USE OF FLUMETHRIN-IMPREGNATED COLLARS TO MANAGE AN EPIDEMIC OF SARCOPTIC MANGE IN AN URBAN POPULATION OF ENDANGERED SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA).

Sarcoptic mange epidemics can have long-lasting impacts on susceptible wildlife populations, potentially contributing to local population declines and extirpation. Since 2013, there have been 460 reported cases of sarcoptic mange in an urban population of endangered San Joaquin kit foxes (Vulpes macrotis mutica) in Bakersfield, CA, with many of them resulting in fatality. As part of a multifaceted response to mitigate mange-caused mortalities and reduce this conservation threat, a 2-yr randomized field trial was conducted to assess the efficacy of long-acting flumethrin collars against sarcoptic mange in kit foxes. Thirty-five kit foxes living in a high-density population on a college campus were captured, examined, administered selamectin, and each fox randomly assigned to either receive a flumethrin collar placed within a VHF radio collar or a VHF radio collar without flumethrin. The survival and mange-infestation status of study animals was monitored via radio telemetry, remote cameras, and periodic recapture examinations and compared among treated and control kit foxes using a Cox proportional hazards model. The average time to onset of mange for treated kit foxes (176 days) was similar to controls (171 days) and treatment with flumethrin did not significantly reduce mange risk for all kit foxes. Kit foxes that had a mild mange infestation at the beginning of the study were four times more likely to develop mange again, regardless of flumethrin treatment, compared with kit foxes that had no signs at initial recruitment. This study demonstrates an approach to evaluating population-level protection and contributes to the limited literature on efficacy, safety, and practicality of acaricides in free-ranging wildlife.

A Novel Hazard for an Endangered Fox in a Novel Environment.

Animals colonizing novel environments can encounter novel hazards. Endangered San Joaquin kit foxes (Vulpes macrotis mutica) are found in the cities of Bakersfield and Taft in central California, USA. We documented 66 incidents of kit foxes becoming entangled in sports netting (e.g., soccer nets, batting-cage nets) occurring from the 1980s through 2022. Overall, 25 of the foxes died. Adults were more likely to get entangled in soccer nets, whereas pups (<1 yr) were more likely to get entangled in batting-cage nets. Pups are more likely to die while entangled, probably due to smaller body mass and lower energy reserves. The reasons that kit foxes get entangled in netting were unclear, although incidents involving batting-cage netting and pups may be due to natal dens being located under or near batting cages. At current rates, this hazard is unlikely to limit urban kit fox populations. However, losses of this endangered species should be minimized and the incidents are easily mitigated by dropping or lifting nets when not in use.

Syntopy between Endangered San Joaquin Kit Foxes and Potential Competitors in an Urban Environment.

The endangered San Joaquin kit fox (Vulpes macrotis mutica; SJKF) occurs in the city of Bakersfield, CA, where several putative competitors also occur, including domestic cats (Felis catus), striped skunks (Mephitis mephitis), raccoons (Procyon lotor), and opossums (Didephis virginiana). We used data from a multi-year (2015-2022) city-wide camera station survey to assess whether the other species were simply sympatric with SJKF or coexisting syntopically (i.e., occurring in the same habitats without apparent competition). Annual detection rates for the other species were not correlated with SJKF rates either within SJKF habitat suitability categories (low, medium, and high) or for all categories combined. Also, detection rates for the other species did not increase in response to a significant decline in SJKF abundance caused by sarcoptic mange. The use of all SJKF habitat suitability categories by the other species and co-detections with SJKF at camera stations indicate high spatial overlap. Interference and exploitative competition between the species are apparently negligible, likely due to similar body sizes and high resource abundance. Thus, SJKF and the other species appear to be coexisting syntopically in the urban environment, resulting in a significant additional SJKF population that facilitates range-wide conservation and recovery of this endangered species.

MOVEMENTS BY SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA) BETWEEN URBAN AND NONURBAN HABITATS: IMPLICATIONS FOR INTERPOPULATION DISEASE TRANSFER.

Sarcoptic mange epidemics erupted in two of the remaining populations of endangered San Joaquin kit foxes (Vulpes macrotis mutica). Both populations are in urban habitats in the cities of Bakersfield and Taft, California, USA. The risk of disease spread from the two urban populations to nearby nonurban populations, and then throughout the species range, is of considerable conservation concern. To date, mange has not been detected in any nonurban populations despite considerable surveillance effort. The reasons for the lack of detections of mange among nonurban foxes are unknown. We monitored urban kit fox movements using geographic positioning system (GPS) collars to test the hypothesis that urban foxes were not venturing into nonurban habitats. Of 24 foxes monitored December 2018 to November 2019, 19 (79%) made excursions from urban into nonurban habitats from 1-124 times. The mean number of excursions per 30 d was 5.5 (range 0.1-13.9 d). The mean proportion of locations in nonurban habitats was 29.0% (range 0.6-99.7%). The mean maximum distance that foxes traveled into nonurban areas from the urban-nonurban interface was 1.1 km (range 0.1-2.9 km). Mean number of excursions, proportion of nonurban locations, and maximum distance into nonurban habitats were similar between Bakersfield and Taft, females and males, and adults and juveniles. At least eight foxes apparently used dens in nonurban habitats; shared use of dens may be an important mode of mange mite transmission between conspecifics. Two of the collared foxes died of mange during the study and two others had mange when captured at the end of the study. Three of these four foxes had made excursions into nonurban habitats. These results confirm a significant potential for mange to spread from urban to nonurban kit fox populations. We recommend continued surveillance in nonurban populations and continued treatment efforts in the affected urban populations.

Intraguild Competition between Endangered Kit Foxes and a Novel Predator in a Novel Environment.

A population of endangered San Joaquin kit foxes inhabits the urban environment in the city of Bakersfield, California, United States. This population is considered important for the conservation and recovery of this species. In this novel environment, kit foxes encounter a novel competitor, that being non-native red foxes. We examined exploitative and interference competition between these two species. Based on scat analysis, both species consumed similar foods and dietary overlap was high. Red foxes also were found to usurp kit fox dens. Direct mortality to kit foxes from red foxes appears to be rare. Kit foxes and red foxes also appear to overlap spatially, although we found evidence of temporal partitioning of shared space. Based on binary logistic regression modeling, habitat attributes in grid cells used by the two species generally were similar, consistent with the spatial overlap. However, differences in specific attributes indicated that kit foxes are more likely to use areas with smaller open spaces and more human activity compared to red foxes. Competition from red foxes may be mitigated by several factors. Critical resources such as food and dens may be sufficiently abundant such that they are not a limiting factor. Some degree of spatial segregation and temporal partitioning of shared space may reduce interference competition. These factors may facilitate coexistence, and consequently, red foxes do not currently appear to constitute a significant competitive risk to this important population of endangered San Joaquin kit foxes.

Molecular epidemiology of a fatal sarcoptic mange epidemic in endangered San Joaquin kit foxes (Vulpes macrotis mutica).

BACKGROUND: In 2013, sarcoptic mange, caused by Sarcoptes scabiei mites, precipitated a catastrophic decline of the formerly stable urban population of endangered San Joaquin kit foxes (Vulpes macrotis mutica) in Bakersfield, California, USA. In 2019, a smaller sarcoptic mange outbreak affected kit foxes 58 km southwest of Bakersfield in the town of Taft, California. To determine whether the Taft outbreak could have occurred as spillover from the Bakersfield outbreak and whether epidemic control efforts must involve not only kit foxes but also sympatric dogs (Canis lupus familiaris), coyotes (Canis latrans), and red foxes (Vulpes vulpes), we evaluated genotypes and gene flow among mites collected from each host species. METHODS: We used 10 Sarcoptes microsatellite markers (SARM) to perform molecular typing of 445 S. scabiei mites collected from skin scrapings from twenty-two infested kit foxes, two dogs, five coyotes, and five red foxes from Bakersfield, Taft, and other nearby cities. RESULTS: We identified 60 alleles across all SARM loci; kit fox- and red fox-derived mites were relatively monomorphic, while genetic variability was greatest in Bakersfield coyote- and dog-derived mites. AMOVA analysis documented distinct mite populations unique to hosts, with an overall FST of 0.467. The lowest FST (i.e. closest genetic relationship, FST = 0.038) was between Bakersfield and Taft kit fox-derived mites while the largest genetic difference was between Ventura coyote- and Taft kit fox-derived mites (FST = 0.843). CONCLUSIONS: These results confirm the close relationship between the Taft and Bakersfield outbreaks. Although a spillover event likely initiated the kit fox mange outbreak, mite transmission is now primarily kit fox-to-kit fox. Therefore, any large-scale population level intervention should focus on treating kit foxes within the city.

Assessing the role of dens in the spread, establishment and persistence of sarcoptic mange in an endangered canid.

Sarcoptic mange is a skin disease caused by the mite Sarcoptes scabiei that can devastate populations of wild species. S. scabiei can survive off-host and remain infective for specific periods. In den-dwelling species, dislodged mites could be protected from the environmental conditions that impair their survival thus supporting pathogen transmission. To assess the potential role of dens in the spread, establishment, and persistence of sarcoptic mange in a population of hosts, we constructed an agent-based model of the endangered San Joaquin kit fox (SJKF; Vulpes macrotis mutica) population in Bakersfield, California, that explicitly considered the denning ecology and behavior of this species. We focused on this SJKF urban population because of their vulnerability and because a sarcoptic mange epizootic is currently ongoing. Further, SJKF is a social species that lives in family groups year-round and contact between individuals from different family groups is rare, but they will occupy the same dens intermittently. If mites remain infective in dens, they could support intra-family disease transmission via direct (den sharing) and indirect (contaminated den) contact, but also inter-family transmission if susceptible individuals from different families occupy contaminated dens. Simulations showed that den-associated transmission significantly increases the chances for the mite to spread, to establish and to persist. These findings hold for different within-den S. scabiei off-host survival periods assessed. Managers dealing with S. scabiei in this species as well as in other den-dwelling species should consider den-associated transmission as they could be targeted as part of the control strategies against this mite.

Land use change and rodenticide exposure trump climate change as the biggest stressors to San Joaquin kit fox.

Animal and plant species often face multiple threats simultaneously. We explored the relative impact of three major threats on populations of the endangered San Joaquin kit fox. This species was once widely distributed across the southern San Joaquin Valley, California, USA, but agriculture and urban development have replaced much of its natural habitat. We modeled impacts of climate change, land-use change, and rodenticide exposure on kit fox populations using a spatially explicit, individual-based population model from 2000 to 2050 for the Central Valley, California. Our study indicates that land-use change will likely have the largest impact on kit fox populations. Land development has the potential to decrease populations by approximately 15% under a compact growth scenario in which projected population increases are accommodated within existing urban areas, and 17% under a business-as-usual scenario in which future population growth increases the developed area around urban centers. Plausible scenarios for exposure to pesticides suggest a reduction in kit fox populations by approximately 13%. By contrast, climate change has the potential to ameliorate some of these impacts. Climate-change induced vegetation shifts have the potential to increase total available kit fox habitat and could drive population increases of up to 7%. These vegetation shifts could also reduce movement barriers and create opportunities for hybridization between the endangered San Joaquin kit fox and the more widely distributed desert kit fox, found in the Mojave Desert. In contrast to these beneficial impacts, increasing climate extremes raise the probability of the kit fox population dropping below critical levels. Taken together, these results paint a complex picture of how an at-risk species is likely to respond to multiple threats.

Assessing personality in San Joaquin kit fox in situ: efficacy of field-based experimental methods and implications for conservation management.

Utilisation of animal personality has potential benefit for conservation management. Due to logistics of robust behavioural evaluation in situ, the majority of studies on wild animals involve taking animals into captivity for testing, potentially compromising results. Three in situ tests for evaluation of boldness in San Joaquin kit fox (Vulpes macrotis mutica) were developed (ENOT: extended novel object test; RNOT: rapid novel object test; TH: trap/handling test). Each test successfully identified variation in boldness within its target age class(es). The TH test was suitable for use across all age classes. Tests were assessed for in situ suitability and for quantity/quality of data yielded. ENOT was rated as requiring high levels of time, cost and labour with greater likelihood of failure. However, it was rated highly for data quantity/quality. The TH test was rated as requiring little time, labour and cost, but yielding lower quality data. RNOT was rated in the middle. Each test had merit and could be adapted to suit project or species constraints. We recommend field-based evaluation of personality, reducing removal of animals from the wild and facilitating routine incorporation of personality assessment into conservation projects.

Comparison of Flea (Siphonaptera) Burdens on the Endangered San Joaquin Kit Fox (Vulpes macrotis mutica (Carnivora, Canidae)) Inhabiting Urban and Nonurban Environments in Central Valley, California.

The San Joaquin kit fox (Vulpes macrotis mutica Merriam (Carnivora, Canidae)) is an endangered small carnivore endemic to the San Joaquin Valley of California. Commercial and agricultural land expansion has contributed to the species' decline and invasion of more cosmopolitan species, providing means for potential ecological shifts in disease vector and host species. Fleas are common ectoparasites that can serve as important indicators of cross-species interactions and disease risk. We compared flea load and species composition on kit foxes inhabiting urban and nonurban habitats to determine how urbanization affects flea diversity and potential disease spillover from co-occurring species. We identified Echidnophaga gallinacea (Westwood) (Siphonaptera, Pulicidae) and Pulex spp. (L.) in both urban and nonurban populations, and Ctenocephalides felis (Bouche) (Siphonaptera, Pulicidae) only in the urban population. Flea load scores differed significantly across capture sites and with respect to concomitant sarcoptic mange infestation in the urban population, with milder flea infestations more typical of healthy foxes. All observed flea species are known vectors for pathogens that have been detected in mesocarnivores. Further examination of kit fox fleas and their associated pathogens will help to direct conservation and disease preventive measures for both wildlife and humans in the region.

SARCOPTIC MANGE IN ENDANGERED KIT FOXES (VULPES MACROTIS MUTICA): CASE HISTORIES, DIAGNOSES, AND IMPLICATIONS FOR CONSERVATION.

The San Joaquin kit fox ( Vulpes macrotis mutica) is a federally endangered small carnivore whose distribution is limited to the San Joaquin Valley in central California. Population decline is due to profound habitat loss, and conservation of all remaining populations is critical. A robust urban population occurs in the city of Bakersfield. In spring of 2013, putative cases of mange were reported in this population. Mites from affected animals were confirmed to be Sarcoptes scabiei morphologically and by DNA sequencing. By the end of 2014, 15 cases of kit foxes with mange had been confirmed. As with other species, sarcoptic mange in kit foxes is characterized by intense pruritus and dermatitis, caused by mites burrowing into the epidermal layers, as well as alopecia, hyperkeratosis, and encrustations, secondary bacterial infections, and finally extreme morbidity and death. Of the 15 cases, six foxes were found dead, six were captured but died during attempted rehabilitation, and three were successfully treated. We have no evidence that untreated kit foxes can recover from mange. Sarcoptic mange constitutes a significant threat to the Bakersfield kit fox population and could pose an even greater threat to this imperiled species if it spreads to populations in nearby natural lands.

Land Use as a Driver of Patterns of Rodenticide Exposure in Modeled Kit Fox Populations.

Although rodenticides are increasingly regulated, they nonetheless cause poisonings in many non-target wildlife species. Second-generation anticoagulant rodenticide use is common in agricultural and residential landscapes. Here, we use an individual-based population model to assess potential population-wide effects of rodenticide exposures on the endangered San Joaquin kit fox (Vulpes macrotis mutica). We estimate likelihood of rodenticide exposure across the species range for each land cover type based on a database of reported pesticide use and literature. Using a spatially-explicit population model, we find that 36% of modeled kit foxes are likely exposed, resulting in a 7-18% decline in the range-wide modeled kit fox population that can be linked to rodenticide use. Exposures of kit foxes in low-density developed areas accounted for 70% of the population-wide exposures to rodenticides. We conclude that exposures of non-target kit foxes could be greatly mitigated by reducing the use of second-generation anticoagulant rodenticides in low-density developed areas near vulnerable populations.