High shrew diversity on Alaska's Seward Peninsula: community assembly and environmental change.
Key words: Alaska, Beringia, climate change, community dynamics, historical biogeography, Long-tailed Shrew, Seward Peninsula, Sorex
Processes of environmental change shape evolutionary dynamics within species and community dynamics within a given ecosystem. The effects of climate change are perhaps most obvious in northern high latitudes not only because of Arctic amplification (IPCC 2007; MacDonald 2010), but also because high-latitude communities are considered simplistic compared with high diversity of communities in the tropics (Post and others 2009). As a consequence, changes in Arctic biodiversity should be more easily recognized, and importantly, have a greater impact per species, particularly considering that Arctic species typically have broad ranges (Callaghan and others 2004a). Yet, our knowledge of Arctic community dynamics through time is still relatively poor, as high-latitude biodiversity research has been afforded comparatively little emphasis (ACIA 2005). I focus on Long-tailed Shrews (genus Sorex), part of the resident terrestrial fauna in Alaska, to report an incidence of remarkably high sympatric diversity and discuss implications for future community change based on genetic evidence.
The Long-tailed Shrews are a diverse group of mammals with 78 species recognized (Hutterer 2005). Their range spans the entire Holarctic in longitude, and from Guatemala in Central America and southern China in Eurasia north to the Arctic Ocean. They occupy virtually every terrestrial habitat except the most arid desert areas. Among mammals, Sorex shrews can be the most diverse and abundant members of a community (Churchfield 1990). Up to 3 species can be found sympatrically in most areas, but on occasion up to 8 species have been recorded at the same locality and within the same habitat (Sheftel 1994). Such high sympatry is rare and generally explained by local habitat heterogeneity resulting from a transition between elevational zones (Rickart and others 2011), or from a mosaic of different ecotypes in proximity (Churchfield and others 1997). Coexistence of Sorex species has also been the focus of numerous investigations dealing with reduction in competiton due to body size (Sheftel 2005) and trophic differences (Churchfield 1991; Churchfield and others 1999), microhabitat use (McCay and others 2004), and temporal and spatial abundance (Mortelliti and Boitani 2009).
Highest shrew diversity in North America is generally found at middle latitudes (Berman and others 2007). Here, I report collection of up to 6 species of Sorex from high-latitude locations across northern Alaska and I suggest that this high diversity is a consequence of variable histories of diversification. In a comparative biogeographic context I review published evidence from genetic signatures of how these species have responded both spatially and temporally to environmental change through the latest Pleistocene and Holocene (130 ka to present). In particular I concentrate on the Seward Peninsula (Kuzitrin Lake), where highest shrew diversity was found, to recreate this shrew fauna through time.
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Beringia (Hulten 1937), a biogeographic region spanning eastern Asia and western North America, served as an ice-free isthmus between the northern continents during cold phases of the Pleistocene (2.6 Ma to 11 ka; Cook and others 2005). An increasing number of studies provide evidence for high ecological and evolutionary complexity through time over this broad area, constituting a shifting mosaic of habitats and community associations responding to high natural climatic variability (for example Hoberg and Brooks 2010). Alaska (Eastern Beringia) currently supports community constituents with both Eurasian and North American evolutionary origins and offers an excellent setting in which to investigate the response of species to a continually changing landscape due to climate change.
Previous surveys of small mammals in Alaska (Cook and MacDonald 2004, 2006) identified a contact zone between 2 closely related species of the cinereus complex of shrews (Van Zyll de Jong 1991; Demboski and Cook 2003) along the forest-tundra ecotone in northern Alaska. Fieldwork in 2010 for the current study was conducted to further sample sympatric sites along this dynamic contact zone.
Field sites (Fig. 1) in order of sampling (dates are provided in Table 1), were located in Gates of the Arctic National Park (Lake Tulilik [UTM: Zone 5W, 453252E, 7556379N, NAD83; elevation: 550 m]; Lake Isiak [UTM: Zone 4W, 620937E, 7514306N, NAD83; elevation: 518 m]), Noatak National Park and Preserve (Aniralik Lake [UTM: Zone 4W, 464329E, 7565936N, NAD83; elevation: 525 m]), Cape Krusenstern National Monument (Imik Lagoon [vicinity of Rabbit Creek; UTM: Zone 3W, 547164E, 7486459N, NAD83; elevation: 5 m]), and Bering Land Bridge National Park (Seward Peninsula [Kuzitrin Lake; UTM: Zone 3W, 582355E, 7251785N, NAD83; elevation: 440 m]). All sites are located in mesic open tundra habitat.
The Seward Peninsula sampling site was located south of Kuzitrin Lake near the outlet of a small stream in flat to gently sloping tundra. This mesic site and surrounding region is open shrub-birch tussock tundra and as such is floristically diverse, but generally homogeneous across the site. Traps were set >100 m south of the lake to avoid recognized cultural sites along the shoreline. Flattest areas contained small water channels lined with thick grasses and sedges, and surrounded by mesic mossy tundra, then sloping uphill to the south and becoming steadily more xeric and rocky into granite talus. The lowest slopes consisted of lichen-rich tussock tundra overlaying intermittently deep peat, clay, and sandy soils. There was a high abundance and richness of mosses and lichens as well as shrub-birch and berry-yielding shrubs. The site is characterized as the Beringian Alaska floristic province (Raynolds and others 2006; Fig. 1) and is located at the juncture of several dominant vegetation zones including lichen communities, prostrate dwarf-shrub lichen communities, erect dwarf shrub lichen communities, non-tussock sedge dwarf-shrub forb moss communities, graminoid dwarf shrub communities, and low shrub communities (Raynolds and others 2006).
Shrews and other small mammal species were collected using Museum Special kill traps (Woodstream Corporation, Lititz, PA) baited with rolled oats and peanut butter, and pitfall traps (white plastic cups; 20 cm deep, 10 cm wide), not baited and set flush with ground level. All sampling was in accordance with guidelines for animal care and use established by the American Society of Mammalogists (Gannon and others 2007), and approved by the University of New Mexico Institutional Animal Care and Use Committee (protocol number 08UNM059-TR-100066) and National Park Service (NPS) including site-specific Cultural Resource guidelines. Traps were set to optimize microhabitat sampling in multiple trap-lines per site, with trap-lines maintained for 2 or 3 nights before moving within each site. Trapping effort per site was similar, ranging from 600 to 700 and 700 to 905 trap nights with Museum Special and pitfall traps, respectively (Table 1). Trap lines were set at least 100 m apart and within 1 km distance of the geo-referenced locality recorded for each site.
For each specimen we recorded standard external measurements, species, sex, age, and reproductive condition. Tissues including heart, kidney, lung, spleen, liver, and muscle were stored in liquid nitrogen or fixed in 95% ethanol. Skeletons were dried in the field. All vouchers, parts, and field notes were archived as a permanent loan from NPS in the Museum of Southwestern Biology (data available at http://arctos.database.museum).
Species were identified in the field based on external measurements, pelage, and dental characteristics. Shrew unicuspid variation coupled with adult external measurements was sufficient to accurately identify most species (MacDonald and Cook 2009). However, members of the cinereus complex of shrews are difficult to discern based on dental morphology, and although Masked Shrew (S. cinereus) and Barrenground Shrew (S. ugyunak) can often be distinguished based on size and pelage differences (MacDonald and Cook 2009), molecular methods were used to identify these 2 species.
Molecular methods for sequencing of 1140 bp of the mitochondrial cytochrome b (cyt b) gene were similar to those outlined in Hope and others (2011); some samples were processed using sequencing protocols as outlined in Jackson and others (2008). Sequences were edited and aligned in Sequencher 4.8 (Genecodes, Ann Arbor, Michigan) or Aligner 2.0 [TM] (LI-COR Inc., Lincoln, Nebraska) and visually checked. For species confirmation, cyt b sequences from other members of the cinereus complex were retrieved from GenBank, from which a phylogeny was estimated using the neighbor-joining algorithm in MEGA v5.0 (Tamura and others 2011). Sequences were deposited in GenBank (all accessions used for phylogeny reconstruction are listed in the Appendix).
To assess the relative abundance of each shrew species, a [chi square] test was performed between observed and expected (equal) sample sizes at each field site.
Each site was sampled for 5 nights (Table 1). A total of 11 small mammal species were collected over all sites (8 to 10 species/site) and total numbers ranged from 50 to 121 individuals/site (Table 1). Trap success ranged from 3.1 to 8.6%. Richness of Sorex was generally high, ranging from 3 species at Lake Tulilik to 6 species at Kuzitrin Lake, constituting on average over half of the small mammal richness and abundance collected at each site. Other species sampled included, in order of abundance, Northern Red-backed Vole (Myodes rutilus), Tundra Vole (Microtus oeconomus), Singing Vole (Microtus miurus), Brown Lemming (Lemmus trimucronatus), and Least Weasel (Mustela nivalis).
Shrew species and abundance from the Seward Peninsula at Kuzitrin Lake over 5 nights included: S. cinereus (n = 14); American Pygmy Shrew (S. hoyi, n = 4); Eurasian Least Shrew (S. minutissimus, n = 5 [reflects formal synonymy of S. yukonicus; Hope and others 2010]); Montane Shrew (S. monticolus, n = 9); Tundra Shrew (S. tundrensis, n = 11); and S. ugyunak (n = 12). Shrew species did not significantly deviate from equal abundance at this site [chi square]5 = 8.60, P = 0.126) although relative abundance at all other sites was significantly different (P < 0.01). Although shrews were widespread at Kuzitrin Lake, all 6 species were also collected on a single pitfall trap line (within 100 m proximity) on 6 September 2011. This trap line was set in deep peat and sandy soil along the east side of the main stream draining this area within lichen-dominated tussock-tundra on a 10[degrees] slope (north aspect). No specifically riparian vegetation characterized any part of the trap line and plants were diverse but homogeneous in distribution. Genetic evidence confirmed identification of both S. cinereus and S. ugyunak at Kuzitrin Lake (GenBank Accessions JQ43213JQ43221). Evolutionary relationships of S. cinereus and S. ugyunak clearly place them in different major clades (Southern and Beringian clades, respectively) of the cinereus complex based on evidence from multiple loci (Demboski and Cook 2003; Hope and others 2012).
High latitudes are generally considered to harbor low diversity on a continental or regional scale (Callaghan and others 2004b). This is often coupled with low habitat heterogeneity, but as a consequence species tend to have broad geographic distributions and may occur in exceptionally high abundances. On a finer scale however, communities of the Arctic may harbor high diversity depending on local conditions (Callaghan and others 2004b). High intrageneric Sorex richness across northern Alaska, particularly on the Seward Peninsula, parallels other instances of exceptional sympatric diversity of Sorex recorded from high latitudes (for example, Sheftel 1994), although highest richness among shrews is more generally coincident with mid-latitude sites (Berman and others 2007). High sympatry generally is facilitated by (1) high structural heterogeneity within mesic forest habitats (Kirkland 1991); (2) overlapping of broadly distributed species coupled with the presence of one or more species having a locally restricted range (Nagorsen and Panter 2009); or (3) unequal abundances, with one or more rare species (Rickart and others 2011). Contrary to these criteria, species of the Seward Peninsula shrew fauna all co-occur in a single, structurally simple habitat type (open tundra), have broad geographic ranges (despite this locality being in the very northwest corner of North America), and appear to co-occur in statistically similar abundance. Uneven abundance of species at the other study sites and only limited trapping nights in the current study highlight the need for more extensive survey efforts.
The Seward Peninsula lies on the periphery of all individual shrew species ranges but is the geographic center of their combined distribution, indicating disparate biogeographic histories among these species. Although Kuzitrin Lake lies within open tundra habitat, the Seward Peninsula straddles the forest-tundra ecotone between southern and northern biogeographic influences that may help to explain high local diversity. A number of studies have addressed the processes of diversification through space and time for most shrew species collected at Kuzitrin Lake. Below, I compare and contrast evidence from each species (summarized in Table 2) to suggest that this diverse Arctic community is a comparatively recent phenomenon, and likely had no analog in previous faunas of the region.
Although Kuzitrin Lake is located in open shrub tundra, S. ugyunak was the only shrew collected that is associated purely with tundra habitats (Table 2). It occurs from the Seward Peninsula east across northern Alaska and Canada to Hudson Bay. Sorex ugyunak is a member of the Beringian clade of the cinereus complex of shrews and is closely allied with 5 other species distributed across Beringia (Van Zyll de Jong 1991; Demboski and Cook 2003). As such, this complex with a Nearctic origin has diversified westward through Beringia into the Palearctic. Evidence from multiple genes indicates a common ancestor for all of these high-latitude species of the cinereus complex as recently as approximately 45 ka and with species of more southern latitudes at approximately 130 ka (Hope and others, in review). Movement north through North America to the high latitudes likely occurred during the previous interglacial (Sangamon; 130 to 90 ka), followed by persistence in the Beringia refugium through the last glacial phase (Wisconsinan; 90 to 11 ka) and subsequent fragmentation through Beringia due to rising sea levels since onset of the Holocene (11 ka to present; Hope and others 2012). Population demography of S. ugyunak within Alaska indicates a strong signal of expansion and population growth since the Last Glacial Maximum (LGM; <20 ka; Hope, unpubl, data; Table 2), coincident with an increase in tundra habitats following retreat of both local and widespread ice cover. Populations can be locally abundant, as is shown by this survey (Table 1).
Also a member of the cinereus complex, S. cinereus (sensu stricto) is evolutionarily distinct from "Beringian" species of the complex (including S. ugyunak), belonging instead to the Southern clade of boreal-associated species (Van Zyll de Jong 1991; Demboski and Cook 2003). Sorex cinereus has a distribution spanning most of the Nearctic and exhibits distinct genetic population structure coincident with geography (Hope and others 2012) reflecting fragmentation in the contiguous United States during the Wisconsinan. Following retreat of the Laurentide and Cordilleran ice sheets (beginning 11 ka), S. cinereus rapidly expanded north to occupy its current distribution. This is evident by strong genetic signals of demographic expansion within northern populations (Hope and others 2012; Table 2). Despite associations with conifer forest, S. cinereus can frequently be found in non-forested wet habitats such as the vicinity of Kuzitrin Lake, and moisture is considered the most important factor determining its distribution (Whitaker 2004). All known localities where S. cinereus and S. ugyunak are found in sympatry are in tundra (Cook and MacDonald 2004). The ability of S. cinereus to extend beyond forest habitats may have important implications for hybrid dynamics and direction of gene flow at this and other contact zones between S. cinereus and non-forest species within the cinereus complex.
Along with S. cinereus, S. hoyi belongs within the Boreo-Cordilleran mammalian faunal element, exemplifying a broad North American distribution loosely coincident with boreal forest habitats (Armstrong 1972), although it is also known from open wet areas (Long 1974). The evolutionary history of S. hoyi is old compared with the cinereus complex, despite a lack of significant diversification into sibling species (Stewart and others 2003). This species is locally rare throughout its range (Long 1974) and warrants further molecular study. There is no evidence of a Beringian clade within S. hoyi, suggesting that it, too, recently underwent rapid northward expansion as ice sheets receded. New records have been documented recently in northern Yukon Territory (Jung and others 2007) and northern Alaska (present study) indicating possible continued northward expansion.
The distribution of S. monticolus in western North America (a Cordilleran species; Armstrong 1972) reflects evolutionary associations with the vagrans complex of multiple shrew species, many with distributions highly restricted to the Pacific coast (Carraway 1990; Demboski and Cook 2001). The latitudinal range of S. monticolus is closely coincident with western coniferous forests, from sky islands of the southwestern US to northern Alaska. This is again indicative of recent rapid northward expansion, and high genetic similarity exists between specimens from Montana through Alaska (Demboski and Cook 2001; Table 2). A distinct lineage of S. monticolus along the Pacific Northwest coast suggests persistence within coastal refugia during the last glacial phase, although individuals from northern Alaska do not belong to this clade (Demboski and Cook 2001). Dense undergrowth, especially associated with riparian zones, constitutes preferred habitat (Smith and Belk 1996) and most S. monticolus collected in this survey occurred in proximity to streams.
Among Sorex shrews, S. minutissimus occupies the widest range, occurring from Scandinavia through Eurasia and across the Bering Strait through Alaska. A very limited Nearctic distribution suggests recent expansion eastward into North America, and genetic evidence clearly illustrates minimal differentiation between east-central Siberia and North America (Hope and others 2010; Table 2). In addition, significant recent demographic expansion is evident in both Siberia and Alaska populations coincident with warm periods following the LGM. Sorex minutissimus occupies multiple habitats including both conifer forest (taiga) and open tundra (Yudin 1971), and is likely limited by cold and arid conditions that may explain distributional gaps in Far East Siberia and northern Alaska coincident with distribution of permafrost. Although widespread, S. minutissimus is considered locally rare (Sheftel 1994). In Alaska this species was first recognized in 1993 (Dokuchaev 1994) and only 33 individuals were known from the Nearctic through 2003 (MacDonald and Cook 2009). The current survey sampled a further 15 individuals (Table 1), all from pitfall traps, indicating that S. minutissimus is more abundant and widespread than previously considered. This highlights the importance of targeted surveys for species such as shrews that are often overlooked with conventional small mammal methods (Nagorsen 1996).
The limited Nearctic distribution of S. tundrensis within Eastern Beringia closely matches S. minutissimus. Sorex tundrensis is the only other Holarctic shrew, and the lack of recognized species-level divergence across the Bering Strait again suggests recent movement into North America. Both S. tundrensis and S. minutissimus have an evolutionary origin in the Palearctic, belonging to the sub-genus Sorex, whereas other species of this study belong to the Nearctic derived sub-genus Otisorex (George 1988). However, unlike S. minutissimus, S. tundrensis in North America are genetically distinct from populations west of the Bering Strait, suggesting prolonged isolation of Alaskan from Siberian lineages (Hope and others 2011). Time to most recent common ancestor of east and west Beringia was estimated to be approximately 120 ka, coincident with the Sangamon interglacial. A signal of demographic expansion and population growth within Alaska indicates regional growth and spread leading up to and following the LGM (Hope and others 2011; Table 2). Sorex tundrensis is strongly associated with river floodplain habitats (Churchfield and others 1997) and multiple distinct genetic lineages are geographically coincident with different major river systems through the Holarctic (Hope and others 2011). It is likely that this species persisted in Alaska through the last glacial period within a climatic buffer associated with major rivers such as the Yukon River basin, subsequently expanding as climate warmed.
Development of the Seward Peninsula Small Mammal Community
Diversification within the genus Sorex has been punctuated with a number of transcontinental movements of shrews through Beringia. Since the middle Miocene (approximately 13 Ma), when ancestors of the sub-genus Otisorex immigrated to North America (Dubey and others 2007), Long-tailed Shrews have contributed to mammal assemblages in the Nearctic. Extant species of Sorex have evolved since the late-Pliocene (approximately 3 Ma; Kurten and Anderson 1980) and rapid speciation of large complexes has occurred in response to the cyclic climate of the Pleistocene coupled with transcontinental movement (Hope and others 2011, 2012). In the middle Pleistocene (approximately 1.5 Ma) ancestors of S. arcticus (a close relative of S. tundrensis) immigrated into North America. During the latest glacial cycle, S. tundrensis moved through Beringia eastward, members of the cinereus complex moved westward, and most recently S. minutissimus also moved eastward. There has been a long history of community change in the vicinity of the study area.
Genetic evidence supports the presence of only 2 species of shrew (S. tundrensis and S. ugyunak) within eastern Beringia through the Wisconsinan glacial (Hope and others 2011, 2012; Table 2). Sorex tundrensis may have persisted in large river basins and both species would likely have been at very low densities. The variable climate towards the end of the glacial phase allowed S. minutissimus to rapidly spread through Beringia, eventually being isolated in North America with rising sea levels approximately 11 ka. All 3 shrew species at this time likely would have expanded regionally, coupled with population growth. By 10 ka, a corridor between Cordilleran and Laurentide continental ice-sheets was available (Ritchie and MacDonald 1986), and by 9 ka extensive spruce forests had shifted as far north as Alaska (Williams and others 2004). The remaining 3 species (S. cinereus, S. hoyi, and S. monticolus) may have arrived as early as 10 ka from south of the ice sheets, although expansion into tundra habitats may be much more recent, possibly only decades ago in response to recent rapid warming. These 3 forest species are commonly found in sympatry wherever their ranges overlap and fossil evidence supports this association further south through at least the Wisconsinan period (Kurten and Anderson 1980).
Virtually no fossil evidence is yet available from Alaska to support historical analogs to the present diverse community (Guthrie 2001). Although it is possible that similar communities existed during previous interglacial warm phases, it seems unlikely. Although a number of shrew species can be found in the tundra biome, very few are adapted for persistence in tundra through a glacial cycle. Only S. ugyunak (including other fragmented Beringian species of the cinereus complex) is found solely within tundra habitats. No other species within Alaska except S. tundrensis exhibits a genetic signature of persistence in the Beringian refugium. Similarly, other wide-ranging species through Eurasia have strong signals of expansion in western Beringia and little population structure (unpubl. data) indicating recent movement into this area.
Shrews provide a clear demonstration that climate change has a significant impact on both species richness and carrying capacity of the Arctic tundra biome through time. Considering the recent history of diversification among these shrews, there have likely been no analogous faunas in this area during previous glacial cycles (Edwards and others 2005; MacDonald 2010). Other small mammal species collected from the Seward Peninsula are perhaps more indicative of a true tundra community. Both M. miurus and L. trimucronatus are tundra-associated species, and M. oeconomus exhibits evidence of persistence in Beringia through climate cycling (Galbreath and Cook 2004). Myodes rutilus exhibits a signal of recent expansion through Beringia similar to S. minutissimus. Unlike shrews, forest associated rodent species have not expanded into open tundra at these study sites, further highlighting the complexity surrounding community turnover (MacDonald 2010). Although Arctic tundra can support an unusually high diversity of small mammals, it is uncertain how an assemblage with such disparate biogeographic histories will respond to future change. Further research should include expanded comparative genetic analyses of multiple faunal groups to address community change scenarios in the Arctic.
Field surveys in 2010 were made possible by financial support from the US Geological Survey's Alaska Regional Executive DOI on the Landscape Initiative (SL Talbot; Molecular Ecology Laboratory of the Alaska Science Center, Anchorage) and from JA Cook (Museum of Southwestern Biology, University of New Mexico) for curation costs associated with specimen archives and field equipment. Additional funding was provided through the US Geological Survey's Alaska Science Center Changing Arctic Ecosystems Initiative. Thanks to GK Sage and SL Talbot for shrew gene sequencing. Logistic and in-kind financial support was kindly provided by the National Park Service Arctic Network, in particular M Flamme, T Whitesell, and S Backensto. I extend special thanks to LH Zeglin and CR Dial for help with fieldwork. As a field crew we thank our pilot E Sieh (US Fish and Wildlife Service, Kotzebue) for safe navigation between sites. I thank RC Terry, JA Cook and SL Talbot for providing insightful comments. DW Nagorsen and EA Rickart kindly reviewed an earlier draft of the manuscript. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.
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Submitted 22 December 2011, accepted 3 April 2012. Corresponding Editor: Thomas Jung.
ANDREW G HOPE
US Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, AK 99508; firstname.lastname@example.org
TABLE 1. Sampling totals of shrews collected during summer 2010. Sites are listed in the order of sampling, coincident with longitude from east to west. Totals include only shrews collected during survey efforts. Trap nights indicate the number of Museum Special (MS) and pitfall (pits) traps set. Lake Tulilik Lake Isiak Aniralik Lake 17-22 Aug 22-26 Aug 26-31 Aug Sorex cinereus 0 4 13 Sorex hoyi 0 0 1 Sorex minutissimus 2 0 4 Sorex monticolus 8 11 0 Sorex tundrensis 0 8 10 Sorex ugyunak 17 39 23 Total 27 62 51 Trap nights (MS/pits) 700/700 600/800 605/900 Imik Lagoon Kuzitrin Lake 31 Aug-5 Sep 5-10 Sep Totals Sorex cinereus 19 14 50 Sorex hoyi 0 4 5 Sorex minutissimus 4 5 15 Sorex monticolus 0 9 28 Sorex tundrensis 6 11 35 Sorex ugyunak 2 12 93 Total 31 55 226 Trap nights (MS/pits) 700/900 700/950 3305/4250 TABLE 2. Comparison of predominant habitat associations and evolutionary and distributional dynamics among shrews found on the Seward Peninsula, based on previous studies. Times of occurrence are estimated possible limits. Time of arrival considers presence on the Seward Peninsula, AK, based on evidence from Kuzitrin Lake. LGM = Last Glacial Maximum. Sorex ugyunak Sorex cinereus Habitat Tundra Boreal Evolutionary Origin Nearctic Nearctic Earliest Occurrence in Alaska (years before present) ~ 130 k ~ 9 k Nearest Distribution Beringia southern North at LGM America Demographics expansion with northward expansion since LGM tundra with forest Latest arrival time < 130 k possibly recent (years before decades present) Order of arrival 1 4 Sorex hoyi Sorex monticolus Habitat Boreal Boreal Evolutionary Origin Nearctic Nearctic Earliest Occurrence in Alaska (years before present) ~ 9 k ~ 9 k Nearest Distribution southern North southern North at LGM America America Demographics northward expansion northward expansion since LGM with forest with forest Latest arrival time possibly recent possibly recent (years before decades decades present) Order of arrival 4 4 Sorex minutissimus Sorex tundrensis Habitat Generalist Generalist Evolutionary Origin Palearctic Palearctic Earliest Occurrence in Alaska (years before present) < 20 k < 130 k Nearest Distribution Far East Asia Beringia at LGM (West Beringia) Demographics eastward expansion local expansion since LGM through Beringia within Beringia Latest arrival time < 20 k < 130 k (years before present) Order of arrival 3 2
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|Author:||Hope, Andrew G.|
|Publication:||Northwestern Naturalist: A Journal of Vertebrate Biology|
|Date:||Sep 22, 2012|
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