Diagnostic Genetic Marker That Differentiates Eastern Fox Squirrels From Eastern Gray Squirrels

Abstract The Delmarva fox squirrel (Sciurus niger cinereus) has been listed as endangered by the United States Department of Interior since 1967. A high-priority task for the recovery of this taxon is to determine its current geographic distribution. Toward this end, we have identified a microsatellite locus that unambiguously differentiates Delmarva fox squirrels from eastern gray squirrels (S. carolinensis), which frequently co-occur with Delmarva fox squirrels. Analysis of this marker in noninvasively collected hair samples will allow unequivocal identification of localities occupied by Delmarva fox squirrels with a minimum investment of funds, time, and effort because handling individuals will be unnecessary. This protocol will expedite site review in connection with the Endangered Species Act consultation process.     

Genetic diversity and population divergence in fragmented habitats: Conservation of Idaho ground squirrels

The Idaho ground squirrel, which consists of a northern (Spermophilus brunneus brunneus) and a southern subspecies (S. b. endemicus), has suffered from habitat loss and fragmentation, resulting in a reduction in both numbers and geographic range of the species. The northern Idaho ground squirrel (NIDGS) is listed as a threatened subspecies under the Endangered Species Act, and the southern Idaho ground squirrel (SIDGS) is a candidate. Because Idaho ground squirrel populations are small and often isolated, they are susceptible to inbreeding and loss of genetic diversity through drift. This research evaluates levels of genetic diversity and patterns of population divergence in both subspecies of Idaho ground squirrels. We hypothesized that NIDGS would exhibit lower genetic diversity and greater population divergence due to a longer period of population isolation relative to most SIDGS populations. Genetic diversity and divergence were quantified using 8 microsatellite loci. Contrary to expectations, SIDGS populations exhibited consistently lower levels of microsatellite diversity. Additionally, NIDGS exhibited only modest divergence among populations, while divergence levels among SIDGS populations were highly varied. Preliminary evaluations of mitochondrial DNA diversity and structure revealed lower diversity in NIDGS and some differences in gene flow that warrant further study. Based on our results, we suggest different management strategies for the two subspecies. Habitat restoration appears to be the most desirable conservation strategy for NIDGS populations. In contrast, low genetic diversity observed in SIDGS may warrant supplementation of isolated populations through translocations or captive breeding to mitigate further loss of genetic variability.     

Characterization of twenty-six polymorphic microsatellite markers for the fox squirrel (Sciurus niger) and their utility in gray squirrels (Sciurus carolinensis) and red squirrels (Tamiasciurus hudsonicus)

Twenty-six polymorphic microsatellite markers were developed for the fox squirrel (Sciurus niger). The number of alleles ranged from 2 to 11 and observed heterozygosities ranged from 0.037 to 0.815. Preliminary screening revealed that numerous loci also were polymorphic in other squirrel species: Sciurus carolinensis and Tamiasciurus hudsonicus. These loci should be useful tools for investigating the social structure, mating tactics and movement behavior of fox squirrels.     

Grey squirrels in central Italy: a new threat for endemic red squirrel subspecies

A new population of the invasive American Eastern grey squirrel (Sciurus carolinensis) has recently settled in central Italy from an accidental release in Perugia, Umbria in the early 2000s. The grey squirrel is known to compete with and exclude native red squirrels (S. vulgaris) in the British Isles and Northern Italy, so it represents a potentially important new conservation threat to the red squirrel subspecies of south and central Italy, S. vulgaris italicus and S. v. meridionalis, which are endemic to peninsular Italy. The grey squirrel population range in Perugia is currently expanding at a rate of about 0.29 km/year (SD 0.19), slower than grey squirrel invasions elsewhere in Europe. Nuclear DNA analysed at 12 different microsatellite loci revealed that the grey squirrels in Perugia have extremely low genetic diversity, consistent with a small founder size. Genetic assignment tests indicate that the Perugia population was founded by translocations from an established population in Piedmont, Italy. No genetic substructure is evident yet in the Perugia population. These results together have serious consequences for the management of the grey squirrel invasion in Perugia and the conservation of the red squirrel subspecies: the Perugia grey squirrel population should be eradicated if politically feasible; otherwise new releases of grey squirrels, especially from sources other than the Piedmont population, should be prevented because such introductions could increase genetic diversity, thereby potentially increasing population range expansion rate to the much higher levels seen for more diverse grey squirrel populations elsewhere in Europe.     

Genetic assessment of the red squirrel in Illinois: Immigrants or Exotics?

Novel populations pose unusual challenges for wildlife managers because knowledge regarding the source of these populations is essential to develop sound management approaches. One example that illustrates the complexity of this issue is the small population of red squirrels (Tamiasciurus hudsonicus) identified in northeastern Illinois in the 1970s. To elucidate the source of the red squirrel population in Illinois, we examined both contemporary and less recent patterns of genetic structure using nuclear microsatellite loci and mitochondrial DNA. Analyses revealed the Illinois subpopulation was primarily comprised of descendents of immigrants from Indiana, but there was also evidence of a translocation of squirrels from Minnesota. We recommend continued protection for the red squirrel in Illinois due to its restricted geographic range, small population size, and status as a native population. © 2011 The Wildlife Society.     

The translocation and post release settlement of red squirrels Sciurus vulgaris to a previously uninhabited woodland

Red squirrels have undergone a 30% contraction of their range in the last 10 years in Ireland, a decline attributed to the introduced grey squirrel. Large regions in the west of Ireland are free of both species of squirrel, due to the isolation of forests there and their relatively recent planting. The potential of these forests as translocation sites for red squirrels was investigated to ascertain the possibility of increasing the range of red squirrels in Ireland. Nineteen red squirrels were moved into Derryclare wood, Co. Galway using a soft release into enclosures, and their subsequent survival and settlement in the wood was monitored, using trapping and radio-tracking. The successful release of 94.7% of squirrels from the enclosure, and 68.4% survival to the start of the following year’s breeding season were in excess of the target survival rates of 75 and 50%, respectively. Five of the females were found to be lactating in May 2006, and seven offspring captured in August 2006. A squirrel was observed in a follow-up visit in October 2007. Radio-tracked red squirrels tended to remain in the general vicinity of release, incorporating supplementary feeders as part of their home ranges. Squirrels also fed on the natural food available in the wood, with feeding signs readily observed in the wider woodland. The techniques used proved very successful in survival, retention and future reproduction of the translocated population. Timing of release may be an important consideration for future translocations with survival better in summer-released animals.     

Forces structuring tree squirrel communities in landscapes fragmented by agriculture: species differences in perceptions of forest connectivity and carrying capacity

The North American red squirrel ( Tamiasciurus hudsonicus ) has expanded its range into the central hardwoods of the United States in conjunction with increasing forest fragmentation and declining gray squirrel ( Sciurus carolinensis ) populations. We used translocation experiments and patch occupancy data to test for interspecific differences in mobility and sensitivity to habitat loss and modification by agriculture. We released squirrels in fencerows to test the hypothesis that gray squirrels display inferior mobility relative to red and fox ( S. niger ) squirrels. Elapsed time to movement from fencerows for 76 individuals increased with distance to forest patches and harvesting of crops. Gray and red squirrels took longer to move from fencerows than fox squirrels, and gray squirrels were less successful at moving from fencerows than red and fox squirrels. Ecologically scaled landscape indices revealed the degree to which interspecific differences in mobility and individual area requirements accounted for the occurrence of these species across landscapes. Gray squirrel distribution was constrained both by individual area requirements and dispersal ability. Occurrence of red and fox squirrels was related to patch size but was unaffected by landscape connectivity.     

Habitat Use of Fox Squirrels in an Urban Environment

Abstract: Tree squirrels are one of the most familiar mammals found in urban areas and are considered both desirable around homes and, conversely, a pest. We examined fox squirrel (Sciurus niger) habitat use in inner city and suburban areas using radiotelemetry. We estimated habitat selection ratios at differing scales by season and fox squirrel activity. Telemetry data suggests that during periods of inactivity radiocollared fox squirrels (n = 82) selected 1) areas with greater tree canopy, 2) live oaks (Quercus fusiromis and Q. virginiana), and 3) trees with larger diameters and canopies. When inactive during the winter and spring, fox squirrels also preferred, within their core areas, to use the inside of buildings, and during periods of activity in the autumn and spring, fox squirrels preferred grassy areas. During periods of activity, fox squirrels avoided using pavement but did not exclude it from their core-area movements. Fox squirrels' ability to use buildings and to tolerate pavement in core-area movements make vast areas of the urban environment available to fox squirrels. In evaluating habitat variables that increased fox squirrel activity in urban areas, we found the number of large and medium trees, amount of pavement and grassy areas, canopy cover, number of oaks, and the area covered by buildings were all important factors in predicting fox squirrel activity in an urban environment. Our data suggests urban planners, animal damage control officials, wildlife managers, and landscapers who want to control urban fox squirrel populations through habitat manipulation should consider the reduction of oaks trees, a reduction of the canopy cover, and restricting the access of fox squirrels to buildings. Alternatively, home owners and squirrel enthusiasts hoping to bolster fox squirrel populations in urban areas should consider increasing the number of large mast—bearing trees and canopy cover and providing nest boxes.     

Microsatellite loci for the Siberian flying squirrel,Pteromys volans

We report the isolation and characterization of polymorphic microsatellite loci for the Siberian flying squirrel Pteromys volans. The seven most useful loci had between six and 11 alleles and expected heterozygosities ranging from 0.477 to 0.866. We also tested the utility of these loci in other squirrel species, northern flying squirrels (Glaucomys sabrinus and G. volans) and the common red squirrel (Sciurus vulgaris). Three of the Siberian flying squirrel loci were polymorphic in other squirrel species, suggesting a limited potential for cross‐species use.     

Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges

For conservation purposes islands are considered safe refuges for many species, particularly in regions where introduced predators form a major threat to the native fauna, but island populations are also known to possess low levels of genetic diversity. The New Zealand archipelago provides an ideal system to compare genetic diversity of large mainland populations where introduced predators are common, to that of smaller offshore islands, which serve as predator-free refuges. We assessed microsatellite variation in South Island robins (Petroica australis australis), and compared large mainland, small mainland, natural island and translocated island populations. Large mainland populations exhibited more polymorphic loci and higher number of alleles than small mainland and natural island populations. Genetic variation did not differ between natural and translocated island populations, even though one of the translocated populations was established with five individuals. Hatching failure was recorded in a subset of the populations and found to be significantly higher in translocated populations than in a large mainland population. Significant population differentiation was largely based on heterogeneity in allele frequencies (including fixation of alleles), as few unique alleles were observed. This study shows that large mainland populations retain higher levels of genetic diversity than natural and translocated island populations. It highlights the importance of protecting these mainland populations and using them as a source for new translocations. In the future, these populations may become extremely valuable for species conservation if existing island populations become adversely affected by low levels of genetic variation and do not persist.     

韩国与中国东北地区松鼠线粒体DNA控制区的序列变异

为了研究松鼠东北亚种(Sciurus vulgaris manchuricusThomas)不同种群的序列变异水平并进一步确定分类地位,我们分析了韩国5个地点和中国东北2个地点的松鼠标本的线粒体DNA控制区的全序列(1 058 bp)。39个韩国松鼠标本显示出21种单倍型,这些单倍型间的平均Tamura-Nei距离为1·0%; 24个中国松鼠标本显示21种单倍型,单倍型间的平均Tamura-Nei距离为1·4% (1 058 bp的全序列中发生变异的位点有119个,占11·2%)。韩国松鼠和中国松鼠间的平均距离为1·3%。并且韩国和中国松鼠的所有42个单倍型形成了一个单系分支,Fst值为0·04,表明在两个国家的松鼠间没有发生遗传分化。因此,序列分析的分子生物学的结果支持现行的分类,即来自韩国的朝鲜亚种(S·v·coreae)是中国北部地区松鼠东北亚种(S·v·manchuricus)的同物异名。这还需要进一步对北朝鲜和中国东北其它地区更多标本的分子和形态学分析来验证这一结论。     

Patterns of genetic diversity in the red squirrel (Sciurus vulgaris L.): Footprints of biogeographic history and artificial introductions

British S. vulgaris are classified as aseparate subspecies, S. v. leucourus, tomainland Europe. While S. vulgaris is notunder threat across most of its Eurasian range,in Britain, Ireland and Italy populations aredeclining, mainly due to the introduction ofthe American grey squirrel (S.carolinensis). In this study, we conducted anextensive survey of mitochondrial DNA variationin British S. vulgaris populations and apreliminary survey of continental Europeanpopulations. Our main aims were to determinethe extent to which any populations of S.vulgaris in Britain are partially or whollythe product of artificial translocation of redsquirrels from continental Europe, and whethercontinental population variation will provideinformation on post-glacial reafforestationpatterns in Europe. We found that the majorityof extant populations of British S.vulgaris are of continental ancestry, manywith a very recent (last 40 years) Scandinavianancestry. The Scandinavian haplotype hasrapidly become the most dominant innortheastern Britain, despite not appearing innorthern English populations until 1966. Thissuggests that these squirrels may have anadaptive advantage in the non-native sprucedominated conifer plantations of northernEngland. Our preliminary examination ofcontinental populations demonstrated that theyare sufficiently differentiated to allow aphylogeographic study of this species.     

A nuclear perspective on endemism in northern flying squirrels (Glaucomys sabrinus) of the Alexander Archipelago, Alaska

We used microsatellites to examine populationstructure and genetic diversity in northernflying squirrels in the Alexander Archipelagoof Southeast Alaska, with an emphasis on theendemic Prince of Wales flying squirrel(Glaucomys sabrinus griseifrons). Previouswork showed this subspecific designationcoincided with a distinct mitochondrial lineageon eleven islands (the Prince of Wales [POW]complex). To obtain a nuclear perspective onthis lineage and to further investigate geneticdiversity among insular populations, weexamined six microsatellite loci in 233 flyingsquirrels representing eight populations inSoutheast Alaska and a population from interiorAlaska (seven island and two mainlandlocalities). Island populations have lowerheterozygosity and allelic diversity thanmainland populations. Overall, populationpairs show a pattern of isolation by distance,indicating there is little long-distance geneflow across the archipelago. Analyses ofmicrosatellite allele frequencies revealsignificant differences between the POW complexpopulations and others we examined, a findingcongruent with the mitochondrial data. Thepopulation from Mitkof Island, a non-POWcomplex island, also differs significantly fromother populations in allele frequencies. Thesix POW complex populations are geneticallyvery similar, suggesting current or recent geneflow among these islands, while there seems tobe no gene flow between the POW complex andother populations in Southeast Alaska. Ourdata corroborate mitochondrial DNA resultsindicating that G. s. griseifrons isgenetically distinct and suggest a generalpattern of isolation of insular flyingsquirrels in Southeast Alaska.     

Tests of hypotheses on predation as a factor maintaining polymorphic melanism in coastalplain fox squirrels (Sciurus niger L.)

Fox squirrels ( Sciurus niger ) in the south-eastern U.S. coastal plain differ from those in the rest of the species' range by having black heads with white nose and ears. Postcranially on the dorsum, they also show interindividual colour variation, ranging from all-light agouti to all-black non-agouti. I present results of experiments undertaken to test whether the evolution of these pigmentary features can be attributed to interactions with predators. Comparative static crypsis (when the squirrels are still) was tested by determining how well specimens of the squirrel morphs matched their backgrounds in terms of intensity (brightness) distributions and patch size. Comparative dynamic effects (when the squirrels are moving) were tested using captive red-tailed hawks ( Buteo jamaicensis ) and models of the fox squirrel morphs. Results indicated that morphs of coastal-plain fox squirrels with all-light backs are better static matches to unburned backgrounds than are the darker morphs with which they coexist. Against fire-blackened backgrounds, fox squirrel morphs with intermediate and all-black backs are better intensity matches than those with all-light backs, but the dark morphs are not better patch-length matches than light morphs. The superiority of dark morphs in intensity matching for a short time after a fire does not seem sufficient to account for their long-term maintenance. Hawks responded more slowly to moving fox squirrel models with intermediate amounts of black on the back than to all-light or all-dark morphs; this result suggests a possible factor that would favour retention of genes for dorsal blackness in the coastal-plain population. Patchy black and white heads appear to promote static crypsis of south-eastern fox squirrels, and hawks reacted more slowly to moving squirrel models with such colouration than to those with plain heads.     

Genetic management of the red squirrel,Sciurus vulgaris: a practical approach to regional conservation

The progressive decline in red squirrel (Sciurus vulgaris) numbers in Wales has led to conservation and reintroduction projects being established on the island of Anglesey. The recovery of the island’s remnant wild population was initially successful, however concern remained over potential loss of genetic diversity resulting from an observed demographic bottleneck. We used mitochondrial DNA (mtDNA) control region sequences and six microsatellite loci to assess current levels of genetic variation in the population. Samples were monomorphic for control region sequences and a historic specimen from the same area carrying a different haplotype demonstrated a loss of mtDNA diversity during the last 20 years. Inclusion of other Welsh haplotypes indicated phylogeographic structure in the region, in contrast to previous UK studies. Genotyping results showed allelic diversity and heterozygosity to be less than 50% of that recorded in other UK populations, with strong evidence for a recent genetic bottleneck. A parallel reintroduction programme on Anglesey included genetic analysis of individuals during the selection of captive breeding pairs. We present analysis of sequence and microsatellite data, and subsequent management decisions taken to maximise diversity in the founder and F1 generations. Population and Habitat Viability Analysis applied to both populations modelled future levels of heterozygosity and allelic diversity. Supplementation of the remnant and reintroduced populations with translocated squirrels was simulated as a potential management tool; results support use of this strategy to reduce loss of diversity and increase survival. The limitations of applying conservation genetic theory within small-scale management projects are discussed.     

Molecular phylogeography of European Sciurus vulgaris: refuge within refugia?

The red squirrel ( Sciurus vulgaris ) is a well-known forest animal distributed all over Europe. Still, we are far from having a firm knowledge of the species' phylogeography. This study investigates the genetic differentiation of S. vulgaris across the species' Eurasian range, using sequence data from the mitochondrial DNA gene (D-loop, 252 base pairs, cytochrome b , 359 base pairs), and eight variable autosomal microsatellite loci genotyped for 236 individuals. The results reveal the presence of two main mitochondrial phylogroups. The first clade comprises the individuals from the region of Calabria in southern Italy, belonging to the subspecies S. v . meridionalis , while the second clade contains the remainder of the studied individuals. Bayesian analysis of microsatellite genotypes resulted in three main clusterings corresponding to the three S. vulgaris subspecies: infuscatus, meridionalis and fuscoater . Geographical distribution of mtDNA haplotypes and mismatch analysis suggest a common refugium for the red squirrel across most of its present range from which expansion happened rather rapidly. The genotype mixing of italicus with northern populations could be a residual of postglacial expansion. The lack of mixing between the Calabrian lineage and the rest of European red squirrel haplotypes can be seen as evidence for distinct histories throughout the Pleistocene. Calabrian mtDNA probably diverged in an ice age contraction and remained isolated from the neighbouring squirrel populations until very recent times.     

Fox Squirrel Survival in Urban and Rural Environments

Abstract A number of studies on mammalian species that have adapted to urban areas suggest survival may be higher for urban populations than rural populations. We examined differences in fatalities between an urban and rural population of fox squirrels (Sciurus niger). We radiocollared (n = 50 rural, n = 78 urban) fox squirrels during approximately 2 years. We found monthly survival of rural fox squirrels (Ŝ = 0.936) was lower than urban fox squirrels (Ŝ = 0.976) over the same 12-month period. Nonetheless, when comparing a 24-month period of survival data on urban squirrels with an 18-month period on the rural squirrels (periods overlapped for 12 months), survival rates were more similar between urban (Ŝ = 0.938) and rural squirrels (Ŝ = 0.945). Our data suggest that sex and season may influence survival of urban squirrels and not rural squirrels. We also found that cause of fatalities differed between the urban and rural squirrels, with >60% of fatalities on the rural site caused by predation. In contrast, <5% of the fatalities on the urban site were caused by predation and >60% of urban fox squirrel fatalities were caused by motor vehicle collisions. This study illustrates the need to advance our ability to understand, predict, and mitigate effects of urbanization on wildlife resources.     

Nest Site Selection by Western Gray Squirrels at Their Northern Range Terminus

ABSTRACT The western gray squirrel (Sciurus griseus) in Washington, USA, is limited to 3 disjunct areas and is a state threatened species. Information is lacking for the North Cascades population, which is the northernmost population for the species. Squirrels in this population exist without oaks (Quercus spp.) that provide forage and cavities for maternal nests elsewhere in their range. During May 2003 to August 2005, we studied selection of nest sites and nest trees by 18 radiocollared squirrels in Okanogan County, Washington. Without oak cavities, females reared their young in dreys. General nest-tree characteristics were similar to characteristics of western gray squirrel nest trees in Southeastern Cascades: relatively tall ponderosa pines (Pinus ponderosa) ≥ 40 cm diameter at breast height. Results from conditional logistic models determined that the odds of a squirrel selecting a tree for nesting increased with greater diameter at breast height and with infection by dwarf mistletoe (Arceuthobium spp.). Nest sites with high selection probability by squirrels had greater basal area and number of tree species than available unselected sites. Retention of forest patches that include a mix of conifer species or conifer and deciduous trees and moderate to high basal area could promote nesting opportunities, connectivity for arboreal travel, as well as abundance and diversity of hypogeous fungi. Experiments to test the efficacy of retaining untreated patches of varying size (including trees infected with mistletoe) on nesting by western gray squirrels within stands managed for fire suppression and forest health would provide important information about the effects of forest fuel management on arboreal wildlife.     

Genetic structure of red deer population in northeastern Poland in relation to the history of human interventions

We studied the genetic structure of a red deer (Cervus elaphus) population in 8 woodlands of northeastern Poland and 1 in western Belarus and compared it with the documented history of the population in the region. Red deer nearly went extinct in the region in the 18th and 19th centuries. In the mid-19th century, reintroductions began and continued until the mid-1960s. Animals were translocated from various sites in Poland and other European countries. We genotyped 303 individuals using 14 microsatellite loci and sequenced 253 individuals for a fragment of the control region (mitochondrial DNA [mtDNA]). The microsatellite analyses demonstrate that 3 genetically separate subpopulations exist, but 4 according to mtDNA. All haplotypes found in northeastern Poland are closely related to haplotypes from northern and northwestern Europe. The only individuals that could have originated from autochthonous red deer populations, rather than introductions, were found in Napiwoda Forest. The present regional genetic structure of the species is consistent with the known history of red deer translocations. Current patterns of genetic diversity in these populations are determined by the interaction of past human management and contemporary natural migrations. © 2012 The Wildlife Society.     

Comparative phylogeography and population genetics within Buteo lineatus reveals evidence of distinct evolutionary lineages

Traditional subspecies classifications may suggest phylogenetic relationships that are discordant with evolutionary history and mislead evolutionary inference. To more accurately describe evolutionary relationships and inform conservation efforts, we investigated the genetic relationships and demographic histories of Buteo lineatus subspecies in eastern and western North America using 21 nuclear microsatellite loci and 375-base pairs of mitochondrial control region sequence. Frequency based analyses of mitochondrial sequence data support significant population distinction between eastern (B. l. lineatus/alleni/texanus) and western (B. l. elegans) subspecies of B. lineatus. This distinction was further supported by frequency and Bayesian analyses of the microsatellite data. We found evidence of differing demographic histories between regions; among eastern sites, mitochondrial data suggested that rapid population expansion occurred following the end of the last glacial maximum, with B. l. texanus population expansion preceding that of B. l. lineatus/alleni. No evidence of post-glacial population expansion was detected among western samples (B. l. elegans). Rather, microsatellite data suggest that the western population has experienced a recent bottleneck, presumably associated with extensive anthropogenic habitat loss during the 19th and 20th centuries. Our data indicate that eastern and western populations of B. lineatus are genetically distinct lineages, have experienced very different demographic histories, and suggest management as separate conservation units may be warranted.