Evolutionary and ecological traps for brown bears Ursus arctos in human‐modified landscapes

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Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears

Models for the development of species distribution in Europe typically invoke restriction in three temperate Mediterranean refugia during glaciations, from where recolonization of central and northern Europe occurred. The brown bear, Ursus arctos, is one of the taxa from which this model is derived. Sequence data generated from brown bear fossils show a complex phylogeographical history for western European populations. Long-term isolation in separate refugia is not required to explain our data when considering the palaeontological distribution of brown bears. We propose continuous gene flow across southern Europe, from which brown bear populations expanded after the last glaciation.     

Conservation genetics of the European brown bear - a study using excremental PCR of nuclear and mitochondrial sequences

In the Brenta area of northern Italy, a brown bear Ursus arctos population is rapidly going extinct. Restocking of the population is planned. In order to study the genetics of this highly vulnerable population with a minimum of stress to the animals we have developed a PCR-based method that allows the study of mitochondrial and nuclear gene sequences from droppings collected in the field. This method is generally applicable to animals in the wild. Using excremental as well as hair samples, we show that the Brenta population is monomorphic for one mitochondrial lineage and that female as well as male bears exist in the area. In addition, 70 samples from other parts of Europe were studied. As others have previously reported, the mitochondrial gene pool of European bears is divided into two major clades, one with a western and the other with an eastern distribution. Whereas populations generally belong to either one or the other mitochondrial clade, the Romanian population contains both clades. The bears in the Brenta belong to the western clade. The implications for the management of brown bears in the Brenta and elsewhere in Europe are discussed.     

Genetic diversity of Dinaric brown bears (Ursus arctos) in Croatia with implications for bear conservation in Europe

Brown bears have lost most of their range on the European continent. The remaining western populations are small, isolated and highly endangered. The Dinaric-Pindos brown bear population is the western-most stable population and the fourth largest in Europe. It has been recognized as a potential source for recolonization of populations whose survival is at risk. Indeed, several translocations of Dinaric bears to Italy, Austria and France have recently been made. Despite the importance of the Dinaric bear population, its genetic status remains poorly understood. Using tissue samples from 156 hunted or accidentally killed Dinaric bears in Croatia, this study analysed genetic diversity at 12 microsatellite loci, as well as population structure and past reductions in size. In addition, a subset of 59 samples was used to assess diversity of the mitochondrial DNA control region. The results indicate that Dinaric bears have high nuclear genetic diversity, as compared to other extant brown bear populations, despite genetic evidence of a bottleneck caused by past persecutions. However, haplotype diversity was low, probably as a result of male-biased dispersal and female philopatry. Not surprisingly, no evidence of population sub-structure was found using nuclear markers, as the bear habitat has remained continuous and the highway network has been built only recently. Management should focus on maintaining habitat connectivity and keeping the effective population size as large as possible. In addition, when removing individuals, care should be taken not to further deplete the population of rare haplotypes. A coordinated transboundary management of the entire Dinaric-Pindos brown bear population should be a priority for its long-term conservation.     

Could brown bears (Ursus arctos) have survived in Ireland during the Last Glacial Maximum?

Brown bears are recorded from Ireland during both the Late Pleistocene and early–mid Holocene. Although most of the Irish landmass was covered by an ice sheet during the Last Glacial Maximum (LGM), Irish brown bears are known to have hybridized with polar bears during the Late Pleistocene, and it is suggested that the Irish brown bear population did not become extinct but instead persisted in situ through the LGM in a southwestern ice-free refugium. We use historical population modelling to demonstrate that brown bears are highly unlikely to have survived through the LGM in Ireland under any combination of life-history parameters shown by living bear populations, but instead would have rapidly become extinct following advance of the British–Irish ice sheet, and probably recolonized Ireland during the end-Pleistocene Woodgrange Interstadial from a closely related nearby source population. The time available for brown bear–polar bear hybridization was therefore restricted to narrow periods at the beginning or end of the LGM. Brown bears would have been extremely vulnerable to extinction in Quaternary habitat refugia and required areas substantially larger than southwestern Ireland to survive adverse glacial conditions.     

Ancient DNA analyses reveal high mitochondrial DNA sequence diversity and parallel morphological evolution of late pleistocene cave bears

Cave bears (Ursus spelaeus) existed in Europe and western Asiauntil the end of the last glaciation some 10,000 years ago.To investigate the genetic diversity, population history, andrelationship among different cave bear populations, we havedetermined mitochondrial DNA sequences from 12 cave bears thatrange in age from about 26,500 to at least 49,000 years andoriginate from nine caves. The samples include one individualfrom the type specimen population, as well as two small-sizedhigh-Alpine bears. The results show that about 49,000 yearsago, the mtDNA diversity among cave bears was about 1.8-foldlower than the current species-wide diversity of brown bears(Ursus arctos). However, the current brown bear mtDNA gene poolconsists of three clades, and cave bear mtDNA diversity is similarto the diversity observed within each of these clades. The resultsalso show that geographically separated populations of the high-Alpinecave bear form were polyphyletic with respect to their mtDNA.This suggests that small size may have been an ancestral traitin cave bears and that large size evolved at least twice independently.     

Post-glacial colonization of Western Europe brown bears from a cryptic Atlantic refugium out of the Iberian Peninsula

The European brown bear (Ursus arctos) shows a particular phylogeography that has been used to illustrate the model for contraction-expansion dynamics related to glacial refugia in Southern European peninsulas. Recent studies, however, have nuanced the once generally accepted paradigm, indicating the existence of cryptic refugia for some species further north. In this paper we collected available data on chronology and mitochondrial haplotypes from Western European brown bears, adding new sequences from present day individuals from the Cantabrian (North Iberia) area, in order to reconstruct the dynamics of the species in the region. Both genetics and chronology show that the Iberian Pleistocene lineages were not the direct ancestors of the Holocene ones, the latter entering the Peninsula belatedly (around 10,000 years BP) with respect to other areas such as the British Isles. We therefore propose the existence of a cryptic refugium in continental Atlantic Europe, from where the bears would expand as the ice receded. The delay in the recolonization of the Iberian Peninsula could be due to the orographic characteristics of the Pyrenean-Cantabrian region and to the abundant presence of humans in the natural entrance to the Peninsula.     

Phylogeography of noble crayfish (Astacus astacus) reveals multiple refugia

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Cranial distinctiveness in the Apennine brown bear: genetic drift effect or ecophenotypic adaptation?

Molecular studies highlighted a strong genetic affinity between the remnant and isolated population of the Apennine brown bear and other southern European populations. Despite this genetic closeness a recent morphometric study revealed a marked phenotypic distinctiveness of the Apennine population, supporting the reinstatement of a distinct taxon (Ursus arctos marsicanus). By building upon previous morphological analyses, we adopted geometric morphometrics to better investigate the skull morphology of the Apennine brown bear with reference to the other, closely related southern European populations. Both skull shape and size differences confirmed the strong divergence of U. arctos marsicanus. In particular, the Apennine bears are characterized by an enlargement of the supraorbital apophysis and a larger distance across the zygomatic arches. Furthermore, our analyses highlighted significant shape differences of the first upper molar in the Apennine bears. Our results suggest that the Apennine bears underwent a rapid morphological change, possibly driven by genetic drift and local selective pressures. Because the greatest morphological differentiation is likely to be related to the muscles involved in mastication, we hypothesize that local selective pressures might be related to a shift in food habits, with highly reduced depredation and feeding on large carcasses in favour of vegetation and hard mast (beech nuts and acorns). These results suggest an adaptive distinctiveness of the Apennine bears, which should be carefully considered in any management and conservation action addressed to this highly endangered population. Although more in‐depth molecular studies are required to better assess the taxonomic and genetic status of the Apennine brown bear population, our study emphasizes the importance of morphological analyses as a complementary tool for a more thorough characterization of variation and divergence in endangered taxa. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

The power of genetic monitoring for studying demography,ecology and genetics of a reintroduced brown bear population

Genetic monitoring has rarely been used for wildlife translocations despite the potential benefits this approach offers, compared to traditional field‐based methods. We applied genetic monitoring to the reintroduced brown bear population in northern Italy. From 2002 to 2008, 2781 hair and faecal samples collected noninvasively plus 12 samples obtained from captured or dead bears were used to follow the demographic and geographical expansion and changes in genetic composition. Individual genotypes were used to reconstruct the wild pedigree and revealed that the population increased rapidly, from nine founders to >27 individuals in 2008 (λ = 1.17–1.19). Spatial mapping of bear samples indicated that most bears were distributed in the region surrounding the translocation site; however, individual bears were found up to 163 km away. Genetic diversity in the population was high, with expected heterozygosity of 0.74–0.79 and allelic richness of 4.55–5.41. However, multi‐year genetic monitoring data showed that mortality rates were elevated, immigration did not occur, one dominant male sired all cubs born from 2002 to 2005, genetic diversity declined, relatedness increased, inbreeding occurred, and the effective population size was extremely small (Ne = 3.03, ecological method). The comprehensive information collected through genetic monitoring is critical for implementing future conservation plans for the brown bear population in the Italian Alps. This study provides a model for other reintroduction programmes by demonstrating how genetic monitoring can be implemented to uncover aspects of the demography, ecology and genetics of small and reintroduced populations that will advance our understanding of the processes influencing their viability, evolution, and successful restoration.     

Denning in brown bears

1. Hibernation represents an adaptation for coping with unfavorable environmental conditions. For brown bears Ursus arctos, hibernation is a critical period as pronounced temporal reductions in several physiological functions occur.
2. Here, we review the three main aspects of brown bear denning: (1) den chronology, (2) den characteristics, and (3) hibernation physiology in order to identify (a) proximate and ultimate factors of hibernation as well as (b) research gaps and conservation priorities.
3. Den chronology, which varies by sex and reproductive status, depends on environmental factors, such as snow, temperature, food availability, and den altitude. Significant variation in hibernation across latitudes occurs for both den entry and exit.
4. The choice of a den and its surroundings may affect individual fitness, for example, loss of offspring and excessive energy consumption. Den selection is the result of broad‐ and fine‐scale habitat selection, mainly linked to den insulation, remoteness, and availability of food in the surroundings of the den location.
5. Hibernation is a metabolic challenge for the brown bears, in which a series of physiological adaptations in tissues and organs enable survival under nutritional deprivation, maintain high levels of lipids, preserve muscle, and bone and prevent cardiovascular pathologies such as atherosclerosis.

It is important to understand: (a) proximate and ultimate factors in denning behavior and the difference between actual drivers of hibernation (i.e., factors to which bears directly respond) and their correlates; (b) how changes in climatic factors might affect the ability of bears to face global climate change and the human‐mediated changes in food availability; (c) hyperphagia (period in which brown bears accumulate fat reserves), predenning and denning periods, including for those populations in which bears do not hibernate every year; and (d) how to approach the study of bear denning merging insights from different perspectives, that is, physiology, ecology, and behavior.     

Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors

• 1 We reviewed worldwide spatial patterns in the food habits of the brown bear Ursus arctos in relation to geographical (latitude, longitude, altitude) and environmental (temperature, snow cover depth and duration, precipitation, primary productivity) variables.
• 2 We collected data from 28 studies on brown bear diet based on faecal analysis, covering the entire geographical range of this widely distributed large carnivore. We analysed separately four data sets based on different methods of diet assessment.
• 3 Temperature and snow conditions were the most important factors determining the composition of brown bear diet. Populations in locations with deeper snow cover, lower temperatures and lower productivity consumed significantly more vertebrates, fewer invertebrates and less mast. Trophic diversity was positively correlated with temperature, precipitation and productivity but negatively correlated with the duration of snow cover and snow depth. Brown bear populations from temperate forest biomes had the most diverse diet. In general, environmental factors were more explicative of diet than geographical variables.
• 4 Dietary spatial patterns were best revealed by the relative biomass and energy content methods of diet analysis, whereas the frequency of occurrence and relative biomass methods were most appropriate for investigating variation in trophic diversity.
• 5 Spatial variation in brown bear diet is the result of environmental conditions, especially climatic factors, which affect the nutritional and energetic requirements of brown bears as well as the local availability of food. The trade‐off between food availability on the one hand, and nutritional and energetic requirements on the other hand, determines brown bear foraging decisions. In hibernating species such as the brown bear, winter severity seems to play a role in determining foraging strategies. Large‐scale reviews of food habits should be based on several measures of diet composition, with special attention to those methods reflecting the energetic value of food.

     

The mating system of the brown bear Ursus arctos

• 1 Research on mating systems and reproductive strategies is valuable for providing ethological knowledge, important for the management and conservation of a species, and in a broader sense, important for biodiversity conservation.
• 2 We reviewed the literature to document the mating system of the brown bear Ursus arctos. We determined that many aspects of the reproduction of the brown bear remain unclear, including (i) biological aspects, such as hormone and oestrous cycling, sperm competition, mate choice, sexually selected infanticide, etc. and (ii) human impacts on the mating system, occurring when humans alter population size and structure, through, for example, hunting or habitat degradation.
• 3 We considered three mating system classification frameworks from the literature ( Emlen & Oring 1977 , Clutton‐Brock 1989 , Shuster & Wade 2003 ) and applied various brown bear populations to them. We did this (i) to document the plasticity of the mating system of the brown bear, and (ii) to find commonalities among the reported mating system classifications in order to provide a general and common classification of the brown bear's mating system.
• 4 The mating system of the brown bear can, in general, be classed as ‘polygamous’. Subclassifications can nevertheless be valuable on smaller spatial scales.
• 5 Within the polygamous mating system of the brown bear, biological aspects and human impacts can influence reproductive strategies at the individual and population level. Mating system classification frameworks often lack a common terminology, which contributes to the variety of published classifications of the mating system of the brown bear.

     

Genetic turnovers and northern survival during the last glacial maximum in European brown bears

The current phylogeographic pattern of European brown bears (Ursus arctos) has commonly been explained by postglacial recolonization out of geographically distinct refugia in southern Europe, a pattern well in accordance with the expansion/contraction model. Studies of ancient DNA from brown bear remains have questioned this pattern, but have failed to explain the glacial distribution of mitochondrial brown bear clades and their subsequent expansion across the European continent. We here present 136 new mitochondrial sequences generated from 346 remains from Europe, ranging in age between the Late Pleistocene and historical times. The genetic data show a high Late Pleistocene diversity across the continent and challenge the strict confinement of bears to traditional southern refugia during the last glacial maximum (LGM). The mitochondrial data further suggest a genetic turnover just before this time, as well as a steep demographic decline starting in the mid‐Holocene. Levels of stable nitrogen isotopes from the remains confirm a previously proposed shift toward increasing herbivory around the LGM in Europe. Overall, these results suggest that in addition to climate, anthropogenic impact and inter‐specific competition may have had more important effects on the brown bear's ecology, demography, and genetic structure than previously thought.     

Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers

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Noninvasive genetic assessment of brown bear population structure in Bulgarian mountain regions

The Balkans are one of the last large refugia for brown bear (Ursus arctos) populations in Europe, and Bulgaria, in particular, contains relatively large areas of suitable brown bear habitat and a potential population of more than 600 individuals. Despite this, the majority of brown bear research remains focused on bear populations in Central and Western Europe. We provide the first assessment of genetic population structure of brown bears in Bulgaria by analysing tissue samples (n = 16) as well as samples collected with noninvasive genetic methods, including hair and faecal samples (n = 189 and n = 163, respectively). Sequence analysis of a 248 base pair fragment of the mitochondrial control region showed that two highly divergent mitochondrial European brown bear lineages form a contact zone in central Bulgaria. Furthermore, the analysis of 13 polymorphic microsatellite markers identified 136 individuals and found substantial genetic variability (H_e = 0.74; N_A = 8.9). The combination of both genetic markers revealed the presence of weak genetic substructure in the study area with considerable degrees of genetic admixture and the likely presence of migration corridors between the two subpopulation in the Rhodope Mountains and Stara Planina as evidenced from the genetic detection of two male long-distance dispersers. A detailed assessment from densely collected samples in the Rhodope Mountains resulted in a population size estimate of 315 (95% CI = 206–334) individuals, indicating that not all available habitat is presently occupied by bears in this region. Efficient management plans should focus on preserving connectivity of suitable habitats in order to maintain gene flow between the two Bulgarian brown bear subpopulations.     

Identifying the risk regions of house break‐ins caused by Tibetan brown bears (Ursus arctos pruinosus) in the Sanjiangyuan region,China

Damage to homesteads by brown bears (Ursus arctos) has become commonplace in Asia, Europe, and the Americas. Science‐based solutions for preventing damages can contribute to the establishment of mechanisms that promote human–bear coexistence. We examined the spatial distribution patterns of house break‐ins by Tibetan brown bears (U. a. pruinosus) in Zhiduo County of the Sanjiangyuan region in China. Occurrence points of bear damage were collected from field surveys completed from 2017 to 2019. The maximum entropy (MaxEnt) model was then used to assess house break‐in risk. Circuit theory modeling was used to simulate risk diffusion paths based on the risk map generated from our MaxEnt model. The results showed that (a) the total risk area of house break‐ins caused by brown bears was 11,577.91 km², accounting for 29.85% of Zhiduo County, with most of the risk areas were distributed in Sanjiangyuan National Park, accounting for 58.31% of the total risk area; (b) regions of alpine meadow located in Sanjiangyuan National Park with a high human population density were associated with higher risk; (c) risk diffusion paths extended southeast to northwest, connecting the inside of Sanjiangyuan National Park to its outside border; and (d) eastern Suojia, southern Zhahe, eastern Duocai, and southern Jiajiboluo had more risk diffusion paths than other areas examined, indicating higher risk for brown bear break‐ins in these areas. Risk diffusion paths will need strong conservation management to facilitate migration and gene flow of brown bears and to alleviate bear damage, and implementation of compensation schemes may be necessary in risk areas to offset financial burdens. Our analytical methods can be applied to conflict reduction efforts and wildlife conservation planning across the Qinghai–Tibet Plateau.     

Andean bear Tremarctos ornatus natural history and conservation

• 1 A wealth of information has been generated for the Andean bear Tremarctos ornatus during the past four decades, and a thorough review of the species' natural history, ecology and conservation is provided here.
• 2 The Andean bear is the only remaining bear species in South America. Evolutionarily, it is the youngest of all ursids and the only remnant taxon within the subfamily Tremarctinae. The species is distributed throughout the Andes mountain range from Venezuela to Bolivia, but the limits of its current and past range are uncertain.
• 3 The species is polyestrous, capable of delayed implantation and a facultative seasonal breeder. Genetic information is scarce, and species‐specific markers need to be developed for a more appropriate assessment of the genetic structure of wild populations.
• 4 Andean bears inhabit a wide variety of habitats across the Andes including different forest types and high‐elevation grasslands. They are omnivorous with a frugivorous/folivorous emphasis that is reflected by adaptations of the typical tremarctine mandible.
• 5 Andean bears are vulnerable to extinction due to land conversion and poaching. Efforts have been made to protect them, but threats have not been reduced significantly. Therefore, the species is expected to move faster towards extinction than any other carnivore in the region.

     

Are polar bear habitat resource selection functions developed from 1985–1995 data still useful?

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Sourcing Eurasian beaver Castor fiber stock for reintroductions in Great Britain and Western Europe

• 1 Eurasian beavers Castor fiber, formerly threatened with extinction, have been widely reintroduced since the 1920s. Reintroductions and studies of possible reintroductions are continuing.
• 2 The International Union for Conservation of Nature (IUCN) guidelines for reintroductions state that ‘the source population should ideally be closely related genetically to the original native stock’.
• 3 Palaeoecological studies suggest that the species survived the last Ice Age in two refugia: in the west in Iberia and Southern France and in the east in the Black Sea region. The post‐Ice Age population of Western Europe, including Great Britain, recolonized from the western refugium. Recent mitochondrial deoxyribonucleic acid studies strongly support this view, and extant beaver populations are clearly divided into eastern and western evolutionarily significant units (ESUs).
• 4 The western ESU is composed of three stocks which survived the 19th and early 20th century as very small, isolated populations. They are very closely related to each other. Each is genetically depauperate, apparently as a result of genetic drift at low population levels.
• 5 There is evidence of inbreeding depression and of phenotypic abnormalities in beaver populations descended from unmixed stocks.
• 6 The evidence suggests three coherent management options for sourcing reintroduction stock for Great Britain and for unoccupied areas of western continental Europe. These are (i) use animals from a single western ESU stock; (ii) intentionally mix animals from two or all three of the surviving western ESU stocks; (iii) make an informed exception to the IUCN guidelines and reintroduce animals of mixed eastern and western ESU provenance.
• 7 These options are discussed with regard to IUCN guidelines, conservation biology and animal welfare considerations. It would be advantageous if a common policy on the origin of reintroduction stock were agreed by the national agencies responsible.