Phylogenetic relationships and genetic diversity of badgers from the Korean Peninsula: Implications for the taxonomic status of the Korean badger

Accurate taxonomic classification of wildlife species is crucial for guiding biological research and for developing effective management and conservation programs. The taxonomic status of Eurasian badgers from South Korea remains poorly resolved. Here we assessed the phylogenetic relationships and genetic variation of Eurasia badgers using partial mitochondrial fragments to elucidate the evolutionary history and taxonomic status of badgers from the Korean Peninsula. Forty-eight unique haplotypes from 125 individuals were observed. Phylogenetic reconstructions and reduced median networks indicate that Eurasian badgers consisted of four geographic clades (Japan, Eastern Eurasia, Western Eurasia, and Caucasus) with a relatively weak split observed within Eastern Eurasia. Estimated divergence time between the Japanese and Eastern Eurasian clades, including the Korean population, was 467,100 years (69,200–1,085,500 years). The results of this study support the hypothesis that the Japanese badger migrated from the Eurasian continent over the Korea-Japan land bridge and that the Korean Peninsula was an important refugia during the Pleistocene. Our study confirmed that the South Korean badger, Meles meles, belongs to the Eastern Eurasian clade. Based on these results and those of previous studies, we recommend that the scientific name of the Korean badger be changed from M. meles to Meles leucurus (Asian badger).     

Genetic structure of Eurasian badgers Meles meles (Carnivora: Mustelidae) and the colonization history of Ireland

The present study examined the contemporary genetic composition of the Eurasian badger, Meles meles, in Ireland, Britain and Western Europe, using six nuclear microsatellite loci and a 215‐bp fragment of the mitochondrial DNA control region. Significant population structure was evident within Europe (global multilocus microsatellite F_ST = 0.205, P < 0.001; global mitochondrial control region Φ_ST = 0.399, P < 0.001). Microsatellite‐based cluster analyses detected one population in Ireland, whereas badgers from Britain could be subdivided into several populations. Excluding the island populations of Ireland and Britain, badgers from Western Europe showed further structuring, with evidence of discrete Scandinavian, Central European, and Spanish populations. Mitochondrial DNA cluster analysis grouped the Irish population with Scandinavia and Spain, whereas the majority of British haplotypes grouped with those from Central Europe. The findings of the present study suggest that British and Irish badger populations colonized from different refugial areas, or that there were different waves of colonization from the source population. There are indications for the presence of an Atlantic fringe element, which has been seen in other Irish species. We discuss the results in light of the controversy about natural versus human‐mediated introductions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Mitochondrial DNA reveals a strong phylogeographic structure in the badger across Eurasia

The badger, Meles meles, is a widely distributed mustelid in Eurasia and shows large geographic variability in morphological characters whose evolutionary significance is unclear and needs to be contrasted with molecular data. We sequenced 512 bp of the mitochondrial DNA control region in 115 Eurasian badgers from 21 countries in order to test for the existence of structuring in their phylogeography, to describe the genetic relationships among their populations across its widespread geographic range, and to infer demographic and biogeographic processes. We found that the Eurasian badger is divided into four groups regarding their mitochondrial DNA: Europe, Southwest Asia, North and East Asia, and Japan. This result suggests that the separation of badgers into phylogeographic groups was influenced by cold Pleistocene glacial stages and permafrost boundaries in Eurasia, and by geographic barriers, such as mountains and deserts. Genetic variation within phylogeographic groups based on distances assuming the Tamura-Nei model with rate heterogeneity and invariable sites (d(T-N) range: 3.3-4.2) was much lower than among them (d(T-N) range: 10.7-38.0), and 80% of the variation could be attributed to differences among regions. Spatial analysis of molecular variance (samova), median-joining network, and Mantel test did not detect genetic structuring within any of the phylogeographic groups with the exception of Europe, where 50% of variation was explained by differences among groups of populations. Our data suggest that the European, Southwest Asian, and North and East Asian badgers evolved separately since the end of Pliocene, at the beginnings of glacial ages, whereas Japanese badgers separated from continental Asian badgers during the middle Pleistocene. Endangered badgers from Crete Island, classified as Meles meles arcalus subspecies, were closely related to badgers from Southwest Asia. We also detected sudden demographic growth in European and Southwest Asian badgers that occurred during the Middle Pleistocene.     

Badgers prefer cattle pasture but avoid cattle: implications for bovine tuberculosis control

Effective management of infectious disease relies upon understanding mechanisms of pathogen transmission. In particular, while models of disease dynamics usually assume transmission through direct contact, transmission through environmental contamination can cause different dynamics. We used Global Positioning System (GPS) collars and proximity‐sensing contact‐collars to explore opportunities for transmission of Mycobacterium bovis [causal agent of bovine tuberculosis] between cattle and badgers (Meles meles). Cattle pasture was badgers’ most preferred habitat. Nevertheless, although collared cattle spent 2914 collar‐nights in the home ranges of contact‐collared badgers, and 5380 collar‐nights in the home ranges of GPS‐collared badgers, we detected no direct contacts between the two species. Simultaneous GPS‐tracking revealed that badgers preferred land > 50 m from cattle. Very infrequent direct contact indicates that badger‐to‐cattle and cattle‐to‐badger M. bovis transmission may typically occur through contamination of the two species’ shared environment. This information should help to inform tuberculosis control by guiding both modelling and farm management.     

Cranial variation in the European badger Meles meles (Carnivora,Mustelidae) in Scandinavia

Morphometric variation in 30 craniometric characters of 465 skulls of the European badgers (Meles meles) from across Europe was analysed. Multivariate analyses revealed that the populations from Norway, Sweden, and Finland differ from other European populations in having smaller skulls. The analyses also revealed significant differences between the ‘south‐western Norwegian’ and ‘main Fennoscandian’ forms. On average, badgers from south‐west Norway were smaller than those of the remaining Fennoscandia. Morphological differences between the ‘south‐western Norwegian’ and ‘main Fennoscandian’ populations of M. meles suggest a possible in situ semisympatric divergence since the beginning of the Holocene warming, or a complex history of two groups involving at least two colonization routes. The small‐sized Scandinavian badgers may be close to the ancestral form that used to be widespread in Denmark and throughout Europe. The animals from south‐west Norway may instead be descendants of ancestors that were the first to penetrate the southern parts of the Scandinavian Peninsula. The ‘main Fennoscandian’ badgers are likely to have been the descendants of the second wave of recolonization of Scandinavia. Specifically, they might have colonized the Scandinavian Peninsula from the east after the last glaciation.     

Distribution and population density of badgers Meles meles in Luxembourg

1. The distribution and density of Eurasian badgers Meles meles in Luxembourg was estimated by gathering information about the location of badger setts with a questionnaire survey, by visiting 708 setts in order to classify them as ‘main setts’ or ‘outliers’, and by estimating social group size by directly counting emerging badgers. 2. Badgers were found to be widely distributed in Luxembourg, with a minimum main sett density of 0.17 setts/km². Setts were sited preferentially in forest habitat. The mean minimum group size was 4.6 badgers. 3. The Luxembourg badger population was conservatively estimated to contain at least 2010 adult and young badgers (95% CI 1674–2347) in spring 2002, equivalent to a density of 0.78 adult and young badgers/km² (95% CI 0.65–0.91). This is moderate compared to most of continental Europe.     

Local feeding specialization by badgers (Meles meles) in a mediterranean environment

A case of local feeding specialization in the European badger (Meles meles), a carnivore species with morphological, physiological and behavioural traits proper to a trophic generalist, is described. For the first time, we report a mammalian species, the European rabbit (Oryctolagus cuniculus), as the preferred prey of badgers. Secondary prey are consumed according to their availability, compensating for temporal fluctuations in the abundance of rabbit kittens. We discuss how both predator (little ability to hunt) and prey (profitability and predictability) features, may favour the observed specialization, as predicted by foraging theory. Badgers show a trend to specialize on different prey in different areas throughout the species range. It is suggested that changes in prey features can reverse the badger feeding strategy at the population level. Such dynamic behavioural responses make difficult to label badgers as generalists or specialists at the species level.     

Helminth parasites of the Eurasian badger (<Emphasis Type="Italic">Meles meles</Emphasis> L.) in the Basque Country (Spain)

The helminthological study of 26 Eurasian badgers (Meles meles L.) in the Basque Country (northern Spain) revealed the presence of two trematode (Euryhelmis squamula and Brachylaima sp.), three cestode (Atriotaenia incisa, Mesocestoides sp. and Taenia sp.) and five nematode (Aonchotheca putorii, Physaloptera sp., Molineus patens, Uncinaria criniformis and Strongyloides sp.) species. All 15 individuals analysed for Trichinella sp. were negative. The coprological analysis (flotation and migration) revealed the excretion of strongylid, capillariid and trematode eggs, and Crenosoma sp. and Angiostrongylus sp. larvae. No sex- or age-related differences were found in the parasite burden or egg and larvae excretion. A. incisa and M. patens abundances were positively correlated, both species being negatively correlated with badger weight. The presence of adults of U. criniformis and strongylid eggs in faeces was not independent. Badgers excreting Angiostrongylus larvae were in poorer condition than those not excreting.     

Molecular phylogeny of Eurasian badgers (Meles) around the distribution boundaries,revealed by analyses of mitochondrial DNA and Y-chromosomal genes

Based on previous molecular and morphological analyses, Eurasian badgers are currently classified into Meles meles distributed in Europe, M. canescens in the Caucasus and Middle East, M. leucurus in continental Asia and M. anakuma in Japan. The precise locations of their distribution boundaries are still unclear. Therefore, in the present study, we clarified the phylogenetic relationships in the genus Meles around its distribution boundaries, based on mitochondrial DNA (mtDNA) and Y-chromosomal genes. From 71 badgers examined, 29 mtDNA haplotypes were identified, including new 26 types. Multiple haplotypes of SRY and CAN-SINEs were identified from 23 males, including two new haplotypes of SRY. The mtDNA phylogeny showed that the Ural Mountains were not a current distribution boundary between M. meles and M. leucurus. In addition, our results supported the hypothesis that the Bosphorus Strait is a geographical barrier between M. meles and M. canescens. The badgers from Bulgaria north of the Bosphorus Strait shared haplotypes with M. meles. On the other hand, badgers from Far Eastern Russia distributed in the eastern peripheral region of the Asian Continent had haplotypes of M. leucurus. The badgers from Norway and Finland shared haplotypes with M. meles.     

The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis

Are setts significant determinants of badger socio‐spatial organisation, and do suitable sett sites represent a limited resource, potentially affecting badger distributions? The factors determining diurnal resting den, or sett, location and selection by Eurasian badgers Meles meles L. were investigated in Wytham Woods, Oxfordshire. 279 sett sites were located. The habitat parameters that were associated with the siting of these setts were analysed and associations were sought between sett location and character and the body condition and body weight of resident badgers Habitat characteristics in the vicinity of setts were significantly different from randomly selected points. Badgers preferentially selected sites with sandy, well‐drained soils, situated on NW‐facing, convex and moderately inclined slopes at moderate altitude. There was no evidence that sett morphology (number of entrances, sett area, number of hinterland latrines) was affected by the surrounding sett site habitat characteristics. Mean body weight was significantly higher for badgers occupying territories with setts in sandy soils, situated on NW‐facing slopes, than in territories with less optimal sett characteristics. Contrary to the hypothesis that the availability of sett sites was limiting, and therefore that sett dispersion dictates the spatial and social organisation of their populations, the badgers were clearly able to excavate new setts. On our measures, these new setts were not inferior to old established ones, despite occupying subsequently exploited sites; the badgers utilising these new setts had neither lighter body weights nor poorer body condition scores. During the period of our study badgers have manifestly been able to dig numerous new setts; as satisfactory sites still remain available, this indicates that suitable sett sites have not yet become a limiting resource. There was no relationship between sett age and the characteristics of the site in which it was dug, as suitable sites were not limiting. Significantly, population expansion during the decade 1987–1997 was not constrained by lack of setts, rather the main proliferation in setts occurred after the population size had peaked in 1996. Some implications for the management and conservation of the Eurasian badger are considered.     

Temporal and geographical variation in skull size of the red fox (Vulpes vulpes) and the Eurasian badger (Meles meles) in Austria

Using museum material, we studied temporal changes in skull size of 185 red foxes (Vulpes vulpes Linnaeus, 1758) and 71 Eurasian badgers (Meles meles Linnaeus, 1758) collected in Austria between 1866 and 2007. Four measurements were taken and combined into principal components by means of a principal components analysis. Akaike's information criterion models indicated that skull size of the red fox and the Eurasian badger is positively related to the year of collection and negatively to altitude but not to latitude or longitude. However, for the Eurasian badger, the relationship between skull size and year is only on the verge of significance. We suggest that the increase in skull size with year is a result of improved food availability during the 20th Century from man‐made resources such as agricultural produce and garbage, and the decrease in skull size with altitude is possibly the result of a parallel decrease in primary productivity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Genetic evidence that culling increases badger movement: implications for the spread of bovine tuberculosis

The Eurasian badger (Meles meles) has been implicated in the transmission of bovine tuberculosis (TB, caused by Mycobacterium bovis) to cattle. However, evidence suggests that attempts to reduce the spread of TB among cattle in Britain by culling badgers have mixed effects. A large-scale field experiment (the randomized badger culling trial, RBCT) showed that widespread proactive badger culling reduced the incidence of TB in cattle within culled areas but that TB incidence increased in adjoining areas. Additionally, localized reactive badger culling increased the incidence of TB in cattle. It has been suggested that culling-induced perturbation of badger social structure may increase individual movements and elevate the risk of disease transmission between badgers and cattle. Field studies support this hypothesis, by demonstrating increases in badger group ranges and the prevalence of TB infection in badgers following culling. However, more evidence on the effect of culling on badger movements is needed in order to predict the epidemiological consequences of this control strategy. Here, analysis of the genetic signatures of badger populations in the RBCT revealed increased dispersal following culling. While standard tests provided evidence for greater dispersal after culling, a novel method indicated that this was due to medium- and long-distance dispersal, in addition to previously reported increases in home-range size. Our results also indicated that, on average, badgers infected with M. bovis moved significantly farther than did uninfected badgers. A disease control strategy that included culling would need to take account of the potentially negative epidemiological consequences of increased badger dispersal.     

Antibodies to Mycobacterium bovis in wild carnivores from Doñana National Park (Spain)

We conducted a retrospective serologic survey for antibodies against the MPB70 protein of Mycobacterium bovis in wild carnivores from Do?ana National Park (southwestern Spain). Serum samples from 118 red foxes (Vulpes vulpes), 39 Iberian lynx (Lynx pardinus), 31 Eurasian badgers (Meles meles), five Egyptian mongoose (Herpestes ichneumon), four European genet (Genetta genetta), and one Eurasian otter (Lutra lutra) were analyzed using an indirect competitive enzyme-linked immunoassay. Antibodies against the MPB70 protein of M. bovis were detected in seven badgers, five foxes, and one lynx. The frequency of positive animals was significantly higher in badger (23%) than in lynx (3%) and fox (4%). Antibodies were not detected in other species. Annual antibody frequency peaked at 38% in badgers and 11% for red fox. These species may contribute to persistence of bovine tuberculosis in Do?ana.     

How many Eurasian badgers <Emphasis Type="Italic">Meles meles</Emphasis> L. are there in the Republic of Ireland?

In Ireland, the badger Meles meles L is a reservoir species for Mycobacterium bovis and, as such, contributes to the maintenance of bovine tuberculosis in cattle. A previous estimate of the badger population in the Republic was 200,000 badgers. In the current study, we obtained data on badger numbers from a large-scale badger removal project (the Four-Area project). The removal areas of the Four-Area Project were surrounded by barriers (either water or buffer areas where removals were also conducted) to prevent badger immigration. Within these areas, a grid of 0.25 km² was created within which we knew the badger numbers and habitat types (based on Corine data). Associations between badger numbers and habitat type were investigated using negative binomial modeling. Extrapolations from the model yielded an estimated badger population in the Republic of approximately 84,000 badgers. The implications of these findings are discussed.     

The diet of the badger Meles meles in the Republic of Ireland

The diet of the Eurasian badger (Meles meles) in the Republic of Ireland was studied by examination of the stomach contents of 686 badgers, collected between March 2005 and September 2006. It was found that the relative importance of different food types, as indicated by their frequency of occurrence and ingested bulk in the diet, fluctuated seasonally. Tipulid larvae (Cl. Insecta, Ord. Tipulidae) dominated the diet in spring; Anura (Cl. Amphibia) and Aculeata (Ord. Hymenoptera) during the summer; and Noctuid larvae (Cl. Insecta, Ord. Noctuidae) in autumn and winter. Thus this type of foraging behaviour supports the contention that badgers are generalist foragers with seasonal food preferences. This feeding behaviour is more similar to that of badgers in Italy and Spain than to badgers in England.     

A survey of helminth infection in Eurasian badgers (Meles meles) in relation to their foraging behaviour in a Mediterranean environment in southwest Portugal

This study provides the first data on the helminth fauna of the Eurasian badger in the southwestern edge of its range (Grândola Mountain, Portugal) and interprets the results in relation to badger diet and feeding behaviour. By examination of 163 badger faecal samples, faecal developmental stages (eliminative forms) of four helminth species and one genus were identified: one cestode (Atriotaenia incisa) and four nematodes (Mastophorus muris, Molineus patens, Uncinaria criniformis and Strongyloides sp.). The overall prevalence of parasites was 62%, with limited seasonal variation. Single parasite excretions were dominant and Strongyloides sp. excretion was the most common. Diet assessment based on 450 faecal samples revealed that badgers consumed mainly insects and fruits. No correlation was detected between helminth prevalence and diet. Apparently, diet (mainly insects) and feeding behaviour (fossorial), together with the species’ social behaviour (anal scent marking of group members), facilitate the infection with helminths. The helminth fauna of Eurasian badgers in Grândola Mountain has isolationist characteristics, apparently indicating low host colonisation.     

Sexual dimorphism of craniological characters in Eurasian badgers, Meles spp. (Carnivora, Mustelidae)

An analysis of 30 craniological characters of Eurasian badgers (Meles spp.) revealed different levels of sexual size dimorphism (SSD) and geographic variation in the three different species. SSD is displayed mostly in the general size of the skull (condylobasal length, zygomatic width, width of rostrum, and cranial height) and mandible (height of the vertical mandibular ramus, total length of the mandible, and length between the angular process and infradentale), and in some dental characters (length of the upper molar M¹). The most stable size dimorphism is manifested in the size of the canines, which is pronounced in all studied samples. SSD is not apparent in the length of the auditory bulla, the postorbital width, the minimum palatal width, the length of the lower molar M₂, and the talonid length of the lower carnassial tooth M₁.In both the European badgers, Meles meles, and the Asian badgers, Meles leucurus, two geographic forms that differ in the degree of SSD have been found. The most pronounced SSD of cranial characters is found in the Transcaucasian form of Meles meles and the Far-Eastern form of Meles leucurus. In the large European form of Meles meles, SSD is less pronounced in both absolute and relative criteria than in the smaller Transcaucasian form. An analogous situation is observed in the larger Siberian and smaller Far-Eastern forms of Meles leucurus. In the Japanese badgers, Meles anakuma, a downsizing of the skull is accompanied by a decrease in SSD (except in canine size) in comparison to the continental species. The significant differences in the manifestation of SSD in the Eurasian badgers support an earlier hypothesis (Abramov, 2001. Proc. Zool. Inst. Russ. Acad. Sci. 288, 221-233; Abramov, 2002. Russ. J. Theriol. 1 (1), 57-60; Abramov, 2003. Small Carnivore Conserv. 29, 5-7) that Meles meles, Meles leucurus, and Meles anakuma are separate species. The differences in the level of SSD among and within these three species of badgers may be attributed not to differences in the diet or social structure, but to the history of speciation events and formation of intraspecific distribution ranges.     

Resource dispersion and badger population density in Mediterranean woodlands: is food,water or geology the limiting factor?

Eurasian badgers, Meles meles, in Mediterranean cork‐oak woodlands live in small groups within territories that embrace a mosaic of habitats where several setts (dens) are scattered. Assuming that their population density was related to home range sizes and that this in turn was influenced by food and water availability and the existence of substrate suitable for sett construction, we explored the relationship between these parameters. Two biotopes were predominantly important in providing food security to badgers in the ‘Grândola’ mountain study area: olive groves and orchards or vegetable gardens. Analysis of the mean total area of these two habitats in the ranges of radio‐tracked badgers permitted us to extrapolate to an estimate that the 66 km² encompassed eleven areas with the capacity to support badger groups each composed by 6–8 individuals. Since only three groups populated the area we concluded that food availability was not limiting badger density. Sites with surface water in summer (the dry season) seem sufficient to support more badger groups than existed, leading us to believe that this factor was also not limiting badger density. Simultaneously, using a logistic regression model and the biophysical characteristics of sett sites as explanatory variables, four predictor variables determined sett location: the existence of a geological fault/discontinuity, ridges, valleys and the distance to abandoned farm houses, of which the former had the higher odds ratio, being thus the best sett location predictor. Indeed, 56% of the areas predicted with >80% confidence to contain a badger sett were encompassed within a known home range. Therefore, our results suggest that, in Mediterranean cork oak woodlands in SW Portugal, the main factor limiting badger's density is the availability of suitable sites for setts. However, in areas where suitable sites for burrows existed, but food patches were absent, badgers were not found. This could indicate that the presence of both factors was necessary for badgers, although in this area sites suitable for digging setts appeared to be the primary limiting factor.     

The ‘omnivorous badger dilemma’: towards an integration of nutrition with the dietary niche in wild mammals

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Isolation of 39 polymorphic microsatellite loci and the development of a fluorescently labelled marker set for the Eurasian badger (Meles meles) (Carnivora: Mustelidae)

We have isolated 78 microsatellite loci from the Eurasian badger (Meles meles). Of the 52 loci characterized, 39 were found to be polymorphic. A fluorescently labelled primer set was developed to enable individual‐specific 17‐locus genotypes to be obtained efficiently.