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. 2020 Feb 13;15(2):e0228668. doi: 10.1371/journal.pone.0228668

Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts

Lia R V Gilmour 1,*, Marc W Holderied 1, Simon P C Pickering 2, Gareth Jones 1
Editor: Michael Smotherman3
PMCID: PMC7018087  PMID: 32053663

Abstract

Where humans and wildlife co-exist, mitigation is often needed to alleviate potential conflicts and impacts. Deterrence methods can be used to reduce impacts of human structures or activities on wildlife, or to resolve conservation conflicts in areas where animals may be regarded as a nuisance or pose a health hazard. Here we test two methods (acoustic and radar) that have shown potential for deterring bats away from areas where they forage and/or roost. Using both infrared video and acoustic methods for counting bat passes, we show that ultrasonic speakers were effective as bat deterrents at foraging sites, but radar was not. Ultrasonic deterrents decreased overall bat activity (filmed on infrared cameras) by ~80% when deployed alone and in combination with radar. However, radar alone had no effect on bat activity when video or acoustic data were analysed using generalised linear mixed effect models. Feeding buzzes of all species were reduced by 79% and 69% in the ultrasound only treatment when compared to the control and radar treatments, but only the ultrasound treatment was significant in post-hoc tests. Species responded differently to the ultrasound treatments and we recorded a deterrent effect on both Pipistrellus pipistrellus (~40–80% reduction in activity) and P. pygmaeus (~30–60% reduction), but not on Myotis species. However, only the ultrasound and radar treatment was significant (when compared to control and radar) in post-hoc tests for P. pipistrellus. Deterrent treatment was marginally non-significant for P. pygmaeus, but the ultrasound only treatment was significant when compared to radar in post-hoc tests. We therefore suggest that acoustic, but not radar methods are explored further as deterrents for bats. The use of acoustic deterrence should always be assessed on a case-by-case basis, with a focus on bat conservation.

Introduction

With an ever-expanding world population, increased incidences of human-wildlife interactions are inevitable. These interactions can lead to detrimental impacts on wildlife, ranging from habitat loss to direct mortality and in some cases can also have significant impacts on human lives [1]. The phrase ‘human-wildlife conflict’ can be misleading, as it pitches humans and animals against each other [2]. In areas where humans and wildlife coexist, conflict often arises between stakeholders wishing to conserve species and those who have other more anthropocentric interests [2]. Therefore, the phrases ‘human-wildlife impacts’ and ‘conservation conflicts’ more adequately sum up human-wildlife interactions [2, 3].

Human-wildlife impacts and conservation conflicts are often key conservation concerns for a wide range of taxa [3]. Many human structures and activities put species at risk, for example by inducing changes in behaviour, degrading habitats or by producing a direct mortality risk [4–6]. Conservation research has therefore focussed on mitigation strategies that exclude animals from areas where they may come to harm, or where they may impact or cause damage to human activities/structures, for example using deterrence [7–15].

Bats are one group for which deterrence has been suggested as a potential mitigation method for reducing human impacts and conservation conflicts [12, 16–19]. Protecting bat species is a key conservation concern for many European countries and many species have legal protection and/or are listed as ‘Endangered’ [20]. Being slow to reproduce, long-lived and subject to the high energy requirements of flight, bats are regarded as vulnerable to threats such as habitat loss, climate change and emerging diseases [20]. Human structures and activities can also put bat populations at risk and are therefore present potential applications for deterrence. For example, wind energy development and construction pose significant threats to bat populations, with large numbers of fatalities documented in North America in recent decades [21, 22]. Fatalities in Europe are not documented on such a large scale, but still have the potential to cause deleterious effects to resident and migratory bat populations [23–27]. Deterrence may therefore provide a way to keep bats away from the rotor-swept zone of wind turbines, reducing fatalities [16]. Similarly, roads and other transport infrastructures are also likely to have significant negative impacts on bat populations, due to habitat loss, noise pollution and mortality due to collision, yet mitigation is at present mostly insufficient [28]. Deterrence could be used alongside existing mitigation such as green bridges or overpasses, diverting bats away from flight lines over roads where they may be at risk from collision, towards safer routes.

Bats can also cause damage and a cleaning burden in historic buildings where they roost [12] and in some cases pose a human health hazard in workplaces, schools and places of worship [29, 30]. Conservation conflicts can therefore arise between those wishing to conserve bat populations and people using a building where bats are roosting and causing problems (usually with their urine and faeces) [12, 29]. In some cases, this leads to exclusion of bats from buildings, which if carried out unlawfully or without careful consideration, can be detrimental to a colony’s survival [30].

Therefore, reducing the impact of human structures, activities and conservation conflicts on bat populations, is crucial for bat conservation, and should be a priority. However, before a deterrence method is implemented, exploration of alternatives should be undertaken, following the mitigation hierarchy, first seeking to avoid or minimise any impacts before moving to reduce or compensate [31]. Indeed, using deterrence to move bats out of an area may cause unintended effects, such as habitat loss, barrier effects and/or stress, which need to be weighed up against alternative mitigation [32]. However, where more benign alternatives fail, deterrence is a method that should be considered, especially in situations where bats are at risk of serious harm or direct mortality.

Potential deterrence methods for bats include light, radar and sound [12, 16, 18, 33–35]. Some bat species are deterred by certain types of lighting, for example streetlights or flood-lights [33, 36–38]. Lighting has recently been tested as a potential bat deterrent for use in churches where urine and faeces can cause damage and a cleaning burden [12, 39]. Illumination of ‘no-fly zones’ within churches limited use of those areas, but bats became entombed in roosts that were directly lit, causing the authors to caution against using this method without careful consideration and further investigation [12]. Indeed, lighting in buildings where bats roost can be problematic and even detrimental for species that roost there, causing delays in emergence, roost abandonment, habitat fragmentation, effects on commuting, foraging and hibernation, and in some cases death [33, 40]. One striking example was the report of a 40watt light bulb causing the sudden deaths of over 1000 Myotis myotis bats in Germany, when it was left on inside a roost for two days [40]. Roosting colonies of Plecotus species were also significantly reduced in churches in Sweden, where flood-lights had been installed, when compared to non-lit churches over the same 25+ years [38]. Ultraviolet (UV) light has also shown potential as a deterrent for Hawaiian hoary bats (Lasiurus cinereus semotus) at wind turbines, where they are at risk of collision [35]. However, light has the potential to be attractive to some bat species, rather than a deterrent [33, 37], probably due to its attractive effect on insects, which often aggregate around street lights, especially those that emit UV [41–43]. Due to the potential for adverse effects of light deterrents for bats outweighing the potential benefits, we decided not to include these methods in this study and focussed instead on radar and acoustic deterrents.

Radar has been proposed as a bat deterrent, specifically for use at wind turbines [18, 19]. Suggested mechanisms of deterrence include a thermal burden effect of the electromagnetic radiation, or a jamming effect on echolocation, by high frequency sound produced during thermoelastic expansion of brain tissue [18]. Bat activity and foraging effort were lower at air traffic control regions in Scotland where radar was deployed [18]. A follow-on study, also in Scotland, recorded reduced bat echolocation call activity and foraging when an X-band (8–12 GHz) marine radar unit was used at riparian foraging sites [18].

The potential for using ultrasound (high frequency sound above 20 kHz) to deter bats has also received attention [12, 16]. Foraging bats tend to avoid noise, whether from natural sources (e.g. high frequency sounds emitted by insects and/or produced by turbulent water) [44, 45] or anthropogenic noise pollution (e.g. traffic noise) [46–49]. Ambient noise may deter bats, as it precludes the use of echolocation for prey detection or orientation, masks sounds made by insect prey, or simply because it produces a disturbing airspace [44–48]. Sources of ultrasound may also affect a bat’s ability to communicate with conspecifics or indeed the ability to eavesdrop on echolocation calls of other bats (which can be beneficial for finding foraging sources and mates) [50, 51]. Bats are also affected by high frequency ultrasonic clicks produced by some noxious moths (and their mimics) and this is due, in part to a ‘jamming’ mechanism that leaves the bat’s echolocation system unusable [52–55]. Therefore, bat deterrent systems are usually designed with the aim to mask or jam the echolocation calls of bats [16]. Field trials of acoustic deterrents at wind farm sites in North America were successful in reducing the numbers of bat fatalities [16]. The same speakers also showed potential in reducing conservation conflicts in historic buildings, where bat droppings and urine can potentially damage valuable historic artefacts [12, 39].

Deterrence is therefore a method that has potential in cases where other measures have failed, to reduce impacts of human structures and activities on bats and alleviate conservation conflicts in areas where bats roost and come into contact with humans. Our study compares the effectiveness of radar and acoustic bat deterrents at foraging sites in the UK. We also discuss the potential for these deterrents to be used in mitigation more widely.

Materials and methods

Site selection, equipment and experimental procedure

We carried out experiments during June-September 2015 at 16 riparian sites (>1 km apart, to minimise the chances of recording the same bats) that contained a stretch of river or canal with an area of still water and a bridge, chosen as they were likely to have relatively high concentrations of foraging bats [56]. River sites were located on the border of England and Wales in Herefordshire/Shropshire and Powys, (area range 52°25'16.62"N, 3°1'34.14"W to 52°20'55.92"N, 2°59'0.59"W) and canal sites in Gloucestershire and Somerset (51°49'22.81"N, 2°17'55.97" to 51°22'57.54"N, 2°23'50.84"W). We deployed ultrasonic speakers (Deaton engineering Inc., Texas, USA) and radar (X-band Marine Radar FR-8062, Furuno Electric Co., Ltd, Tokyo, Japan), together and in isolation, alternately with a silent control (no sound/radar) for 10 minutes per treatment, over 4 treatment time blocks (with a 5-minute recovery period after each treatment time block where no sound/radar was deployed). Experiments lasted 1 hour, starting 30–45 minutes after sunset (depending on ambient light levels), when bat activity was likely to be at its highest. We alternated the four treatments over the 16 sites, following a temporal Latin square design, so that each of the four treatments was deployed at least once in each of the four 10-minute time blocks. However, we could not use data from two sites in the analysis due to equipment failure. We therefore performed statistical analysis on the data using generalized linear mixed effect models (GLMMs), which control for unbalanced order in experimental design [57]. We also included time block as a fixed effect in statistical analysis, to control for temporal changes in bat activity during the experiment.

We used a near-infrared (NIR) security camera (Y-cam HD, Y-cam Inc., Twickenham, UK), with IR illumination (2 LED lamps, ShantouScene, Shenzhen, China) and a laptop computer to film the ‘treated airspace’ for 1 hour (Fig 1). We recorded bat activity acoustically using an SM2BAT+ bat detector with an SMX-US omnidirectional ultrasonic microphone (Wildlife Acoustics Inc., Massachusetts, USA; continuous .wav recording; 384 kHz sampling rate; SNR 10), placed at the edge of the treatment zone at ~20 m from the NIR camera (covering a range of ~30 m). We placed the radar unit on a table at 0.5 m in front of the camera, with the antenna at 1 m height, in the fixed position (rather than rotating) and set it to emit a pulse length of 0.3 μs (repetition rate 1200 Hz, peak power 6 kW), as this was the most likely set-up and duty cycle to affect bat activity [18] (beam width: horizontal = 1.9°, vertical = 22.0°). We placed ultrasonic speaker units on chairs at ~0.5 m height and ~0.5 m apart and angled them in the same direction as the radar beam towards the middle of the treatment area, perpendicular to the baseline of the treatment area (where the camera was placed). Speakers were the same units as used at a wind energy facility in North America [16] and in churches in the UK [12, 39] and had 16 transducers capable of emitting continuous broadband ultrasound at 20–100 kHz, with a frequency of most energy of 50 kHz (Senscomp, Michigan, USA; source level at 1 m 110 dB SPL min at 50 kHz; 85 dB SPL at 20 meters, 20°C, 10% relative humidity and 101.33 kPa [16]; beam angle 15° at -6 dB) (Fig 2). The speakers were chosen for testing as their frequency of most energy overlapped with the echolocation call frequencies of British bat species likely to be present during experiments, including Pipistrellus pipistrellus (frequency of most energy 45 kHz), P. pygmaeus (55 kHz) and Myotis species (30–50 kHz) (Fig 2). We recorded temperature every 15 minutes using a Watson W-8681-SOLAR weather station (Watson Inc., Beijing, China). Experiments were carried out on low wind nights (wind speeds <5 m/s) when there was no rainfall forecast, as wind and rain can reduce bat activity. We powered the camera and acoustic deterrents using a low-noise generator (Honda EU10i, Honda, Tokyo, Japan), placed >10 m from the treatment area, and the radar unit by a Bosch 12 V battery (Robert Bosch Ltd., Uxbridge, UK). The generator was running during both control and treatment periods and a previous study using a similar model found no generator effect on bat activity [34].

Fig 1. Schematic of example experiment set-up at riparian sites.

Fig 1

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Schematic of experiment set-up at riparian sites, including treated airspace (textured area) in an area of river/canal with a bridge, flanked by a tree line or hedge on one side. Near infrared (NIR) video camera and laptop were set up at 0 m (a.), the radar unit on a table at 0.5 m from the camera (b.), the acoustic deterrent speaker units on chairs at 1 m (c.) and the SM2 BAT+ bat detector at ~20 m (d.).

Fig 2. Spectrogram and power spectrum of acoustic deterrent speaker output and spectrograms of echolocation calls of bat species recorded.

Fig 2

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Spectrogram (A.) and power spectrum (B.) calculated from acoustic deterrent speaker unit output recorded on-axis in an anechoic chamber using a Sanken CO-100K Super Wide Range Microphone and calibrated using a type 4231 Brüel & Kjær calibrator (114 dB SPL at 1 kHz). Power spectrum dB SPL measurements calculated at 1 m and adjusted for spectral sensitivity of microphone and distance (original distance 2.2 m, FFT 128, Hamming window, calculated in Avisoft SASLab Pro). Spectrograms of bat echolocation calls (C.), including two calls from a sequence identified as Pipistrellus pipistrellus (a.), P. pygmaeus (b.) and Myotis species (c.). Both spectrograms were created using Raven Lite 2.0.0 with the same settings (spectrogram window Hann, size 512, brightness 69, contrast 71).

Video and acoustic analysis

We calculated bat activity from NIR footage for each treatment (number of bats moving in and out of frame) using Quick Time Player (v7.7.8, Apple Inc, Cupertino, USA). Video analysis was carried out blind to treatment and results were validated by an independent observer (for five randomly selected sites). We identified bat passes manually to genus or species level where possible using Bat Sound (v4.1.4, Pettersson, Uppsala, Sweden; FFT size: 1024; FFT window: Hanning) and calculated acoustic bat activity, as the number of passes or feeding buzzes in 10 s (a new pass was identified as a sequence of calls >1 s from the last and feeding buzzes are discernible due to their high repetition rate) [58, 59].

Speaker noise completely masked bat calls recorded at eight sites (peak frequency threshold of >40 kHz). For the remaining six sites, calls were discernible in ultrasound treatment files, but still less so than in radar and control files, where no deterrent sound was broadcast. We therefore added the deterrent noise to files recorded at six sites recorded during non-ultrasound treatments using MATLAB 2016a sum wave files function (Mathworks, Natick, USA), to avoid any bias introduced by some files being easier to score.

Variables and model specification

We analysed the following response variables using GLMMs: visual bat activity (NIR video), acoustic bat activity (Pipistrellus pipistrellus, P. pygmaeus and Myotis species) and bat feeding buzzes for all species. We included the fixed effects of deterrent treatment (with levels: radar, ultrasound, ultrasound and radar, control), time block (levels: A-D), temperature and an interaction term between deterrent treatment and time block in full models for the video data. We also included an interaction term between deterrent treatment and temperature, to examine any effects of temperature on the transmission of radar and/or ultrasound through the treatment area. However, temperature data were missing at one site, due to equipment failure and were substituted for the mean of all sites (<10% of data). Full models for acoustic data were the same but did not contain temperature data, due to missing data representing >10%. We also did not include an interaction term between deterrent treatment and time block in acoustic models, due to the low sample size precluding the use of a more complex model (rank deficiency). We retained the random effects of site (N = 14 for NIR data, N = 6 for acoustic data) and time block (A-D) in final models to control for the repeated measures design and to reduce pseudoreplication.

Statistical analysis

We analysed bat pass count data with generalized linear mixed effect models (GLMMs), with a Poisson family and log link function in R (v3.6.1), using the lme4 package (v.1.1–21)[60]. We followed the backwards step-wise model selection method to find the most parsimonious, yet best-fit model for the data (final model) [57, 61]. We removed terms sequentially from a more complicated model when likelihood ratio tests (LRT) were non-significant and retained significant terms in the final model. LRT statistics are presented as χ2, df and p value and were obtained from LRTs between a model containing a term, and a restricted model without that term (or the null model). We present effect sizes and standard errors for final models in a table and post-hoc Tukey contrast test results in the text as z-statistics and p values obtained using the multcomp package (v1.4–1) [62]. We validated final models by simulation using the R package DHARMa v.0.2.0, using residual plots to check for overdispersion, heteroscedasticity and zero inflation [63].

Ethics statement

This study was approved by the University of Bristol Animal Welfare and Ethical Review Body (licence no: UB/17/045) and carried out in accordance with, and under strict recommendations from the government licensing departments Natural England (2015-12272-SCI-SCI) and Natural Resources Wales (66141:OTH:CSAB:2015). Privately owned sites and those managed by the Canals and Rivers Trust were accessed with permission for all field experiments.

Results

Near-infrared video passes

We recorded a total of 3668 bat passes from 14 hours of near infrared (NIR) video footage (electronic supplementary material S1 Table) and a mean number of bat passes (± SD) of 489.07 ± 253.04 per site. The final model for NIR video data did not show overdispersion, zero-inflation or heteroscedasticity, when data were simulated using the R package DHARMa (v.0.2.0) [63]. The model included the fixed effect deterrent treatment, but there was no effect of temperature, time block or either interaction terms (between deterrent treatment and temperature/time block) (Table 1). Bat activity (NIR video passes) was significantly reduced when an ultrasonic deterrent was deployed, but radar had no effect (Table 1 and Fig 3). Post-hoc Tukey contrast tests showed there was a significant reduction in bat activity, during ultrasound treatment blocks compared to the control periods and to radar treatment alone (81 and 84% reduction respectively) (ultrasound-control: z = -4.63, p < 0.001; ultrasound-radar: z = -4.89, p < 0.001). Bat passes were also significantly reduced (by 78 and 82%) when ultrasound and radar where deployed together, compared to the control, and to radar, respectively (Tukey contrasts: ultrasound & radar-control: z = -4.30, p < 0.001; ultrasound & radar-radar: z = -4.56, p < 0.001). Tukey contrasts showed there was no difference between ultrasound treatments and there was no reduction in bat activity when radar was compared to the control (ultrasound & radar-ultrasound: z = -1.46, p = 0.46; radar-control z = 0.28, p = 0.99).

Table 1. Final model estimates (± SE) and likelihood ratio test statistics for near infrared (NIR) video and acoustic bat pass data, including Pipistrellus pipistrellus, P. pygmaeus and Myotis spp. passes and feeding buzzes of all species.

Model Model terms Estimates SE χ2 df p
NIR video (Intercept) 3.32 0.28
Deterrent treatment 29.92 3 < 0.001
 Radar 0.09 0.31
 Ultrasound -1.51 0.33
 Ultrasound & radar -1.39 0.32
Time block 0.69 3 0.88
Temperature 1.53 1 0.22
Deterrent treatment * temperature 3.63 3 0.30
Deterrent treatment * time block 13.87 9 0.13
Random effects Variance SD % total
Time block (within site) (N = 4) 0.62 0.79 59.12
Site (N = 14) 0.43 0.65 40.88
P. pipistrellus (Intercept) 3.62 0.36
Deterrent treatment 11.72 3 < 0.01
 Radar -0.52 0.44
 Ultrasound -1.06 0.45
 Ultrasound & radar -1.76 0.47
Time block 0.04 1 0.84
Random effects Variance SD % total
Time block (nested within site) (N = 4) 0.55 0.74 74.45
Site (N = 6) 0.19 0.43 25.55
Feeding buzzes (Intercept) 3.04 0.46
Deterrent treatment 10.8 3 < 0.01
 Radar -0.36 0.38
 Ultrasound -1.45 0.41
 Ultrasound & radar -0.72 0.39
Time block 2.05 3 0.56
Random effects Variance SD % total
Time block (nested within site) (N = 4) 0.35 0.59 29.2
Site (N = 6) 0.84 0.92 70.8
P. pygmaeus Deterrent treatment 7.36 3 0.06
Time block <0.01 1 0.95
Random effects Variance SD % total
Time block (nested within site) (N = 4) 0.84 0.92 64.12
Site (N = 6) 0.47 0.69 35.88
Myotis spp. Deterrent treatment 2.68 3 0.44
Time block 3.78 3 0.29
Random effects Variance SD % total
Time block (nested within site) (N = 4) 1.22 1.1 59.22
Site (N = 6) 0.84 0.92 40.78
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Fig 3. Number of near infrared video (NIR) and acoustic bat passes recorded during control and deterrent treatments.

Fig 3

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Bat activity (mean number of passes) during 4 treatments of ultrasound (U), radar (R), ultrasound and radar (U+R) and a control (C), including counts of bat passes recorded on near-infrared (NIR) video footage (a) and acoustic bat passes identified as Pipistrellus pipistrellus (b), P. pygmaeus (c), Myotis spp. (d) and feeding buzzes of all species (e). Including SE error bars and p values from post-hoc Tukey comparisons, presented as significance stars and associated label of treatment comparison (* = p < 0.05, ** = p < 0.01, *** = p < 0.001, **** = p < 0.0001). NIR video N = 14, acoustic data N = 6.

Acoustic passes

A total of 3073 acoustic bat passes were identified at 6 sites and a mean number of bat passes per site of 512.17 (± SD 287.79), including 1518 Pipistrellus pygmaeus, 618 P. pipistrellus and 388 Myotis species passes and 514 feeding buzzes (representing 49, 20, 13 and 17% of passes) (electronic supplementary material S2–S5 Tables). Rhinolophus hipposideros, unknown Pipistrellus species, Eptesicus serotinus and Nyctalus species made up the remaining passes (1%). Final models for acoustic data were not overdispersed or zero-inflated and also did not show heteroscedasticity in DHARMa (v.0.2.0) simulations [63]. Final models for P. pipistrellus data included the fixed effect of deterrent treatment, but there was no effect of time block on the number of passes recorded. P. pipistrellus passes were significantly reduced by 52 and 79% respectively during ultrasound treatments (ultrasound only; ultrasound and radar, compared to control). There was also a 39 and 72% reduction in P. pipistrellus passes during the ultrasound only, and ultrasound and radar treatments respectively, when compared to the radar only treatment. However, only ultrasound and radar treatments were significantly different in Tukey tests (Table 1 and Fig 3; Tukey contrasts: ultrasound & radar-control: z = -3.75, p < 0.01; ultrasound & radar-radar: z = -2.61, p < 0.05; ultrasound-control: z = -2.34, p = 0.09; ultrasound-radar: z = -1.17, p = 0.65; radar-control: z = -1.18, p = 0.64, ultrasound & radar-ultrasound: z = -1.46, p = 0.46). We recorded a 61 and 40% reduction in P. pygmaeus activity compared to the control, and a 56 and 33% reduction compared to radar, when ultrasound was deployed alone and combined with radar. However, the null model was the most parsimonious when P. pygmaeus data were analysed using a GLMM and deterrent treatment was marginally non-significant in LRT tests (Table 1). Despite this, ultrasound and radar were significantly different in Tukey contrast tests (ultrasound-radar: z = -2.63, p < 0.05; ultrasound-control: z = -2.01, p = 0.93; ultrasound & radar-control: z = -1.44, p = 0.47; ultrasound & radar-radar: z = -2.05, p = 0.17; radar-control: z = 0.61, p = 0.93; ultrasound & radar-ultrasound: z = 0.56, p = 0.94). Myotis species activity was not affected by any of the deterrent treatments, with similar numbers of passes recorded for all treatments. Bat feeding activity was significantly reduced (by 79 and 69%) during the ultrasound treatment, compared to the control and radar treatments and by 48% during ultrasound and radar treatment when compared to the control. However, bat activity was higher (25% increase) in ultrasound and radar treatments when compared to radar, although no significant effect of the ultrasound and radar treatment, or radar was observed in Tukey contrast tests (ultrasound-control: z = -3.57, p < 0.01; ultrasound-radar: z = -2.65, p < 0.05; ultrasound & radar-control: z = -1.87, p = 0.24; ultrasound & radar-radar: z = -0.92, p = 0.79; radar-control: z = -0.96, p = 0.77; ultrasound & radar-ultrasound: z = 1.75, p = 0.30).

Discussion

In this study, we have shown that radar was ineffective as a deterrent for bats at foraging sites, but acoustic methods showed considerable promise. Previous work suggested that bat activity was reduced at foraging sites in Scotland, UK, by radar deployment over a 10–30 m range [18]. However, we could not confirm this deterrent effect, using video nor acoustic data, despite using similar methodology and recording over the same range of up to 30 m. The radar beam area projected by the unit used in both our study and the previous work in Scotland was highly directional. The horizontal and vertical beam angle of 1.9° and 22°, respectively, would result in a treated airspace of ~0.7–1 m wide and 8–12 m tall (at ~20–30 m from the deterrents). In comparison, the 15° beam angle of the speakers would have resulted in a ~5–8 m treated airspace both horizontally and vertically. Therefore, bats may have only encountered the radar beam briefly at the centre of the treatment area, when flying through it, possibly limiting any potential for deterrence, if any exists. However, the speakers were positioned with the same line of site of the radar beam, with one speaker either side of the centre of the antenna (Fig 1) and so were likely to have covered the same treatment area vertically. Despite this and the fact that the radar unit and methodology were very similar, it is unclear why the results of our study did not corroborate the findings from the Scottish study [18].

Bats are known to avoid ambient and broadcast noise and this study supports previous research in this area [12, 16, 45, 47, 48]. However, this study is the first to show a reduction in bat activity at foraging sites using broadcast ultrasound in a European context. We recorded a clear effect of ultrasound on bat activity with an ~80% reduction seen in the video footage data (when compared to control and radar treatments) (Fig 3). However, the acoustic data does not show such a clear trend, possibly due to unavoidable noise in the data from bat echolocation calls being recorded outside the range of the deterrent and small sample sizes that were unavoidable due to the deterrent masking echolocation calls at some sites. It was also not possible to discern feeding buzzes to species level due to high levels of overall activity and often more than one species in each file. Despite this, ultrasound treatments had the lowest mean number of bat passes recorded for all datasets, excluding Myotis species (Fig 3). We also found an effect of the ultrasound and radar treatment (when compared to control and radar only) and the ultrasound only treatment (when compared to radar) on Pipistrellus pipistrellus and P. pygmaeus activity respectively. There was also an effect of ultrasound only on feeding activity of all species. Myotis species were not significantly affected by any deterrent treatment.

The lack of response to acoustic deterrence by Myotis bats compared to Pipistrellus species, may have been due differences in hearing and/or the mechanisms underpinning deterrence. For example, the deterrent sound could have acted as an aversive stimulus rather than a masking one, as was the case in traffic noise playback experiments on M. daubentonii [46]. How a bat species responds to a deterrent sound may be in part due to its hearing threshold, which in bats typically range from about 20–30 dB, but may be as low as 0 dB [64–66]. Hearing thresholds of bats are largely understudied, but can depend on frequency, the hearing system of the individual and even the time of day [64–66]. Therefore, a difference in hearing thresholds may account for the differences in response to acoustic deterrence in this study. The different response to the deterrent of Myotis bats may also have been due to the experimental site selection and set-up. Due to the nature of the riparian sites, the Myotis species bats recorded were likely to be Myotis daubentonii, which feed directing their echolocation calls towards the water [67]. The Myotis bats may therefore have moved along the water during ultrasound treatments, away from the speakers, to nearer the bridge, where we had placed the bat detector, resulting in more passes recorded during ultrasound treatments. As Pipistrellus species are not limited to feeding over water, they may have dispersed in different directions when the sound was broadcast, rather than in the direction of the bat detector microphone. Myotis nattereri were deterred from specific roosting areas, with no habituation effect found after 15 days when the same acoustic deterrents as used in this study were tested in churches in Norfolk in the UK [12]. Therefore, a deterrent effect of ultrasound can not be ruled out for Myotis daubentonii, without a follow-up exploration of acoustic deterrents focussed on this species in this context (e.g. with speakers pointing at the water’s surface).

Our findings support the premise that ultrasonic speakers show promise for use as bat deterrents. We therefore recommend that these methods be considered as a way of reducing impacts on bats from human structures and activities, and in situations where conservation conflicts arise from bats roosting in buildings. For example, these methods could be used at wind turbines to reduce bat fatalities in Europe, as has been done in North America [16]. Acoustic deterrence could also be used to manage bats that roost in buildings where people live, work, study and worship, alleviating cleaning burdens, damage and risks to human health. For example, the US Centre for Disease Control and Prevention (CDC) regards bats roosting in buildings as a reservoir for histoplasmosis and therefore recommends exclusion to prevent the threat to human health [68]. However, currently the CDC guidelines explicitly state that deterrents are ineffective in this context. Therefore, we recommend updating these guidelines to reflect the potential of ultrasonic deterrence.

Another application for acoustic deterrence is as part of transport infrastructure mitigation. For example, acoustic deterrence methods could be used in combination with existing mitigation methods (e.g. over/underpasses, green bridges), to prevent bats from crossing roads or train-lines, where they may be at risk from collision and mortality [28]. For example, acoustic deterrence has been tested as a potential mitigation strategy for use in areas where woodland bats may be affected by new train lines [69]. Current bat mitigation strategies for roads are at present regarded as largely insufficient [28]. Methods such as overpasses that are currently ineffective [70], could therefore be used in combination with acoustic deterrence, allowing bats to utilise safer flight lines over roads.

Despite its potential, acoustic bat deterrence may have welfare implications that need to be considered when weighing up its use against alternative mitigation methods. Deterrence, by its design, acts to move animals out of an area, which may mean a reduction in access to foraging resources or habitat features (such as roosts or commuting routes). If these resources are rare in the remaining habitat not affected by deterrence, or if the noise degrades surrounding habitats due to overspill effects, this could lead to unwanted impacts on the target species (and non-target species). However, small-scale movement of bats to new roosts within churches using acoustic deterrence did not affect where radio-tracked bats from the same church went to forage and also had no other obvious impacts on behaviour [12, 39]. Bats are likely to respond to an acoustic deterrent stimulus in a similar way to that from an anthropogenic source, such as traffic or gas compressor noise [46–49]. Anthropogenic noise can induce measurable stress responses in some animals such as an increase in cortisol levels or heart rate [32]. However, any results of stress indication should also be weighed up against the short and long-term effects of the human activity being mitigated for, which may cause more harm to bats in the long term.

In conclusion, acoustic deterrence shows great potential for use as a mitigation measure, to reduce human impacts on bats in a wide range of contexts. However, we found no evidence of radar being an effective deterrent. We caution against the wide-spread use of acoustic deterrence as a universal solution to bat mitigation and recommend exploration of its use on a case-by-case basis, following the mitigation hierarchy [31]. Displacement of bats may often seem a legitimate way forward for conservation, but as with any mitigation measure, the methods need to be weighed up against less invasive methods, avoiding any potentially detrimental effects. Further work therefore needs to focus on safe, effective, practical and targeted implementation of deterrents in the applications discussed. As species-specific responses to acoustic deterrence may also influence the efficacy and safe use of these methods, behavioural mechanisms underpinning deterrence should also be explored, along with differences in hearing and the distance over which these methods are effective for different species.

Supporting information

S1 Table. Number of bat passes recorded on near infrared video during deterrent treatments and control.

(DOCX)

Click here for additional data file. (26KB, docx)
S2 Table. Number of Pipistrellus pygmaeus passes recorded during deterrent treatments and control.

(DOCX)

Click here for additional data file. (21.5KB, docx)
S3 Table. Number of Pipistrellus pipistrellus passes recorded during deterrent treatments and control.

(DOCX)

Click here for additional data file. (21.7KB, docx)
S4 Table. Number of Myotis spp. passes recorded during deterrent treatments and control.

(DOCX)

Click here for additional data file. (21.5KB, docx)
S5 Table. Number of feeding buzzes recorded during deterrent treatments and control.

(DOCX)

Click here for additional data file. (21.5KB, docx)

Acknowledgments

We thank the Bats and Wind Energy Cooperative for use of their speakers. We also thank all the project volunteers for their hard work, with special thanks to Eleanor Field for carrying out video analysis. We thank all the landowners of the sites used in the study for their cooperation, including Canals and Rivers Trust and private landowners that do not wish to be named.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This study was funded by the National Environment Research Council (NERC) (NE/K007610/1), with CASE contribution from Ecotricity (www.ecotricity.co.uk), received by LRVG and PI was GJ. The funders (NERC) had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. SPCP of Ecotricity Group Limited also provided a supervisory role in the project and review of the manuscript before submission for publication.

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PONE-D-19-23958

Deterrence as a mitigation measure to reduce conflict between bats and humans

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

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Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This manuscript is very well written and describes a straightforward set of experiments testing the effects of broadband noise and radar on localized bat activity. There are only a few previous studies on the topic, and none were nearly as rigorous and thorough as this one. The experiments provide what I consider to be the best evidence so far that broadband noise can be used to deter bats from using or entering an area. The study also does a good job of challenging the hypothesis that radar can be an effective deterrent, which was dubious from the start but very difficult to test. The large sample size and the rigorous comparison of the differences in results obtained with audio and video also makes this paper very strong. Thus, I think this paper will become highly cited in the field and a cornerstone of future efforts.

I only have a few suggestions and comments.

1) The manuscript provides compelling evidence of species differences in the response to the ultrasonic deterrent. This species effect is worthy of being mentioned in the abstract even if the underlying reasons are not yet clear, because this should be a point of emphasis for future studies.

2) I would recommend including the supplementary figure S1 in the main text, and I suggest adding either representative spectrograms or power spectra of the bat pulse emissions to illustrate the extent to which the stimulus overlapped with the main bat species being studied. Alternatively, in the methods section after line 91, it would be helpful to provide the reader with a brief description of the pulse acoustic properties in relation to the stimulus acoustic properties. The extent of overlap between the bandwidth of the noise and the pulses may be important for predicting species differences in the response.

3) Line 91: for completeness, do you have information about the beam projection angle? The radar beam angle was provided on line 86, and it was discussed that the narrow beam angle may be the reason radar was ineffective. However, the ultrasonic beam angle is needed for comparison.

4) Introduction, and Line 63-64. An important motivation for deterring bats from buildings that is not mentioned in the introduction/discussion is that bat colonies pose health hazards, particularly when they invade schools or other public buildings. The US Center for Disease Control (CDC) guidelines for dealing with bats explicitly states that ultrasonic deterrents are ineffective (https://www.cdc.gov/niosh/docs/2005-109/pdfs/2005-109.pdf ), citing Tuttle, 1988. This topic might be something worth addressing in the manuscript.

Typos: line 78 (latest/lasted)

Line 230 (moved/moving?)

Reviewer #2: Manuscript Number: PONE-D-19-23958

Manuscript Title: Deterrence as a mitigation measure to reduce conflict between bats and humans

This study aimed at testing two acoustic measures to deter bats from their foraging sites: ultrasonic sound and radar, alone and in combination. While acoustics play an important role in the lives of bats, the rationale for doing this study somewhat missed me. As the authors indicate, there already exists evidence of bats being deterred from wind turbines (and churches). Thus this study only corroborated this without adding more knowledge, e.g. regarding why bats are deterred. I also have some concerns regarding the framing of the manuscript. They focus is on deterrence in general, while the literature cited mainly is from wind turbine deterrence. While deterrence may be an option for mitigation, when other measures (e.g. avoid, minimize) have been tried I fail to see how it can be employed in the general sense. The authors mention, besides wind turbines, also deterring bats from roads and foraging sites. However, both would have detrimental effects to bat populations; the latter depriving them from their food sources and the first creating barrier effects. I guess this was unattended by the authors, but the framing of using acoustics indiscriminately does neither help bats nor humans in my eyes. Below follow more specific comments:

L11: “impacts of threats” – what is this, did the authors mean “risk of impact”?

L12: “sensitive areas such as protected artifacts” is somewhat unclear to me: sensitive to whom, bats of humans? Why not just say historic buildings or human structures?

L12-13: specify where you deterred bats from, i.e. their riparian foraging sites.

L16: Pp echolocation call activity was reduced by ~40-80% not 70-80%! Only the combination of ultrasound + radar was significant. This needs to be clarified. Include also the non-significant effects on Myotis and P pygmeus.

L17-19: Why would you suggest that only ultrasound should be used as deterrent, when in some of the cases only the combination significantly reduced bat activity?!

L22: I find the wording of “parties” somewhat misleading: are bats a party (politically, socially or other) in this? What do you mean by “impact”; mortality of individuals, loss of habitat or population reductions?

L23: I guess that in 99% of the time it is wildlife that is impacted by humans and not vice versa. This, either by taking into use species’ habitats, or killing them when they cause nuisance.

L25-26: maybe better to say that we are mainly talking about human-human conflicts here?!

L28: I would suggest using “human structures and activities” (omitting “-built”) as then “human” links to both structures and activities; now it doesn’t.

L31: “…where they may come to harm” or cause harm to human structures and activities (i.e., avoiding conflict).

L33-34: Be clearer why bats would need to be deterred. All references are from wind turbines apart from one; would it not be more realistic to either extend the scope of structures/activities or set specific focus on wind energy?

L34-35: “…bats are already…” already vulnerable relative to what? One example given (habitat loss) is mainly human-caused; isn’t that part of the human-wildlife conflict? Or do you see HWC mainly as bats causing nuisance for humans?

L39-42: In this example I fail to clearly see the stakeholder conflict. What is this conflict centered on?

L42-43: Maybe indicate how bats may be affected by roads. Also I fail to see the link to deterrence here.

L47: Before going into reducing impacts, may clarify that in all cases the mitigation hierarchy should be the leading line (avoid, minimize, reduce, compensate, restore). Also, clarify when deterrence may be implemented: in itself it may enhance functional habitat loss and barrier effects for bats, so maybe not preferred over other more benign measures?! The references that are supposed to cover light, sound and radar seem to miss those relating to light (e.g. [23,24]), and what about [12]?

L52: I would suggest moving this sentence after L52-55.

L57: Bats avoid insect noise? If this was actually meant, please include references (also for turbulent water).

L58-60: All these references relate to anthropogenic noise? Still the statement is generic, and should therefore also include natural causes of noise.

L61: What is the difference between communication and eavesdropping exactly? Is eavesdropping not a specific form of communication? Also, I would suggest explaining what eavesdropping is for the non-expert.

L66: Why was light not also included? While it is mentioned above, this is not included. Explain why the focus lies on acoustics.

L65: Can you give examples where bats actually cause conflict? Where would deterrence be needed, contrary to other mitigation measures?

L77: Isn’t this called “time blocks” in the models? Please clarify.

L78: Did the experiments last (spelling mistake here) 1 hour or 55 minutes? (4x 10 min + 3x 5 min in-between = 55 minutes)

L80: Was this alternation only done spatially or also temporarily?

L84: 0.3 milli sec (ms) or 0.3 micro sec (μs)?

L87-89: how directional were the speakers exactly? Was their sound emission measured? Could it also be that the narrow horizontal radar beam caused non-significant effects in this measure contrary to the ultrasound? What would the results be if the radar was tilted 90 degrees giving a narrow vertical beam but wide horizontal beam? Also, I would suggest inclusion of a picture presenting the exact practical layout of the design spatially.

L90: What was the peak power of the speakers?

L97: 20m from the radar or speakers or camera? Unclear.

L114: “in” instead of “during”?

L115-117: I don’t understand, the results speak of 6 sites being included in the analyses, here it states that all were included after having added deterrent noise. Which is it?

L118-132: I would move this section after the next “Variables and model specification”. In addition, it seems you have used both a information theoretic AND frequentist approach in the statistical model/term selection. This is somewhat confusing, I would urge you to choose one of the two.

L126: “restricted model” instead of “nested model”?

L127: How were the final model validated exactly? I do not find any information on this in the results.

L130-132: I do not follow this sentence.

L133-143: What was the generic design of the study, did it follow a Control-Impact design? If so, maybe it is more illustrative to only show the full models to be able to see the effects or non-effects of the treatment?! Unless you wish to better understand in what circumstances deterrence worked well (or not); such as temperature or wind speed. I was somewhat baffled to notice that wind speed, which clearly affects both bat activity and sound emission and ambient noise, was not included in the models. Was ambient background noise measures at all?

L153: maybe clarify that this is the mean number of bat passes and give the unit (i.e. per day, per experiment, per hour, per 10-minute interval, per minute?).

L156: “per time unit” – what is the time unit used? Be clear.

L166 (table): What is the difference between the fixed effect “Time block” and the random effect “Block”? Why was an interaction between deterrent and temperature included? Should also an interaction between deterrent and time block be considered?

L181-185: No results are given regarding which of the models were most parsimonious (Table S2). This table clearly indicates that the most parsimonious model (the one with lowest AIC, whereby usually ΔAIC<2 are seen as being equally good) would be the null model and not the deterrent treatment model?! This would mean that none of the echolocation models rendered any significant outcomes.

L196-197: Were related Tukey tests also non-significant?

L203-204: What were the results for all bat species pooled regarding acoustic passes? This would enable a direct comparison to the visual video-footage.

L205 & L214: This is not a chapter I mam afraid…

L215-216: Tja, although done at a new site, this study merely corroborates earlier finding. What new insights have been obtained?

L222: Discuss why the combination of ultrasound and radar led to a better result.

L228-230: Why? The radar beam has a wide vertical beam which should be expected to cover both the water surface and the airspace above (unless it was placed too close to the foraging site). I have not seen any information regarding the directionality of the speakers (horizontally and vertically). Is there also any specifics of the riparian sites regarding habitat (e.g. treed vegetation, topography) that may have affected the results?

L230: the bats “may have been moved”? By whom? Maybe rephrase.

L239: Are there clear difference in hearing between these species that might explain their responses (or lack thereof)?

L240-241: Why would anyone wish to exclude bats from their foraging sites, especially riparian areas? What may be expected to be built there (not likely to be wind turbines or churches)? What human activities will conflict with bat presence?

L244-246: Are you really suggesting to deter bats from roads, increasing barrier effects roads already pose even more? I fail to see how this may help conserve bat species. Reference [22] suggests underpasses instead. Although roads may affect bats through noise, your study fails to give any indication how bats are affected by ambient noise.

L246: What other human structure and activities, other than wind turbines and roads, are you thinking of here?

L247-248: What “specific scenarios” are you thinking of here? Different spatial planning and development scenarios? Scenarios of locating different structures or activities and their expected effect? It is unclear to me what is meant here.

L249: The distance over which speakers or radar have an effect in deterring bats should preferentially have been part of this study.

L249-250: This comes back to my earlier question whether the different results might have been caused by differences in hearing among species? The same rationale would also matter for radar (e.g. different emission bands)? Please add references to indicate to which extent this would be possible.

L251.255: This is in fact the first time you indicate that possible deterrence may not be the first and foremost preferred measure to implement. PI think this point should be raised already in the introduction, together with an indication when it might be best to implement (and when not). Now the manuscript seems to say that acoustic deterrence will work ate wind turbines, churches, roads, foraging sites, etc. Also, something that may be discussed is how practical the implementation of acoustic deterrence is: can it really be implemented along (long stretches of) roads?

Cheers Roel May

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Reviewer #1: Yes: Michael Smotherman

Reviewer #2: Yes: Roel May

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PLoS One. 2020 Feb 13;15(2):e0228668. doi: 10.1371/journal.pone.0228668.r002

Author response to Decision Letter 0

4 Dec 2019

School of Biological Sciences

University of Bristol

24 Tyndall Avenue

Bristol BS8 1TQ

03/12/19

Rebuttal letter for re-submission to PLoS ONE

Manuscript reference: PONE-D-19-23958

Manuscript title: Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts

Dear Dr Baker,

Thank you for your invitation to submit a revised version of our manuscript for consideration by PLoS ONE. The submitted comments from both reviewers were very helpful in allowing us to provide a revised manuscript that thoroughly introduces the topic and background of bat deterrence methods, as well as framing our research within the field.

Reviewer 1’s (R#1) comments are very encouraging and complimentary and they clearly understood the main aims of the study and how it contributes to the field of bat deterrence methods. R#1 also describes our methods of using acoustic and near infrared video as a rigorous and our approach thorough. We welcome their suggestions to include bat echolocation call spectrograms for comparison with the deterrent output and thank them for drawing our attention to the US CDC guidelines.

R#2 provided comments and questions in the detailed line-by-line analysis of the manuscript that were very helpful in allowing us to identify areas of the manuscript that needed more information or description. Many of the comments and criticisms given by R#2 were likely due to the manuscript being too concise and have been easily be remedied by additional information. We hope that the rationale behind the study is now clearer.

We also acknowledge that R#1’s background is in bat ecology, bioacoustics and conservation, unlike R#2. Therefore, the context in which this study sits and the wider issues it addresses may be less obvious for someone with a background in broader areas of conservation, such as R#2. It is therefore useful to have both reviewers contrasting comments, as it allows us to make sure we frame the manuscript, so that it is explicit in what the study is trying to achieve, the issues it addresses and its applicability in different scenarios. The comments have therefore been very helpful in allowing us to make sure the manuscript is useful for a wider readership, not just those who have a specific interest in bat conservation.

Below is a general and line-by-line response to each of the referee’s comments. We have also made the required changes (where possible) to the manuscript in line with your request to adhere to the journal requirements (see below). We hope that our careful attention to the reviewers’ comments will now make our manuscript suitable for publication in PLoS ONE.

Yours sincerely,

Lia Gilmour

Journal requirements:

- Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

- We have checked all our file names and made sure the manuscript meets PLOS ONE’s style requirements.

- In your Methods section, please provide additional location information of the experimental sites, including geographic coordinates for the data set if available.

- We have included a range of geographic locations for the areas that we carried out experiments in on L136-137.

- However, we were asked by the landowners of our sites not include the exact locations of these sites and therefore cannot provide locations to any higher level of resolution.

- Thank you for stating the following in the Financial Disclosure section…Please provide an amended Competing Interests Statement that explicitly states this commercial funder, along with any other relevant declarations relating to employment, consultancy, patents, products in development, marketed products, etc

- As requested, we have provided an amended competing interests statement and financial disclosure statement (below), explicitly stating the commercial funder and the contribution provided towards the PhD stipend of Lia Gilmour, the student carrying out this PhD project.

Financial Disclosure Statement

This study was funded by the National Environment Research Council (NERC) (NE/K007610/1), with CASE contribution from Ecotricity (www.ecotricity.co.uk), received by LRVG and PI was GJ. The funders (NERC) had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. SPCP of Ecotricity Group Limited also provided a supervisory role in the project and review of the manuscript before submission for publication.

Competing Interests Statement

This study was part of a PhD funded by the National Environment Research Council (NERC) (NE/K007610/1). As part of the PhD funding, £3000 was provided towards stipend costs for LRVG as a CASE contribution by the commercial funder Ecotricity Group Limited (www.ecotricity.co.uk). SPCP of Ecotricity Group Limited also provided a supervisory role in the project and review of the manuscript before submission for publication. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Rebuttal letter for re-submission to PLoS ONE

Manuscript reference: PONE-D-19-23958

Manuscript title: Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts

General response to Reviewer #1:

R#1:

“This manuscript is very well written and describes a straightforward set of experiments testing the effects of broadband noise and radar on localized bat activity. There are only a few previous studies on the topic, and none were nearly as rigorous and thorough as this one. The experiments provide what I consider to be the best evidence so far that broadband noise can be used to deter bats from using or entering an area. The study also does a good job of challenging the hypothesis that radar can be an effective deterrent, which was dubious from the start but very difficult to test. The large sample size and the rigorous comparison of the differences in results obtained with audio and video also makes this paper very strong. Thus, I think this paper will become highly cited in the field and a cornerstone of future efforts.”

Response:

- We thank R#1 for such positive comments about our manuscript and experimental design. We believe that they have understood the rationale for the study and the need to test and compare the two bat deterrence methods.

- We also thank R#1 for drawing attention to our “rigorous comparison” of results from both video and acoustic data, which stands our study out from the small number previously done.

Line-by-line response to R#1 comments:

I only have a few suggestions and comments.

1) The manuscript provides compelling evidence of species differences in the response to the ultrasonic deterrent. This species effect is worthy of being mentioned in the abstract even if the underlying reasons are not yet clear, because this should be a point of emphasis for future studies.

- We agree that it is important to include the differing results in terms of species and have therefore added in a more detailed explanation of the results in the abstract, including a line pointing out the differences between the species. L23-29.

- These comments are also in line with some of the comments from R#2. We accept that we may have not been clear with the overall message and outcome of the results regarding the NIR video data and how the acoustics back this up. We have therefore made this clearer in the abstract and included the key results from models and % reduction figures. We believe this makes the message clearer and allows the reader to get a more detail understanding of the main results with regards to the overall trend (NIR video data) and species information (acoustic data).

- In response to R#2’s comment regarding L196-197, we also reanalysed the data and carried out Tukey contrast tests for Pipistrellus pygmaeus pass count data. Although there was no significant effect of deterrent treatment overall on P. pygmaeus, there was a significant effect of ultrasound when compared to radar for this species. Therefore, we have updated the results and abstract accordingly and stated that we see a deterrent effect of ultrasound on both Pipistrellus species, but not Myotis species.

2) I would recommend including the supplementary figure S1 in the main text, and I suggest adding either representative spectrograms or power spectra of the bat pulse emissions to illustrate the extent to which the stimulus overlapped with the main bat species being studied. Alternatively, in the methods section after line 91, it would be helpful to provide the reader with a brief description of the pulse acoustic properties in relation to the stimulus acoustic properties. The extent of overlap between the bandwidth of the noise and the pulses may be important for predicting species differences in the response.

- In line with R#2’s comments we have created a new figure including a spectrogram of the three species’ echolocation calls incorporated into what was Figure S1. This new figure should allow comparison of species’ calls with the acoustic deterrent output and illustrate the extent of overlapping frequencies, as suggested.

- We also make a point of explaining that the deterrent’s output overlaps with the species’ echolocation calls in the text (L167-170). We have also given the frequency of most energy for each species/species group in the text to draw the reader’s attention to how the “stimulus acoustic properties” relate to the bat species’ echolocation call properties.

3) Line 91: for completeness, do you have information about the beam projection angle? The radar beam angle was provided on line 86, and it was discussed that the narrow beam angle may be the reason radar was ineffective. However, the ultrasonic beam angle is needed for comparison.

- We have included the beam angle for the speaker unit transducers (L167).

4) Introduction, and Line 63-64. An important motivation for deterring bats from buildings that is not mentioned in the introduction/discussion is that bat colonies pose health hazards, particularly when they invade schools or other public buildings. The US Center for Disease Control (CDC) guidelines for dealing with bats explicitly states that ultrasonic deterrents are ineffective (https://www.cdc.gov/niosh/docs/2005-109/pdfs/2005-109.pdf ), citing Tuttle, 1988. This topic might be something worth addressing in the manuscript.

- We thank R#1 for drawing our attention to the US CDC guidelines and also to the potential wider application for bat deterrence in buildings in general; where bat roost (i.e. not just in churches, which we had already referred to).

- In response to these comments by R#1 and some comments by R#2 regarding the specific applications for bat deterrence, we have made changes to the abstract, introduction and discussion. We have introduced the context of bats in historic buildings and also when bats roost in other buildings such as workplaces, schools etc. We have also included a reference to the health risks to people in buildings where bats roost.

- We have also included a recommendation to update the US CDC guidelines for dealing with bats that roost in buildings, so that they include acoustic deterrence as a potential method for exclusion (L374-378).

General response to Referee #2:

Reviewer #2:

Manuscript Number: PONE-D-19-23958

Manuscript Title: Deterrence as a mitigation measure to reduce conflict between bats and humans

This study aimed at testing two acoustic measures to deter bats from their foraging sites: ultrasonic sound and radar, alone and in combination. While acoustics play an important role in the lives of bats, the rationale for doing this study somewhat missed me. As the authors indicate, there already exists evidence of bats being deterred from wind turbines (and churches). Thus this study only corroborated this without adding more knowledge, e.g. regarding why bats are deterred. I also have some concerns regarding the framing of the manuscript. They focus is on deterrence in general, while the literature cited mainly is from wind turbine deterrence. While deterrence may be an option for mitigation, when other measures (e.g. avoid, minimize) have been tried I fail to see how it can be employed in the general sense. The authors mention, besides wind turbines, also deterring bats from roads and foraging sites. However, both would have detrimental effects to bat populations; the latter depriving them from their food sources and the first creating barrier effects. I guess this was unattended by the authors, but the framing of using acoustics indiscriminately does neither help bats nor humans in my eyes.

Response:

The comments from R#2 are thorough and helpful, although we believe that they may have misunderstood our rationale and intentions with regards to the study. We acknowledge that the manuscript was over concise and may have therefore seemed to generalise our results to applications that do not seem relevant. However, we believe that having elaborated on the rationale and application scenarios, we have alleviated many of the issues raised in the review. Most of the comments have been easily remedied with additional information, which we have provided in response to the line-by-line comments below.

However, we do not accept that this study simply corroborates previous studies. It is the first study to directly compare two methods for deterrence in bats and also to do so in the European context at foraging sites. Previous acoustic deterrence research has been carried out at wind turbines in North America and in roosts in historic buildings in the UK, which both represent different contexts and species. Radar has been tested as a deterrent in foraging sites in the UK but has not been compared directly to other types of deterrence. As stated by R#1, the findings of the studies examining radar as a deterrent carried out at UK bat foraging sites are considered controversial. Our study therefore aimed to replicate the studies testing radar as a potential deterrent and also compare the methods with acoustic deterrence in the same context. Our results do not corroborate the findings of those previous studies testing radar at foraging sites and therefore we believe our findings are novel and important, as explained by R#1. R#2 also seems to misunderstand that we are testing acoustic methods and a form of electromagnetic radiation, which is not acoustic. While the suggested mechanism for radar’s effect on animals may have some acoustic component, this has not been tested. Therefore, it is not clear why R#2 is placing so much emphasis on our study being solely about acoustics, when radar is also not explicitly regarded as an acoustic method of deterrence.

Regarding R#2’s comments on the framing of the manuscript, we accept that the Introduction does not elaborate enough on the potential applications of deterrence and focusses only on the wind farm scenario. Therefore, we have ameliorated this by including a more detailed introduction to acoustic deterrence applications (L52-71). We have also added more information on how these methods could be used in the discussion, as well as welfare implications and suggestions for future research (L368-410). For example, R#2 also had misgivings about the use of deterrence in the context of roads and other areas where bats forage, but where they may be at risk from human activities. We have therefore updated the manuscript with a caveat that acoustic deterrence be used on a case-by-case basis and discuss some of the potential impacts of using deterrence. We also discuss that deterrence may be an important tool in conserving bat populations in areas where they are at risk of impacts or indeed mortality (such as at wind turbines or roads) and that there may be a trade-off with the associated impacts of the acoustic deterrence.

In the line-by-line comments, there are a number of points where R#2 picks up on issues with our use of the phrase ‘human-wildlife conflict’ or similar. We acknowledge that our use of the phrase was somewhat confusing and although many papers in the field still use it, we have made substantial changes to the manuscript removing it. Instead, we have included an introduction to the alternative phrases ‘human-wildlife impacts’ and ‘conservation conflicts’, in line with suggestions in the literature. We have also changed the title to include these phrases. We believe the manuscript now provides a clear introduction to these phrases before using them in relation to bat deterrence methods and applications. We thank R#2 for picking up on this as it has allowed us to be more accurate in describing how our work fits in the wider fields of human wildlife impacts and conservation conflicts.

Line-by-line response to R#2:

Below follow more specific comments:

L11: “impacts of threats” – what is this, did the authors mean “risk of impact”?

- We have reworded this to make the sentence clearer, to “impacts of human structures or activities on wildlife” L12-13

L12: “sensitive areas such as protected artifacts” is somewhat unclear to me: sensitive to whom, bats of humans? Why not just say historic buildings or human structures?

- We agree that this was an unclear phrase and was alluding to historic artefacts in churches and protecting these from urine and faeces.

- We have reworded the whole sentence to make the point clearer and to incorporate all human built structures and activities and buildings where bats may be regarded as a nuisance or health hazard. We have also made these changes after the advice from R#1 (point 4), who suggested we mention public buildings more generally and not just historic buildings such as churches. L12-14

L12-13: specify where you deterred bats from, i.e. their riparian foraging sites.

- We have updated this sentence to make it clear that we are testing two methods that have shown potential in the literature for deterring bats in a number of scenarios, including where bats may forage (i.e. around roads, wind turbines) or roost (in buildings, bridges). L15

L16: Pp echolocation call activity was reduced by ~40-80% not 70-80%! Only the combination of ultrasound + radar was significant. This needs to be clarified. Include also the non-significant effects on Myotis and P pygmeus.

- We have updated the abstract to include all results for the different species and have altered the % reduction for P. pipistrellus to ~40-80%.

- We quoted the 70-80% reduction initially as this was the range of % reduction seen in the ultrasound and radar (U+R) treatment as compared to the control and radar only. However, we understand this may have been misleading.

- All species’ % reductions have been updated in the same way, giving the whole range of all ultrasound treatments (U and U+R) as compared to both control and radar only treatments. L23-25

L17-19: Why would you suggest that only ultrasound should be used as deterrent, when in some of the cases only the combination significantly reduced bat activity?!

- The results from the near infrared video footage show a clear effect of both ultrasound treatments, but no effect of radar.

- It is also clear from Fig 3 that for both the Pipistrellus species and feeding buzzes, the trend is a reduction in activity in both ultrasound treatments and in all cases the radar treatment has a higher mean number of bat passes.

- We would therefore deduce that it is the ultrasound that is having an effect and radar is not.

- The species information is a little less clear, probably due to a smaller sample size, unavoidable due to the masking effect of the deterrent making it impossible to identify bat passes at some sites for the acoustic data.

- However, we do see a significant effect of ultrasound only treatment in post-hoc tests (in the case of feeding buzzes, when compared to both radar and control treatments, and P. pygmaeus, when compared to radar) and also in combination with radar in P. pipistrellus (when compared to both control and radar).

- But we do not see an effect of radar on its own in any of the tests. Indeed, bat activity in ultrasound and radar treatments is significantly reduced when compared to radar and radar is therefore unlikely to be having an effect on bat activity.

- We have added a sentence to the abstract making the lack of an effect of radar in either video or acoustic data clearer L19-20

L22: I find the wording of “parties” somewhat misleading: are bats a party (politically, socially or other) in this? What do you mean by “impact”; mortality of individuals, loss of habitat or population reductions?

- We have reworded this, taking out the word “parties” as suggested by R#2.

- We have also added in examples of impacts so this statement is more clear. L34-35

L23: I guess that in 99% of the time it is wildlife that is impacted by humans and not vice versa. This, either by taking into use species’ habitats, or killing them when they cause nuisance.

- We agree with this point and have updated the sentence to reflect this (please see the previous point).

L25-26: maybe better to say that we are mainly talking about human-human conflicts here?!

- We agree that the phrase ‘human-wildlife conflict’ (HWC) is a misleading one and we have therefore changed the manuscript to include the alternative terms ‘human-wildlife impacts’ and ‘conservation conflicts’ (terms suggested by Redpath et al. 2015 references [2-3]).

- We have reworded the title to include these terms instead of HWC, as well as the rest of the manuscript (abstract, introduction and discussion)

- We have also included an explanation of why the phrase HWC is misleading in lines… of the introduction and introduce the alternative phrases of ‘human-wildlife impacts’ and ‘conservation conflicts’. L36-40

L28: I would suggest using “human structures and activities” (omitting “-built”) as then “human” links to both structures and activities; now it doesn’t.

- We have done as R#2 suggests and removed “-built” from this line and also in all places we have used it in the manuscript.

L31: “…where they may come to harm” or cause harm to human structures and activities (i.e., avoiding conflict).

- We have reworded this section so that it includes the human element, which is suggested in the phrase above by R#2. L44-46

L33-34: Be clearer why bats would need to be deterred. All references are from wind turbines apart from one; would it not be more realistic to either extend the scope of structures/activities or set specific focus on wind energy?

- The reason the references are mainly from wind turbines is that there has not been that much published on bat deterrence in any other contexts to date.

- Although we can not add in more references for different applications, we have included more explicit reference to the other potential applications and scenarios where bat deterrence could be used. L47-71.

L34-35: “…bats are already…” already vulnerable relative to what? One example given (habitat loss) is mainly human-caused; isn’t that part of the human-wildlife conflict? Or do you see HWC mainly as bats causing nuisance for humans?

- We have removed the phrase “bats are already” and any mention of human-wildlife conflict (please see L25-26 response).

- We have now rephrased these lines explaining the threats generally to bats, irrespective of the human context. L50-52

- This is part of a general re-wording of the whole section, where we have added in more detail and removed any reference to human-wildlife conflict and instead referring to ‘human-wildlife impacts’ and/or ‘conservation conflicts’.

L39-42: In this example I fail to clearly see the stakeholder conflict. What is this conflict centered on?

- We have removed this example as it does not clearly explain the message we are trying to convey and have replaced it with some background about the impact of wind turbines on bats in the US and European context. L53-59

L42-43: Maybe indicate how bats may be affected by roads. Also I fail to see the link to deterrence here.

- As suggested, we have added in some examples of impacts of roads on bat populations (habitat loss, noise pollution and mortality due to collision).

- In this section we are introducing potential applications for deterrence, where bats are at risk from human structures and/or activities.

- We have added in two sentences, firstly after the wind turbine application introduction and secondly after the section on roads/transport infrastructure. We explain in these sentences how deterrence might be used to reduce impacts on bats, or more specifically to reduce direct mortality due to collision with either turbine blades or vehicles. L58-64

L47: Before going into reducing impacts, may clarify that in all cases the mitigation hierarchy should be the leading line (avoid, minimize, reduce, compensate, restore). Also, clarify when deterrence may be implemented: in itself it may enhance functional habitat loss and barrier effects for bats, so maybe not preferred over other more benign measures?! The references that are supposed to cover light, sound and radar seem to miss those relating to light (e.g. [23,24]), and what about [12]?

- We agree that bat conservation should be the focus of any mitigation measure that aims to reduce impacts of human structures/activities on bats.

- We welcome the suggestion to include reference to the mitigation hierarchy and have added in a paragraph that relates to bats. L72-80

- We have also added in an example of possible unwanted side effects of deterrents on target and non-target animals, as suggested by R#2.

- Our aim is to make sure the reader fully understands where bat deterrence is a viable method for reducing human impacts on bats and conservation conflicts involving bats. But we do not wish to advocate its widespread use for any bat related issue. We therefore welcome R#2’s comments and believe that they enhance and clarify our message.

L52: I would suggest moving this sentence after L52-55.

- We have done as R#2 suggests and moved the sentence explaining the studies on the effect of radar on bats after the sentence about the suggested mechanism for deterrence. L101-107

- We have also added more detail about the two Scottish studies involving radar, to allow more accurate and informed comparison of our study in the discussion.

L57: Bats avoid insect noise? If this was actually meant, please include references (also for turbulent water).

- Bats did indeed avoid areas where high frequency insect noise was broadcast in a study on Brazilian free-tailed bats in the USA. However, we have added in the missing reference Gillam et al. 2007 (reference number [44]) and thank R#2 for picking this up. L109-111

- The reference relating to turbulent water was already included as reference, Mackey & Barclay, 1989 [45], but we have inserted it along with reference [44] after the first mention and included the references relating to anthropogenic noise pollution [46-49] at the end of the sentence, for increased clarity.

L58-60: All these references relate to anthropogenic noise? Still the statement is generic, and should therefore also include natural causes of noise.

- We have included reference [44] and [45] which relate to insect noise and noise from turbulent water. L111-113

L61: What is the difference between communication and eavesdropping exactly? Is eavesdropping not a specific form of communication? Also, I would suggest explaining what eavesdropping is for the non-expert.

- We have reworded the reference to eavesdropping to explain its difference to communication and why it may be beneficial to a bat. Bats tend to ‘eavesdrop’ on the echolocation calls of other bats, which are produced when bats are foraging or orientating in their environment. Eavesdropping is therefore a passive form of listening in, rather than active communication. L113-116

L66: Why was light not also included? While it is mentioned above, this is not included. Explain why the focus lies on acoustics.

- The focus of this study is on acoustics and radar, not just acoustics, which are differing methods that have shown potential as deterrents for bats. Radar is a type of electromagnetic radiation, which differs from sound waves.

- The mechanism for the effect of radar (if there is one) is unknown. It is suggested by the authors of the Scottish radar studies [18-19] that there may be an acoustic component, in that the brain of bats may vibrate, producing a noise, which causes the deterrent effect, but this has not been tested. We therefore regard the two methods as separate.

- Light was not included due to its potentially serious detrimental effects on roosting and foraging bats.

- We realise that we did not introduce light deterrents in enough detail, which has been picked up by R#2. Therefore, we have added in an explanation of why they were left out of the study and have included a section detailing the effect of light deterrents and light in general on bats and given examples of why light deterrents should, in our opinion, not be used. L81-100.

L65: Can you give examples where bats actually cause conflict? Where would deterrence be needed, contrary to other mitigation measures?

- We have reworded this sentence in line with the manuscript-wide changes to remove the phrase ‘human-wildlife conflict’, please see response to point about L25-26. We have instead referred to ‘impacts’ and ‘conservation conflicts’. L124-126.

L77: Isn’t this called “time blocks” in the models? Please clarify.

- We have clarified by changing “treatment blocks” to “ treatment time blocks”. L140-141.

L78: Did the experiments last (spelling mistake here) 1 hour or 55 minutes? (4x 10 min + 3x 5 min in-between = 55 minutes)

- The experiments lasted for one hour and each treatment time block was followed by a 5-min recovery period.

- We have updated the sentence to reflect this. L140-141.

L80: Was this alternation only done spatially or also temporarily?

- This alternation was only done temporally following a temporal Latin square design, initially deployed over 16 sites, although due to equipment failure at two sites, we could only use 14 in analysis.

- However, generalized linear mixed effect models allow for unbalanced design.

- Please see response to point about line L133-143 below for a more detailed explanation of the experimental design and changes we have made to the manuscript for increased clarity with regards to statistics performed.

- The topography of the riparian sites and the way in which bats used them prevented us from following a spatial design. Bats occupied areas nearer bridges present at the site earlier on, when light levels were high and flew more over the water away from the bridges as light levels decreased over the experiment hour. Therefore, deploying the deterrents in different areas spatially within the site was not technically feasible and would have reduced our ability to record an effect of either deterrent method.

L84: 0.3 milli sec (ms) or 0.3 micro sec (μs)?

- We have changed it the mistake to 0.3 μs. L158-159.

L87-89: how directional were the speakers exactly? Was their sound emission measured? Could it also be that the narrow horizontal radar beam caused non-significant effects in this measure contrary to the ultrasound? What would the results be if the radar was tilted 90 degrees giving a narrow vertical beam but wide horizontal beam? Also, I would suggest inclusion of a picture presenting the exact practical layout of the design spatially.

- The point about the speakers’ beam projection angle was also picked up by R#1 point 3.

- We have included the beam projection angle of 15° at -6 dB, provided by Senscomp specification from www.Senscomp.com in L167.

- The aim of our experiment was to compare radar and acoustic methods in a similar way as had been done in previous studies. We wanted to replicate the methods and equipment used in the Scottish radar study in order to hopefully corroborate their findings, however we did not find an effect of radar. We followed Nicholls & Racey’s methodology and deployed a similar marine radar unit, using the same specifications, in a similar way at riparian foraging sites. As they were able to find an effect of radar on bat activity in their study, this seemed an effective way to compare it to acoustic methods.

- It is possible that the narrow horizontal radar beam caused non-significant effects in our study, but as it was very similar equipment and methodology as used in the Scottish radar study, it is unclear why we did not find the same result.

- We have calculated the area of treated airspace from the beam angles for both the radar and speaker units, to enable more accurate comparison of the deterrent propagation in the environment. We have included this as part of our Discussion. L317-329

- We have created a schematic of the experiment set-up and included it in the methods section, as well as referring to it in the discussion. L152, L326

L90: What was the peak power of the speakers?

- We do not have information on the peak power of the speaker units/transducers, but have provided information of the source dB level at 1 m and at 20 m, for the 50 kHz (the frequency of maximum energy). L162-167

- In response to R#1’s comments we have also included Fig S1 in the main text, including a spectrogram and a power spectrum of the deterrent output, as well as spectrograms of relevant bat species echolocation calls. L170

L97: 20m from the radar or speakers or camera? Unclear.

- The SM2 bat detector was placed at ~20 m from the cameras, which were at 0 m of the treatment zone, in line with the camera. We have updated this sentence to include a reference to the camera. L155

- We have included a schematic detailing where all the equipment was placed and set-up at a site, which we refer to in the methods and also the discussion. L152, L326

L114: “in” instead of “during”?

- Changed L206

L115-117: I don’t understand, the results speak of 6 sites being included in the analyses, here it states that all were included after having added deterrent noise. Which is it?

- Only recordings from six sites were included in analysis as bat calls were completely masked by deterrent noise in all other sites.

- We have added “files recorded at six sites” to the second sentence, to make it clear that ultrasound was added to only those remaining six sites i.e. those that were not completely masked by ultrasound. L205-210

L118-132: I would move this section after the next “Variables and model specification”.

- We agree, it makes more sense to move this section and have done as R#2 suggests. L211-226

In addition, it seems you have used both a information theoretic AND frequentist approach in the statistical model/term selection. This is somewhat confusing, I would urge you to choose one of the two.

- We acknowledge that our approach to modelling and presentation of model selection statistics was confusing. Our method for model selection was a frequentist approach using likelihood ratio tests (LRTs), including p values obtained from comparing models containing a term with one with that term removed. We also obtained AICc values and pseudo R squared values to compare the models, which are generally more used in the information theoretic (IT) approach.

- Therefore, as suggested by R#1 we have now focussed on the frequentist approach only and have made the following changes to the manuscript:

- We have removed the model selection statistics tables presented in Table S2 and focussed on the frequentist approach only (as AICc values are usually used in the information theoretic approach rather than the frequentist approach)

- We have re-run the models using only the frequentist approach and checked the statistics against the tables originally submitted.

- Re-running the models produced no change to the statistics from those originally presented.

- However, there was a mistake in the original manuscript regarding the GLMM distribution, which was Poisson, rather than negative binomial. L227-239.

L126: “restricted model” instead of “nested model”?

- We have changed “nested model” to “restricted model” as R#2 suggests, as the latter is a clearer phrase describing a model with a term removed. L234

L127: How were the final model validated exactly? I do not find any information on this in the results.

- We validated models using the R package DHARMa, which uses simulation of the data to produce simulated residual plots and tests for overdispersion, zero inflation and heteroscedasticity. Use of this package for validation is becoming more widespread, as it allows simulation of the data and validation of Poisson and negative binomial count data, which are often difficult to validate using normal residual plots. See https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html for more information.

- We have updated the methods to make the method of validation clearer. L237-239

- We have included a sentence the both the NIR video and acoustic data results sections explaining that final models did not show overdispersion, zero-inflation or heteroscedasticity when tested with the R package DHARMa and we have included the reference again. We have also included which models were chosen as the final models in the results section. L250-252, L284-285.

L130-132: I do not follow this sentence.

- We have reworded the statistical analysis section and removed this sentence as it was confusing. The explanation of our methods is now clearer and explains how LRT statistics were obtained. L227-239.

L133-143: What was the generic design of the study, did it follow a Control-Impact design?

If so, maybe it is more illustrative to only show the full models to be able to see the effects or non-effects of the treatment?!

Unless you wish to better understand in what circumstances deterrence worked well (or not); such as temperature or wind speed. I was somewhat baffled to notice that wind speed, which clearly affects both bat activity and sound emission and ambient noise, was not included in the models. Was ambient background noise measures at all?

- We followed a temporal Latin square design, alternating treatment order (four treatments) over 16 sites. However, we had an equipment failure which meant we couldn’t use two of the sites in the analysis. We therefore used GLMMs which control for unbalanced designs and also included time block as a fixed effect in the models.

- These methods follow a within-subject or repeated measures design, where each treatment is tested within one subject, or in our case each site. We chose to use these methods as they allow analysis of effects on bat activity, which can vary significantly between sites and on different nights. Therefore, testing all four treatments within one night, but alternating those treatments on different nights was, in our minds, the best way to test these deterrent methods on bats.

- It is normal practice to present effect sizes for final models rather than full models and also LRT statistics for terms/fixed effects included in those models, when using backwards stepwise model selection methods.

- We did not measure ambient background noise, as any differences between sites were controlled for using the within-site design. Our aim was simply to test the different deterrent methods at sites where bat activity was high enough to record differences (i.e. which is why we chose riparian sites). Recording ambient noise would therefore not have added to our results or conclusions in this instance.

- We did not include wind speed or rainfall in the models and did not measure these variables during experiments as we purposely chose nights where there was no rainfall and wind speeds were below 10 m/s. Wind speed and rainfall can significantly reduce bat activity. Carrying out experiments in higher wind speeds would have resulted in reduced numbers of bat passes being recorded, making it more difficult to see a difference in the effects of the treatments. Therefore, in order to get meaningful results and test these deterrents effectively on bats, we needed to ensure sufficient bat activity as baseline at chosen sites. This is not to say that these environmental variables are not important to consider in deterrent application. Future studies should indeed include an investigation into the effects of weather variables and other factors such as site topography on the spread of high frequency sound in the environment.

- We have therefore updated the methods in light of R#2’s comments, explaining our study design in more detail and making both the experimental design and statistics methods clearer. L143-149

- We have also added in our rationale behind not including wind speed and rainfall in our study design. L172-173

L153: maybe clarify that this is the mean number of bat passes and give the unit (i.e. per day, per experiment, per hour, per 10-minute interval, per minute?).

- The mean and SD we give was calculated as a mean per site (for 14 sites) and we have updated the results to reflect this as suggested. L249-250

- We have done the same for the acoustic bat passes results section. L280

L156: “per time unit” – what is the time unit used? Be clear.

- We agree this phrase is confusing and have removed it from the sentence, instead referring to ultrasound treatment blocks. L286-287

L166 (table): What is the difference between the fixed effect “Time block” and the random effect “Block”? Why was an interaction between deterrent and temperature included? Should also an interaction between deterrent and time block be considered?

- There is no difference between the fixed or random effect time block, they are the same variable. We have updated the Table to reflect this, with the same name fixed and random effect variable. L265-268

- We included an interaction between temperature and treatment as the propagation of sound and EM waves can be affected by the temperature of the air the waves are travelling through. This might therefore affect how bats respond to the deterrent.

- We did originally include an interaction between deterrent treatment and time block in the NIR video models and this was non-significant, so we have included it in the table.

- However, due to low sample sizes, acoustic models that included an interaction between deterrent treatment and time block were rank deficient (i.e. not enough data to use a more complex model). Therefore, specifying a more complex model (i.e. with an interaction term) was more likely to cause inaccurate results. We therefore included the simpler models in analyses to avoid spurious results.

- We have therefore updated the reasoning for inclusion (or not) of the two interaction terms in lines and also included the interaction term results in Table 1 for the NIR video response variable. L212-226

L181-185: No results are given regarding which of the models were most parsimonious (Table S2). This table clearly indicates that the most parsimonious model (the one with lowest AIC, whereby usually ΔAIC<2 are seen as being equally good) would be the null model and not the deterrent treatment model?! This would mean that none of the echolocation models rendered any significant outcomes.

- Please see response to point made on L118-132 regarding approach to modelling.

- We re-ran the models and found there was a mistake in Table S2 due to a comparison being made between a negative binomial model and the full model, rather than a Poisson model.

- However, we have removed Table S2 as AIC values were associated with an information theoretic approach to modelling and we have now focussed on a frequentist approach.

- We have included information on which models were the most parsimonious (and therefore chosen as the final models) for all response variables in the Results section and which also explained which effects were significant and which were non-significant. L252-254, L285-287

L196-197: Were related Tukey tests also non-significant?

- We have re-run the Tukey tests for the P. pygmaeus data and included the results in the manuscript. L299-303

- We have also updated the discussion and abstract to reflect this result.

L203-204: What were the results for all bat species pooled regarding acoustic passes? This would enable a direct comparison to the visual video-footage.

- We did not run models for all species’ acoustic data pooled as we did not think this would add anything more to the results and conclusions.

- Species’ responses to the deterrent were different and therefore pooling all species and running models would likely give an outcome skewed towards one particular species and does not give us any more accurate information than looking at species individually.

- We also do not believe the pooled acoustic data would be comparable to the video data, as it was recorded at 20 m from the camera/deterrent set up, covering a range of ~30 m in all directions, to certain degrees depending on the species. Therefore, the data includes a lot of noise and is not necessarily representative of the treatment area filmed on the cameras.

- We included the species acoustic information in the manuscript to mainly get an idea of the species present during experiments that may have been deterred in the video data.

- It is very difficult to record accurate species data that is equivalent to video without placing the bat detectors in the same place as the video cameras, or indeed closer to the cameras than we did, which was not possible due to the masking effect of the deterrent sound on bat echolocation call data. Indeed, we could only use 6 out of 14 of the sites that acoustic data were recorded for, due to this problem of masking.

- Despite this, we did find differences in species responses to the acoustic deterrent.

L205 & L214: This is not a chapter I mam afraid…

- Changed “chapter” to “study” L314

L215-216: Tja, although done at a new site, this study merely corroborates earlier finding. What new insights have been obtained?

- We do not accept that our study is merely corroborating earlier findings on bat responses to ultrasound. Please see the response to the general comments made by R#2 on this matter at the beginning of the review response.

L222: Discuss why the combination of ultrasound and radar led to a better result.

- We do not believe that the combination of ultrasound and radar led to a ‘better’ result, it is more likely an artefact of a smaller sample size and noise introduced into the data by the range of SM2 bat detector microphone.

- Please see more detailed response this point in response to comment about line L17-19

- We have added in a point about the overall trend of reduced bat activity during ultrasound treatments seen in Fig 3. L339-340

- We have updated the Tukey results for P. pygmaeus and added a comment on this in the discussion. P. pygmaeus activity was reduced during ultrasound only treatments when compared to radar, but there was no effect on combined treatments. L340-344

L228-230: Why? The radar beam has a wide vertical beam which should be expected to cover both the water surface and the airspace above (unless it was placed too close to the foraging site). I have not seen any information regarding the directionality of the speakers (horizontally and vertically). Is there also any specifics of the riparian sites regarding habitat (e.g. treed vegetation, topography) that may have affected the results?

- We are referring here to the directionality of the acoustic deterrent system not the radar, however we agree with the point generally that the acoustic deterrent beam would be expected to cover the surface of the water and have taken this sentence out.

- It is more likely that as Myotis bats feed over the water, they are more likely to have been deterred away along the river closer to the bat detector during deterrent treatments, compared to the Pipistrellus species which feed higher above the water.

L230: the bats “may have been moved”? By whom? Maybe rephrase.

- We have rephrased this to “may have moved”. L357

L239: Are there clear difference in hearing between these species that might explain their responses (or lack thereof)?

- Hearing sensitivity and thresholds in bats are largely understudied but could play a part in different responses of bat species to acoustic deterrent sounds.

- There also may be some differences in the mechanism underpinning deterrence and how the species feed over water, which may explain why an effect of acoustic deterrence was not seen in Myotis species.

- We have updated the discussion to include reference to bat hearing thresholds and the potential mechanisms for acoustic deterrence. L348-353

L240-241: Why would anyone wish to exclude bats from their foraging sites, especially riparian areas? What may be expected to be built there (not likely to be wind turbines or churches)? What human activities will conflict with bat presence?

- The premise of this study was to examine bat responses to acoustic and radar deterrents as proof-of-concept for their use in other applications.

- The reason we chose riparian foraging sites, was due to the high bat activity at these sites, which enabled us to detect an effect of the deterrent methods more easily.

- We acknowledge that the phrasing of this sentence seems centred around foraging sites. Therefore, we have removed the reference to foraging sites in order to make the sentence more general. L367

- We have also re-written the discussion, to include specific examples where acoustic deterrence may have application. We appreciate that as it was, the discussion seemed to suggest that deterrence was just intended to remove bats from foraging sites and this was no our aim. Therefore, we have added specific examples relating to wind farms, roads/train lines and buildings, where deterrence may be useful. L368-387

L244-246: Are you really suggesting to deter bats from roads, increasing barrier effects roads already pose even more? I fail to see how this may help conserve bat species. Reference [22] suggests underpasses instead. Although roads may affect bats through noise, your study fails to give any indication how bats are affected by ambient noise.

- Current mitigation for roads is deemed currently insufficient (see Altringham & Kerth 2016 [28]). Therefore, acoustic deterrence has potential in being used alongside current structures such as green bridges and overpasses, in order to divert bat flight lines over these structures or other safer alternative routes over roads.

- We have updated the discussion and introduction to include a more detailed explanation of the transport infrastructure application. L379-387

- Acoustic deterrence also has potential for use in reducing impacts of train lines on bats and we have included a reference to a blog detailing some work we did in collaboration with industry partners, Wevill et al. 2019 [70]. L382-384

- We have also updated the discussion with a section on welfare implications, including the effects of ambient and anthropogenic noise on bats. L388-401

L246: What other human structure and activities, other than wind turbines and roads, are you thinking of here?

- We have taken this sentence out and instead focussed on specific examples of applications (please see responses to two previous points).

L247-248: What “specific scenarios” are you thinking of here? Different spatial planning and development scenarios? Scenarios of locating different structures or activities and their expected effect? It is unclear to me what is meant here.

- We have removed this phrase and included specific applications for deterrence more generally (please see previous points on roads etc).

L249: The distance over which speakers or radar have an effect in deterring bats should preferentially have been part of this study.

- The Scottish radar study [19] found a deterrent effect of radar over 30 m. We replicated their methodology and failed to find an effect of radar over these distances.

- We believe that investigating the effect of the acoustic deterrents is out of the remit of this study, which had the main aim of comparing two bat deterrent methods that have shown promise in the literature, but that have not been compared at foraging sites in the UK or Europe.

- We have carried out experiments examining the response of bats to the acoustic deterrent speakers over different distances and are currently preparing a separate manuscript including these results.

L249-250: This comes back to my earlier question whether the different results might have been caused by differences in hearing among species? The same rationale would also matter for radar (e.g. different emission bands)? Please add references to indicate to which extent this would be possible.

- We have included a discussion about bat hearing thresholds in relation to differing species response to deterrence. Please see response to point about L239.

- We have not discussed hearing in relation to radar as we did not find an effect of radar and would therefore not seem relevant to the discussion.

- We have however, included a reference to bat hearing in the recommendations for future work. L409-414

L251.255: This is in fact the first time you indicate that possible deterrence may not be the first and foremost preferred measure to implement. PI think this point should be raised already in the introduction, together with an indication when it might be best to implement (and when not). Now the manuscript seems to say that acoustic deterrence will work ate wind turbines, churches, roads, foraging sites, etc. Also, something that may be discussed is how practical the implementation of acoustic deterrence is: can it really be implemented along (long stretches of) roads?

- We have included in both the introduction and discussion reference to the mitigation hierarchy in response to the point raised. L75, L406

- We have also made sure we are clear in explaining that deterrence should be considered once all other more benign or less invasive alternatives have been exhausted. L402-414

- We have included a more detailed and explicit discussion of the relevant applications of deterrents, being careful to point out that they should only be used on a case-by-case basis. We have also updated the introduction, so that we introduce potential scenarios where deterrence might be applicable.

- We have also included a section on welfare implications and finish on a warning that deterrents should not be rolled out for use anywhere a bat is regarded a ‘nuisance’.

- We are not suggesting that deterrence be implemented along long stretches of roads, but rather at key points to divert key bat flight lines along safer routes and we have updated the discussion and introduction to reflect this. L379-387

- We have also explained that when deterrence is used it should be done so in an effective, safe, practical and targeted manner. L409-410

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Decision Letter 1

Michael Smotherman

22 Jan 2020

Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts

PONE-D-19-23958R1

Dear Dr. Gilmour,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

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Reviewers' comments:

Acceptance letter

Michael Smotherman

28 Jan 2020

PONE-D-19-23958R1

Comparing acoustic and radar deterrence methods as mitigation measures to reduce human-bat impacts and conservation conflicts

Dear Dr. Gilmour:

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on behalf of

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Table. Number of bat passes recorded on near infrared video during deterrent treatments and control.

    (DOCX)

    Click here for additional data file. (26KB, docx)
    S2 Table. Number of Pipistrellus pygmaeus passes recorded during deterrent treatments and control.

    (DOCX)

    Click here for additional data file. (21.5KB, docx)
    S3 Table. Number of Pipistrellus pipistrellus passes recorded during deterrent treatments and control.

    (DOCX)

    Click here for additional data file. (21.7KB, docx)
    S4 Table. Number of Myotis spp. passes recorded during deterrent treatments and control.

    (DOCX)

    Click here for additional data file. (21.5KB, docx)
    S5 Table. Number of feeding buzzes recorded during deterrent treatments and control.

    (DOCX)

    Click here for additional data file. (21.5KB, docx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    Click here for additional data file. (78.6KB, docx)

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.

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