Gestural sequences in wild spider monkeys (Ateles geoffroyi)

doi:10.21203/rs.3.rs-3981827/v1

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Gestural sequences in wild spider monkeys (Ateles geoffroyi)

https://doi.org/10.21203/rs.3.rs-3981827/v1

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To date, research on gestural communication in species other than great apes has been quite limited, especially in their natural habitat. In this study, we aimed to explore the use of gestural sequences in an understudied neotropical primate species, Geoffroy’s spider monkeys (Ateles geoffroyi). To this aim, we conducted behavioural observations via focal sampling on a wild group consisting of 54 individuals and collected 709 gestures, including 125 sequences and 182 gestures that were not part of a sequence. Most sequences included 2-4 gestures and were produced in the play context. Sequences often continued even after triggering the recipient’s response and were mostly produced by males and younger individuals, toward younger recipients. Only three sequences (i.e., embrace-pectoral sniff, push-present climb, grab-grab pull) occurred more than twice and were not mere repetitions of the same gesture type. Our results suggest that sequences are common in the gestural communication of spider monkeys and that they are likely the result of increased emotional arousal, rather than an attempt to convey novel meaning.

Gestural communication in non-human primates (hereafter primates) has been systematically studied since the 1960s (see: Cartmill and Hobaiter 2019; Graham et al. 2022; Plooij 1978; Tomasello and Call 2019; van Lawick-Goodall 1968, 1972), with a particular focus on great apes (Bezanson and McNamara 2019). Much of the interest in ape gestural communication originally stemmed from the hypothesis that gestures played a central role in the evolution of language, as the first forms of human language might have been gestural (Arbib et al. 2008; Dediu and Levinson 2013; Fitch 2010; Levinson 2023; Tomasello 2008). Therefore, the study of gestural communication in apes was thought to provide valuable insights into crucial evolutionary aspects of human communication (Liebal et al. 2013).

To date, our current understanding of gestural communication in great apes suggests that apes can use a rich system of gestures (Byrne et al. 2017; Hobaiter and Byrne 2011a; Tomasello and Call 2019) to convey specific meanings (Hobaiter and Byrne 2014) in an intentional and flexible way (Hobaiter and Byrne 2011a; Hobaiter et al. 2022; Kalan et al. 2023; Liebal et al. 2004; Pika and Deschner 2019). The basic forms and meanings of ape gestures are mostly considered to be largely innate, with social experience providing individuals with the opportunity to refine their gestural communication systems and enhance effectiveness over time (Amici and Liebal 2022; Byrne et al. 2017; Graham et al. 2018; Hobaiter and Byrne, 2011a, 2011b).

In recent years, the study of primate gestural communication has partially extended beyond great apes, although certain primate species, particularly neotropical and nocturnal primates, still remain largely understudied (Gursky and Nekaris, 2019; Liebal et al. 2022; Lisboa et al. 2021). These studies have started revealing the existence of large communication systems characterized by intentionality and flexibility in several monkey species, including mangabeys (Cercocebus torquatus: Aychet et al. 2020; Maille et al. 2012; Schel et al. 2022), macaques (Macaca tonkeana: Canteloup et al. 2015; Macaca radiata: Deshpande et al. 2018), baboons (Papio anubis: Meunier et al. 2013; Molesti et al. 2020) and neotropical species like capuchin monkeys (Sapajus apella: Defolie et al. 2015; Hattori et al. 2007), squirrel monkeys (Saimiri sciureus: Anderson et al. 2010) and spider monkeys (Ateles geoffroyi: Villa-Larenas et al. in press).

One crucial aspect of gestural communication systems that remains largely understudied is the possibility that primates may combine gestures into sequences, to convey novel meaning. In great apes, gestures are usually considered to be part of the same sequence when they are produced by the same individual toward the same partner, within a short timeframe (e.g., up to 1 second: Genty and Byrne 2010; Hobaiter and Byrne 2011b; Tanner 2004; up to 5 seconds: Liebal et al. 2004; Tempelmann and Liebal 2012). With this approach, several studies have provided evidence of sequence production in ape gestural communication (Bard 1992; Genty and Byrne 2010; Hobaiter and Byrne 2011b; Liebal et al. 2004; Tanner 2004; Tanner and Perlman 2017; Tempelmann and Liebal 2012; Tomasello et al. 1985, 1994), revealing significant variation in the number of gestures within a sequence across species and studies (chimpanzees, Pan troglodytes: 1–3 according to Tomasello et al. 1994; 2–5 according to Roberts et al. 2013; 2–11 according to Hobaiter and Byrne 2011b; 2–39 according to Liebal et al. 2004; gorillas, Gorilla gorilla: 2–8 according to Genty and Byrne 2010, and Tanner 2004; orangutans, Pongo abelii: 2–8 according to Tempelmann and Liebal 2012).

Although gestural sequences are relatively common in primates, their function remains a subject of debate. Initially, sequences were considered as syntactic and semantic combinations of gestures (Tanner 2004; Tomasello et al. 1989, 1994), where the initial gesture could also serve as an attention getter (Tomasello and Call 2007). However, quantitative investigations failed to provide evidence to this hypothesis. In great apes, gestural sequences are often redundant repetitions of the same gesture types, which are mostly produced during playful interactions, or when recipients are unresponsive (Genty and Byrne 2010; Liebal et al. 2004; Roberts et al. 2013; Tempelmann and Liebal 2012). Moreover, individuals may often continue to gesture even after being responded, suggesting that the production of sequences may be linked to emotional arousal, rather than intentional communicative intent (Tempelmann and Liebal 2012). Overall, these findings suggest that gestural sequences of great apes are unlikely to be complex syntactic and semantic combinations increasing the effectiveness of communication; in contrast, they appear to be used in an emotionally state of arousal (e.g., in a play context, or after failed communicative attempts) to emphasize rather than alter the meaning of single gestures (Amici and Liebal 2022; Genty and Byrne 2010; Graham et al. 2020; Hobaiter and Byrne 2011b; Hobaiter et al. 2022; Rendall 2021; Tanner and Perlman 2017; Tempelmann and Liebal 2012).

In line with this, studies comparing the occurrence of gestural sequences across individuals show that sequences are more frequently produced by younger than older apes, likely due to an increase in communicative success as individuals grow older and become more experienced (Amici and Liebal 2022; Hobaiter and Byrne 2011b; Liebal et al. 2004). In contrast, it is not clear whether there are sex differences in the probability of producing gestural sequences. For instance, Liebal and colleagues (2004) reported that sequences of ten or more gestures were produced by only two males in the group, whereas Amici and Liebal (2022) found that sequences are more likely to be produced within dyads including at least one male, as compared to dyads that only include females. Nevertheless, males were not more likely than females to produce gestural sequences (Amici and Liebal 2022).

In this study, we aimed to study gestural sequences in an understudied neotropical primate species, Geoffroy’s spider monkeys (Ateles geoffroyi). To date, research on gestural communication in species other than great apes has been quite limited, especially in their natural habitat. However, spider monkeys provide an intriguing model to study gestural communication. First, spider monkeys exhibit high levels of fission-fusion dynamics, residing in social groups that frequently split and merge into subgroups of different size and composition (Aureli and Schaffner 2008; Aureli et al. 2008). These high levels of fission-fusion dynamics have been linked to complex gestural communication, as individuals may require larger and more complex communication systems to effectively cope with the social challenges of dynamic and highly differentiated social relationships (Aureli et al. 2008). Second, the only study on gestural communication in this species has shown the presence of large gestural repertoires, that are used intentionally and accounting for recipients’ attentional state (Villa-Larenas et al. in press).

We hypothesized that, as in apes, gestural sequences would be present in spider monkeys, but they would reflect emotional arousal rather than syntactic and semantic combinations. Based on literature in apes, we therefore predicted that gestural sequences would be mostly produced in play contexts (Prediction 1) and/or continue even after triggering the recipient’s response (Prediction 2). We further predicted that gestural sequences would be more likely produced by males than females (Prediction 3) and by younger than older individuals, as younger individuals are less experienced (Prediction 4). Finally, we predicted that gestural sequences would be more likely directed toward younger than older individuals, as less experienced recipients may be less responsive or less effective in their communication and increase signallers’ arousal (Prediction 5).

Study site and subjects. We conducted behavioural observations in the Otoch Ma’ax Yetel Kooh protected area, situated in the Yucatan Peninsula, Mexico (20° 38’ N, 87° 38’ W). This area is characterized by an undisturbed fragment of semi-evergreen medium forest with trees reaching heights of up to 25 meters, along with successional forest, regenerating forest and various bodies of water (Ramos-Fernández and Ayala-Orozco 2003). The area is inhabited by Geoffroy’s spider monkeys (Ateles geoffroyi), who have been studied in this natural area for over a quarter of a century. The study group was therefore fully habituated to humans, monkeys could be individually recognized using differences in their facial and body traits, and age was known thanks to the demographic records spanning over 25 years.

The group consisted of 54 individuals, including 13 adult females, 10 adult males, 3 subadult females, 1 subadult male, 9 juvenile females, 6 juvenile males, 3 infant females, 8 infant males and 1 infant of unknown sex (see Shimooka et al. 2008, for a definition of the age categories). Out of these 54 monkeys, 42 were observed as focal subjects during the study (see below): we excluded individuals that were born after the study started (N = 2), infants that did not detach from their mother’s body (N = 4), and individuals that appeared infrequently and sporadically during observations, despite belonging to the main group (N = 6). However, all group members could be considered recipients of the gestures. Moreover, one of the adult males was only observed from January 2023, when he joined the group.

Data collection. We collected data during a 6-month period (beginning in October 2022), 5 days a week, from 6.30 to 14.00. The initial fortnight was allocated to train the two observers (EC and SCR) and ensure 80% inter-observer reliability before data collection started. We conducted 10-minute focal animal samples for a total of 1119 focal samples (mean ± SD: 3.7 ± 1.14 hours per focal animal). We selected focal subjects based on a pseudorandomized list that we prepared daily, giving priority to focal subjects that had been more rarely observed. One observer used CyberTracker software to enter the data on a tablet, whereas the other observer dictated the data and video-recorded the focal with a camera (Panasonic FULL-HD HC-V180), maintaining a broad focus on the focal subject to also record the focal’s partners. To identify gestures, we used the ethogram for spider monkeys, which describes 42 different gesture types that monkeys produce across different contexts and modalities (Villa Larenas et al. in press).

Whenever a gesture occurred, we recorded and/or vocally described on camera: (i) the gesture type produced, (ii) the identity of the signaller and (iii) recipient, (iv) the context in which the gesture was produced (i.e., aggression, feeding, foraging, play, resting, sexual behaviour, affiliative interaction, travelling), (v) the recipient’s response, (v) the recipient’s attentional state (i.e., if they maintained direct eye contact with the focal individual, or if their body was facing the focal individual and the focal individual was within their field of vision when the gesture was produced); and (vii) modality of the gesture (see Villa-Larenas et al. in press). We recorded a total of 709 gestures during focal observations: 527 gestures that were produced as part of a sequence (i.e., with less than 3 seconds between two following gestures, and gestures being produced by the same focal individual to the same recipient, in the same context; see Liebal et al. 2004), and 182 that were not produced within a sequence. We selected a 3-second timeframe based on preliminary observations on the same group of spider monkeys, and in line with previous studies on other species that used a timeframe between 1 and 5 seconds (e.g., Genty and Byrne, 2010; Liebal et al. 2004), although we are aware that setting a priori temporal timeframe might have important limitations (see Amici et al. 2022).

Statistical analyses. We conducted statistical analyses using generalized linear mixed models (Baayen et al. 2008) in R (R Core Team, 2020), employing the glmmTMB package (Brooks et al. 2017). We prepared our dataset entering one line for each gesture or gestural sequence (N = 307). We specified the signaller and recipient’s sex, age class (i.e., infant, juvenile, subadult, adult) and identity, observation day, context, and whether it was a single gesture or a sequence. If any of this information was missing (e.g., unclear recipient identification), we excluded those data points before running our model (N = 258). We used this dataset to run a model with a binomial distribution, predicting whether the probability of producing a sequence (1) or a single gesture (0) varied depending on the following test predictors: signaller’s sex, signaller’s age class and recipient’s age class. Context could not be included as test predictor in the model as it led to convergence issues. Finally, we included as random factors the observation day and the signaller’s and recipient’s identities.

We checked model assumptions with the “performance” package (Lüdecke et al. 2021) and the “DHARMa” package (Hartig, 2022), and found no convergence, multicollinearity (max VIF: 1.54; Miles, 2005) and dispersion issues. We ran a chi-square test to compare the full model and the null model, which was identical to the full model but without test predictors. Upon significant difference, we used the drop1 function to determine the significance of the single test predictors. In case of a significant categorical predictor with more than two categories, like signaller’s and recipient’s age, we used the emmeans package to assess the estimates of each predictor level (Lenth, 2020).

Characteristics of gestures and gestural sequences. The largest majority of gestures observed in our study (i.e., 527/709) were part of a sequence. We documented a total of 125 sequences, with the longest one consisting of 18 gestures, but the majority containing only 2 (N = 49), 3 (N = 25) or 4 gestures (N = 19). Only eight sequences occurred more than once: grab-grab pull sequences were the most frequent ones (N = 10), followed by embrace-pectoral sniff (N = 7), push-present climb (N = 3), open mouth-present genitals (N = 2) and slap-grab-grab pull (N = 2). The last three sequences that occurred more than once were simple repetitions of the same gestures (i.e., grab pull, present grooming, open mouth).

Most gestures were observed in the contexts of play (N = 118) and other social interactions (N = 107). Additionally, gestures were noted in the context of travelling (N = 30), sexual behaviour (N = 17), resting (N = 15), aggression (N = 14), feeding (N = 3) and foraging (N = 3). The proportion of gestures produced as part of a sequence (rather than as single gestures) differed across contexts. The highest proportions of sequences were observed in play (73%), aggression (64%) and sexual behaviour (59%), suggesting a prevalent use of sequences in these situations. Conversely, the lowest proportion of sequences occurred in the contexts of travelling (27%), resting (13%), social interactions (9%), feeding and foraging (both 0%).

The proportion of gestures and sequences that received a response was similar, with 88% of sequences and 84% of single gestures receiving a response. However, in the largest majority of sequences that received a response (i.e., 102/110), the response was produced before the end of the sequence, usually after the very first gesture (N = 97). In contrast, only 8 gesture sequences received a response at the end of the sequence. Finally, the probability of producing gestures when the recipient was attentive was 92% in the case of sequences, and 84% for single gestures.

Probability of producing sequences. The full model significantly differed from the null model (GLMM, χ² = 30.81, df = 7, p < 0.001), with signaller’s sex (p = 0.001; Fig. 1), signaller’s age (p = 0.037; Fig. 2) and recipient’s age (p = 0.071; Fig. 3) all having a significant effect on the probability that the focal subject produced a gestural sequence. In particular, sequences were more likely produced by males than females (Fig. 1). Moreover, post-hoc tests showed that the probability of producing sequences was highest for juveniles (mean estimated probability ± SE: 0.55 ± 0.09) and infants (0.40 ± 0.12), and lowest for subadults (0.35 ± 0.24) and adults (0.24 ± 0.07; Fig. 2). Similarly, post-hoc tests revealed that the probability of producing gestures was highest toward infants (0.55 ± 0.11) and juveniles (0.47 ± 0.10), and lowest toward subadults (0.36 ± 0.18) and adults (0.19 ± 0.07; Fig. 3).

Our study provides a first description of gestural sequence use in a wild group of neotropical primate species, Geoffroy’s spider monkeys. Our results largely confirmed our hypotheses. As in apes, gestural sequences were common in spider monkeys and appeared to be triggered by emotional arousal. In particular, gestural sequences were mostly produced in play contexts (in line with Prediction 1) and often continued even after triggering the recipient’s response (in line with Prediction 2). Moreover, gestural sequences were mostly produced by males (in line with Prediction 3) and younger individuals (in line with Prediction 4), mostly toward younger recipients (in line with Prediction 5).

This study provides the first evidence of gestural sequence use in species other than apes. Spider monkeys strongly relied on gestural sequences to communicate. The majority of gestures were incorporated into sequences, which mostly included 2–4 gestures, and up to 18 gestures. However, sequences did not appear to be complex combinations used to convey different meanings to recipients. In line with Prediction 1, and with literature in apes (Genty and Byrne 2010; Liebal et al. 2004; Tanner and Perlman 2017; Tempelmann and Liebal 2012), most gestural sequences were produced in a play context. In particular, the proportion of gestures produced as part of a sequence (rather than as single gestures) was highest in the contexts of play, aggression and sexual behaviour, which are likely to imply higher arousal than contexts like travelling, resting, grooming, feeding or foraging. Also in line with Prediction 2 and with literature on apes (Tempelmann and Liebal 2012), gestural sequences persisted regardless of whether recipients responded, suggesting that they were likely triggered by emotional arousal.

Out of the 125 sequences observed during this study, only three (i.e., embrace-pectoral sniff, push-present climb, grab-grab pull) occurred more than twice and were not mere repetitions of the same gesture type. This suggests that these three specific sequences might be recurrent in the gestural communication system of spider monkeys. In literature, embraces (i.e., monkeys wrap one or two arms around the recipient’s back or shoulder, while facing each other) and pectoral sniffs (i.e., monkeys orient their face and nose toward the recipient’s chest-axilla; Schaffner and Aureli 2005; Villa-Larenas et al. in press) are indeed described as species-specific affiliative gestures that often occur concurrently (Rondinelli and Lewis 1976; Schaffner and Aureli 2005). Both embraces and pectoral sniffs are thought to facilitate the regulation of social relationships in spider monkeys, by reducing the risk of aggression in contexts that are likely to be associated with tension (Schaffner and Aureli 2005; Schaffner et al. 2012), like fusion events and infant handling (Aureli and Schaffner 2007; Rondinelli and Lewis 1976; Schaffner and Aureli 2005; Slater et al. 2009). By implying physical contact and exposing vulnerable body parts to other group members, however, also embraces and pectoral sniffs can entail some risk (Schaffner and Aureli 2005). Therefore, their co-occurrence may be adaptive to increase the likelihood of clearly conveying the sender’s affiliative intention and to prevent aggressive escalations in potentially dangerous contexts.

With regards to push-present climb, there is no literature we are aware of on spider monkeys, but it seems plausible that these gestures co-occur because they may serve a complimentary function, to attract the recipient’s attention before facilitating climbing onto the signaller’s body. Finally, grab and grab pull are defined in a very similar way in literature, as the signaller holding the hand firmly closed over the recipient’s body, but also exerting some force to move the recipient from his position in case of grab pull (e.g., in spider monkeys: Villa-Larenas et al. in press; in chimpanzees: Hobaiter and Byrne 2011). There are therefore at least two reasons why grab and grab pull may often co-occur. First, they might serve a very similar function and thus often be used concurrently in the same situation. Second, top-down classifications might have wrongly considered grab and grab pull as two different gesture types, whereas they might be simple variations of the same gesture type, so that their co-occurrence is rather a repetition than a sequence of different gesture types. To address this issue, it will be essential in the future to use more objective bottom-up approaches to identify gesture types in this species (see Mielke et al. 2023).

Across individuals, the probability of producing gestural sequences varied in line with our predictions. First, in line with Prediction 3, males were more likely than females to produce gestural sequences. These findings are in line with literature on apes. In chimpanzees, for instance, long gestural sequences were only produced by males (Liebal et al. 2004), and sequences were more likely produced in dyads that included at least one male, rather than only females (Amici and Liebal 2022). Male chimpanzees have also been reported to show high levels of persistence and produce long gestural sequences in consort to recalcitrant females – a context which is likely to imply high arousal as compared to other contexts (Hobaiter and Byrne 2011b). Notably, sex differences in the production of gestures in spider monkey appear to be limited to gestural sequences, rather than to single gestures (Villa-Larenas et al. in press). Second, in line with Prediction 4, younger signallers (i.e., infants and juveniles) were more likely than older ones (i.e., subadults and adults) to produce sequences. These results are in line with previous studies in apes (Amici and Liebal 2022; Hobaiter and Byrne 2011b; Liebal et al. 2004), and confirm that gestural sequences are mostly used by inexperienced individuals and become less likely through age, as communication becomes more effective through interactional experience and exposure to others’ gestures (Amici and Liebal 2022; Fröhlich et al. 2018; Hobaiter and Byrne 2011b). Finally, in line with Prediction 5, individuals were more likely to produce gestural sequences toward younger recipients (i.e., infants and juveniles) than toward older ones (i.e., subadults and adults). These results suggest that signallers are more likely to produce sequences when interacting with less experienced recipients, who may be less responsive or less effective in their communication and thus increase signallers’ arousal.

Our study faced several limitations. First, it was based on relatively few observations (i.e., 709 gestures and 125 sequences), so that additional observational effort might allow detecting other recurrent sequences with different properties. However, some studies in great apes have also relied on a comparable number of sequences (e.g., Liebal et al. 2004). In the same line, our study only included one group of monkeys, failing to capture possible intra-specific variation. Second, our study relied on a top-down categorization of gesture types and sequences, which might have failed to faithfully capture the meaning and function of single gestures. Although they have been seldom used in literature (Bard et al., 2019; Mielke et al. 2023), finer-grained classifications based on bottom-up approaches might allow a better identification of gesture types and sequences, and provide different results (Amici et al. 2022). Third, the study of gestural sequences would surely benefit from a multimodal approach, as it cannot be excluded that monkeys rather rely on multicomponent and multimodal combinations of signals to convey novel meanings (Amici et al. 2022). Future studies should address this gap by evaluating whether and how spider monkeys combine gestures, vocalizations and/or facial expressions, and how recipients respond to these sequences. Fourth, it would be interesting to also incorporate physiological measures to assess emotional arousal when individuals produce gestures and gestural sequences. In the wild, thermos-cameras represent a promising non-invasive tool for such investigations (Nieuwburg et al. 2021; Travain et al. 2021). Finally, it would be important to complement our study with observations in captivity, as visibility in the wild might sometimes be limited for arboreal species, and this may have compromised visibility during observations in some contexts (e.g. while travelling).

Overall, our results showed that sequences are recurrent in the gestural communication of wild spider monkeys and that they are likely the result of increased emotional arousal, resembling patterns observed in great apes. These findings provide a first contribution to the study of gestural sequences in monkeys, and confirm neotropical primate species as a valid complimentary model to the study of primate gestural communication.

Ethical approval

The investigation was entirely observational and non-invasive. We obtained official permits to conduct our research by the CONANP (Comisión Nacional de Áreas Naturales Protegidas) and SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales), and received the consent of the Mayan community of Punta Laguna residing in the protected area where the study took place. Our methods adhered to the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Nonhuman Primates and the Code of Best Practices for Field Primatology by the American Society of Primatologists.

Human ethics and consent to participate

Not applicable.

Competing interests

The authors have no competing interests or other interests that might be perceived to influence the results and/or discussion reported in this paper.

Authors' contributions

FA, KL and ML defined the research questions and methods. EC and SCR collected the data, under the supervision of FA and ML. EC analyzed the data and wrote the manuscript with support from FA and feedback from all the other coauthors. All authors reviewed the manuscript.

Funding

ML was supported by the Spanish Ministerio de Ciencia e Innovación (PID2020–118419 GB-I00; PLEISHOATA [PID2021–122355NB-C32]) and the Universitat de Girona (Programa d’Ajuts de Suport a la Recerca del Departament de Psicologia 2023). ML is also a Serra Húnter Fellow, recognized by the Generalitat de Catalunya.

Availability of data and materials

Data will be made available upon reasonable request to the corresponding author.

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Table 1. Results of the generalized linear mixed model run, with estimates, standard errors (SE), confidence intervals (CIs), likelihood ratio tests (LRT), degrees of freedom (df), and p values for each test predictor (marked with an asterisk when significant), with the reference category in parentheses.

TEST PREDICTORS	Estimate	SE	2.5% to 97.5% CIs	*LRT*	df	P
Intercept	-2.87	0.57	-3.99 to -1.75	-	-	-
Signaller’s sex (male)	1.50	0.45	0.61 to 2.39	10.17	1	0.001*
Signaller’s age (infant)	0.75	0.62	-0.46 to 1.96	8.47	3	0.037*
Signaller’s age (juvenile)	1.35	0.49	0.38 to 2.31
Signaller’s age (subadult)	0.53	1.09	-1.62 to 2.67
Recipient’s age (infant)	1.65	0.56	0.55 to 2.74	10.20	3	0.017*
Recipient’s age (juvenile)	1.34	0.52	0.33 to 2.36
Recipient’s age (subadult)	0.88	0.84	-0.76 to 2.51

No competing interests reported.

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Gestural sequences in wild spider monkeys (Ateles geoffroyi)

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