Barbastelle Bats in a Wind Farm: Are They at Risk?

Home , Common noctule, Eptesicus, Northern bat, Western barbastelle

European Journal of Wildlife Research (2018) 64:43 https://doi.org/10.1007/s10344-018-1202-1

ORIGINAL ARTICLE

Barbastelle bats in a wind farm: are they at risk?

Grzegorz Apoznański1 & Sonia Sánchez-Navarro2,3 & Tomasz Kokurewicz1 & Stefan Pettersson4 & Jens Rydell2

Received: 13 December 2017 /Revised: 6 June 2018 /Accepted: 11 June 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract We need to know if and how western barbastelles Barbastella barbastellus are affected by wind farming in Sweden. This is because wind turbines are frequently constructed in barbastelle habitats and yet there is no national guideline on how the arising conflict should be handled. We studied the movement, behavior and mortality of a barbastelle population at a wind farm in southern Sweden, using radio-telemetry, automatic bat detectors and carcass searches. The tagged bats (6 males and 8 females) roosted mainly under loose bark of dead oak trees and foraged in patches of mature deciduous woodlands or pockets of mature spruce trees within 15 km of the roosts. Extensive areas of young spruce plantation, open farmland and lakes were not used for roosting or foraging but were crossed by commuting bats. Continuous recordings with bat detectors frequently picked up barbastelles at forest edges 30 m from the turbines, but rarely over the turbine pads within 10 m from the turbines and never at heights of 30 and 100 m at the turbine towers. Barbastelles were apparently not attracted to the wind turbines and did not seem to interact with them in any way. Carcass searches under 10 wind turbines at 1-week intervals over three summers did not reveal any dead barbastelles, although three other species were recovered. We conclude that wind farming is not nessarily incompatible with effective conservation of barbastelles in Sweden, but instead of focusing on wind turbines, effors should concentrate on (a) preservation and restoration of mature, age-structured deciduous woodlands and spruce forests, including very small and isolated patches, which provide food and roosts, and probably also (b) avoidance of outdoor lighting in areas used by barbastelles. Designating large circular buffer zones around each known or suspected colony according to current practice would be inefficient or meaningless in our case, because barbastelles use extensive home ranges and switch roost frequently. We argue that barbastelle management must be applied on a landscape scale.

Keywords Acoustic monitoring . Carcass search . Echolocation . Radio-telemetry . Wind energy

Introduction * Sonia Sánchez-Navarro [email protected] The increasing demand for electricity worldwide inevitably Grzegorz Apoznański leads to environmental impacts in one form or another [email protected] (Sánchez-Zapata et al. 2016). For example, wind turbines have become a serious problem in areas where there is bat Tomasz Kokurewicz [email protected] activity. Bats (Chiroptera, Mammalia) are killed, sometimes in large Stefan Pettersson [email protected] numbers, by the moving rotor blades or by pressure differ- ences causing so called barotrauma, when flying and feeding Jens Rydell around the turbine towers (Kunz et al. 2007; Lehnert et al. [email protected] 2014; Frick et al. 2017). The threat from wind turbines does 1 Wrocław University of Environmental and Life Sciences, Institute of not apply to all bats, however, and it is important to distinguish Biology, Department of Vertebrate Ecology and Palaeontology, those that are affected from those that are not, so that mitiga- Kożuchowska 5b, 51-631 Wrocław, Poland tion measures can be adequately aimed at the right targets. Bat 2 Biology Department, Lund University, SE-223 62 Lund, Sweden species that live among or below the forest canopy are be- 3 Department of Evolutionary Ecology, Estación Biológica de lieved to be much less at risk than those that fly and feed in Doñana-CSIC, Américo Vespucio 26, 41092 Sevilla, Spain the open air at higher altitude and it is the latter category that 4 EnviroPlanning AB, SE-411 04 Göteborg, Sweden needs most attention (Arnett et al. 2015). 43 Page 2 of 10 Eur J Wildl Res (2018) 64:43

The western barbastelle Barbastella barbastellus of Halland (57° 00′ N, 12° 40′ E), on the west-facing slope (Schreber, 1774), the focal species of this study, is associated forming the transition zone between the coastal alluvial plain, with forests (Russo et al. 2004), but sometimes feeds above mostly used for agriculture, and the slightly elevated (approx. the canopy (Sierro 1999) and in other open situations 100 m a.s.l.) inland plateau with moraine, which is mostly (Eriksson 2004; Greenaway 2005; Ancillotto et al. 2014). covered by coniferous forests and bogs and managed for for- The possible vulnerability of barbastelles to wind turbines estry (Fig. 1). has never been studied in detail and remains unknown. The area that is now the wind farm was historically trans- However, there is an explicit need to investigate if and how formed into heathland with patches of deciduous or mixed barbastelles react to wind turbines in Sweden, partly because forest, including birch Betula spp., beech Fagus sylvatica, this species often lives in areas of interest for wind farming oak Quercus robur and spruce Picea abies.Overthelast (Ahlén 2015). It may also be important to find suitable 150 years, extensive areas were planted with spruce and pine methods for effective conservation of barbastelles in wind Pinus sylvestris, much of which was subsequently either cut or farm areas. destroyed in two severe storms in 2005 and 2007. At present The barbastelle is more or less rare over much of its range the study area (including the wind farm) is dominated by and shows a decreasing population trend (IUCN 2016). It is planted spruce in different aged stands (ca 70% of the area). included in Annexes II and IV of the EU Habitats Directive Some semi-natural deciduous forest (ca 15%), old spruce and is classified as ‘near threatened’ on a global scale (IUCN stands (ca 10%) and natural bog vegetation with alder 2016). In Sweden, where this study took place, it is classified (Alnus spp.), birch (Betula spp.) and pine (Pinus sylvestris) as ‘vulnerable’ (ArtDatabanken 2015). (5%) also remain, however, particularly in wet, steep, rocky The deciduous forests in the coastal province of Halland in or otherwise inaccessible places, where most of it is still un- southwestern Sweden are a stronghold for the barbastelle in affected by forestry. In addition, deciduous woodland remains northern Europe and harbours what seems to be a thriving as islands of different sizes on low hills on the open fields west population. This area has been intensively surveyed for bats. of the wind farm. The distribution of these habitats is illustrat- The barbastelle shows a continuous distribution and is one of ed in Table 1 and the maps (Figs. 1, 2 and 3). the commonest bats in the area (Petterson and Gylje Blank 2016). However, Halland is also exposed to the prevailing Bat recordings south-western winds from the sea and is therefore of interest for wind farming. Hence, there is a potential conflict between We monitored bat activity continuously near the wind turbines exploitation of the wind resource and conservation of from June to the end of September 2014–2016, using three barbastelles (and other bats) in that region. automatic real-time full spectrum bat detectors (Pettersson D- To identify the impact that wind turbines may have on 500X, Pettersson Elektronik, Sweden). The detectors were barbastelles, we studied the bats’ behaviour in and near a wind installed inside the base of the turbine towers and connected farm in Halland, with strong emphasis on the use of space near via cables to external electret microphones mounted on the wind turbines for roosting, foraging and commuting. We test- nacelle housing at a height of ca 100 m and on the tower at ed the following specific questions. a height of ca 30 m. The microphones at the nacelles and (a) Are barbastelles attracted to wind turbines for feeding, towers were directed ca 20o downwards and were shielded commuting or roosting? from rain and wind. We also monitored bats from the ground (b) Are barbastelles subject to increased mortality caused at the turbine pads (gravel plain surrounding the tower) near by wind turbines? (< 10 m) the base of the turbines, using the same equipment (c) Are barbastelles dependent on other features occurring but with the microphones directed horizontally. For shorter within or near the wind farm? periods, we also placed additional detectors at the adjacent forest edge with the microphones directed parallel to it. The detectors were run either on external power from the facility Materials and methods (when the detector was placed on or inside the tower) or on four 1.5 V AA-batteries (when the detector was placed away Study area from the turbine). The three turbines used for bat detector recordings (no. 5, 6 and 10) were selected based on the result The Askome wind farm, where this work was done, consists of a post-construction survey of all turbines in 2014–2015 and of 10 General Electric 2.75-103 turbines, with hub height which showed that barbastelle activity was most frequent at 98 m, rotor diameter 103 m and rotor sweep area 8332 m2 turbines 5, 6 and 10 (Rydell et al. 2018). (https://en.wind-turbine-models.com/turbines/747-general- Detectors were activated from sunset to sunrise and set to electric-ge-2.75-103#datasheet). The wind farm has been in automatic triggering with low-pass filter on, sensitivity at ‘me- operation since 2013. It is located in the Swedish province dium’, 500-kHz sampling rate and 3-s recording time. Eur J Wildl Res (2018) 64:43 Page 3 of 10 43

Fig. 1 Map of the study area at Askome wind farm in Halland and its location in southern Sweden. Black stars denote wind turbines

Recording settings were input gain 45, trigger level 80 and female caught in 2016 was tracked back to the maternity col- trigger interval 5 s. Recorded signals were stored as wave-files ony, where another seven lactating females were captured the on 64 GB Compact Flash memory cards, which were checked following day (25 July). The netting efforts were made on and changed two or three times per month. Recordings were mild and dry nights with slow wind. later automatically sorted using SonoChiro version 3.33 and We used three 9 m and one 6 m monofilament nets files containing bat calls were analysed manually using (Ecotone, Poland) on poles (2.5 m) fixed to the vegetation BatSound version 4.03. Barbastelles were easily and unam- by ropes, except at the maternity roost, where we used a 6- biguously recognised to species by their unique echolocation m hand-held net. The nets on poles were checked every calls (Russ 2012)(Table2). 15 min, while the hand-held net obviously was attended constantly in front of the roost for the few minutes it took Mist netting and radio-telemetry to catch a sufficient number of bats. Each captured bat was identified to species, sexed and aged (adult vs. juvenile, The barbastelles were captured in mist-nets set over roads based on ossification of the phalangeal epiphyses). within the wind farm. The first capture attempt was made 24 Females were classified as lactating if the mammary glands July 2016, when two males and one lactating female were were swollen and enlarged nipples surrounded by hairless captured. In 2017, we caught four males 14 July. The captured areas were present. Other species caught during netting bats were tagged (see below) and then released. The first sessions were immediately released.

Table 1 The density of potential barbastelle roosts in various Habitat No. of transects Area covered No. of potential Density of potential −1 woodland habitats near the wind (ha) roosts roosts (ha ) farm as assessed visually in daytime by walking transects 50– Oak forest 4 2.3 60 26.1 100-m long. Dead or dying trees Beech forest 6 1.8 74 17.9 with loose bark were recorded Woodland remnants on fields 3 3.0 35 11.8 within 50 m (25 m in dense forest) from the transect Mires and bogs 6 3.2 29 9.1 Planted spruce 6 5.1 19 3.7 43 Page 4 of 10 Eur J Wildl Res (2018) 64:43

Fig. 2 Movements of tagged bats in the study area at Askome wind farm 2016 (above) and 2017 (below). The dots represent foraging locations used by the females in 2016 and the six males separately. The red pentagon shows the maternity roost and the triangles show other roosts. Minimum convex polygons (MCP) encompassing the feeding and commuting points of the females and each of the males are also indicated. The wind turbines are shown as black stars. Maps from Lantmäteriet (2016)

Additionally, an evening emergence count made later, sug- antennas (Titley Electronics, Australia). Cars permitted quick gested that the colony consisted of ca. 30 females and their shifts between tracking locations e.g. at the wind turbines on babies and that females forming the maternity roost were lac- top of hills and other good tracking locations, mostly using the tating during the time of study (July–August 2016). In 2017, access roads connecting the turbines. In a few locations that we did not find the colony and we did not catch any females, were inaccessible to cars, we proceeded on foot. When a sig- although we searched intensively with automatic bat detectors nal from a tagged bat was received, its GPS location, azimuth, and visual observations at known roosts during the expected receiver gain and signal strength were noted. The bat’sposi- time of emergence. tion was later estimated based on triangulation of the fixes After assuring that the weight of the transmitter did not acquired by each individual team. In case of a bat remaining exceed 5% of the bat’s body mass (Aldridge and Brigham in contact with only one team, a homing-in-approach was 1988), LB-2X transmitters (0.32 g; Holohil Systems, used. This method relies on getting close to a foraging indi- Canada) were attached to the inter-scapular region by bonding vidual in order to obtain the best information regarding its adhesive (Torbot, Rhode Island, USA). The tagged bats were position. released within 30 min after capture. They were subsequently Bearings were compared daily in order to estimate the best followed by three experienced and mobile tracking teams dur- positions for further deployment of field teams during the ing 12 nights in 2016 (25 July–7 August; the night of 31 July following night, but after a few days of tracking we had ob- was excluded because of rain) and 16 nights in 2017 (14–30 tained enough information about flight patterns and foraging June). We used three Australis 26k receivers with Y-3 sites to initially locate the teams along predicted commuting Eur J Wildl Res (2018) 64:43 Page 5 of 10 43

Fig. 3 Movements of barbastelles within the Askome wind farm. The wind turbines are shown as black stars. The black dots are commuting bearings and the red lines represent commuting routes as identified by radio-tracking and, near turbines 5, 6 and 10, also using bat detectors. The pink dots represent foraging locations. Legends as in Fig. 1.Mapfrom Lantmäteriet (2016)

Table 2 Home range size, based on minimum convex polygons, Category Year Home Number (%) of foraging locations and habitat use of barbastelles range based on radio-tracking data (ha) Deciduous Wooded Mires Spruce Spruce Farmland woodland wetland and bogs >15yrs <15yrs

Females n = 8 2016 6415 21 (44.7) 11 (23.4) 4 (8.5) 11 (23.4) 0 0 Male 1 2016 1145 9 (47.4) 5 (26.3) 2 (10.5) 3 (15.8) 0 0 Male 2 2016 1115 6 (35.3) 1 (5.9) 3 (17.6) 6 (35.3) 1 (5.9) 0 Male 3 2017 1970 13 (41.9) 1 (3.2) 0 9 (29.1) 7 (22.6) 1 (3.2) Male 4 2017 1382 12 (31.6) 5 (13.2) 1 (2.6) 16 (42.1) 4 (10.5) 0 Male 5 2017 1497 12 (52.2) 5 (21.7) 0 4 (17.4) 2 (8.7) 0 Male 6 2017 1470 6 (37.5) 3 (18.8) 2 (12.5) 4 (25.0) 0 1 (6.2) Total 79 (41.4) 31 (16.2) 12 (6.3) 53 (27.8) 14 (7.3) 2 (1.0) 43 Page 6 of 10 Eur J Wildl Res (2018) 64:43 paths. Subsequently, the tracking teams either followed the in dense forest) from the transect was recorded on a GPS bats from cars or sent information on their position and the receiver. As potential roosts were considered dead or dying bat’s flight direction to another team, located in a position trees of at least 25 cm diameter at breast height (DBH) and more favourable for continued tracking. To track the move- with loose bark with access to the cavity under the bark from ments of the bats in relation to the wind turbines, which was below. For each potential roost we also recorded the tree spe- one of the main goals of this study, the teams tracked from the cies and if the tree was dead or alive. Roosts also occurred in turbine pads in the beginning and the end of each night, i.e., wooden barns, which are a common feature of Swedish rural when the bats were commuting between the roost and the landscape. They are widely available and therefore we did not wind farm. From these positions the bats’ flight routes towards quantify their availability in situ. and past the turbines could be followed. At the end of each night, one team checked the known roosts for tagged individ- Carcass searches uals. In cases when a bat did not return to its known roost in the morning, further searching was carried out in daytime to We searched the turbine pad, access roads and other search- find the new roost. able areas within 50 m of each of the 10 turbines for bat The distance between the observer and the tracked bat was carcasses. The searchability of the area within the 50 m circle estimated for each fix from the receiver gain and signal was classified as difficult, medium or easy; and we omitted strength. We defined ‘foraging’ as a bat flying constantly areas classified as difficult. On average, the searched area was within the same habitat patch for > 5 min, usually with fre- 54% of the total area within the 50 m radius (7850 m2 per quent changes in direction back and forth. If such behaviour turbine) at approximately weekly intervals between June and was observed for < 5 min., it was treated as a single bearing, September 2014–2016, i.e. we made 12–14 visits to the park but if it stayed longer, every subsequent 5-min period was each year and 86–128 searches per year. The main purpose of treated as a new bearing/record and the azimuth and signal this exercise was to obtain an estimate of the fatality rate of strength were measured again. ‘Commuting’ was normally a barbastelles (and other bats) in the wind farm. unidirectional movement, e.g. with the signal strength first In summer 2016, we also made experiments to estimate the increasing from one direction, then decreasing and finally searcher efficiency and carcass removal rate for later calcula- vanishing in the opposite direction, but when a bat stayed < tion of the total fatality rate at the site, using the methodology 5 min within the same patch it was also considered as com- suggested by Brinkmann et al. (2011). For the experiments, muting (Ciechanowski et al. 2016). we used dead but fresh bats of different species found in other Acquired fixes were applied on a ‘blank’ map in Map wind farms (N = 19), but we also had to complement with grey Source 6.14 (Garmin Inc., USA). The idea behind this was to house mice in some cases (N = 30) because of shortage of bat control for human errors due to the tendency to adjust fixes to carcasses. The mice were purchased frozen in a zoological suitable habitats. The outcome of the process was put into shop. Estimation of the detection rate was calculated in the ArcEditor 10.0 (Environmental Systems Research Institute web-based application available at Wildlife Fatality Estimator Inc. USA), which allowed us to calculate distances of particu- platform (wildlifefatalityestimator.com). Detectability was 30 lar bearings from the roost and also to draw the individual and and 21% for easy and medium search ability areas, colony home ranges by use of minimum convex polygon respectively. To estimate the fatality rate at the wind turbines method (MCP). After uploading the tracking data into the in Askome, we used the free software EoA (Evidence of mapping software, we made a rough estimate of the error, Absence) v. 2.0 (Dalthorp et al. 2017). This program was using the distance between the fix point and points five degrees developed specifically for estimation of fatality rates in wind to the right and to the left of it, respectively, at a distance of farms where few carcasses are found. 500 m. With this method our estimated error was ± 40 m from the fix point at this distance and ± 10 m at a distance of 100 m. This means that our maximum error was about 4% (3600/ Results 1000 = 3.6) or smaller than the length of the turbine pads (ca. 50 × 50m). Comparing several simultaneous fixes of the same Reaction to the wind turbines bat sometimes allowed us to reduce the error even further. One of our principal purposes was to find out how the bats Roost availability move and use the area in the immediate vicinity of the wind turbines. Hence, at the beginning of each tracking night, one The availability of potential roost trees in and near the wind observer was placed at turbine no. 7, from which the tagged farm was assessed by walking transects in each of five habitats females could be detected while still in the maternity roost present in the study area. Each transect was 50–100 m long 8 km away, while other observers scanned from beneath other and the position of each potential roost tree within 50 m (25 m turbines. After emergence from the roost, the females usually Eur J Wildl Res (2018) 64:43 Page 7 of 10 43 approached the wind farm in almost straight flight, as evident Based on the data from 2016, the area used by the females by successive bearings along a line and increasing signal was extensive (64 km2) and reached far beyond the wind farm. strength, but a few hundred meters from the turbine they al- The males also used large home ranges (10–20 km2 each), ways turned, as noted from rapid changes in the bearings. which overlapped in early summer (2017) but apparently not They usually flew at least 100 m from the turbines and never in late summer (2016). Home ranges for the females and each crossed the turbine pads. The sudden increase in signal of the males, based on minimum convex polygons (MCP), are strength that would be expected over open ground was never shown in Fig. 2. heard in this situation. Likewise, observers standing under a Many regularly used feeding sites were located 10–14 km turbine never recorded the 180 degree change in bearing, west of the maternity roost, up to 3 km on either side of the which would have been obvious if the bats flew over them. boundarybetweenforestandopenfarmlandtothewest. Hence, it is clear that tagged bats ignored or avoided the top of Several small isolated patches of woodland on open farmland the hills with the turbines (Fig. 3). were also used. The bats freely crossed quite extensive (1– The bat detectors placed at ground level on the turbine 2 km) open areas, including crop fields, young spruce planta- pad—edge of the forest interface, picked up echolocation calls tions and lakes, on their commuting flights. of barbastelles relatively frequently, but those placed on the pad near the turbines seldom did so (Table 3). Barbastelles Roosts were never detected by microphones mounted at the turbine towers at 30 m or on the nacelle housing at 100 m, despite Using radio-tracking, we found 17 roosts, three of which were continuous monitoring at nacelle level during 851 detector- used by the females of the maternity colony and located in nights (Table 3). For comparison, the microphones at the na- narrow spaces behind the planks in the walls of wooden barns celles picked up about 1000 passes of at least 4 other species (Fig. 2). The other 14 roosts were used by six different males (soprano pipistrelle Pipistrellus pygmaeus, parti-coloured bat and were located behind loose bark on oaks (N =6)orpines Vespertilio murinus,commonnoctuleNyctalus noctula and (N = 2) or in the walls of wooden barns, similar to those used northern bat Eptesicus nilssonii) during the same time by the females (N = 6). The tree roosts were all inside patches (Rydell et al. 2018). of deciduous forest or, in the case of pines, on a peat bog, while the barn roosts were found among other buildings on Spatial distribution and movement open farmland mostly west of the wind park. For male no. 4, which was tracked in June 2017, we found indication of night Altogether we identified 191 feeding sites used by the bats, 83 roosting in deciduous forest, but because of very short time in 2016 and another 108 in 2017. Most of them were located spent there by the bat we could not locate it precisely. The bats in or near pockets of mature deciduous woodland (79 sites), never used the wind turbines or associated structures for day- among mature spruce (53) and on wooded wetlands (31; or night-roosting, as suggested for other bat species (Cryan Table 2). 2008).

Table 3 The horizontal and vertical distribution of barbastelle activity base of the turbine, (b) at tree-top level (30 m elevation) with near wind turbines as recorded by 3 or 4 automatic bat detectors from microphones mounted on the surface of the turbine tower and (c) at June to the end of September 2014–2016. The microphones were nacelle level (100 m) with a microphone mounted on the nacelle house mounted at (a) ground level, either at the forest edge 30 m from the surface. The number of recording nights are in parentheses. The locations base of the wind turbine or on the adjacent turbine pad < 10 m from the of the turbines are shown in Fig. 2

Turbine number Year Mean number of barbastelle recordings per night (number of nights)

(a) Ground level—0 m (b) Treetop level—30 m (c) Nacelle level—100 m

Forest edge—30 m from turbine Gravel area—< 10 m from turbine

5 2014 0.52 (21) ––0 (103) 5 2015 1.47 (19) ––0 (105) 6 2014 2.91 (11) ––– 6 2015 2.47 (19) ––– 6 2016 2.00 (12) 0.05 (114) 0 (113) 0 (114) 10 2014 3.82 (23) ––0 (103) 10 2015 0.37 (19) ––0 (105) 10 2016 0 (7) 0.46 (94) 0 (94) 0 (114) 43 Page 8 of 10 Eur J Wildl Res (2018) 64:43

The availability of potential tree roosts, as assessed visually suggesting that barbastelles may visit and investigate other in daytime, was high (9–26 roosts per ha) in all habitats except high structures (lattice towers) located within forest (Budenz in the spruce plantations and on open farmland (Table 1). et al. 2018). However, in light of our observations, we suggest They were nearly always found in dead or dying oaks, even that barbastelles are less likely to be killed at the wind facilities in forests dominated by beech and other deciduous species. and in support of this, we did not find any dead barbastelles However, on bogs and mires, potential roosts were located in during our searches. Indeed, only four dead barbastelles have pines, and in spruce plantations, where trees had been attacked ever been found under wind turbines in Europe, three in the by bark beetles (Kortmann et al. 2017). We retroactively esti- south (Rodrigues et al. 2014; one of them was subsequently mated (from the map) that there were at least 100 barns within identified by one of us (SSN) as a lesser noctule Nyctalus the area used by the bats. Most of them were probably poten- leisleri) and one in Denmark (www.eurobats.org). tial barbastelle roosts. The barbastelles tagged in our study freely crossed open areas such as fields, lakes and young spruce plantations and in Carcass searches another study barbastelles routinely crossed a major motorway (Kerth and Melber 2009). We therefore consider it un- The carcass searches near the turbines revealed 8 dead bats in likely that barbastelles would be hindered by the access roads total (3, 1 and 4 in 2014, 2015 and 2016, respectively), be- or other wind farm infrastructure. However, new access roads longingto3species(2Nyctalus noctula,4Pipistrellus may increase the accessibility of the area and open it up to pygmaeus and 2 Eptesicus nilssonii), but no barbastelles. forestry and other forms of exploitation. Barbastelles could The estimated total mortality for the park was 28, i.e. 2.8 bats therefore be affected indirectly by the new infrastructures at per turbine per year. wind farms.

Suggestions for conservation of barbastelles in wind Discussion farm areas

The barbastelle is usually regarded as a forest species (Sierro Currently suggested practices for conservation of barbastelles and Arlettaz 1997;Sierro1999; Russo et al. 2004)anda in Sweden and elsewhere in Europe include establishment of highly specialised predator on moths (Lepidoptera), particu- buffer zones around each known or suspected maternity col- larly on moths that possess a bat defence system based on ony. The protected area is intended to be free from wind tur- ultrasonic hearing (Andreas et al. 2012). Barbastelles employ bines and presumably also from other forms of exploitation. a unique and sophisticated echolocation system called ‘stealth The suggested size of such zones is based on radio-telemetry echolocation’ to overcome this trait (Görlitz et al. 2010). The studies and varies from 2-km radius in Sweden (Ahlén 2015) specialised foraging and feeding requirements of the and 4 km in Germany (Hillen et al. 2009) to 7 km in England barbastelle probably means that it relies on particular feeding (Zeale et al. 2012). In our case, this approach would be inef- patches that provide a high diversity and abundance of its ficient regardless of chosen zone size, because most of the area preferred food. Such patches include natural deciduous and used by the females and all of that used by the males would coniferous woodland as well as wooded wetlands and wooded fall outside the protected zone. meadows (Eriksson 2004;Greenaway2005). In some cases, Rather than focusing on wind turbines, efforts to conserve barbastelles forage over areas of bare rock, which radiate heat and manage barbastelles in Halland should concentrate on the and attract moths in late summer (Ancillotto et al. 2014). Our preservation and perhaps restoration of remaining old forest tagged bats used many small high-quality patches of wood- and woodland patches, deciduous as well as coniferous, that land or mature spruce forest over an extensive area for forag- maintain a diverse tree species and age structure. Such habitat ing and roosting and routinely crossed quite extensive open patches are most likely of critical importance for barbastelles, areas on their way to and from these patches. Our findings are as they provide both food (moths) and roosts (in trees). Since generally consistent with previous studies (Eriksson 2004; barbastelles often feed in relatively open places and ecotones Russo et al. 2004; Greenaway 2005; Hillen et al. 2009; within and around the patches (Sierro 1999; Eriksson 2004), Zeale et al. 2012), although the bats flew relatively long dis- even very small and isolated patches are likely to be impor- tances between roost and feeding sites in our case. tant. Indeed, a fragmented landscape with many small patches of good habitat provides suitable feeding sites along ecotones. Barbastelles’ reaction to wind turbines Small deciduous woodland patches on open land may serve as mating stations for hill-topping moths and other insects, which Some species of bats are attracted to wind turbines, which they may be attracted from surrounding farmland (Alcock 1987) visit during their foraging or commuting flights (Cryan et al. and provide ephemeral food sources for barbastelles. In our 2014; Roeleke et al. 2016) and there is a recent study study area in central Halland where the barbastelle population Eur J Wildl Res (2018) 64:43 Page 9 of 10 43 probably is continuous (Pettersson and Gylje Blank 2016) Alcock J (1987) Leks and hilltopping in insects. J Nat Hist 21:319–328 conservation measures should be applied at a landscape scale. Aldridge HDJN, Brigham RM (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% "rule" of radio-telemetry. J We do not know why the maternity roost was located so far Mammal 69:379–382. https://doi.org/10.2307/1381393 from the major feeding area. However, a similar situation was Ancillotto L, Rydell J, Nardone V, Russo D (2014) Coastal cliffs on observed in two British studies of barbastelles (Greenaway islands as foraging habitats for bats. Acta Chiropterologica 16: – 2005; Zeale et al. 2012). 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The fort was a designated Natura 2000 site because of MM, Hayman DTS, Fricker PD, Bonaccorso FJ, Johnson DH, Heist K, Dalton DC (2014) Behavior of bats at wind turbines. Proc Natl the barbastelles, but it was delisted after the bats disappeared Acad Sci 111:15126–15131. https://doi.org/10.1073/pnas. (Rydell 2006). We suspect, so far on somewhat loose grounds, 1406672111 that barbastelles are very light-averse bats, and until we know Dalthorp D, Huso M, and Dail D (2017). Evidence of absence (v 2.0) better, uninterrupted darkness should be considered as an im- software user guide: U.S. Geological Survey Data Series 1055, 109 p portant resource for this bat as well as for its food, the .doi:https://doi.org/10.3133/ds1055 Eriksson, A (2004). Habitat selection in a colony of Barbastella tympanate moths (McGregor et al. 2016; Wakefield et al. barbastellus in south Sweden. B.Sc. Thesis. Department 2017). Conservation Biology, SLU, Uppsala Frick W, Baerwald E, Pollock JF, Barclay RMR, Szymanski JA, Weller Acknowledgments We acknowledge the owners of the wind turbines TJ, Russel AL, Loeb SC, Medellin RA, McGuire LP (2017) Askome Vind AB for their participation in this project, including practical Fatalities at wind turbines may threaten population viability of a help with the detectors and microphones, Justyna Błesznowska. Ewelina migratory bat. Biol Conserv 209:172–177. https://doi.org/10.1016/ Małkowicz and Julio Rabadán for assistance in the field, and last but not j.biocon.2017.02.023 least all the land owners who more or less deliberately accepted our Görlitz HR, ter Hofstede HM, Zeale MRK, Jones G, Holderied MW presence around their houses at night in search of tagged bats. We also (2010) An aerial-hawking bat uses stealth echolocation to counter like to thank Tim Hipkiss for checking our English text. moth hearing. Curr Biol 20:1568–1572. https://doi.org/10.1016/j. cub.2010.07.046 Funding information This project was funded by the Swedish Energy Greenaway F (2005). Advice for the management of flightlines and for- Agency through the Vindval program (no. 2016-000101). Capture and aging habitats of the barbastelle bat Barbastella barbastellus. tagging of bats were carried out under licence from the Swedish English Nature 657 Environmental Protection Agency (NV-08056-11) and the Ethical Hillen J, Kiefer A, Veith M (2009) Foraging site fidelity shapes the spatial Committee in Malmö/Lund (M 65-16). organization of population of female western barbastelle bats. Biol Conserv 142:817–823. https://doi.org/10.1016/j.biocon.2008.12. 017 Hillen J, Kiefer A, Veith M (2010) International fidelity to roosting hab- References itat and flight paths by female western barbastelle bats. 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