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Unusual Bat Behavior During Winter in Great Smoky Mountains National Park
James A. Carr, Riley F. Bernard, and William H. Stiver

Southeastern Naturalist, Volume 13, Issue 2 (2014): N18–N21

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2014 Southeastern Naturalist Notes Vol. 13, No. 2 N18 J.A. Carr, R.F. Bernard, and W.H. Stiver Unusual Bat Behavior During Winter in Great Smoky Mountains National Park James A. Carr1,*, Riley F. Bernard2, and William H. Stiver1 Abstract - Between December 2012 and April 2013, bats were observed flying during daylight hours throughout the Great Smoky Mountains National Park. Although some bats displayed typical foraging and drinking behavior, others appeared sick or incapable of flying, some were flying erratically, and one collided with a hiker. These observations tended to be reported on warmer-than-average days. Nine bats were collected and tested negative for rabies; 6 that were tested for White-nose Syndrome (WNS) via histology were all diagnosed as WNS positive. An additional 6 bats that were not tested for rabies were also WNS positive. We hypothesize bats were becoming increasingly active and emerging from hibernacula due to WNS. Sixteen known caves and 2 mine complexes serve as wintering habitat for bats within Great Smoky Mountains National Park (GRSM), which is situated on the border of North Carolina and Tennessee. White Oak Blowhole Cave (WOBC) is critical habitat for the endangered Myotis sodalis Miller and Allen (Indiana Bat) and is the largest known hibernaculum for the species in Tennessee (USFWS 2007). Since 1974, the population of Indiana Bats in WOBC has been routinely surveyed to monitor recovery efforts for the species. The 2 GRSM mine complexes provide winter habitat for Corynorhinus rafinesquii Lesson (Rafinesque’s Big-eared Bat), a species of concern in North Carolina (USFWS 2006). Since 1991, the mines have been routinely surveyed to monitor the population of Rafinesque’s Big-eared Bats. In 2009, the other 15 GRSM caves also were surveyed to determine winter bat use (Nolfi 2011). Previous bat surveys in GRSM provided baseline data for the 7 species of bats (Indiana Bat, M. lucifugus Le Conte [Little Brown Bat], M. septentrionalis Trouessart [Northern Long-eared Bat], M. leibii Audubon and Bachman [Eastern Small-footed Bat], Eptesicus fuscus Beauvois [Big Brown Bat], Perimyotis subflavus Cubier [Tri-colored Bat], and Rafinesque’s Big-eared Bat) known to hibernate in GRSM caves and mines before the emergence and rapid spread of white-nose syndrome (WNS). WNS is a novel disease caused by the newly described fungus, Pseudogymnoascus destructans (Blehert et al. 2011, Minnis and Lindner 2013). Lesions associated with P. destructans have been found to cause increased frequency of arousal from torpor, possibly leading to dehydration, electrolyte imbalance, and critical loss of fat stores necessary to survive winter hibernation (Cryan et al. 2010, 2013; Lorch et al. 2011, Reeder et al. 2012; Warnecke et al. 2012, 2013). In the northeastern US, mortality in some bat colonies infected with WNS has exceeded 90% in a single season (Frick et al. 2010). During 2010, P. destructans was found on a Little Brown Bat within a GRSM cave; however, no bats showed obvious visible signs of WNS. By 2011, 1 Tri-colored Bat and 2 Little Brown Bats at GRSM were confirmed, via histology, with WNS. Beginning in late December 2012, GRSM wildlife biologists began receiving reports from park visitors of unusual daytime activity of bats in various regions of GRSM. The most commonly reported observation involved bats exhibiting lethargic, foraging-like flight. On 14 January 2013, GRSM staff issued a press release to address potential public health 1Great Smoky Mountains National Park, 107 Park Headquarters Road, Gatlinburg, TN 37738. 2Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996. *Corresponding author - james.a.carr@aphis.usda.gov. Manuscript Editor: Renn Tumlison Notes of the Southeastern Naturalist, Issue 13/2, 2014 N19 2014 Southeastern Naturalist Notes Vol. 13, No. 2 J.A. Carr, R.F. Bernard, and W.H. Stiver concerns regarding exposure to sick bats and asked park patrons to continue reporting any unusual bat behavior. Subsequent to the press release, there were a substantial number of reports of bats out during the day. Some reports were of bats appearing to forage normally and some described bats flying erratically or struggling on the ground. Ten bats found on the landscape throughout GRSM were collected; 8 were euthanized, 2 were found dead, and all were sent for rabies and WNS testing to the National Park Service (NPS) Wildlife Health Branch in Ft. Collins, CO. The 8 bats that were euthanized were found flailing in the leaf litter and displayed severe dehydration of wing and tail membranes, holes in wings, and visible white fungus (Table 1). Days with reports of unusual bat activity (n = 31 between 28 December 2012 and 15 April 2013) were significantly warmer (11.42 ± 0.75 °C) than all other days (7.30 ± 1.20 °C) within that same time period (2-sample t-test: t-ratio = 2.89, P = 0.006). We hypothesized that the abnormal behaviors are due to infection by WNS. Seven of the 10 bats collected from the landscape were found at sites of considerable distance from known hibernacula, including one Little Brown Bat discovered approximately 40 km (25 miles) from the nearest known hibernaculum. Since the discovery of WNS within the GRSM cave and mine complex, biologists expected to find significant mortality within the caves during the winter 2013 census. In many northern caves, significant mortality tends to occur in the two years following discovery of P. destructans in the hibernaculum (Kunz and Reichard 2010). During the winter of 2013, we did not observe any drastic changes in overall bat numbers in any cave or mine within Table 1. Bats collected from the landscape and in caves around Great Smoky Mountains National Park during the winter of 2012–2013 and submitted for rabies and WNS testing. Average temperature (15-minute intervals) was taken from an Onset temperature/relative humidity HOBO meter located at White Oak Blowhole Cave within the park. MY spp. = Myotis species, PESU = Perimyotis subflavus, MYLU = Myotis lucifugus, MYSO = Myotis sodalis, MYLE = Myotis leibii. Avg. Temp. Where Rabies White-nose Date (°C) Species Sex found Status results results 2/1/13 -2.25 MY spp. ? Cave Found dead Not tested Not tested 2/1/13 -2.25 PESU M Cave Found dead Not tested Positive 2/1/13 -2.25 PESU ? Cave Found dead Not tested Positive 2/8/13 6.09 PESU F Landscape Found dead Negative Positive 2/9/13 3.70 PESU M Cave Found dead Not tested Not tested 2/9/13 3.70 PESU M Cave Found dead Not tested Not tested 2/9/13 3.70 PESU M Cave Found dead Not tested Not tested 2/9/13 3.70 PESU M Cave Found dead Not tested Positive 2/9/13 3.70 PESU M Cave Found dead Not tested Not tested 2/9/13 3.70 PESU M Cave Found dead Not tested Not tested 2/10/13 8.18 PESU M Landscape Euthanized Negative Positive 2/11/13 10.38 MYLU M Landscape Euthanized Negative Positive 2/12/13 5.50 PESU M Landscape Euthanized Negative Positive 2/15/13 3.67 MYSE M Landscape Euthanized Not tested Positive 2/20/13 0.15 PESU M Landscape Found dead Not tested Positive 2/20/13 0.15 PESU M Cave Found dead Not tested Positive 2/20/13 0.15 PESU M Cave Euthanized Negative Positive 3/8/13 2.54 MYSO M Landscape Euthanized Negative Positive 3/19/13 7.59 MYSO M Landscape Euthanized Negative Not tested 3/30/13 9.27 MYLE M Landscape Euthanized Negative Not tested 3/31/13 11.75 PESU F Landscape Euthanized Negative Not tested 2014 Southeastern Naturalist Notes Vol. 13, No. 2 N20 J.A. Carr, R.F. Bernard, and W.H. Stiver the GRSM complex. We collected 11 bats found dead or dying while clinging to cave gates and/or rock features outside the entrances. Of these, 10 were Tri-colored Bats (9 males and 1 individual too deteriorated for sex determination) and 1 Myotis spp. (too deteriorated for sex or species determination). Ten bats (5 Tri-colored Bats, 2 Indiana Bats, 1 Little Brown Bat, 1 Northern Long-eared Bat, and 1 Eastern Small-footed Bat) were collected from the landscape. No bats from mines were sent in for testing. All specimens collected from caves and the landscape (n = 21) were sent to the NPS Wildlife Health Branch for necropsy. Nine of the bats were tested for rabies, and all were negative. Twelve bats (including 6 of the 9 bats screened for rabies) were tested for WNS via histology, with each of them determined to be WNS positive (Table 1). In Tennessee, erratic behavior of bats on the landscape during winter appears to be unique to GRSM. Although approximately 65 caves and mines were surveyed during winter 2013 in Tennessee, GRSM was the only karst area within the state with bats documented exhibiting noticeable erratic behavior (C. Holliday, The Nature Conservancy, Nashville, TN, 2013 unpubl. data). One passive acoustic detector (Anabat II Detector, Titley Scientific ®) has been deployed near the entrance of WOBC (a WNS+ cave within the park) over the last 2 years to measure winter activity of bats. WOBC is the largest known Indiana Bat hibernaculum in Tennessee, and also contains Little Brown Bats, Northern Long-eared Bats, and Tri-colored Bats. Activity measurements based on the number of bat calls per hour have highlighted several interesting trends. Bats in GRSM remained active throughout the day Figure 1. Comparison of bat activity and temperature between winters 2012 and 2013 at WOBC in GRSM. Only data from January–April are shown. Bat activity (solid lines) as determined by acoustic monitoring is represented on the left Y-axis and temperature (hashed lines) on the right Y-axis. These data are part of a long-term multi-cave monitoring project by R . Bernard. N21 2014 Southeastern Naturalist Notes Vol. 13, No. 2 J.A. Carr, R.F. Bernard, and W.H. Stiver during winter, with peak activity an hour after sunset. Although activity levels increased on warm nights, bat activity has been detected on nights with temperatures reaching ≤5 °C (Figure 1; R. Bernard, University of Tennessee, Knoxville, TN, unpubl. data). Daytime winter bat activity at this cave during winter 2012–2013 shows an increase compared to the previous year, indicating an increase in activity possibly from disturbance due to P. destructans (R. Bernard, unpubl. data). Continued monitoring efforts within the GRSM complex will aid in determining if increased daytime activity of bats i s due to WNS. Acknowledgments. We thank Kevin Castle and Joy O’Keefe for providing editorial guidance during the writing of this manuscript, and Cory Holliday for input relating to winter activity of bats throughout Tennessee. We thank the National Park Service Wildlife Health Branch in Fort Collins, CO, for necropsy through an agreement with the Colorado State University Veterinary Diagnostic Laboratory. This project was funded in part by the Basically Bats Wildlife Conservation Society, Inc. WNS Student Research Grant. Literature Cited Blehert, D.S., J.M. Lorch, A.E. Ballmann, P.M. Cryan, and C.U Meteyer. 2011. Bat white-nose syndrome in North America. Microbe 6:267–273. Cryan, P.M, C. Meteyer, J. Boyles, and D. Blehert. 2010. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biology 8:135. Cryan, P.M., C. Meteyer, D. Blehert, J. Lorch, D. Reeder, G. Turner, J. Webb, M. Behr, M. Verant, R. Russell, and K. Castle. 2013. Electrolyte depletion in white-nose syndrome bats. Journal of Wildlife Diseases 49:398–402. Frick, W.F., J. Pollack, A. Hicks, K. Langwig, D. Reynolds, G. Turner, C. Butchkoski, and T. Kunz. 2010. An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682. Kunz, T.H., and J.D. Reichard. 2010. Status review of the Little Brown Myotis (Myotis lucifugus) and determination that immediate listing under the Endangered Species Act is scientifically and legally warranted. Available online at http://www.bu.edu/cecb/files/2010/12/Final-Status-Review. pdf. Accessed 21 October 2013. Lorch, J.M. , C. Meteyer, M. Behr, J. Boyles, P. Cryan, A. Hicks, A. Ballmann, J. Coleman, D. Redell, D. Reeder, and D. Blehert. 2011. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376–378. Minnis, A.M., and D.L. Lindner. 2013. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biology 117:638–649. Nolfi, D.C. 2011. National Park Service cave and karst resources management case study: Great Smoky Mountains National Park. M.Sc. Thesis. Western Kentucky University, Bowling Green, KY. 270 pp. Reeder, D.M., C.L. Frank, G.G. Turner, C.U. Meteyer, A. Kurta, E.R. Britzke, M.E. Vodzak, S.R. Darling, C.W. Stihler, A.C. Hicks, R. Jacob, L.E. Grienseisen, S.A. Brownlee, L.K. Muller, and D.S. Blehert. 2012. Frequent arousals from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7:e38920. United States Fish and Wildlife Service (USFWS). 2006. The US Fish and Wildlife Service’s county species list for North Carolina. Asheville, NC. 77 pp. USFWS. 2007. Indiana Bat (Myotis sodalis) draft recovery plan: First revision. Fort Snelling, MN. 258 pp. Warnecke, L., J.M. Turner, T.K. Bollinger, J.M. Lorch, V. Misra, P.M. Cryan, G. Wibbelt, D.S. Blehert, and C.K.R. Willis. 2012. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proceedings of the National Academy of Sciences 109:6999–7003. Warnecke, L., J.M. Turner, T.K. Bollinger, V. Misra, P.M. Cryan, D.S. Blehert, G. Wibbelt, and C.K.R. Willis. 2013. Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality. Biology Letters 9:20130177.