Invading parasites cause a structural shift in red fox dynamics

The influence of parasites on host life histories and populations is pronounced. Among several diseases affecting animal populations throughout the world, sarcoptic mange has influenced many carnivore populations dramatically and during the latest epizootic in Fennoscandia reduced the abundance of red fox by over 70%. While the numerical responses of red fox populations, their prey and their competitors as well as clinical implications are well known, knowledge of how sarcoptic mange affects the structure of the dynamics of red fox populations is lacking. Integrating ecological theory and statistical modelling, we analysed the long-term dynamics (1955-1996) of 14 Danish red fox populations. As suggested by the model, invading sarcoptic mange significantly affected direct and delayed density dependence in red fox dynamics and concomitant shifts in fluctuation patterns were observed. Our statistical analyses also revealed that the spatial progressive spread of mange mites was mirrored in the autocovariate structures of red fox populations progressively exposed to sarcoptic mange.     

Clinical Picture and Antibody Response to Experimental Sarcoptes scabiei var. vulpes Infection in Red Foxes (Vulpes vulpes)

Three red foxes (Vulpes vulpes) were experimentally infected with Sarcoptes scabiei isolated from a naturally infected wild red fox. A fourth red fox served as a control. The first signs of sarcoptic mange became evident on the 31st day post infection (dpi). The signs gradually increased thereafter and between dpi 49 and 77 characteristic lesions of hyperkeratosis developed. Two of the infected foxes developed severe sarcoptic mange, and one of these animals died on dpi 121. The third fox developed a chronic hyperkeratotic lesion on its back, at the site where the mites had been applied. On dpi 127 the surviving foxes were treated systemically with ivermectin, and within 4 weeks the skin lesions had healed except on the pinnae of one animal. Antibodies to S. scabiei var. vulpes were demonstrated in the infected foxes by an ELISA with which seroconversion was seen around 4 weeks post infection (wpi). Western blot analysis of sequential sera of the infected animals demonstrated antibody activity consistently after the 2nd wpi. The fourth, non-infected, fox did not show any skin lesions throughout the experimental period nor any specific antibodies to S. scabiei var. vulpes. kw|Keywords|k]sarcoptic mange; k]red fox; k]serodiagnosis; k]ELISA     

Demonstrating frequency-dependent transmission of sarcoptic mange in red foxes

Understanding the relationship between disease transmission and host density is essential for predicting disease spread and control. Using long-term data on sarcoptic mange in a red fox Vulpes vulpes population, we tested long-held assumptions of density- and frequency-dependent direct disease transmission. We also assessed the role of indirect transmission. Contrary to assumptions typical of epidemiological models, mange dynamics are better explained by frequency-dependent disease transmission than by density-dependent transmission in this canid. We found no support for indirect transmission. We present the first estimates of R₀ and age-specific transmission coefficients for mange in foxes. These parameters are important for managing this poorly understood but highly contagious and economically damaging disease.     

Sarcoptic mange vulnerability in carnivores of the Białowieża Primeval Forest,Poland: underlying determinant factors

Sarcoptic mange caused by Sarcoptes scabiei, is a highly contagious worldwide mite infection responsible for epizootic skin disease in populations of wild and domestic mammals. It causes skin disorders that may lead to severe generalized skin disease (mange). We investigated the spread and dynamics of sarcoptic mange in one of the best preserved carnivore communities in the Bia?owie?a Primeval Forest over the last 20 years. Sarcoptic mange was found in 6 of 10 investigated species. The highest percentage of infected individuals was recorded in red foxes (19 %), European badgers (9 %), grey wolves (7 %), raccoon dogs (6 %), and stone martens (5 %). Other species were not infected (least weasel, American mink, European polecat, pine marten) or infected sporadically (Eurasian lynx––1 case). Rate of infection was correlated with the sum of ecological and behavioral features, which may increase the spread of infection. Outbreaks of sarcoptic mange occurred simultaneously in several species of carnivores, which indicates the occurrence of between species transmission. We found that the source of investigated individuals (trapped, culled and found dead) may influence the results of the analysis. Our study shows that in carnivore communities such as in Bia?owie?a Forest, numerous species may serve as a reservoir of the pathogen and favor its persistence in the environment. This study indicates that sociality and use of den sites are important factors affecting sarcoptic mange spread and prevalence in wild populations of carnivores.     

An Invasive Vector of Zoonotic Disease Sustained by Anthropogenic Resources: The Raccoon Dog in Northern Europe

The raccoon dog (Nyctereutes procyonoides) is an introduced species in Europe with a continually expanding range. Since the species is capable of affecting local ecosystems and is a vector for a number of severe zoonotic diseases, it is important to understand its food habits. Raccoon dog diet was studied in Estonia by examining the contents of 223 stomach samples collected during the coldest period of the year, August to March, in 2010–2012. The most frequently consumed food categories were anthropogenic plants (e.g. cereals, fruits; FO = 56.1%) and carrion (e.g. carcasses of artiodactyls and carnivores; FO = 48.4%). Carrion was also the only food category that was consumed significantly more frequently by raccoon dogs exhibiting symptoms of sarcoptic mange than by uninfected animals. Small mammals, which represent intermediate hosts for the zoonotic tapeworm Echinococcus multilocularis, were more commonly recorded in samples also containing anthropogenic plants than expected by chance. Comparison of raccoon dog and red fox (Vulpes vulpes) diet in Estonia revealed higher overlap than found elsewhere in Europe, with ‘carrion’ and ‘anthropogenic plants’ making up the bulk of both species’ diet; however, raccoon dogs were more omnivorous than red foxes. Our results suggest that while the use of most food categories reflects the phenology of natural food sources, ‘anthropogenic plants’ and ‘carrion’ provide an essential resource for raccoon dogs during the coldest period of the year, with the latter resource especially important for individuals infected with sarcoptic mange. Since both of these food categories and small mammals are often found at supplementary feeding sites for wild boar (Sus scrofa), this game management practice may facilitate high densities of mesocarnivores and promote the spread of some severe zoonotic diseases, including alveolar echinococcosis, trichinellosis, rabies and sarcoptic mange.     

Cyclic voles, prey switching in red fox, and roe deer dynamics – a test of the alternative prey hypothesis

Medium-sized predators sometimes switch to alternative prey species as their main prey declines. Our objective of this study was to test the alternative prey hypothesis for a medium sized predator (red fox, Vulpes vulpes ), a small cyclically fluctuating main prey (microtine voles) and larger alternative prey (roe deer fawns, Capreolus capreolus ). We used long-term time series (28 years) on voles, red fox and roe deer from the Grimsö Wildlife Research Area (59°40'N, 15°25'E) in south-central Sweden to investigate interspecific relationships in the annual fluctuations in numbers of the studied species. Annual variation in number of roe deer fawns in autumn was significantly and positively related to vole density and significantly and negatively related to the number of fox litters in the previous year. In years of high vole density, predation on roe deer fawns was small, but in years of low vole density predation was more severe. The time lag between number of fox litters and predation on fawns was due to the time lag in functional response of red fox in relation to voles. This study demonstrates for the first time that the alternative prey hypothesis is applicable to the system red fox, voles and roe deer fawns.     

Synchronous and nonsynchronous population fluctuations of some predators and their prey in central Sweden

To test the alternative prey hypothesis (APH), we examined 29-yr time series of bank voles (indexed by snap-trapping) and 6 game species (indexed by bag records) from Gavleborg county, central Sweden, for the occurrence of synchronous population fluctuations Only voles and the 3 grouse species exhibited cyclic fluctuations, grouse fluctuations were highly synchronous, and positively correlated with vole fluctuations Although hares were positively correlated with grouse, they were negatively correlated with voles Fox were positively correlated with voles and grouse, however, a strong negative relationship was observed between fox and hares During a sharp decline in fox numbers during the early 1980's due to sarcoptic mange, both grouse and hares exhibited a strong positive numerical response, but, not in synchrony In addition, grouse exhibited large fluctuations during the fox decrease whereas hares did not Due to the contradictory predator-prey interactions observed, these results provide only partial support for APH     

Development of resistance to sarcoptic mange in ibex

Sarcoptic mange affects mammal host species worldwide and, particularly, wild Caprinae throughout much of Eurasia. In the Iberian Peninsula, several outbreaks of sarcoptic mange in Iberian ibex (Capra pyrenaica) have been reported since the 1980s. Using data from a period of long-term monitoring and a seasonal autoregressive integrated moving average (SARIMA)-generalized autoregressive conditional heteroscedasticity (GARCH) model approach, we performed a time-series analysis of the monthly prevalence of sarcoptic mange in the Iberian ibex population in Sierra Nevada Natural Space in southern Spain. In January 2003–March 2021, we documented a significant negative trend in sarcoptic mange prevalence, albeit with some interannual peaks. These findings can only be explained if a certain level of resistance to sarcoptic mange exists in hosts that, along with other factors, could provoke this reduced prevalence. Prevalence values varied seasonally, with maximum values in spring and minimum values at the end of summer, which may be due to factors linked to climate, host behavior, and endocrine activity. Our model predicts that the prevalence of sarcoptic mange in the Iberian ibex will continue to decrease over the next 2 years. Despite the inherent challenges involved, diagnosing and monitoring of wildlife diseases are integral to obtaining reliable epidemiological data and designing appropriate management strategies.     

Sarcoptic mange in raccoons in Michigan

Sarcoptic mange is a cause of pruritic skin disease in domestic dogs and a wide range of wildlife species. We describe sarcoptic mange in free-ranging raccoons (Procyon lotor). Three adult raccoons from upper Wayne County, Michigan (USA), were captured, killed, and submitted for diagnostic evaluation. The animals were intensely pruritic, and two had advanced alopecic and crusting lesions over their dorsum and hind limbs. Skin scrapings and skin biopsies revealed crusting and hyperkeratotic dermatitis with high numbers of Sarcoptes scabiei adults, larvae, nymphs, and eggs. These raccoons were not otherwise debilitated, with minimal internal parasites, good body condition, and no evidence of infectious bacterial or viral diseases. Because sarcoptic mange is highly contagious and affects many species, including humans, transiently, it is important that wildlife biologists and rehabilitators include sarcoptic mange in their differential list for raccoons exhibiting pruritus and alopecia.     

Survival and Cause-Specific Mortality of Red Foxes in Agricultural and Urban Areas of Illinois

Abstract: Range expansion and population increase by coyotes (Canis latrans), reduced hunting and trapping, and intensified agricultural practices in the Midwest have altered red fox (Vulpes vulpes) mortality, although relative impacts of these factors are unknown. We examined mortality causes and survival of red foxes in urban and rural agricultural areas of Illinois, using radio telemetry data from 335 foxes (Nov 1996 to May 2002). We used Akaike's Information Criterion to evaluate six survival models for foxes reflecting 1) environmental effects, 2) intrinsic effects, 3) temporal effects, 4) behavioral effects, 5) social effects, and 6) a global model. Environmental and intrinsic models of survival were optimal for adult foxes. Adult foxes with low (0-20%) and high (80-100%) percentages of row crops in their home ranges had higher survival than adults with moderate percentages (40-70%). Heavier adults at capture also survived better. A global model (all covariates) was optimal for juvenile foxes. Higher juvenile survival associated with larger litters, lower body fat, and reduced dispersal time. Yearly survival ranged from 0.18 for rural male juveniles to 0.44 for rural female adults. Adult survival rates (0.35) were 11% higher than juvenile survival rates (0.24). Yearly survival varied for urban foxes due to cyclic outbreaks of sarcoptic mange (Sarcoptes scabei). Thus, summer survival (May-Sep) of urban juveniles ranged from 0.10 (mange present) to 0.83 (no mange recorded). Mange was the most common (45% of all fatalities) source of mortality for urban foxes, followed by road kill (31%). We recorded only 4 mange fatalities (2%) for rural foxes. Rural foxes experienced low hunting mortality (7%) and equivalent road kill and coyote predation fatalities (40% each). Sources of mortality for midwestern foxes have dramatically changed since the 1970s when hunting was the major cause of mortality. Coyote predation has effectively replaced hunting mortality, and cyclic patterns of mange outbreaks in urban fox populations might indicate a dynamic source or sink relationship to surrounding rural fox populations. Absent mange, urban areas might provide refugia for red foxes where coyote populations persist at high densities in rural areas. Managers of sympatric urban and rural wildlife populations must understand survival dynamics influencing the population at the landscape level.     

Trophic niche overlap and wild ungulate consumption by red fox and wolf in a mountain area in Italy

Red fox (Vulpes vulpes) and wolf (Canis lupus) are two widespread opportunistic predators living in simpatry in many areas. Nonetheless, scarce information are available on their trophic interactions. We investigated food habits of these two carnivores in a mountain area in Italy and assessed the extent of their trophic niche overlap, focusing on the consumption of wild ungulates. Thereby we analyzed the content of 669 red fox scats and 253 wolf scats collected between May 2008 and April 2009. Red foxes resulted to have a more than three times higher niche breadth than wolves. Vegetables, small mammals, wild ungulates, and invertebrates were major items (altogether 92% of volume) of the red fox annual diet. On the contrary wolf annual diet relied on wild ungulates (94% of volume) with wild boar (Sus scrofa) being the main food item. The degree of trophic niche overlap between the two species was found to be low (Pianka's O = 0.356). Diet variation between the warm and the cold seasons was limited in both species, and higher in red fox than in wolf. The two canids appeared to use wild ungulates unevenly being the former more selective for younger preys, smaller in size (newborn piglets and roe deer Capreolus capreolus fawns), whereas the latter exhibited a preference for medium-sized and large ungulates (10–35 kg wild boar and adult roe deer). Even if wild ungulates represent the main shared food category, the different use of age/weight classes by the two predators, together with their possible consumption as carrions by red fox, suggests a very limited trophic competition between wolf and red fox.This study represents a contribution to the knowledge of trophic interaction in predator–prey systems where sympatric carnivores are present.     

Immune response induced by candidate Sarcoptes scabiei var. cuniculi DNA vaccine encoding paramyosin in mice

Sarcoptes scabiei is the causal agent of the highly contagious disease sarcoptic mange (scabies) that affects animals and humans worldwide. An increasing number of cases of treatment failure is being reported because of drug resistance. The development of a specific vaccine would be a sustainable option for control of this disease. In this study, we cloned and expressed a S. scabiei gene encoding paramyosin (PAR) and investigated the immune response elicited by DNA encoding PAR in mice. The ability of the DNA vaccine to express antigen in COS-7 cells was confirmed by RT-PCR and IFA. The immune response induced by DNA vaccine was investigated by ELISA, splenocyte proliferation assay, and cytokine production assay. Compared to the pVAX1 control group, the PAR DNA vaccination group showed the higher levels of IgG, IgG1, IgG2a, IgE, IgM, stronger lymphocyte proliferation in mouse spleen, and larger production of IL-2, IL-4, IL-5, and IFN-γ in the supernatant of cultures from splenocytes. These results indicated that the PAR DNA vaccine induced a mixed Th1/Th2 response in mice. In conclusion, our results revealed that the S. scabiei PAR DNA vaccine induced both a humoral and cellular immune response, which would provide basic data for the further study to develop an effective vaccine against sarcoptic mange.     

Morbidity and mortality of red foxes (Vulpes vulpes) and gray foxes (Urocyon cinereoargenteus) admitted to the Wildlife Center of Virginia, 1993-2001

The medical records of 48 red foxes (Vulpes vulpes) and 35 gray foxes (Urocyon cinereoargenteus) examined at the Wildlife Center of Virginia (Waynesboro, Virginia, USA) from 1993 to 2001 were reviewed. The most common diagnosis in red foxes was orphaned (33%), followed by trauma (27%), undetermined diagnosis (23%), and sarcoptic mange (17%). Trauma (46%) was the most frequent cause of morbidity and mortality in gray foxes followed by orphaned (23%), undetermined (20%), toxoplasmosis (6%), presumptive canine distemper (3%), and rabies (3%). One gray fox had concurrent toxoplasmosis and presumptive canine distemper (3%). Similar diseases were detected in previous studies at a diagnostic laboratory; however in this study, trauma and orphaned animals were more common than infectious diseases. The lack of diagnostic information on some cases limited the usefulness of this study, and more emphasis should be placed on performing postmortem examinations of wildlife presented to wildlife rehabilitation centers.     

Sarcoptes scabiei: The Mange Mite with Mighty Effects on the Common Wombat (Vombatus ursinus)

Parasitism has both direct and indirect effects on hosts. Indirect effects (such as behavioural changes) may be common, although are often poorly described. This study examined sarcoptic mange (caused by the mite Sarcoptes scabiei) in the common wombat (Vombatus ursinus), a species that shows severe symptoms of infection and often causes mortality. Wombats showed alterations to above ground behaviours associated with mange. Infected wombats were shown to be active outside of the burrow for longer than healthy individuals. Additionally, they spent more time scratching and drinking, and less time walking as a proportion of time spent above ground when compared with healthy individuals. They did not spend a higher proportion of time feeding, but did have a slower feeding rate and were in poorer body condition. Thermal images showed that wombats with mange lost considerably more heat to the environment due to a diminished insulation layer. Infection status did not have an effect on burrow emergence time, although this was strongly dependent on maximum daily temperature. This study, through the most detailed behavioural observations of wombats to date, contributes to a broader understanding of how mange affects wombat health and abundance, and also to our understanding of the evolution of host responses to this parasite. Despite being globally dispersed and impacting over 100 species with diverse intrinsic host traits, the effects of mange on hosts are relatively poorly understood, and it is possible that similar effects of this disease are conserved in other host species. The indirect effects that we observed may extend to other pathogen types.     

Functional responses of an apex predator and a mesopredator to an invading ungulate: Dingoes,red foxes and sambar deer in south‐east Australia

Biological invasions by large herbivores involve the establishment of novel interactions with the receiving mammalian carnivore community, but understanding these interactions is difficult due to the large spatiotemporal scales at which such dynamics would occur. We quantified the functional responses of a native apex predator (the dingo (Canis familiaris), which includes wild dogs and their hybrids) and a non‐native mesopredator (red fox; Vulpes vulpes) to an invading non‐native ungulate (sambar deer; Cervus unicolor) in Australia. We predicted that the apex predator would exhibit a stronger functional response to increasing sambar deer abundance than the mesopredator. We used a state–space model to link two 30‐year time series: (i) sambar deer abundance (hunter catch‐per‐unit‐effort); and (ii) percentages of sambar deer in dingo (N = 4531) and fox (N = 5002) scats. Sambar deer abundance increased over fourfold during 1984?2013. The percentages of sambar deer in dingo and fox scats increased during this 30‐year period, from nil in both species in 1984 to 8.2% in dingoes and 0.5% in foxes in 2013. Dingoes exhibited a much stronger functional response to increasing sambar deer abundance than foxes. The prediction that invading deer would be utilized more by the apex predator than by the mesopredator was therefore supported. The increasing abundance of sambar deer during the period 1984?2013 provided an increasingly important food source for dingoes. In contrast, the smaller red fox utilized sambar deer much less. Our study demonstrates that prey enrichment can be an important consequence of large herbivore invasions and that the effect varies predictably with the trophic position of the mammalian carnivores in the receiving community.     

Arctic fox versus red fox in the warming Arctic: four decades of den surveys in north Yukon

During the last century, the red fox (Vulpes vulpes) has expanded its distribution into the Arctic, where it competes with the arctic fox (Vulpes lagopus), an ecologically similar tundra predator. The red fox expansion correlates with climate warming, and the ultimate determinant of the outcome of the competition between the two species is hypothesized to be climate. We conducted aerial and ground fox den surveys in the northern Yukon (Herschel Island and the coastal mainland) to investigate the relative abundance of red and arctic foxes over the last four decades. This region has undergone the most intense warming observed in North America, and we hypothesized that this climate change led to increasing dominance of red fox over arctic fox. Results of recent surveys fall within the range of previous ones, indicating little change in the relative abundance of the two species. North Yukon fox dens are mostly occupied by arctic fox, with active red fox dens occurring sympatrically. While vegetation changes have been reported, there is no indication that secondary productivity and food abundance for foxes have increased. Our study shows that in the western Arctic of North America, where climate warming was intense, the competitive balance between red and arctic foxes changed little in 40?years. Our results challenge the hypotheses linking climate to red fox expansion, and we discuss how climate warming’s negative effects on predators may be overriding positive effects of milder temperatures and longer growing seasons.     

Sarcoptes scabiei: Specific immune response to sarcoptic mange in the Iberian ibex Capra pyrenaica depends on previous exposure and sex

Host acquired immunity is a critical factor that conditions the survival of parasites. Nevertheless, there is a shortage of data concerning inter-individual immunological inequalities in wild mammals. Sarcoptic mange is a widespread parasitosis that severely affects mammals such as the Iberian ibex (Capra pyrenaica). Despite some work on the subject, the immune response to sarcoptic mange infestation is still a complex and poorly understood phenomenon. To improve knowledge of the host-Sarcoptes immunological interaction, 18 Iberian ibexes were experimentally infested. IgG levels were assessed using ELISA to test for potential factors determining the specific immune response to infestation. Previous exposure and sex appeared to affect the IgG response to infestation and our results suggest a sex-biased immunomodulation. We discuss the immunological pattern of host-Sarcoptes interactions and also suggest further lines of work that may improve the understanding of immunological interactions of host-Sarcoptes systems.     

Fox predation on cyclic field vole populations in Britain

The diet of the red fox Vulpes vulpes L. was studied during three winter periods in spruce pklantations in Britain, during which time the cyclic field vole Microtus agrestis L. populations varied in abundance. Field voles and roe deer Capreolus capreolus L. were the two main prey species in the diet of the red fox. The contribution of lagomorphs to fox diet never exceeded 35% and species of small mammal other than field voles were of minor importance. The contribution of field voles was dependent on vole density. The non-linear density dependent relationship with a rather abrupt increase of field voles in fox did when vole density exceeded ca 100 voles ha⁻¹ was consistent with a prey-switching response. The contribution of field voles to fox diet during the low phase of population cycles was lower in Kielder Forest than in other ecosystems with cyclic vole populations. The number of foxes killed annually by forestry rangers was consistent with the evidence from other studies that foxes preying on cyclic small rodents might show a delayed numerical response to changes in vole abundance. Estimates of the maximum predation rate of the fox alone (200–290 voles ha⁻¹ of vole habitat year⁻¹) was well above a previously predicted value for the whole generalist predator community in Kielder Forest. Our data on the functional response of red foxes and estimates of their predation rates suggest that foxes should have a strong stabilising impact on vole populations, yet voles show characteristic 3-4 yr cycles.     

First description of sarcoptic mange in wild European rabbit (Oryctolagus cuniculus)

The European wild rabbit (Oryctolagus cuniculus) is a keystone species in the Iberian Mediterranean ecosystems being the staple prey of protected and endangered predators. Wild rabbits were once widespread, but the introduction of two viral diseases, myxomatosis in the 1950s and the rabbit hemorrhagic disease in 1989, resulted into a dramatic decline of its populations. Sarcoptic mange is a highly contagious parasitic infection caused by Sarcoptes scabiei. The first cases of sarcoptic mange in a wild rabbit population are recorded from a hunting area in Majorca (Balearic Islands, Spain). Five of 32 inspected rabbits (14.7%) were affected, with similar prevalences in summer and autumn. Sarcoptes scabiei were obtained from the edge of the lesions of two of the rabbits. The most frequently observed lesions were small areas of alopecia and crusts in the limbs. Affected limbs presented also a marked hypertrichosis and an apparent abnormal growth of the nails. One rabbit also presented lesions around mouth and nostrils. Parasitized rabbits were in significant lower body condition than healthy ones. According to previous reports of mange epizooties in other naïve wild species that caused marked short-term effects in their populations, this disease may pose a risk for the conservation of wild rabbit and their predators. Whether mange is endemic in rabbits from Majorca or it has been introduced is unknown. Game managers are encouraged to be aware of introducing sarcoptic mange during rabbit translocations.