Identification of skunk species submitted for rabies testing in the desert southwest

Skunks usually are identified by their common name (skunk) when submitted for rabies testing. In the desert southwest (Arizona, New Mexico, Texas, USA; and northern Mexico), there are five species of skunks; four of which can occur in sympatry. To better understand the ecology of skunk rabies in these areas, it is imperative that species be properly identified. We used the displacement loop (d-loop) of the mitochondrial genome to identify to species 24 skunk brain samples submitted for rabies testing in New Mexico from 2001 to 2002. Most were identified as striped skunks (Mephitis mephitis), but hooded (Mephitis macroura) and hog-nosed (Conepatus leuconotus) skunks were also found.     

Habitat Use of Western Spotted Skunks and Striped Skunks in Texas

ABSTRACT Little information on foraging habitats of sympatric species of skunks in Texas, USA, is available. We compared 11 western spotted skunks (Spilogale gracilis) and 10 striped skunks (Mephitis mephitis) using radiotelemetry data to assess habitat use during foraging at broad levels of selection in a fragmented habitat. Western spotted skunks used areas with more large mesquite (Prosopis glandulosa) trees than did striped skunks and randomly selected points. Striped skunk habitat use was not different from randomly chosen locations. Contrary to previous research, both species appear to avoid agricultural habitat. A habitat management plan may be difficult to implement for striped skunks in Texas because they did not favor any available habitat. Conservation of western spotted skunks in west-central Texas should focus on areas with older mesquite trees, areas that are now often brush controlled for management of livestock.     

Presence of neutralizing antibodies to rabies virus in striped skunks from areas free of skunk rabies in Alberta

Nine percent of 198 serum samples from striped skunks, Mephitis mephitis (Schreber) from five areas of Alberta were positive for rabies neutralizing antibody. Positive samples were minimal (2%) from specimens sampled in an area enzootic for rabies and occurred at greater rates in areas negative for skunk rabies. Transmission of rabies virus to skunks may have been from a source other than skunks in those areas, most probably from bats.     

Rabies and rabies control in striped skunks (Mephitis mephitis) in three prairie regions of western North America

The number and geographic distribution of rabies cases in striped skunks (Mephitis mephitis) from Saskatchewan (n = 2,506 cases), Montana (n = 1,142), and Alberta (n = 199) since 1963 were reviewed. In Saskatchewan the number of cases increased steadily for 5 yr and then fluctuated consistently in a 4 yr cyclic pattern. Similarly an initial sweep across the province was followed by a cyclic pattern of geographic expansion (3 to 4 yr) and reduction (1 to 2 yr). No organized control efforts were conducted in Saskatchewan. Similar cyclic pattern were not seen in data from Montana or Alberta. In the latter areas, the number and distribution of rabies cases in skunks appeared to reflect efforts to reduce the population of skunks. An integrated program of skunk removal using poison and live-traps in association with research and public education successfully contributed to limiting the spread and establishment of rabies in striped skunks within prairie habitats. Rabies did not persist in skunks in other habitats.     

Rabies challenge of captive striped skunks (Mephitis mephitis) following oral administration of a live vaccinia-vectored rabies vaccine

Twenty-four adult striped skunks (Mephitis mephitis) were administered the raccoon product formulation of Rabies Vaccine, Live Vaccinia-Vectored (Raboral V-RG, Merial Limited, Athens, Georgia, USA), either by oral instillation or in vaccine-filled coated sachets either as single or multiple doses. A control group remained unvaccinated. Twenty-three of the skunks were challenged 116 days postvaccination with rabies virus (skunk isolate). Six of six naive skunks succumbed to challenge. Four of six skunks that received the vaccine by oral instillation survived challenge. The skunks that did not survive failed to seroconvert following vaccination. None of the skunks that accepted multiple doses of the vaccine offered in coated sachets survived challenge, nor were rabies virus-neutralizing antibodies (VNAs) detected in the sera. Likewise, none of the five skunks ingesting a single sachet developed VNA against rabies. However, in this group one skunk did survive rabies challenge. This preliminary study showed that the vaccinia-vectored oral rabies vaccine Raboral V-RG, as formulated for use in raccoons, is capable of protecting a percentage of skunks against rabies. However, although the fishmeal-coated sachets were readily consumed, subsequent challenge of these animals revealed poor vaccine delivery efficiency.     

High-density baiting with ONRAB® rabies vaccine baits to control Arctic-variant rabies in striped skunks in Ontario, Canada

The Arctic variant of rabies virus has been maintained in striped skunks in small foci in southwestern Ontario, Canada, despite the control of the disease in red foxes. To control the disease in skunks, high-density baiting with ONRAB(?) oral rabies vaccine baits was conducted by air and by hand distribution of baits in the vicinity of skunk cases. During 2009, antibody prevalences in skunks were higher in areas baited at a density of 300 baits/km(2) and flight-line spacing of 0.25 km than at 0.5-km spacing. Once an area containing Arctic-variant cases was treated with high densities of ONRAB baits, the disease did not reoccur in skunks in those areas. During 2009, only eight skunks were diagnosed with the Arctic variant of rabies virus in Ontario.     

Skunk rabies in California (1992-2003)--implications for oral rabies vaccination

Skunk-variant rabies is endemic in California (United States), and the development of oral vaccines and baits to vaccinate skunks is in progress. In 2003, the California Department of Public Health (CDPH) began to quantify the impacts of skunk-variant rabies and to assess the feasibility of using oral rabies vaccination (ORV) as a containment measure. The CDPH rabies case data for skunks were spatially depicted and analyzed using a geographic information system. Statewide, rabid skunks (1992-2003) primarily occurred in seven physiographic regions: Central Coast, North Coast, North Sierra, Sacramento Valley, San Francisco Bay and Delta, San Joaquin Valley, and South Sierra. Detailed analysis of rabid skunks in San Luis Obispo (SLO) and Santa Barbara (SB) counties showed that skunk rabies was endemic in the coastal plain of SLO County between 1992 and 2000, but only became epizootic in SB County during 2002. Despite the widespread distribution of striped skunks (Mephitis mephitis) throughout most of California, the skunk rabies variant has not been found in Los Angeles County since 1979. Results imply that future ORV campaigns for skunk-variant rabies in the Pacific Coastal Plain could deter spread from SLO into SB County, as well as deterring the reintroduction of skunk-variant rabies into southern California.     

Energetic consequences and ecological significance of heterothermy and social thermoregulation in striped skunks (Mephitis mephitis)

We assessed patterns and energetic consequences of different overwintering strategies, torpor, and social thermoregulation in the striped skunk (Mephitis mephitis) under natural ambient temperature and photoperiod. Striped skunks entered spontaneous daily torpor, with the lowest torpid body temperature (T(b)) reaching 26.0 degrees C, the lowest recorded T(b) for a carnivore. Patterns of daily torpor differed between solitary and grouped skunks: all solitary skunks regularly entered daily torpor, but only some individuals in communal dens employed torpor. When they did, it was shallow and infrequent. Solitary skunks entered torpor on average 50 times (in 120 d) compared with 6 times for grouped skunks. During torpor, solitary skunks had average minimum T(b) of 26.8 degrees C and bout duration of 7.8 h, whereas grouped skunks had average minimum T(b) of 30.9 degrees C and bout duration of 5.4 h. Torpor by solitary skunks occurred during their activity phase, but grouped skunks' shallow torpor bouts were restricted to their diurnal resting phase. On average, grouped skunks experienced lower percent daily fat loss, and they emerged in spring with higher percent body fat of 25.5%. In contrast, solitary skunks emerged in spring with only 9.3% body fat. In conclusion, the use of daily torpor and social thermoregulation in northern populations of striped skunks represent two strikingly different mechanisms to minimize energetic costs and increase individual fitness in response to unfavorable environmental conditions.     

Hepatitis in skunks caused by the virus of infectious canine hepatitis.

Two cases of acute, fatal, hepatitis occurred in young, striped skunks (Mephitis mephitis) trapped in southern Ontario. Histologically, lesions in the liver were similar to infectious canine hepatitis. A virus was isolated which produced large intranuclear inclusions in dog kidney cell cultures. These inclusions were Feulgen-positive and fluoresced green with acridine orange stain. The skunk hepatitis isolate was identified as the virus of infectious canine hepatitis by virus neutralization tests.     

Powassan virus in Ixodes cookei and Mustelidae in New England.

Powassan virus was recovered from a pool of 3 nymphal and 1 adult female Ixodes cookei removed from a striped skunk (Mephitis mephitis) trapped in Massachusetts during 1967 and from a pool of 9 nymphal I. cookei from a long-tailed weasel (Mustela frenata) captured in Connecticut during 1978. Virus was detected in the blood of both mammals. Hemagglutination-inhibiting (HI) antibody to Powassan virus was demonstrated in 16.0% of the skunks sampled in Connecticut, and neutralizing antibody was detected in 83.3% of the skunks tested from Massachusetts. HI antibody was found in 1 of 6 long-tailed weasels from Connecticut and 1 of 6 short-tailed weasels (Mustela erminea) from Maine.     

Experimental Toxoplasma gondii infection in striped skunk (Mephitis mephitis)

Twenty-three striped skunks (Mephitis mephitis) without demonstrable antibodies in 1:25 serum dilution in the modified agglutination test (MAT) were fed sporulated Toxoplasma gondii oocysts (9 skunks) or tissue cysts (10 skunks), and 4 skunks (controls) were not fed T. gondii. Skunks were bled before feeding T. gondii, 10 and 23- 25 days postinoculation (PI). All 9 seronegative skunks fed oocysts died of acute toxoplasmosis between 7 and 19 days PI; T. gondii tachyzoites were found in histological sections of many tissues. One of the 10 skunks fed tissue cysts and 1 of the 4 controls also died of acute toxoplasmosis days 19 and 20 PI; these animals probably became infected by ingestion of unexcysted oocysts passed in feces of skunks fed oocysts that were housed in the same room that skunks fed tissue cysts were housed. The remaining 9 skunks fed tissue cysts and the 3 controls developed only a mild illness and were killed in good health on days 23-25 PI. Antibodies to T. gondii were not found in 1:25 serum dilution of any of the 19 of 23 skunks that were alive on day 10 PI; 12 of 13 skunks had antibodies (MAT 1:80 or higher) on the day they were killed. Antibodies were not found in 1 skunk. Results indicate that skunks can develop IgG antibodies to T. gondii within 3 wk PI, and primary toxoplasmosis can be fatal in skunks.     

Aposematic Behaviour in the Striped Skunk,Mephitis mephitis

From April to August, 1993 to 1995, we studied the aposematic behaviour patterns of striped skunks, Mephitis mephitis, incidentally while ground-tracking radio-marked animals. During 2668 h of tracking, 207 defensive postures were displayed by 34 radio-collared (27 females, 7 males) and 21 unidentified skunks. Skunks most often advertised their noxiousness using Tail-up (69.1 % occurrence) and Stomp (17.4%). Encounters were frequently (42.5 %) terminated by the skunk running away from the source of disturbance. Most warning behaviour was directed at radio-trackers (95.7 %), and the remainder was displayed to a variety of predatory and non-predatory animals or objects. Stomp occurred more frequently in taller vegetation, where visual advertisement was limited. Reaction distance of skunks disturbed by observers (median = 6 m) was not affected by wind, movement or vegetation height. The small awareness circle and high tolerance of skunks to disturbance are consistent with the life history traits of aposematic animals.     

Ineffectiveness and comparative pathogenicity of attenuated rabies virus vaccines for the striped skunk (Mephitis mephitis)

Three attenuated rabies virus vaccines (SAD-B19, ERA/BHK-21, AZA 2) were compared for efficacy and safety in the striped skunk (Mephitis mephitis) by the oral and intranasal routes. The SAD-B19 and ERA/BHK-21 vaccines were given orally; all three vaccines were given intranasally. Oral administration of SAD-B19 and ERA/BHK-21 vaccines induced neither seroconversion nor significant protection against rabies challenge. One skunk which consumed a SAD-B19 vaccine-laden bait succumbed to vaccine-induced rabies. Intranasal instillation of the three vaccines resulted in the deaths of two of six (AZA 2), three of six (ERA/BHK-21) and six of six (SAD-B19) skunks.     

Population reduction as a factor in the control of skunk rabies in Alberta

Population reduction is being used currently to combat skunk rabies in Alberta. A total of 2,398 striped skunks (Mephitis mephitis) were removed from three counties of southern Alberta during 1980-1983 in an effort to combat rabies outbreaks in those areas. The methods employed included trapping, poisoning, and shooting. Skunks in Forty Mile County have been rabies-free for 4 yr and the outbreaks in Newell and Warner counties appear to be under control. The data suggest that population reduction has been effective in controlling rabies in those areas.     

The striped skunk (Mephitis mephitis) is an intermediate host for Sarcocystis neurona

Striped skunks, initially negative for antibodies to Sarcocystis neurona, formed sarcocysts in skeletal muscles after inoculation with S. neurona sporocysts collected from a naturally infected Virginia opossum (Didelphis virginiana). Skunks developed antibodies to S. neurona by immunoblot and muscles containing sarcocysts were fed to laboratory-reared opossums which then shed sporulated Sarcocystis sporocysts in their faeces. Mean dimensions for sporocysts were 11.0 x 7.5 microm and each contained four sporozoites and a residuum. Sarcocysts from skunks and sporocysts from opossums fed infected skunk muscle were identified as S. neurona using PCR and DNA sequence analysis. A 2-month-old, S. neurona-naive pony foal was orally inoculated with 5 x 10(5) sporocysts. Commercial immunoblot for antibodies to S. neurona performed using CSF collected from the inoculated pony was low positive at 4 weeks p.i., positive at 6 weeks p.i., and strong positive at 8 weeks p.i. Gamma-interferon gene knockout mice inoculated with skunk/opossum derived sporocysts developed serum antibodies to S. neurona and clinical neurologic disease. Merozoites of S. neurona present in the lung, cerebrum, and cerebellum of mice were detected by immunohistochemistry using polyclonal antibodies to S. neurona. Based on the results of this study, the striped skunk is an intermediate host of S. neurona.     

Prevalence of agglutinating antibodies to Sarcocystis neurona in skunks (Mephitis Mephitis), raccoons (Procyon lotor), and opossums (Didelphis Virginiana) from Connecticut

Equine protozoal myeloencephalitis is the most important protozoan disease of horses in North America and is usually caused by Sarcocystis neurona. Natural cases of encephalitis caused by S. neurona have been reported in skunks (Mephitis mephitis) and raccoons (Procyon lotor). Opossums (Didelphis spp.) are the only known definitive host. Sera from 24 striped skunks, 12 raccoons, and 7 opossums (D. virginiana) from Connecticut were examined for agglutinating antibodies to S. neurona using the S. neurona agglutination test (SAT) employing formalin-fixed merozoites as antigen. The SAT was validated for skunk sera using pre- and postinfection serum samples from 2 experimentally infected skunks. Of the 24 (46%) skunks 11 were positive, and all 12 raccoons were positive for S. neurona antibodies. None of the 7 opossums was positive for antibodies to S. neurona. These results suggest that exposure to sporocysts of S. neurona by intermediate hosts is high in Connecticut. The absence of antibodies in opossums collected from the same areas is most likely because of the absence of systemic infection in the definitive host.     

Husbandry,overwinter care,and reproduction of captive striped skunks (Mephitis mephitis)

The striped skunk (Mephitis mephitis) is the focus of research interest for a variety of reasons, including its roles as a rabies reservoir, urban pest, predator of bird eggs, and parasite host. Some research programmes may require husbandry and breeding of captive animals, and because skunks are inactive in the winter in northern environments, special methods are needed to maintain the animals over winter. We report on the establishment of a colony of striped skunks kept in captivity in the northern part of their range. Our goals were to develop simple and effective methods to keep skunks in captivity over winter, and successfully breed skunks in a manner that resembles conditions in the wild. In the spring of 2002, three wild‐caught, pregnant females gave birth in captivity (mean litter size=7). During the first year, 11 of 12 females kept in captivity over winter reproduced successfully in the spring of 2003, with a mean litter size of 5.5 (range=4–8, n=11). In the summer of 2003, 91 of 93 juveniles (97.9%) survived >60 days past weaning. Our high survival and reproduction rates testify to the success of this program, and provide insights into the husbandry of a species that is inactive during winter. Zoo Biol 24:83–91, 2005. © 2005 Wiley‐Liss, Inc.     

Attempted use of an uncommon bay scallop color morph for tracking the contribution of restoration efforts to population recovery

In our ongoing bay scallop restoration efforts in eastern Long Island, NY, United States, we have planted millions of hatchery‐reared juveniles to serve as broodstock when they mature. These plantings have driven the resurgence of larval recruitment, benthic population sizes, and commercial fishery landings over a 12‐year period. In this article, we detail an attempt to track the contribution of our restoration efforts to population rebuilding using planted “skunks,” an uncommon color morph, by looking for increased skunk frequencies in subsequent wild cohorts. Although we saw higher skunk frequencies among large juveniles in natural populations in the first 3 years after extensive skunk plantings, supporting use of uncommon color morphs as a passive tracer, this conclusion was not supported when examined over a 12‐year period, as no strong correlations were seen between skunk frequencies at different life stages (adult broodstock, small and large F1 juveniles, F1 adults) for respective cohorts. Potential reasons for poor correlation between skunk frequencies and restoration efforts include lower than expected production of skunk offspring, dilution of out‐planted contribution to growing natural populations, interannual variability in skunk frequencies that may have obscured the expected skunk signal, and/or differentially higher mortality of skunks at postset and larger juvenile stages. In the latter case, skunks experienced higher overwinter mortality, most likely due to predation, in 9 of 11 years. This led us to suspend skunk plantings after 3 years. Nevertheless, commercial fishermen perceived skunks to be “our” scallops, helping raise the profile of and support for our restoration efforts.     

Biologic and molecular characteristics of Toxoplasma gondii isolates from striped skunk (Mephitis mephitis), Canada goose (Branta canadensis), black-winged lory (Eos cyanogenia), and cats (Felis catus)

Toxoplasma gondii isolates can be grouped into 3 genetic lineages. Type I isolates are considered virulent to outbred mice, whereas Type II and III isolates are not. In the present report, viable T. gondii was isolated for the first time from striped skunk (Mephitis mephitis), Canada goose (Branta canadensis), and black-winged lory (Eos cyanogenia). For the isolation of T. gondii, tissues were bioassayed in mice, and genotyping was based on the SAG2 locus. Toxoplasma gondii was isolated from 3 of 6 skunks, 1 of 4 Canada geese, and 2 of 2 feral cats (Felis catus) from Mississippi. All donor animals were asymptomatic. Viable T. gondii was also isolated from 5 of 5 lories that had died of acute toxoplasmosis in an aviary in South Carolina. Genotypes of T. gondii isolates were Type III (all skunks, lories, and the goose) and Type II (both cats). All 5 Type III isolates from birds and 2 of the 3 isolates from skunks were mouse virulent.     

Contrasting landscape epidemiology of two sympatric rabies virus strains

Viral strain evolution and disease emergence are influenced by anthropogenic change to the environment. We investigated viral characteristics, host ecology, and landscape features in the rabies‐striped skunk disease system of the central Great Plains to determine how these factors interact to influence disease emergence. We amplified portions of the N and G genes of rabies viral RNA from 269 samples extracted from striped skunk brains throughout the distribution of two different rabies strains for which striped skunks were the reservoir. Because the distribution of these two strains overlapped on the landscape and were present in the same host population, we could evaluate how viral properties influenced epidemiological patterns in the area of sympatry. We found that South Central Skunk rabies (SCSK) exhibited intense purifying selection and high infectivity, which are both characteristics of an epizootic virus. Conversely, North Central Skunk rabies (NCSK) exhibited relaxed purifying selection and comparatively lower infectivity, suggesting the presence of an enzootic virus. The host population in the area of sympatry was highly admixed, and skunks among allopatric and sympatric areas had similar effective population sizes. Spatial analysis indicated that landscape features had minimal influence on NCSK movement across the landscape, but those same features were partial barriers to the spread of SCSK. We conclude that NCSK and SCSK have different epidemiological properties that interact differently with both host and landscape features to influence rabies spread in the central Great Plains. We suggest a holistic approach for future studies of emerging infectious diseases that includes studies of viral properties, host characteristics, and spatial features.