Effects of sarcoptic mange on the behaviour of the red fox and influence on other fox-born zoonoses in Geneva, Switzerland

Résumé : Une épidémie de gale sarcoptique (Sarcoptes scabiei) touche le canton de Genève depuis 1996. Nous avons étudié l'impact de cette maladie sur différents caractères comportementaux du renard roux (Vulpes vulpes) : l'écologie alimentaire, les comportements spatiaux et l'activité, ainsi que les contacts sociaux. Nous avons également évalué si la gale pouvait influencer la composition et la transmission de la communauté helminthique intestinale du renard. En effet, cette espèce est l'hôte de parasites qui sont liés à des zoonoses importantes, en particulier le ténia échinocoque du renard (Echinococcus multilocularis) pour lequel Genève est considérée comme une zone de haute endémie. Durant 5 années, des carcasses de renards ont été récoltées sur l'ensemble du canton. Nous les avons disséquées et avons conservé différents échantillons pour des analyses ultérieures. Des données sur le poids, l'âge et le statut reproductif des femelles ont ainsi pu être obtenues. Les contenus stomacaux ont été analysés pour déterminer le régime alimentaire, les intestins pour collecter des helminthes, des échantillons de sang pour faire des sérologies et des échantillons de peau pour récupérer les sarcoptes. Des renards sauvages ont également été capturés et équipés de colliers émetteurs afin de déterminer leur activité et leur utilisation de l'espace. Finalement, nous avons réalisé des affûts sur des terriers et des observations nocturnes à l'aide d'un détecteur thermique afin d'étudier les contacts sociaux. Nous avons ensuite considéré tous ces aspects pour comparer les renards galeux aux individus sains. Trois catégories de gale ont été prises en compte selon l'importance de l'infection. L'épidémie a traversé le canton en 8 ans environ et elle a provoqué une forte diminution des populations de renard. Les animaux malades étaient caractérisés par un poids réduit, ils utilisaient des domaines vitaux réduits et présentaient un rythme d'activité irrégulier. En ce qui concerne le régime alimentaire, les renards galeux avaient souvent des estomacs vides ou contenant peu d'aliments d'origine animale. Cette réduction de l'alimentation ne semble pas seulement être liée à des capacités de prédation réduite, mais également à un désintérêt face à la nourriture. Tous les changements de comportement cités étaient plus marqués chez les animaux soumis à une forte infestation. Dix taxons d'helminthes ont été identifiés dans les intestins des renards analysés. Deux d'entre eux représentent un risque de santé publique: Echinococcus multilocularis et Toxocara carvis. Pour ces helminthes, nous n'avons pas identifié de différences de prévalence entre les renards galeux et les animaux sains, mais la charge parasitaire était significativement supérieure chez les individus galeux, en particulier ceux souffrant d'une infestation importante. Ceci est probablement lié à une susceptibilité accrue des individus qui présentent une condition physique amoindrie et des défenses immunitaire affaiblies. Selon nos résultats, nous pouvons conclure que la gale induit des changements comportementaux importants et que ces changements ont une influence potentielle sur la transmission de la gale elle-même, mais également sur la transmission du reste de la communauté parasitaire de l'hôte. Les individus qui souffrent d'une infestation importante sont susceptibles de provoquer une contamination de l'environnement accrue en ce qui concerne des helminthes pouvant provoquer des zoonoses. La gale apparaît être un facteur à ne pas négliger dans le cadre de la gestion de la faune sauvage, mais également en ce qui concerne des problématiques de santé publique. Summary An epidemic outbreak of sarcoptic mange (Sarcoptes scabiei) has struck the canton of Geneva since 1996. The impact of the disease on various behavioural traits of the main host, the red fox (Vulpes vulpes), was investigated: feeding ecology, spatial behaviour and activity, and social contacts. We also evaluated if mange might have an influence on the composition and transmission of the intestinal helminth community of foxes. Indeed, this species is host of parasites with potential zoonotic importance, particularly the fox tapeworm (Echinococcus multilocularis) for which Geneva is reported as endemic area. During 5 years, red fox carcasses have been collected throughout the canton. They were then dissected and various samples conserved for further analysis. Data on weight, age, and reproductive status of females were obtained. Stomach content were analysed for diet analysis, intestines to recover helminths, blood to proceed to ELISAs and skin samples to check for the presence of Sarcoptes mites. Further, wild foxes were captured and fitted with transmitters in order to determine their activity pattern and space use. Finally, we proceeded to direct observations at dens and using a thermal imaging sensor at night to gain information about social contacts. A comparison between healthy and mangy foxes was made for all these aspects. Three categories of mangy foxes were considered from moderately to severely infected. The epidemic wave crossed the canton in about 8 years and induced a significant reduction in fox densities. Mangy individuals appeared to have reduced body weights, to use more restricted home ranges and exhibited an irregular activity pattern. Regarding food, sick foxes often had empty stomachs and consumed less food items of animal origin. The reduction in food intake appeared to be linked not only to a reduced ability to hunt, but also to a reduced interest in food. The changes observed were particularly pronounced in individuals with severe infestation. Ten helminth taxa were recovered from the intestines on the analysed fox carcasses. Two of them have an importance with regard to human public health: Echinococcus multilocularis and Toxocara cams. The prevalence of these helminths did not differ between healthy and mangy foxes, however the worm burden was significantly higher in mangy foxes, particularly those with severe mange. This is probably linked to an increased susceptibility in individuals with a reduced body condition and weakened immune defences. From our observations, we can conclude that mange induces pronounced behavioural changes in the red fox, and that those changes influence the transmission risks of mange itself, but also of the rest of the parasite community of the host. Individuals with severe mange are for example likely to increase the environment contamination of free living stages of helminths with zoonotic importance. Mange appears thus to represent a factor not to be neglected for the management of wild species and for public health issues.

Long-distance wolf recolonization of France and Switzerland inferred from non-invasive genetic sampling over a period of 10 years

In the early 1900s, the wolf (Canis lupus) was extirpated from France and Switzerland. There is growing evidence that the species is presently recolonizing these countries in the western Alps. By sequencing the mitochondrial DNA (mtDNA) control region of various samples mainly collected in the field (scats, hairs, regurgitates, blood or tissue; n = 292), we could (1) develop a non-invasive method enabling the unambiguous attribution of these samples to wolf, fox (Vulpes vulpes) or dog (Canis familiaris), among others; (2) demonstrate that Italian, French and Swiss wolves share the same mtDNA haplotype, a haplotype that has never been found in any other wolf population world-wide. Combined together, field and genetic data collected over 10 years corroborate the scenario of a natural expansion of wolves from the Italian source population. Furthermore, such a genetic approach is of conservation significance, since it has important consequences for management decisions. This first long-term report using non-invasive sampling demonstrates that long-distance dispersers are common, supporting the hypothesis that individuals may often attempt to colonize far from their native pack, even in the absence of suitable corridors across habitats characterized by intense human activities.

Trophic cascades in boreal landscapes: top predator protection on tree seedlings and forest grouse

Changes in the abundance of top predators have brought about notable, cascading effects in ecosystems around the world. In this thesis, I examined several potential trophic cascades in boreal ecosystems, and their separate interspecific interactions. The main aim of the thesis was to investigate whether predators in the boreal forests have direct or indirect cascading effects on the lower trophic levels. First, I compared the browsing effects of different mammalian herbivores by excluding varying combinations of voles, hares and cervids from accessing the seedlings of silver birch (Betula pendula), Scots pine (Pinus sylvestris) and Norway spruce (Picea abies). Additionally, I studied the effect of simulated predation risk on vole browsing by using auditory cues of owls. Moving upwards on the trophic levels, I examined the intraguild interactions between the golden eagle (Aquila chrysaetos), and its mesopredator prey, the red fox (Vulpes vulpes) and the pine marten (Martes martes). To look at an entire potential trophic cascade, I further studied the combined impacts of eagles and mesopredators on the black grouse (Tetrao tetrix) and the hazel grouse (Tetrastes bonasia), predicting that the shared forest grouse prey would benefit from eagle presence. From the tree species studied, birch appears to be the most palatable one for the mammalian herbivores. I observed growth reductions in the presences of cervids and low survival associated with hares and voles, which suggests that they all weaken regeneration in birch stands. Furthermore, the simulated owl predation risk appeared to reduce vole browsing on birches in late summer, although the preferred grass forage is then old and less palatable. Browsing by voles and hares had a negative effect on the condition and survival of Scots pine, but in contrast, the impact of mammalian herbivores on spruce was found to be small, at least when more preferred food is available. I observed that the presence of golden eagles had a negative effect on the abundance of adult black grouse but a positive, protective effect on the proportion of juveniles in both black grouse and hazel grouse. Yet, this positive effect was not dependent on the abundance foxes or martens, nor did eagles seem to effectively decrease the abundance of these mesopredators. Conversely, the protection effect on grouse could arise from fear effects and also be mediated by other mesopredators. The results of this thesis provide important new information about trophic interactions in the boreal food webs. They highlight how different groups of mammalian herbivores vary in their effects on the growth and condition of different tree seedlings. Lowered cervid abundances could improve birch regeneration, which indirectly supports the idea that the key predators of cervids could cause cascading effects also in Fennoscandian forests. Owls seem to reduce vole browsing through an intimidation effect, which is a novel result of the cascading effects of owl vocalisation and could even have applications for protecting birch seedlings. In the third cascade examined in this thesis, I found the golden eagle to have a protective effect on the reproducing forest grouse, but it remains unclear through which smaller predators this effect is mediated. Overall, the results of this thesis further support the idea that there are cascading effects in the forests of Northern Europe, and that they are triggered by both direct and non‐lethal effects of predation.

Behavioral changes associated with a population density decline in the facultatively social red fox

Understanding the causal mechanisms promoting group formation in carnivores has been widely investigated, particularly how fitness components affect group formation. Population density may affect the relative benefits of natal philopatry versus dispersal. Density effects on individual behavioral strategies have previously been studied through comparisons of different populations, where differences could be confounded by between-site effects. We used a single population of red foxes (Vulpes vulpes) in the city of Bristol, UK, that underwent a natural perturbation in density to compare key changes in 1) group structure, 2) within-group relatedness, 3) mating system, 4) dispersal, and 5) dominance attainment. At high densities (19.6-27.6 adults km(-2)), group sex ratios were equal and included related and unrelated individuals. At low densities (4.0-5.5 adults km(-2)), groups became female biased and were structured around philopatric females. However, levels of within-group relatedness were unchanged. The genetic mating patterns changed with no instances of multiple-paternity litters and a decline in the frequency of extrapair litters of cubs from <= 77% to <= 38%. However, the number of genetically monogynous groups did not differ between periods. Dispersal was male biased at both high and low densities. At high density, most dominant males in the study groups appeared to have gained dominance after dispersing, but natal philopatry was an equally successful strategy at low density; conversely, most dominant females were philopatric individuals at both high and low densities. These results illustrate how density may alter behavioral strategies such as mating patterns and how this, in turn, alters group structure in a single population.

Environmental variation at the onset of independent foraging affects full-grown body mass in the red fox

The period following the withdrawal of parental care has been highlighted as a key developmental period for juveniles. One reason for this is that juveniles cannot forage as competently as adults, potentially placing them at greater risk from environmentally-induced changes in food availability. However, no study has examined this topic. Using a long-term dataset on red foxes (Vulpes vulpes), we examined (i) dietary changes that occurred in the one-month period following the attainment of nutritional independence, (ii) diet composition in relation to climatic variation, and (iii) the effect of climatic variation on subsequent full-grown mass. Diet at nutritional independence contained increased quantities of easy-to-catch food items (earthworms and insects) when compared with pre-independence. Interannual variation in the volume of rainfall at nutritional independence was positively correlated to the proportion of earthworms in cub diet. Pre-independence cub mass and rainfall immediately following nutritional independence explained a significant proportion of variance in full-grown mass, with environmental variation affecting full-grown mass of the entire cohorts. Thus, weather-mediated availability of easy-to-catch food items at a key developmental stage has lifelong implications for the development of juvenile foxes by affecting full-grown mass, which in turn appears to be an important component of individual reproductive potential.

Urban mammals: what does the future hold? An analysis of the factors affecting patterns of use of residential gardens in Great Britain

1Urban areas are predicted to grow significantly in the foreseeable future because of increasing human population growth. Predicting the impact of urban development and expansion on mammal populations is of considerable interest due to possible effects on biodiversity and human-wildlife conflict. 2The British government has recently announced a substantial housing programme to meet the demands of its growing population and changing socio-economic profile. This is likely to result in the construction of high-density, low-cost housing with small residential gardens. To assess the potential effects of this programme, we analysed the factors affecting the current pattern of use of residential gardens by a range of mammal species using a questionnaire distributed in wildlife and gardening magazines and via The Mammal Society. 3Twenty-two species/species groups were recorded. However, the pattern of garden use by individual species was limited, with only six species/species groups (bats, red fox Vulpes vulpes, grey squirrel Sciurus carolinensis, hedgehog Erinaceus europaeus, mice, voles) recorded as frequent visitors to > 20% of gardens in the survey. 4There was a high degree of association between the variables recorded in the study, such that it was difficult to quantify the effects of individual variables. However, all species/species groups appeared to be negatively affected by the increased fragmentation and reduced proximity of natural and semi-natural habitats, decreasing garden size and garden structure, but to differing degrees. Patterns of garden use were most clearly affected by house location (city, town, village, rural), with garden use declining with increasing urbanization for the majority of species/species groups, except red foxes and grey squirrels. Increasing urbanization is likely to be related to a wide range of interrelated factors, any or all of which may affect a range of mammal species. 5Overall, the probable effects of the planned housing development programme in Britain are not likely to be beneficial to mammal populations, although the pattern of use examined in this study may represent patterns of habitat selection by species rather than differences in distribution or abundance. Consequently, additional data are required on the factors affecting the density of species within urban environments.

A Preliminary Note on Trichinosis Investigations in Alaska

Trichinosis in the arctic regions of the world has received considerable attention during recent years, particularly since the work of Roth (1948) in Greenland. In Connell's (1949) review of arctic trichinosis some Alaskan and Canadian records were included but, until now, little has been known of the status of the disease in Alaska. Information available at the present time indicates that the incidence of trichinosis is high in circumpolar carnivores and that marine mammals have a definite place in its epizootiology. Present knowledge cannot explain the survival of trichinosis in marine mammal populations, but it is evident that they may serve as important sources of human infection. Up to the present time the following mammals from Alaska have been found to be infected: From the arctic coast-polar bear, Thalarctas maritimus; arctic fox, Alapex lagapus irmuitus; red fox, Vulpes fulva alascemis; white whale, Delphinapterus leucas; Eskimo dog. From south of the Brooks Range--brown and grizzly bears, Ursus spp.; wolf, Canis lupus ssp.; wolverine. Gula l. luscus. At the time of writing, nearly ail species of land carnivores in Alaska have been examined as well as many other mammalian species less likely to be infected, including various rodents, shrews, and others.

Multi-locus microsatellite analysis supports the hypothesis of an autochthonous focus of Echinococcus multilocularis in northern Italy

Echinococcus multilocularis is characterised by a wide geographical distribution, encompassing three continents (North America, Asia and Europe) yet very low genetic variability is documented. Recently, this parasite has been detected in red foxes (Vulpes vulpes) circulating in an Alpine region of Italy, close to Austria. This finding raised the question as to whether an autochthonous cycle exists in Italy or whether the infected foxes originated from the neighbouring regions of Austria. Studies have shown that multi-locus microsatellite analysis can identify genomic regions carrying mutations that result in a local adaptation. We used a tandem repeated multi-locus microsatellite (EmsB) to evaluate the genetic differences amongst adult worms of E. multilocularis collected in Italy, worms from neighbouring Austria and from other European and extra-European countries. Fluorescent PCR was performed on a panel of E. multilocularis samples to assess intra-specific polymorphism. The analysis revealed four closed genotypes for Italian samples of E. multilocularis which were unique compared with the other 25 genotypes from Europe and the five genotypes from Alaska. An analysis in the Alpine watershed, comparing Italian adult worms with those from neighbouring areas in Austria, showed a unique cluster for Italian samples. This result supports the hypothesis of the presence of an autochthonous cycle of E. multilocularis in Italy. EmsB can be useful for 'tracking' the source of infection of this zoonotic parasite and developing appropriate measures for preventing or reducing the risk of human alveolar echinococcosis.

Emergence of Canine Distemper Virus Strains With Modified Molecular Signature and Enhanced Neuronal Tropism Leading to High Mortality in Wild Carnivores

An ongoing canine distemper epidemic was first detected in Switzerland in the spring of 2009. Compared to previous local canine distemper outbreaks, it was characterized by unusually high morbidity and mortality, rapid spread over the country, and susceptibility of several wild carnivore species. Here, the authors describe the associated pathologic changes and phylogenetic and biological features of a multiple highly virulent canine distemper virus (CDV) strain detected in and/or isolated from red foxes (Vulpes vulpes), Eurasian badgers (Meles meles), stone (Martes foina) and pine (Martes martes) martens, from a Eurasian lynx (Lynx lynx), and a domestic dog. The main lesions included interstitial to bronchointerstitial pneumonia and meningopolioencephalitis, whereas demyelination-the classic presentation of CDV infection-was observed in few cases only. In the brain lesions, viral inclusions were mainly in the nuclei of the neurons. Some significant differences in brain and lung lesions were observed between foxes and mustelids. Swiss CDV isolates shared together with a Hungarian CDV strain detected in 2004. In vitro analysis of the hemagglutinin protein from one of the Swiss CDV strains revealed functional and structural differences from that of the reference strain A75/17, with the Swiss strain showing increased surface expression and binding efficiency to the signaling lymphocyte activation molecule (SLAM). These features might be part of a novel molecular signature, which might have contributed to an increase in virus pathogenicity, partially explaining the high morbidity and mortality, the rapid spread, and the large host spectrum observed in this outbreak.