Abstract

Anthropogenic landscape changes contributed to the reduction of availability of habitats to wild animals. Hence, the presence of wild terrestrial carnivores in urban and peri-urban sites has increased considerably over the years implying an increased risk of interspecies spillover of infectious diseases and the transmission of zoonoses. The present study provides a detailed characterisation of the health status of the red fox (Vulpes vulpes), stone marten (Martes foina) and raccoon dog (Nyctereutes procyonoides) in their natural rural and peri-urban habitats in Schleswig-Holstein, Germany between November 2013 and January 2016 with focus on zoonoses and infectious diseases that are potentially threatening to other wildlife or domestic animal species. 79 red foxes, 17 stone martens and 10 raccoon dogs were collected from traps or hunts. In order to detect morphological changes and potential infectious diseases, necropsy and pathohistological work-up was performed. Additionally, in selected animals immunohistochemistry (influenza A virus, parvovirus, feline leukemia virus, Borna disease virus, tick-borne encephalitis, canine adenovirus, Neospora caninum, Toxoplasma gondii and Listeria monocytogenes), next-generation sequencing, polymerase chain reaction (fox circovirus) and serum-neutralisation analysis (canine distemper virus) were performed. Furthermore, all animals were screened for fox rabies virus (immunofluorescence), canine distemper virus (immunohistochemistry) and Aujeszky’s disease (virus cultivation). The most important findings included encephalitis (n = 16) and pneumonia (n = 20). None of the investigations revealed a specific cause for the observed morphological alterations except for one animal with an elevated serum titer of 1:160 for canine distemper. Animals displayed macroscopically and/or histopathologically detectable infections with parasites, including Taenia sp., Toxocara sp. and Alaria alata. In summary, wildlife predators carry zoonotic parasitic disease and suffer from inflammatory diseases of yet unknown etiology, possibly bearing infectious potential for other animal species and humans. This study highlights the value of monitoring terrestrial wildlife following the “One Health” notion, to estimate the incidence and the possible spread of zoonotic pathogens and to avoid animal to animal spillover as well as transmission to humans.

Highlights

  • Wild carnivores have increasingly entered human habitats within the past decades, mainly due to anthropogenic habitat alterations as a result of the growing human population [1,2,3,4]

  • While the fox rabies virus (Rabies lyssavirus) has been eradicated in Germany [13], other infectious diseases of wild carnivores, including zoonotic parasitoses such as Echinococcus multilocularis, viral (e.g. canine distemper virus (CDV) or avian influenza virus and bacterial (e.g. Listeria monocytogenes) pathogens, still represent a potential threat to humans who come into contact with those predators or their excretions [2, 14, 15]

  • The major findings included (i) 46 cases (45.6% foxes, 35.3% stone martens and 40% raccoon dogs) of endoparasitism including agents with high zoonotic potential; (ii) 17 cases (11.4% foxes, 23.5% stone martens and 30% raccoon dogs) of encephalitis and (iii) 28 cases (24% foxes, 17.6% stone martens and 60% raccoon dogs) with pneumonia of unknown origin

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Summary

Introduction

Wild carnivores have increasingly entered human habitats within the past decades, mainly due to anthropogenic habitat alterations as a result of the growing human population [1,2,3,4]. The unintentional convergence of human and wildlife populations has been enhanced by several predator species which readily learn to take advantage of accessible food sources in urban and peri-urban habitats [2, 4] One of these highly adaptable predators is the red fox (Vulpes vulpes), that is the most widespread wild terrestrial carnivore in European countries like Germany, Estonia, Great Britain, and Switzerland [5,6,7,8]. The raccoon dog (Nyctereutes procyonoides), an invasive species, imported from Asia as a fur-bearing animal to Eastern Europe has expanded its range throughout Germany since the 1960s [11] All these species have started to invade human habitats due to the benefits of urbanisation and live in close contact with humans, exposing them to a number of potentially zoonotic diseases. While the fox rabies virus (Rabies lyssavirus) has been eradicated in Germany [13], other infectious diseases of wild carnivores, including zoonotic parasitoses such as Echinococcus multilocularis, viral (e.g. canine distemper virus (CDV) or avian influenza virus and bacterial (e.g. Listeria monocytogenes) pathogens, still represent a potential threat to humans who come into contact with those predators or their excretions [2, 14, 15]

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