Genetic analysis of sable (<Emphasis Type="Italic">Martes zibellina</Emphasis>) and pine marten (<Emphasis Type="Italic">M. martes</Emphasis>) populations in sympatric part of distribution area in the northern Urals

Analysis of nucleotide sequences of the mitochondrial DNA (mtDNA) control region (495 bp) of sables (Martes zibellina) and pine martens (M. martes) from allopatric parts of the species ranges has shown a considerable interspecific genetic distance (>3%). In sympatric populations of these species in the northern Urals, differences between two species-specific mtDNA lineages are still large; however, classification of each individual nucleotide sequence with one of the two lineages is not correlated with whether the given animal is phenotypically a sable, a pine marten, or a potential hybrid (the so-called “kidas”). This indicates a high degree of reciprocal introgression of the sable and pine marten mtDNA in the northern Urals and suggests that their interspecific hybridization is common in the sympatric zone.     

Biological invasions provide a framework for reintroductions: selecting areas in England for pine marten releases

We suggest that reintroductions, like biological invasions, have two phases: establishment when a new population becomes self-sustaining, and spread when a population increases its distribution. Stochastic effects on mortality and sex ratios are most likely to determine whether a population becomes established, while factors influencing birth rates will probably most influence spread. Using this establishment-spread structure, we evaluate the autecological suitability of regions in England for pine marten Martes martes reintroductions. Risks of mortality from predator control, traffic accidents and predation by foxes were used to evaluate suitability for establishment. Mortality risk was higher in all potential release regions in England (selected as having 25% or more woodland cover) than in regions of current pine marten distribution in Scotland; risk of predation was higher in the latter. Indices of prey abundance were used to evaluate suitability for populations to spread. Prey indices in potential release regions were generally higher than in regions of current distribution. A relation between prey, woodland cover, and known pine marten densities suggested that potential release regions are capable of supporting relatively high densities of pine martens, though these might be reduced by higher mortality. We concluded that all potential release regions are suitable for pine marten populations to spread. However, reintroductions should first be to regions with lower risk of mortality, in case higher levels of the latter prevent establishment. The suitability of relict regions of distribution in northern England was low until post-war afforestation, suggesting that habitat suitability constrained recovery of relict populations. These regions remain less suitable for reintroductions.     

Linking habitat characteristics with genetic diversity of the European pine marten (Martes martes) in France

Although typically considered as a forest specialist species, the European pine marten (Martes martes) is an example of a number of species that have recently been found to also live in fragmented landscapes. Considering that habitat fragmentation and loss is a major threat to the persistence of mammal species in such landscapes, we investigated the association between habitat characteristics and genetic diversity across four pine marten populations occupying contrasting landscapes in France with different degrees of forest availability and fragmentation. Bayesian and multivariate clustering methods evidenced the presence of three genetic clusters and isolation by distance between populations was found at the national scale. We found an overall moderate level of genetic variability, but no evidence of a bottleneck or deficit in heterozygosity in any of the populations. No pattern of isolation by distance was found within the populations, except in the one located in the Pyrenean Mountains which appeared partly isolated from other continental populations and also showed a lower level of genetic diversity. No obvious association between the pattern of genetic variability and the pattern of forested habitat characteristics was found. We discuss the possibility that pine martens show greater behavioural plasticity than typically expected allowing them to adapt to different habitat types.     

Nutritional ecology provides insights into competitive interactions between closely related Martes species

1. Closely related predator species often share several prey items, making it hard to differentiate the effects on their feeding habits of variation in food availability and of competition. We hypothesised that we could overcome this obstacle by quantifying and comparing nutritional niches.
2. We reviewed dietary studies that assessed the relative bulk of each food item, as either per cent biomass or per cent mean volume, in the diet of two closely related species, pine marten Martes martes and stone marten Martes foina, and calculated the nutrient profiles (intakes of protein, lipids and carbohydrates) of each diet.
3. Both martens’ diets were tightly clustered (mean values: 47% of energy from protein, 39% from lipid, and 14% from carbohydrate). In allopatry, the nutritional niches of the two species did not differ, but in sympatry, the stone marten ate more carbohydrates and less protein than the pine marten. In allopatry, the protein intake of the stone marten remained high (45–52%) in very different habitats, from cultivated lowland to Alpine forests.
4. Our data suggest that stone marten frugivory may, at least partially, be the result of interspecific competition. By analysing dietary data in the framework of nutritional ecology, we could compare the feeding requirements of pine martens and stone martens more effectively than by using classical estimates of trophic niche overlap at the food item level. This approach may help to shed light on the trophic relationships of other competing species.

     

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 PCR-RFLP-based method to distinguish sable (<Emphasis Type="Italic">Martes zibellina</Emphasis>) and pine marten (<Emphasis Type="Italic">Martes martes</Emphasis>)

Species identification is an important issue in conservation and a particular focus for wildlife forensics. Molecular biological methods retain a unique power to differentiate between difficult samples that lack other identifiable characteristics. The pine marten (Martes martes) and sable (Martes zibellina) are closely related species with very similar pelage characteristics and are often difficult to distinguish from each other. The sable, however, in contrast to the pine marten, remains an endangered and protected animal in China with both hunting and fur trade strictly prohibited for this species. Here, we present a polymerase chain reaction-based restriction fragment length polymorphism method for distinguishing the two species. We sequenced a 638-bp fragment of cytochrome b gene in 39 sables, 68 pine martens, and 10 stone martens and identified all variable nucleotides. A new primer pair was subsequently designed to amplify a 316-bp fragment containing restriction sites of enzyme BseG I and BamH I that are different among martens. When the fragment was cut using BseG I, the resulting restriction pattern was identical in the sable and pine marten, but differed from all other martens. When cut using BamH I, the fragment generated two diagnostic fragments in the sable which could distinguish them from pine martens. This method was valid for all haplotypes of sable and pine marten thus far identified and has high potentially applicability for the identification of the two species.     

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.     

Summer food of sympatric red fox and pine marten in the German Alps

Based on fecal analyses, we compared summer diet composition and trophic niche breadth for the sympatric red fox Vulpes vulpes (n=55 scats) and pine marten Martes martes (n=64) in the foothills of the German Alps. Mammals accounted for 41 and 51% of the consumed biomass by pine martens and red foxes, respectively, and no single mammal species exceeded 8% of the diet. The larger red fox consumed a wider range of prey sizes than the smaller pine marten, and both consumed large amounts of plants and also insects. Whereas the Levins index suggested that both predators have specialist feeding niches, the Shannon-Wiener index showed that both predators were relatively generalist. Despite its preliminary nature, our study suggests that a strict distinction between generalist and specialist trophic niches is not justified for medium-sized carnivores in the Alps, particularly as results greatly depend on the indices used.     

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.     

Intraguild dietary overlap and its possible relationship to the coexistence of mesocarnivores in intensive agricultural habitats

The stone marten (Martes foina) and the pine marten (M. martes) are closely related mammalian carnivores potentially subject to exploitative competition. The recent expansion of the pine marten into the intensively cultivated plain of the River Po (NW Italy), where previously only stone marten occurred, offered an interesting opportunity to analyse their relationships. We studied the distribution and diet of Martes species and trophic niche overlap between martens and red foxes (Vulpes vulpes) in two study areas, each with two pseudoreplicates, by analysing genotyped faeces. Our results seem to confirm the displacement of the stone marten from one study area, the pine marten being the only Martes species occurring where previously the stone marten had been reported. We found a large food niche overlap between red fox and both stone and pine martens, but with evidence of size-related differences in the consumption of some food items. We hypothesised that, due to the poor prey-base of the environment, highly altered by intensive crop cultivation, intense interspecific competition originally occurred between the red fox and stone marten. The heightening of interspecific competition caused by the entry of the pine marten in the predator guild may have caused the displacement of the stone marten, at least temporarily. The mechanism of such displacement needs to be clarified through further surveys in areas where the three species occur sympatrically.     

Widespread distribution of Pine martens (<Emphasis Type="Italic">Martes martes</Emphasis>) in a fragmented suburban landscape

Pine martens (Martes martes) are forest specialists that depend either on large patches of forest or on the absence of barriers between smaller forest patches. It thus seems likely that they would disappear from landscapes with heavily fragmented forests and a high density of presumptive barriers that are typical of Central Europe. We studied the distribution of pine martens in a suburban landscape characterised by fragmented forests and a high density of presumptive barriers (e.g. housing areas, roads). We assessed the presence of pine martens using camera traps in a sample of 170 1?×?1-km quadrats and used occupancy modelling to account for imperfect detection. We found an almost complete and countrywide distribution of the pine marten. Larger roads and housing areas were not negatively related to its current distribution as we predicted. We conclude that pine martens are capable to survive in some heavily fragmented landscapes.     

Avian top predator and the landscape of fear: responses of mammalian mesopredators to risk imposed by the golden eagle

Top predators may induce extensive cascading effects on lower trophic levels, for example, through intraguild predation (IGP). The impacts of both mammalian and avian top predators on species of the same class have been extensively studied, but the effects of the latter upon mammalian mesopredators are not yet as well known. We examined the impact of the predation risk imposed by a large avian predator, the golden eagle (Aquila chrysaetos, L.), on its potential mammalian mesopredator prey, the red fox (Vulpes vulpes, L.), and the pine marten (Martes martes, L.). The study combined 23 years of countrywide data from nesting records of eagles and wildlife track counts of mesopredators in Finland, northern Europe. The predation risk of the golden eagle was modeled as a function of territory density, density of fledglings produced, and distance to nearest active eagle territory, with the expectation that a high predation risk would reduce the abundances of smaller sized pine martens in particular. Red foxes appeared not to suffer from eagle predation, being in fact most numerous close to eagle nests and in areas with more eagle territories. This is likely due to similar prey preferences of the two predators and the larger size of foxes enabling them to escape eagle predation risk. Somewhat contrary to our prediction, the abundance of pine martens increased from low to intermediate territory density and at close proximity to eagle nests, possibly because of similar habitat preferences of martens and eagles. We found a slightly decreasing trend of marten abundance at high territory density, which could indicate that the response in marten populations is dependent on eagle density. However, more research is needed to better establish whether mesopredators are intimidated or predated by golden eagles, and whether such effects could in turn cascade to lower trophic levels, benefitting herbivorous species.     

Scent marking and social relationships in pine martens (Martes martes)

Scent marking was studied in pine martens (Martes martes) in female-female and male-female pairs. Results show that agonistically dominant individuals generally had higher scent marking frequencies. However, environmental familiarity can modify the social relationship, whatever the previous social experiences, and, consequently, marking activity. Despite important intra-and interindividual variations, the subjects appeared to react to physical and social modifications by an increased marking rate. One factor affecting marking activity in both novel and established pairs was the activity level of the conspecific partner. the data support the hypothesis that pine martens react in the same way to physical and social modifications, but with different response levels. The discussion focuses on possible functions of scent marking. © 1993 Wiley-Liss, Inc.     

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.     

Snow tracking reveals different foraging patterns of red foxes and pine martens

Red fox (Vulpes vulpes) shares similar prey preferences and co-occurs with several other carnivores, and is together with pine marten (Martes martes), the most common mesocarnivore in the northern boreal forest. Voles are important prey for both species, but it is unclear to what extent they compete for the same food resources in winter. Here, we use 2139 km and 533 km of meticulous snow tracking of red foxes and pine martens to evaluate their food niches. We measured hunting and digging behaviour, whether successful or not, and the effect of snow depth and temperature. Pine martens were restricted to forested habitats, whereas red foxes used a wide range of habitats. Red foxes were found to dig more often than pine martens, 0.67 vs. 0.39 digging events per kilometre. Hunting was less common and similar in both species, about 0.1 hunting event per kilometre. Pine martens were more efficient in hunting and finding food remains compared to red foxes. Increasing snow depth reduced hunting success and also reduced dig success of red foxes. Food niche overlap was small. Red foxes used mostly voles and carrion remains of ungulates, whereas pine martens used cached eggs and small birds. We suggest that caching eggs is an important strategy for pine martens to survive winter in northern latitudes. Snow depth was important for capturing voles, and thick snow cover appeared to mask the effect of vole peaks. Intensified land use, as clear-cutting and leaving slaughter remains from harvest, will benefit red foxes on the expense of pine martens. The ongoing climate change with warmer winters and less snow will likely further benefit the red fox.     

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.

     

Spatial Niche Segregation of Sympatric Stone Marten and Pine Marten – Avoidance of Competition or Selection of Optimal Habitat?

Coexistence of ecologically similar species relies on differences in one or more dimensions of their ecological niches, such as space, time and resources in diel and/or seasonal scales. However, niche differentiation may result from other mechanisms such as avoidance of high predation pressure, different adaptations or requirements of ecologically similar species. Stone marten (Martes foina) and pine marten (Martes martes) occur sympatrically over a large area in Central Europe and utilize similar habitats and food, therefore it is expected that their coexistence requires differentiation in at least one of their niche dimensions or the mechanisms through which these dimensions are used. To test this hypothesis, we used differences in the species activity patterns and habitat selection, estimated with a resource selection function (RSF), to predict the relative probability of occurrence of the two species within a large forest complex in the northern geographic range of the stone marten. Stone martens were significantly heavier, have a longer body and a better body condition than pine martens. We found weak evidence for temporal niche segregation between the species. Stone and pine martens were both primarily nocturnal, but pine martens were active more frequently during the day and significantly reduced the duration of activity during autumn-winter. Stone and pine martens utilized different habitats and almost completely separated their habitat niches. Stone marten strongly preferred developed areas and avoided meadows and coniferous or deciduous forests. Pine marten preferred deciduous forest and small patches covered by trees, and avoided developed areas and meadows. We conclude that complete habitat segregation of the two marten species facilitates sympatric coexistence in this area. However, spatial niche segregation between these species was more likely due to differences in adaptation to cold climate, avoidance of high predator pressure and/or food preferences by both species than competitive interaction between them.     

On the ratio of phenotype and genotype of sable and pine marten in sympatry zone in the Northern Urals

Analysis of allele frequencies of nine nuclear DNA microsatellite loci in the sable (Martes zibellina) and pine marten (M. martes) demonstrated that these species from allopatric parts of the area differ with a high degree of significance, while hybridization regularly occurs between them in the sympatry zone in the Northern Urals. In total, populations of the sable and pine marten maintain genetic isolation in the sympatry area; however, individual phenotypes do not always correlate with their specific (or hybrid) belonging, which is determined by a genetic method.     

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.