No evidence of past bottlenecks in two Danish mustelids: results of craniometric and genetic studies in time and space

A craniometric and molecular genetic investigation was conducted in Danish stoat (Mustela erminea) and weasel (Mustela nivalis) populations. Specimens used were collected over a wide time span (stoat: 1864–2002; weasel: 1863–1990) and from several geographical regions (Jutland peninsula and the two islands of Funen and Zealand). The study was made with a temporal and a spatial perspective, allowing the estimation of differences in genetic diversity and craniometrical trait means between geographical regions and through time with the use of ancient DNA techniques. Univariate statistics of 11 trait lengths did not reveal geographical differentiation in size and shape among the different regions for the stoat, but a geographical differentiation in shape was found for the weasel. There was evidence for reductions in skull size with the year of collection in male stoats, but not in females, which suggests that some selective pressures or environmental factors have affected male stoats to a greater extent than female stoats and the weasel. Relatively high values of heterozygosity were found in both the stoat and weasel, using microsatellite markers. The level of genetic variability of the stoat collected recently was compared with the level of genetic variability in the historical samples, demonstrating that the stoat has not suffered severe loss of genetic variability through the investigated period. A comparison of recent and historical genetic variability of the weasel was not possible because the ancient DNA extracted from the weasels was too degraded. Pairwise F_ST values and assignment tests showed small but significant genetic differentiation between the different geographical regions for both the stoat and weasel. No genetic differentiation between the recent and historical samples of the stoat was found. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88 , 541–553.     

Body size of the weasel Mustela nivalis and the stoat M. erminea in Sweden

In this study we examined temporal and geographical variations in a sample of 124 skulls of the weasel Mustela nivalis and 146 skulls of the stoat M. erminea, collected in Sweden between 1959-1992 and 1913-1990, respectively.We used Principal Component Analysis (PCA) to combine the effects of latitude, longitude, year of collection, mean ambient temperature and Net Primary Productivity (NPP). The first principal component (PC1) contained latitude, ambient temperature and NPP and was significantly and positively related to male (but not female) skull size of both stoats and weasels. None of the other factors or their interactions were significantly related to skull size.We conclude that ambient temperature, either directly through energy savings, or indirectly through improved food availability (increased NPP), had a significant effect on determining body size of male stoats and weasels in Sweden. Our results support the hypothesis that male and female of these species are affected by different selection pressures and thus react differently to changing environmental conditions.     

Intrageneric diversity of the cytochrome B gene and phylogeny of eurasian species of the genus mustela (mustelidae, carnivora)

To illuminate molecular phylogenetic relationships among Eurasian species of the genus Mustela (Mustelidae, Carnivora), we determined nucleotide sequences of the complete mitochondrial cytochrome b gene region (1,140 base pairs). Molecular phylogenetic trees, constructed using the neighbor-joining and the maximum likelihood methods, showed the common topology of species relationships to each other. The American mink M. vison first branched off and was positioned very remotely from the other species of Mustela. Excluding M. vison, the ermine M. erminea first split from the rest of the species. Two small body-sized weasels, the least weasel M. nivalis and the mountain weasel M. altaica, comprised one cluster (named "the small weasel group"). The other species formed another cluster, where the remarkably close relationships among the domestic ferret M. furo, the European polecat M. putorius, and the steppe polecat M. eversmanni were noticed with 87-94% bootstrap values (named "the ferret group"), supporting the history that the ferret was domesticated from M. putorius and/or M. eversmanni. The European mink M. lutreola was the closest to the ferret group. The genetic distance between the Siberian weasel M. sibirica and the Japanese weasel M. itatsi corresponded to differences of interspecific level, while the two species were relatively close to M. lutreola and the ferret group. These results provide invaluable insight for understanding the evolution of Mustela as well as for investigating the hybridization status between native and introduced species for conservation.     

The stoat Mustela erminea population decline in northern Belarus and its consequences for weasels Mustela nivalis

Abstract

In northern Belarus, we have documented a decline in the local stoat Mustela erminea population following the naturalisation of the American mink Mustela vison. The most likely cause is the reduction in the density and distribution of the main prey of stoats, the riparian voles (the water vole Arvicola terrestris and the root vole Microtus oeconomus), due to excessive predation by mink. Since the stoat population has declined, the number of weasels Mustela nivalis in marshlands has increased and their mean body mass has increased, correlated with the higher number and mean weights of rodents available for weasels in marshland compared with forest habitats.     

Secondary poisoning of mammalian predators during possum and rodent control operations at Trounson Kauri Park, Northland, New Zealand

A poison baiting operation at Trounson Kauri Park in Northland, New Zealand using first 1080 and then brodifacoum targeted possums (Trichosurus vulpecula) and rodents (Rattus rattus, Rattus norvegicus and Mus musculus). Predatory mammals were monitored by radio telemetry during the operation. All six feral cats (Felis catus), the single stoat (Mustela erminea) and the single ferret (Mustela furo) being monitored at the beginning of the operation died of secondary poisoning following the 1080 operation. A further two cats and four stoats were monitored through the ongoing poisoning campaign using brodifacoum in a continuous baiting regime. None of these radio tagged carnivores died of secondary poisoning. However, tissue analysis of additional carnivores trapped at Trounson found that cats, weasels (Mustela nivalis) and, to a lesser extent, stoats did contain brodifacoum residues. The duration that the radio-tagged predators were alive in and around Trounson Kauri Park suggests that the secondary poisoning effect was much reduced under the continuous baiting strategy compared to the initial 1080 poison operation.     

Rhodamine B as a systemic hair marker for assessment of bait acceptance by stoats (Mustela erminea)

Abstract

Rhodamine B (RB) is a dye that becomes incorporated into the structure of growing hair of animals that ingest it, appearing as an orange‐red fluorescent band detectable under a fluorescent‐light microscope. This marker was evaluated as a means of assessing bait acceptance by stoats (Mustela erminea L.). Eleven wild‐caught captive stoats were each fed a broken hen egg injected with 25 mg of RB on two occasions, 5 weeks apart. This was equivalent to 62–108 mg kg^–1, depending upon stoat weight, on each occasion. At least three facial whiskers were collected from each dosed stoat on each of two sampling dates (giving a total of at least six whiskers from each stoat). The sampling dates varied from 1 to 17 weeks after first dosing. Whiskers were also collected from one of the dosed stoats that died of other causes 19 weeks after first dosing, and from four stoats not dosed with RB. All 11 of the stoats fed RB had at least one fluorescent band in at least one of the sampled whiskers. None of the four stoats not fed RB had fluorescent bands in their whiskers. The marking persisted in all dosed stoats for at least 6 weeks, and in one dosed stoat for at least 19 weeks after dosing. However, only 56% of the 91 whiskers inspected from the dosed stoats had fluorescent bands, and only 9% of the whiskers had two fluorescent bands, representing the two doses of RB. The distance between the two fluorescent bands indicated a mean whisker growth of 0.6 mm day^‐1. The distance from the base of the whiskers to the base of the fluorescent bands was broadly related to the time after ingestion of bait containing RB. However, the variation was too great for distance along the whisker to be reliably used as a quantitative measure of time after bait ingestion. The technique can be used to assess bait acceptance in the field provided all stoats are sampled within c. 4–6 weeks of baiting, and at least 6–9 whiskers are sampled from each stoat.     

Sexual dimorphism in the skull of the European mink<Emphasis Type="Italic">Mustela lutreola</Emphasis> from NW part of Russia

Morphometric variation in 22 characters of 86 skulls of the European minkMustela lutreola (Linnaeus, 1761), from the NW part of Russia, has been analysed. Stepwise discriminant analysis was used to estimate craniometric variables for sex determinations. Two characters (zygomatic breadth and interorbital width) are enough for the 96.5% correct classification. The male skull ofM. lutreola is characterised by a relatively high neurocranium, widely arranged zygomatic arches, a wide rostrum, and by wider auditory bullae and higher mandibles. Sexual size dimorphism ofM. lutreola is less than that of other similar-sized mustelids —Mustela putorius, M. eversmanii, M. sibirica, Neovison vison. The results are discussed in relation to the existing theories on sexual dimorphism in mustelids.     

Serologic survey for selected viral pathogens in free-ranging endangered European mink (Mustela lutreola) and other mustelids from south-western France

To investigate the possible role of selected pathogens in the decline of endangered European mink (Mustela lutreola) populations and the potential for these pathogens to affect mink survival, a serologic survey was conducted using serum samples collected from March 1996 to March 2003 in eight departments of south-western France. In total, 481 free-ranging individuals of five mustelid species (including the European mink) were tested. Sympatric mustelids can serve as sentinels to determine the presence of antibodies to viruses in the study area that could potentially infect mink. Antibodies to Canine distemper virus (CDV) were detected in all species; 9% of 127 European mink, 20% of 210 polecats (Mustela putorius), 5% of 112 American mink (Mustela vison), 33% of 21 stone marten (Martes foina) and 5% of 20 pine marten (Martes martes). Antibody prevalence was significantly higher in stone marten and polecats, possibly because their ranges overlap more closely with that of domestic species than that of the other species tested. Antibodies to Canine adenovirus were detected in all species but the pine marten; antibody prevalence estimates ranging from 2% to 10%. Antibodies to canine parainfluenza virus were detected in 1% of European mink, 1% of American mink and 5% of tested polecats but were not detected in Martes species. Antibodies to Rabies virus (RV) were detected in three animals, possibly because of interspecies transmission of bat lyssaviruses as the sampling area is considered to be free of RV, or to a lack of test specificity, as antibody titers were low. The high antibody prevalence to potentially lethal CDV suggests that this pathogen could have significant effects on the free-ranging populations and has implications for the conservation efforts for the endangered European mink.     

Using genetics and Bayesian modelling to evaluate the eradication of stoats (

The New Zealand Department of Conservation recently (May 2008) began a programme to eradicate stoats (Mustela erminea) from Resolution Island (Fiordland, New Zealand) using kill traps. In conjunction with this eradication effort we have the following 3 objectives: (1) to measure the population abundance of stoats prior to trapping using hair tubes and forensic DNA methods; (2) optimise techniques for detecting individual stoats, in order to quantify the probability of stoat persistence given no detections after several months of trapping; and (3) use genetic analyses to identify the possible origins (mainland incursions or in situ breeding) of new stoats captured in a control zone. We present Bayesian modelling techniques used to determine the probability of stoat persistence on the island after the initial population reduction, when individual stoats are no longer captured in traps. We also provide details on an effective level of monitoring and trapping effort required to maintain a comfortable level of confidence that stoats no longer persist on the island. Improving these techniques adds to variety of valuable tools for management of invasive mammal species in a range of natural environments worldwide.     

Stoats (Mustela erminea) provide evidence of natural overland colonization of Ireland

The current Irish biota has controversial origins. Ireland was largely covered by ice at the Last Glacial Maximum (LGM) and may not have had land connections to continental Europe and Britain thereafter. Given the potential difficulty for terrestrial species to colonize Ireland except by human introduction, we investigated the stoat (Mustela erminea) as a possible cold-tolerant model species for natural colonization of Ireland at the LGM itself. The stoat currently lives in Ireland and Britain and across much of the Holarctic region including the high Arctic. We studied mitochondrial DNA variation (1771 bp) over the whole geographical range of the stoat (186 individuals and 142 localities), but with particular emphasis on the British Isles and continental Europe. Irish stoats showed considerably greater nucleotide and haplotype diversity than those in Britain. Bayesian dating is consistent with an LGM colonization of Ireland and suggests that Britain was colonized later. This later colonization probably reflects a replacement event, which can explain why Irish and British stoats belong to different mitochondrial lineages as well as different morphologically defined subspecies. The molecular data strongly indicate that stoats colonized Ireland naturally and that their genetic variability reflects accumulation of mutations during a population expansion on the island.     

Genetic influences on cranial form: variation among ranch and feral American mink Mustela vison (Mammalia: Mustelidae)

Multivariate statistical techniques were used to examine craniometric variation within and between ranch and feral populations of American mink (Mustela vison). An examination of variation between ranches revealed that differences are greater between ranches than within ranches, although all comparisons were statistically significant. There is highly significant variation within a population of mink sampled from a single ranch during a short time period; female mink of different pelt colour are differentiable by their skull shape but not by skull size. This offers evidence for a genetic background to cranial variation in ranch mink. Cranial sexual dimorphism is reduced in ranch mink, when compared to feral populations, and size accounts for a lesser proportion of the variation between the sexes in ranched populations. In addition, the skulls of ranched mink are larger, have a relatively shorter palate and a relatively narrower postorbital constriction compared to their feral counterparts. We believe this reduced dimorphism to be a product of relaxed sexual selection, lack of resource competition and selective breeding for larger specimens of both sexes within ranch populations.     

Spring home range, spatial organisation and activity of stoats Mustela erminea in a South Island Nothofagus forest, New Zealand

This radio-tracking study reports the spring home range, spatial organisation and activity of 11 stoats Mustela erminea in a New Zealand Nothofagus forest, 1,5 yr after significant seedfall when rodent density was low, but stoat density was high. The average home range of 4 male stoats was 223 (SE = 45) ha, significantly larger than the average range area of 94 (SE = 13) ha recorded for 7 female stoats. Stoats were generally tolerant of sharing space and did not maintain intra- or intersexual territorial spacing systems. There was no evidence of temporal avoidance with several stoats of the same sex showing slight attraction to one another. However, stoats still may avoid one another when in close proximity. Long-term radio-tracking studies are required to determine the general patterns of spacing behaviour in stoats, Male stoats showed higher levels of activity during daylight than females.     

Phylogeny, evolutionary history and taxonomy of the Mustelidae based on sequences of the cytochrome b gene and a complex repetitive flanking region

The Mustelidae is a diverse family of carnivores which includes weasels, polecats, mink, tayra, martens, otters, badgers and, according to some authors, skunks. Evolutionary relationships within the family are under debate at a number of different taxonomic levels, and incongruencies between molecular and morphological results are important. We analysed a total of 241 cytochrome b (cyt b) gene sequences and 33 sequences of a complex repetitive flanking region from 33 different species to compile an extensive molecular phylogeny for the Mustelidae. We analysed these sequences and constructed phylogenetic trees using Bayesian and neighbor‐joining methods that are evaluated to propose changes to the taxonomy of the family. The peripheral position of skunks in phylogenetic trees based on both loci suggests that they should be considered a separate family, Mephitidae. The subfamily Melinae is the basal group within the Mustelidae and trees based on the cyt b gene suggest that the American badger, Taxidea taxus, should be considered a separate monotypic subfamily, Taxidiinae. Otters classified within the genera Lutra, Amblonyx and Aonyx are grouped within the same clade in cyt b and combined partial cyt b and flanking region trees and show reduced levels of inter specific divergence, suggesting that they could be classified together under a single genus, Lutra. The Bayesian tree based on combined data from both loci supports the idea that subfamily Mustelinae is paraphyletic, as otters (subfamily Lutrinae) are included in this subfamily. Low levels of genetic divergence among European polecat, Mustela putorius, steppe polecat, Mustela eversmannii, and European mink, Mustela lutreola, suggest that these species could be considered subspecies within a single species, Mustela putorius. Our results are consistent with a rapid diversification of mustelid lineages in six different radiation episodes identified since the Early Eocene, the oldest events being the separation of subfamilies and the split of marten (Martes, Gulo) and weasel (Mustela) lineages in the Early Middle Miocene. The separation of New World from Old World lineages and the split of the remaining genera are estimated to have occurred in Late Miocene. The most recent events have been the differentiation of species within genera and this probably occurred in four radiation episodes at the end of Late Miocene, Early Pliocene, Late Pliocene and Pleistocene epochs.     

Evidence of secondary poisoning of free-ranging riparian mustelids by anticoagulant rodenticides in France: implications for conservation of European mink (Mustela lutreola)

Because of the rapid decline of the endangered European mink (Mustela lutreola) populations in France, a national conservation program has been put into action, including research to understand the causes of decline. As part of this research, concentrations of eight anticoagulant rodenticides were examined in livers from 122 carcasses of four species of free-ranging mustelids collected between 1990 and 2002 in southwestern France. Bromadiolone residue was found in all species and 9% of the sample (one of 31 European mink, three of 47 American mink [Mustela vison], five of 33 polecats [Mustela putorius], and two of 11 European otters [Lutra lutra]). Liver concentrations ranged from 0.6 mug/g to 9.0 mug/g. Chlorophacinone residue was found in two species and 4% of the sample (in four of the American mink and in one of the otters), with liver concentrations ranging from 3.4 mug/g to 8.5 mug/g. Two polecats and one American mink had lesions and liver residues indicating bromadiolone was directly responsible for their death. However, most of our study animals survived secondary poisoning until they were caught; this study certainly underestimates the extent of fatal exposure of mustelids to rodenticides. Moreover, anticoagulant poisoning could increase their vulnerability to other causes of death. The current status of the endangered European mink population is such that any additional risk factor for mortality is important, and it is thus urgent to monitor and reduce the extensive use of bromadiolone and chlorophacinone against field rodents in France.     

Antibodies to Aleutian mink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France

Owing to the rapid decline of the European mink (Mustela lutreola) in France, a national conservation action plan has been initiated, in which scientific research to improve understanding of the causes of the decline is one of the primary objectives. In order to investigate the possible role of Aleutian disease parvovirus (ADV) in decline of the species, a serologic survey was conducted from March 1996 to March 2002 in 420 free-ranging individuals of six species of small carnivores distributed in eight departments of southwestern France. Antibodies to ADV were detected in 17 of 75 American mink (Mustela vison), 12 of 99 European mink, 16 of 145 polecats (Mustela putorius), four of 17 stone martens (Martes foina), one of 16 pine martens (Martes martes), and three of 68 common genets (Genetta genetta). Seroprevalence was significantly higher in American mink than in other species. Seropositive individuals with gamma globulin levels >20% were observed in four European mink, four American mink, two stone martens, and one pine marten. Geographic distribution of positive animals indicates the virus has spread to all areas where European mink are found. Furthermore, a trend of increasing prevalence seems to appear in Mustela sp. sympatric with American mink. Although further investigations are necessary to evaluate the role of ADV in decline of European mink, evidence of the virus in the wild at the levels found in our study has implications for conservation of this species.     

Managing an invasive predator pre-adapted to a pulsed resource: a model of stoat (Mustela erminea) irruptions in New Zealand beech forests

The stoat (Mustela erminea) is a specialist predator that evolved to exploit the unstable populations of northern voles and lemmings. It was introduced to New Zealand, where it is pre-adapted to respond with a population irruption to the resource pulses that follow a heavy seedfall of southern beech (Nothofagus spp.). Culling stoats during an irruption is necessary to reduce damaging predation on nesting endemic birds. Culling might not reduce the stoat population long term, however, if high natural mortality exceeds culling mortality in peak years. During other phases of the beech-mast cycle, culling might have a greater effect on a smaller stoat population, whether or not damage prevention is critical. We developed a 4-matrix model to predict the effects of culling on λ, the annual rate of change in the size of the stoat population, through the four annual phases of an average masting cycle, explicitly distinguishing between apparent and real culling. In the Post-seedfall phase of the cycle, large numbers of stoats are killed, but little of this extra mortality is additive; in other phases, culling removes larger proportions of smaller total numbers of stoats that would otherwise have lived. Culling throughout all phases is most effective at reducing stoat populations, but is also the most expensive option. Culling in Post-seedfall plus Seed or Crash years is somewhat less effective but better than culling in one phase only. Culling has different short-term effects on stoat age distribution depending on the phase of the cycle when culling begins.     

Bovine tuberculosis in a free ranging red fox (Vulpes vulpes) from Doñana National Park (Spain)

During 1997 and 1998, a survey of Iberian carnivores was conducted to study the epidemiology of bovine tuberculosis in the Do?ana National Park and surrounding areas in southwestern Spain. Post-mortem examinations were done on seven red foxes (Vulpes vulpes), two Egyptian mongoose (Herpestes ichneumon), one weasel (Mustela nivalis), two genets (Genetta genetta), one Iberian lynx (Lynx pardinus), one Eurasian badger (Meles meles), and two polecats (Mustela putorius). Lesions suggestive of bovine tuberculosis were not detected but, in culture, Mycobacterium bovis was isolated from the retropharyngeal lymph nodes of one adult male red fox. This is the first report of M. bovis infection in red fox in Spain.     

Leptospirosis in free-ranging endangered European mink (Mustela lutreola) and other small carnivores (Mustelidae, Viverridae) from southwestern France

To study the possible role of disease in the decline of endangered European mink (Mustela lutreola), we conducted a survey of antibody prevalence and renal carriage of pathogenic leptospira (Leptospira interrogans sensu lato) using serum and kidney samples collected from 1990 to 2007 from several free-ranging small carnivores and farmed American mink (Mustela vison) in southwestern France. An indirect microscopic agglutination test using a panel of 16 serovars belonging to 6 serogroups (Australis, Autumnalis, Icteroh?morrhagi?, Grippotyphosa, Panama, Sejroe) revealed antibodies in all species, with significant differences in antibody prevalences: 74% in European mink (n=99), 65.4% in European polecats (Mustela putorius, n=133), 86% in American mink (n=74), 89% in stone martens (Martes foina, n=19), 74% in pine martens (Martes martes, n=19), 35% in common genets (Genetta genetta, n=79), and 31% in farmed American mink (n=51). Serogroups Australis and Icteroh?morragi? were dominant in most free-ranging species; serogroup Grippotyphosa had high prevalences in European mink. Such high antibody prevalences have never been reported. They are probably related to the large number of known reservoirs, rats (Rattus spp.), muskrat (Ondatra zibethicus), and coypu (Myocastor coypu), in the study area. The polymerase chain reaction test specific for pathogenic leptospiral DNA detected renal carriage in 23% of 34 European mink, 22% of 18 polecats, and 15% of 33 free-ranging American mink, with no significant differences. Renal carriage shows that mustelids may shed leptospira for short periods, but their epidemiologic role is probably limited. High antibody prevalences suggest that the disease is unlikely to be highly pathogenic for these species; however, chronic forms of the disease (abortions, renal lesions) could reduce the reproductive success or life span of infected animals. Further studies on the pathogenicity of leptospirosis in these populations are needed to measure its impact on the population dynamics of these rodent predators.     

The potential for biological control of stoats (Mustela erminea)

Abstract

Accelerating the mortality of stoats (Mustela erminea) using biological agents, or reducing their fertility using chemosterilants or biological agents, are increasingly seen as more sustainable and more humane than trapping and poisoning. Obligate delayed implantation in fertilised female stoats of all ages allows 10–11 months for an applied biological agent or chemosterilant to interfere with gestation. Two chemosterilants (cabergoline and mifepristone) disrupt pregnancy in some species and may be effective on stoats, although they are not species‐specific and are probably more expensive than poisoning. For the longer term, more recent fertility control research has explored potentially more species‐specific options for other species based on inducing an immune response to an animal's own reproductive hormones, gametes, or products from embryos. Conception will be difficult to disrupt in stoats because females are sexually mature and are mated in the nest during a short period before they are weaned. A large research effort will be required to determine which of the immunosterilants being developed could be suitable candidates for stoat control. There are fewer options apparent for using biological agents to increase stoat mortality, although species‐specific strains of canine distemper virus may be effective against stoats.

The greatest impediment to controlling stoat fertility will be effective delivery of sterilants. For the foreseeable future, it will probably be necessary to rely on baits, but they are unlikely to put all target stoats at risk, and will be incapable of delivery over larger scales than at present.

Before undertaking expensive field trials and development of anti‐fertility and biological agents, the effects of putative compensatory changes in demographics that may be associated with changes in stoat density should be modelled to see if the sterilisation and mortality rates that are required to achieve a given level of population control are realistic targets. Also, population control should be defined in terms of accrued benefit for wildlife by establishing the relationships between stoat densities and the viability of prey populations.

Biological control of fertility or mortality may never be suitable as stand‐alone control options for stoats, particularly when some native fauna survive only if stoats are reduced to very low densities. Biological control may have greater potential when integrated with conventional control.     

Responses of stoats to scent lures in tracking tunnels

Abstract

Scent lures made from the anal sac secretions of stoats (Mustela ermined) in a long‐life formulation increased the number of visits by stoats to footprint tracking tunnels set near the shoreline of Lake Waikaremoana. Lures derived from female stoats received a similar number of visits to those derived from males. Blank lures with no active ingredient did not attract stoats. Most of the lures remained intact and active for about seven weeks in summer. Rodents were unaffected by the lures, being neither repelled by the scent of stoats, nor attracted to the edible casein‐based carrier compound. Our results suggest that scent lures could be useful for indexing stoat populations. Trials are needed to compare the effectiveness of lures and bait, and to determine seasonal changes in lure attractiveness. Problems of supply of the active ingredients will need to be overcome.