Open access

Effects of turbine height and cut-in speed on bat and swallow fatalities at wind energy facilities

Publication: FACETS
6 October 2022

Abstract

Understanding the relationship between the height of wind turbines and wildlife fatalities is important for informing and mitigating wildlife collisions as ever taller and denser arrays of wind turbines are erected across the landscape. We examined relationships between turbine height and fatalities of bats and swallows at 811 turbines in Ontario, Canada, ranging from 119 to 186 m tall. We accounted for cut-in speeds, operational mitigation, and taller turbines projecting carcasses farther from the turbine base than shorter turbines. Fatalities of hoary bats (Lasiurus cinereus Palisot de Beauvois, 1796), silver-haired bats (Lasionycteris noctivagans Le Conte, 1831), and big brown bats (Eptesicus fuscus Palisot de Beauvois, 1796) increased with increased maximum blade height of turbines. In contrast, fatalities of little brown bat (Myotis lucifugus Le Conte, 1831) and eastern red bat (Lasiurus borealis Müller, 1776) decreased with increased turbine height. Fatalities of purple martins (Progne subis Linnaeus, 1758) and tree swallows (Tachycineta bicolor Vieillot, 1808) were higher at taller turbines than shorter turbines. However, fatalities of cliff swallow (Petrochelidon pyrrhonota Vieillot, 1817) and barn swallow (Hirundo rustica Linnaeus, 1758) were not associated with turbine height. Our results suggest that varying flight height among species may be one factor affecting collision risk.

Introduction

Renewable energy sources, such as wind energy, are a critical tool in divesting from fossil fuels and slowing the rate of climate change (Rogelj et al. 2018), but collisions with wind turbines can harm wildlife (Smallwood 2013; Zimmerling et al. 2013; Zimmerling and Francis 2016). Mortality at turbines may have population-level consequences for some species, especially migratory bats (Kunz et al. 2007; Frick et al. 2017). Understanding what factors contribute to fatalities can inform wildlife-friendly wind energy operations.
Fatalities of wildlife at wind turbines vary with several factors, including proximity to key habitats, such as migration corridors, and cut-in speeds, the wind speeds at which turbines begin generating electricity (Cryan and Brown 2007; Arnett et al. 2011; Thompson et al. 2017; Davy et al. 2020). Fatalities also may vary with turbine size (Table 1), which is important because wind turbines are increasing in height to maximize energy capture (Wiser et al. 2011, 2018). Taller turbines presumably increase exposure risk for wildlife flying at higher altitudes (Davy et al. 2017; Wellig et al. 2018; Roemer et al. 2019), and longer rotors sweep a larger area of aerial habitats used by wildlife.
Table 1.
Table 1. Studies examining the effects of onshore wind turbine size on number of bat and bird fatalities.
    Turbine size measurement 
    Hub/nacelle heightMBH (hub height + blade length)Rotor swept area or rotor diameterPower capacity 
TypeTaxaCP and SE correctionLattice turbines includedEffectSize (m)EffectSize (m)EffectRotor diameter (m)EffectRange (MW)Study
within sitebatsyesno+36 & 50NA +33, 46, & 48+0.33–0.75Johnson et al. (2003), reviewed in Arnett et al. (2008)
within sitebatsyesno+65 & 78NA +46 & 84+0.66 & 1.8Fiedler et al. (2007), reviewed in Arnett et al. (2011)
across sitesbirdsyesyesO24–94NA* O15–80O<0.1–1.8Barclay et al. (2007)
 batsyesyes+24–94NA* O15–80+<0.1–1.8 
across sitesbirds (raptors)noyes+21–36NA NA NA de Lucas et al. (2008)
across sitesbatsyesNA+50–84NA NA NA Baerwald and Barclay (2009)
across sitesbatsyesNA+24–98NA +NANA Rydell et al. (2010)
across sitesbatsnoNA+44–60NA O52–90NA Georgiakakis et al. (2012)
across sitesbirdsyesno+36–80NA* NA* NA Loss et al. (2013)
across sitesbirds (raptors)yesyesNA NA NA <0.1–3.0Smallwood (2013)
 batsyesyesNA NA NA O<0.1–3.0 
 birdsyesyesNA NA NA O and –<0.1–3.0 
across sitesbirdsSE onlyNANA NA O23–82NA Everaert (2014)
across sitesbirdsyesNANA NA O0.9–15O<0.1Minderman et al. (2015)
across sitesbatsyesnoNA O90–135NA NA Zimmerling and Francis (2016)
across sitesbatsyesnoONANA* NA NA Thompson et al. (2017)
across sitesbatsyesno+83–110NA NA NA Davy et al. (2020)
within sitebirdsyesNANA +42–126+19–93+0.1–2.5Huso et al. (2021)
 batsyesNANA +42–126+19–93+0.1–2.5 

Note: NA, not examined or not available in the published study; NA*, not examined in the study because of correlation with hub height; ∞, not considered informative but in top predictive models; O, neither a positive or negative effect; +, a positive effect; and –, a negative effect. Type of study “within site” is a single wind energy facility with two types of turbine models and “across sites” is comparison of models across wind energy facilities.

Evidence for the effect of turbine size on bird and bat fatalities is equivocal (Table 1), possibly reflecting the wide variation in locations, affected species, and turbine type and sizes among studies. Variation in the area searched under turbines also affects fatality estimates. Taller turbines propel carcasses further, potentially causing them to land outside standard search areas (Hull and Muir 2010; Huso and Dalthorp 2014; Choi et al. 2020) and biasing estimates of fatalities low at taller turbines compared to shorter turbines with equivalent search areas. Finally, low sample sizes can preclude analyses of species-specific patterns in fatalities in studies based on smaller datasets, but analyzing total fatalities (i.e., with all species or groups of species pooled) may obscure patterns between turbine height and species-specific fatalities (Davy et al. 2020).
Wind turbines in Ontario, Canada, have increased 42% in size, from 120 to 170 m maximum blade height (MBH), between 2006 and 2019 (Fig. 1a and Table S1), a result of increases in hub height (Fig. 1b) and rotor diameter (Fig. 1c). A previous analysis suggested that turbine hub height may contribute to fatalities of some bat species in Ontario, but confidence in the relationship was not strong (Davy et al. 2020). Here, we conducted a detailed investigation of the effects of turbine height on fatalities in two groups of aerial insectivores, bats (nocturnal) and swallows (diurnal), which are experiencing population declines (Nebel et al. 2010; Committee on the Status of Endangered Wildlife in Canada 2013; Smith et al. 2015; Rodhouse et al. 2019). We expanded on previous work by including data from newer, taller turbines and accounting for carcasses falling outside of search areas at taller turbines. We also used MBH as a measure of turbine height because it is more relevant than hub height to measure the altitudes where species may interact with turbine blades.
Fig. 1.
Fig. 1. Changes in wind turbine (a) maximum blade height, (b) hub height, (c) rotor diameter, and (d) manufacturer’s cut-in speed in Ontario, Canada, between 2006–2019. Points represent new turbines added to the landscape in Ontario each year, and the size of the points indicates the total number of turbines with the specified size or speed. Trend lines represent results of linear models with year (and year2 where applicable) as predictors (Table S1).

Methods

Data sources

We obtained searcher efficiency, scavenging, and carcass survey data from post-construction monitoring of onshore monopole turbines at wind energy facilities in southern Ontario (south of 48°N) and submitted to the Wind Energy Bird and Bat Monitoring Database (Birds Canada 2020). The database included turbine model names, hub heights, and rotor diameters gathered from facility reports or online (thewindpower.net) and manufacturer-specified cut-in speeds from a repository of wind turbine models (wind-turbine-models.com/turbines).
We used MBH (hub height plus half the rotor diameter) to quantify turbine height in our analyses because hub height and rotor diameter are correlated, and MBH is more ecologically meaningful than hub height alone. Hub height and rotor diameter are moderately correlated in Ontario (ρ = 0.49), and including both variables in models could lead to unstable parameter estimates, inflated standard errors, and difficulty assessing the relative importance of the variables (Dormann et al. 2012). Additionally, MBH incorporates hub height and rotor diameter into a single metric representing the true height of a turbine, which has implications for animals flying at different altitudes.

Study species

We modelled the relationship between MBH and fatalities of each bat and swallow species sufficiently represented in the database. These included five species of bat (big brown bat Eptesicus fuscus Palisot de Beauvois, 1796; little brown bat Myotis lucifugus Le Conte, 1831; eastern red bat Lasiurus borealis Müller, 1776; hoary bat Lasiurus cinereus Palisot de Beauvois, 1796; and silver-haired bat Lasionycteris noctivagans Le Conte, 1831) and four species of swallow (barn swallow Hirundo rustica Linnaeus, 1758; tree swallow Tachycineta bicolor Vieillot, 1808; cliff swallow Petrochelidon pyrrhonota Vieillot, 1817; and purple martin Progne subis Linnaeus, 1758).

Fatality estimation

We estimated the number of individuals of each species killed (M^) at monitored wind turbines using GenEst (Dalthorp et al. 2018) in R (R Core Team 2020). GenEst is a generalized estimator that corrects the number of carcasses found by the probability of detecting a carcass and adjusts for carcasses falling outside of searched areas. Details of the specifications we used to calculate M^ in GenEst follows.

Search schedules

We retained data from wind turbines that were consistently monitored (twice per week for 98% of datasets, 2% searched once per week) during spring (May–Jun) and (or) late summer (mid-Jul through end-Sep). We only estimated fatalities for swallows in late summer because few carcasses were found at turbines during spring (n = 19, 6% of all swallow carcasses found in our data subset).
GenEst requires users to enter search dates for each turbine to estimate mortality, including searches where no carcasses were found. However, only search dates when carcasses were found were available for a subset of facilities and years (n = 28, 23% of all facility years). To create full search schedules for these facilities and years, we simulated probable search dates for each turbine using rule-based data mining and hierarchical clustering analysis in the arules package in R (Hahsler et al. 2005, 2020). In short, we used a priori association rules to group turbines that were often searched on the same days and assigned search dates to the whole group. We then filled gaps in the search schedules of each group so that searches occurred at intervals specified in the database (e.g., every 3 or 4 days for twice-weekly searches) and throughout the survey period (e.g., 15 Jul–30 Sep for late summer).

Detection probability

We used facility- and year-specific searcher efficiency and carcass persistence survey data to produce facility-corrected fatality estimates. Our analysis included facilities and years for which ≥10 searcher efficiency and ≥10 carcass persistence surveys were conducted (n = 59 facilities surveyed in at least one year during 2010–2019). Carcasses used in searcher efficiency and carcass persistence surveys were small bats and non-raptor birds. We assumed a constant proportional decline in searcher efficiency (k = 0.7) with each subsequent search (Korner-Nievergelt et al. 2012; Simonis et al. 2018), because carcasses missed on the first search may be more difficult to find as a result of decay, cryptic colouration, etc. We could not estimate k from available data because test carcasses were removed after each searcher efficiency trial. We modelled carcass persistence over time with exponential, Weibull, lognormal, and loglogistic survival models and constant scale and location parameters. Of the four candidate models for each facility and year, we selected the top model with the lowest ΔAICc value.

Search area correction

All carcass searches were conducted by walking concentric circles out to a maximum distance of 50 m (as required by government guidelines; Ontario Ministry of Natural Resources and Forestry 2011), regardless of turbine height. Ballistics models estimate that ∼95% of 14 g bat carcasses (and ∼80% of 12 g bird carcasses) fall within 50 m of turbines with MBH = 125 m (i.e., “medium-sized” turbines; Hull & Muir 2010), which were typical sizes of turbines on the landscape at the beginning of our study period (2010, Fig. 1a). However, newer turbines are now much larger (∼170 m max turbine blade height in 2019, Fig. 1a), and therefore, a larger proportion of carcasses should land outside of 50 m search areas than for older, shorter turbines.
We used ballistics models (Hull and Muir 2010), field observations of carcasses, and the proportion of the search area covered by searchers to estimate the proportion of carcasses expected to fall in the search area of each turbine (dwp). First, for each type of turbine at a facility, we estimated the maximum distance that bat and small bird carcasses should fall from the base of turbines (henceforth, “maximum fall distance”) depending on the blade length (half of rotor diameter) and hub height (i.e., from linear regression equations, Hull and Muir 2010). Next, for the same turbine groups, we counted the number of bat and bird carcasses found every 10 m from the base of turbines out to 50 m. Carcasses tended to peak closer to the turbine base at shorter turbines (Fig. S1) and roughly followed a triangular distribution (Fig. 2). We assumed that the triangular distribution extended to the maximum fall distance, with the number of carcasses declining linearly from the peak out to the maximum fall distance. We then estimated the proportion of carcasses that should fall in the 50 m search radius (psearch) as the proportion of the total triangular distribution within 50 m of the turbine base (Fig. 2). Carcass distribution data were limited or unavailable for a subset of facilities (23% of facilities for bats and 49% for birds), so we estimated psearch for the subset using predictive equations from a linear regression between calculated psearch estimates and taxa type (bird or bat) and MBH (Fig. S2). Finally, we estimated dwp for each turbine by multiplying psearch for each facility and turbine type by the average percent of the 50 m search area covered by searchers.
Fig. 2.
Fig. 2. Examples of data used to estimate the proportion of carcasses that fall in the search radius (psearch) at wind turbines from two facilities in Ontario, Canada: a facility with (a) shorter turbines (MBH = 121 m) and (b) taller turbines (MBH = 150 m). Dark grey bars represent field observations of bat carcasses, and the light grey triangle represents a simple, assumed distribution for carcass fall distances. The triangle distribution is determined by maximum carcass fall distances (dmax) estimated by ballistics models and the observed peak in carcass numbers at a given distance from the turbine base (dpeak). psearch is the proportion of the area under the triangle distribution that falls within 50 m from the turbine (i.e., left of the dashed line).

M^ Estimation

We used search schedule, dwp, carcass persistence, searcher efficiency, and carcass observation data to calculate M^ using the estM function with 10 000 iterations and the calcSplits function to estimate M^ per turbine and season (spring or late summer). We used the R package purrr (Henry and Wickham 2020) to simultaneously estimate M^ for each facility, year, and species, and we retained median M^ values for analyses in linear mixed effects models.

Mixed effects models

We examined the effects of MBH on bat and swallow fatalities using generalized linear mixed effects models (GLMMs) with M^ per turbine as the response variable. We included species and manufacturer’s cut-in speed as predictors, as well as the interactions between species and MBH, and species and cut-in speed. In addition, we included turbine ID and facility ID as random factors to account for repeated measures and for other potential turbine- or facility-specific sources of variation. We could not include year as a continuous predictor because the number of facilities monitored in some years was low (n = 2 facilities in 2010, 2012, and 2019, respectively). We, therefore, included a random factor of year to estimate the effects of turbine height and cut-in speed while accounting for annual variation in fatalities.
We ran separate models for spring and late summer monitoring seasons (Ontario Ministry of Natural Resources and Forestry 2011). Some turbines in Ontario undergo operational mitigation at night (by increasing turbine cut-in speeds to 5.5 m/s) in late summer to reduce bat fatalities (Ontario Ministry of Natural Resources and Forestry 2011). Therefore, we included mitigation status (turbine undergoing operational mitigation: yes or no) as a predictor in late summer but not in spring models for bats.
We fit GLMMs and zero-inflated GLMMs with Poisson and negative binomial distributions using the R package glmmTMB and compared the fits of global models using AIC (Brooks et al. 2017) via the function “AICtab” in the bbmle package (Bolker and R Development Core Team 2020). We also used the package DHARMa (Hartig 2020) to examine patterns in residuals. We selected the global model with the best fit, indicated by the lowest ΔAIC: zero-inflated negative binomial models for bats and swallows in late summer and zero-inflated Poisson models for bats in spring (Table S2). We subsequently used “drop1” function with a chi-square test to drop non-significant terms (α = 0.05) from the model. We calculated marginal and conditional R2 following Nakagawa et al. (2017).

Results

We examined the effects of MBH and manufacturer’s cut-in speed on fatalities of aerial insectivores (bats and swallows) at 652 turbines at 53 facilities in spring and 811 turbines from 59 facilities in late summer. Turbines consisted of 19 types (make and models), with MBH ranging from 119–186 m (139 ± 13 m, mean ± SD) and manufacturer’s cut-in speeds ranging from 2.0–4.0 m/s (3.2 ± 0.4 m/s). We were able to include >1 year of monitoring data for 67% of turbines.

Turbine height

MBH was a significant predictor (Table S3) of the number of bats killed per turbine (M^). This effect differed among species (species by MBH interaction in spring: χ2 = 14.3, d.f. = 4, p < 0.01; late summer: χ2 = 43.3, d.f. = 4, p < 0.001) though confidence intervals overlapped for fatality estimates at the shortest and tallest turbines (Table 2). The relationship between MBH and bat fatalities was less clear in spring (Fig. 3a) than late summer. In spring, more silver-haired bat, hoary bat, and big brown bat and fewer little brown bat and eastern red bat fatalities were estimated at taller turbines than shorter turbines (Fig. 3a; Table 2). In late summer, more bats were killed at taller turbines than at shorter turbines for all species except little brown bats, which continued to exhibit fewer fatalities at taller turbines (Fig. 3b; Table 2).
Table 2.
Table 2. Back-transformed model predicted estimates (and 95% confidence intervals) of the number of bats killed per turbine (M^) at the shortest and tallest turbines in our study.
Bats in spring
 Maximum blade height (m) 
 119 m, shortest turbines186 m, tallest turbines 
SpeciesM^ (CI)M^ (CI)% change
Eastern red bat2.5 (1.5–4.2)0.7 (0.2–2.5)−72
Big brown bat2.1 (1.4–3.1)3.4 (1.6–7.3)62
Hoary bat2.0 (1.4–3.0)2.8 (1.3–6.0)40
Silver-haired bat2.1 (1.5–3.1)3.2 (1.6–6.4)52
Little brown bat4.3 (2.6–7.0)0.5 (0.2–1.9)−88
Bats in late summer
SpeciesM^ (CI)M^ (CI)% change
Eastern red bat3.6 (2.5–5.1)4.5 (2.5–8.3)25
Big brown bat2.7 (1.9–3.9)4.9 (2.7–9.1)81
Hoary bat4.3 (3.0–6.1)8.6 (4.8–15.3)100
Silver-haired bat3.6 (2.5–5.1)5.9 (3.2–10.8)64
Little brown bat2.1 (1.4–3.3)0.3 (0.1–0.7)−86
Swallows in late summer
SpeciesM^ (CI)M^ (CI)% change
Barn swallow0.1 (0–0.2)0.1 (0–0.5)0
Cliff swallow0.1 (0–0.3)0.1 (0–0.7)0
Purple martin0.1 (0–0.3)0.4 (0.1–2.1)300
Tree swallow0.1 (0–0.3)1 (0.2–4.6)900

Note: Estimates were calculated assuming that turbines were not undergoing operational mitigation.

Fig. 3.
Fig. 3. The relationship between maximum blade height of wind turbines and the estimated number of bats killed per turbine (M^) in Ontario, Canada, during (a) spring and (b) late summer. Lines and 95% confidence intervals were predicted from generalized linear mixed effects models.
Estimated fatalities of swallows in late summer were low, and confidence intervals overlapped for fatality estimates at the shortest and tallest turbines (Fig. 4; Table 2). Fatalities of purple martins and tree swallows were greater at taller turbines than shorter turbines (Fig. 4, species by MBH interaction: χ2 = 9.4, d.f. = 3, p = 0.02). Incidence rate ratios from final models (Table S3) showed interspecific differences in the number of fatalities per turbine, with fewer for barn swallow, followed by cliff swallow, purple martin, and tree swallow (Fig. 5).
Fig. 4.
Fig. 4. The relationship between maximum blade height of wind turbines and the estimated number of swallows killed per turbine (M^) in Ontario, Canada. Lines and 95% confidence intervals were predicted from generalized linear mixed effects models.
Fig. 5.
Fig. 5. Back-transformed estimated marginal means (and 95% confidence intervals) of the number of swallows killed per turbine in Ontario, Canada, by species. Means were calculated at the average turbine size in the study area, 139 m maximum blade height.

Turbine cut-in speed and operational mitigation

Manufacturer’s cut-in speed was not a predictor of bat or swallow fatalities in either season and was dropped from final models (bats spring: χ2 = 0.007, p = 0.93; bats late summer: χ2 = 0.60, p = 0.44; swallows late summer: χ2 = 0.002, p = 0.97). Turbines under operational, nocturnal mitigation killed 33% fewer bats than turbines without cut-in speed adjustments in late summer (back-transformed β = 0.67, 95% CI = 0.56–0.79).

Discussion

Our results demonstrate an association between wind turbine height and fatality counts of some species of bats and swallows, based on a large dataset of turbines extending 119 to 186 m into the aerosphere. Our findings are consistent with previous studies showing that turbine height explains a portion of bat fatalities at wind energy facilities (Johnson et al. 2003; Fiedler et al. 2007; Barclay et al. 2007; Baerwald and Barclay 2009; Rydell et al. 2010; Georgiakakis et al. 2012; Huso et al. 2021), although other factors, such as the proximity of wind energy facilities to key habitats, migration corridors, and roosts, also play a role (Barclay et al. 2007; Cryan and Brown 2007; Ferreira et al. 2015; Thompson et al. 2017; Davy et al. 2020). Greater uncertainty in the relationship between turbine height and fatalities that we observed in spring could be the result of fewer carcass observations in spring (Birds Canada 2018; Davy et al. 2020) or could indicate seasonal differences in use of the aerosphere.
We estimated fewer bat fatalities at turbines undergoing operational mitigation (i.e., raising cut-in speeds), which agrees with previous findings (Arnett et al. 2011; Davy et al. 2020; Whitby et al. 2021). Despite fewer fatalities at turbines with raised cut-in speeds, cut-in speeds specified by manufacturers were poor predictors of estimated bat and swallow fatalities. Bat activity tends to drop sharply at wind speeds greater than 5–6 m/s (Reynolds 2006; Wellig et al. 2018); therefore, bat activity may not have differed substantially between wind speeds of 2–4 m/s (the range of cut-in speeds specified by manufacturers in our dataset). However, turbine-specific operational cut-in speeds from our study area were not available, so we used manufacturer’s specified cut-in speeds as a proxy for operational cut-in speeds. We recognize that wind farms sometimes allow turbines to “free-wheel” (i.e., to continue to spin at low wind speeds prior to the onset of electricity generation) and that some facilities may have used different cut-in speeds than that specified by the manufacturer, and both scenarios would obscure the relationship we predicted. Wildlife collide with both free-wheeling turbines and turbines that are generating power (Baerwald et al. 2009; Whitby et al. 2021), so if turbines in our study area were free-wheeling, then manufacturer specified cut-in speed would become a poor proxy for turbine movement at low wind speeds and a poor predictor of fatalities. To address this potential confounding factor, we recommend that future studies obtain and examine operational cut-in speeds and data on free-wheeling turbines whenever possible.
Population size and flight altitudes of bats are not well understood (Voigt et al. 2018) relative to swallows’ population size and flight altitudes (Table S4). Although few swallow carcasses (n = 341) were found at turbines compared to bats (n = 4850), we speculate that quantitative data about swallow flight altitudes, population size, and fatalities at turbines could provide biologically meaningful interpretations of bat fatality data. Despite their higher relative abundance in Ontario (Partners in Flight 2020; Table S4), barn swallows had the lowest per turbine fatalities compared to other higher-flying swallow species (e.g., tree swallow and purple martin; Dreelin et al. 2018). Additionally, fatalities of purple martins, the least abundant but highest-flying species in Ontario (Table S4), were greater at taller turbines than shorter turbines. We, thus, speculate that differences in fatalities of avian aerial insectivores at turbines are due to differences in flight altitude, not necessarily abundance. Likely, both flight altitude and relative abundance contribute to fatalities, as demonstrated by tree swallow fatality data; tree swallows had the highest number of fatalities per turbine, and they are abundant (Table S4) and also often fly in the rotor swept area of turbines in Ontario (Fig. S3).
If the same relationship between flight altitude and fatalities holds true for bats, then the pattern we observed between turbine height and fatalities of hoary, silver-haired, and big brown bats may reflect these species use of higher altitudes. Collisions of hoary and silver-haired bats with planes support the assertion that they are high-altitude flyers (Peurach 2003; Peurach et al. 2009; McCracken et al. 2021). Perhaps little brown bats and eastern red bats fly at lower altitudes, spending more time below the rotor swept area of newer turbines that tend to be further from the ground than older turbine models, but at this point, this interpretation is speculation that is not yet supported by quantitative data. New, lightweight tracking devices such as GPS units and altimeters can help explicitly test hypotheses about bat flight altitudes (Roeleke et al. 2016; Weller et al. 2016; Conenna et al. 2019; O’Mara et al. 2019, 2021; though see Péron et al. 2020).
Broadly, our results and those of other studies (Johnson et al. 2003; Fiedler et al. 2007; Barclay et al. 2007; Baerwald and Barclay 2009; Rydell et al. 2010; Georgiakakis et al. 2012) indicate a general, ongoing pattern of more bat fatalities at taller turbines. While more bat fatalities at taller turbines is a concern with the increasing size of turbines (Wiser et al. 2011, 2018), fatality rates of bats and birds appear to be relatively consistent per unit of energy produced (GWh) by a turbine (Huso et al. 2021). Therefore, taller turbines that tend to produce more energy may kill more birds and bats than smaller turbines, but the number of animals killed per GWh may remain constant. If we consider how this result can inform efforts to maximize energy production while minimizing wildlife collisions, considering turbine height in the new construction or the repowering of turbines is likely a less effective strategy for reducing wildlife fatalities than efforts such as minimizing turbine blade movement during high-risk periods, for example at night, during migratory periods, and in certain weather conditions for bats (Arnett et al. 2011; Squires et al. 2021) and during the post-breeding and southbound migration period for swallows (Erickson et al. 2014).
Nevertheless, our species-level analyses reveal that turbine height does predict the number of fatalities for some species of bats and birds. Where possible, future analyses of wildlife mortality at wind turbines should explicitly consider interspecific variation in fatalities at wind turbines. Species-specific analyses can inform more accurate risk assessments for each species and may provide insight into aerial habitat selection by each species. Finally, we acknowledge that using mortality as a proxy for exploring flight altitudes is indirect and laden with assumptions. We expect that the increasing availability of altimeters for wildlife tracking will improve interpretation of fatality data at wind turbines and clarify the association between flight altitude and collision risk.

Acknowledgements

This work was supported by Birds Canada, Environment and Climate Change Canada, MITACS Accelerate, and the Government of Ontario. We thank the members of the Wind Energy Bird and Bat Monitoring Database steering committee and proponents who collected and submitted data to the database. We also thank E. Nkwonta for help with data management, W. Burr for advice on model correlations and zero-inflated models, and A. Dreelin for providing summary statistics of swallow altimeter data.

References

Arnett EB, Brown WK, Erickson WP, Fiedler JK, Hamilton BL, Henry TH, et al. 2008. Patterns of bat fatalities at wind energy facilities in North America. Journal of Wildlife Management, 72: 61–78.
Arnett EB, Huso MM, Schirmacher MR, and Hayes JP. 2011. Altering turbine speed reduces bat mortality at wind-energy facilities. Frontiers in Ecology and the Environment, 9(4): 209–214.
Baerwald EF, and Barclay RMR. 2009. Geographic variation in activity and fatality of migratory bats at wind energy facilities. Journal of Mammalogy, 90(6): 1341–1349.
Baerwald EF, Edworthy J, Holder M, and Barclay RMR. 2009. A large-scale mitigation experiment to reduce bat fatalities at wind energy facilities. Journal of Wildlife Management, 73(7): 1077–1081.
Barclay RMR, Baerwald EF, and Gruver JC. 2007. Variation in bat and bird fatalities at wind energy facilities: assessing the effects of rotor size and tower height. Canadian Journal of Zoology, 85(3): 381–387.
Birds Canada. 2018. Wind energy bird and bat monitoring database summary of the findings from post-construction monitoring reports [online]: Available from birdscanada.org/resources/wind/2018_Database_Summary_Report.pdf
Birds Canada. 2020. Wind energy bird and bat monitoring database [online]: Available from birdscanada.org/birdmon/wind/main.jsp
Bolker B, and R Development Core Team. 2020. bbmle: tools for general maximum likelihood estimation. R package version 1.0.23.1. [online]: Available from CRAN.R-project.org/package=bbmle
Brooks ME, Kristensen K, Benthem KJ, van Magnusson A, Berg CW, Nielsen A, Skaug HJ, et al. 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9(2): 378.
Choi DY, Wittig TW, and Kluever BM. 2020. An evaluation of bird and bat mortality at wind turbines in the Northeastern United States. PLoS ONE, 15(8): e0238034.
Committee on the Status of Endangered Wildlife in Canada. 2013. COSEWIC assessment and status report on the Little Brown Myotis (Myotis lucifugus), Northern Myotis (Myotis septentrionalis), Tri-colored Bat (Perimyotis subflavus) in Canada Ottawa. [online]: Available from registrelep-sararegistry.gc.ca/default_e.cfm
Conenna I, López-Baucells A, Rocha R, Ripperger S, and Cabeza M. 2019. Movement seasonality in a desert-dwelling bat revealed by miniature GPS loggers. Movement Ecology, 7(1): 27.
Cryan PM, and Brown AC. 2007. Migration of bats past a remote island offers clues toward the problem of bat fatalities at wind turbines. Biological Conservation, 139(1): 1–11.
Dalthorp D, Madsen L, Huso MMP, Rabie P, Wolpert R, Studyvin J, Simonis J, and Mintz J. 2018. GenEst statistical models—a generalized estimator of mortality. In: US Geol Surv Tech Methods Book 7 Chap A2. U.S. Geological Survey, Reston, Virginia, p. 13.
Davy CM, Ford AT, and Fraser KC. 2017. Aeroconservation for the fragmented skies. Conservation Letters, 10(6): 773–780.
Davy CM, Squires K, and Zimmerling JR. 2020. Estimation of spatiotemporal trends in bat abundance from mortality data collected at wind turbines. Conservation Biology, 35(1): 227–238.
de Lucas M, Janss GFE, Whitfield DP, and Ferrer M. 2008. Collision fatality of raptors in wind farms does not depend on raptor abundance. Journal of Applied Ecology, 45(6): 1695–1703.
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, et al. 2012. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 36(1): 27–46.
Dreelin RA, Shipley JR, and Winkler DW. 2018. Flight behavior of individual aerial insectivores revealed by novel altitudinal dataloggers. Front Ecol Evol. 6: 182.
Erickson WP, Wolfe MM, Bay KJ, Johnson DH, and Gehring JL. 2014. A comprehensive analysis of small-passerine fatalities from collision with turbines at wind energy facilities. PLoS ONE 9(9): e107491.
Everaert J. 2014. Collision risk and micro-avoidance rates of birds with wind turbines in Flanders. Bird Study, 61(2): 220–230.
Ferreira D, Freixo C, Cabral JA, Santos R, and Santos M. 2015. Do habitat characteristics determine mortality risk for bats at wind farms? Modelling susceptible species activity patterns and anticipating possible mortality events. Ecological Informatics, 28: 7–18.
Fiedler JK, Henry TH, Tankersley RD, and Nicholson CP. 2007. Results of bat and bird mortality monitoring at the expanded Buffalo Mountain Windfarm, 2005. Tennessee Valley Authority.
Frick WF, Baerwald EF, Pollock JF, Barclay RMR, Szymanski JA, Weller TJ, et al. 2017. Fatalities at wind turbines may threaten population viability of a migratory bat. Biological Conservation, 209: 172–177.
Georgiakakis P, Kret E, Cárcamo B, Doutau B, Kafkaletou-Diez A, Vasilakis D, et al. 2012. Bat fatalities at wind farms in north-eastern Greece. Acta Chiropterologica. 14(2): 459–468.
Hahsler M, Buchta C, Gruen B, and Hornik K. 2020. arules: Mining association rules and frequent itemsets. R package version 1.6-6. [online]: Available from CRAN.R-project.org/package=arules
Hahsler M, Grün B, and Hornik K. 2005. arules - a computational environment for mining association rules and frequent item sets. Journal of Statistical Software, 14(15): 1–25.
Hartig F. 2020. DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.3.3.0. [online]: Available from CRAN.R-project.org/package=DHARMa
Henry L, and Wickham H. 2020. purrr: functional programming tools. R package version 0.3.4. [online]: Available from CRAN.R-project.org/package=purrr
Hull CL, and Muir S. 2010. Search areas for monitoring bird and bat carcasses at wind farms using a Monte-Carlo model. Australasian Journal of Environmental Management, 17(2): 77–87.
Huso M, Conkling T, Dalthorp D, Davis M, Smith H, Fesnock A, et al. 2021. Relative energy production determines effect of repowering on wildlife mortality at wind energy facilities. Journal of Applied Ecology, 58(6): 1284–1290.
Huso MMP, and Dalthorp D. 2014. Accounting for unsearched areas in estimating wind turbine-caused fatality. Journal of Wildlife Management, 78(2): 347–358.
Johnson GD, Erickson WP, Dale Strickland M, Shepherd MF, Shepherd DA, Sarappo SA. et al. 2003. Mortality of bats at a large-scale wind power development at Buffalo Ridge, Minnesota. The American Midland Naturalist, 150(2): 332–342.
Korner-Nievergelt F, Korner P, Behr O, Niermann I, Brinkmann R, and Hellriegel B. 2012. A new method to determine bird and bat fatality at wind energy turbines from carcass searches. Wildlife Biology, 17:350–363.
Kunz TH, Arnett EB, Erickson WP, Hoar AR, Johnson GD, Larkin RP, et al. 2007. Ecological impacts of wind energy development on bats: questions, research needs, and hypotheses. Frontiers in Ecology and the Environment, 5(6): 315–324.
Loss SR, Will T, and Marra PP. 2013. Estimates of bird collision mortality at wind facilities in the contiguous United States. Biological Conservation, 168: 201–209.
McCracken G, Lee Y, Gillam E, Frick W, and Krauel J. 2021. Bats Flying at High Altitudes. In 50 Years Bat Research. Springer, Cham. pp. 189–205.
Minderman J, Fuentes-Montemayor E, Pearce-Higgins JW, Pendlebury CJ, and Park KJ. 2015. Estimates and correlates of bird and bat mortality at small wind turbine sites. Biodiversity and Conservation, 24(3): 467–482.
Nakagawa S, Johnson PCD, and Schielzeth H. 2017. The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. Journal of the Royal Society Interface, 14(134).
Nebel S, Mills A, McCracken J, and Taylor P. 2010. Declines of aerial insectivores in North America follow a geographic gradient. Avian Conservation and Ecology, 5(2): 1.
O’Mara MT, Amorim F, Scacco M, McCracken GF, Safi K, Mata V, et al. 2021. Bats use topography and nocturnal updrafts to fly high and fast. Current Biology, 31(6): 1311–1316.e4.
O’Mara MT, Wikelski M, Kranstauber B, and Dechmann DKN. 2019. Common noctules exploit low levels of the aerosphere. Royal Society Open Science, 6(2): 181942.
Ontario Ministry of Natural Resources and Forestry. 2011. Bats and bat habitats: guidelines for wind power projects. Queen’s Printer for Ontario, Ontario Canada. [online]: Available from ontario.ca/page/bats-and-bat-habitats-guidelines-wind-power-projects
Partners in Flight. 2020. Population estimates database. Version 3.1. [online]: Available from pif.birdconservancy.org/#
Péron G, Calabrese JM, Duriez O, Fleming CH, García-Jiménez R, Johnston A, et al. 2020. The challenges of estimating the distribution of flight heights from telemetry or altimetry data. Animal Biotelemetry, 8(1): 5.
Peurach SC. 2003. High-altitude collision between an airplane and a hoary bat, Lasiurus cinereus. Bat Research News, 44(1): 2–3.
Peurach SC, Dove CJ, and Stepko L. 2009. A decade of U.S. Air Force bat strikes. Human-Wildlife Conflict, 3(2): 199–207.
R Core Team. 2020. R: A language and environment for statistical computing [online]: Available from R-project.org/
Reynolds DS. 2006. Monitoring the potential impact of a wind development site on bats in the Northeast. Journal of Wildlife Management, 70(5): 1219–1227.
Rodhouse TJ, Rodriguez RM, Banner KM, Ormsbee PC, Barnett J, and Irvine KM. 2019. Evidence of region-wide bat population decline from long-term monitoring and Bayesian occupancy models with empirically informed priors. Ecology and Evolution, 9(19): 11078–11088.
Roeleke M, Blohm T, Kramer-Schadt S, Yovel Y, and Voigt CC. 2016. Habitat use of bats in relation to wind turbines revealed by GPS tracking. Scientific Reports, 6(1): 28961.
Roemer C, Coulon A, Disca T, and Bas Y. 2019. Bat sonar and wing morphology predict species vertical niche. The Journal of the Acoustical Society of America, 145(5): 3242–3251.
Rogelj J, Shindell D, Jiang K, Fifita S, Forster P, Ginzburg V, et al. 2018. Mitigation pathways compatible with 1.5°C in the context of sustainable development. In Glob Warm 15°C IPCC Spec Rep Impacts Glob Warm 15°C Pre-Ind Levels Relat Glob Greenh Gas Emiss Pathw Context Strength Glob Response Threat Clim Change Sustain Dev Efforts Eradicate Poverty [online]. Edited by Masson-Delmotte V, Zhai P, Pörtner H-O, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MT, Lonnoy E, Maycock T, Tignor M, and T Waterfield [online]: Available from ipcc.ch/site/assets/uploads/sites/2/2019/05/SR15_Chapter2_Low_Res.pdf.
Rydell J, Bach L, Dubourg-Savage M-J, Green M, Rodrigues L, and Hedenström A. 2010. Bat mortality at wind turbines in Northwestern Europe. Acta Chiropterologica, 12(2): 261–274.
Simonis J, Dalthorp D, Huso MMP, Mintz J, Madsen L, Rabie P, and Studyvin J. 2018. GenEst user guide—software for a generalized estimator of mortality. In: US Geol Surv Tech Methods 7-C19 [online]. U.S. Geological Survey, Reston, Virginia. p. 72.
Smallwood KS. 2013. Comparing bird and bat fatality-rate estimates among North American wind-energy projects. Wildlife Society Bulletin, 37(1): 19–33.
Smith AC, Hudson M-AR, Downes CM, and Francis CM. 2015. Change points in the population trends of aerial-insectivorous birds in North America: synchronized in time across species and regions. PLoS ONE, 10(7): e0130768.
Squires KA, Thurber BG, Zimmerling JR, and Francis CM. 2021. Timing and weather offer alternative mitigation strategies for lowering bat mortality at wind energy facilities in Ontario. Animals. 11(12):3503.
Thompson M, Beston JA, Etterson M, Diffendorfer JE, and Loss SR. 2017. Factors associated with bat mortality at wind energy facilities in the United States. Biological Conservation, 215: 241–245.
Voigt CC, Currie SE, Fritze M, Roeleke M, and Lindecke O. 2018. Conservation strategies for bats flying at high altitudes. Bioscience, 68(6): 427–435.
Weller TJ, Castle KT, Liechti F, Hein CD, Schirmacher MR, and Cryan PM. 2016. First direct evidence of long-distance seasonal movements and hibernation in a migratory bat. Scientific Reports, 6(1): 34585.
Wellig SD, Nusslé S, Miltner D, Kohle O, Glaizot O, Braunisch V, et al. 2018. Mitigating the negative impacts of tall wind turbines on bats: vertical activity profiles and relationships to wind speed. PLoS ONE, 13(3): e0192493.
Whitby MD, Schirmacher MR, and Frick WF. 2021. The state of the science on operational minimization to reduce bat fatality at wind energy facilities. The National Renewable Energy Laboratory. Bat Conservation International, Austin, Texas.
Wiser R, Yang Z, Hand M, Hohmeyer O, Infield D, Jensen PH, et al. 2011. Wind energy. In: IPCC Spec Rep Renew Energy Sources Clim Change Mitig. Edited by O. Edenhofer, R. Pichs-Madruga, Y. Sokona, K. Seyboth, P. Matschoss, S. Kadneret al. Cambridge University Press Cambridge, United Kingdom and New York, NY, USA [online]: Available from ipcc.ch/report/renewable-energy-sources-and-climate-change-mitigation/wind-energy/
Wiser R, Bolinger M, Barbose G, Darghouth N, Hoen B, Mills A, et al. 2018. 2018 wind technologies market report [online]: Available from emp.lbl.gov/sites/default/files/wtmr_final_for_posting_8-9-19.pdf.
Zimmerling JR, and Francis CM. 2016. Bat mortality due to wind turbines in Canada. J Wildl Manag. 80(8): 1360–1369.
Zimmerling JR, Pomeroy A, d’Entremont M, and Francis C. 2013. Canadian estimate of bird mortality due to collisions and direct habitat loss associated with wind turbine developments. Avian Conserv Ecol. 8(2): 10.

Supplementary material

Supplementary Material 1

Information & Authors

Information

Published In

cover image FACETS
FACETS
Volume 7Number 1January 2022
Pages: 1281 - 1297
Editor: Brock Fenton

History

Received: 29 April 2022
Accepted: 16 August 2022
Version of record online: 6 October 2022

Data Availability Statement

Data used for this study are stored in the Wind Energy Bird and Bat Monitoring Database. Reasonable requests to access the database can be made to Birds Canada (bsc-eoc.org/birdmon/wind/terms.jsp). Code used in our analyses is available at osf.io/kd873/?view_only=586b03778dea4aa78ec82078696be1f4.

Key Words

  1. aerial insectivore
  2. fatality estimator
  3. Ontario
  4. turbine height
  5. wildlife mortality
  6. wind turbine

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Subjects

Plain Language Summary

Taller wind turbines may generally kill more bats and swallows, but species matters
Renewable energy sources such as wind energy are critical to reduce our reliance on fossil fuels and slow the rate of climate change. Bats and birds sometimes collide with turbine blades, and understanding factors causing wildlife collisions with turbines can help conserve biodiversity while generating essential, renewable energy. A previous study identified turbine height as a risk factor for wildlife collisions, but turbine height has increased significantly since that analysis. Since 2006, the height of wind turbines has increased from approximately 120 to 170 m in Canada. Our study aimed to test whether this trend represented a greater collision risk for wildlife, or not. To test whether turbine height affects the number of bats and swallows killed by turbines, we used a dataset from 811 wind turbines in Ontario, Canada.
We found that taller turbines were associated with more fatalities for three bat species, big brown bat, hoary bat, and silver-haired bat, but fewer fatalities for little brown bats and eastern red bats. Fatalities of purple martins and tree swallows also were higher at taller turbines than shorter turbines, but fatalities of cliff swallows and barn swallows were not associated with turbine height.
Fatalities of bats and swallows increased with turbine height for some species but not all. Therefore, increasing turbine height represents an increased risk of collision for only a subset of affected species. Species differences such as flight altitude and relative abundance (the number of individuals flying around) may contribute to differences in fatalities at turbines. Because population estimates and flight altitudes of swallows are better understood than those of bats, we speculate that swallow fatalities may provide clues about aspects of bat ecology that are not well understood, such as flight altitudes.
Although we found a relationship between turbine height and fatalities for some species, a recent study found that the number of animals killed at a turbine depends on the amount of energy the turbine produces. Therefore, although larger turbines that produce more energy may kill more animals than smaller turbines that produce less energy, the number of fatalities per amount of energy produced may remain the same. Because of this, proven methods to reduce fatalities for bats, such as preventing turbine blades from spinning when wind speeds are low, may be a more effective tool for bat conservation than regulating turbine size.

Plain Language Summary

Taller wind turbines may generally kill more bats and swallows, but species matter.

Authors

Affiliations

Alexandra M. Anderson
Department of Biology, Trent University, Peterborough, ON, Canada
Catherine B. Jardine
Birds Canada, Delta, BC, Canada
J.R. Zimmerling
Environment and Climate Change Canada, Gatineau, QC, Canada
Erin F. Baerwald
Department of Ecosystem Science and Management, University of Northern British Columbia, BC, Canada
Christina M. Davy [email protected]
Department of Biology, Trent University, Peterborough, ON, Canada
Ontario Ministry of Northern Development, Mines, Natural Resources and Forestry, Peterborough, ON, Canada
Department of Biology, Carleton University, Ottawa, ON, Canada

Author Contributions

All conceived and designed the study.
AMA performed the experiments/collected the data.
AMA analyzed and interpreted the data.
All contributed resources.
All drafted or revised the manuscript.

Competing Interests

The authors declare there are no competing interests.

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