552 P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 22001133 NORNTHorEthAeSaTsEteRrnN NNaAtuTrUaRliAstLIST 2V0o(4l.) :2505,2 N–5o5. 84 Changes in Capture Rates in a Community of Bats in New Hampshire during the Progression of White-nose Syndrome Paul R. Moosman, Jr.1,*, Jacques P. Veilleux2, Gary W. Pelton3, and Howard H. Thomas4 Abstract - Effects of white-nose syndrome (WNS) have mainly been assessed in bats at hibernacula, but this method may not be appropriate for species with poorly understood overwintering habits. We assessed effects of WNS on summer captures of Myotis leibii (Eastern Small-footed Bat), M. lucifugus (Little Brown Bat), M. septentrionalis (Northern Long-eared Bat), and Eptesicus fuscus (Big Brown Bat) in New Hampshire from 2005– 2011. Declines in rates and probability of capture varied among species but were greatest in the Myotis. Trends generally agreed with previous studies, except that declines in captures of Eastern Small-footed Bats were disproportionately higher than expected from winter estimates. Monitoring of Eastern Small-footed Bats during the non-hibernation period likely will help to clarify the effects of WNS on this uncommon species. Introduction White-nose syndrome (WNS) has caused precipitous declines in populations of several species of bats across much of the eastern US and Canada (Blehert et al. 2009, Turner et al. 2011). Mortality from WNS has been determined primarily through surveys of hibernating bats, but it remains to be determined how closely such estimates represent actual rates of population decline. This is a particular concern in species that are difficult to census during winter, such as Myotis leibii Audubon and Bachman (Eastern Small-footed Bat) and M. septentrionalis Trouessart (Northern Long-eared Bat). Both species are observed in low numbers during winter, and hibernate in cryptic locations, making it possible that visual surveys at hibernacula underestimate their populations (Best and Jennings 1997, Caceres and Barclay 2000, Saugey et al. 1993). Monitoring of bats during the non-hibernation period is an alternative method of assessing impacts of WNS on bats. Brooks (2011) and Dzal et al. (2011) detected substantial declines in acoustic activity of bats in the genus Myotis, most likely M. lucifugus LeConte (Little Brown Bats) and Northern Long-eared Bats, in New England. Additionally, Francl et al. (2012) compared relative abundance of bats captured in mist nets in West Virginia from 12 years before WNS, to data gathered the year after WNS was first observed in that state. They are the only authors to examine responses by Eastern Small-footed Bats, and their results suggest Eastern Small-footed Bat populations and those of 5 other species were reduced following the arrival of WNS (Francl et al. 2012). 1Virginia Military Institute, Lexington, VA 24450. 2Franklin Pierce University, Rindge, NH, 03461. 3US Army Corps of Engineers, Perkinsville, VT 05151. 4Fitchburg State University, Fitchburg, MA 01420. *Corresponding author - moosmanpr@vmi.edu. P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 553 Northeastern Naturalist Vol. 20, No. 4 Threats facing bats in the Northeast warrant further population monitoring during the non-hibernation period and, therefore, we assessed rates of capture in a community of bats that was dominated by Eptesicus fuscus Palisot de Beauvois (Big Brown Bat), Eastern Small-footed Bats, Little Brown Bats, and Northern Long-eared Bats, during the non-hibernation periods of 2005–2011, at a site in New Hampshire only 65–173 km from hibernacula affected by WNS during the earliest phases of the outbreak. We were particularly interested in comparing rates of capture in Eastern Small-footed Bats and Northern Long-eared Bats to those of Little Brown Bats, a species with better- documented responses to WNS (Frick et al. 2010). Site Description Research was conducted at Surry Mountain Lake, an impoundment of the Ashuelot River in Cheshire County, NH. The site was unique because it supported a community of bats that included Eastern Small-footed Bats, and it was the focus of annual mist-netting surveys beginning in 2005. In addition to the 4 focal species, the community included Lasiurus borealis Müller (Eastern Red Bat), L. cinereus Beauvois (Hoary Bat), and Perimyotis subflavus Cuvier (Tricolored Bat), all of which were captured too infrequently for analysis. Eastern Small-footed Bats used boulder-covered surfaces of Surry Mountain Dam and natural rock outcrops as diurnal roosts, and foraged in the surrounding forest. Some of the Big Brown Bats that we studied roosted in buildings ≈400 m from the dam. Roosting sites of Little Brown Bats and Northern Long-eared Bats were unknown, but presumably occurred in buildings and under exfoliating bark of trees nearby, respectively. The surrounding habitat was mainly contiguous, mixed-deciduous and coniferous forest, consisting of medium-aged secondary growth with some old-growth of Tsuga canadensis L. (Eastern Hemlock) and Pinus strobus L. (Eastern White Pine). Methods We captured bats using mist-nets (Avinet, Dryden, NY) that typically were 6–18 m wide and stacked 6–9 m high (each of these stacked systems are herein referred to as a single net). Nets were placed across roads or perpendicular to forest edges and 10–500 m from a large cluster of previously documented roosts of Eastern Small-footed Bats, with ≥30 m between nets. Nets were operated from 30 min before sunset until 4 h after sunset. Only data collected from 15 May–15 August were analyzed, because captured bats were likely to be residents and not migrants during this time. Data were obtained over 7 years on 99 calendar nights during which neither precipitation nor wind >4 km/h occurred within the netting period. Mean sampling intensity was 3.2 ± 0.2 (SE) nets deployed per visit. Visits were generally limited to 1–2 times per week, and we changed net locations every 1–2 visits; we used a pool of 40 potential locations to reduce the tendency for bats to become netshy. Bats were identified to species, fitted with a numbered aluminum band with rounded edges (Porzana Ltd., Birmingham, UK) on the forearm, and released at the site of capture. After the emergence of WNS, our methods included the decon554 P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 Northeastern Naturalist Vol. 20, No. 4 tamination protocols suggested by the US Fish and Wildlife Service (http://www. whitenosesyndrome.org/sites/default/files/resource/national_wns_final_6.25.12. pdf). Methods were approved by the New Hampshire Fish and Game Department and the Animal Care Committee of Fitchburg State University. The effects of WNS on the bat community were assessed in two ways, with date of visit as the sampling unit for both methods. In the first method, we pooled data into 1st (2005–2006), 2nd (2007–2009), and 3rd (2010–2011) periods of the disease. These categories were used because it was impossible to determine precisely when various species of bats at our site became exposed to WNS, and because it reduced effects of high inter-annual variation in capture success. We tested the effect of disease period on rates of capture using separate negative binomial models for each species. Parameter estimates were adjusted to reflect sampling intensity by including number of net-nights as an offset variable. Differences in rates of capture among the 3 periods were examined using pairwise comparisons with Bonferroni adjustments. In the second method, we tested for changes in the probability of capturing ≥1 individual per visit over the course of the study, using a separate logistic regression analysis for each species. Date and number of net-nights were used as covariates, and nightly capture results were coded into a dichotomous dependent variable, with no bats captured as “0” and ≥1 bat captured as “1.” Likelihood ratio tests were used to assess logistic models, with a forward selection process. Analyses were performed using SPSS 20.0 (IBM Corp., Armonk, NY) with α set at 0.05. Results During the 1st period of WNS, overall rate of capture at Surry Mountain Lake (mean ± SE) was 3.7 ± 0.7 bats/net-night. Species-specific rates during the 1st period were 1.4 ± 0.4 Big Brown Bats/net-night, 0.9 ± 0.2 Eastern Small-footed Bats/ net-night, 0.8 ± 0.3 Little Brown Bats/net-night, and 0.6 ± 0.2 Northern Long-eared Bats/net-night (Fig. 1). Overall rate of capture during the 3rd period of WNS was 1.0 ± 0.2 bats/net-night, a decline of 73% from the 1st period. This trend corresponded with reductions in captures of 98% for Little Brown Bats and Northern Long-eared Bats (< 0.1 bat/net-night), 68% for Eastern Small-footed Bats (0.3 ± 0.4 bat/netnight), and 49% for Big Brown Bats (0.7 ± 0.2 bat/net-night) by the 3rd period. Effects of period on capture rates were significant for Eastern Small-footed Bats (likelihood ratio χ2 = 17.9, d.f. = 2, P < 0.001), Northern Long-eared Bats (likelihood ratio χ2 = 34.8, d.f. = 2, P < 0.001), and Little Brown Bats (likelihood ratio χ2 = 40.0, d.f. = 2, P < 0.001), but capture rates of Big Brown Bats were statistically similar across disease periods (P = 0.08). Pairwise comparisons indicated capture rates for Eastern Small-footed Bats declined significantly following the 1st disease period (1st–2nd P = 0.026 and 1st–3rd P < 0.027), but were similar between the last two periods (P = 1.0). Rates of capture between the 1st and 2nd disease periods were similar for Northern Long-eared Bats (P = 0.36) and Little Brown Bats (P = 0.09), but declined significantly by the 3rd period in both species (Northern Long-eared Bat: 1st–3rd P = 0.007 and 2nd–3rd P < 0.001; Little Brown Bat: 1st–3rd P = 0.003 and 2nd–3rd P < 0.001). P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 555 Northeastern Naturalist Vol. 20, No. 4 Logistic regression analyses suggested that the probability of capturing at least 1 bat on a given visit remained similar over the study for Eastern Small-footed Bats (P = 0.92), but probability of capturing Big Brown Bats (omnibus χ2 = 15.4, d.f.=2, P < 0.001), Little Brown Bats (omnibus χ2 = 30.2, d.f. = 2, P < 0.001) and Northern Long-eared Bats (omnibus χ2 = 12.5, d.f. = 1, P ≤ 0.001) declined over time (Fig. 2). Including net-nights as a covariate significantly improved the logistic regression models for Big Brown Bats (change if term removed P < 0.001) and Little Brown Bats (P < 0.001), but not for Northern Long-eared Bats (P = 0.06). Discussion Rates of capture observed during the progression of WNS in New Hampshire suggest the disease caused large reductions in overall abundance of bats, but severity varied among species. Our data indicate declines in rates of capture were greatest in Little Brown Bats and Northern Long-eared Bats, intermediate in Eastern Smallfooted Bats, and least in Big Brown Bats. The declines appeared to happen later for Little Brown Bats and Northern Long-eared Bats than for Eastern Small-footed Bats. We did not assess abundance of a fifth species, Tricolored Bats, because they were rare in New Hampshire prior to WNS, but estimates from hibernacula suggest that the species has experienced exceptionally high rates of WNS-induced Figure 1. Mean (± SE) capture success in 4 species of bats during the progression of whitenose syndrome in New Hampshire. Asterisks indicate species with significant effects (P less than 0.001) across all periods of the disease. 556 P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 Northeastern Naturalist Vol. 20, No. 4 mortality (Langwig et al. 2012, Turner et al. 2011). Thus, the community of bats at Surry Mountain Lake likely had declined from 7 species before WNS to effectively 4 species (Big Brown Bat, Eastern Small-footed Bat, Eastern Red Bat, and Hoary Bat) by 2010–2011. Declines in capture rates that we observed largely agree with those presented in previous studies, suggesting populations of Little Brown Bats and Northern Longeared Bats experienced drastic declines in the Northeast following arrival of WNS, which were more severe than those experienced by Big Brown Bats (Brooks 2011, Dzal et al. 2011, Francl et al. 2012, Langwig et al. 2012, Turner et al. 2011, Wilder et al. 2011). There is less agreement among studies of Eastern Small-footed Bats. Our results were somewhat similar to those of Francl et al. (2012), who detected declines in Eastern Small-footed Bats (84%) that were comparable to those of Little Brown Bats (80%) and Northern Long-eared Bats (77%). In contrast, estimates from overwintering bats suggest lower rates of decline in Eastern Small-footed Bats (12%) than in other species affected by WNS (Turner et al. 2011). The reasons for these differences are unclear. They may reflect geographic variation in susceptibility to WNS or differential timing of its spread among populations, but we also suspect that censuses of hibernating bats have underestimated effects of WNS on Eastern Small-footed Bats. This is an important question that needs to be resolved quickly, particularly in light of the ongoing review of whether the Eastern Small- Figure 2. Declines in the predicted probability of capturing Big Brown Bats (black bars), Little Brown Bats (crosshatched bars), and Northern Long-eared Bats (white bars) during the progression of white-nose syndrome in New Hampshire. Data represent results of logistic regression models. Error bars show standard error of the mean. P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 557 Northeastern Naturalist Vol. 20, No. 4 footed Bat should be added to the federal list of endangered species (US Fish and Wildlife Service 2011). Interestingly, the probability of capturing at least 1 bat during a given night of sampling declined in all species except Eastern Small-footed Bats. This finding may be due to the placement of nets closer to roosts of Eastern Small-footed Bats than to those of other species. Thus, although the number of Eastern Small-footed Bats that were captured declined during the study, the remaining bats were caught relatively consistently. Traditionally, population monitoring has been based on censuses of hibernating or colony-roosting bats, in part due to concerns about bats becoming netshy (O’Shea and Bogan 2003, Weller 2007). However, net-shyness has mainly been linked with sampling the same location on consecutive nights (Robbins et al. 2008, Winhold and Kurta 2008). Our results and those of similar studies suggest annual mist-netting near important habitat features allows monitoring of bats outside of the hibernation period (Boyles and Robbins 2006, Perry 2011). In conclusion, our data indicate that populations of all three Myotis (M. leibii, M. lucifugus, and M. septentrionalis) at Surry Mountain Lake declined following arrival of WNS in the Northeast. Trends that we observed indicate that the effects of the disease on Little Brown Bats, Northern Long-eared Bats, and Big Brown Bats have been consistent with winter estimates, but hibernaculum surveys may underestimate the impact on Eastern Small-footed Bats. The continued existence of Eastern Small-footed Bats at Surry Mountain Lake as of 2011 was encouraging, but we are uncertain whether rates of mortality from WNS will allow the species to persist in the region. Identification and monitoring of additional populations of Eastern Small-footed Bats are needed, both to resolve this question and to inform conservation efforts at regional and local scales. Acknowledgments We thank J. Lewis and the rest of the US Army Corps of Engineers staff at Surry Mountain Lake for facilitating our work, and our many students who helped conduct field-work. Additionally, we are grateful to R. Humston for advice about statistical analyses, R.M. Brigham for comments on an early draft of our work, and anonymous reviewers for their help in revising this manuscript. Literature Cited Best, T.L., and J.B. Jennings. 1997. Myotis leibii. Mammalian Species 547:1–6. Blehert, D.S., A.C. Hicks, M. Behr, C.U. Meteyer, B.M. Berlowski-Zier, E.L. Buckles, J.T.H. Coleman, S.R. Darling, A. Gargas, R. Niver, J.C. Okoniewski, R.J. Rudd, and W.B. Stone. 2009. Bat white-nose syndrome: An emerging fungal pathogen? Science 323:227. Boyles, J.G., and L.W. Robbins. 2006. Characteristics of summer and winter roost trees used by Evening Bats (Nycticeius humeralis) in Southwestern Missouri. American Midland Naturalist 155:210–220. Brooks, R.T. 2011. Declines in summer bat activity in central New England 4 years following the initial detection of white-nose syndrome. Biodiversity Conservation 20:2537–2541. 558 P.R. Moosman, Jr., J.P. Veilleux, G.W. Pelton, and H.H. Thomas 2013 Northeastern Naturalist Vol. 20, No. 4 Caceres, M.C., and R.M.R. Barclay. 2000. Myotis septentrionalis. Mammalian Species 634:1–4. Dzal, Y., L.P. McGuire, N. Veselka, and M.B. Fenton. 2011. Going, going, gone: The impact of white-nose syndrome on the summer activity of the Little Brown Bat (Myotis lucifugus). Biology Letters 7:392–394. Francl, K.E., W.M. Ford, D.W. Sparks, and V.E. Brack, Jr. 2012. Capture and reproductive trends in summer bat communities in West Virginia: Assessing the impact of white-nose syndrome. Journal of Fish and Wildlife Management 3:33–42. Frick, W.F., J.E. Pollock, A.C. Hicks, K.E. Langwig, D.S. Reynolds, G.G. Turner, C.M. Butchkoski, and T.H. Kunz. 2010. An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682. Langwig, K.E., W.F. Frick, J.T. Bried, A.C. Hicks, T.H. Kunz, and A.M. Kilpatrick. 2012. Sociality, density-dependence, and microclimates determine the persistence of populations suffering from the novel fungal disease, white-nose syndrome. Ecology Letters 15:1050–1057. O’Shea, T.J., and M.A. Bogan (Eds.). 2003. Monitoring trends in bat populations of the United States and territories: Problems and prospects. US Geological Survey, Biological Resources Discipline, Information and Technology. Report USGS/BRD/ITR–2003- 0003. 274 pp. Perry, R.W. 2011. Fidelity of bats to forest sites revealed from mist-netting recaptures. Journal of Fish and Wildlife Management 2:112–116. Robbins, L.W., K.L. Murray, and P.M. McKenzie. 2008. Evaluating the effectiveness of the standard mist-netting protocol for the endangered Indiana Bat (Myotis sodalis). Northeastern Naturalist 15:275–282. Saugey, D.A., V.R. McDaniel, D.R. England, M.C. Rowe, L.R. Chandler-Mozisek, and B.G. Cochran. 1993. Arkansas range extensions of the Eastern Small-footed Bat (Myotis leibii) and Northern Long-eared Bat (Myotis septentrionalis), and additional county records for the Silver-haired Bat (Lasionycteris noctivagans), Hoary Bat (Lasiurus cinereus), Southeastern Bat (Myotis austroriparius), and Rafinesque's Big-eared Bat (Plecotus rafinesquii). Proceedings of the Arkansas Academy of Science 47:102–106. Turner, G.G., D.M. Reeder, and J.T.H. Coleman. 2011. A five-year assessment of mortality and geographic spread of white nose syndrome in North American bats and a look into the future. Bat Research News 52:13–27. US Fish and Wildlife Service. 2011. 90-day finding on a petition to list the Eastern Smallfooted Bat and Northern Long-Eared Bat as threatened or endangered. Federal Register 76:38,095-38,106. Weller, T.J. 2007. Assessing population status of bats in forests: Challenges and opportunities. Pp. 263–291, In M.J. Lacki, J.P. Hayes, and A. Kurta (Eds.). Bats in Forests: Conservation and Management. John Hopkins University Press, Baltimore, MD. 329 pp. Wilder, A.P., W.F. Frick, K.E. Langwig, and T.H. Kunz. 2011. Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biology Letters 7:950–953. Winhold, L., and A. Kurta. 2008. Netting surveys for bats in the Northeast: Differences associated with habitat, duration of netting, and use of consecutive nights. Northeastern Naturalist 15:263–274.