Exceptional maternal lineage diversity in brown bears (Ursus arctos) from Turkey

The genetic diversity and phylogeography of maternal lineages in Ursus arctos Linnaeus, 1758 (the brown bear) have been studied extensively over the last two decades; however, sampling has largely been limited to the northern Holarctic, and was possibly biased towards lineages that recolonized the vast expanses of the north as the Last Glacial Maximum (LGM) ended. Here we report the genetic diversity and phylogeography of U. arctos from Turkey based on 35 non‐invasive samples, including five from captive individuals. Bayesian phylogenetic analyses based on a 269‐bp fragment of the mitochondrial DNA control region revealed 14 novel haplotypes belonging to three major lineages. The most widespread lineage was found to be the Eastern clade 3a, whereas geographically more restricted Western and Middle Eastern lineages were reported for the first time in Turkey. A specimen from the Taurus mountain range carried a haplotype closely related to the presumably extinct bears in Lebanon. Moreover, we identify a unique new lineage that appears to have split early within the Middle Eastern clade. Despite limited sampling, our study reveals a high level of mitochondrial diversity in Turkish U. arctos, shows that the ranges of both European and Middle Eastern clades extend into Turkey, and identifies a new divergent lineage of possibly wider historical occurrence. Obtaining these results with 35 samples also demonstrates the value of proper sampling from regions that have not been significantly affected by the LGM. © 2015 The Linnean Society of London     

Genetics and conservation of European brown bears Ursus arctos

• 1 We review the genetics research that has been conducted on the European brown bear Ursus arctos, one of the genetically best‐studied mammalian species.
• 2 The first genetics studies on European brown bears were on phylogeography, as a basis for proposed population augmentations. Two major mitochondrial DNA lineages, western and eastern, and two clades within the western lineage were found. This led to a hypothesis that brown bears had contracted to southern refugia during the last glacial maximum. More recent results suggest that gene flow among brown bears blurred this structure and they survived north of these putative refugia. Thus, today's structure might be a result of population fragmentation caused by humans.
• 3 The nuclear diversity of European brown bears is similar in range to that in North American bears: low levels occur in the small populations and high levels in the large populations.
• 4 Many non‐invasive genetic methods, developed during research on brown bears, have been used for individual identification, censusing populations, monitoring migration and gene flow, and testing methods that are easier to use in endangered populations and over large areas.
• 5 Genetics has been used to study many behavioural and population ecological questions that have relevance for the conservation and management of brown bears.
• 6 The European brown bear has served, and will continue to serve, as a model for the development of methods, analyses and hypotheses in conservation genetics.

     

Activity patterns of brown bears (Ursus arctos) in Slovenia and Croatia

In most of Europe, true wilderness areas do not exist and brown bears Ursus arctos generally have to cope with human disturbance and infrastructure. The few studies in Europe that have investigated brown bear activity have demonstrated a predominantly nocturnal and 'shy' behaviour in bears. There is still quite a debate on whether the shy, nocturnal bears of Europe are the result of centuries of persecution by men (genetically fixed trait) or whether hunting and the high disturbance potential in the multi-use landscapes are the driving force (individually learnt trait). We analysed the activity pattern of 16 individual bears monitored for 3372 h between May and October 1982–1998 in the Dinaric Mountains of Slovenia and Croatia. The data were collected via time sampling and basically analysed using two approaches: a general linear model with seasonal component to delineate the most important variables influencing the activity pattern and level and cluster analysis to group bears according to their 24-h activity pattern. Time of day and age were the most important variables predicting activity. Although individual variation in the activity pattern was high among individual bears, in general, yearlings were more diurnal and had a less distinct difference between day- and night-time activity levels than adult bears. Subadults were somewhat intermediate to adults and yearlings. We believe that nocturnal behaviour is most likely driven through negative experiences with humans, giving space for much individual variation. More research is needed to prove the causal relationship of nocturnal behaviour and the degree of disturbance that an individual bear is exposed to.     

Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis)

The aims of this study were to validate a radioimmunoassay (RIA) for quantifying glucocorticoid metabolite concentrations in the feces of Alaskan brown bears (Ursus arctos horribilis) and to investigate whether any of the following factors are associated with those concentrations: the presence of humans or other bears, fishing difficulty, sex-age class, diet, and season. We tested an established corticosterone RIA for assay sensitivity, similarity, precision, and sample matrix effects of brown bear feces, and it proved satisfactory. We collected fecal samples from brown bears along salmon-spawning streams and assessed fecal glucocorticoid (FG) concentrations. We observed that the factors explaining the most variation in measured concentrations were date and diet type and that there was a significant interaction between the two. We did not observe a significant effect of human and bear activities or sex-age class on FG concentrations. This study demonstrates that although FG concentrations may be assessed in brown bears, complex dietary patterns and seasonal variations must be taken into consideration in the study design in order to make inferences regarding stress.     

Use of Arctic ground squirrels (Urocitellus parryii) by brown bears (Ursus arctos)

Polar Biology - Brown bears (Ursus arctos) in the Mackenzie Delta in the Northwest Territories of Canada are at the northern edge of their range and persist in a nutrient poor environment with...     

Liver and kidney structure and iron content in romanian brown bears (Ursus arctos) before and after hibernation

The annual cycle of the brown bear (Ursus arctos) in the Carpathian Mountains (Romania) consists of an active period from April to November, and an inactive period (hibernation) of approximately 4-5 months between November and March. During hibernation, the brown bears sleep continually and do not feed or drink water. Analyses of liver and kidney of male brown bears showed that liver iron content was 3 times higher in bears at the end of hibernation than at the end of the active period. A possible trend towards a decrease in iron content was noted for the kidney. The presence of iron in the liver was confirmed by the presence of the Perls-positive granules in the cytoplasm of Kupffer cells, in other non-parenchymal cells and also in some hepatocytes. The hepatic veins of the bear liver samples obtained in early spring showed narrower lumens with pleated walls, compared to the normal outline of the hepatic veins in the liver from the bears sampled during autumn. Also in the early spring bears, the renal glomeruli were partially fibrosed. Renal glomerular fibrosis was sometimes observed in samples from the prehibernation period. The tissue iron values from the livers and kidneys of brown bears in early spring or autumn might provide useful data on iron metabolism under conditions of hibernation and accompanying starvation.     

Selection of rub trees by brown bears (Ursus arctos) in Hokkaido, Japan

Tree rubbing by brown bears (Ursus arctos) is a well-known behavior throughout the animal’s distribution. There is still insufficient information on the characteristics and function of the behavior. We investigated seasonal frequency of tree rubbing by brown bears, characteristics and reasons for selection of rub trees, and characteristics of bear signs on and around rub trees in a mixed coniferous–broad-leaved deciduous forest in Hokkaido, Japan. Between 1998 and 2009, we found 172 rub trees and confirmed 995 tree rubbings. We found that the rub trees were used repeatedly by bears within a year and for multiple years (more than 10 years). Tree rubbing by brown bears was observed from April to November, with a peak between May and June that corresponds to the mating season of brown bears. Abies sachalinensis was selected and broad-leaved trees were avoided for tree rubbing based on estimated availability in natural forest. The preference for Abies sachalinensis might be because the strong odor of resin attracts bears for rubbing their head and neck in resinous substances and for increasing the detectability of their markings by receptor bears. Selected trees for rubbing were located right beside the trail on relatively level ground among trees along roads or trails. Trees had a relatively large diameter at breast height. These characteristics would also serve to increase the access and detectability of their markings. Series of pad-shaped depressions was the most frequently observed (70 %) indication of bear rubbing, followed by debarking (51 %) and clawing (30 %). In terms of visual and olfactory signal amplification, physical damage by bears to the trees might have a function to enhance the smell as a result of increase in outflow of the resin. We conclude that tree rubbing behavior is associated with the mating season of brown bears and that the main purpose of this behavior is scent marking to communicate intraspecifically during the mating season.     

Capture, anesthesia, and disturbance of free-ranging brown bears (Ursus arctos) during hibernation

We conducted thirteen immobilizations of previously collared hibernating two- to four-year-old brown bears (Ursus arctos) weighing 21-66 kg in central Sweden in winter 2010 and 2011 for comparative physiology research. Here we report, for the first time, an effective protocol for the capture and anesthesia of free-ranging brown bears during hibernation and an assessment of the disturbance the captures caused. Bears were darted in anthill, soil, or uprooted tree dens on eleven occasions, but two bears in rock dens fled and were darted outside the den. We used medetomidine at 0.02-0.06 mg/kg and zolazepam-tiletamine at 0.9-2.8 mg/kg for anesthesia. In addition, ketamine at 1.5 mg/kg was hand-injected intramuscularly in four bears and in six it was included in the dart at 1.1-3.0 mg/kg. Once anesthetized, bears were removed from the dens. In nine bears, arterial blood samples were analyzed immediately with a portable blood gas analyzer. We corrected hypoxemia in seven bears (PaO(2) 57-74 mmHg) with supplemental oxygen. We placed the bears back into the dens and antagonized the effect of medetomidine with atipamezole. Capturing bears in the den significantly increased the risk of den abandonment. One of twelve collared bears that were captured remained at the original den until spring, and eleven, left their dens (mean ± standard deviation) 3.2±3.6 (range 0.5-10.5) days after capture. They used 1.9±0.9 intermediate resting sites, during 6.2±7.8 days before entering a new permanent den. The eleven new permanent dens were located 730±589 m from the original dens. We documented that it was feasible and safe to capture hibernating brown bears, although they behaved differently than black bears. When doing so, researchers should use 25% of the doses used for helicopter darting during the active period and should consider increased energetic costs associated with den abandonment.     

Genetic monitoring of a founder population of brown bears (Ursus arctos) in central Austria

The small population of brown bears in central Austria originated from a single migrant bear that had settled in the area in 1972 and three bears that were released in the years 1989–1993. Subsequently, the population has been monitored by radio-tracking and collecting data on bear signs and observations. In 2000 we started a genetic monitoring program of the population with the aim to obtain data on population size, sex ratio, relationships as well as movements of individuals. We present results from six years of genetic monitoring, which were combined with field observations. During this time 1,005 hair and faecal samples were gathered in an area of >3,000 km2, most of them in the core area of <1,000 km². Furthermore we analysed blood samples from captured individuals. Eight microsatellite and two sex determination loci were employed for DNA profiling. The number of detected individuals is surprisingly low, ranging from 5–8 per year. Concerning relationships the analysis reveals that all genotyped individuals are descendants of the founder individuals indicating that no immigration took place. Only one male and three females (mother and 2 daughters) took part in reproduction. Considering the fact that 28 bears were born in this region since 1991 the question arises where the bears disappear to. Our results suggest that subadult bears migrate from the core area. However, indices of bear occurrence outside the core area are rare and migration could be proved only for two young males. Other explanations, such as increased natural mortality and illegal hunting are discussed.     

Subadult brown bears (Ursus arctos) discriminate between unfamiliar adult male and female anal gland secretion

Olfactory cues have been investigated in social carnivores, many of which use anal/anogenital gland secretion (AGS) for scent marking. However, little is known about how solitary carnivores, such as ursids, use AGS in communication. We hypothesized that subadult (1–3 years) brown bears (Ursus arctos) have the ability to discriminate between unfamiliar adult male and female AGS. Confrontations, especially with adult males, carry high risks for dispersing subadults, so they benefit from the ability to assess potential threats based on olfactory cues, including sex, enabling them to avoid risky encounters. We presented AGS from free-ranging adult brown bears (male = 10, female = 10) to subadult brown bears (male = 13, female = 7) in outdoor zoo experiments, and predicted that subadults would avoid male more than female AGS. Neither male nor female AGS were avoided, but subadults quickly habituated to female AGS. However, male AGS was investigated more intensively and the subadults delayed revisiting it. Subadult tended to take longer to complete 6 visits to male than female AGS, which indicated sexual discrimination. We suggest that subadults that store information for the purpose of scent matching in future encounters may reduce their potential costs of conflict based on their prior assessment of the likely outcome of the encounter.     

The influence of diet on faecal DNA amplification and sex identification in brown bears (Ursus arctos)

To evaluate the influence of diet on faecal DNA amplification, 11 captive brown bears (Ursus arctos) were placed on six restricted diets: grass (Trifolium spp., Haplopappus hirtus and Poa pratensis), alfalfa (Lupinus spp.), carrots (Daucus spp.), white-tailed deer (Odocoileus virginianus), blueberries (Vaccinium spp.) and salmon (Salmo spp.). DNA was extracted from 50 faecal samples of each restricted diet, and amplification of brown bear DNA was attempted for a mitochondrial DNA (mtDNA) locus and nuclear DNA (nDNA) locus. For mtDNA, no significant differences were observed in amplification success rates across diets. For nDNA, amplification success rates for salmon diet extracts were significantly lower than all other diet extracts (P < 0.001). To evaluate the accuracy of faecal DNA sex identification when female carnivores consume male mammalian prey, female bears were fed male white-tailed deer. Four of 10 extracts amplified, and all extracts were incorrectly scored as male due to amplification of X and Y-chromosome fragments. The potential biases highlighted in this study have broad implications for researchers using faecal DNA for individual and sex identification, and should be evaluated in other species.     

Behaviour of solitary adult Scandinavian brown bears (Ursus arctos) when approached by humans on foot

Successful management has brought the Scandinavian brown bear (Ursus arctos L.) back from the brink of extinction, but as the population grows and expands the probability of bear-human encounters increases. More people express concerns about spending time in the forest, because of the possibility of encountering bears, and acceptance for the bear is decreasing. In this context, reliable information about the bear's normal behaviour during bear-human encounters is important. Here we describe the behaviour of brown bears when encountering humans on foot. During 2006-2009, we approached 30 adult (21 females, 9 males) GPS-collared bears 169 times during midday, using 1-minute positioning before, during and after the approach. Observer movements were registered with a handheld GPS. The approaches started 869±348 m from the bears, with the wind towards the bear when passing it at approximately 50 m. The bears were detected in 15% of the approaches, and none of the bears displayed any aggressive behaviour. Most bears (80%) left the initial site during the approach, going away from the observers, whereas some remained at the initial site after being approached (20%). Young bears left more often than older bears, possibly due to differences in experience, but the difference between ages decreased during the berry season compared to the pre-berry season. The flight initiation distance was longer for active bears (115±94 m) than passive bears (69±47 m), and was further affected by horizontal vegetation cover and the bear's age. Our findings show that bears try to avoid confrontations with humans on foot, and support the conclusions of earlier studies that the Scandinavian brown bear is normally not aggressive during encounters with humans.     

First report of Taenia arctos (Cestoda: Taeniidae) from grizzly (Ursus arctos horribilis) and black bears (Ursus americanus) in North America

The cestode Taenia arctos was found at necropsy in the small intestine of a grizzly (Ursus arctos horribilis) and a black bear (Ursus americanus) from Kananaskis Country in southwestern Alberta, Canada. The autolysis of the tapeworm specimens precluded detailed morphological characterization of the parasites but molecular analysis based on mitochondrial DNA cytochrome c oxidase subunit 1 gene confirmed their identity as T. arctos. This is the first report of T. arctos from definitive hosts in North America. Its detection in Canadian grizzly and black bears further supports the Holarctic distribution of this tapeworm species and its specificity for ursids as final hosts. Previously, T. arctos was unambiguously described at its adult stage in brown bears (Ursus arctos arctos) from Finland, and as larval stages in Eurasian elk (Alces alces) from Finland and moose (Alces americanus) from Alaska, USA. Given the morphological similarity between T. arctos and other Taenia species, the present study underlines the potential for misidentification of tapeworm taxa in previous parasitological reports from bears and moose across North America. The biogeographical history of both definitive and intermediate hosts in the Holarctic suggests an ancient interaction between U. arctos, Alces spp., and T. arctos, and a relatively recent host-switching event in U. americanus.     

Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem

We quantified the amount, spatial distribution, and importance of salmon (Oncorhynchus spp.)-derived nitrogen (N) by brown bears (Ursus arctos) on the Kenai Peninsula, Alaska. We tested and confirmed the hypothesis that the stable isotope signature (δ¹⁵N) of N in foliage of white spruce (Picea glauca) was inversely proportional to the distance from salmon-spawning streams (r=–0.99 and P<0.05 in two separate watersheds). Locations of radio-collared brown bears, relative to their distance from a stream, were highly correlated with δ¹⁵N depletion of foliage across the same gradient (r=–0.98 and –0.96 and P<0.05 in the same two separate watersheds). Mean rates of redistribution of salmon-derived N by adult female brown bears were 37.2±2.9 kg/year per bear (range 23.1–56.3), of which 96% (35.7±2.7 kg/year per bear) was excreted in urine, 3% (1.1±0.1 kg/year per bear) was excreted in feces, and <1% (0.3± 0.1 kg/year per bear) was retained in the body. On an area basis, salmon-N redistribution rates were as high as 5.1±0.7 mg/m² per year per bear within 500 m of the stream but dropped off greatly with increasing distance. We estimated that 15.5–17.8% of the total N in spruce foliage within 500 m of the stream was derived from salmon. Of that, bears had distributed 83–84%. Thus, brown bears can be an important vector of salmon-derived N into riparian ecosystems, but their effects are highly variable spatially and a function of bear density. Received: 11 February 1999 / Accepted: 7 July 1999     

A study of predominant aerobic microflora of black bears (Ursus americanus) and grizzly bears (Ursus arctos) in northwestern Alberta

Swab specimens were obtained from nasal, rectal, and preputial or vaginal areas of 37 grizzly and 17 black bears, captured during May to June of 1981 to 1983, to determine the types and frequency of predominant aerobic microflora. Bacterial genera most frequently isolated from bears were Escherichia, Citrobacter, Hafnia, Proteus, Staphylococcus, and Streptococcus species, comprising about 65% of the isolates. Erwinia, Xanthomonas, Agrobacterium, Rhizobium, and Gluconobacter/Acetobacter were also isolated but at lower frequencies (less than 5%). Comparison of bacterial generic composition using similarity quotient values showed no appreciable differences between grizzly and black bear flora. Also, no outstanding differences in bacterial generic composition were observed among grizzly bear samples; however, differences were noted among black bear samples. Fungal genera most commonly encountered included Cryptococcus, Rhodotorula, Cladosporium, Penicillium, Sporobolomyces, and Candida. In general, the microflora of both bear types were marked by generic diversity and random distribution. The majority of microorganisms isolated from the plant samples in the study area were also found in bear samples. This observation and the presence of certain water and soil bacteria in samples from bears suggest that the predominant microflora of both grizzly and black bears were transient and probably influenced by their foraging habits and surrounding environments.     

Cardiac function adaptations in hibernating grizzly bears (Ursus arctos horribilis)

Research on the cardiovascular physiology of hibernating mammals may provide insight into evolutionary adaptations; however, anesthesia used to handle wild animals may affect the cardiovascular parameters of interest. To overcome these potential biases, we investigated the functional cardiac phenotype of the hibernating grizzly bear (Ursus arctos horribilis) during the active, transitional and hibernating phases over a 4 year period in conscious rather than anesthetized bears. The bears were captive born and serially studied from the age of 5 months to 4 years. Heart rate was significantly different from active (82.6 ± 7.7 beats/min) to hibernating states (17.8 ± 2.8 beats/min). There was no difference from the active to the hibernating state in diastolic and stroke volume parameters or in left atrial area. Left ventricular volume:mass was significantly increased during hibernation indicating decreased ventricular mass. Ejection fraction of the left ventricle was not different between active and hibernating states. In contrast, total left atrial emptying fraction was significantly reduced during hibernation (17.8 ± 2.8%) as compared to the active state (40.8 ± 1.9%). Reduced atrial chamber function was also supported by reduced atrial contraction blood flow velocities and atrial contraction ejection fraction during hibernation; 7.1 ± 2.8% as compared to 20.7 ± 3% during the active state. Changes in the diastolic cardiac filling cycle, especially atrial chamber contribution to ventricular filling, appear to be the most prominent macroscopic functional change during hibernation. Thus, we propose that these changes in atrial chamber function constitute a major adaptation during hibernation which allows the myocardium to conserve energy, avoid chamber dilation and remain healthy during a period of extremely low heart rates. These findings will aid in rational approaches to identifying underlying molecular mechanisms.     

Comparison of the behaviour of European brown bears (Ursus arctos arctos) in six different parks, with particular attention to stereotypies

In order to assess the influence of environmental parameters on their behaviour, 16 European brown bears were observed in six different zoological parks. Activities were measured by scan sampling and their relationships to housing conditions were established by multifactorial correspondence analysis and cluster analysis. The largest enclosures were characterised by high scores of play, social behaviours, eating, and interest in the inside as well as the outside of the enclosure. Because these parks were newer, their bears were the youngest of those studied. Stereotypies were associated with medium age animals and small enclosures. The oldest subjects were characterised by high frequencies of resting. Stereotyped walk was observed only in those parks where keepers throw food to the bears. This result and detailed observation of stereotyped movements suggest that the meaning of the stereotypy for the animal could be to induce the keeper's arrival.