Abstract

The northern long-eared bat Myotis septentrionalis was discovered in coastal North Carolina in 2007. Work began in 2015 to document the species' distribution and behavior in eastern North Carolina, and the known range of the species has expanded from 4 coastal counties to 19. Captures occurred in all months of the year and mostly occurred in or adjacent to wetland forest. Captures occurred exclusively in the Middle Atlantic Coastal Plain ecoregion of the state, and the species has not been documented in the Southeastern Plains or Piedmont ecoregions. The lack of captures in the middle of the state suggests spatially disjunct populations in North Carolina. The bats were observed to be active throughout most of the winter and roosted in trees. During late fall–winter 2015–2018, 43 bats were tracked to 165 winter roost trees located mostly in wetland forest. The species' winter activity in coastal North Carolina represents a novel survival strategy as opposed to the hibernation behavior it is assumed to use in the rest of its range. This portion of the state is nearly devoid of caves or mines suitable for hibernacula, but has milder winters with insect activity. During spring 2019, 21 reproductive females were captured in the northern coastal plain and tracked to 64 maternity roost trees located mostly in wetland forest. Pregnant females began to be captured on April 25 and juveniles on June 16, indicating that pups are likely born in late May. Swab samples collected during late fall–winter from species susceptible to white-nose syndrome provided no evidence of Pseudogymnoascus destructans. Since northern long-eared bats in coastal North Carolina are active most of the winter and not dependent upon caves or mines for hibernation, they are likely not susceptible to white-nose syndrome. With the species in sharp decline elsewhere due to white-nose syndrome, this coastal population may serve as a refugium.

Introduction

The northern long-eared bat Myotis septentrionalis is a small (∼5–8 g) insectivorous bat that occurs in much of the eastern and north-central United States and southern Canada (Caceres and Barclay 2000; Federal Register 2015). During spring and summer months, they roost primarily in cavities, cracks, crevices, and exfoliating bark of trees of a variety of species and sizes (Foster and Kurta 1999; Caceres and Barclay 2000; Lacki et al. 2009; Silvis et al. 2016). Until recently, all northern long-eared bats were thought to hibernate, with caves and mines being the primary hibernacula (Caceres and Barclay 2000; Federal Register 2016). Despite formerly being one of the most abundant bat species in much of its range, their populations are declining rapidly across a large portion of their range because of white-nose syndrome (WNS), a disease caused by the fungus Pseudogymnoascus destructans (USFWS 2020).

Although the presence of the northern long-eared bat was well documented within the Blue Ridge ecoregion of western North Carolina before WNS (Rojas et al. 2017; North Carolina Wildlife Resources Commission, unpublished data), there was little information regarding the presence of the species in eastern North Carolina. It had only recently been discovered in coastal North Carolina when it was listed as a federally threatened species in 2015 under the U.S. Endangered Species Act (ESA 1973, as amended; Federal Register 2015). The species was first mist-netted and identification confirmed through deoxyribonucleic acid analysis in Washington County in 2007 (Morris et al. 2009) and subsequently caught in Camden County in 2012 (Grider et al. 2016) and Currituck County in 2014 (Tetra Tech 2015). In addition to mist-netting records, a specimen of unknown origin presumably collected from New Hanover County in 1996 is stored in the University of North Carolina Wilmington Natural History Collection (UNCW 4925). These county records occur within the Coastal Plain where no known hibernacula occur, presumably because of the near absence of caves or mines suitable for hibernation. Since they are not considered long-distance migrators (Federal Register 2015), Morris et al. (2009) suggested that northern long-eared bats in coastal North Carolina either 1) travel much farther to hibernacula than previously thought, 2) utilize alternative hibernacula such as tree cavities, or 3) do not hibernate at all in the milder winters of the Coastal Plain. Work began in 2015 to explore these possibilities and to determine the range of the species in eastern North Carolina. An ad hoc and adaptive approach was utilized for these investigations, and most of the fieldwork was conducted by environmental consultants through multiple contracts. The following information and analysis are a synthesis of multiple reports submitted to the U.S. Fish and Wildlife Service by environmental consultants and supplemented by data collected by the author, North Carolina Wildlife Resources Commission biologists, and other wildlife professionals. My objectives are to provide a current and comprehensive status of the northern long-eared bat in eastern North Carolina, to report novel behavior for the species, and to provide natural history data for this unique population.

Study area

The study area included numerous sites within the easternmost 59 counties of North Carolina (Figure 1). Three Environmental Protection Agency Level III ecoregions occur within the study area: from west to east, Piedmont, Southeastern Plains, and Middle Atlantic Coastal Plain (Griffith et al. 2002a, 2002b). Although some small caves are present in the Piedmont, caves potentially suitable as bat hibernacula are extremely rare in the Southeastern Plains and Middle Atlantic Coastal Plain of North Carolina (Culver et al. 1999; Grotto Center 2020). Underground mines are common in the Piedmont but are absent from the Southeastern Plains and Middle Atlantic Coastal Plain (Carpenter 1976; North Carolina Department of Environmental Quality 2020). Although many natural forest types are present in the study area, they were lumped into either wetland forest or upland forest on the basis of descriptions in Schafale and Weakley (1990) and Schafale (2012). Pine plantation, an unnatural forest type usually consisting of planted and intensively managed loblolly pine Pinus taeda, is also common in the study area.

Figure 1.

Map depicting study area in 2015–2020 with superimposed Environmental Protection Agency Level III ecoregions. Study area corresponds to the boundaries of the U.S. Fish and Wildlife Service's Raleigh Ecological Services Field Office work area.

Figure 1.

Map depicting study area in 2015–2020 with superimposed Environmental Protection Agency Level III ecoregions. Study area corresponds to the boundaries of the U.S. Fish and Wildlife Service's Raleigh Ecological Services Field Office work area.

Methods

Review of previous museum records

All known information on previous northern long-eared bat records from eastern North Carolina was reviewed. Inquiries were made to the University of North Carolina Wilmington Natural History Collection and North Carolina Museum of Natural Sciences regarding specimens of questionable identification. The mammal curators at each institution subsequently re-examined all specimens suspected of misidentification or mislabeling.

Presence–absence mist-net surveys

To map out the distribution of northern long-eared bats in eastern North Carolina, environmental consulting companies were contracted to conduct mist-net presence–absence surveys in multiple counties across the study area over three spring–summer seasons. Consultants netted a combined 210 nights during 2016–2018. Additionally, the author conducted 110 nights of netting throughout all seasons March 2016–March 2020, and North Carolina Wildlife Resources Commission biologists conducted 51 nights of netting across the spring, summer, and fall seasons of 2016–2019. Single-, double-, or triple-high mist nets (Avinet Research Supplies, Portland, Maine) 2.6–18 m wide were used to capture bats along trails, forest roads, or other flyways. Netting generally occurred from sunset to 5 h after sunset, although occasional deviations occurred. The number of nets utilized per night varied. Data recorded for each bat captured included date, time, location, forest type, species, sex, age, reproductive status, forearm length, weight, wing damage index score (Reichard and Kunz 2009), and band number. Each northern long-eared bat was fitted with a 2.9-mm numbered band (Porzana Ltd., East Sussex, UK). In addition to the efforts of the aforementioned consultants and government biologists, additional entities (e.g., universities and other consultants working on unrelated projects) performed mist-net surveys within the study area during the spring, summer, and fall seasons of 2015–2019. Northern long-eared bat records from all known surveys were pooled for this review.

Late fall–winter mist netting and radiotelemetry

To determine whether northern long-eared bats were present and active during the winter in coastal North Carolina, mist netting and radiotelemetry were conducted during a season when such activities are normally not conducted. Environmental consulting companies were contracted to capture bats and track them to roost sites over three late fall–winter seasons 2015–2018. Study locations occurred in the best available habitat across multiple counties in the Middle Atlantic Coastal Plain ecoregion (Figure 2). Initially, netting occurred when temperatures were ≥ 7.2°C but was later revised to ≥ 4.4°C because of activity documented at lower temperatures. Data recorded for each bat captured included date, time, location, forest type, species, sex, age, reproductive status, forearm length, weight, wing damage index score, band number, and temperature at time of capture. Each northern long-eared bat was fitted with a 2.9-mm numbered band. During late fall–winter 2016–2017, all captured WNS-susceptible species were swabbed for Pseudogymnoascus destructans and samples were submitted to the Southeastern Cooperative Wildlife Disease Study (University of Georgia, Athens). During late fall–winter 2017–2018, all captured WNS-susceptible species were swabbed and samples were submitted initially to the BioInnovation Laboratory at Kennesaw State University (Kennesaw, Georgia), with some retests later being sent to the National Wildlife Health Center (Madison, Wisconsin).

Figure 2.

Map depicting general locations of northern long-eared bat Myotis septentrionalis tracking and roost studies in Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018 and spring maternity season of 2019.

Figure 2.

Map depicting general locations of northern long-eared bat Myotis septentrionalis tracking and roost studies in Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018 and spring maternity season of 2019.

Northern long-eared bats ≥ 6.0 g were fitted with either a Holohil model LB-2X (Holohil Systems Ltd, Carp, Ontario, Canada), ATS model #A2414 (Advanced Telemetry Systems, Isanti, Minnesota), or Lotek PicoPip (Lotek Wireless, Newmarket, Ontario, Canada) radio transmitter. Tracking was conducted primarily by terrestrial (pedestrian or vehicular) means; however, on a few occasions an airplane was used. Various models of receivers and antennae were utilized. An attempt was made to track each bat for a minimum of 21 d. Data recorded for each roost tree included location, date, forest type, type of roost, tree species, diameter at breast height (dbh), and tree condition (live or dead). Ten of the radio transmitters deployed in 2017–2018 were temperature-sensitive models, and model R4500SD receiver data loggers (Advanced Telemetry Systems) and DS1923 iButton® temperature–humidity data loggers (Maxim Integrated, San Jose, California) were placed near roost trees to collect information on bat body temperature and activity level (normothermic or torpid). An attempt was made to conduct at least one emergence survey at each roost tree and was generally conducted from 1 half hour before dusk to 1 h after dusk.

Maternity studies

To determine the maternity season for northern long-eared bats in coastal North Carolina, environmental consulting companies were contracted to capture bats at North River Game Land (Camden and Currituck counties), Merchants Millpond State Park (Gates County), and Alligator River National Wildlife Refuge (Dare County) from late April 2019 to mid-July 2019 and use radiotelemetry to track pregnant and lactating females to roost sites (Figure 2). Data recorded for each bat captured included date, time, location, forest type, species, sex, age, reproductive status, forearm length, weight, wing damage index score, and band number. Most adult northern long-eared bats and some juveniles were fitted with a 2.9-mm numbered band. Pregnant or lactating females were fitted with a Holohil model LB-2X radio transmitter. Tracking was conducted by terrestrial means (pedestrian or vehicular), and various models of receivers and antennae were utilized. An attempt was made to track each bat for a minimum of 12 d. Data recorded for each roost tree included location, date, forest type, type of roost, tree species, dbh, and tree condition (live or dead). One emergence survey was conducted at each roost tree and was generally conducted from 1 half hour before dusk to 1 h after dusk. In addition to the consultants' efforts, researchers from the Conservation Management Institute at Virginia Tech also captured and tracked reproductive female northern long-eared bats during June 2019 at North River Game Land. These data were pooled with the consultants' data for this review.

Results

Review of previous museum records

Three specimens within the University of North Carolina Wilmington Natural History Collection representing purported county records for the northern long-eared bat within the Piedmont ecoregion in Lee (UNCW 9143), Davidson (UNCW 9148), and Mecklenburg (UNCW 22483) counties were re-examined by the mammal curator in 2017. A range map provided in White et al. (2018) was partially based on these museum records. After re-examination, two of these specimens were determined to be evening bats Nycticeius humeralis and one specimen was determined to be a little brown bat Myotis lucifugus (W.D. Webster, University of North Carolina Wilmington, personal communication). The mammal curator re-examined the two specimens within the North Carolina Museum of Natural Sciences (NCSM 45 and NCSM 3582) representing purported county records in Wake County (Piedmont ecoregion) in 2020. Range maps provided in Morris et al. (2009) and White et al. (2018) were partially based on these museum records. After re-examination, these specimens were determined to be little brown bats (L.J. Gatens, North Carolina Museum of Natural Sciences, personal communication).

Presence–absence mist-net surveys

From 2007 when the species was first identified in eastern North Carolina to March 2020, 181 unique northern long-eared bats were captured by mist netting, with 163 captured since 2015 (Table S1, Supplemental Material). Captures included 146 adults, 32 juveniles, and 3 of unknown age and occurred in all months of the year, with 35 captures in winter (December–February). Captures occurred in wetland forest (73.5%), upland forest (24.9%), and pine plantations (1.7%). However, upland forest and pine plantation capture sites were generally in proximity (< 0.5 km) to wetland forest. Captures occurred exclusively within the Middle Atlantic Coastal Plain ecoregion. All but one capture occurred < 50 km from the Atlantic Ocean or one of its major sounds, with the lone outlier captured ∼87 km from the Atlantic Ocean. Despite significant survey efforts (Table S2, Supplemental Material), northern long-eared bats have never been captured within the Piedmont or Southeastern Plains ecoregions. Nineteen coastal counties in North Carolina currently have records for the species (Figure 3). These data were synthesized from multiple sources (Morris et al. 2009; Tetra Tech 2015, 2016; Ecological Engineering 2016, 2018; Grider et al. 2016; Three Oaks Engineering 2016, 2017, 2018; Calyx Engineers + Consultants 2017a, 2017b, 2018a, 2018b, 2019; Copperhead Environmental Consulting 2017, 2018, 2019; VHB Engineering NC 2019; De La Cruz et al. 2020; North Carolina Wildlife Resources Commission, unpublished data; U.S. Fish and Wildlife Service, unpublished data).

Figure 3.

Map depicting the known range of the northern long-eared bat Myotis septentrionalis as of March 2020 in North Carolina by county. Note that some western county boundaries overlap both the Blue Ridge and Piedmont ecoregions, and some eastern county boundaries overlap both the Middle Atlantic Coastal Plain and Southeastern Plains ecoregions. However, the record collection locations in the western counties occur entirely within the Blue Ridge ecoregion, and the record collection locations in the eastern counties occur entirely within the Middle Atlantic Coastal Plain ecoregion.

Figure 3.

Map depicting the known range of the northern long-eared bat Myotis septentrionalis as of March 2020 in North Carolina by county. Note that some western county boundaries overlap both the Blue Ridge and Piedmont ecoregions, and some eastern county boundaries overlap both the Middle Atlantic Coastal Plain and Southeastern Plains ecoregions. However, the record collection locations in the western counties occur entirely within the Blue Ridge ecoregion, and the record collection locations in the eastern counties occur entirely within the Middle Atlantic Coastal Plain ecoregion.

Late fall–winter mist netting and radiotelemetry

The northern long-eared bat was documented to be active during most of the winter at multiple locations throughout the Middle Atlantic Coastal Plain ecoregion of North Carolina. The lowest temperature at which the species was captured was 7.8°C, but it is important to note that a tricolored bat Perimyotis subflavus was captured at 3.3°C. Cumulatively, 43 northern long-eared bats were tracked to 165 winter roost trees (Table 1; Figure 2; Table S3, Supplemental Material; Ecological Engineering 2016; Copperhead Environmental Consulting 2017; Calyx Engineers + Consultants 2018a; Copperhead Environmental Consulting 2018; Ecological Engineering 2018). Winter roost trees occurred in wetland forest (94.6%), upland forest (1.2%), pine plantation (1.2%), and unknown forest (3.0%) and were represented by at least 22 species (Table 2). The mean dbh of winter roost trees was 30.9 cm (27.6–34.3 cm, 95% confidence interval [CI]; Figure 4). Most trees were live (84.2%), but dead trees (9.1%) and those of unknown status (6.7%) were also used. Roost types included cavities (55.8%), cracks or crevices (11.5%), exfoliating bark (4.8%), and unknown (27.9%). Emergence surveys were conducted at most roost trees, with some being repeated one or more times for a total of 195 surveys. The mean number of bats observed emerging per survey was 0.5 (0.4–0.6, 95% CI).

Table 1.

Number of northern long-eared bats Myotis septentrionalis tracked, number of days each bat tracked, mean days tracked, and number of roost trees documented in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.

Number of northern long-eared bats Myotis septentrionalis tracked, number of days each bat tracked, mean days tracked, and number of roost trees documented in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.
Number of northern long-eared bats Myotis septentrionalis tracked, number of days each bat tracked, mean days tracked, and number of roost trees documented in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.
Table 2.

Percentage of total for each tree species used for 165 roost sites by northern long-eared bats Myotis septentrionalis in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.

Percentage of total for each tree species used for 165 roost sites by northern long-eared bats Myotis septentrionalis in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.
Percentage of total for each tree species used for 165 roost sites by northern long-eared bats Myotis septentrionalis in the Coastal Plain of North Carolina during late fall–winter seasons of 2015–2018.
Figure 4.

Distribution of sizes (diameter at breast height) of trees used as winter roosts (n = 165) during late fall–winter seasons of 2015–2018 and as maternity roosts during spring 2019 (n = 64) by northern long-eared bats Myotis septentrionalis in the coastal plain of North Carolina. Of 165 total winter roost trees, 12 trees of unknown size were not factored into the analysis.

Figure 4.

Distribution of sizes (diameter at breast height) of trees used as winter roosts (n = 165) during late fall–winter seasons of 2015–2018 and as maternity roosts during spring 2019 (n = 64) by northern long-eared bats Myotis septentrionalis in the coastal plain of North Carolina. Of 165 total winter roost trees, 12 trees of unknown size were not factored into the analysis.

Utilizing temperature-sensitive transmitters, Copperhead Environmental Consulting (2018) documented 10 northern long-eared bats in sustained torpor during late fall–winter 2017–2018. The longest sustained torpor bout for each radio-tagged bat averaged 6.8 d (4.1–9.5 d, 95% CI), and the coldest temperature for a normothermic bat was 3.0°C. However, Ecological Engineering (2018) documented a northern long-eared bat on December 31, 2017 that moved 4.9 km from one roost tree to another sometime after sunset when the air temperature was −2.0°C (Figure 5).

Figure 5.

Photograph of a bald cypress tree Taxodium distichum cavity occupied by a northern long-eared bat Myotis septentrionalis on January 5, 2018 in the Croatan National Forest, Craven County, North Carolina. The snow depicts a rare weather event for the southern Coastal Plain of North Carolina. Photograph credit: Dottie Brown.

Figure 5.

Photograph of a bald cypress tree Taxodium distichum cavity occupied by a northern long-eared bat Myotis septentrionalis on January 5, 2018 in the Croatan National Forest, Craven County, North Carolina. The snow depicts a rare weather event for the southern Coastal Plain of North Carolina. Photograph credit: Dottie Brown.

None of the northern long-eared bats captured in coastal North Carolina showed clinical symptoms for WNS. Swab samples collected from 67 bats of three species (northern long-eared bat, southeastern myotis Myotis austroriparius, and big brown bat Eptesicus fuscus) during late fall–winter 2016–2017 were submitted to the Southeastern Cooperative Wildlife Disease Study. Pseudogymnoascus destructans was not detected on any sample (Southeastern Cooperative Wildlife Disease Study 2017). Swab samples collected from 131 bats of five species (northern long-eared bat, southeastern myotis, big brown bat, tricolored bat, and little brown bat) during late fall–winter 2017–2018 were submitted to the BioInnovation Laboratory at Kennesaw State University. Four samples initially tested positive for P. destructans (C. Cornelison, Kennesaw State University, unpublished data). These four samples were subsequently submitted to the National Wildlife Health Center, and more refined testing yielded a negative result for three samples and an equivocal result for one sample (National Wildlife Health Center 2019).

Maternity studies

During spring–summer 2019, 14 pregnant females were captured April 25–June 1, 12 lactating females were captured June 3–June 27, 6 postlactating females were captured June 16–July 15, and 24 juveniles were captured June 16–July 15. Twenty-one pregnant or lactating northern long-eared bats were fitted with transmitters and tracked for 1–15 d to 64 maternity roost trees (Figure 2; Table S4, Supplemental Material; Calyx Engineers + Consultants 2019; Copperhead Environmental Consulting 2019; VHB Engineering NC 2019; De La Cruz et al. 2020). Maternity roost trees were found in wetland forest (92.2%) and upland forest (7.8%) and were represented by at least 14 species (Table 3). The mean dbh of maternity roost trees was 20.6 cm (17.5–23.6 cm, 95% CI; Figure 4). Both live trees (59.4%) and dead trees (40.6%) were used. Roost types included cavities (59.4%), exfoliating bark (29.7%), cracks or crevices (4.7%), and unknown (6.2%). Emergence surveys were conducted at all 64 maternity roost trees, and the mean number of bats observed emerging per survey was 4.7 (1.8–7.6, 95% CI); however, the median number was one.

Table 3.

Percentage of total for each tree species used for 64 maternity roost sites by northern long-eared bats Myotis septentrionalis in the northern Coastal Plain of North Carolina during spring 2019.

Percentage of total for each tree species used for 64 maternity roost sites by northern long-eared bats Myotis septentrionalis in the northern Coastal Plain of North Carolina during spring 2019.
Percentage of total for each tree species used for 64 maternity roost sites by northern long-eared bats Myotis septentrionalis in the northern Coastal Plain of North Carolina during spring 2019.

Discussion

At the time of listing as a threatened species under the ESA (1973) in 2015 and accounting for recent museum record identification corrections, only four eastern North Carolina counties had records for northern long-eared bats. The increase to 19 counties (Figure 3) reflects substantial improvement in the knowledge of the species' range in eastern North Carolina. This expansion is almost certainly the result of increased survey effort and not a true range expansion. Despite the encouraging number of recent captures, the numbers caught in mist nets are relatively low when compared with other parts of its range pre-WNS (e.g., Rojas et al. 2017), but this low capture rate could be a result of coastal North Carolina being on the periphery of the species' overall range.

Captures occurring in every month of the year confirm the presence of a year-round population of northern long-eared bats in the Middle Atlantic Coastal Plain ecoregion within North Carolina. However, it is unclear if the bats are an entirely resident population or if some individuals make seasonal movements. The lack of captures from recent and previous efforts within the Piedmont (including the portion outside the study area) and Southeastern Plains ecoregions (Table S2, Supplemental Material; Lambiase et al. 2000, 2005; Cameron et al. 2004; Kalcounis-Rueppell and Li 2016) strongly suggests spatially disjunct populations of northern long-eared bats in North Carolina. A formerly robust population in the Blue Ridge ecoregion of western North Carolina appears separated from the population in the Middle Atlantic Coastal Plain ecoregion by a large unpopulated area in the middle of the state (Figure 3), despite the populations being genetically nearly identical (Morris et al. 2009). This separation is similar to the findings of the North American Bat Monitoring Program (Li and Kalcounis-Rueppell 2019). This bimodal distribution in North Carolina is also comparable with the species' known range in South Carolina where a Blue Ridge Mountains population appears separated from a recently discovered population along South Carolina's Atlantic Coast (South Carolina Department of Natural Resources 2019).

All captures occurred ≤ 87 km from either the Atlantic Ocean or its major sounds. This distance roughly corresponds to the western boundary of the Middle Atlantic Coastal Plain ecoregion within North Carolina. Nearly all captures, winter roost sites, and maternity roost sites occurred either within or very close to wetland forest. Northern long-eared bats were often captured along with southeastern myotis, a species associated with swamps (Clement and Castleberry 2013; Fleming et al. 2013). The Middle Atlantic Coastal Plain has a preponderance of swamps (Griffith et al. 2002b), and these wetland forests are the most intact and least disturbed habitat on the landscape. Thus, it is unclear if northern long-eared bats are selecting for specific qualities of wetland forests, or if they are simply utilizing the largest intact forest tracts available regardless of hydrology. Nearly all northern long-eared bat captures in coastal North Carolina have occurred on large public lands, which indicates the importance of these conservation lands. Moving westward from the Middle Atlantic Coastal Plain ecoregion into the Southeastern Plains ecoregion, the dominant land use is agriculture, and the forest tracts are generally smaller, more fragmented, and more disturbed. Farther west, urbanization and agriculture similarly affect forest tracts in the Piedmont ecoregion. These land uses may contribute to the seeming absence of northern long-eared bats in the Southeastern Plains and Piedmont ecoregions.

The documentation of extensive winter activity confirms a novel survival strategy as opposed to the hibernation strategy that the species is assumed to use in the rest of its range (Federal Register 2015). Although low-level winter activity has previously been documented for northern long-eared bats, those observations were near cave or mine openings at known hibernacula (Whitaker and Rissler 1992; Boyles et al. 2006; Bernard and McCracken 2017). Despite the near absence of caves and mines as suitable hibernacula, Grider et al. (2016) documented year-round activity of multiple species of bats while using acoustic methods in the Coastal Plain of North Carolina. In contrast to the Piedmont ecoregion, the Middle Atlantic Coastal Plain ecoregion maintains insect activity throughout most of the winter, though at a lower level than the rest of the year (personal observation). With higher nightly winter temperatures (Grider et al. 2016), the Coastal Plain appears to provide more opportunities for winter foraging than does the Piedmont. For example, Whitaker et al. (1997) documented feeding in eastern red bats Lasiurus borealis during winter in the Great Dismal Swamp of southeastern Virginia and northeastern North Carolina by examining the stomach contents of sacrificed bats. Moths (Lepidoptera) and flies (Diptera) are commonly observed during winter in coastal North Carolina (Padgett and Rose 1991).

Although southeastern myotis and Rafinesque's big-eared bats Corynorhinus rafinesquii in the southeastern United States are known to roost in tree cavities during winter (Clement and Castleberry 2013; Fleming et al. 2013), this work provides the first documentation of northern long-eared bats utilizing trees as winter roost sites. Most (84.2%) of the tracked bats selected live trees over dead trees, but the species and size varied greatly. Although the mean winter roost tree dbh was 30.9 cm, bats utilized trees as small as 4.1 cm. This may be indicative of the relatively warmer winter temperatures in coastal areas and therefore less need for thermal protection. The winter roost emergence surveys revealed that the northern long-eared bats roosted in very small numbers, with the majority roosting alone.

Though northern long-eared bats were observed to be active most of the winter, the use of temperature-sensitive transmitters during late fall–winter 2017–2018 did document bats in torpor. Torpor is used to minimize the thermoregulatory costs during periods of extreme conditions such as low ambient temperature or decreased food availability (Dunbar and Tomasi 2006). The longest sustained torpor bout for each bat averaged 6.8 d, and the lowest temperature at which a bat was recorded to be normothermic was 3.0°C. Since torpor duration is inversely related to ambient temperature (Dunbar and Tomasi 2006), these relatively short sustained torpor bouts are indicative of nighttime winter temperatures commonly being greater than 3.0°C in coastal North Carolina.

Captures of juvenile northern long-eared bats beginning on June 16 and juvenile volancy occurring by 21 d (Krochmal and Sparks 2007) indicates that birth of pups begins no later than late May. However, weather and staff scheduling issues may have prevented earlier documentation of juveniles. Additionally, it must be noted that these data were obtained from the northern portion of the coastal plain in North Carolina. Kindel (2019) captured heavily pregnant northern long-eared bats in late April and juveniles in early June in coastal South Carolina, indicating birth occurring in early to mid-May. Birth time in the Coastal Plain of North Carolina likely occurs along a continuum from north to south. Given this birth chronology, and due to the fact that no pregnant females were captured after June 1, I suggest a conservative pup season for eastern North Carolina as May 1–June 30. This is in contrast to the June 1–July 31 pup season published in the Federal Register (2015).

The species and size of maternity roost trees varied greatly, but the mean maternity roost tree dbh (20.6 cm) was much smaller than the mean winter roost tree dbh (30.9 cm). Despite larger trees being available, some females selected trees as small as 6.1 cm. This may be indicative of the relatively warmer spring temperatures in coastal areas and therefore less need for thermal protection. The maternity roost tree emergence surveys indicate variability in roosting strategy. Although the mean number of bats observed emerging at roost sites was 4.7, the median number was 1. However, notable outliers of 61 and 63 occurred. Since northern long-eared bats were often captured with the similar southeastern myotis, this raises the question of possible coroosting with this species. This bears further study.

Although WNS has decimated the western population of northern long-eared bats in North Carolina (Caldwell 2016), there is currently no evidence of WNS or P. destructans in the Middle Atlantic Coastal Plain or Southeastern Plains ecoregions of North Carolina, likely due to the rarity of caves and subsurface mines and milder winters permitting bats to be active during winter. The discovery of a population of northern long-eared bats that forgoes long-term hibernation is particularly important from a conservation standpoint. Since this coastal population is not dependent upon hibernation in caves or mines and exhibits only relatively short torpor durations, it is likely not susceptible to WNS-induced mortality. If the coastal population is truly spatially separated from the population in western North Carolina, the lack of contact between the two populations would further reduce the likelihood of the spread of P. destructans into coastal areas. Northern long-eared bats were recently discovered in coastal South Carolina (White et al. 2018), an area with similar conditions to coastal North Carolina. With the species in sharp decline elsewhere from WNS, coastal North Carolina and South Carolina could ultimately serve as a refugium for the species. However, the viability and population trends of this unique population of bats are currently unknown and thus further study is warranted.

Supplemental Material

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article.

Table S1. Chronological list of all known northern long-eared bat Myotis septentrionalis captures in eastern North Carolina through March 2020 with location, sex, age, forest type, and source.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S1 (27 KB XLSX).

Table S2. Bat mist-netting level of effort within eastern North Carolina counties from all sources April 2015 to March 2020. The number of nights indicated are calendar nights, not net nights. A calendar night was generally one netting crew at one site, but because of inconsistency in reporting across multiple sources, in some instances a calendar night may have represented multiple netting crews at different sites on the same date in the same county. Thus the number of calendar nights should be considered minimum numbers. Netting effort per calendar night (i.e., number of nets and number of hours that nets were open) varied greatly. The number of calendar nights of netting in some counties was heavily biased because of certain productive sites being selected as focus areas for winter behavior or maternity studies. Therefore, this data should not be used to determine catch per unit effort.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S2 (21 KB XLSX).

Table S3. List of all northern long-eared bat Myotis septentrionalis winter roost trees documented in eastern North Carolina 2015–2018 with species, size (diameter at breast height), status (live or dead), roost type, forest type, and emergence survey data. The numbers in the emergence column indicate the number of bats observed per emergence survey, with some winter roost trees having multiple surveys. A blank cell in the emergence column indicates that no emergence survey was conducted at that roost tree.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S3 (32 KB XLSX).

Table S4. List of all northern long-eared bat Myotis septentrionalis maternity roost trees documented in eastern North Carolina in spring 2019 with species, size (diameter at breast height), status (live or dead), roost type, forest type, and emergence survey data. The numbers in the emergence column indicate the number of bats observed per emergence survey. One emergence survey was conducted for each maternity roost tree.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S4 (25 KB XLSX).

Reference S1.Caldwell K. 2016. White-nose syndrome surveillance and bat monitoring in North Carolina, October 1, 2015–September 30, 2016. Final performance report under white-nose syndrome grant to states, grant number E-17. North Carolina Wildlife Resources Commission, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S5 (403 KB PDF).

Reference S2.Calyx Engineers + Consultants. 2017a. Federally protected bat survey report; eastern North Carolina; northern long-eared bat (Myotis septentrionalis) research study; Beaufort, Bladen, Craven, New Hanover, Pamlico, Pender, and Wayne Counties, North Carolina; survey phase 2: summer 2016. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S6 (25.26 MB PDF).

Reference S3.Calyx Engineers + Consultants. 2017b. Federally protected bat survey report; eastern North Carolina; northern long-eared bat (Myotis septentrionalis) research study; Brunswick, Columbus, Onslow, Pender, Robeson, Rockingham, and Sampson Counties, North Carolina; survey phase 2: summer 2017. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S7 (87.63 MB PDF).

Reference S4.Calyx Engineers + Consultants. 2018a. Federally protected bat survey report; eastern North Carolina; northern long-eared bat (Myotis septentrionalis) research study; Camden, Currituck, and Gates Counties, North Carolina; survey phase v winter 2017/2018. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S8 (33.81 MB PDF).

Reference S5.Calyx Engineers + Consultants. 2018b. Federally protected bat survey report; eastern North Carolina; northern long-eared bat (Myotis septentrionalis) research study; Edgecombe, Halifax, Hertford, and Northampton Counties, North Carolina; spring/summer 2018 phase vi survey. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S9 (16.26 MB PDF).

Reference S6.Calyx Engineers + Consultants. 2019. Federally protected bat survey report; eastern North Carolina; northern long-eared bat (Myotis septentrionalis) research study; Gates County, North Carolina; survey phase vii spring/summer 2019. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S10 (26.21 MB PDF).

Reference S7.Copperhead Environmental Consulting, Inc. 2017. Final report: fall 2016/winter 2017 NCDOT northern long-eared bat research project, Bertie, Bladen, Hyde, Martin, and Tyrrell Counties, North Carolina. Report to North Carolina Department of Transportation and U.S. Fish and Wildlife Service, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S11 (121.54 MB PDF).

Reference S8.Copperhead Environmental Consulting, Inc. 2018. Final report: fall 2017/winter 2018 NCDOT northern long-eared bat research project, Dare and Hyde Counties, North Carolina. Report to North Carolina Department of Transportation and U.S. Fish and Wildlife Service, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S12 (64.2 MB PDF).

Reference S9.Copperhead Environmental Consulting, Inc. 2019. Final report: 2019 eastern North Carolina northern long-eared bat research project, phase VII, Dare County, North Carolina. Report to North Carolina Department of Transportation and U.S. Fish and Wildlife Service, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S13 (25.15 MB PDF).

Reference S10.De La Cruz JL, True M, Taylor H, Brown D, Ford WM. 2020. Occupancy and roost ecology of the northern long-eared and Indiana bat on the coastal plain of North Carolina. U.S. Geological Survey Science Support Program Project G17AC00288 to Virginia Tech, Blacksburg. Report to U.S. Fish and Wildlife Service, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S14 (15.01 MB PDF).

Reference S11.Ecological Engineering. 2016. Protected bat species survey report, northern long-eared bat research project, eastern North Carolina, survey phase 1, sessions 1 & 2: fall 2015 and winter 2016. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

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Reference S12.Ecological Engineering. 2018. Protected bat species survey report, northern long-eared bat research project, eastern North Carolina, fall 2017 and winter 2018, phase v. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S16 (47.73 MB PDF).

Reference S13.Kalcounis-Rueppell MC, Li H. 2016. Bats of the Uwharrie National Forest: mist-netting (2014 and 2015) and acoustic sampling (2013–2015). University of North Carolina at Greensboro. Report to North Carolina Wildlife Resources Commission, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S17 (48.03 MB PDF).

Reference S14.Lambiase SJ, Clark MK, Gatens LJ. 2000. Bat (chiroptera) inventory of North Carolina state parks 1999–2000. North Carolina Division of Parks and Recreation, Raleigh, North Carolina. Unpublished report.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S18 (658 KB PDF).

Reference S15.Lambiase SJ, Clark MK, Gatens LJ. 2005. Bat (chiroptera) inventory of North Carolina state parks, 2005 addendum. North Carolina Division of Parks and Recreation, Raleigh, North Carolina. Unpublished report.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S19 (204 KB PDF).

Reference S16.Li H, Kalcounis-Rueppell M. 2019. Final report for WM-0321: acoustic monitoring of bats in North Carolina May 2017–October 2019. University of North Carolina at Greensboro. Report to North Carolina Wildlife Resources Commission, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S20 (1.49 MB PDF).

Reference S17.National Wildlife Health Center. 2019. Diagnostic services case report: case 29023. Madison, Wisconsin.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S21 (26 KB PDF).

Reference S18.Southeastern Cooperative Wildlife Disease Study. 2017. White-nose syndrome surveillance diagnostic results. Case number CC17-204 A-NNN. University of Georgia, Athens.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S22 (146 MB PDF).

Reference S19.Tetra Tech, Inc. 2015. Northern long-eared bat survey report, NSAHR Northwest Annex, Virginia and North Carolina. Report to Naval Facilities Engineering Command Mid-Atlantic, Norfolk, Virginia.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S23 (21.91 MB PDF).

Reference S20.Tetra Tech, Inc. 2016. Northern long-eared bat survey report, NSAHR Northwest Annex, Virginia and North Carolina. Report to Naval Facilities Engineering Command Mid-Atlantic, Norfolk, Virginia.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S24 (26.72 MB PDF).

Reference S21.Three Oaks Engineering. 2016. Northern long-eared bat research project, eastern North Carolina, survey phase 2: summer 2016, northeast section report. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S25 (23.51 MB PDF).

Reference S22.Three Oaks Engineering. 2017. Northern long-eared bat research project, eastern North Carolina, summer 2017 survey phase iv, northeast section report. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S26 (30.46 MB PDF).

Reference S23.Three Oaks Engineering. 2018. Northern long-eared bat research project, eastern North Carolina, spring/summer 2018 survey phase vi, southeast section report. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S27 (12.76 MB PDF).

Reference S24.VHB Engineering NC. 2019. Protected bat species survey report, northern long-eared bat research project, eastern North Carolina, spring and summer 2019, phase vii. Report to North Carolina Department of Transportation, Raleigh, North Carolina.

Found at DOI: https://doi.org/10.3996/JFWM-20-018.S28 (212.9 MB PDF).

Acknowledgments

The North Carolina Department of Transportation provided funding for this work, and I thank the following former and current staff for all their assistance with study designs, contracts, and fieldwork: Heather Wallace, Mary Frazer, Chris Manley, Neil Medlin, and Cheryl Knepp. I thank all the staff from the following environmental consulting companies that did most of the fieldwork: Ecological Engineering, Ecological Solutions, Three Oaks Engineering, Calyx Engineers + Consultants, Copperhead Environmental Consulting, and VHB Engineering NC. I thank Katherine Etchison (North Carolina Wildlife Resources Commission) and Jesse De La Cruz (Conservation Management Institute at Virginia Tech) for sharing their data. I also thank all the volunteers who assisted me with my mist-netting efforts. Valuable comments on my first draft of this article were provided by Piper Roby, Theresa Wetzel, Mary Frazer, Heather Wallace, and Kathryn Cunningham. The comments of the Associate Editor and two anonymous reviewers also helped me focus and substantially improve this article.

Any use of trade, product, website, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Author notes

Citation: Jordan GW. 2020. Status of an anomalous population of northern long-eared bats in coastal North Carolina. Journal of Fish and Wildlife Management 11(2):665–678; e1944-687X. https://doi.org/10.3996/JFWM-20-018

Competing Interests

The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.