Late- and Post-Glacial history of the Mustelidae in Europe

1. Analyses of the subfossil records of mustelid species in Europe indicate specific differences in the pattern of temporal and spatial recolonization of central Europe after the maximum glaciation of the last glacial period. 2. For Meles meles, Martes martes and (with some reservations) Mustela putorius it can be seen that the populations were separated in several glacial refugia during the maximum glaciation of the Weichselian. In contrast, the European population of Lutra lutra was restricted to a single glacial refuge, which had not been clearly localized until now. 3. Besides the known glacial refugia of the Iberian Peninsula, Italian Peninsula and the Balkans, there is evidence of possible additional glacial refugia for mustelids near the Carpathians, in western Moldova and in the northern Pontic region. 4. Gulo gulo, Mustela nivalis, and Mustela erminea show adaptations for survival in Pleistocene conditions, but they were historically also distributed in the warmer areas of southern Europe. 5. Among the more thermophilic mustelid species, Mustela putorius is likely to have been the earliest immigrant following the maximum glaciation. Meles meles has been recorded in comparably early times and also seems to be relatively tolerant of climatic extremes. It is clear that Martes martes had already arrived in central Europe during the Allerød, in connection with the recolonization by birch and pine woods. Lutra lutra, by contrast, seems to have been an absolute Holocene immigrant.     

Fruit consumption by carnivores in Mediterranean Europe

• 1 We reviewed patterns of fruit consumption amongst 10 species of mesocarnivores: red fox Vulpes vulpes, weasel Mustela nivalis, stoat Mustela erminea, polecat Mustela putorius, stone marten Martes foina, pine marten Martes martes, Eurasian badger Meles meles, common genet Genetta genetta, Egyptian mongoose Herpestes ichneumon and wildcat Felis silvestris in Mediterranean Europe.
• 2 The 65 reviewed studies recorded 79 different fruits eaten by carnivores, 58 of which were identified to species. Most records (63%) were of fleshy fruits with high pulp content. The frequency of occurrence of fruit items varied widely amongst species and regions. Four of the carnivore species (red fox, stone marten, badger and common genet) included more than 30 fruit species in their diet.
• 3 A longitudinal pattern was detected in the consumption of fruit in the Mediterranean region, with the frequency of occurrence of fruit consumption increasing towards the east.

     

Importance of free living mustelid carnivores in circulation of adiaspiromycosis

The study of adiaspiromycosis in 8 species of free living mustelid carnivores (266 specimens) revealed the average intensity of infection to be 41.4%. The highest incidence rate was found in the exoanthropic species Putorius eversmanni (73.1 %) and Martes martes (72.2%) while the lowest was observed in the hemisynanthropic species Putorius putorius (30.6%). The stone marten (Martes foina) is a new, still unknown reservoir host of C. parvum var. crescens, C. parvum for which Putorius eversmanni and Mustela nivalis are new hosts, was also demonstrated in 3 cases. In the present paper, the role of mustelid carnivores in natural foci of adiaspiromycosis is discussed and evaluated. The importance of these predators in the circulation of C. parvum var. crescens is relatively wide. They make possible the liberation of adiaspores from the lungs of their prey — primarily small mammals — into the environment and participate in the spread of infection in both the horizontal and vertical directions. They play a part in the process of distributing of the organism to the vicinity of human dwellings, in the development of new elementary foci, and also act as important reservoir hosts of C. parvum var. crescens.     

A PCR-RFLP method on faecal samples to distinguish <Emphasis Type="Italic">Martes martes</Emphasis>, <Emphasis Type="Italic">Martes foina</Emphasis>, <Emphasis Type="Italic">Mustela putorius</Emphasis> and <Emphasis Type="Italic">Vulpes vulpes</Emphasis>

A non-invasive genetic approach has been recently employed in the population genetics of wild species, using faeces that could be easily collected, particularly of elusive or endangered species. However, faeces of pine (Martes martes) and beech marten (M. foina) can be morphologically similar and could be confused with those of polecat (Mustela putorius) and red fox (Vulpes vulpes). On this basis, a rapid, simple and inexpensive RFLP protocol using a cytochrome b (Cyt b) gene fragment of mtDNA, isolated from faecal samples, was performed to distinguish the above-mentioned species.     

Identification of the subgenus Martes str. species (Martes zibellina, M. martes, M. foina, and M. melampus; Carnivora, Mustelidae) according to the mandibular metric characteristics

A comparative analysis involving 21 mandibular metric characteristics of Martes zibellina (n = 114), M. martes (117), M. foina (110), and M. melampus (6) has been performed using a graphical method (scatter diagrams) and stepwise discriminant analysis. The best metric characteristics allowing for discrimination between the lower jaws of these species have been identified and used to plot scatter diagrams. The discriminant analysis has been conducted for three groups of characteristics, namely, those of the whole mandible, ramus ascendens, and corpus mandibulae. As a result, optimal statistical models based on the diagnostic characteristics have been constructed and tested. The corresponding classification functions for species identification of whole mandibles and their fragments have been calculated. These results can be used for species identification of the mandibles of M. zibellina, M. martes, M. foina, and M. melampus.     

Population aspects of sexual dimorphism in Mustelidae from the example of four species (Mustela lutreola, Neovison vison, Mustela putorius, and Martes martes)

Size sexual dimorphism was studied on 695 crania of four species of the Mustelidae. According to the degree of increasing differences between sexes, the species were arranged in the following order: common marten (Martes martes), European mink (Mustela lutreola), American mink (Neovison vison), and black polecat (Mustela putorius). The value of dimorphism characterizes the ecological flexibility of species and is an integrated population characteristic. It was demonstrated that M. martes occupies a specific and relatively narrow ecological niche of the forest ecosystem and joins weak competitive relations with smaller species of Mustelidae. The level of sexual dimorphism in M. lutreola and N. vison, as well as M. putorius, reflects the tension of their interspecific relationships in a given territory. A high level of sexual dimorphism in M. putorius is caused by further divergence of the ecological niches of males and females, being a compensatory mechanism, which mitigates the consequences of toughened environmental requirements.     

A comparative analysis of craniological variability of Eurasian (sable and pine marten) and North American (American marten) species of the <Emphasis Type="Italic">Martes</Emphasis> genus

This paper studies the craniological variability of closely related species—the pine marten Martes martes, the American marten M. americana, and the sable M. zibellina. The study included the data on 22 nonmetric characters of skulls in 2344 individuals. The studied Martes species were revealed to have an evident species-specific manifestation of the investigated craniological characters. Sables stand apart most of all in the interspecific comparison of populations. The degree of epigenetic variability is somewhat higher in the sable than in the pine marten. The American marten significantly differs from Eurasian species in the manifestation of the nonmetric skull characters, which is noted when analyzing even a small number of samples.     

New methods for species and sex determination in three sympatric Mustelids, Mustela itatsi, Mustela sibirica and Martes melampus

We developed novel species and sex determination methods for three Japanese mustelid species. We used DDX3Y to determine sex and generated a primer set to amplify both DDX3X and DDX3Y DNA in Mustela itatsi, M. sibirica and Martes melampus. To determine species and sex simultaneously, we generated fluorescence-labelled primers that give different fragment lengths at D-loop, DDX3X and DDX3Y of these three species using a DNA sequencer.     

Trophic and spatial relationships of the pine marten (Martes martes) and American mink (Neovison vison) on mountain rivers of the Southern Urals

The American mink (Neovison vison) and pine marten (Martes martes) are the most common mustelid species in mountain forests of the Southern Urals. The bulk of the diet (85.3%) in the American mink consists of small mammals (35.8%), insects (22.7%), gastropods (14.1%), and fish (12.7%). In the pine marten, the main components comprising 79.6% of the diet are vegetable foods (29.8%), small mammals (27.0%), and insects (22.8%). The low diversity of their food spectra is accounted for by landscape and ecological features of the study region. The abundance of rodents is low, their distribution has a mosaic pattern, and other kinds of food are more abundant near rivers and streams, which explains the preference of both mustelid species for riparian biotopes. The breadth of trophic niches in the pine marten and American mink are 1.67 and 1.62, respectively, and the coefficient of their overlap is 0.75.     

Isoenzyme spectra of lactate dehydrogenase in tissues of mammals of the Mustelidae family

A comparative analysis of distribution of lactate dehydrogenase (LDH) isoenzymes in the heart, kidneys, lungs, spleen, liver and skeletal muscle was performed in 4 species of carnivorous mammals (Mustelidae family): American mink (Mustela vison Schr.), polecat (Mustela putorius L.), sable (Martes zibellina L.) and pine marten (Martes martes L.). It was found that in the mink, unlike pure terrestrial mustelids (polecat, sable, pine marten), the anaerobic LDH-5 fraction was predominant in the LDH isoenzyme spectrum in the liver, skeletal muscle, lungs and spleen. In all species studied, aerobic B(H) subunits of LDH were found to prevail in the heart and kidney, whereas anaerobic A(M) subunits prevailed in the liver and spleen. The tissue- and species-specific features of LDH isoenzyme spectra revealed in different mustelids reflect the biochemical adaptation of the animals to environmental conditions.     

Genetic analysis of Turkish martens: Do two species of the genus Martes occur in Anatolia?

Stone marten (Martes foina) and European pine marten (M. martes) occur in western Eurasia. Current distributions of martens within Turkey and phylogenetic relationships among the Turkish and other populations of the two species within Eurasia remain relatively unknown. In this study, we aimed to determine genetic diversity within Martes populations inhabiting Turkey and to reveal the phylogenetic relationships among the Turkish and conspecific populations of the two marten species, using mitochondrial cytochrome b (CytB) sequences. Twenty‐four (24) haplotypes were identified among 86 marten samples collected across Turkey, including 23 novel haplotypes. Genetic distances among the Turkish haplotypes ranged from 0.1% to 0.8%, with an average of 0.3%. The 24 Turkish haplotypes were analysed together with those of conspecific populations deposited in GenBank. Phylogenetic (Bayesian Inference, maximum likelihood, neighbor‐joining) and network analyses revealed that all of the Turkish samples belonged to M. foina and that samples of M. martes were not encountered. Haplotypes of M. foina were divided into five haplogroups. The haplogroup including the two Chinese samples differed markedly from other the haplogroups. The remaining haplogroups contained samples from both the Turkish and European populations. We found that there was a genetically close relationship between the Turkish and the European stone marten populations. As a result of this study, M. martes may not be distributed in the Anatolian part of Turkey, possibly due to a barrier effect of two straits (Dardanelles and Bosporus) and the Caucasus Mountains. On the other hand, M. foina is distributed in both the Anatolian and Thracian parts of Turkey. Our results suggest that Turkey was likely one of the refuges for M. foina during Pleistocene glacial periods and is one of the centres of distribution of stone marten for Europe and the surrounding regions.     

A non-invasive genetic method to identify the sympatric mustelids pine marten (<Emphasis Type="Italic">Martes martes</Emphasis>) and stone marten (<Emphasis Type="Italic">Martes foina</Emphasis>): preliminary distribution survey on the northern Iberian Peninsula

The closely related mustelids European pine marten (Martes martes) and stone marten (Martes foina) sympatrically inhabit a large area of Europe. However, given our limited knowledge of their bioecological relationships, their extremely elusive behaviour and the fact that their faeces cannot be distinguished on the basis of morphology alone, it is very difficult to monitor their populations. In this study, we describe a reliable non-invasive polymerase chain reaction (PCR)–restriction fragment length polymorphism (PCR-RFLP) method for distinguishing between M. martes and M. foina based on the analysis of deoxyribonucleic acid extracted from faeces samples. The method was specifically designed to avoid possible interference from potential prey mammals and other sympatric carnivores. The procedure consists of PCR amplifying a mitochondrial D-loop region followed by digesting the resulting 276-bp-long amplicons with the restriction enzymes HaeIII and RsaI. To assess the efficiency of this technique, we conducted a preliminary field study across the potential sympatric distribution areas of both marten species in the northern Iberian Peninsula. Out of 359 faeces samples collected, we identified 80 as specimens from the stone marten and 235 from the pine marten. Unequivocal species identification was thus possible in 88% of the faeces samples collected. These findings reveal the combined use of non-invasive genetic sampling and GIS technology to be a reliable and cost-effective procedure for improving our knowledge of the spatial distributions of sympatric marten species. This protocol could also be used to identify and improve information gaps, to develop effective research and management programmes and in population and landscape genetics studies of marten species. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Remotely plucked hair genotyping: a reliable and non-invasive method for censusing pine marten (Martes martes,L. 1758) populations

We investigated the feasibility of using genetic techniques to census pine marten (Martes martes) populations by genotyping non-invasively collected samples (plucked hair and scats), with particular reference to the genetically depauperate Irish population. Novel real-time polymerase chain reaction methods were developed for species and sex identification, targeting short DNA sequences. Background genetic variation at 17 microsatellite loci was very low in the Irish population, with an average of 2.29 alleles per locus and expected heterozygosity of 0.35. Despite such low polymorphism, a panel of eight loci with a sibling probability of identity of 0.011 reliably identified individual pine marten and their gender, as determined by reference to genotypes of live trapped individuals. With high nuclear DNA amplification success rates (93.8%) and low genotyping error rates (1.8%), plucked hairs may represent a more reliable and cost-effective DNA source than scats for monitoring populations of this elusive carnivore, and similar taxa such as the sympatric stone marten Martes foina.

     

Far from the madding crowd: Tolerance toward human disturbance shapes distribution and connectivity patterns of closely related Martes spp.

To assess niche overlap between the most similar European sympatric carnivores, the pine marten Martes martes and stone marten Martes foina, and outline their potential distributions and connectivity corridors in Central Italy, we applied a multivariate kernel density procedure which allowed to assess both species' ecological hypervolumes based on a set of 16 environmental predictors and used the resulting probability of occurrence map as a resistance surface in electrical circuit theory-based models. Distance to watercourses and percent cover of deciduous forest and shrubland were the most relevant factors shaping pine marten ecological niche, while stone marten distribution was mainly shaped by human population density and cover of both human settlements and deciduous forest. Overlap between the hypervolumes of the two martens was low-to-moderate, while, on average, landscape connectivity was higher for the stone marten. The inclusion in the models of human disturbance-related variables enabled to define a possible mechanism driving habitat partitioning in human-altered landscapes. Based on our results, increasing human density and urbanization of European lowland and hilly landscapes are expected to represent a greater threat to the pine marten than the stone marten.     

Is sexual size dimorphism variable? Data on species of the genus <Emphasis Type="Italic">Martes</Emphasis> in the Urals

Sexual dimorphism in cranial measurements was studied in Ural populations of two species of the genus Martes, M. martes and M. zibellina. The index of sexual dimorphism averaged 8.39% in the former and 9.03% in the latter, being subject to geographic variation. For the first time, temporal variability of sexual dimorphism in dimensional characters was revealed in mammals by analyzing M. zibellina samples collected in different decades of the second half of the 20th century. The majority of corresponding microtrends had reciprocating dynamics.     

Ticks (Acari: Ixodidae) from medium-sized to large mammals in Ehime Prefecture, Japan

Ixodid ticks were collected from medium-sized to large mammals in Ehime Prefecture, Shikoku, Japan. Ten species of ticks (Amblyomma testudinarium, Dermacentor taiwanensis, Haemaphysalis flava, H. formosensis, H. hystricis, H. longicornis, H. megaspinosa, Ixodes nipponensis, I. ovatus, and I. tanuki) were collected from a total of 29 mammals comprising 11 species. Haemaphysalis hystricis, a possible vector of Japanese spotted fever in Ehime prefecture, was collected from Canis lupus familiaris (domestic dog), Martes melampus melampus, and Sus scrofa leucomystax. This is a first report of H. hystricis from the domesticated dog in the endemic area of Japanese spotted fever. This suggests that it is necessary to pay attention to dogs as a host of the vector ticks for Japanese spotted fever control. Nyctereutes procyonoides and Ma. melampus are new hosts for A. testudinarium. Nyctereutes procyonoides, Mustela itatsi, and Lepus brachyurus are new hosts for H. formosensis. Martes melampus is a new host for H. hystricis.     

The NATURA 2000 database as a tool in the analysis of habitat selection at large scales: factors affecting the occurrence of pine and stone martens in Southern Europe

Most studies on habitat selection among animals are conducted at local scales, whereas reliable determination of species requirements at larger spatial scales can be problematic. We used data available for NATURA 2000 sites to determine the habitat requirements of two relatively widespread and common species—pine marten Martes martes and stone marten Martes foina—in Southern Europe. Using presence-absence data, we applied statistical models at two spatial scales. At the local scale (within the dispersal distances of the species), sites occupied by martens were compared with unoccupied sites using buffers of different sizes, whereas at the regional scale, unoccupied sites were selected randomly. To adjust for spatial autocorrelation of data, penalised quasi-likelihood approximations were used. Both species of martens demonstrated preferences for areas with higher proportions of forest cover and steeper terrain. At the local, but not at the regional, scale, pine martens occurred at lower elevations, whilst stone martens occurred at higher elevations. We found that climatic variables (mean temperature, precipitation) had no significant effect on the presence of the martens. The results of our analyses generally confirmed findings of previous studies on habitat selection of both marten species in Southern Europe. This demonstrates the utility of data collected for NATURA 2000 sites for use in various analyses such as conservation planning and evaluating the impact of climate change on the distribution of animal species.     

Non-invasive genetic sampling of sympatric marten species (Martes martes and Martes foina): assessing species and individual identification success rates on faecal DNA genotyping

The use of non-invasive genetic sampling (NGS) has become increasingly popular in wildlife research but needs well-planned sampling strategies and reliable laboratory protocols. In this study, we planned to assess the reliability and success of species and individual identifications of sympatric martens (European pine marten Martes martes and stone marten Martes foina) by genotyping non-invasively collected faecal samples. First, we developed a novel and accurate multiplex panel of 15 microsatellite loci, selected by cross species amplification of 41 loci. The application of this panel facilitated species distinction, discarding the presence of putative hybrids. Then, we assessed the impact of sample collector skills on the lab protocol performances. The faecal DNA quality was evaluated by (a) the success of polymerase chain reaction–restriction fragment length polymorphism identification of the two Martes species and (b) the genotyping success and error rates of individual pine marten identifications. The survey was conducted over all the sympatric range of the two species in the Iberian Peninsula by three groups of sample collectors with different experience: expert wildlife biologist, trained volunteers and technical staff from natural parks. Results show that the different expertise between sample collectors significantly influences the success rate of pine marten individual genotyping, but not the species identification success rate. Based on our results, we recommend conducting sampling by experienced field biologist to maximise the quality of NGS and ensure accurate genotyping success. Application of our methods to field collected scats can be used in a cost-effective way to investigate distribution, patterns of genetic diversity and structure as well as to estimate population abundance for sympatric martens.     

Range expansion of the pine marten (Martes martes) in an agricultural landscape matrix (NW Italy)

Habitat segregation is considered to favour the coexistence of sympatric pine martens Martes martes and stone martens M. foina, the latter being displaced to agricultural and urbanised areas. Subsequent to the report of pine martens in cultivated areas of the western River Po plain (NW Italy), we reviewed all available information on the presence of this species in plain areas of northern Italy and, for two study areas, applied a non-invasive PCR-RFLP method for the identification of Martes species from faecal mtDNA.A total of 24 pine marten records were collected, grouped in the western part of the River Po plain. The number of records showed an exponential increase from 1988 to 2007, the percentage of woods in a 10 km² wide circular plot surrounding the location of records being inversely correlated to its distance from the 300 m a.s.l. contour line. In the two study areas, 36 out of 119 “marten-like” faeces were assigned to the pine marten, whilst none belonged to the stone marten. In the best monitored area, the pine marten was present almost constantly.Our results suggest that the pine marten is expanding its range to include cultivated areas which were previously considered a prerogative of the more synanthropic stone marten.