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Genetic Consequences of Habitat Fragmentation and Loss: the Case of the Florida Black Bear (Ursus Americanus floridanus)

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Genetic Consequences of Habitat Fragmentation and Loss: the Case of the Florida Black Bear (Ursus Americanus floridanus) Conserv Genet (2007) 8:455–464 DOI 10.1007/s10592-006-9184-z ORIGINAL PAPER Genetic consequences of habitat fragmentation and loss: the case of the Florida black bear (Ursus americanus floridanus) Jeremy D. Dixon Æ Madan K. Oli Æ Michael C. Wooten Æ Thomas H. Eason Æ J. Walter McCown Æ Mark W. Cunningham Received: 23 November 2005 / Accepted: 28 June 2006 / Published online: 28 September 2006 Ó Springer Science+Business Media B.V. 2006 Abstract Habitat loss and fragmentation can influ- genetically distinct populations. There was no isola- ence the genetic structure of biological populations. tion-by-distance relationship among Florida black bear We studied the genetic consequences of habitat frag- populations, likely because of barriers to gene flow mentation in Florida black bear (Ursus americanus created by habitat fragmentation and other anthropo- floridanus) populations. Genetic samples were col- genic disturbances. These factors resulted in genetic lected from 339 bears, representing nine populations. differentiation among populations, even those that Bears were genotyped for 12 microsatellite loci to were geographically close. Population assignment tests estimate genetic variation and to characterize genetic indicated that most individuals were genetically as- structure. None of the nine study populations deviated signed to the population where they were sampled. from Hardy–Weinberg equilibrium. Genetic variation, Habitat fragmentation and anthropogenic barriers to quantified by mean expected heterozygosity (HE), movement appear to have limited the dispersal capa- ranged from 0.27 to 0.71 and was substantially lower in bilities of the Florida black bear, thereby reducing smaller and less connected populations. High levels of gene flow among populations. Regional corridors or genetic differentiation among populations (global translocation of bears may be needed to restore his- FST = 0.224; global RST = 0.245) suggest that frag- torical levels of genetic variation. Our results suggest mentation of once contiguous habitat has resulted in that management actions to mitigate genetic conse- quences of habitat fragmentation are needed to ensure long-term persistence of the Florida black bear. J. D. Dixon (&) Florida Fish and Wildlife Conservation Commission, P.O. Keywords Florida black bears Æ Genetic variation Æ Box 177, Olustee, FL 32072, USA Gene flow Æ Habitat fragmentation Æ Microsatellites Æ e-mail: [email protected] Ursus americanus floridanus M. K. Oli Æ J. D. Dixon Department of Wildlife Ecology and Conservation, University of Florida, P.O. Box 110430, Gainesville, FL Introduction 32611, USA M. C. Wooten The fragmentation and loss of habitat is one of the Department of Biological Sciences, Auburn University, 334 most serious problems facing the conservation of bio- Funchess Hall, Auburn, AL 36849, USA diversity worldwide (Harris 1984; Meffe and Carroll T. H. Eason 1997). Habitat fragmentation can increase mortality Florida Fish and Wildlife Conservation Commission, 620 rates (Jules 1998), reduce abundance (Flather and South Meridian Street, Tallahassee, FL 32399, USA Bevers 2002), alter movement patterns (Brooker and Brooker 2002), disrupt the social structure of popula- J. W. McCown Æ M. W. Cunningham Florida Fish and Wildlife Conservation Commission, 4005 tions (Ims and Andreassen 1999; Cale 2003), and may South Main Street, Gainesville, FL 32601, USA reduce population viability (Harrison and Bruna 1999; 123 456 Conserv Genet (2007) 8:455–464 Davies et al. 2001). Additionally, habitat fragmenta- The Florida black bear historically roamed tion can lead to isolation of populations and reduction throughout the peninsula of Florida and southern in population size which may cause a decrease in ge- portions of Georgia, Alabama and Mississippi (Brady netic variation (Frankham 1996). The loss of genetic and Maehr 1985). From the 1800s to the 1970s, num- variation may reduce the ability of individuals to adapt bers of Florida black bears were significantly reduced to a changing environment, cause inbreeding depres- due to loss and fragmentation of habitat and unregu- sion (Ebert et al. 2002), reduce survival and repro- lated hunting (Cory 1896; Hendry et al. 1982). Only an duction (Frankham 1995; Reed and Frankham 2003) estimated 300–500 bears remained in the state of and increase the probability of extinction (Saccheri Florida in the 1970s (McDaniel 1974; Brady and Maehr et al. 1998; Westemeier et al. 1998). 1985). Consequently, the Florida Game and Freshwa- Populations that occur within contiguous habitats are ter Fish Commission classified the Florida black bear expected to follow an isolation-by-distance model, as a threatened species in most Florida counties in 1974 where the distance between populations is the overrid- (Wooding 1993). Destruction and fragmentation of ing factor contributing to genetic differentiation (Slat- once contiguous habitat has reduced the distribution of kin 1993). However, the process of habitat Florida black bears to nine disjunct populations: Eglin fragmentation can create dispersal barriers, which can (EG), Apalachicola (AP), Aucilla (AU), Osceola deter gene flow and lead to isolation of populations (OS), Ocala (OC), St. Johns (SJ), Chassahowitzka (Hitchings and Beebee 1997; Gerlach and Musolf 2000). (CH), Highlands/Glades (HG) and Big Cypress (BC) Large mammalian carnivores are particularly vul- (Fig. 1). nerable to habitat loss and fragmentation because of Fragmentation of populations can reduce genetic their relatively low numbers, large home ranges, and variation (Sherwin and Moritz 2000), gene flow (Vos interactions with humans (Noss et al. 1996; Crooks et al. 2001) and increase the probability of extinction 2002). The plight of the Florida panther (Puma (Saccheri et al. 1998; Westemeier et al. 1998), but the concolor coryi) and the giant panda (Ailuropoda genetic consequences of habitat fragmentation on melanoleuca) are examples of large carnivores that Florida black bear populations are unknown. Using have been reduced to small numbers due largely to microsatellite analyses, our objectives were to estimate the impacts of habitat fragmentation and loss. As a within-population genetic variation, and to investigate result of the low fecundity and long generation times, the level of genetic differentiation among populations. large carnivores tend to have reduced levels of ge- Theory predicts a positive correlation between genetic netic variation (Roelke et al. 1993; Lu et al. 2001). variation and population size (Frankham 1996), and Another large carnivore that has been negatively between genetic differentiation and geographic dis- impacted by habitat fragmentation is the Florida tance among populations (Slatkin 1993). Thus, we black bear (Ursus americanus floridanus) (Hellgren tested these predictions by examining the relationship and Maehr 1993). between measures of genetic variation and recent Fig. 1 Geographic distribution of the Florida black bear populations in Florida. Populations are: Eglin (EG), Apalachicola (AP), Aucilla (AU), Osceola (OS), Ocala (OC), St. Johns (SJ), Chassahowitzka (CH), Highlands/Glades (HG), and OS Big Cypress (BC). The OC distribution map was EG compiled by the Florida Fish AP Kilometers AU and Wildlife Conservation 0 1,000 SJ Commission CH Gulf of Mexico HG BC Kilometers 0 300 123 Conserv Genet (2007) 8:455–464 457 estimates of population size, and between measures of Genetic differentiation was estimated using Gene- genetic differentiation and geographic distances among pop 3.4 (Raymond and Rousset 1995) with global FST populations. Finally, we used population assignment (across all populations), pairwise FST (Weir and tests to identify potential dispersers among our study Cockerham 1984) and pairwise RST (Michalakis and populations. Excoffier 1996). The significance of population differ- entiation was tested using the genic differentiation test in Genepop 3.4, and P-values were adjusted for mul- Methods tiple comparisons using a Bonferroni sequential cor- rection (Rice 1989). The likelihood ratio genetic Hair and tissue samples from individual bears were distance, DLR (Paetkau et al. 1995) was estimated for collected from Florida black bear populations during each pair of populations using the Doh assignment 1989–2004. The majority of samples were collected calculator (http://www2.biology.ualberta.ca/jbrzusto/ from field studies, some using non-invasive techniques Doh.php). This genetic distance is based on the ratio of (Woods et al. 1999), but samples also were collected genotype likelihoods between pairs of populations. from translocated animals and from bears killed on The software program Phylip 3.5c (Felsenstein 1993) roadways. Hair and tissue samples were sent to Wild- and the subprogram FITCH (Fitch and Margolia 1967) life Genetics International (http://www.wildlifegenet- were used to generate an unrooted phylogenetic tree, ics.ca/) for microsatellite analysis. DNA was extracted with branch lengths corresponding to DLR values. using QIAGEN’s DNeasy Tissue kits, as per QIA- Geographic distances among populations were esti- GEN’s instructions (http://www.qiagen.com/literature/ mated as the shortest land distance between population genomlit.asp), and microsatellite loci were amplified centroids using least cost path analysis in ArcGIS 8.1.2 using polymearse chain reaction (PCR). Each individ- (McCoy and Johnston 2000). Centroids were estimated ual was genotyped for 12 microsatellite loci G1A, as the harmonic mean of the sample collection loca- G10B, G1D,
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