TY - JOUR
AU - Barclay, Robert M, R
AB - Abstract As development of wind energy facilities continues, questions of why fatalities of migrating insectivorous bats occur at turbines still remain. Numerous hypotheses have been proposed, including a feeding-attraction hypothesis that suggests bats may be attracted to insects congregating near turbine nacelles. To test this hypothesis, we analyzed echolocation calls of hoary (Lasiurus cinereus) and silver-haired (Lasionycteris noctivagans) bats recorded over 72 nights at a wind energy facility in Southern Alberta, Canada. We recorded calls at 3 heights: 67 m at turbine nacelles, 30 m at meteorological towers, and ground level at turbines and meteorological towers. We used feeding buzzes as indicators of foraging behavior. We compared the occurrence of feeding buzzes across heights, and between turbines and meteorological towers to test the prediction that if bats are attracted to turbines for foraging, there will be a greater proportion of feeding buzzes at turbines, and in particular, at nacelle height. We found no significant evidence that foraging rates were higher at nacelle height compared to 30 m or ground level, or between turbines and meteorological towers for either species. For silver-haired bats, foraging activity was greater at meteorological towers, and in particular, at 30 m height. These results do not support the feeding-attraction hypothesis for silver-haired or hoary bats, and suggest that while some bats forage in the vicinity of wind turbines, they are not specifically attracted to turbines to feed. bats, bat fatalities, foraging, hoary bat, silver-haired bat, wind turbine Wind energy production continues to grow rapidly worldwide (AWEA 2017; GWEC 2017; CanWEA 2018). Although wind energy is often viewed as an environmentally friendly alternative to burning fossil fuels, the impact on bats remains a concern (Arnett et al. 2016; Barclay et al. 2017; Frick et al. 2017). In North America, the majority of bat fatalities at wind turbines are migratory species (Arnett and Baerwald 2013). Numerous hypotheses have been developed to explain these deaths, including proposed reasons for bats to be attracted to turbines (Kunz et al. 2007; Cryan 2008; Cryan and Barclay 2009). We explored one of these hypotheses: concentrations of insects around wind turbines (Ahlén 2003) attract insectivorous bats, resulting in fatalities by direct collision with moving turbine blades or barotrauma (Baerwald et al. 2008; Rollins et al. 2012). It is proposed that insects are attracted to the warmth of the nacelle or the color of the wind turbine, or use the turbine for swarming associated with mating behaviors (Ahlén 2003; Kunz et al. 2007; Cryan and Barclay 2009; Rydell et al. 2010; Long et al. 2011). As detection of insects by bats via echolocation occurs over relatively short distances (i.e., typically < 10 m; e.g., Surlykke and Kalko 2008), the hypothesis is that bats initially encounter insect concentrations at turbine nacelles and spend more time foraging in that location, or learn to associate turbines with foraging opportunities (Cryan and Barclay 2009). Previous studies investigating whether bats feed around turbines produced conflicting conclusions. Some studies observed concentrations of bats hunting around turbines (Ahlén 2003, 2007; Horn et al. 2008). Other studies recorded few (Foo et al. 2017) or no (Johnson et al. 2004) feeding buzzes (the characteristic echolocation calls associated with the final stages of prey capture—Griffin et al. 1960; Fenton and Bell 1979) around turbines, suggesting that bats were not preferentially feeding at them. However, no studies to date have assessed the foraging attraction hypothesis by comparing bat foraging activity at turbines, versus away from turbines, or between ground level and nacelle height. Studies that have investigated feeding behavior of migrating bats while en route indicate that hoary (Lasiurus cinereus) and silver-haired (Lasionycteris noctivagans) bats feed during migration (Valdez and Cryan 2009; Reimer et al. 2010; Foo et al. 2017), yet were inconclusive regarding where feeding took place (i.e., around turbine rotors, or away from them). Therefore, the goal of our study was to test the feeding-attraction hypothesis by comparing the acoustic activity and feeding behavior of migrating bats at wind turbines and away from turbines, and at different heights. We analyzed echolocation recordings to determine whether foraging activity varied between locations and among heights. We predicted that if bats are attracted to wind turbines because of concentrations of insects around the nacelle, then the total acoustic activity recorded and the proportion of acoustic activity involving feeding buzzes would be significantly greater at turbines than away from them, and significantly greater at nacelle height than at lower heights. Materials and Methods We recorded echolocation calls at the 2,023-ha Summerview wind energy facility, in southwestern Alberta, Canada (49°35′04″N, 113°47′48″W). There were 39 Vestas V80 turbines at the installation. The surrounding habitat consisted of mixed agriculture and native mixed grasslands (see Baerwald and Barclay 2011 for details). We recorded echolocation activity using 8 calibrated Anabat II ultrasonic detectors with CFZCAIMs (Titley Electronics, Ballina, Australia). These were rotated weekly among 10 turbines and kept stationary at 2 meteorological towers from 15 July to 30 September 2007, the period of migration and highest fatality rate of bats at our site (Baerwald and Barclay 2011). To select turbines for echolocation monitoring, we divided the wind energy facility into 4 quadrants (NW, NE, SW, SE) and categorized each turbine as having a high or low fatality rate, based on carcass searches performed in 2005. We then randomly chose 1 “high-fatality” and 1 “low-fatality” turbine within each quadrant. In addition to the initial 8 turbines selected, 1 additional “high-fatality” and 1 “low-fatality” turbine were randomly selected from the remaining turbines with no preference for quadrant location (Baerwald 2008). Anabat detectors were mounted in weatherproof boxes on turbines and meteorological (met) towers to record echolocation calls at ground level, 30 m, and 67 m. Met towers were located an average of 3.8 km away from the focal turbines (range: 1.03–6.25 km). Ground-level detectors were mounted approximately 1.5 m above the ground at both met towers and at the base of wind turbines. Detectors at 30 m were mounted on 50-m tall met towers. Detectors at 67 m were attached to turbine nacelles at hub height. All detectors at ground level and 30 m pointed north. We positioned detectors on turbines toward the back of the nacelle, parallel to the blades. Because nacelles rotate with the wind, we could not fix detectors to always point north, so we positioned detectors to point north as often as possible given the dominant wind direction (west-southwest). Each turbine and meteorological tower was sampled at least twice throughout the study period. The Anabats collected data from sunset to sunrise. This study conforms to published ASM guidelines for the use of wild mammals in research (Sikes et al. 2016). We reviewed Anabat files both visually and acoustically using AnaLookW version 3.2.15 and wave files. We classified passes (defined as a sequence of calls contained in a single recorded acoustic data file) into 2 categories: 1) passes containing a feeding buzz (terminal phase), indicative of foraging behavior, and 2) passes lacking a feeding buzz, containing search or track phases only (Fig. 1). A third type of pass was observed during analysis and was classified as an “abrupt-detection” pass. It consisted of track- or terminal-phase calls with no initial search phase; these abrupt passes occurred within the first 100 ms of a recording and represented the sudden start of a rapid series of echolocation calls, rather than a more typical pass involving calls that increase in intensity as the bat approaches the microphone. Changes in call phase were identified by a change in frequency and repetition rate. We defined search, track, and terminal phases by duration and frequency of the calls based on Barclay (1986) (Table 1; Fig. 1). The typical time interval between calls for each phase was determined by observing complete feeding buzzes found in the data set, and calculating the typical range of inter-call intervals observed (Table 1). Using a combination of call characteristics (minimum frequency [Fmin], duration, and slope), passes were identified as hoary bat or silver-haired bat (see Baerwald and Barclay 2009 for details). Silver-haired bat and big brown bat (Eptesicus fuscus) echolocation calls are difficult to distinguish from each other (Betts 1998), but because of the strong seasonal timing of activity and the rarity of big brown bats found at our study site (Baerwald and Barclay 2011), we considered these passes to be silver-haired bats. Passes identified as Myotis spp. (n = 161) and passes that could not be identified to species (n = 39) were omitted from the data set. Fig. 1. View largeDownload slide Visual representation of an echolocation recording of Lasionycteris noctivagans illustrating the 3 phases of a pass. Recorded using an Anabat detector at Summerview wind energy facility, Alberta, Canada, 2007; viewed with AnaLook version 3.8s with between-call intervals removed. Fig. 1. View largeDownload slide Visual representation of an echolocation recording of Lasionycteris noctivagans illustrating the 3 phases of a pass. Recorded using an Anabat detector at Summerview wind energy facility, Alberta, Canada, 2007; viewed with AnaLook version 3.8s with between-call intervals removed. Table 1. Echolocation-phase call definitions for (a) silver-haired bats (Lasionycteris noctivagans) and (b) hoary bats (Lasiurus cinereus), including mean maximum and minimum frequencies (kHz) with SEs, call durations (ms), and inter-call intervals (ms) (revised from Barclay 1986). Phase Max freq (kHz) Min freq (kHz) Duration (ms) Inter-call interval (ms) (a) Lasionycteris noctivagans  Search 46.3 ± 5.1 25.1 ± 3.0 9.4 ± 1.8 > 300  Tracking 54.7 ± 5.3 25.6 ± 2.5 6.3 ± 1.9 150–220  Terminal 47.1 ± 7.4 22.9 ± 2.3 2.2 ± 1.1 < 120 (b) Lasiurus cinereus  Search 19.9 ± 1.6 16.9 ± 0.9 10.3 ± 2.0 > 300  Tracking 41.2 ± 12.2 21.5 ± 2.4 8.8 ± 2.7 160–300  Terminal 43.2 ± 9.1 18.0 ± 1.6 2.4 ± 1.2 < 100 Phase Max freq (kHz) Min freq (kHz) Duration (ms) Inter-call interval (ms) (a) Lasionycteris noctivagans  Search 46.3 ± 5.1 25.1 ± 3.0 9.4 ± 1.8 > 300  Tracking 54.7 ± 5.3 25.6 ± 2.5 6.3 ± 1.9 150–220  Terminal 47.1 ± 7.4 22.9 ± 2.3 2.2 ± 1.1 < 120 (b) Lasiurus cinereus  Search 19.9 ± 1.6 16.9 ± 0.9 10.3 ± 2.0 > 300  Tracking 41.2 ± 12.2 21.5 ± 2.4 8.8 ± 2.7 160–300  Terminal 43.2 ± 9.1 18.0 ± 1.6 2.4 ± 1.2 < 100 View Large Table 1. Echolocation-phase call definitions for (a) silver-haired bats (Lasionycteris noctivagans) and (b) hoary bats (Lasiurus cinereus), including mean maximum and minimum frequencies (kHz) with SEs, call durations (ms), and inter-call intervals (ms) (revised from Barclay 1986). Phase Max freq (kHz) Min freq (kHz) Duration (ms) Inter-call interval (ms) (a) Lasionycteris noctivagans  Search 46.3 ± 5.1 25.1 ± 3.0 9.4 ± 1.8 > 300  Tracking 54.7 ± 5.3 25.6 ± 2.5 6.3 ± 1.9 150–220  Terminal 47.1 ± 7.4 22.9 ± 2.3 2.2 ± 1.1 < 120 (b) Lasiurus cinereus  Search 19.9 ± 1.6 16.9 ± 0.9 10.3 ± 2.0 > 300  Tracking 41.2 ± 12.2 21.5 ± 2.4 8.8 ± 2.7 160–300  Terminal 43.2 ± 9.1 18.0 ± 1.6 2.4 ± 1.2 < 100 Phase Max freq (kHz) Min freq (kHz) Duration (ms) Inter-call interval (ms) (a) Lasionycteris noctivagans  Search 46.3 ± 5.1 25.1 ± 3.0 9.4 ± 1.8 > 300  Tracking 54.7 ± 5.3 25.6 ± 2.5 6.3 ± 1.9 150–220  Terminal 47.1 ± 7.4 22.9 ± 2.3 2.2 ± 1.1 < 120 (b) Lasiurus cinereus  Search 19.9 ± 1.6 16.9 ± 0.9 10.3 ± 2.0 > 300  Tracking 41.2 ± 12.2 21.5 ± 2.4 8.8 ± 2.7 160–300  Terminal 43.2 ± 9.1 18.0 ± 1.6 2.4 ± 1.2 < 100 View Large To estimate feeding-buzz rates between turbine and met tower sites for each species, we ran separate species-specific linear regressions of presence of feeding buzzes on dummy variables for turbine and met tower sites. To estimate feeding-buzz rates at each height, for each species, we ran separate species-specific linear regressions of presence of feeding buzzes on dummy variables for each height. To estimate the proportion of abrupt-detection passes at each height for each species, we ran separate species-specific linear regressions of presence of abrupt-detection passes on dummy variables for each height. We performed a Wald test (Judge et al. 1985) for each species and each call type to test the null hypothesis that there were no differences in rates of feeding buzzes or abrupt-detection passes between turbines and met tower sites. We performed a Wald test for each species and each call type to test the null hypotheses that there were no differences in rates of feeding buzzes or abrupt-detection passes across heights. We used Tukey’s post hoc comparisons to identify which heights had significantly different means as indicated by the Wald test, and a posterior 2-sample t-test to compare total feeding-buzz rates between species. We conducted statistical analyses with Stata SE 12.0 (StataCorp LP, College Station, Texas). Results Over 72 nights of recording, we recorded a total of 1,194 echolocation passes of migratory bats. Of these, 505 passes were emitted by L. cinereus. There was no significant difference in mean feeding-buzz rate between turbine and met tower sites (Wald test, F1, 500 = 3.30, P = 0.084; Table 2), or across heights (Wald test, F3, 500 = 1.50, P = 0.215; Fig. 2). Abrupt-detection passes were observed at both turbines and met towers, and at all heights. There was no significant difference between the mean rate at turbines and met towers (Wald test, F1, 500 = 0.64, P = 0.424), or across heights (Wald test, F3, 500 = 1.28, P = 0.280). Table 2. Echolocation passes of (a) silver-haired bats (Lasionycteris noctivagans) and (b) hoary bats (Lasiurus cinereus) recorded at a wind energy facility in southern Alberta, Canada. Height Total recording nights Total passes Total feeding buzzes Passes/night Feeding buzzes/night (a) Lasionycteris noctivagans  Ground—turbine 56 203 47 3.62 0.84  67 m—turbine 53 187 42 3.53 0.79  Ground—met tower 31 181 61 5.84 1.97  30 m—met tower 27 120 47 4.44 1.74 (b) Lasiurus cinereus  Ground—turbine 56 98 25 1.75 0.45  67 m—turbine 53 233 51 4.40 1.75  Ground—met tower 31 58 6 1.87 1.64  30 m—met tower 27 90 15 3.33 0.56 Height Total recording nights Total passes Total feeding buzzes Passes/night Feeding buzzes/night (a) Lasionycteris noctivagans  Ground—turbine 56 203 47 3.62 0.84  67 m—turbine 53 187 42 3.53 0.79  Ground—met tower 31 181 61 5.84 1.97  30 m—met tower 27 120 47 4.44 1.74 (b) Lasiurus cinereus  Ground—turbine 56 98 25 1.75 0.45  67 m—turbine 53 233 51 4.40 1.75  Ground—met tower 31 58 6 1.87 1.64  30 m—met tower 27 90 15 3.33 0.56 View Large Table 2. Echolocation passes of (a) silver-haired bats (Lasionycteris noctivagans) and (b) hoary bats (Lasiurus cinereus) recorded at a wind energy facility in southern Alberta, Canada. Height Total recording nights Total passes Total feeding buzzes Passes/night Feeding buzzes/night (a) Lasionycteris noctivagans  Ground—turbine 56 203 47 3.62 0.84  67 m—turbine 53 187 42 3.53 0.79  Ground—met tower 31 181 61 5.84 1.97  30 m—met tower 27 120 47 4.44 1.74 (b) Lasiurus cinereus  Ground—turbine 56 98 25 1.75 0.45  67 m—turbine 53 233 51 4.40 1.75  Ground—met tower 31 58 6 1.87 1.64  30 m—met tower 27 90 15 3.33 0.56 Height Total recording nights Total passes Total feeding buzzes Passes/night Feeding buzzes/night (a) Lasionycteris noctivagans  Ground—turbine 56 203 47 3.62 0.84  67 m—turbine 53 187 42 3.53 0.79  Ground—met tower 31 181 61 5.84 1.97  30 m—met tower 27 120 47 4.44 1.74 (b) Lasiurus cinereus  Ground—turbine 56 98 25 1.75 0.45  67 m—turbine 53 233 51 4.40 1.75  Ground—met tower 31 58 6 1.87 1.64  30 m—met tower 27 90 15 3.33 0.56 View Large Fig. 2. View largeDownload slide Proportion of passes (with SE) containing feeding buzzes at various heights and locations, July to September 2007, Summerview wind energy facility, Alberta, Canada. Mean feeding-buzz rates as observed in Manitoba at 2 m height (Barclay 1985) are included for comparison. Fig. 2. View largeDownload slide Proportion of passes (with SE) containing feeding buzzes at various heights and locations, July to September 2007, Summerview wind energy facility, Alberta, Canada. Mean feeding-buzz rates as observed in Manitoba at 2 m height (Barclay 1985) are included for comparison. We analyzed a total of 689 L. noctivagans passes. Feeding-buzz rates were significantly lower at turbines than met towers (Wald test, F1, 687 = 11.62, P = 0.001; Table 2). There was also a significant difference in feeding-buzz rate across heights (Wald test, F3, 687 = 5.18, P = 0.001; Fig. 2), and Tukey’s post hoc comparisons indicated a higher proportion of feeding buzzes at 30 m than 67 m (P = 0.008) or turbine ground level (P = 0.01). There was no significant difference in the proportion of passes with a feeding buzz at ground level between meteorological towers and turbines (P = 0.098). Abrupt-detection passes were observed at all heights and we found no significant difference in mean rate across heights (Wald test, F3, 687 = 1.78, P = 0.150). When we compared feeding-buzz rates between species, we observed a significantly greater proportion of passes containing feeding buzzes (combined for all levels at turbines and met towers) for L. noctivagans (29%) than L. cinereus (19%) (2-sample t-test, t1, 1197 = −3.77, P = 0.0002). Feeding-buzz rates at ground-level meteorological towers for both species were similar to those found at a non-turbine site in Manitoba (Fig. 2; Barclay 1986). Discussion Based on the hypothesis that bats are attracted to concentrations of insects present at the nacelle of wind turbines (Ahlen 2003; Kunz et al. 2007; Cryan and Barclay 2009; Rydell et al. 2010), we predicted that foraging rates would be greater at nacelle height (67 m) than at lower heights, and at turbines than at met towers. Our data did not support these predictions. There was no significant difference in the proportion of passes with a feeding buzz between ground level and 67 m for either L. cinereus or L. noctivagans. In addition, the feeding-buzz rate for L. noctivagans was greater at met towers than at turbines. If bats were attracted to foraging on insect concentrations around nacelles, we should observe a greater proportion of feeding buzzes associated with increased prey density (Racey and Swift 1985; Rydell 1989). The similarity of echolocation behavior between ground level and 67 m, and between turbine and met tower sites, suggests that neither L. cinereus nor L. noctivagans are attracted to turbines to forage on high insect densities at nacelle height. While previous studies showed that the majority of bats killed at wind energy facilities have full or partially full stomachs, indicating recent feeding (Reimer et al. 2010; Rydell et al. 2016; Foo et al. 2017), the presence of insects with aquatic stages in the diet of both species at our study site (Reimer et al. 2010) suggests that bats forage away from the wind energy facility before being killed. In addition, a recent dietary analysis of bats killed at wind turbines in Sweden revealed a diet resembling the insect diversity collected at the base of the turbine rather than at nacelle height (Rydell et al. 2016), further weakening the idea that bats are attracted to insects at turbine nacelles. Observations of insect aggregations and foraging activity of bats around turbine blades at offshore wind facilities in Europe (Ahlén 2003; Ahlén et al. 2007) may be unique to offshore sites and gleaning bat species (those that take prey from surfaces), where turbines are the only dry mass on the landscape, and may not hold true for inland sites or large, aerial-hawking species. Altitude had no significant effect on the occurrence of feeding buzzes for L. cinereus. Although altitude had a significant effect for L. noctivagans, the main difference was a greater proportion of feeding buzzes at 30 m at met towers than at ground level or nacelle height. These results indicate that relative foraging activity for L. noctivagans was greatest at 30 m around meteorological towers. As heat is not generated at the meteorological towers and hill-topping insects would congregate at the top of the structure (50 m), not 20 m below the highest point, this suggests that increased foraging activity by bats is not a direct result of attraction to insects, and further contradicts the feeding-attraction hypothesis. In addition, some of the “feeding buzzes” recorded may have been in response to detection of the towers, blades, or nacelles, not insects, and this may thus have inflated the estimation of foraging activity at each height. When we first observed abrupt-detection passes, we considered the hypothesis that bats sometimes do not echolocate while migrating but upon approaching a turbine, detect and react to the sight or sound of the rapidly moving turbine blades (Cryan and Barclay 2009). Recent studies have supported the idea some bats do not regularly echolocate while migrating (Gorresen et al. 2017; Corcoran and Weller 2018), but the consistent presence of this type of pass at all heights for both species suggests that these calls are not produced as a reaction to fast-moving blades. While L. noctivagans passes constituted 58% of the echolocation passes we recorded, this species represented only 34% of the fatalities observed at the site during the same sampling period, with L. cinereus comprising 60% of total fatalities (Baerwald and Barclay 2011). Across North America, L. cinereus is the bat species most commonly killed by wind turbines, making up 38% of all bat fatalities, while L. noctivagans make up 19% (Arnett and Baerwald 2013). One interpretation of this result might be that faster flight, reduced maneuverability, and increased activity at higher altitudes, combined with a lack of echolocation during migration for L. cinereus (Kunz et al. 2007; Cryan and Barclay 2009; Gorresen et al. 2017; Corcoran and Weller 2018), may make them more susceptible to being killed by wind turbines than other species, such as L. noctivagans (Erickson et al. 2002). Our study suggests that although bats do forage in the vicinity of turbines (see also Horn 2008), feeding is not their primary activity around turbine blades, nor is there more foraging activity at turbines than nearby sites. Although migrating L. cinereus and L. noctivagans feed while en route (Valdez and Cryan 2009; Reimer et al. 2010; Foo et al. 2017), we found no evidence to support the hypothesis that there is greater feeding activity around turbines nacelles in response to increased insect concentrations. While our data cannot be used to test the hypothesis that bats foraging around turbines are more susceptible to being killed than those not actively foraging, our assessment of the feeding-attraction hypothesis is important for informing mitigation strategies, as mitigating an activity that is evenly distributed across the landscape may require a different strategy than mitigating an attraction to turbines. Other attraction hypotheses proposed to explain bat fatalities at turbines, such as turbines as potential roosts (Kunz et al. 2007) or mating sites (Cryan 2008; Cryan et al. 2012) still need to be explored. In addition, as non-echolocating individuals would not be detected in our study, a combination of acoustic detection and thermal imaging or radar (as in Cryan et al. 2014) will help determine whether all bats echolocate as they migrate and if a lack of echolocation makes them more susceptible to fatality at turbine sites. Acknowledgments We thank J. Carpenter, K. Jonasson, B. Baerwald, and B. McKnight for assistance in the field. Logistical support for fieldwork was provided by J. Edworthy, the late M. Holder, T. Kwas, M. Hopkins, and B. Brown. M. Reimer provided assistance with statistical analysis. R. Cartar, R. M. Brigham, students in the Brigham lab, and 2 anonymous reviewers provided helpful comments on a preliminary draft of this manuscript. The research was funded by grants from the Natural Sciences and Engineering Research Council of Canada, Bat Conservation International, TransAlta Wind, Suncor, Enmax, Alberta Wind Energy, Alberta Conservation Association, Alberta Innovates – Technology Futures, and the Institute for Sustainable Energy, Environment and Economy at the University of Calgary. Literature Cited Ahlén , I . 2003 . Wind turbines and bats—a pilot study . Report to the Swedish National Energy Administration. Dnr 5210P-2002-00473, P-nr P20272-1. pp. 5. https://docs.wind-watch.org/Ahlen-windturbines-bats-2003.pdf. Accessed October 2018. Ahlén , I. , L. Bach , H. J. Baagøe , and J. Pettersson . 2007 . Bats and offshore wind turbines studied in southern Scandinavia . Report #5571 to the Swedish Environmental Protection Agency. doi:620-5571-2. American Wind Energy Association . 2017 . 2017 U.S. Wind Industry Market Report . http://www.awea.org/wind-energy-facts-at-a-glance. Accessed April 2018 . Arnett , E. B. , and E. F. Baerwald . 2013 . Impacts of wind energy development on bats: implications for conservation . Pp. 435 – 456 in Bat evolution, ecology, and conservation (R. A. Adams and S. C. Pedersen , eds.). Springer Science+Business Media , New York . Arnett , E. B. , et al. 2016 . Impacts of wind energy development on bats: a global perspective . Pp. 295 – 323 in Bats in the anthropocene: conservation of bats in a changing world (C. C. Voigt and T. Kingston , eds.). Springer International Publishing, Springer Cham, Switzerland . Baerwald , E. F . 2008 . Variation in the activity and fatality of migratory bats at wind energy facilities in southern Alberta: causes and consequences . Thesis , University of Calgary , Calgary, Alberta, Canada . Baerwald , E. F. , and R. M. R. Barclay 2009 . Geographic variation in activity and fatality of migratory bats at wind energy facilities . Journal of Mammalogy 90 : 1341 – 1349 . Google Scholar Crossref Search ADS Baerwald , E. F. , and R. M. R. Barclay . 2011 . Patterns of activity and fatality of migratory bats at a wind energy facility in Alberta, Canada . Journal of Wildlife Management 75 : 1103 – 1114 . Google Scholar Crossref Search ADS Baerwald , E. , G. D’Amours , B. Klug , and R. M. R. Barclay . 2008 . Barotrauma is a significant cause of bat fatalities at wind turbines . Current Biology 16 : 695 – 696 . Google Scholar Crossref Search ADS Barclay , R. M. R . 1985 . Long- versus short-range foraging strategies of hoary (Lasiurus cinereus) and silver-haired (Lasionycteris noctivagans) bats and the consequences for prey selection . Canadian Journal of Zoology 63 : 2507 – 2515 . Google Scholar Crossref Search ADS Barclay , R. M. R . 1986 . The echolocation calls of hoary (Lasiurus cinereus) and silver-haired (Lasionycteris noctivagans) bats as adaptations for long-versus short-range foraging strategies and the consequences for prey selection . Canadian Journal of Zoology 64 : 2700 – 2705 . Google Scholar Crossref Search ADS Barclay , R. M. R. , E. F. Baerwald , and J. Rydell . 2017 . Bats . Chapter 9 in Wildlife and wind farms: conflicts and solutions, Volume 1 (M. Perrow , ed.). Pelagic Publishing , Exeter, United Kingdom . Betts , B . 1998 . Effects of interindividual variation in echolocation calls on identification of big brown and silver-haired bats . Journal of Wildlife Management 62 : 1003 – 1010 . Google Scholar Crossref Search ADS Canadian Wind Energy Association (CanWEA) . 2018 . Wind market report: CanWEA market updates spring forum 2018 . https://canwea.ca/wp-content/uploads/2018/04/CanWEA-Market-Updates-Spring-Forum-2018.pdf. Accessed September 2018 . Corcoran , A. J. , and T. J. Weller . 2018 . Inconspicuous echolocation in hoary bats (Lasiurus cinereus) . Proceedings of the Royal Society of London, B. Biological Sciences 285 : 20180441 . Google Scholar Crossref Search ADS Cryan , P. M . 2008 . Mating behavior as a possible cause of bat fatalities at wind turbines . The Journal of Wildlife Management 72 : 845 – 849 . Google Scholar Crossref Search ADS Cryan , P. M. , and R. M. R. Barclay 2009 . Causes of bat fatalities at wind turbines: hypotheses and predictions . Journal of Mammalogy 90 : 1330 – 1340 . Google Scholar Crossref Search ADS Cryan , P. M. , et al. 2014 . Behavior of bats at wind turbines . Proceedings of the National Academy of Sciences 111 : 15126 – 15131 . Google Scholar Crossref Search ADS Cryan , P. M. , et al. 2012 . Evidence of late-summer mating readiness and early sexual maturation in migratory tree-roosting bats found dead at wind turbines . PLoS One 7 : e47586 . Google Scholar Crossref Search ADS PubMed Erickson , W. P. , et al. 2002 . Synthesis and comparison of baseline avian and bat use, raptor nesting and mortality information from proposed and existing wind developments . Report prepared for Bonneville Power Administration , Portland, Oregon . WEST, Incorporated. Fenton , M. B. , and G. P. Bell . 1979 . Echolocation and feeding behaviour in four species of Myotis (Chiroptera) . Canadian Journal of Zoology 57 : 1271 – 1277 . Google Scholar Crossref Search ADS Foo , C. F. , V. J. Bennett , A. M. Hale , J. M. Korstian , A. J. Schildt , and D. A. Williams . 2017 . Increasing evidence that bats actively forage at wind turbines . PeerJ 5 : e3985 . Google Scholar Crossref Search ADS PubMed Frick , W. F. , et al. 2017 . Fatalities at wind turbines may threaten population viability of a migratory bat . Biological Conservation 209 : 172 – 177 . Google Scholar Crossref Search ADS Global Wind Energy Council . 2017 . Global wind market report . http://www.gwec.net/global-figures/graphs. Accessed April 2018 . Gorresen , P. M. , P. M. Cryan , K. Montoya-Aiona , and F. J. Bonaccorso . 2017 . Do you hear what I see? Vocalization relative to visual detection rates of Hawaiian hoary bats (Lasiurus cinereus semotus) . Ecology and Evolution 7 : 6669 – 6679 . Google Scholar Crossref Search ADS PubMed Griffin , D. R. , F. A. Webster , and C. R. Michael . 1960 . The echolocation of flying insects by bats . Animal Behaviour 8 : 141 – 154 . Google Scholar Crossref Search ADS Horn , J. W. , E. B. Arnett , and T. H. Kunz . 2008 . Behavioral responses of bats to operating wind turbines . Journal of Wildlife Management 72 : 123 – 132 . Google Scholar Crossref Search ADS Johnson , G. D. , M. K. Perlik , W. P. Erickson , and M. D. Strickland . 2004 . Bat activity, composition, and collision mortality at a large wind plant in Minnesota . Wildlife Society Bulletin 32 : 1278 – 1288 . Google Scholar Crossref Search ADS Judge , G. G. , W. E. Griffiths , R. C. Hill , H. Lütkepohl , and T. C. Lee . 1985 . The theory and practice of econometrics . 2 nd ed. Wiley , New York . Kunz , T. H. , et al. 2007 . Ecological impacts of wind energy development on bats: questions, research needs, and hypotheses . Frontiers in Ecology and the Environment 5 : 315 – 324 . Google Scholar Crossref Search ADS Long , C. V. , J. A. Flint , and P. A. Lepper . 2011 . Insect attraction to wind turbines: does colour play a role ? European Journal of Wildlife Research 57 : 323 – 331 . Google Scholar Crossref Search ADS Racey , P. A. , and S. M. Swift . 1985 . Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour . The Journal of Animal Ecology 54 : 205 – 215 . Google Scholar Crossref Search ADS Reimer , J. P. , E. F. Baerwald , and R. M. R. Barclay . 2010 . Diet of hoary (Lasiurus cinereus) and silver-haired (Lasionycteris noctivagans) bats while migrating through southwestern Alberta in late summer and autumn . American Midland Naturalist 164 : 230 – 237 . Google Scholar Crossref Search ADS Rollins , K. E. , D. K. Meyerholz , G. D. Johnson , A. P. Capparella , and S. S. Loew . 2012 . A forensic investigation into the etiology of bat mortality at a wind farm: barotrauma or traumatic injury ? Veterinary Pathology 49 : 362 – 371 . Google Scholar Crossref Search ADS PubMed Rydell , J . 1989 . Feeding activity of the northern bat Eptesicus nilssoni during pregnancy and lactation . Oecologia 80 : 562 – 565 . Google Scholar Crossref Search ADS PubMed Rydell , J. , L. Bach , M.-J. Dubourg-Savage , M. Green , L. Rodrigues , and A. Hedenström . 2010 . Mortality of bats at wind turbines links to nocturnal insect migration ? European Journal of Wildlife Research 56 : 823 – 827 . Google Scholar Crossref Search ADS Rydell , J. , W. Bogdanowicz , A. Boonman , S. Pettersson , E. Suchecka , and J. J. Pomorski . 2016 . Bats may eat diurnal flies that rest on wind turbines . Mammalian Biology 81 : 331 – 339 . Google Scholar Crossref Search ADS Sikes , R. S. , and The Animal Care and Use Committee of the American Society of Mammalogists . 2016 . 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education . Journal of Mammalogy 97 : 663 – 688 . Google Scholar Crossref Search ADS PubMed Surlykke , A. , and E. K. V. Kalko . 2008 . Echolocating bats cry out loud to detect their prey . PLoS ONE 3 : e2036 . doi:10.1371/journal.pone.0002036 Valdez , E. W. , and P. M. Cryan . 2009 . Food habits of the hoary bat (Lasiurus cinereus) during spring migration through New Mexico . Southwestern Naturalist 54 : 195 – 200 . Google Scholar Crossref Search ADS © 2018 American Society of Mammalogists, www.mammalogy.org This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Echolocation activity of migratory bats at a wind energy facility: testing the feeding-attraction hypothesis to explain fatalities
JF - Journal of Mammalogy
DO - 10.1093/jmammal/gyy143
DA - 2018-12-05
UR - https://www.deepdyve.com/lp/oxford-university-press/echolocation-activity-of-migratory-bats-at-a-wind-energy-facility-Ev4zIEWdwV
SP - 1472
VL - 99
IS - 6
DP - DeepDyve
ER -