The Journal of Heredity 2001:92(3)
© 2001 The American Genetic Association 92:226-233
Subspecific Affinity of Black Bears in the White River National Wildlife Refuge
From the Department of Fisheries and Wildlife Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA. J. Warrillow is currently at the Department of Fisheries and Wildlife, Michigan State University, East Lansing, Michigan. M. Vaughan is currently at the USGS/BRD—Virginia Cooperative Fish and Wildlife Research Unit, Virginia Polytechnic Institute and State University, Blacksburg, Virginia.
Address correspondence to Melanie Culver at the address above or e-mail: culver{at}vt.edu.
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Abstract |
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The black bear population of the White River National Wildlife Refuge (NWR) is adjacent to populations of black bear in Louisiana (Urusus americanus luteolus) which are listed as threatened under the U.S. Endangered Species Act. Wildlife management plans can pose restrictions on bear harvests and timber extraction; therefore the management plan for the White River NWR is sensitive to subspecific classification of its bear population. The objective of this study was to analyze genetic variation in the White River NWR and seven adjacent populations of black bears to assess the subspecific affinity of the White River NWR population. Here we report the variation at seven microsatellite DNA loci among eight black bear populations. The patterns of genetic variation gave strong support for distinguishing a southern group of black bears comprised of the White River, Arkansas; Tensas River, Louisiana; Upper Atchafalaya, Louisiana; Lower Atchafalaya, Louisiana; and Alabama/Mississippi populations. Phylogenetic analysis of individual variation suggested that historical black bear introductions into Arkansas and Louisiana affected gene pools of certain southern receiving populations, but did not significantly change interpopulation relatedness. Phylogenetic inferences at both the population and individual levels support the hypothesis that the White River NWR population of black bears belongs to the U. a. luteolus subspecies.
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Introduction |
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The black bear (Ursus americanus) is comprised of 16 subspecies, including the American black bear (U. a. americanus) distributed throughout most of eastern North America, the Louisiana black bear (U. a. luteolus) in Louisiana and adjacent areas (Hall 1981), and the Florida black bear (U. a. floridanus) in Florida and adjacent areas. The Louisiana black bear was listed as threatened under the U.S. Endangered Species Act (ESA) in 1992. In December 1998, the U.S. Fish and Wildlife Service concluded in a final ruling that listing for the Florida black bear was not warranted under the ESA.
Although black bears once ranged throughout most of North America (Vaughan and Pelton 1995), recent fragmentation has isolated many populations, such as the White River National Wildlife Refuge (NWR) population in Arkansas. Genetic characterization of the bear population's subspecific affinity is important with regard to formulating the management plan for the refuge because the two subspecies in question (U. a. americanus and U. a. luteolus) differ in terms of ESA Protection. This is particularly important with regard to harvest regulations, and also poses possible restrictions on timber extraction and on a river channelization proposal in areas adjacent to the White River NWR. Currently the subspecific affinity of the White River NWR black bear population is unclear. In a general synthesis of mammalian distribution and systematics, Hall (1981) classified the White River NWR population as U. a. americanus. Using DNA fingerprinting techniques to characterize variation of nuclear DNA, Miller (1995) tentatively concluded that the White River NWR population exhibited greater affinity to U. a. luteolus than to U. a. americanus. However, that study did not focus on the White River NWR population, and did not include all population-by-population comparisons relevant for reaching a firm conclusion regarding its subspecific classification. Kennedy et al. (1996) concluded that the White River NWR population belonged to U. a. americanus, based on morphometric comparisons on a small number of skulls (n = 6). Other black bear population genetic and phylogeographic studies, using either mitochondrial control region sequence (Wooding and Ward 1997) or microsatellite DNA markers (Paetkau and Strobeck 1994), did not include black bear samples from the southeastern United States (although Wooding and Ward included a single individual from Florida out of 258 total black bears).
Development of the management plan for the White River NWR and planning of economic activities adjacent to the refuge are sensitive to the subspecies classification of its black bear population. Hence the objective of this study was to analyze genetic variation in White River NWR and adjacent populations of black bears to assess the classification of the White River NWR population based on genetic evidence. The recent development of microsatellite DNA markers for bears (Paetkau et al. 1995; Paetkau and Strobeck 1994) offers the opportunity to screen allelic variation at particular genetic loci and to analyze departures from Hardy–Weinberg expectations. Here we report the results of analyses of allelic variation at seven microsatellite loci among eight populations of black bear.
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Materials and Methods |
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DNA Purification
Samples of blood or other tissues were collected from 151 individuals representing eight black bear populations (Figure 1). Sampling included three populations of the American black bear (U. a. americanus): Ouachita National Forest, Arkansas (OU); Ozark National Forest, Arkansas (OZ); and Cook County, Minnesota (CC). The Cook County population was sampled because it represents the source population for many historic translocations into the other populations in this study. Individuals from Mobile River, Alabama (n = 11) and Red Creek Wildlife Management Area (WMA), Mississippi (n = 2) were taken as representing the Florida subspecies of black bear (U. a. floridanus) (AL). These populations are separated by only 60 km, although the Red Creek WMA falls within Hall's (1981) view of the range of nominal U. a. luteolus (see results below regarding individual phylogeny). Three populations of the Louisiana black bear (U. a. luteolus) included the Lower Atchafalaya River Basin, Louisiana (LA); Upper Atchafalaya River Basin, Louisiana (UA); and Tensas River NWR, Louisiana (TR). The White River NWR population (WR), the subspecific affinity of which is uncertain, also was sampled. DNA was purified from blood or other tissues following a proteinase-K digestion and phenol-chloroform extraction protocol (Miller 1995). DNA samples were frozen at -20°C in 1x TE buffer.
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Microsatellite Markers
Dinucleotide microsatellite repeats of genomic DNA were amplified by the polymerase chain reaction (PCR) using seven primer pairs. Primer pair sequences were obtained from Paetkau et al. (1995) and Paetkau and Strobeck (1994). Primer pairs were custom-produced by Operon Technologies (Alameda, CA) or IDT (Coralville, IA). Primer sequences, PCR conditions, and reagents were used as described in Paetkau and Strobeck (1994). Amplification was performed using the following cycling conditions: 2 min at 94°C; 30 cycles of 15 s at 94°C, 30 s at 55°C, and 15 s at 72°C; and 5 min at 72°C. After amplification, the PCR products were subjected to electrophoresis through a 7% native TBE polyacrylamide gel (Hoefer SE 600 gel apparatus, Amersham Pharmacia Biotech, San Francisco, CA) and visualized by silver staining (Naish KA, personal communication). Amplification product sizes were estimated using a 10 bp molecular weight ladder (GibcoBRL, Life Technologies). Allele size estimates were not regarded as exact, but were standardized between gels by running samples of known genotypes on every gel, after every second or third test sample. All primers produced light "shadow bands" (Hauge and Litt 1993) approximately 8 bp larger than the alleles. Homozygotes were distinguished by noting only one shadow band in the target area.
Genetic Diversity and Population Structure
Measures of genetic diversity were estimated at the individual level, as well as within and between populations. Average expected heterozygosity, average number of alleles, total number of alleles, number of unique alleles, average variance in number of repeats, and average range in number of repeats were estimated from microsatellite data using the program MICROSAT (version 1.5; Minch et al. 1999). Deviations from Hardy–Weinberg equilibrium (Guo and Thompson 1992) were tested for each microsatellite locus using the Arlequin program (version 1.1; Schneider et al. 1997). The degree of population differentiation among the eight populations was estimated using analysis of fixation indices. Two estimators, FST (number of different alleles; Michalakis and Excoffier 1996; Reynolds et al. 1983; Weir and Cockerham 1984) and RST (sum of squared size differences; Slatkin 1995), for microsatellite data, as implemented in the Arlequin program (version 1.1; Schneider et al. 1997), were used to quantify population subdivision (Table 1). The significance levels of FST were assessed after employing a Bonferroni adjustment (Weir 1996) for multiple comparisons. An analysis of molecular variance (AMOVA) for detecting subdivision (Excoffier et al. 1992) was performed among populations and within groupings of populations, using both FST and RST, for two grouping strategies: (1) with two groups comprised of the southern group (Upper Atchafalaya, Lower Atchafalaya, White River, Tensas River, Alabama/Mississippi) and the northern group (Cook County, Ouachita, Ozark); and (2) with three groups comprised of Alabama/Mississippi, the rest of the southern group (Upper Atchafalaya, Lower Atchafalaya, White River, Tensas River), and the northern group (Cook County, Ouachita, Ozark). Significant differences among populations for the average number of alleles per locus were assessed using analysis of variance (ANOVA), and grouped using the LSD multiple comparison procedure. Significant differences among observed average heterozygosities were tested using GENMOD, and significant pairs were found using the CONTRAST procedure in SAS version 6.12 (SAS Institute Inc., Cary, NC). In addition, the Assignment Calculator program (Brzustowski 2000) was used to determine the frequencies at which an individual's composite genotype could be used to successfully assign individuals to the population from which they were actually sampled (Paetkau et al. 1995, 1997). When an allele was missing from a population, instead of zero, a frequency of 0.01 was selected, 1000 randomized runs were performed; and randomization was accomplished by shuffling alleles at each locus within populations with no replacement.
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Phylogenetic Analyses
The MICROSAT program (version 1.5; Minch et al. 1999) was employed to estimate pairwise genetic distances both among individuals and populations using the kinship coefficient (Dkf) and proportion of shared alleles (Dps; Bowcock et al. 1994) metrics; these metrics previously have been used to study several felid species (Culver et al. 2000; Johnson et al. 1999). Dkf and Dps both measure the proportion of shared alleles between individuals or populations, but Dps weights shared, rare alleles, whereas Dkf is sensitive to frequencies of shared alleles. In addition, Nei's standard distance metric (GST; Nei 1987) was used to quantify re-[fj latedness among populations, as has previously been applied to populations of canids (Garcia-Moreno et al. 1996; Roy et al. 1994) and wombat (Taylor et al. 1994). The nomenclature of GST, used by the MICROSAT program, refers to Nei's identity, and as used here is equivalent to Nei's standard genetic distance. In this study, genetic distance among populations and individuals was estimated using several metrics (Dkf, Dps, and GST), each with a particular strength. Rather than attempt to select one best metric, we chose to examine the variety of metrics and look for agreement among all results. The phylogenetic analysis of individuals was performed using data both for all individuals (n = 151) and for only individuals whose DNA supported amplification for six or more loci (n = 145). Phylogenetic trees were constructed from the Dkf, Dps, and GST distance matrices using the NEIGHBOR option of the program PHYLIP (version 3.5c; Felsenstein 1993). The data were entered into NEIGHBOR both sequentially from the data file and also in randomized order. Phylogenetic trees were drawn using the program TREEVIEW (version 1.5; Page 1998).
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Results |
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Diversity Measures
Seventy-one alleles were observed at seven microsatellite loci (Table 2). The degree of variation ranged from 8 to 14 alleles per locus, with an average of 5.6 alleles per population at each locus. Allele frequencies were different among the eight populations. Cook County and Ouachita black bear populations exhibited a more even distribution of allele frequencies, with maximum frequencies of 0.45 and 0.50, respectively, while the other populations showed some allele frequencies in the 0.61 to 1.00 range. Overall the Cook County population exhibited the greatest amount of genetic diversity relative to the other populations, quantified in terms of the average number of alleles per locus (8.71 versus a range of 2.43–6.14, P < .0001) (Table 3), total number of alleles (36 versus 14–32), number of unique alleles (4 versus 0–2), and average range in number of repeats (9.43 versus 4.14–8.00) (Table 4). The White River and Alabama/Mississippi populations consistently exhibited relatively low genetic variation at all seven microsatellite loci (Tables 3 and 4), notably in terms of the low average number of alleles (P < .0001). Observed average heterozygosities were statistically higher for the Cook County population (H = 0.54) relative to three southern populations (Alabama/Mississippi, Lower Atchafalaya, and White River, H = 0.38–0.42) (P < .0167, P < .0153, and P < .0022, respectively).
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Population-Level Relatedness and Phylogeny
Phylogenetic relationships were inferred from pairwise genetic distances using Dkf, Dps (Bowcock et al. 1994), and GST (Nei 1987) distance measures. All metrics produced similar distance matrices, therefore only those for Dkf and Dps are shown (Table 5). The greatest genetic distance estimate, for all distance metrics, was observed between two southern popula-[fj tions, Alabama/Mississippi and White River (Dkf = 0.44, Dps = 0.71, GST = 0.67), that is, between populations of nominally different subspecies. Otherwise the greatest distances occurred between populations representing the U. a. americanus and U. a. luteolus subspecies. The smallest genetic distances were observed between Cook County and Ouachita (Dkf = 0.04, GST = 0.00), or White River and Tensas River (Dps = 0.30) populations. Generally, smaller genetic distance values were observed among populations of the same subspecies.
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Phylogenetic associations among populations were inferred by the minimum evolution method as estimated by the Neighbor-Joining (NJ) algorithm (Felsenstein 1993) using Dkf, Dps, and GST distances. Bootstrap (BS) values of 70% or greater were regarded as significant; a 70% BS value corresponds to a probability of
95% that the corresponding clade is real (Hillis and Bull 1993). All three distance measures resulted in construction of trees with similar topologies, with the GST and Dps trees identical; therefore only the Dkf and Dps trees are shown (Figure 2). All trees showed strong support for associations between the Tensas River and White River populations (BS values: Dkf = 100, Dps = 99, GST = 100), and between the Upper Atchafalaya and Lower Atchafalaya populations (BS values: Dkf = 93, Dps = 77, GST = 88). Two of the trees (Dps and GST) also gave strong support for a genetically distinct southern group comprised of the White River, Tensas River, Upper Atchafalaya, Lower Atchafalaya, and Alabama/Mississippi populations (BS = 98 and 71, respectively). The Dkf tree gave weak support for the association of these 5 southern populations. The Ozark and Ouachita populations were significantly grouped in the Dps and GST trees (BS = 87 and 71, respectively). For all three trees (Dkf, Dps, and GST), there was a relationship, although weak, of the Cook County population with the Ozark/Ouachita group (BS values: Dkf = 59, Dps = 45 and GST = 40), and the position of the Alabama population was uncertain within the southern group (BS values: Dkf = 36, Dps = 47, GST = 47). The structure of the trees was identical, as were significant bootstrap values, when the data were reentered using randomized input order.
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Population Structure
Allele frequencies within the seven southern populations did not differ significantly (P > .05) from those expected under Hardy–Weinberg equilibrium. However, the Cook County population was not in Hardy–Weinberg equilibrium (P < .05).
Most pairwise comparisons using the FST and RST statistics reflected significant genetic differentiation (P < .002, following Bonferroni correction) among populations (Table 1). However, differences between Ouachita and Ozark, Ouachita and Upper Atchafalaya, and Ouachita and Cook County were not significant (P > .002) with either estimator. Ten additional comparisons were not significantly different (P > .002) using the RST estimator, particularly those involving the Ouachita population. Those pairwise comparisons that were significantly different from RST included all comparisons involving Alabama/Mississippi, all comparisons between Cook County and members of the southern group, and all comparisons between Ozark and the southern group (with the previously mentioned exception of Ozark and Upper Atchafalaya).
A hierarchical analysis of populations (AMOVA) within and between the two groups (northern and southern) consistently found significant subdivision among populations (19.8% of variation, P = .00 for FST; 7.7% of variation, P = .00 for RST) but not among groups of populations (2.7% of variation, P = .12 for FST; 8.2% of variation, P = .02 for RST). However, when the Alabama/Mississippi population was removed from the southern group and considered separately, the subsequent three-group AMOVA (northern, southern, and Alabama/Mississippi) found significant subdivision both among populations (P = .00 for FST and RST) and among groups of populations (P = .03 for FST and P = .00 for RST), with a smaller percent of variation among populations (15.1% for FST and 5.1% for RST) and a larger percent among groups of populations (8.9% for FST and 10.8% for RST).
The Assignment Calculator program (Brzustowski 2000), correctly assigned 118 of 151 individuals (78%) to their population of origin, 11 (7%) were assigned to the closest neighboring population, and 22 (15%) were assigned incorrectly (Table 6). The closely neighboring populations were Upper Atchafalaya and Lower Atchafalaya, White River and Tensas River, and Ouachita and Ozark. Alabama/Mississippi and Cook County were not considered to have a close neighboring population. Four populations had >91% correct assignment rates: Alabama/Mississippi (100%), White River (95%), Tensas River (93%), and Lower Atchafalaya (92%). None of the six Ouachita bears were correctly assigned and three of them were assigned to the Cook County population.
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Individual-Level Phylogeny
Each black bear exhibited a unique composite genotype using seven microsatellite markers. Removing data for individuals lacking genotypes at two or more loci (n = 145) did not change the relationships among individuals; therefore only analyses using all individuals (n = 151) will be presented. Phylogenetic patterns were examined considering each individual as a taxonomic unit. Both genetic distance measures relevant for comparing individual genotypes, Dkf and Dps (Bowcock et al. 1994), resulted in construction of "correct" trees in which samples from the same geographic area tended to cluster together, although not surprisingly, with little bootstrap support (Figure 3). Because both trees yielded similar clustering, only the Dps tree is shown. The inferred minimum evolution (NJ) phylogenies (Felsenstein 1993) depicted several notable fea[bu791]tures. White River and Alabama/Mississippi bears formed two monophyletic groups, with two exceptions in the White River group (inclusion of OU141 and exclusion of WR536); these two individuals also were incorrectly assigned using the assignment test. The two Red Creek WMA bears (U. a. luteolus) clustered very closely with individuals from Mobile River (U. a. floridanus), suggesting the close genetic relationship of bears in these respective geographic regions; although of nominally different subspecies, these regions are separated by only about 60 km. The Tensas River population formed a tight cluster, although not monophyletic, and the White River group branched from the Tensas River cluster. Individuals from the Cook County population consistently associated with Ozark, Ouachita, Upper Atchafalaya, and Lower Atchafalaya populations, but never associated with White River or Alabama/Mississippi populations. Ouachita individuals did not form a unique cluster in either tree. When the data were reentered using randomized input order, the same pattern of grouping was observed for all populations, except that the single Lower Atchafalaya group was split into two groups on the Dkf tree.
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Discussion |
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Population-Level Relatedness
Genetic diversity within the eight black bear populations studied differed between the U. a. americanus and U. a. luteolus subspecies. Diversity was greater within U. a. americanus. which corroborates previous results of Miller (1995). The Cook County population exhibited the highest level of diversity observed. The lowest variation was found in the White River and Alabama/Mississippi populations. Overall the level of microsatellite variation observed in this study is within the range observed for other black bear populations, where heterozygosities ranged from 0.35 to 0.80 and the average number of alleles ranged from 2.3 to 8.0 among populations (Paetkau and Strobeck 1994).
The observed patterns of genetic variation distinguished a southern group of black bear populations (White River, Tensas River, Upper Atchafalaya, Lower Atchafalaya, and Alabama/Mississippi), which differed from the northern populations using all three distance measures. Further, two of the distance measures (Dps and GST) provided significant statistical support for this relationship. Within this southern group, the White River and Tensas River populations were grouped with statistical significance, as were the Upper Atchafalaya and Lower Atchafalaya populations. All populations in the southern group are nominally U. a. luteolus, except White River is U. a. americanus and Alabama/Mississippi is U. a. floridanus. However, the genetic relationship between the White River and Tensas River populations was as close as those inferred for other consubspecific pairwise comparisons (e.g., UA/LA and OU/OZ) in this study, leading to our inference that the White River and Tensas River populations are members of the same subspecies, and supporting reclassification of the White River population as U. a. luteolus. This is because of the close association of the White River population with the Tensas River population and other southern (U. a. luteolus) populations, and the nonassociation of the White River population with the Ozark and Ouachita (U. a. americanus) populations.
A larger genetic distance between Alabama/Mississippi and the other four southern populations (LA, UA, WR, and TR), significant group subdivisions using AMOVA when Alabama/Mississippi was not grouped with the other southern populations, and the inconsistent phylogenetic positioning of the Alabama population within the southern group suggest that the Alabama/Mississippi population may be genetically distinct from other southern populations. In order to be verified, this hypothesis requires further testing involving additional U. a. floridanus populations, which may associate with the AL/ MS population. However, other work (Miller 1995) suggested that the distinction between U. a. floridanus and U. a. luteolus may be unwarranted.
Individual-Level Relatedness
Black bears from Cook, Lake, and St. Louis Counties, Minnesota, and from Manitoba, Canada were released into the Ozark, Ouachita, Upper Atchafalaya and Tensas River populations from 1958 to 1966 (Rogers 1973; Smith and Clark 1994). These reintroductions, and subsequent reproduction, may have contributed to the phylogenetic similarities of Cook County bears with Ozark, Ouachita, and Atchafalaya individuals. Cook County individuals, however, did not associate phylogenetically with Tensas River individuals using the Dkf metric; using the Dps metric, only one Cook County individual associated with Tensas River individuals. This is presumably because the Tensas River reintroduction was relatively small (35 individuals versus 130–200 individuals into the other areas of Arkansas and Louisiana) (Taylor 1971, cited in Pelton 1989), and introduced individuals may not have contributed considerably to the Tensas River gene pool. Had there been no genetic effect of reintroduction, we would expect to find that the individuals from the source populations would not have associated phylogenetically with individuals from the recipient populations. Further, since the source populations (Minnesota, Manitoba) are spatially and temporally separated from the recipient populations, a considerable degree of genetic differentiation would be expected between source and recipient. The White River, Tensas River, and Alabama/Mississippi populations appear to have unique evolutionary histories relative to the other populations. This is consistent with the fact that two of these populations were not augmented with Cook County individuals. In addition, the Alabama/Mississippi, White River, and Tensas River populations were found to be more cohesive relative to other populations for two reasons: (1) 93–100% of individuals were assigned to their originating populations and (2) individuals assigned incorrectly from these three populations were still assigned within the southern group of populations. Thus the White River, Tensas River, and Alabama/Mississippi populations may be taken as more representative of native southern black bear populations which have not been affected by introgression of northern genes. Ouachita is the only population not differentiated from all other populations, as evidenced by several nonsignificant FST values; further, no Ouachita individuals were assigned correctly to the Ouachita population, and half were assigned to Cook County. This observation could be explained if the Ouachita population represents a natural or artificial intergrade population between the northern (U. a. americanus) and southern (U. a. luteolus) types. Hence we infer that while black bear introductions have affected the gene pools of several southern populations, the overall pattern of interpopulation relatedness was not altered. Earlier work using DNA fingerprinting and analysis of band- sharing frequencies (Miller et al. 1998) did not detect reintroduction effects. Greater sensitivity to interpopulation hybridization may have resulted from the use of allelic microsatellite markers in this study, as well as the larger number of interpopulation comparisons available.
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Management Implications |
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Phylogenetic inferences at both the population and individual levels, based on variation at seven microsatellite loci, support the hypothesis that the White River NWR population of black bear belongs to the U. a. luteolus subspecies, which has threatened status under the U.S. Endangered Species Act. These inferences are being considered by the U.S. Fish and Wildlife Service to reach a finding regarding subspecific affinity of that black bear population. In particular, the issue of black bear harvest from the White River NWR is likely to be affected. Other data sets regarding genetic and morphologic characters might also be assessed to support or refute our inference regarding the subspecific status of the White River NWR population.
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Acknowledgments |
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We thank the U.S. Fish and Wildlife Service (FWS) for funding this research, and W. McDearman of the U.S. FWS at Jackson, MS, for constructive comments on an earlier version of this manuscript. We also would like to thank the following individuals and agencies for assistance in trapping bears and collecting blood and tissue samples: D. Garshelis with the Minnesota Department of Forestry and Wildlife; D. Goad with the Arkansas Game and Fish Commission; M. Hurdle and N. Hunter with the U.S. FWS at White River NWR, AR; H. Jacobson and T. White at Mississippi State University; T. Edwards with the U.S. FWS at Tensas River NWR, LA; R. Pace at Louisiana State University; K. Shropshire with the Mississippi Department of Wildlife, Fisheries, and Parks; K. Guyse with the Alabama Department of Natural Resources; J. Kasbohm with the U.S. FWS; and D. Miller with the Florida Game and Freshwater Fish Commission.
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Footnotes |
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Corresponding Editor: Stephen J. O'Brien
Received June 11, 2000
Accepted February 14, 2001
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References |
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