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New Records for Sorex hoyi (American Pygmy Shrew) in Alabama
Helen A. Czech, Allison A. Bohlman, and William B. Sutton

Southeastern Naturalist, Volume 16, Issue 3 (2017): 464–472

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Southeastern Naturalist H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 464 2017 SOUTHEASTERN NATURALIST 16(3):464–472 New Records for Sorex hoyi (American Pygmy Shrew) in Alabama Helen A. Czech1,*, Allison A. Bohlman1, and William B. Sutton2 Abstract – We report the first records of Sorex hoyi (American Pygmy Shrew) for Lawrence County, AL. We discovered 5 specimens in a specimen lot stored at Alabama A&M University. The shrews were incidental captures collected from pitfall traps used to study amphibian and reptile communities in the William B. Bankhead National Forest. A follow- up survey at the same sites during December 2015 resulted in the capture of 1 adult American Pygmy Shrew. Surveys at additional sites in Madison, Lawrence, and Winston counties, AL, during 2015–2016 yielded no further specimens. These records are 120 km southwest of the nearest records in Jackson County, AL, and expand the known southernmost edge of the geographic range by 35 km. Introduction Sorex hoyi Baird (American Pygmy Shrew) is one of the smallest mammals in North America and also one of the least known, despite a distribution that includes Alaska and much of Canada and the Eastern US (Long 1974, Whitaker and Hamilton 1998). The subspecies S. h. winnemana (Preble) (Southern Pygmy Shrew) inhabits an area from southern Illinois to northeastern Alabama (Diersing 1980, Laerm et al. 1996), where it is uncommon, but occurs in a wide range of habitats and at elevations from <5 m to >1600 m (Webster and Spivey 2001). Although the subspecies is considered a habitat generalist, it is most often collected in moderate to xeric early successional stage sites with upland hardwood, mixed pine–hardwood, or intensely managed yellow pine communities (Laerm et al. 2000). At the southernmost periphery of its distribution, the species is considered rare and poorly understood. In Alabama, the Southern Pygmy Shrew is listed as a species of greatest conservation need, with a protection ranking of priority 2 (P2; high conservation concern), due to its limited state-wide range and rarity (ADCNR-DWFF 2016). First collected in Alabama in 1995 (Laerm et al. 1996), the species was known only from northeastern Jackson County, where it had been detected at sites between 336 m and 534 m in elevation, and in deciduous forest communities with canopies dominated by Quercus spp. (oaks), Acer spp. (maples), Carya spp. (hickories), and Liriodendron tulipifera L. (Yellow-Poplar). Understory trees included Vaccinium spp., Viburnum spp., Oxydendrum arboreum (L.) DC. (Sourwood), Cornus florida L. (Flowering Dogwood), Cercis canadensis L. (Eastern Redbud), and Sassafras 1Department of Biological and Environmental Sciences, 100 Drake Drive, Room 101 ARC Building, Alabama A&M University, Normal, AL 35762. 2Department of Agricultural and Environmental Sciences, Tennessee State University, Nashville, TN 37209. *Corresponding author - helen.czech@aamu.edu. Manuscript Editor: Andrew Edelman Southeastern Naturalist 465 H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 albidum (Nutt.) Nees (Sassafras) (Felix et al. 2009, Laerm et al. 1996, Moss 2015). Soils ranged from riparian sand (Moss 2015) to well-drained stony and gravelly loam or clays (Felix et al. 2009). Most were captured within the current boundary of the James D. Martin–Skyline Wildlife Management Area. Researchers have continued to detect Southern Pygmy Shrews in Jackson County; the most recent collections were made in 2014 (Hitch et al. 2008, Moss 2015, NCSM 2015). Surveys have yielded too few specimens of this species to be able to estimate habitat associations (Hitch et al. 2008, Moss 2015). Due to the lack of knowledge regarding the status and distribution of the Southern Pygmy Shrew in Alabama, we sought to determine if the species was present elsewhere in the state by examining specimens and performing field surveys in regions where habitats were similar to those of Jackson County. Field-site Descriptions We conducted sampling in Madison, Lawrence, and Winston counties, AL. This region of Alabama experiences yearly temperatures ranging from an average low of 10 °C to an average high of 22 °C. The average yearly precipitation is about 1450 mm (SERCC 2012). Sites in Lawrence and Winston counties were within the William B. Bankhead National Forest (BNF) (34º20'24''N, -87º20'24''W). The 140,126-ha forest is in the Dissected Plateau ecoregion of the Southwestern Appalachians (Griffith et al. 2001) and in the Warrior Basin physiographic region of the Cumberland Plateau. The terrain is strongly sloping, with occasional sandstone cliffs, steepsided gorges, and elevations nearing 300 m. About half of the BNF is composed of hardwood forests dominated by oaks and hickories and the other half by Pinus taeda L. (Loblolly Pine). Mixed mesophytic forests composed of maples, Fagus grandifolia Ehrh. (American Beech), Tsuga canadensis (Eastern Hemlock), and Yellow-Poplar are in coves, along streams, and on north- and east-facing slopes (Gaines and Creed 2003). Sites in Madison County were within the Plateau Escarpment Ecoregion of the Southwestern Appalachians and the Eastern Highland Rim ecoregion of the Interior Plateau (Griffith et al. 2001) and included the Jackson County Mountains physiographic region of the Cumberland Plateau and the Tennessee Valley physiographic region of the Highland Rim. Sites were near the city of Huntsville, AL (34º43'48''N, -86º35'6''W). Terrain in the Cumberland Plateau region is strongly shaped by underlying karst geology, and is steeply sloping with limestone outcroppings and elevations nearing 500 m. Forests have canopies dominated by oaks, hickories, and maples as well as Fraxinus spp. (ash), and Juniperus virginiana L. (Eastern Red Cedar). Mixed mesophytic forests composed of maples, Aesculus spp. (buckeyes) and Tilia spp. (basswoods) are in coves and on sheltered north- and east-facing slopes. Terrain in the Highland Rim region is rolling, with elevations nearing 300 m, and is dominated by row-crop and pasture agriculture. Southeastern Naturalist H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 466 Methods We examined small-mammal specimens stored at Alabama A&M University (AAMU) prior to field sampling. The specimens were collected during 2005–2008 from 15 sites in Lawrence County and 4 sites in Jackson County. We identified shrew specimens to genus by counting the number of upper unicuspid teeth, as seen in lateral and ventral views (Whitaker and Hamilton 1998). We did not identify to species shrews of the cryptic genus Blarina or mice of the genus Peromyscus because our study sites were in a region where the ranges of B. carolinensis (Bachman) (Southern Short-tailed Shrew) and B. brevicauda (Say) (Northern Short-tailed Shrew) potentially overlap (Best and Dusi 2014) and P. leucopus (Rafinesque) (White-footed Mouse) and P. gossypinus (Le Conte) (Cotton Mouse) overlap. These pairs cannot be reliably separated without using DNA sequencing. We distinguished Southern Pygmy Shrews from other longtailed Sorex shrews by the miniscule size of their 3rd and 5th upper unicuspids (Diersing 1980, Junge and Hoffman 1981). We surveyed Madison County, which was not represented among the specimens, during April–October 2015 using 250 2-L pitfall traps. We employed small traps to exclude non-target Murids. Traps were distributed equally across 5 sites with upland forest, cove forest, Loblolly Pine, and field habitat types represented at each site. We opened pitfall traps for 4 consecutive nights and checked traps daily. We placed a moistened sponge, cotton batting, and a mixture of sunflower seeds, dried mealworms, and dog kibble in each trap to provide water, shelter, and food (Shonfield et al. 2013). We photographed, identified, and measured all small-mammal captures and collected, identified, and deposited mortalities at AAMU. We surveyed 16 sites in Lawrence County using fifty-four 19-L pitfall traps. We placed 18 traps in stands of Loblolly Pine, 6 in pine-hardwood, 6 in oak-hickory, and 24 in riparian forest. We also utilized sixteen 19-L pitfall traps installed at 4 sites in Winston County. Four traps were in stands of oak–hickory, 4 in Loblolly Pine, and 8 in riparian forest. We opened arrays during May–July 2015, December 2015, June–August 2016, and December 2016. We followed the same trapping protocols as for sites in Madison County. Results A collection dated April 2008 from Lawrence County contained 5 adult Southern Pygmy Shrews. The shrews were incidentally captured in pitfall traps that were being used for a study examining the effects of differing intensities of timber harvesting and prescribed burning on amphibian and reptile communities (Sutton 2010). Four were captured in Loblolly Pine stands that were 20–50 years of age with south–southwest-facing aspects, and 1 was captured in a pine–hardwood stand with a northwest-facing aspect. Sites were at 269–279 m elevation. The Loblolly Pine stands were on a 3-y burn rotation; the most recent treatments occurred in 2007 and 2012. Harvesting of timber in the stands ranged from none to a partial removal that occurred in 2006. Southeastern Naturalist 467 H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 We resurveyed these 4 sites in December 2015 and captured 1 adult Southern Pygmy Shrew in 96 trap-nights in a lightly harvested Loblolly Pine stand with under- and midstory canopies dominated by Acer rubrum L. (Red Maple) and underlain by sandy loam soil. The site had a southwest-facing aspect and an elevation of 277 m. The mean total length of the shrews (n = 6) captured in Lawrence County was 64 mm ± 0.2 SE (range = 56–74 mm), which is smaller than had been previously reported for the Southern Pygmy Shrew. Researchers have found similar trends with other peripheral populations of shrews (Felix et al. 2009), and the decrease in size may be due to a combination of the size of available food and the presence of heterospecific soricids (Huggins and Kennedy 1989). We also captured 2 short-tailed shrews during this trapping period. No Southern Pygmy Shrews were captured at the other 12 sites in Lawrence County during 274 trap-nights or at sites in Winston County during 160 trap-nights. We captured 4 short-tailed shrews, 2 Sorex longirostris Bachman (Southeastern Shrew), 13 Peromyscus spp. (deer mice), 1 Ochrotomys nuttalli (Harlan) (Golden Mouse), and 1 Scalopus aquaticus (L.) (Eastern Mole). Our Madison County surveys yielded no Southern Pygmy Shrews during 6965 trap-nights. We captured 22 individuals of 3 shrew species including 15 short-tailed shrews, 1 Southeastern Shrew, and 6 Cryptotis parva Say (North American Least Shrew). The latter 2 shrew species had not been previously documented in the county. Cricetid captures included 2 Microtus pinetorum (Le Conte) (Woodland Vole) and 1 M. ochrogaster (Wagner) (Prairie Vole). Mortality rates for shrews were between 33% and 100%, with the lowest rates among North American Least Shrews and highest among Sorex spp. The mortality rate for all species captured during the study was greatest in traps that flooded following heavy rainfall. Discussion The archived specimens we examined during this study were incidental captures found in traps set to capture amphibians, reptiles, and insects. We recommend that researchers consider identifying small-mammal bycatch present in pitfall traps (and vice versa). Edwards and Jones (2014) and Pearce et al. (2005) explored these issues and suggested techniques for preventing bycatch, when preferred. Bycatch data could assist with the discovery of populations of rare and uncommon species. These data would be integral to the larger goal of conserving and managing smallmammal species biodiversity in the southern Appalachians. There remain large gaps in the known ranges of many small mammals (Campbell et al. 2010) and a continued need for biotic surveys in the southeastern US (Felix et al. 2009). Our records for the Southern Pygmy Shrew are 120 km southwest of those in Jackson County and expand the southernmost edge of the range by 35 km (Fig. 1). Although the habitat composition and elevation of sites in the BNF differ from those found in Jackson County, the Southern Pygmy Shrew is a well-documented habitat generalist found at a wide range of elevations. However, because surveys in Madison County failed to detect the species, the population in the BNF may have Southeastern Naturalist H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 468 a disjunct distribution. Much of the trapping in Madison County took place when S. hoyi may not have been active above ground due to thermal and moisture limits (Best and Dusi 2014, Feldhamer et al. 1993) which could have resulted in no captures. Additionally, we did not trap during November–March, which is when the subspecies was almost exclusively captured in western Kentucky and Tennessee (Feldhamer et al. 1993). In Alabama and Georgia, Southern Pygmy Shrews were captured during all months, with peak captures occurring in June, September, and November, which is similar to what was observed by McCay et al. (1998) in Georgia and North Carolina. These records suggest that patterns of Southern Pygmy Shrew activity vary across the southeastern US and may be site- or region-specific. Laerm et al. (1999) cautioned against making assumptions regarding the distribution of poorly known and uncommon soricids, and Laerm et al. (1994) considered the Southern Pygmy Shrew to be widespread, but nowhere abundant. However, nonfederal forests in Alabama are highly fragmented (Li et al. 2009), and the region located between Jackson County and the BNF experienced a 100–600% net Figure 1. Distributional records for Sorex hoyi (American Pygmy Shrew) in Alabama and adjacent regions. Locations obtained from digitized museum records, state-record databases, and this study are depicted. The white circles with black centers indicate new records reported in this study from Alabama A&M University collections and pitfall traps. Black circles indicate records obtained from the Alabama Department of Conservation and Natural Resources, the Georgia Museum of Natural History, the North Carolina State Museum of Natural Sciences, the Sam Noble Oklahoma Museum of Natural History, the Tennessee Department of Environment and Conservation, and the University of Tennessee-Chattanooga, Mammals Collection, Natural History Museum. Southeastern Naturalist 469 H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 addition of urban areas during the period 1982–2010 (Rahman 2014). Therefore, the Southern Pygmy Shrew population in the BNF may be isolated and at the periphery of the geographic range of the species. Local populations of small-sized Sorex spp. are hypothesized to be highly vulnerable to extirpation (Hanski 1994), and even when a species is geographically widespread, peripheral populations can be valuable for conservation (Lesica and Allendorf 1995). Genetic and morphological analysis could elucidate if the population is distinct. The Southern Pygmy Shrew is a species of high conservation concern in Alabama; thus, it is important to have an accurate understanding of the distribution, habitat use, and abundance of the species (ADCNR-DWFF 2016). In the southern Appalachians, negative impacts to Southern Pygmy Shrew populations have not been found following low-intensity restorative and fuel-reducing prescribed burns and partial timber harvests (Ford and Rodrigue 2001, Ford et al. 1999, Greenberg et al. 2007). However, forest disturbances, such as high-intensity prescribed burns and clearcutting, and ground-disturbing actions such as road creation and patch cuts, may have a serious impact on Pygmy Shrew populations (Beauvais and Mc- Cumber 2006, Greenberg et al. 2007) due to their short life span of ~1 year, low reproductive rate of a single litter (Long 1974), home ranges of less than 0.5 ha, and low dispersal rates (Beauvais and McCumber 2006). In Montana, 2–3-month-old Pygmy Shrews captured in sites with complete overstory removal showed increased morphological variations in their lower mandibles (Badyaev and Foresman 2004). This stress-induced change may be beneficial when habitat alterations change the composition of local prey and the novel jaw morphology allows for the exploitation of previously unavailable prey. Since the early 2000s, the US Forest Service (USFS) has managed the BNF with the immediate goal of reducing fuel loads and treating areas damaged by Dendroctonus frontinalis Zimmermann (Southern Pine Beetle) and with the long-term goal of restoring forest and plant community types that were once common throughout the region. To meet these goals, thinning and prescribed burning have been used along with the restoration of Pinus echinata Mill. (Shortleaf Pine)–Andropogoninae spp. (bluestem grasses) woodlands (Addor and Birkhoff 2004). Prescribed burning and heavy and light thinning occurred at sites in the BNF where Southern Pygmy Shrews were captured. Sites are also located in areas where the management goal is hardwood restoration. More research is needed to assess the impacts of these activities on the life history, abundance, and distribution of this Alabama species of high conservation concern. Acknowledgments We thank field technician Jessica Billings. Patience Knight was invaluable during trap installation. H. Howell, R. Borthwick, K. Burns, and AAMU undergraduate students provided assistance in the field. We greatly appreciate W. Stone for facilitating the grantapplication process and research activities. This material is based upon work supported by the Alabama Division of Wildlife and Freshwater Fisheries Cooperative Endangered Species Conservation Fund under Traditional Section 6 Grant Project 183, the National Science Southeastern Naturalist H.A. Czech, A.A. Bohlman, and W.B. Sutton 2017 Vol. 16, No. 3 470 Foundation under HBCU-UP Grant No. TIP-1437001, and through the Department of Biological and Environmental Sciences at AAMU. Thank you to Y. Wang and C. Schweitzer for granting access to and use of trapping arrays, A. Cantrell for site suggestions, L. Gardner and K. Ward for access to specimens, and N. Sharp for identification verification. We are grateful to the Georgia Museum of Natural History (N. Castleberry and B. Freeman) for sharing data on specimens. We thank the Forever Wild Land Trust Program, the Land Trust of North Alabama (A. Prewett), and the AAMU Winfred A. Thomas Agricultural Research Station (E. Cebert) for allowing research to be performed on their properties. Dawn Lemke and D. Andy Scott provided helpful comments on an early draft. This research was conducted under the Alabama Department of Conservation and Natural Resources collecting permits #8202, 8172, 8855, and 8918. Literature Cited Addor, M.L., and J. Birkhoff. 2004. Bankhead National Forest health and restoration initiative: Final report. National Resources Leadership Institute. Ra leigh, NC. 61 pp. Alabama Department of Conservation and Natural Resources - Division of Wildlife and Freshwater Fisheries (ADCNR-DWFF). 2016. Alabama Wildlife Action Plan. Available online at http://www.outdooralabama.com/sites/default/files/AL%20SWAP%20FINAL %20POST- REVIEW%2004-22-2016.pdf. Accessed 4 April 2017. Badyaev, A.V., and K.R. 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