Biogeographical variation in the diet of Holarctic martens (genus Martes,Mammalia: Carnivora: Mustelidae): adaptive foraging in generalists

Aim Studies comparing feeding habits across a genus in different geographical regions or habitats can identify factors associated with adaptive feeding behaviour, linking key ecological traits between consumers and their environment. We investigated biogeographical patterns in dietary composition and trophic diversity across the genus Martes in relation to geographical range and environmental variables. We hypothesized that widely distributed opportunistic Martes species should demonstrate adaptive variations in dietary composition and trophic diversity relative to regional geographical location (e.g. latitude, elevation), environmental variation (e.g. temperature, rainfall, snow cover and primary productivity) and concomitant variation in food supply. Location Europe, Asia and North America. Methods We examined the dietary habits of martens (Martes spp.) using original data expressed as relative frequency of occurrence, and using principal components analysis to extract the main gradients in diet composition. These were then used as response variables in regression analyses, predicted from latitude or elevation. Multiple regression analyses were performed to assess the influence of food types and environmental variables on the trophic diversity index. Results A clear latitudinal gradient in dietary composition was observed. Small mammals were the primary food type, but were less abundant in the diet of martens at lower latitude and elevation. Vegetable matter and insects were consumed more frequently in southerly and/or lower‐elevation localities. Trophic diversity was lower at higher elevation, and increased with a decline in consumption of the dominant food types, i.e. rodents, fruits and insects. Trophic diversity also increased with increasing mean temperature. Main conclusions Biogeographical variations in feeding habits across the genus Martes proved to be associated with latitude, local climate (especially temperature regime) and the availability of alternative potential foods. On an extensive geographical scale, martens respond to varying food availability by adjusting their foraging strategy and thus should be considered facultative generalists. At the species level, however, different climatic variables emerged as differentially important, indicative of adaptations to local conditions. Martes species are opportunistic and flexible feeders, and thus their conservation requires informed management, mindful of how changes in environmental conditions might influence their varied food supply.     

Post-glacial colonization of northwestern North America by the forest-associated American marten (Martes americana,Mammalia: Carnivora: Mustelidae)

Phylogeographic patterns were used to assess intraspecific diversification of American martens (Martes americana). Within martens, two morphological groups (americana and caurina) have been recognized, though the level of distinction between them has been debated. We examined mitochondrial cytochrome b gene haplotypes from 680 martens to explore the colonization history of the Pacific Northwest and found two clades that correspond to the morphological groups. The widespread americana clade extends from interior Alaska south to Montana and eastward to Newfoundland and New England (i.e. northwestern, north-central and northeastern North America). The caurina clade occurs in western North America, minimally extending from Admiralty Island (southeastern Alaska) south to Oregon and Wyoming. Our data indicated two colonization events for the Pacific Northwest (one by members of each clade) and were consistent with the persistence of populations throughout past glacial periods in eastern and western refugia. Due to vegetational and geological history following the past deglaciation, we hypothesize that martens of the caurina clade spread along the North Pacific Coast, and into southeastern Alaska, earlier than martens of the americana clade. Mismatch distributions for the americana clade were indicative of populations that recently experienced demographic expansion, while mismatch distributions for the caurina clade suggested that populations were at equilibrium. These clades are reciprocally monophyletic and distinctive (interclade divergence ranged from 2.5 to 3.0% (uncorrected p), whereas, intraclade divergence was < 0.7%), and two regions of sympatry have been identified. Genetic signatures of past admixture in hybrid zones may have been extinguished during subsequent glacial periods when ranges contracted. This recurrent pattern of relatively restricted western, or Pacific coastal, lineages and more widespread eastern, or interior continental, lineages exists across broad taxonomic groups and suggests a shared biogeographical history.     

Carnivora: the primary structure of the beach marten (Martes foina, Mustelidae) hemoglobin

The primary structures of alpha- and beta-chains from the hemoglobin of the Beach Marten (Martes foina, Carnivora) are presented. The globin chains were separated on CM-cellulose in 8M urea buffer. The amino-acid sequences were established by automatic liquid- and gas-phase Edman degradation of the intact chains and the tryptic peptides from oxidized chains. Comparison of the sequences with human hemoglobin shows 21 exchanges in the alpha- and 12 in the beta-chains. The differences concerning heme and interchain contact sites as well as the substitution alpha 77 (EF6)Pro----Ala are discussed. The latter is observed for the first time in a mammalian hemoglobin. The sequences are compared with those of other Carnivora. The beta-chains of Martes foina and Pteronura brasiliensis (Giant Otter) are found to be identical, but their alpha-chains differ in 7 positions. The surprising small numbers of exchanges between the hemoglobin from Beach marten and that from Lesser and Greater Panda are discussed.     

Mitochondrial genome of the eurasian otterLutra lutra (Mammalia, Carnivora, Mustelidae)

We determined the complete mitochondrial genome of the Eurasian otterLutra lutra, which is an endangered species in Korea. The circle genome (16,536 bp in size) consists of 13 protein-coding, 22 tRNA, and 2 rRNA genes, and a control region, as found in other metazoan animals. Out of the 37 genes, 28 are encoded on the H-strand, and the nine (ND6 and 8 tRNA genes) on the L-strand. Three overlaps among the 13 protein-coding genes were found: ATP8-ATP6, ND4L-ND4, and ND5-ND6. A control region (1090 bp) including the origin of H-strand replication (OH), TAS (a conserved motif TACAT-16bp-ATGTA) and CSB (CSB-1, CSB-2. and CSB-3) was observed between tRNA-Pro and tRNA-Phe genes, and O_L, with 36 highly conserved nucleotides between tRNA-Asn (N) and tRNA-Cys (C) within a cluster of five tRNA genes (WANCY), as typically found in vertebrates. The other important characteristics of theL. lutra mitochondrial genome were described in detail. In addition, a maximum likelihood and Bayesian trees of 9 mustelid species and 1 outgroup were reconstructed based on the nucleotide sequences of 11 protein-coding genes excluding ATP8 and ND6. It showed that Lutrinae formed a monophyletic group with Mustelinae that is not monophyletic. Within the subfamily Lutrinae,L. lutra andEnhydra lutris were grouped together and thenLontra canadentis placed as a sister of the clade. The present result is the first complete mitochondrial genome sequence reported from the genusLutra, and is applicable to molecular phylogenetic, phylogeographic, conservation biological studies for mustelid members. In particular, exploration of sequence variations of the control region may be helpful for analyzing inter-and intra-species variations in the genusLutra.     

Mink (Mammalia; Carnivora; Mustelidae): correction of a widely quoted error

Since the European Mink Mustela lutreola and the introduced American Mink M. vison are now sympatric in some parts of the former's native range, and since the two species are similar in appearance, ecology, and behaviour, a need has arisen for a simple way of discriminating live specimens of the two species in the field. Many publications, particularly field guides, have recommended diagnosis on the basis of the presence of white hair on the upper lip of the European species, and its absence in the American species. This is a mistaken suggestion, which should be avoided by authors. American Mink seldom if ever show the large white moustachial bands seen in some European Mink, and may indeed have no white hairs on the upper lip; but white patches of lesser size are common enough to be a possible cause of confusion.     

Cytogenetics of albinism in polecats of the genus Putorius (Carnivora, Mustelidae)

Karyotypes of two ferret species, Putorius eversmanni (2n = 38) and P. putorius (2n = 40), differ in a single Robertsonian rearrangement, resulting in decreased chromosome number in P. eversmanni. Interspecific hybrids from crosses between P. eversmanni and domesticated albino ferret P. putorius furo are fertile. Hybrid individuals have a chromosome set 2 = 39. Analysis of offspring from crosses of these hybrids showed that albinism is a recessive character. Offspring obtained from crosses between interspecific hybrid ferrets and between these hybrids and parental species was subjected to chromosome analysis. A statistically significant correlation was observed between the chromosome number and albinism. As a rule, albino hybrids have a chromosome number 2n = 40. This suggests that the locus, controlling albinism, is located at one of the two pairs of acrocentric chromsomes involved in Robertsonian rearrangement. The rare occurrence of albino hybrids with 2n = 39 may be attributed to recombination. According to our data, recombination probability is less than 0.5 which indicates that the albinism locus located near the centromere. Possible extrapolation of the data obtained for ferrets to other Mustelidae is discussed.     

Evolution of major histocompatibility complex class I genes in the sable Martes zibellina (Carnivora,Mustelidae)

The molecules encoded by major histocompatibility complex (MHC) genes play an essential role in the adaptive immune response among vertebrates. We investigated the molecular evolution of MHC class I genes in the sable Martes zibellina. We isolated 26 MHC class I sequences, including 12 putatively functional sequences and 14 pseudogene sequences, from 24 individuals from two geographic areas of northeast China. The number of putatively functional sequences found in a single individual ranged from one to five, which might be at least 1–3 loci. We found that both balancing selection and recombination contribute to evolution of MHC class I genes in M. zibellina. In addition, we identified a candidate nonclassical MHC class I lineage in Carnivora, which may have preceded the divergence (about 52–57 Mya) of Caniformia and Feliformia. This may contribute to further understanding of the origin and evolution of nonclassical MHC class I genes. Our study provides important immune information of MHC for M. zibellina, as well as other carnivores.     

Does seasonality explain the evolution and maintenance of delayed implantation in the family Mustelidae (Mammalia: Carnivora)?

Understanding the evolutionary pressures that may have led to the development and retention of delayed implantation in mammals remains an enigmatic puzzle for evolutionary ecologists. Recent studies suggest a strong role of environmental conditions but other attributes of species, notably body size and life history traits, may obscure primary mechanisms. Following the recommendation of Lindenfors et al., we examined environmental correlates related to the evolution of delayed implantation and its subsequent maintenance or loss in the family Mustelidae (Mammalia: Carnivora). We focused on the Mustelidae because evolution and subsequent loss of delayed implantation occurred most commonly within this group. Data on 34 species of mustelids from around the world suggest that delayed implantation may have evolved when optimal times for mating and birthing are separated by more than a gestation period, characteristic of environments with long winters that reduce the opportunities to find mates. Environmental characteristics (seasonality, temperature, snow, latitude, and primary productivity) were highly intercorrelated but seasonality was the best predictor of the evolution or loss of delayed implantation via population traits. Here, structural equations on phylogenetic independent contrasts revealed that high seasonality was correlated with low population density and large individual home range size, which in turn was correlated with presence/absence of delayed implantation. We argue that the evolution of delayed implantation provides the reproductive means to mate during the season (summer) with the greatest prospects for females to ‘choose’ mates when living in high‐latitude seasonal environments that generally reduce these opportunities (i.e. low population density and large ranges). Body mass of female mustelids did not differ between species with and without delayed implantation, refuting the hypothesis that loss of delayed implantation is an evolutionary by‐product of evolving to smaller size. We conclude that understanding the environmental selection pressures responsible for the evolution of life history traits related to density and spacing behaviour allows for a more complete picture of the evolution and subsequent loss of delayed implantation.     

Approaches to pregnancy diagnosis in the sable (Martes zibellina, Mustelidae, Carnivora) by noninvasive methods: Postimplantation period

To develop a reliable approach to pregnancy diagnosis in sables based on noninvasive methods of hormonal status assessment, the concentrations of immunoreactive compounds (IRC) binding with antibodies to progesterone have been measured in the feces of females at different stages of the reproductive cycle. The results show that this concentration is higher in truly pregnant than in mated but nonreproducing females. An increase in the IRC concentration relative to its individual baseline level may be regarded as a reliable indication of true pregnancy.     

Allometry of the baculum and sexual size dimorphism in American martens and fishers (Mammalia: Mustelidae)

Genitalia are among the most variable of morphological traits, and recent research suggests that this variability may be the result of sexual selection. For example, large bacula may undergo post‐copulatory selection by females as a signal of male size and age. This should lead to positive allometry in baculum size. In addition to hyperallometry, sexually selected traits that undergo strong directional selection should exhibit high phenotypic variation. Nonetheless, in species in which pre‐copulatory selection predominates over post‐copulatory selection (such as those with male‐biased sexual size dimorphism), baculum allometry may be isometric or exhibit negative allometry. We tested this hypothesis using data collected from two highly dimorphic species of the Mustelidae, the American marten (Martes americana) and the fisher (Martes pennanti). Allometric relationships were weak, with only 4.5–10.1% of the variation in baculum length explained by body length. Because of this weak relationship, there was a large discrepancy in slope estimates derived from ordinary least squares and reduced major axis regression models. We conclude that stabilizing selection rather than sexual selection is the evolutionary force shaping variation in baculum length because allometric slopes were less than one (using the ordinary least squares regression model), a very low proportion of variance in baculum length was explained by body length, and there was low phenotypic variability in baculum length relative to other traits. We hypothesize that this pattern occurs because post‐copulatory selection plays a smaller role than pre‐copulatory selection (manifested as male‐biased sexual size dimorphism). We suggest a broader analysis of baculum allometry and sexual size dimorphism in the Mustelidae, and other taxonomic groups, coupled with a comparative analysis and with phylogenetic contrasts to test our hypothesis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 955–963.     

Patterns of postnatal development in skulls of lynxes,genus Lynx (Mammalia: Carnivora)

Studies on ossification patterns and other ontogenetic events associated with postnatal cranial growth of wild felids are scarce. An analysis of developmental processes undergone by several cranial structures (presphenoidal and sphenooccipital synchondroses, temporal and sagittal crests, and deciduous and permanent teeth) during postnatal growth has been conducted on a sample of 336 specimens belonging to the four Recent species of lynxes (Lynx pardinus, Lynx lynx, Lynx rufus, and Lynx canadensis). Age has been estimated based on tooth replacement, skull size, and by counting the annual lines of cementum growth. Comparison of the results obtained for each of the four species reveal (1) a single pattern for both tooth replacement and ossification of the sphenooccipital synchondrosis, (2) two ossification patterns for the presphenoidal synchondrosis, (3) a common pattern for development of temporal ridges and sagittal crest showing different degrees of morphological expression, and (4) evidence suggesting the involvement of a heterochronic process, neoteny, in the morphological differentiation of several populations and species of the genus Lynx. These data also support the hypothesis that processes involved in the replacement of carnassials are based on functional requirements. © 1996 Wiley-Liss, Inc.     

The mountain weasel Mustela kathiah (Carnivora: Mustelidae): Molecular and Karyological data

The karyotype of Mustela kathiah was first described. Its structure is most similar to the karyotype of M. altaica, differing in the morphological peculiarities of five pairs of large chromosomes. A comparative analysis of mitochondrial genes in the species Mustela allowed us to clarify understanding of the place of M. kathiah in the system of the genus. The earlier hypothesized proximity of the species to a group of small weasels (altaica, nivalis) or to a group of South Asian species (strigidorsa, nudipes) was not confirmed. A high level of differences between M. kathiah of Vietnam and specimens from southern China in nucleotide sequences of the cytochrome b (7.7%) and ND2 (6–6.2%) genes was found. It is supposed that difference in the two gene sequences found in geographically distanced populations of M. kathiah may be adaptive.     

Systematics,evolution, and biogeography of the Pliocene stem meline badger Ferinestrix (Carnivora: Mustelidae)

Ferinestrix vorax is an extinct mustelid carnivoran of enigmatic relationships, known from a partial mandible and femur collected from the 3.2‐ and 3.6‐Myr‐old deposits of Hagerman Fossil Beds National Monument, Idaho, USA. Here, we report Ferinestrix rapax sp. nov. based on 80 remains of skull and dentition from a 3.1–3.6‐Myr‐old deposit of Udunga, Transbaikal, Russia. We demonstrate that Ferinestrix is a stem genus of the badger subfamily Melinae. This genus is distinctly larger and more carnivorous than any other total‐clade meline. We show that Ferinestrix originated in Asia and immigrated to North America no later than at the early (Zanclean) to late (Piacenzian) Pliocene transition, and that the North American F. vorax and Asian F. rapax underwent parallel evolution toward increased carnivory. © 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 167 , 208–226.     

Late Miocene Carnivora from Chad: Lutrinae (Mustelidae)

We describe extensive Late Miocene fossil Lutrinae from Toros-Menalla, Chad. A minimum of four species are present in this fossiliferous area. Such a large number of species, diverse in size and dental morphology, is significant and unique in the fossil record of the subfamily Lutrinae in the Neogene of Africa. Two new taxa are described, Sivaonyx beyi sp. nov. and Djourabus dabba gen. nov. sp. nov. ; the two other species, which are represented by more fragmentary remains, are assigned to Lutrinae indet. aff. Torolutra sp. and Lutrinae indet. aff. Aonyx sp. Sivaonyx beyi is the best known of the species. It is represented by many dental remains and a subcomplete skeleton. Postcranial characters of this species are not particularly specialized. It is interpreted here as a terrestrial predator with poorly developed aquatic adaptations. Fossils of otters are known from ten different localities at Toros-Menalla, each of which yielded a single individual of one or two species. The presence of four morphologically distinct otters in the area is indicative of a palaeoenvironment with a relatively well-developed freshwater system of lakes and/or rivers.  © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society , 2008, 152 , 793–846.     

On Certain Properties of Water and Energy Metabolism in Representatives of Martes and Mustela Genera (Mammalia: Mustelidae)

The quantities of consumed food and water, quantity and moisture contents of faeces as well as quantity and concentration of excreted urine were determined in representatives of Martes—European pine marten (M. martes) and sable (M. zibellina)—as well as in polecat (Mustela putorius). Under the same cage conditions and free access to food, all three species have similar energy value of their daily diet. However, the level of drinking water consumption and the ratio between the daily total water and energy intake was reliably higher in both Martes species than in polecat. In addition, both marten and sable featured much higher rate of evaporation loss in the overall water balance and, consequently, a higher quantity of heat dissipated with evaporation as compared to polecat. Comparison of the obtained and previous data (Sokolov et al., 1995; Rozhnov, 1991) allowed us to propose that the mentioned differences are specific for representatives of Martes and Mustela genera irrespective of ecological specialization of particular species.     

The geographic ranges of Martes species (Carnivora,Mustelidae) in the Middle Urals in the Late Pleistocene and Holocene

Martes mandibles from Late Pleistocene and Holocene sites in the Middle Urals were identified to the species level using discriminant analysis. As has been shown, sable lived there in the Late Pleistocene, with its geographic range covering all this area until the end of the 18th century; however, its range started to reduce towards the north and northeast in the early 19th century. Over 150 years, the southwestern boundary of the sable range shifted by 3° to reach the current position by the mid-20th century. The pine marten appeared in the Middle Urals in the Holocene no later than 8000 years ago and inhabits this territory at present.     

Cope's rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora)

Cope's rule describes the evolutionary trend for animal lineages to increase in body size over time. In this study, we tested the validity of Cope's rule for a marine mammal clade, the Pinnipedimorpha, which includes the extinct Desmatophocidae, and extant Phocidae (earless seals), Otariidae (fur seals and sea lions), and Odobenidae (walruses). We tested for the presence of Cope's rule by compiling a large dataset of body size data for extant and fossil pinnipeds and then examined how body size evolved through time. We found that there was a positive relationship between geologic age and body size. However, this trend is the result of differences between early assemblages of small-bodied pinnipeds (Oligocene to early Miocene) and later assemblages (middle Miocene to Pliocene) for which species exhibited greater size diversity. No significant differences were found between the number of increases or decreases in body size within Pinnipedimorpha or within specific pinniped clades. This suggests that the pinniped body size increase was driven by passive diversification into vacant niche space, with the common ancestor of Pinnipedimorpha occurring near the minimum adult body size possible for a marine mammal. Based upon the above results, the evolutionary history of pinnipeds does not follow Cope's rule.