Natural rewilding of the Great Basin: Genetic consequences of recolonization by black bears (Ursus americanus)

Aim

In the mid‐20th century, many populations of large‐bodied mammals experienced declines throughout North America. Fortunately, within the last several decades, some have begun to rebound and even recolonize extirpated portions of their native range, including black bears (Ursus americanus) in the montane areas of the western Great Basin. In this study, we examine genetic variation in source and recolonized areas to better understand the genetic consequences of recolonization.

Location

Western Great Basin, USA.

Methods

Using multiple loci, we characterized genetic variation among source and recently recolonized areas occupied by black bears, tested for population structure and applied approximate Bayesian computation to test competing hypotheses of demographic history. We assessed signals of gene flow using expectations of genetic consequences derived from alternative modes of recolonization (bottleneck, metapopulation, island model) and tested for significant signals of genetic bottlenecks in areas recently recolonized by black bears.

Results

As anticipated from field survey data and hypothesized expectations, genetic variation of western Great Basin black bears retain an overall signature of demographic decline followed by recent rebound. Furthermore, results reveal that bears in the recolonized range are minimally differentiated from the source area, but newly established subpopulations have lower effective population sizes and reduced allelic diversity. Nevertheless, recolonized areas fail to show a significant signal of a genetic bottleneck. Moreover, bears occupying recolonized areas experience asymmetric gene flow, yielding strong support for a model of genetic connectivity that is best described as a metapopulation.

Main Conclusion

This study presents one of the few empirical examples of genetic consequences of natural recolonization in large‐bodied mammals. Furthermore, these results have implications for understanding the complexities associated with the genetic consequences of recent and ongoing recolonization and highlight the need to develop management strategies uniquely tailored to support connectivity between source and recolonized areas.

     

Prevalence of sarcocysts in Florida black bears (Ursus americanus floridanus)

Sections of muscle from Florida black bears (Ursus americanus floridanus) collected in the state of Florida were observed for the presence of Sarcocystis sp. sarcocysts. Two of 132 (1.5%) black bears had muscle sections containing sarcocysts. One sarcocyst was observed per muscle section. The sarcocysts averaged 181.5 x 99.0 microm by light microscopy of hematoxylin and eosin-stained sections.     

Activity patterns of Asiatic black bears (Ursus thibetanus) in the Central Mountains of Taiwan

Shifts in activity patterns and time budgets in response to environmental variables may yield insights into key factors affecting animal life histories. Activity data on wild Asiatic black bears Ursus thibetanus are limited, and non-existent in tropical portions of their geographic range. During November 1998–November 2000, we monitored the activity (active vs. inactive) of bears within a national park in the tropics of central Taiwan. On the basis of 4630 readings from motion-sensitive transmitters obtained in 24-h monitoring sessions, bears were active 54–57% of the time over the course of the year. However, bears were more active during summer (60±15% sd ) and fall (60±15%) than in spring (47±13%). They were active mainly during daylight hours in spring and summer, and also during fall when acorns, a principal fall food, were scarce. However, extensive nocturnal activity occurred in fall when acorns were abundant. Increased nocturnal activity in fall is consistent with studies of the related American black bear Ursus americanus , and suggests that this behavior is not necessarily driven by preparation for winter denning or because of disturbance by hunters (as posited in previous studies), as bears in our study did not den (except parturient females) and were not hunted or otherwise disturbed by people.     

Tetranucleotide microsatellite loci from the black bear (Ursus americanus)

We describe primers and polymerase chain reaction conditions to amplify 21 tetranucleotide microsatellite DNA loci in black bears (Ursus americanus). We tested primers using individuals from two populations, one each in Georgia and Florida. Among individuals from Georgia (n = 29), primer pairs yielded an average of 2.9 alleles (range, one to four) and an average observed heterozygosity (H_O) of 0.50 (range, 0.00 to 0.79). Among individuals from Florida (n = 19), primer pairs yielded an average of 5.7 alleles (range, one to 14) and an H_O of 0.55 (range, 0.00 to 1.00). A comparison of previously developed markers with individuals from Georgia suggests that bear populations in Georgia and Florida have reduced allelic diversity relative to other populations.     

Social structure and facultative mating systems of hoary marmots (Marmota caligata)

Mate-choice theory predicts different optimal mating systems depending on resource availability and habitat stability. Regions with limited resources are thought to promote monogamy. We tested predictions of monogamy in a social rodent, the hoary marmot (Marmota caligata), at the northern climatic extreme of its distribution. Mating systems, social structure and genetic relationships were investigated within and among neighbouring colonies of marmots within a 4 km(2) valley near Kluane National Park, Yukon, Canada, using 21 microsatellite loci. While both monogamous and polygynous populations of hoary marmots have been observed in the southern reaches of this species' range; northern populations of this species are thought to be predominantly monogamous. Contrary to previous studies, we did not find northern hoary marmot social groups to be predominantly monogamous; rather, the mating system seemed to be facultative, varying between monogamy and polygyny within, as well as among, social groups. These findings reveal that the mating systems within colonies of this species are more flexible than previously thought, potentially reflecting local variation in resource availability.     

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.     

Negative density-dependent dispersal in the American black bear (Ursus americanus) revealed by noninvasive sampling and genotyping

Although the dispersal of animals is influenced by a variety of factors, few studies have used a condition-dependent approach to assess it. The mechanisms underlying dispersal are thus poorly known in many species, especially in large mammals. We used 10 microsatellite loci to examine population density effects on sex-specific dispersal behavior in the American black bear, Ursus americanus. We tested whether dispersal increases with population density in both sexes. Fine-scale genetic structure was investigated in each of four sampling areas using Mantel tests and spatial autocorrelation analyses. Our results revealed male-biased dispersal pattern in low-density areas. As population density increased, females appeared to exhibit philopatry at smaller scales. Fine-scale genetic structure for males at higher densities may indicate reduced dispersal distances and delayed dispersal by subadults.     

Seroprevalence of Toxoplasma gondii from free-ranging black bears ( Ursus americanus ) from Florida

Toxoplasma gondii is a significant worldwide parasitic protozoan. In the present study, prevalence of antibodies of T. gondii was examined from 29 free-ranging black bears ( Ursus americanus ) from south-central Florida where the host species was listed as state threatened during this project. Overall T. gondii prevalence was found to be 44.8%, specifically 46.2% in male and 43.8% in female U. americanus , using a modified agglutination test (1:25 titer). Seroprevalence differences between sexes were not significant (P > 0.05). Results of the present study add supportive data to the growing body of evidence suggesting that U. americanus has one of the highest T. gondii seroprevalences among all known intermediate hosts. In addition, our data emphasize the importance of understanding parasitic disease dynamics from a conservation perspective.     

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.     

Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears

The adaptation of black and polar bears to their environments is proportional to the severity of climate and food restriction. Both black and polar bears mate during the spring, despite differences in their recent metabolic state. Reproductive activity in black bears follows 4 mo of torpor, whereas reproduction in polar bears occurs prior to torpor. The goals of this study were to measure the annual changes in serum sex steroids in male and female black and polar bears, and to determine if changes in serum levels of these steroids were associated with metabolic condition or photoperiod. Serum testosterone (T) concentrations were elevated during spring in black and polar bears. Moreover, this increase in serum T in polar bears during spring was correlated with age and testis size. Serum progesterone (P4) concentrations increased in pregnant polar bears in fall coincident with the time of expected implantation. No increases in serum P4 were observed in nonpregnant black and polar bears. Serum estradiol (E2) was elevated in nonpregnant and pregnant polar bears 2 mo prior to the time of expected implantation. We found that serum sex steroids measured in black and polar bears change independent of torpor. Therefore, our results suggest that photoperiod may be a more important regulator of serum steroid levels and reproduction than metabolic condition.     

Hibernating black bears (Ursus americanus) experience skeletal muscle protein balance during winter anorexia

Black bears spend four to seven months every winter confined to their den and anorexic. Despite potential for skeletal muscle atrophy and protein loss, bears appear to retain muscle integrity throughout winter dormancy. Other authors have suggested that bears are capable of net protein anabolism during this time. The present study was performed to test this hypothesis by directly measuring skeletal muscle protein metabolism during the summer, as well as early and late hibernation periods. Muscle biopsies were taken from the vastus lateralis of six free-ranging bears in the summer, and from six others early in hibernation and again in late winter. Protein synthesis and breakdown were measured on biopsies using (14)C-phenylalanine as a tracer. Muscle protein, nitrogen, and nucleic acid content, as well as nitrogen stable isotope enrichment, were also measured. Protein synthesis was greater than breakdown in summer bears, suggesting that they accumulate muscle protein during periods of seasonal food availability. Protein synthesis and breakdown were both lower in winter compared to summer but were equal during both early and late denning, indicating that bears are in protein balance during hibernation. Protein and nitrogen content, nucleic acid, and stable isotope enrichment measurements of the biopsies support this conclusion.     

Unraveling the mystery of the glacier bear: Genetic population structure of black bears (Ursus americanus) within the range of a rare pelage type

Glacier bears are a rare grey color morph of American black bear (Ursus americanus) found only in northern Southeast Alaska and a small portion of western Canada. We examine contemporary genetic population structure of black bears within the geographic extent of glacier bears and explore how this structure relates to pelage color and landscape features of a recently glaciated and highly fragmented landscape. We used existing radiocollar data to quantify black bear home‐range size within the geographic range of glacier bears. The mean home‐range size of female black bears in the study area was 13 km² (n = 11), whereas the home range of a single male was 86.9 km². We genotyped 284 bears using 21 microsatellites extracted from noninvasively collected hair as well as tissue samples from harvested bears. We found ten populations of black bears in the study area, including several new populations not previously identified, divided largely by geographic features such as glaciers and marine fjords. Glacier bears were assigned to four populations found on the north and east side of Lynn Canal and the north and west side of Glacier Bay with a curious absence in the nonglaciated peninsula between. Lack of genetic relatedness and geographic continuity between black bear populations containing glacier bears suggest a possible unsampled population or an association with ice fields. Further investigation is needed to determine the genetic basis and the adaptive and evolutionary significance of the glacier bear color morph to help focus black bear conservation management to maximize and preserve genetic diversity.     

Serologic evidence of West Nile virus infection in black bears (Ursus americanus) from New Jersey

Serum samples obtained from 51 free-ranging black bears (Ursus americanus) in northwestern New Jersey in February and March 2002 were analyzed for neutralizing antibodies to West Nile virus (WNV) and St. Louis encephalitis virus. Three (6%) of the black bears tested positive for WNV-neutralizing antibodies. One additional sample was positive for flavivirus-neutralizing antibodies but could not be differentiated for a specific virus type. This is the first report of WNV infection in black bears.     

Dietary adjustability of grizzly bears and American black bears in Yellowstone National Park

Grizzly bears (Ursus arctos) and American black bears (U. americanus) are sympatric in much of Yellowstone National Park. Three primary bear foods, cutthroat trout (Oncorhynchus clarki), whitebark pine (Pinus albicaulis) nuts, and elk (Cervus elaphus), have declined in recent years. Because park managers and the public are concerned about the impact created by reductions in these foods, we quantified bear diets to determine how bears living near Yellowstone Lake are adjusting. We estimated diets using: 1) stable isotope and mercury analyses of hair samples collected from captured bears and from hair collection sites established along cutthroat trout spawning streams and 2) visits to recent locations occupied by bears wearing Global Positioning System collars to identify signs of feeding behavior and to collect scats for macroscopic identification of residues. Approximately 45 ± 22% ( ± SD) of the assimilated nitrogen consumed by male grizzly bears, 38 ± 20% by female grizzly bears, and 23 ± 7% by male and female black bears came from animal matter. These assimilated dietary proportions for female grizzly bears were the same as 10 years earlier in the Lake area and 30 years earlier in the Greater Yellowstone Ecosystem. However, the proportion of meat in the assimilated diet of male grizzly bears decreased over both time frames. The estimated biomass of cutthroat trout consumed by grizzly bears and black bears declined 70% and 95%, respectively, in the decade between 1997–2000 and 2007–2009. Grizzly bears killed an elk calf every 4.3 ± 2.7 days and black bears every 8.0 ± 4.0 days during June. Elk accounted for 84% of all ungulates consumed by both bear species. Whitebark pine nuts continue to be a primary food source for both grizzly bears and black bears when abundant, but are replaced by false-truffles (Rhizopogon spp.) in the diets of female grizzly bears and black bears when nut crops are minimal. Thus, both grizzly bears and black bears continue to adjust to changing resources, with larger grizzly bears continuing to occupy a more carnivorous niche than the smaller, more herbivorous black bear. © 2012 The Wildlife Society.     

Prevalence of Trichinella spiralis in black bears (Ursus americanus) from Newfoundland and Labrador, Canada.

Tongue and diaphragm samples from 158 black bears (Ursus americanus) from Newfoundland and Labrador were examined for Trichinella spiralis. No larvae were detected in samples from the island of Newfoundland but one animal from the Labrador samples was infected. The results of this and other studies suggest a lack of involvement of the black bear in a sylvatic cycle of T. spiralis in eastern Canada.     

Use of Ketamine hydrochloride and xylazine hydrochloride to immobilize black bears (Ursus americanus).

Ketamine hydrochloride (KH) and xylazine hydrochloride (XH) used in combination (KH-XH) were effective immobilants for captive and wild black bears (Ursus americanus). Single intramuscular injections of 1.5-17.1 mg of KH per kg body weight combined in an approximate ratio of 2:1 with 0.9-10.0 mg of XH per kg body weight immobilized bears for 1.5-197 min. Dosages most frequently used were 4.5-9 mg KH/kg with 2-4.5 mg XH kg. Supplemental administrations maintained tractability for up to 31 h. Immobilization was characterized by smooth induction, relaxed muscles, occasional groaning and vomition, no eye closure, no defecation, and a smooth recovery phase of variable length. Male and female bears responded similarly to KH-XH. Induction times for small bears (less than or equal to 25 kg) were shorter than for larger bears.     

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.