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/lp/springer-journals/context-dependent-alarm-responses-in-wild-vervet-monkeys-jqBShBNaEW
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- Springer Journals
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- Copyright © The Author(s) 2023
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- 1435-9448
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- 1435-9456
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- 10.1007/s10071-023-01767-0
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Abstract
The alarm calls of nonhuman primates are occasionally cited as functionally equivalent to lexical word meaning in human language. Recently, however, it has become increasingly unlikely that one-to-one relations between alarm call structures and predator categories are the default, mainly because many call types are produced in multiple contexts, requiring more complex notions of meaning. For example, male vervet monkeys produce the same alarm calls during encounters with ter- restrial predators and neighbouring groups, suggesting that recipients require additional information to attribute meaning to the calls. We empirically tested the hypothesis that vervet monkeys take contextual information into account when responding to each other's alarm calls. In playback experiments, we exposed subjects to recordings of male alarm barks during actual intergroup encounters (predator unlikely) or when there was no intergroup encounter (predator likely). Subjects responded more strongly in the no intergroup encounter situations, typically associated with discovering a hiding predator, measured in terms of startle responses, vigilance behaviour and gazing towards the presumed caller. We discuss the significance of using contextual information for meaning attribution in nonhuman primate communication. Keywords Evolution of language · Vocal communication · Nonhuman primates Introduction 1993; Seyfarth et al. 1980a). In animal communication, the evidence is typically in the form of acoustically distinct calls A significant milestone in the Darwinian quest for evolution- produced in context-specific ways, in analogy with lexical ary continuities in cognition (Darwin 1872) has been the semantics in linguistics with mental representations refer- discovery that vervet monkeys (Chlorocebus pygerythrus ring to the meaning of words. For example, monkeys give hilgerti) produce acoustically distinct alarm calls to refer 'eagle' alarm calls to particular species of raptors, or 'snake' to different types of predators (Struhsaker 1967), which has alarm calls given to some dangerous snake species (Pereira led to the suggestion that animal alarm calls can function as and Macedonia 1991; Zuberbühler 2000a, 2001; Manser if they possessed lexical meaning (Macedonia and Evans 2001; Kirchhof and Hammerschmidt 2006; Cunningham and Magrath 2017). However, with the advancement of acoustic analysis tech- * Adwait Deshpande niques and long-term behavioural observations, the tight adwait.deshpande2390@gmail.com one-to-one links between acoustically distinct alarm calls and their eliciting predator contexts have mostly dissolved. Department of Comparative Cognition, Institute of Biology, University of Neuchatel, Neuchatel, Switzerland What initially looked like a predator-specific alarm call turned out to be a call given to multiple situations, often with Inkawu Vervet Project, Mawana Game Reserve, KwaZulu-Natal, South Africa no obvious underlying coherence (Price et al. 2015). But why would natural selection favour the evolution of contex- Department of Collective Behavior, Max Planck Institute of Animal Behavior, Constance, Germany tually ambiguous alarm signals in the predation context? If the alarm calls do not refer to specific types of danger, how Centre for the Advanced Study of Collective Behaviour, University of Konstanz, Constance, Germany can recipients ever make adaptive anti-predator decisions, one of the presumed functions of animal alarm calling? Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland It is important to remember that the predator fauna often varies within a species' geographic range and can School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK Vol.:(0123456789) 1 3 Animal Cognition also change rapidly over time, which requires consider- Arseneau et al. 2016, 2018). As a result, different subgroups able mental flexibility by the recipients. One solution to the of individuals participate in frontline aggression during each conundrum is that recipients attend to contextual informa- encounter, while others stay back and appear uninterested. tion beyond the acoustic structure of the calls themselves We took advantage of this fact to examine whether disen- to make inferences about the most likely cause of an alarm gaged individuals used contextual information when hearing call (Fischer and Price 2017). A few empirical studies have the male alarm barks of frontline males during between- already provided relevant evidence for the influence of con- group encounters. To control for the acoustic variant text on call inference. First, putty-nosed monkeys show less hypothesis, we recorded male alarm bark variants originally vigilance to terrestrial alarm calls if the calls are preceded produced during terrestrial predator encounters or between- by the sound of a falling tree compared to no preceding cues group encounters as playback stimuli. We predicted that if (Arnold and Zuberbühler 2013). In addition, Diana monkeys non-participating and uninterested individuals took context respond differently to the playback of Guinea fowl alarm into account, they should show differential (strong or weak) calls, depending on the priming of different predator types responses to the playback of alarm barks presented dur- before the playback (Zuberbühler 2000a, b, c). ing ongoing between-group encounters compared to when Of course, it is always possible that what appears to be there was no ongoing encounter. Alternatively, if the context one call type is, in fact, a group of subtle, acoustically dis- played no role in how an individual responded to the alarm tinct call variants, which refer to separate external events and bark, we expected no significant difference in responses so facilitate meaning attribution for recipients. In line with across treatments. Finally, if the call variant alone drove this, call variants appear to be a fairly frequent phenomenon the responses, we predicted that the subject would respond in primate communication, with evidence in Campbell's differentially on the basis of the call variants they heard, monkey alarm calls (Keenan et al. 2013) or chimpanzee soft regardless of the context. We discuss our results in light of ‘hoos’ (Crockford et al. 2018). Like humans, some primates different explanations for the use of contextual information. appear to be able to perceive acoustically graded signals in categorical ways (e.g., Barbary macaques: Hammerschmidt and Fischer 1998), adding plausibility to the acoustic vari- Methods ant hypothesis. Here, we revisit the alarm call system of vervet monkeys, Study site and groups the classic example of ‘lexical semantics’ in animal com- munication. In the South African subspecies (Chlorocebus The study was conducted between July and November 2019 pygerythrus pygerythrus), males have been observed to at the Inkawu Vervet Project (IVP), located in the Mawana produce alarm barks to terrestrial predators but also during Game Reserve, Kwazulu Natal, South Africa (S 28° 00.327; within- and between-group aggression (Price et al. 2015). E 031° 12.348). All observers complete a standard training Thus, the male alarm bark in this subspecies is an ideal call protocol and complete inter-observer reliability and individ- type to investigate whether listeners take additional informa- ual identification tests before participating in data collection. tion into account to make inferences about a call's meaning. Researchers have access to several neighbouring groups of We experimentally tested how free-ranging South African wild South African vervet monkeys that are well-habituated vervet monkeys responded to male alarm barks when primed to human presence and allow close observations by multi- with or without intergroup encounters. We used naturally ple observers. Data for this study were collected from one occurring intergroup encounters and no ongoing intergroup group (BD), consisting of 57 individuals (adult females: encounter situations as contexts, during which we played N = 16; adult males: N = 12; juvenile females: N = 15; juve- back recordings of male alarm barks in controlled ways. nile males: N = 14). Encounters between two neighbouring monkey groups are regular events ranging from peaceful co-foraging to Experimental procedure severe physical aggression (Willems et al. 2015). Inter- estingly, during aggressive encounters, males from both We tested the effects of alarm bark variants on subjects groups sometimes produce alarm barks that acoustically engaged in either a between-group encounter (BGE trials, resemble terrestrial predator alarms, along with other N = 8) or no between-group encounter (non-BGE trials, aggressive vocalisations (Price et al. 2015). The responses N = 8), using a within-subject design (N = 8 adult female to these alarm barks during aggressive encounters are var- subjects; N = 16 trials). ied and sometimes include calls by other males. Participa- We recorded alarm barks produced by adult males tion in intergroup aggression varies from case to case but is of three groups in both between-group encounter (BGE most common for high-ranked individuals, although it also variant) and terrestrial predator encounter (PRE variant) depends on prior social interactions (Willems et al. 2015; situations. Calls were acoustically highly similar (see 1 3 Animal Cognition Supplementary material for acoustic) (Price et al. 2015; BGE trials Besson 2017). Out of all the call recordings, we selected one BGE and one PRE variant produced by a single adult Since between-group encounters occurred unpredictably, we male in the BD group who was present in the group for conducted BGE trials opportunistically, provided the fol- the entire duration of the experiment as playback stimuli lowing conditions were met. First, we only initiated a trial for the experiment (Fig. 1). Both exemplars were from the after visible intergroup aggression. This was because male same adult male and were the only ones in our database alarm barks were usually given during intergroup encounters with the sufficiently high acoustic quality required for that involved physical aggression between the two groups. playbacks. We randomly assigned the BGE variant as a The caller usually actively participated during intergroup playback stimulus to four subjects and the PRE variant to aggressions and most likely remained on the frontline (see the remaining four subjects. We used the same call variant below). Second, previous studies (Ducheminsky et al. 2014) for BGE and non-BGE trials for each subject. suggested that habitat type and the group spread affected We removed background noise and padded the calls responses to alarm calls, so we only conducted experiments with two seconds of silence before and after the utter- in mixed habitat type (i.e., canopy cover > 50% to < 100%) ances using Raven Pro 1.5 (Center for Conservation Bio- and the group spread approximately 100 m (i.e., the distance acoustics 2014). Recordings were played back using a between the subject and all other group members no more Motorola XPlay phone and an Anchor AN-MINI-RST-01 than 100 m). speaker. Call amplitudes were adjusted and kept constant An intergroup encounter started when members of across trials, such that they matched natural calls at a another group were within 50 m of any individual of the distance of 30–50 m which was also the usual distance study group (BD) or if BD individuals were vocally react- between subjects and BGE frontline during BGE trials ing to another group with grunts, screams or chutter calls (see below) (Fig. 2). (Cheney and Seyfarth 1982). All eight trials were conducted when BD encountered either habituated group of AK (N = 5) or a semi-habituated group CR (N = 3), which made it pos- sible to observe monkeys without interfering with their Fig. 1 Spectrograms (Hamming window at 1024 DFT and 93.8% a terrestrial predator encounter B BGE variant: Alarm bark recorded overlap) of the exemplars of calls from a BD male used as playback during between-group encounters calls for the experiment A PRE variant: Alarm bark recorded during 1 3 Animal Cognition Fig. 2 Schematic illustration (not to scale) showing BGE trial design behaviour. Once the encounter had started, we waited for at communicated with each other via Motorola radios, and least 5 min before carrying out a trial. We only conducted once all conditions were met, the first observer played a male a trial if there were between-group aggressive interactions alarm bark variant from the speaker near the front line. The (running towards the opposing group, aggressive vocalisa- second observer video-recorded the subject's behaviours for tions, chasing, grabbing, and biting individuals of the oppos- the next 10 min from the onset of the playback. The average ing group) during this period. However, if any male from time gap between the two consecutive BGE trials on differ - either group produced an alarm bark during this period, ent subjects was 8.7 days. we aborted the trial. We also made sure the caller male of the playback call was not present in the vicinity (approx. 10–15 m) of the subject of the trial and not directly visible Non‑BGE trials to the subject. Two observers were present during each experiment. The same individuals were tested during non-BGE trials The first observer positioned herself on the front line of with the same playback stimulus with a minimum gap of the encounter, i.e., the imaginary line that separated the three days from the BGE trials, but this time in the absence two groups, where most between-group interactions hap- of intergroup encounter, when most group members were pen (Arseneau et al. 2016, 2018; Willems et al. 2015). All either foraging, resting or grooming. We ensured that no individuals within 10 m of the front line were considered intergroup encounter and no natural alarm-calling event participants in the encounter. Frontlines could shift during occurred for at least 2 h before a trial. As with BGE trials, encounters, particularly when one group decides to retreat we only conducted non-BGE trials in mixed habitats and (Fig. 2). The first observer continuously monitored the front- with a group spread of about 100 m. The second observer line and also operated the playback speaker. located the subject and followed it for at least 10 min. If no The second observer selected and monitored the sub- relevant event occurred during this time period (participation ject provided it was not participating in the encounter (i.e., in intra-group aggression), the second observer informed the located at least 30 m from the front line, not showing any first observer to start the trial. Similar to BGE trials, the first interest in the encounter but engaged in foraging, resting observer then positioned herself between 30 and 50 m from or grooming). The subject was continuously filmed using the subject hidden behind a bush to broadcast the playback a JVC quad-proof EverioR camcorder. Both observers stimulus upon the instructions from the second observer on 1 3 Animal Cognition the radio. The second observer video-recorded the subject We could not use the same approach to assess the effect of continuously for 10 min from the onset of the playback call. treatments on the binary variables, appropriate anti-predator reaction and startle due to the small sample size. We tested the effect of trial type using the Mcnemar test on the startle Behavioural responses responses. For both types of trials, the second observer continuously scored the overall group activity, the number of individuals Results present within 5 m of the subject before each trial (audi- ence size), and any other significant behaviours by the group Subjects looked toward the speaker for significantly less time members. in the BGE compared to the non-BGE trials (two-tailed Wil- We coded key behaviours during the first minute follow - coxon test (paired): Z = 33, p = 0.03, r = 0.74; Fig. 3). The ing each playback trial using BORIS V. 7.10.2 coding soft- duration of looking toward the speaker was not affected by ware (Friard and Gamba 2016). We were specifically inter - the PRE and BGE call variants (two-tailed Wilcoxon test ested in the following behaviours by the subject: (1) Looking (paired): Z = 25, p = 0.383, r = 0.34). They also showed towards the speaker (duration of looking in the direction lower vigilance in BGE compared to non-BGE trials (two- of the speaker (s), as inferred from head orientation); (2) tailed Wilcoxon test (paired): Z = 23, p = 0.04, r = 0.72; vigilance [duration of scanning environment with alert body Fig. 4). Vigilance was not affected by the PRE and BGE call posture (s)]; (3) startle [sudden complete or upper body jerk variants (two-tailed Wilcoxon test (paired): Z = 27, p = 0.25, movement, with a rapid head movement in any direction r = 0.44). Fewer subjects showed startle responses in BGE (yes/no)] (Ducheminsky et al. 2014); (4) predator-specific compared to non-BGE trials (McNemar Test, p = 0.04). responses (running into the nearest tree or bush for terrestrial Startle responses were never observed in the non-BGE tri- predator (yes/no) (Seyfarth et al. 1980b, c). als and in only half of the BGE trials. Additionally, during To assess inter-observer reliability, 8 out of 16 trial videos N = 2 BGE trials, the adult male from the other group (AK) were randomly selected and scored by a second coder blind responded with alarm barks after hearing the playback of the to the hypotheses and objectives of the study but familiar calls. Predator-specific responses never occurred, neither in with primate behaviour. We then compared the key behav- the BGE nor in the non-BGE trials. iours described above between the two observers. As the direction of the speaker was not obvious in the video to the naïve coder, he was informed about the direction of the Discussion speaker at the start of the video. We calculated Pearson's correlations coefficients and ran paired t tests between two We investigated the hypothesis that vervet monkeys relied coders for the continuous variables (Looking towards the on contextual information to infer the meaning of one of speaker: r = 0.78, p = 0.02, t = 0.05, p = 0.96; Vigilance: their calls, the male alarm bark, which is given to terrestrial r = 0.88, p = 0.003, t = 0.90, p = 0.39) and Cohen's kappa was predators, but also during non-predatory intergroup aggres- calculated for the startle responses (k = 0.91). Both coders sion. We were able to show experimentally that recipients agreed that no predator-specific responses occurred. Thus, reacted differently to the same call, depending on the con- the inter-observer agreement was sufficiently high for all texts in which it was presented. When male alarm barks three key behaviours. were produced during ongoing intergroup encounters, non- participating subjects were less reactive to the calls, i.e., Statistical analyses they looked at the speaker for less time, were less vigilant and never showed startle responses, compared to when the All statistical analyses were conducted in R v4.0.3 (Team same calls were produced during non-BGE trials. 2020). We used non-parametric repeated measures tests to We selected the variable 'looking towards the speaker' verify the effects of treatments and call variants used as play - because it was most likely an indication that the subject was back stimuli on the response variables (Duration of look- looking for information about the reason for the call from ing towards the speaker, vigilance, and startle response). the caller (Struhsaker 1967; Seyfarth et al. 1980a). The fact To test our prediction that both duration of looking towards that subjects either looked for less time towards the speaker the speaker and vigilance is lower in the BGE trial, we used or one subject did not look when trials were administered one-tailed paired Wilcoxon signed rank tests. Similarly, to during between-group interactions suggested that they had test the effect of call variants, we used two-tailed paired already made interpretations regarding the call. During BGE Wilcoxon signed rank tests. We also calculated effect sizes trials, subjects already had time to learn about the inter- for all the tests. group context, either due to other vocalisations typical for 1 3 Animal Cognition p= 0.03 Playback BD BGE BD PRE No Between Group Enconter Between Group Encounter (non−BGE) (BGE) Context Fig. 3 Box plot showing a comparison of duration of looking sent raw data points for each subject (N = 8) across treatments. Signif- towards the speaker in two treatments. Solid line in the box denotes icance of Wilcoxon tests is represented by ‘p’. The call variant used the median, Δ denotes the mean, solid dots connected by lines repre- as a playback during the trial is denoted by the shape of the dots this context or due to having spotted members of the neigh- in the likelihood of negative consequences resulting from bouring group before the playback. Thus, the uncertainty the uncertainty regarding the cause of the call can increase about the cause of the (playback) call was low. In contrast, information-seeking efforts during non-BGE trials. when the same calls were played during non-BGE trials, Another argument for additional information seeking subjects had no relevant prior information available about from the caller in non-BGE trials could be a higher rate of the call's cause. false alarms in large groups, which could drive individuals to In BGE trials, low uncertainty also indicates a low like- seek more information before responding, probably to avoid lihood of negative consequences. The subjects were adult energetic costs (Beauchamp and Ruxton 2007). Furthermore, females who were away from the frontline of the encounter. additional information seeking in a non-BGE context can be Thus, the potential negative consequences were minimal for used as a strategic response to counter the deceptive alarm them. On the other hand, the likelihood of negative conse- calls (Wheeler 2009; Wheeler and Hammerschmidt 2013). quences could be higher (e.g. ambush by a predator) for Many subject monkeys spent significantly less time being the same subjects in the non-BGE trial. Such differences vigilant or seeking information from the environment during 1 3 Looking at Speaker (sec) Animal Cognition p= 0.04 Playback BD BGE BD PRE No Between Group Enconter Between Group Encounter (non−BGE) (BGE) Context Fig. 4 Box plot showing comparison of duration of vigilance behav- points for each subject (N = 8) across treatments. Significance of Wil- iour in two treatments. Solid line in the box denotes the median, Δ coxon tests is represented by ‘p’. The call variant used as a playback denotes the mean, solid dots connected by lines represent raw data during the trial is denoted by the shape of the dots BGE trials. Furthermore, three subjects showed no vigilance and the adult males and other individuals from both groups during BGE trials (Fig. 4). As the subjects, per design, did produced male alarm barks on the frontline. However, not participate in the intergroup encounter and stayed away during the encounter, a jackal (Lupulella mesomelas) was from the frontline, a reasonable interpretation for them was spotted by the observer (AD) stalking a non-participating that the call was directed at a neighbouring group rather individual (AD, personal obs.). Several frontline individu- than at a predator or themselves. In non-BGE trials, how- als also saw the jackal and produced alarm calls to it, but ever, no further contextual information was available, which the non-participating individuals did not react strongly with increased the uncertainty about the call's cause and might anti-predator behaviour or vigilance to the alarm calls (as have resulted in increased vigilance. predicted for this context and as documented in the experi- Here, it is important to mention a relevant natural obser- ment). In this case, the jackal's hunting attempt was unsuc- vation of aggressive encounter between two other groups in cessful as, at the last moment, the targeted monkey saw the this population made outside this study. On 8th February jackal and escaped onto a tree. However, the observation 2018, the NH and AK groups had an aggressive encounter, highlights a rare situation in which listeners are likely to 1 3 Vigilance (sec) Animal Cognition draw wrong conclusions, which could be fatal. Ambiguous the population in this study (Robert Seyfarth personal com- contexts, like the one described here, are probably very rare, munication). Such differences in predatory pressure among such that contextual information is generally reliable. populations could also explain the differences in predator- Finally, startle responses, which are indicative of specific responses to male alarm barks. unexpectedness, were absent during BGE trials but were Recent similar experiments on closely related green mon- observed in half of the non-BGE trials. This result is in line keys (Chlorocebus sabaeus) are relevant here. During these with the interpretation that monkeys assumed the presence experiments, researchers primed subjects one hour before of a predator in the absence of a disambiguating intergroup the playbacks, which did not have a lasting impact on their context. In other words, the most plausible interpretation is subsequent behaviour. In our study, calling context was an that subjects in non-BGE trials were more affected by an ongoing event that may represent a more natural case and unanticipated male alarm bark than in the intergroup context explain the diverging results, despite the fact that contextual in which such calls are common. The fact that only some information could impact long-term responses, albeit weakly subjects responded this way might be linked to individual (Price and Fischer 2014). Another difference between our differences in age, sex, or social position. As we could not study and the green monkey experiment relates to the nature conduct proper statistical analyses for this variable, our of the playback stimulus (male alarm barks vs female ter- results remain suggestive. restrial predator alarm chirps, respectively). It is possible Overall, the behavioural responses in the BGE condition that male and female calls evoke different responses or serve indicated that if recipients already had an expectation for different functions (Zuberbühler 2005; Mehon and Stephan why a male alarm bark was produced (in this case, due to 2021). The function of the male alarm bark in South Afri- the intergroup encounter), they were not specifically affected can vervet monkeys has not yet been studied systematically. by the call, in contrast to non-BGE situations where the However, the playback call during two BGE trials triggered alarm bark was distinctive with the ongoing context and, alarm barks from a male of the opposing group, pointing in all likelihood, predicted that the male unexpectedly spot- towards a possibility that these alarm calls also communi- ted a terrestrial predator. In other words, it appeared that cate to both predators and conspecific competitors, as noted the non-BGE condition in our experiment was perceived by previous studies (Cheney and Seyfarth 1992; Price et al. as a potential predator encounter. Furthermore, we did not 2015). find any support for acoustic variant hypotheses. Although Whatever the function of alarm barks might serve, the it does not necessarily mean those variants of male alarm critical point remains that male alarm barks in all con- barks are acoustically indistinguishable from each other. Per- texts might have predicted the presence of potential threats haps, graded acoustic differences in the call variants (Price (although of different types) to receivers. And the contextual et al. 2015) might not be enough to make accurate inferences information facilitated locating and specifying the source without considering the external contextual information. of the threat, allowing individuals to respond appropriately It is essential to note that we never saw predator-specific (Deshpande et al. 2022). escape responses, as sometimes seen in response to terres- Generally, our results can be interpreted as a systematic trial predators. For terrestrial carnivores, the most adaptive use of contextual information to assign meaning to primate anti-predator response is to climb rapidly into the nearest alarm calls. Similarly, Diana monkey responses to hetero- tree or bush (Seyfarth et al. 1980a). Nevertheless, such rapid specific alarm calls are based on prior information about flight responses have been observed in the study groups, but probable causes (Zuberbühler 2000b, c). Capuchin mon- they typically occur when individuals forage close to each keys ignore alarm calls given during competitive feeding other (AD unpublished data 2019). Thus, these textbook- events. However, they respond strongly to the same calls style antipredator responses may occur primarily under in other situations (Wheeler and Hammerschmidt 2013), specific circumstances when social contagion overrides and baboons respond to grunts depending on the context individual decision-making (Armstrong 1951; Hoppitt et al. in which they were produced (Rendall et al. 1999). Taken 2007). Similar observations about the general lack of appro- together with these studies, our results suggest primates can priate predator-specific responses and its occurrence due to take into account social and environmental cues to infer the social contagion were made in a study on a different popula- most probable cause and the potential consequences of call tion of the same species (Ducheminsky et al. 2014). These production, i.e., causal inference becomes the basis for the observations reiterate that responses to alarm calls are not attribution of meaning. stereotyped as described in earlier studies; i.e. each alarm Supplementary Information The online version contains supplemen- call type evokes a specific response from the recipients (Sey - tary material available at https://doi. or g/10. 1007/ s10071- 023- 01767-0 . farth et al. 1980a). Alternatively, the Amboseli population in Kenya, on which the original study was conducted, was Author contributions AD conceived the study with help from KZ. AD conducted the experiments, analyses and wrote the first draft, which KZ regularly encountered and predated by leopards compared to 1 3 Animal Cognition reviewed. AD and KZ wrote the final version of the manuscript. EvdW Besson E (2017) Vervet monkeys alarm calls: context specific or not? provided resources and access to the study groups at IVP and reviewed University of Neuchatel, Neuchatel the final version of the manuscript. Center for Conservation Bioacoustics (2014) Raven Pro: interactive sound analysis software Funding Open access funding provided by University of Neuchâtel. Cheney DL, Seyfarth RM (1982) How vervet monkeys perceive their This study was primarily funded by the Swiss National Science Foun- grunts: field playback experiments. Anim Behav 30:739–751. dation through grants (31003A_166458 and 310030_185324) awarded https:// doi. org/ 10. 1016/ S0003- 3472(82) 80146-2 to KZ and (PP00P3_170624) to EvdW as well as the Branco Weiss Cheney DL, Seyfarth RM (1992) How monkeys see the world: inside Fellowship—Society in Science. AD is additionally supported by the the mind of another species. The University of Chicago Press, Swiss National Science Foundation through grant (P2NEP3_200190). Chicago Crockford C, Gruber T, Zuberbühler K (2018) Chimpanzee quiet hoo Data availability Data and the code for the analyses are available on variants differ according to context. R Soc Open Sci 5:172066. the following link: https://osf. io/ kw5qg/? vie w_onl y=8ff2c f2f00 164c0 https:// doi. org/ 10. 1098/ rsos. 172066 fbacc 6ee4c 8e568 e5. Cunningham S, Magrath RD (2017) Functionally referential alarm calls in noisy miners communicate about predator behaviour. Anim Behav 129:171–179. https:// doi. org/ 10. 1016/j. anbeh av. Declarations 2017. 05. 021 Darwin C (1872) The expression of the emotions in man and ani- Conflict of interest The authors have no conflicts of interest to declare mals. J. Murray, London that are relevant to the content of this article. Deshpande A, Van Boekholt B, Zuberbuhler K (2022) Preliminary evidence for one-trial social learning of vervet monkey alarm Ethics statement The experiment involved the playback of an indi- calling. R Soc Open Sci 9:210560. https://doi. or g/10. 1098/ rsos. vidual who was present in the group for the entire duration of the experiment. To avoid any potential effects of the playbacks on the caller Ducheminsky N, Henzi SP, Barrett L (2014) Responses of vervet mon- individual, we kept our sample size to a minimum. We did not observe keys in large troops to terrestrial and aerial predator alarm calls. any significant changes in the caller individual's behaviour during and Behav Ecol 25:1474–1484. https://doi. or g/10. 1093/ beheco/ ar u151 after the experiment. The experiment and observational data collection Fischer J, Price T (2017) Meaning, intention, and inference in primate protocols were approved by Ezemvelo KZN Wildlife, South Africa vocal communication. Neurosci Biobehav Rev 82:22–31. https:// and the Ethics Commission of the University of Neuchâtel (permit doi. org/ 10. 1016/j. neubi orev. 2016. 10. 014 number 28/2018). Friard O, Gamba M (2016) BORIS: a free, versatile open-source event- logging software for video/audio coding and live observations. Open Access This article is licensed under a Creative Commons Attri- Methods Ecol Evol 7:1325–1330. https:// doi. org/ 10. 1111/ 2041- bution 4.0 International License, which permits use, sharing, adapta- 210X. 12584 tion, distribution and reproduction in any medium or format, as long Hammerschmidt K, Fischer J (1998) The vocal repertoire of Barbary as you give appropriate credit to the original author(s) and the source, macaques: a quantitative analysis of a graded signal system. Ethol- provide a link to the Creative Commons licence, and indicate if changes ogy 104:203–216. https:// doi. or g/ 10. 1111/j. 1439- 0310. 1998. were made. 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Journal
Animal Cognition – Springer Journals
Published: Mar 17, 2023
Keywords: Evolution of language; Vocal communication; Nonhuman primates