High-frequency hearing sensitivity does not systematically imply aversion to ultrasounds in large terrestrial mammals

Anna Terrade, Loïc Prosnier, Colin Vion, Yann Locatelli, Nicolas Mathevon, David Reby

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Anna Terrade, Loïc Prosnier, Colin Vion, Yann Locatelli, Nicolas Mathevon, et al. High-frequency hearing sensitivity does not systematically imply aversion to ultrasounds in large terrestrial mammals. Bioacoustics, 2024, 33 (5), pp.448-459. 10.1080/09524622.2024.2377552. hal-04791162

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# High-frequency hearing sensitivity does not systematically imply aversion to ultrasounds in large terrestrial mammals

Anna Terrade¹,² ID, Loïc Prosnier¹ ID, Colin Vion³ ID, Yann Locatelli³† ID,
Nicolas Mathevon¹,⁴,⁵† ID & David Reby*¹,⁴† ID

1. ENES Bioacoustics Research Laboratory, CRNL, University of Saint Etienne, CNRS, Inserm, Saint-Etienne, France

2. Direction technologies innovation et projets groupe, SNCF, Saint-Denis, France

3. Réserve zoologique de la Haute-Touche, Museum National d'Histoire Naturelle, Obterre, France

4. Institut universitaire de France, 75231, Paris, France

5. Ecole Pratique des Hautes Etudes, Chart Lab, PSL University, Paris, France.

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This article has been peer-reviewed and published in
*Bioacoustics, 33(5): 448–559 (2024)*
https://doi.org/10.1080/09524622.2024.2377552

## RESEARCH ARTICLE

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Open Access

Open Data

Open Code

**Associate Editor:**

Peter McGregor

**Reviewers:**

Two anonymous reviewers

**Cite as:** Terrade A, L. Prosnier, C. Vion, Y. Locatelli, N. Mathevon, D. Reby (2024). High-frequency hearing sensitivity does not systematically imply aversion to ultrasounds in large terrestrial mammals. *Bioacoustics*

https://doi.org/10.1080/09524622.2024.2377552

## ABSTRACT

Crop damages and vehicle collisions caused by wild ungulates require effective deterrents. Many commercial acoustic devices use ultrasonic signals, presenting them as aversive to these animals. However, unconvincing results reported in previous studies using (non-frequency modulated) ultrasounds bring their effectiveness as deterrent signals into question. Here, we explored the deterrent effectiveness of ultrasounds in several large mammalian species that are expected to perceive these high frequencies. Specifically, we tested the effect of different ultrasonic signals on red deer, peccaries, and wolves. Animals were exposed to sequences of nine acoustic signals in the 20-30 kHz frequency range, and to a lower-pitched signal (2–3 kHz). While red deer showed no aversion to ultrasonic signals (inaudible for humans), lower frequency (audible for humans) modulations increased aversive responses. Conversely, peccaries showed strong flight responses to several ultrasonic signals. Wolves also reacted to ultrasounds but did not flee. Our study confirms that ultrasonic signals are not suitable for deterring European red deer. However, our results suggest that their effectiveness in other species should be systematically tested, without assuming that their hearing frequency range is a reliable predictor of their behavioural responses to ultrasonic signals.

**Keyword:** Wildlife – vehicle collisions, Acoustic deterrence, Ultrasounds, Red deer, Peccary, Wolf.

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<footnote>* Corresponding author: annaterrade.pro@gmail.com</footnote>

<footnote>† Joint senior authors</footnote>
Introduction

Populations of wild ungulates are becoming overabundant throughout the world because of large food availability provided by intensive agriculture and lack of predation, leading to conflicts with human activities (i.e., crop damages or wildlife-vehicle collisions) (Côté et al. 2004; Carpio, Apollonio, and Acevedo 2021; Valente et al. 2020; Iijima et al. 2023). Various damage mitigation techniques have been tried throughout the years, including fences (Rodrigues et al. 2017), olfactory (Kušta et al. 2015), visual [e.g., warning reflectors (Curtis 1995; Benten et al. 2018; Brieger et al. 2017)] or acoustic (Valitzski et al. 2009) deterrents. In particular, affordable ultrasonic devices have been promoted as being aversive for a wide range of species (Bomford and O’Brien 1990; Curtis 1995) while inaudible and thus convenient for humans. Yet, the efficacy of these devices remains debated and require scientific scrutiny.

A limited number of studies reports ungulate audiograms, including whitetail deer (Odocoileus virginianus) (Heffner and Heffner 2010; D'Angelo et al. 2007), reindeer (Rangifer tarandus) (Flydal et al. 2001) and domestic pigs (Heffner and Heffner 1990). They indicate that, while these species have a hearing range going up to 30 kHz for deer and 40 kHz for pigs, their optimal sensitivity lies around 8 kHz and decreases rapidly as frequencies enter the ultrasonic range (>20 kHz). In addition to this biological limitation, these high frequencies have poor propagation properties. Indeed, not only ultrasounds attenuate very rapidly as the distance from the source increases (Lawrence and Simmons 1982), but they are also highly dependent on environmental conditions (i.e., pressure, humidity, obstacles) (Bass, Sutherland, and Zuckerwar 1990). Furthermore, several reviews have shown that ultrasonic devices are ineffective at frightening pests, deterring deer from crossing highways, or reducing damages to crops or gardens (Bomford and O'Brien 1990; Koehler, Marsh, and Salmon 1990). The few existing studies, which all involved white-tailed deer (Odocoileus virginianus), either tested flat tones or signals from existing commercial devices without specifying their nature. They showed that neither the motion activated Yard Gard (Weitech, Inc., Sisters, Oregon, which emits 7-seconds signals of unspecified nature ranging from 20 to 28 kHz), nor the Usonic Sentry (Medlinc of Colorado, Grand Junction, which emits signals of unspecified nature ranging from 23 to 35 kHz), were effective for deterring animals from preferred feeding areas (Curtis 1995; Belant, Seamans, and Tyson 1998). Another study also demonstrated that the playback of flat tones (from 0.28 to 28 kHz and thus including ultrasonic frequencies) inspired by commercialised “deer whistles” did not alter the behaviour of white-tailed deer and was consequently ineffective for preventing collisions with vehicles (Valitzski et al. 2009). More recent deterrent devices such as the Doxmand© Normal device also includes sine-triangle modulated signals (ranging from 19 to 30 kHz), which are more similar to natural vocalisations and may thus be more effective at triggering reactions in target animals (Bomford and O'Brien 1990; Aubin 2008). Yet, to the best of our knowledge, the effectiveness of such deterrent systems has not been scientifically investigated.

Therefore, to plug this gap, we investigated whether detailed frequency-modulated ultrasonic signals (20 – 30 kHz) can be effective at deterring large terrestrial mammals. We conducted playback experiments on two ungulates species: red deer *Cervus elaphus*, which are often involved in vehicle collisions in mainland Europe, and peccary *Tayassu pecari*, native from Central and South America (and belong to the same suborder as European wild boars); as well as on a canid species: wolf, *Canis lupus*. As all three species may be able to perceive ultrasound signals falling within this frequency range (as predicted from audiograms performed in closely related species [whitetail deer (*Odocoileus virginianus*) (Heffner and Heffner 2010; D'Angelo et al. 2007); reindeer (*Rangifer tarandus*) (Flydal et al. 2001); domestic pigs (Heffner and Heffner 1990); domestic dogs (Heffner 1983); red fox (*Vulpes vulpes*) (Malkemper, Topinka, and Burda 2015)]), we predict that they will all at least display some reactions in response to the playback of ultrasonic acoustic signals. We also predict that deer and peccaries may be alarmed by these unusual artificial signals, while wolves, as predators, should be less reactive.
# Material and Methods

## Acoustic signals

To assess the deterrence efficiency of ultrasounds, we created nine 5-seconds ultrasonic acoustic signals (named S1 to S9, Figure 1A), containing frequencies between 20 and 30 kHz - within the hearing range determined by ungulate audiograms. We generated 3 flat tones (S3: 20 kHz, S4: 25 kHz, and S5: 30 kHz) and different frequency modulations as follows: trains of 20 decreasing (S1) and 20 increasing (S8) sweeps between 20 and 30 kHz, a parabola between 20 and 30 kHz (S6), a sinusoid between 20 and 26 kHz (S7), and sweeps decreasing (S2) or increasing (S9) between 20 and 30 kHz. These signals are comparable to those used by commercialised devices (Doxmand© Normal - flat and sine-triangle modulated signals ranging from 19 to 30 kHz). To evaluate the behavioural response of the species to our ultrasonic signals, we also created control signals consisting of four frequency modulations within the human audible range. To match with the ultrasonic signals, we chose a 2 kHz pure tone (A2), an increasing sweep from 2 to 3 kHz

<figure><img src="image_6.png" /><figcaption>**Figure 1.** Spectrograms of the two types of signals, ultrasonic (A), from S1 to S9, and controls (B), from A1 to A4. (C) Example of a sequence structure with nine ultrasonic signals followed by one control signal.</figcaption></figure>
(A1), a sinusoid between 2 and 3 kHz (A3) and a train of increasing sweeps from 2 to 3 kHz (A4) (see Figure 1B). Each acoustic signal was created with MATLAB (version R2021a), filtered by bandpass filters, from 2 to 3 kHz for control, and from 20 to 30 kHz for the ultrasound signals, and RMS normalised with R (version 4.0.3). During the playback experiments, groups were exposed to randomly generated sequences, including the nine ultrasonic signals (preceded and separated by intervals of 30 seconds of silence) and concluded by one of the control signals (Figure 1C).

## Study site and species

The playback experiments were conducted at the zoological reserve of La Haute-Touche, Obterre, France (46°53'4'' N, 1°4'22'' E), on three different species all assumed to have hearing sensitivity in the ultrasound domain and for which we had access to a sufficient number of individuals (N >= 10) to conduct robust statistical analyses. We performed a first session of experiments on two prey species likely to fear deterrent signals, red deer (*Cervus elaphus*), and peccaries (*Tayassu pecari*), and one predator species, wolves (*Canis lupus*), less likely to fear them. Playback experiments in red deer were performed in two sessions. The first session was conducted between the 18th and the 29th of October 2021, with 29 hinds divided into 4 groups of 6 individuals and one group of 5 individuals, aged 3 to 16 years, and identified with coloured collars. The second session took place between the 25th and the 29th of April 2022, involving the same red deer hinds (except one) distributed in 4 groups (of respectively 6, 7, 7 and 8 individuals) in order to get more samples. All experiments took place in 1-ha enclosure, 200 metres away from sight and hearing range of other groups in order to preserve signal novelty. Each red deer hind group was introduced to the experimental enclosure the day before the playback, to ensure that animals habituated to their environment.

We also decided to conduct playback experiments on peccaries, because they are closely related to wild boars (same suborder (Suiformes) but different family (Tayassuidae)), as wild boars were not available in sufficient numbers (N = 4) to be included in the study. For them, experiments were performed between the 25th and the 29th of April 2022, on a single group of 10 individuals, aged 2 to 10 years and kept in a 4500 m² enclosure. Finally, we performed playback experiments on 2 groups of wolves, between the 18th and the 29th of October 2021, to assess reactivity in a species whose auditory sensitivity to ultrasound is likely, given its phylogenetic closeness with two species that share this ability (domestic dog (Heffner 1983); red fox (Malkemper, Topinka, and Burda 2015)). The first group consisted of 10 north-western wolves (*Canis lupus occidentalis*), aged 1 to 5 years, in a 6000 m² enclosure. The second group included 6 European wolves (*Canis lupus lupus*), aged 3 to 6 years, in an 8400 m² enclosure.

## Experimental design

Playback experiments consisted of several trials corresponding to the broadcast of one sequence including the nine randomly ordered ultrasonic signals and terminated with a control signal. To ensure that acoustic signals were potentially detectable, the sound source, a pair of tweeters (TL 16H, © VISATON), was set to 96 dB sound pressure level (SPL) (re 20 µPa) at 1 metre using a Rion NL-52 sonometer. The broadcast system was positioned at ear height of each species (red deer: 130 cm; peccaries: 70 cm; wolves: 80 cm). The keeper fed animals in an area about 8 metres away from the sound source, to regroup animals within an area where signals were potentially audible. When most animals were within this area and once the keeper was out of sight, sequences were played with Avisoft Recorder (Sound Recording Software from Avisoft Bioacoustics ©) on a laptop connected to a power amplifier (© Avisoft Bioacoustics). We video-recorded the animals' behaviour during each playback with three cameras, one (Canon XA45/XA40) directly positioned above the sound source and the other two (Sony HDR-CX220) positioned on each side, to cover most of the enclosure.

Each group was exposed to multiple playbacks with a minimum of 4 hours between trials. During the first phase, the 5 groups of red deer (i.e., 29 individuals) were exposed to 2 sequences, one in the morning and one in the afternoon. Of these 10 playback trials, one was excluded from the behavioural analysis due
to a technical problem involving the loudspeakers, leaving a total of 9 trials. Both groups of wolves (i.e., 16 individuals) were exposed to two sequences, each on different days. In the second phase, the 28 red deer hinds (divided into 4 groups) were subjected to 4 different sequences, again with 2 trials per day (i.e., a total of 16 playbacks). Finally, for the peccaries, each ultrasonic signal was broadcast 6 times (not more than once per day) on the full group of 10 individuals. Finally, 25 playbacks were performed in red deer, 6 in peccaries, 2 in north-western wolves and 2 in European wolves.

## Video analysis

We used the BORIS open-source software (version 7.12.2) (Friard and Gamba 2016) to quantify the behavioural response of each individual from the video recordings, applying the focal animal sampling method. We combined published ethograms for the three species (da Silva et al. 2020; Mehrkam and Thompson 2015; Clutton-Brock, Guinness, and Albon 1982) into a general, synthetic ethogram (table 1), which we used to describe each individual's response within the 30 s following the playback of each acoustic signal. The expression of a behaviour was coded as a binary variable (absence = 0, presence = 1).

## Statistical analyses

Statistical analyses were performed using R with a significance threshold at 5 %. The nature of the acoustic signal was encoded using the variable ("Signal": ultrasound or control). We ran generalised linear mixed-effect models (GLMM) with a binomial error term and 'logit' link, to test the effect of this variable on the occurrence of behavioural responses (binomial variable "Response": absence (0) or presence (1)). We used one GLMM for each species, and considered as random factors, the tested group of individuals ("Group"), the sequence containing our randomly ordered signals ("Sequence"), and the time of the day ("Time": morning or afternoon) nested in the day of playback ("Date"). This results in the following model syntax:

Response ~ Signal + (1|Group) + (1|Sequence) + (1|Date/Time).

In addition, to assess the deterrence efficiency of ultrasonic signals, we compared the reactions of red deer with those of two other species. Peccaries were chosen because they displayed strong flight responses during our pilot studies, and thus potentially characterised reactions that would signify efficacy in deterrence. Wolves were chosen as a reference group expected to hear frequencies in the ultrasonic range

<table><caption>**Table 1.** The ethogram illustrates the behavioural responses to ultrasonic and control signals for *Cervus elaphus*, *Tayassu pecari*, and *Canis lupus*. "State events" represent behaviours that have a duration, while "Point events" refer to behaviours that do not last in time.</caption><thead><tr><td>Behavior</td><td>Description</td><td>Variable</td></tr></thead><tbody><tr><td>VIGILANCE</td><td>The animal stops with its head raised high and staring at the sound source.</td><td>State event</td></tr><tr><td>DETECTION</td><td>The animal turns one or both ears in the direction of the sound source during the acoustic signal or within 5 seconds of it.</td><td>Point event</td></tr><tr><td>APPROACH</td><td>The animal is approaching the sound source.</td><td>State event</td></tr><tr><td>MOVING</td><td>The animal is moving in any direction, looking in the direction of the sound source.</td><td>State event</td></tr><tr><td>AVOIDANCE</td><td>The animal is walking in the opposite direction to the sound source.</td><td>State event</td></tr><tr><td>FLIGHT</td><td>The animal is running in the opposite direction to the sound source.</td><td>State event</td></tr></tbody></table>
given their phylogenetic proximity with species that share this ability (domestic dog (Heffner 1983); red fox (Malkemper, Topinka, and Burda 2015)), but unlikely to perceive them as a threat given their predator status. Behavioural responses (i.e., vigilance, avoidance, and flight) between species we compared by performing an additional GLMM including species as a fixed factor and followed by Tukey contrasts.

## Results

Behavioural responses to playbacks varied significantly across species and signal types. Across the 25 trials, red deer hinds responded significantly more to audible control sounds (54.3%) than to ultrasonic ones (8.7%) ($Z = -13.86, p<0.001$; Figure 2A). This significant difference in response was consistent when examining specific behaviours such as vigilance (controls = 25.0% vs ultrasounds = 4.9%, $Z = -8.88, p < 0.001$), detection (controls = 25.0% vs ultrasounds = 3.0%; $Z = -10.25, p < 0.001$) and avoidance (controls = 4.3% vs ultrasounds = 0.5%; $Z = -4.06, p < 0.001$). Out of the total of 25 trials conducted on the 9 groups, we only counted three flight responses, which involved three red deer hinds from the same group, simultaneously responding to the playback of a single ultrasonic signal.

In contrast, there were no significant difference in the overall proportion of reactions by the peccaries to ultrasonic (55.6%) versus control signals (41.7%) over the 6 trials ($Z = 1.46, p = 0.143$). This lack of difference extended to specific behaviours like avoidance (controls = 13.3% vs ultrasounds = 21.7%, $Z = 1.54, p = 0.123$), vigilance (controls = 16.7% vs ultrasounds = 15.7%, $Z = -0.19, p = 0.850$), and detection (controls = 8.3% vs ultrasounds = 4.8%, $Z = -1.19, p = 0.233$). However, peccaries showed more aversive behavioural responses to ultrasounds, as flight responses (13.0%) were triggered exclusively by these signals. Unlike red deer hinds, peccaries approached the sound source, particularly in response to control sounds (3.3%) compared to ultrasounds (0.2%) ($Z = -2.43, p = 0.015$).

Wolves, on the other hand, reacted significantly less to ultrasonic (46.2%) than to control signals (84.4%) ($Z = -3.13, p = 0.002$) over the 4 trials. This also affected vigilance behaviour (controls = 72.0% vs ultrasounds = 36.1%, $Z = -3.79, p < 0.001$) but this is not significant for detection behaviour (controls = 9.4% vs ultrasounds = 6.6%, $Z = -0.62, p = 0.536$). While this confirms their ability to perceive ultrasonic frequencies, flight responses were never reported. However, we noted a small proportion of avoidance (2.8%) and approach (0.7%) behaviours in response to ultrasonic acoustic signals, which were not observed in response to control sounds.

Significant differences were observed in the proportions of aversive responses (vigilance, avoidance, and flight) to ultrasounds when comparing the three species (see Figure 2B). Wolves were more vigilant (36.1%) to ultrasonic signals than red deer (5.0%, $Z = 3.92, p < 0.001$). Regarding avoidance, peccaries (21.7%) reacted much more than red deer (0.5%, $Z = 5.49, p < 0.001$) and wolves (2.8%, $Z = 2.85, p = 0.012$). Finally, wolves did not flee, unlike peccaries (13.0%), who fled far more than red deer hinds (only once, 0.2%, $Z = 4.06, p < 0.001$).

## Discussion

In our study, we observed very few responses of red deer to the playback of ultrasonic signals. However, both wolves and peccaries exhibited different but strong reactions to these signals. We suggest that these contrasted responses are likely to reflect the different trophic levels occupied by these species.

Red deer hinds appeared to detect signals above 20 kHz, which is consistent with ungulate audiograms (Heffner and Heffner 2010; D'Angelo et al. 2007; Flydal et al. 2001; Heffner and Heffner 1990). However, their reactions, which mainly consisted of detection, vigilance, and avoidance of the sound source, were much rarer and weaker than those in response to control signals which are closer to the range of optimal auditory sensitivity (from 4 to 8 kHz in white-tailed deer, D'Angelo et al. 2007). The fact that we only observed a single simultaneous flight response from three individuals in the same group may not be
<figure><img src="image_7.png" /><figcaption>**Figure 2.** A. Comparison of percentages of overall behavioural responses between ultrasonic and control signals for each species: *Red deer* (*Cervus elaphus*), *Peccaries* (*Tayassu pecari*) and *Wolves* (*Canis lupus*). The columns represent the frequency, for each behaviour, with which the animals reacted when the acoustic signal was presented (the number at the bottom of each column corresponds to the number of playbacks multiplied by the number of individuals exposed). S1 (Train of decreasing sweeps), S2 (Decreasing sweep), S3 (Pure tone: 20 kHz), S4 (Pure tone: 25 kHz), S5 (Pure tone: 30 kHz), S6 (Parabola), S7 (Sinusoid), S8 (Train of increasing sweeps), S9 (Increasing sweep), A1 (Control increasing sweep), A2 (Control pure tone: 2 kHz), A3 (Control sinusoid), A4 (Control train of increasing sweeps). B. Comparison of vigilance, avoidance, and flight behavioural responses to ultrasound between the three species. \* p<0.05, \*\* p<0.01, \*\*\* p<0.001.</figcaption></figure>

surprising because, to the best of our knowledge, signals with frequencies in the ultrasonic range do not have perceptual properties that make them *a priori* more aversive than signals composed of frequencies in the human audible range (Bomford and O'Brien 1990). Our observations confirm results from previous studies of ultrasonic deterrents (Koehler, Marsh, and Salmon 1990; Curtis 1995; Belant, Seamans, and Tyson 1998; Valitzski et al. 2009) and is consistent with the fact that ultrasounds are unlikely to signal danger in the natural environment of red deer hinds. Indeed, in western Europe, the main natural predators of
ungulates, e.g., wolves and brown bears (*Ursus arctos*), are not known to emit ultrasonic sounds. Ultrasonic calls are more common in small species such as bats (Griffin and Galambos 1941; Knörnschild, Glöckner, and Helversen 2010) or rodents (Whitney 1970; Riede 2014), which do not represent a threat for large terrestrial mammals. As such red deer were not expected to have evolved an aversion to ultrasonic acoustic signals.

We can contrast the reaction of red deer hinds with that of peccaries, whose very strong reactions to ultrasound signals not only reveal that they must be sensitive to these frequencies (to the best of our knowledge no audiometric data is available for this species), but also that these frequencies could signal a threat in their natural environment (e.g. predator calls, heterospecific or conspecific alarm sounds). Indeed, we observed strong flight responses at each onset of a sequence, indicating little habituation between sequences. However, individuals did get progressively habituated (Rankin et al. 2009) to signals within the sequence. Interestingly, peccaries reacted less to controls and sometimes even approached the sound source. This could either be because our control sounds were always positioned at the end of the playback sequence, or because they did not represent a threat to this species. In contrast, the significant rebound in reaction observed in red deer and in wolves to these controls (positioned at the end of sequences) shows that acoustic signals in the human audible range are more evocative for them than very high-frequency signals (in the human ultrasonic range). In any case, wild boars' response to ultrasounds should now be investigated as they are likely to have a hearing range close to that of domestic pigs.

The weak behavioural responses of red deer to ultrasounds can also be contrasted with those of wolves, who typically responded by either directly looking at the loudspeakers, sniffing the air, pausing, or taking a step to the side, but did not run away. We expected wolves to demonstrate detection behaviours as the hearing range of closely related species, extends beyond 30 kHz (domestic dog (Heffner 1983); red fox (Malkemper, Topinka, and Burda 2015))). Yet, we did not expect them to exhibit a strong aversive reaction to ultrasound signals given their predator status which make them unlikely to fear any ultrasound-emitting threat. Indeed, compared to prey species, wolves are only expected to be threatened by human as super predator (Ydenberg and Dill 1986; Stankowich and Blumstein 2005; Cooper and Frederick 2007). Instead, we expected wolves to seek out prey emitting in this range, such as rodents (Whitney 1970; Riede 2014). This sensitivity range may also facilitate communication among individuals, as observed in domestic dogs where polyphonic whines can reach frequencies up to 23.3 kHz (Sibiryakova, Volodin, and Volodina 2021).

The proportion of flight behaviour in reaction to ultrasonic signals was negligible in red deer hinds, even when these signals were frequency modulated. This makes ultrasonic sounds poor candidates as efficient acoustic deterrents for this species. This weak behavioural effect is likely to be amplified by the high directivity and fast attenuation of very high-frequency sounds that significantly limit their efficient propagation (Koehler, Marsh, and Salmon 1990). These inherent limitations prompted us to carry out our experiments under optimal conditions, to ensure that the ultrasonic signals were potentially audible to the animals by attracting them close to the sound source before the playback was initiated. Hence, the already weak detection and vigilance reactions observed in our study are unlikely to generalise to real-world scenarios where deterrence is required.

Together the results of this study lead us to suggest that future work aimed at designing acoustic deterrence tools for eliciting flight responses in red deer hinds should explore alternative approaches, using acoustic signals that fall within the frequency range where ungulates (or their predators) vocalise and where they possess heightened auditory sensitivity (Heffner and Heffner 2010; D'Angelo et al. 2007; Flydal et al. 2001; Heffner and Heffner 1990). Indeed, previous studies of deterrence signals, in birds and mammals, have shown that natural or biologically inspired sounds, such as alarm, distress, or predator calls, are typically more aversive and less impacted by habituation than ultrasonic signals or pure tones (Bomford and O'Brien 1990; Babińska-Werka et al. 2015).
Acknowledgments

A special thanks, to Christophe Audureau and Charly Binaud, from the zoological reserve of La Haute-Touche, who contributed to field work. We thank Léo Papet and Léo Perrier who provided technical support, Nicolas Boyer who build the playback devices, and Florian Eneau for second-coding the behavioural responses.

Declaration of interest statement

The authors declare no competing interests.

Ethical statement

The experiment was conducted under the zoological reserve of La Haute-Touche’s experimental
Agreement n° 36145002. The animals were never restrained while the sound was being sent and the
enclosures were chosen so that they always had the opportunity to avoid the signal.

Author contributions

AT, DR, and YL conceived the idea. AT created acoustic signals and analysed animal behaviours. AT and CV conducted the playback experiments. AT and LP analysed the data. AT and DR wrote the original draft of the paper and led the revisions, and all authors critically reviewed several versions of the manuscript.

Fundings

AT and this work, including experimental costs, were funded by the French railway company, SNCF, and
the ANRT under the contract number CIFRE 2021-0011. This PhD is co-managed by Claire Chaufour and
Yannick Matillon (SNCF VOYAGEURS), Anne Petit (SNCF RESEAU) and Patryk Dec (SNCF). DR was also
supported by a grant from the French National Research Agency (“SCREAM”, ANR-21-CE28-0007-01). NM
and DR were also supported by the Institut universitaire de France and LP by Pôle emploi.

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