Northeastern Naturalist 154 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 22001144 NORTHEASTERN NATURALIST 2V1(o2l). :2115,4 N–1o6. 32 Offshore Activity of Bats along the Mid-Atlantic Coast Angela L. Sjollema1,*, J. Edward Gates2, Robert H. Hilderbrand2, and John Sherwell3 Abstract - Bat mortality caused by terrestrial wind-power plants has been documented and offshore wind-power developments may have similar effects. Determining which bat species occur offshore, how far they range from shore, and predictors of high activity may be helpful to developers and wildlife managers. We studied bat activity off the mid-Atlantic coast, using ultrasonic detectors mounted on ships in spring and fall 2009 and 2010. We investigated the association between nightly bat activity and weather variables, including wind speed, air temperature, and barometric pressure. Echolocation passes of bats totaled 166; maximum detection distance from shore was 21.9 km, and mean distance was 8.4 km. Most passes were identified as Lasiurus borealis (Eastern Red Bats), representing 78% of bats identified to species or species group. Bat activity decreased as wind speed increased, but activity did not differ with distance from shore. Offshore wind projects proposed for locations beyond the maximum detection distances noted in our study would likely have few impacts on seasonal movements; however, depending on their location and operating protocols, projects closer to shore could result in fatalities similar to those reported at onshore wind facilities. Introduction Worldwide, utility-scale wind-energy projects have been gaining governmental support for many reasons including the desire for increased energy production and reduced greenhouse gas emissions (Nadaï and van der Horst 2010). However, bat fatalities at wind-power plants received attention when many deaths were reported at the Mountaineer Wind Energy Center in West Virginia in 2003 (Kerns and Kerlinger 2004). Since then, high mortality has been reported at wind-power facilities across North America (Arnett et al. 2008, Baerwald et al. 2009, Gruver et al. 2009). The fatalities are caused by direct contact with turbine blades (Horn et al. 2008) and barotrauma, which occurs when air-containing organs in the body sustain damage due to rapid pressure change (Baerwald et al. 2008). Although bats are long lived, they have low fecundity (Barclay and Harder 2003), and it is unknown whether their populations can withstand the annual mortality caused by large-scale windpower developments (Kunz et al. 2007). Recently, many states along the Atlantic coast have proposed offshore windpower facilities, including Maryland, Delaware, and New Jersey (BOEM 2013). An important issue in evaluating these proposals is whether bats occur away from the 1Stantec Consulting, Inc., 1500 Lake Shore Drive, Columbus, OH 43204, 2University of Maryland Center for Environmental Science, Appalachian Laboratory, 301 Braddock Road, Frostburg, MD 21532. 3Maryland Department of Natural Resources, Power Plant Research Program, Annapolis, MD 21401. *Corresponding author - angela.sjollema@stantec.com. Manuscript Editor: Allen Kurta Northeastern Naturalist Vol. 21, No. 2 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 155 coast in areas where these developments may occur. Bats have been observed many kilometers offshore for over a century (Peterson et al. 2014), and in North America, these records generally involve migratory tree bats, such as Lasiurus borealis (Müller) (Eastern Red Bat), Lasiurus cinereus (Palisot de Beauvois) (Hoary Bat), and Lasionycteris noctivagans (Le Conte) (Silver-haired Bat). For example, Cryan and Brown (2007) reported lasiurine bats consistently using Southeast Farallon Island, 30 km west of San Francisco, CA, as a stopover site during fall migration. Investigators on Long Point, ON, Canada, found activity of Hoary Bats and Silver-haired Bats to be higher in August than June and demonstrated the importance of the peninsula as a migratory stopover site before the 38-km flight over Lake Erie (Dzal et al. 2009, McGuire et al. 2012). In addition, Eastern Red Bats have been found occasionally roosting on or flying by ships in the northern Atlantic Ocean (Allen 1923, Brown 1953, Czenze et al. 2011, Norton 1930, Peterson 1970). Our objectives were to assess which species of bats or groups of species were active off the Atlantic coast, to document whether activity was greater near shore than farther from it, and to determine if certain weather conditions affected activity. We used acoustic monitoring to identify the species or species groups of bats most active off the Atlantic coast, between Massachusetts and northern North Carolina, in an area of the Atlantic Ocean that has not been explored previously for bat activity. Determining levels of activity and factors influencing it is important for evaluating sites proposed for offshore wind developments. Materials and Methods Field studies Acoustic-monitoring equipment was attached to 5 ships: research vessel (R/V) Hugh R. Sharp, fishing vessel (F/V) Darana R, R/V Integrity, ocean survey vessel (OSV) Bold, and Lewestown Lady (Tables 1, 2). The primary duties of 3 vessels, the R/V Hugh R. Sharp, F/V Darana R, and the OSV Bold, were to perform research projects unrelated to the acoustic monitoring. The Darana R was mostly anchored during night hours, but occasionally trawled for fish in the early evening or traveled between study sites. The crew of the R/V Hugh R. Sharp collected their data on transects during day and night hours, which kept the vessel moving, and the OSV Bold had similar tasks and often traveled during night hours. The R/V Integrity, however, was specifically contracted to perform acoustic monitoring and moved Table 1. Name and length of vessel, distance traveled from shore, and height of microphone above the ocean during offshore acoustic surveys. Distance from shore (km) Name of vessel Mean Maximum Height of microphone (m) R/V Hugh R. Sharp 20 73 12.2 F/V Darana R 12 26 4.6 OSV Bold 18 24 10.0 R/V Integrity 6 16 1.8 Lewestown Lady 85 166 4.0 Northeastern Naturalist 156 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 Vol. 21, No. 2 slowly during all night hours, completing transects of about 6 km in length, 6–8 times per night. Unlike the other vessels, the Lewestown Lady was used for pelagicbird tours and deep-sea fishing. It traveled very quickly throughout the night toward deep waters far offshore and returned the next evening. We monitored bat activity in spring and fall of 2009 and 2010, but the duration of monitoring was dependent upon availability of the ships. We used Anabat II detectors with zero-crossings analysis interface modules (ZCAIMs; Titley Scientific, Ballina, NSW, Australia), and Anabat Storage Detectors (SD1) interchangeably for acoustic monitoring. These units are broadband, frequency-division detectors sensitive to sound from 10–200 kHz. The ZCAIM is a recording unit, which records ultrasonic detections and saves them to a compact flash (CF) card, along with the date and time. The SD1 combines a detector and ZCAIM in 1 unit. The 2 detector models have no significant differences in detection ability (Steve Duren, Titley Scientific, Columbia, MO, pers. comm.). We attached 2 recording units to each ship to minimize loss of data due to malfunctions and to provide data from both the starboard and port sides of the ship. Specific positioning was dependent on individual characteristics of each vessel. We used a waterproof fiberglass box (28 x 22 x 13 cm) to house the monitors, ZCAIMs, and batteries, and we enclosed the microphone in a piece of pipe made from polyvinylchloride and attached it to the top of the box. The microphone was directed down toward a 20 x 20-cm sheet of acrylic plastic, which was angled at 45° to the horizontal. This arrangement shielded the microphone from the elements, while the acrylic plastic reflected ultrasonic sounds toward the microphone. We calibrated each detector to a maximum detection distance of approximately 30 m, using a high-frequency, short-wave ultrasonic pest-repeller before placement. The units Table 2. Starting and ending date for 15 acoustic-monitoring cruises along the mid-Atlantic coast in 2009 and 2010. Monitoring occurred from 1800 to 0800 hours or 1900 to 0700 hours depending on time of sunset/sunrise and availability of the vessel to perform the survey. Acoustic monitoring cruise Vessel Start End R/V Hugh R. Sharp 11 March 2009 17 March 2009 R/V Hugh R. Sharp 7 April 2009 10 April 2009 R/V Hugh R. Sharp 1 May 2009 6 May 2009 R/V Hugh R. Sharp 2 June 2009 6 June 2009 R/V Hugh R. Sharp 31 July 2009 5 August 2009 R/V Integrity 6 August 2009 8 August 2009 R/V Integrity 17 August 2009 18 August 2009 R/V Integrity 25 August 2009 27 August 2009 R/V Hugh R. Sharp 29 August 2009 3 September 2009 R/V Hugh R. Sharp 28 September 2009 3 October 2009 F/V Darana R 24 September 2009 31 October 2009 F/V Darana R 21 April 2010 7 May 2010 R/V Integrity 7 May 2010 8 May 2010 Lewestown Lady 19 August 2010 20 August 2010 OSV Bold 21 August 2010 26 August 2010 Northeastern Naturalist Vol. 21, No. 2 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 157 were set to record from approximately dusk to dawn. The time and date associated with each pass (via the ZCAIM) allowed us later to match the recordings with the vessel track-log or approximate global positioning system (GPS) locations. When acoustic units were retrieved from the ships, we downloaded the data from CF cards using the program CFCread, and the files were viewed using Analook, version 3.7w (Corben 2009). We qualitatively assigned bat passes to species or groups, using a library of passes and an acoustic identification key for bats of the region (Amelon 2005). We required ≥3 individual pulses within a pass to identify it to species or species group. We combined Eptesicus fuscus (Palisot de Beauvois) (Big Brown Bat) and Silver-haired Bats into 1 species group because the pulses are very similar (Betts 1998). Likewise, the different species of Myotis are difficult to distinguish, and we identified these calls only to genus following standard practice (e.g., Brooks 2009). Passes identified as Myotis may have been from any of the species that occur on the nearby mainland (Harvey et al. 1999), including Myotis leibii (Audubon and Bachman) (Eastern Small-footed Bat), M. lucifugus (LeConte) (Little Brown Bat), M. septentrionalis (Trouessart) (Northern Long-eared Bat), or M. sodalis (Miller and Allen) (Indiana Bat). We classified passes with ≤3 pulses as unidentified bats; however, we used all passes in our statistical analysis. Weather data We examined air temperature (°C), barometric pressure (kPa), and wind speed (m/s) because these weather variables can influence nightly bat activity (Ahlén 1997, Ahlén et al. 2007, Ciechanowski et al. 2007, Fiedler 2004, Johnson et al. 2011, Kerns et al. 2005, Reynolds 2006). The R/V Hugh R. Sharp was equipped with an onboard weather station, but for the other vessels, we obtained data from a weather station nearest each vessel at a given time. Data on weather were recorded by 13 stations and downloaded from 2 online sources: the New Jersey Weather and Climate Network (http://climate.rutgers.edu/njwxnet/; accessed 1 February 2011) and the National Data Buoy Center of the National Oceanic and Atmospheric Administration (http://www.ndbc.noaa.gov/; accessed 3 February 2011). Weather data on the R/V Hugh R. Sharp were automatically recorded every 10 sec, but the stations took observations on an hourly basis. We averaged each weather variable per monitoring-hour occurring each night, with a monitoring-hour defined as each hour the ship was away from land. The number of monitoring-hours/night ranged from 2–14, depending on the amount of time each ship was offshore. Consequently, bat activity was standardized for time by dividing total number of passes recorded by total number of hours that the boat was offshore (bat activity/hours of offshore effort). Statistical analysis To test if there was a gradient of declining activity with increasing distance from shore, we divided the offshore area into 5-km intervals and calculated bat passes/ monitoring-hour for the distance intervals of each cruise. Because there was variation in time offshore, speed of boat, and height of microphone among the vessels, we used an incomplete block design for our analyses (Federer and Nguyen 2002), Northeastern Naturalist 158 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 Vol. 21, No. 2 in which the ship was the block, the distances were treatments, and the response variable was bat passes (Federer and Nguyen 2002). We analyzed only the first 5 distance intervals because passes were not recorded beyond 22 km. The non-normal characteristics of the acoustic data required that we rank-transform them before applying the blocked analysis of variance (Hilderbrand and Kershner 2000, SAS 2004). We used the non-parametric Spearman’s rank correlation (SAS 2004, Zar 1999) to examine relationships between activity and weather. We set α = 0.05 for all statistical tests; all means are presented as ± SE. Results We conducted offshore acoustic monitoring for 86 nights (partial and full nights) from March 2009 to August 2010 in spring (March–beginning of June) and fall (August–October). The total number of monitoring hours was 898. We recorded 166 total passes by bats, with the Eastern Red Bat identified most often (44.0%), followed by Big Brown/Silver-haired Bat (6.6%), Myotis (4.2%), and Hoary Bat (1.8%). Many passes (43.4%) did not meet the minimum criterion of 3 pulses or were otherwise difficult to distinguish and we considered those passes to be unidentifiable. The mean distance that bats were recorded off the mid-Atlantic coast was 8.7 ± 0.4 km, (n = 166). The species recorded farthest from shore were Eastern Red Bat (21.9 km) and Big Brown/Silver-haired Bat (19.2 km) (Table 3). The number of passes detected in each distance category varied greatly for each species or group of species (Fig. 1). After accounting for ship-to-ship differences in monitoring times, we found no difference in nightly bat activity among the intervals (F4,69 = 0.61; P = 0.66). We found a negative association between bat activity and mean nightly wind speed (rs = -0.23, P = 0.04, n = 85). However, mean nightly air temperature (rs = 0.17, P = 0.12, n = 86) and barometric pressure (rs = 0.07, P = 0.52, n = 86) were not significantly associated with activity. Discussion Prior studies of bats observed or detected over open water typically involved bats crossing a barrier between seasonal habitats (Ahlén et al. 2009, Cryan and Brown 2007, Czenze et al. 2011, Dzal et al. 2009, McGuire et al. 2012), but this Table 3. Distances from shore that species or species groups of bats were detected along the mid- Atlantic coast during 2009–2010. Distances from shore (km) Species/species group Minimum Maximum Mean Median Eastern Red Bat 1.2 21.9 8.4 8.8 Big Brown/Silver-haired Bat 2.8 19.2 8.7 8.0 Myotis 2.8 11.5 10.1 11.5 Hoary Bat 5.4 11.5 8.4 8.4 Northeastern Naturalist Vol. 21, No. 2 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 159 explanation is unlikely for our study. Because bats are terrestrial mammals that fly, we expected their detections would be greater near shore and decrease with distance from shore over the Atlantic Ocean. However, we found no differences in bat activity among our 5 distance categories. Our small sample size could make it difficult to identify patterns in bat activity versus distance from shore. Because bats can use the position of the sun at sunset to determine west as well as to calibrate the magnetic field of the Earth for use as a compass, it seems that they could easily navigate over open water (Holland et al. 2006, 2008, 2010; Moser 2011). Why some bats occur over the open ocean many kilometers from shore rather than over land where they can easily find a roost will require further study . The species composition of identified passes suggests that migration by some bats may be occurring off the Atlantic coast. As defined by Fleming and Eby (2003), longdistance migrants are bats that travel >1000 km between summer and winter roosts. Two long-distance migrants, Eastern Red Bat and Hoary Bat, accounted for 81% of the identified passes, with individual contributions of 78 and 3%, respectively. Silver- haired Bats also are long-distance migrants, but Big Brown Bats are considered sedentary, traveling <50 km between seasonal roosts (Fleming and Eby 2003). Furthermore, Big Brown Bats were captured more often during summer months on the Atlantic Coastal Plain, whereas Silver-haired Bats were recorded using acoustic detectors primarily during spring and fall (Johnson and Gates 2008, Johnson et al. 2011, Limpert et al. 2007). Although we cannot rule out offshore foraging by Big Brown Bats (Ahlén et al. 2009), passes labeled as Big Brown/Silver-haired Bat, were most likely made by Silver-haired Bats, and if so, the percentage of long-distance migrants among identified passes could be as high as 93%. Figure 1. Number of passes of each species, group of species, and unidentified bats (NOID) found in each distance category off the Mid-Atlantic Coast in 2009–2010. Northeastern Naturalist 160 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 Vol. 21, No. 2 Regional migrants may also use open water for either migration or feeding. Myotis, specifically Little Brown Bats, are categorized as regional migrants that typically travel 100–500 km between summer and winter roosts (Fleming and Eby 2003), although a recent long-term study on Little Brown Bats found that distance of travel between seasonal roosts could be over 560 km (Norquay et al. 2013). Myotis represented about 7% of identified passes in our study, and the occurrence of Myotis offshore was unexpected, especially because they exhibited low abundance in the coastal region (Johnson and Gates 2008, Limpert et al. 2007, Menzel et al. 2003). The only weather variable associated with bat activity off the mid-Atlantic coast was a negative correlation with wind velocity, indicating that activity decreased as wind speed increased. A similar relationship was found offshore in Europe and on barrier islands in Maryland and Virginia (Ahlén 1997, Ahlén et al. 2007, Johnson et al. 2011). Nevertheless, on some nights we detected bats at wind speeds greater than those reported in terrestrial studies (e.g., Fiedler 2004, Kerns et al. 2005, Reynolds 2006). For example, 37 bat passes occurred at a mean wind speed of 6.1 m/s on 24 September 2009, and 12 bat passes were recorded at a mean wind speed of 6.8 m/s on 25 August 2010. Reynolds (2006), in contrast, reported greatly reduced activity on nights with wind speeds >5.4 m/s in New York, and Fiedler (2004) found few fatalities at wind-power plants, indicating less activity, after nights with wind speeds >4 m/s in Tennessee. We suggest that the dearth of roosting sites available offshore requires the bats to remain volant until they can reach shore, even if wind speeds increase above optimum levels. Although raising the nightly cut-in speed for turbines (i.e., the wind velocity at which a turbine starts to rotate) to 5.0–6.5 m/s reduces fatalities at terrestrial wind-power plants by 44–93% (Arnett et al. 2011, Baerwald et al. 2009), higher cut-in speeds at offshore sites may be necessary because of the frequent bat activity observed at greater wind speeds. Predicting how offshore wind-power plants may affect populations of bats active off the mid-Atlantic coast is difficult. Because bats migrating over land often appear concentrated in certain areas, rather than distributed evenly across the landscape, measuring migratory activity on transects near the proposed sites of wind-energy facilities could provide much needed data for directing development (Baerwald and Barclay 2009, McGuire et al. 2012). Attaching acoustic monitoring equipment to meteorological towers during the pre-construction phase of windpower development onshore has been an effective tool for collecting data on bats (Baerwald and Barclay 2009), and perhaps this method could be employed offshore. In addition, monitoring throughout the months of activity could be done at offshore sites to provide information on seasonal fluctuations in activity. Most developers of offshore wind projects have proposed locations at or beyond the maximum distance at which we recorded bats. For example, 1 wind facility in New Jersey may be located at least 26 km from shore, and a proposal from Delaware plans to site turbines 21 km from shore (BOEM 2013). We postulate that wind-power projects at these distances may have minimal effects on bats, although we caution that our acoustic surveys only detected bats flying near the surface and not at the height of the rotor-swept zone of typical turbines. Overall, relatively few Northeastern Naturalist Vol. 21, No. 2 A.L. Sjollema, J.E. Gates, R.H. Hilderbrand, and J. Sherwell 2014 161 passes of bats were recorded during our study, compared to onshore coastal studies that typically record hundreds of passes of bats nightly (Johnson and Gates 2008, Sjollema 2011), suggesting that mortality of bats at offshore wind turbines may not be as great a problem as it is onshore. Acknowledgments Thanks are extended to the crews of the OSV Bold, F/V Darana R, R/V Hugh R. Sharp, R/V Integrity, and the Lewestown Lady. We are grateful to J. Gartland; F. Kelley; N. Primrose; R. Searfoss; GeoMarine, Inc.; Versar, Inc.; the New Jersey Department of Environmental Protection; See-Life Paulagics; and the US Environmental Protection Agency for facilitating data collection. For help in the field, we thank K. Duren, J. Saville, and J. Smith. This study was funded by the Maryland Department of Natural Resources, Power Plant Research Program. 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