslie A. Reperant
  • Daniel Hegglin
  • Claude Fischer
  • Lucia Kohler
  • Jean-Marc Weber
  • Peter DeplazesEmail author
Original Paper

Abstract

Dixenous helminths that depend on rodent intermediate hosts are supposed to be negatively affected by urbanization due to lower supply of rodents in urbanized environments. Prevalence rates of dixenous, non-strictly monoxenous, and monoxenous helminths in 228 red foxes (Vulpes vulpes) along a gradient of increasing urbanization were assessed by morphological parasite identification in the city of Geneva, Switzerland. Multivariate analyses for the five most prevalent helminth species or genera revealed a significant decrease of prevalence rates for the dixenous helminths Echinococcus multilocularis and Taenia spp. from the rural (52.1 and 54.3%, respectively) to the urban area (30.0 and 20.0%, respectively), but not for the monoxenous nematode Uncinaria stenocephala (overall prevalence of 78.2%) and the non-strictly monoxenous nematode Toxocara canis (overall prevalence of 44.3%). The lower prevalence of Toxascaris leonina in the urban area (8.0%) compared to the rural area (59.6%) raises the question of whether rodent paratenic hosts play a major role for the population dynamics of this species.

Keywords

Canis Urbanization Zone Paratenic Host Intestinal Helminth Echinococcus Multilocularis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

The study was funded by the Swiss Federal Office for Education and Science (EU FAIR Projekt CT97-3515/BBW no. 97.0586) and the European Commission (Project Echinorisk, contract QLK2-CT-2001-01995/BBW no. 00.0586-2). This publication represents part of the dissertation of Leslie Reperant, veterinarian.

References

  1. Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B 265:1283–1289CrossRefGoogle Scholar
  2. Artois M, Stahl P, Leger F, Morvan P, Barbillon E (1989) Prédation des rongeurs par le renard roux (Vulpes vulpes) en Lorraine. Gibier Faune Sauvage 6:279–294Google Scholar
  3. Burke TM, Roberson EL (1985a) Prenatal and lactational transmission of Toxocara canis and Ancylostoma caninum. Experimental infection of the bitch before pregnancy. Int J Parasitol 15:71–75PubMedCrossRefGoogle Scholar
  4. Burke TM, Roberson EL (1985b) Prenatal and lactational transmission of Toxocara canis and Ancylostoma caninum. Experimental infection of the bitch at mid-pregnancy and at parturition. Int J Parasitol 15:485–490PubMedCrossRefGoogle Scholar
  5. Clopper CJ, Pearson ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26:404–413CrossRefGoogle Scholar
  6. Contesse P, Hegglin D, Gloor S, Bontadina F, Deplazes P (2004) The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zürich, Switzerland. Mamm Biol 69:81–95CrossRefGoogle Scholar
  7. Criado-Fornelio A, Gutierrez-Garcia L, Rodriguez-Caabeiro F, Reus-Garcia E, Roldan-Soriano MA, Diaz-Sanchez MA (2000) A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Vet Parasitol 92:245–251PubMedCrossRefGoogle Scholar
  8. Deplazes P, Hegglin D, Gloor S, Romig T (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol 20:77–84PubMedCrossRefGoogle Scholar
  9. Despommier D (2003) Toxocariasis: clinical aspects, epidemiology, medical ecology and molecular aspects. Clin Microbiol Rev 16:265–272PubMedCrossRefGoogle Scholar
  10. Doncaster CP, Dickman CR, MacDonald DW (1990) Feeding ecology of red foxes (Vulpes vulpes) in the city of Oxford, England. J Mammal 71:188–194CrossRefGoogle Scholar
  11. Eckert J, Deplazes P (2004) Biological, epidemiological, and clinical aspects of Echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17:107–135PubMedCrossRefGoogle Scholar
  12. Epe C, Meuwissen M, Stoye M, Schnieder T (1999) Transmission trials, ITS2–PCR and RAPD–PCR show identity of Toxocara canis isolates from red fox and dog. Vet Parasitol 84:101–112PubMedCrossRefGoogle Scholar
  13. Ferrari N, Weber JM (1995) Influence of the abundance of food resources on the feeding habits of the red fox, Vulpes vulpes, in western Switzerland. J Zool London 236:117–129CrossRefGoogle Scholar
  14. Fischer C, Reperant LA, Weber JM, Hegglin D, Deplazes P (2005) Echinococcus multilocularis infections of rural, residential and urban red foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12:339–346PubMedGoogle Scholar
  15. Giacometti A, Cirioni O, Fortuna M, Osimati P, Antonicelli L, Del Prete MS, Riva A, D’Errico MM, Petrelli E, Scalise G (2000) Environmental and serological evidence for the presence of toxocariasis in the urban area of Ancona, Italy. Eur J Epidemiol 16:1023–1026PubMedCrossRefGoogle Scholar
  16. Gloor S, Bontadina F, Hegglin D, Deplazes P, Breitenmoser U (2001) The rise of urban fox population in Switzerland. Mamm Biol 66:155–164Google Scholar
  17. Gortazar C, Villafuerte R, Lucientes J, Fernandez-de-Luco D (1998) Habitat related differences in helminth parasites of red foxes in the Ebro Valley. Vet Parasitol 80:75–81PubMedCrossRefGoogle Scholar
  18. Habluetzel A, Traldi G, Ruggieri S, Attili AR, Scuppa P, Marchetti R, Menghini G, Esposito F (2003) An estimation of Toxocara canis prevalence in dogs, environmental egg contamination and risk of human infection in the Marche region of Italy. Vet Parasitol 113:243–252PubMedCrossRefGoogle Scholar
  19. Harris S, Rayner JMV (1986) Urban fox (Vulpes vulpes) population estimates and habitat requirements in several British cities. J Anim Ecol 55:575–591CrossRefGoogle Scholar
  20. Hegglin D, Bontadina F, Contesse P, Gloor S, Deplazes P (2007) Plasticity of predation behaviour as a putative driving force for parasite life cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Funct Ecol (in press) DOI 10.111/j.1365-2435.2007.01257.x
  21. Hofer S, Gloor S, Müller U, Mathis A, Hegglin D, Deplazes P (2000) High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology 120:135–142PubMedCrossRefGoogle Scholar
  22. Kappeler A (1991) Die orale Immunisierung von Füchsen gegen Tollwut in der Schweiz. Dissertation, University of Bern, SwitzerlandGoogle Scholar
  23. Luty T (2001) Prevalence of species of Toxocara in dogs, cats and red foxes from the Poznan region, Poland. J Helminthol 75:153–156PubMedGoogle Scholar
  24. Magnaval JF, Glickman LT, Dorchies P (1998) Toxocarose. In: Epidémiologie des Maladies Parasitaires, Tome 2, Helminthoses. Editions Médicales Internationales, ParisGoogle Scholar
  25. Mizgajska H (1997) The role of some environmental factors in the contamination of soil with Toxocara spp. and other geohelminth eggs. Parasitol Int 46:67–72CrossRefGoogle Scholar
  26. Mizgajska H (2001) Eggs of Toxocara spp. in the environment and their public health implications. J Helminthol 75:147–151PubMedGoogle Scholar
  27. Mozgovoi AA (1968) Ascaridata of animals and man and the diseases caused by them. Essentials of nematodology. Israel Program for Scientific Translations, JerusalemGoogle Scholar
  28. Overgaauw PA (1997) Aspects of Toxocara epidemiology: human toxocarosis. Crit Rev Microbiol 23:215–231PubMedCrossRefGoogle Scholar
  29. Richards DT, Lewis JW (2001) Fecundity and egg output by Toxocara canis in the red fox, Vulpes vulpes. J Helminthol 75:157–164PubMedGoogle Scholar
  30. Richards DT, Harris S, Lewis JW (1993) Epidemiology of toxocara canis in red foxes (Vulpes vulpes) from urban areas of Bristol. Parasitology 107:167–173PubMedCrossRefGoogle Scholar
  31. Richards DT, Harris S, Lewis JW (1995) Epidemiological studies on intestinal helminth parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Vet Parasitol 59:39–51PubMedCrossRefGoogle Scholar
  32. Saeed I, Taira K, Kapel CMO (2005) Toxocara canis in experimentally infected silver and arctic foxes. Parasitol Res 97:160–166PubMedCrossRefGoogle Scholar
  33. Saeed I, Maddox-Hyttel C, Monrad J, Kapel CMO (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179PubMedCrossRefGoogle Scholar
  34. Smith GC, Gangadharan B, Taylor Z, Laurenson MK, Bradshaw H, Hide G, Hughes JM, Dinkel A, Romig T, Craig PS (2003) Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain. Vet Parasitol 118:133–142PubMedCrossRefGoogle Scholar
  35. Weber JM, Aubry S (1993) Predation by foxes, Vulpes vulpes, on the fossorial form of the water vole, Arvicola terrestris scherman, in western Sitzerland. J Zool (London) 229:553–559Google Scholar
  36. Willingham AL, Ockens NW, Kapel CMO, Monrad J (1996) A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. J Helminthol 70:259–263PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Leslie A. Reperant
    • 1
    • 2
  • Daniel Hegglin
    • 1
  • Claude Fischer
    • 3
  • Lucia Kohler
    • 1
  • Jean-Marc Weber
    • 4
  • Peter Deplazes
    • 1
    Email author
  1. 1.Institute of ParasitologyUniversity of ZurichZurichSwitzerland
  2. 2.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA
  3. 3.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  4. 4.KORA (Co-ordinated Carnivore Research Projects)MuriSwitzerland

Personalised recommendations