# The development of communication in alarm contexts in wild chimpanzees

Guillaume Dezecache, Catherine Crockford, Klaus Zuberbühler

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Guillaume Dezecache, Catherine Crockford, Klaus Zuberbühler. The development of communication in alarm contexts in wild chimpanzees. Behavioral Ecology and Sociobiology, 2019, 73 (8), 10.1007/s00265-019-2716-6. hal-02454678

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# The development of communication in alarm contexts in wild chimpanzees

Guillaume Dezecache¹,²,³ ID • Catherine Crockford⁴ • Klaus Zuberbühler²,⁵,⁶

Received: 1 February 2019 / Revised: 14 June 2019 / Accepted: 19 June 2019 / Published online: 6 July 2019
© The Author(s) 2019

## Abstract

Animals have evolved a range of communicative behaviours in the presence of danger. Although the mechanisms and functions of some of these behaviours have been relatively well researched, comparatively little is known about their ontogeny, including how animals learn to inform social partners about impending danger. In adult chimpanzees, behaviours in response to dangers involve several channels, particularly alarm calls and simultaneous gaze alternations with nearby recipients. Gaze alternations may allow inexperienced individuals to learn from more experienced ones by assessing their reactions to unfamiliar objects or events, but they may also provide the basis for more advanced social referencing. Here, we were interested in the development of these two common behaviours, alarm calling and gaze alternations, in wild chimpanzees (*Pan troglodytes schweinfurthii*) confronted with a threat. Using a cross-sectional design, we investigated those in 8 infant and 8 juveniles by experimentally exposing them to an unfamiliar but potentially dangerous object, a large, remotely controlled, moving spider model. For alarm calling, we found a positive relation with age, starting at around 28 months, although alarm calls were not consistently emitted until after 80 months. For gaze alternations, we found no age effect, with some of the youngest infants already showing the behaviour. Although its function remains unclear in infant and juvenile chimpanzees, gaze alternations emerge early in chimpanzee development. Alarm calling may require more advanced developmental stages, such as greater perceptual abilities, categorical capacities or more sophisticated social cognition, i.e. an understanding that danger is a collective experience that requires communication.

## Significance statement

Alarm calling and other anti-predatory behaviours have been the topic of much research but their ontogenies are still poorly described and understood. Recent studies on the behaviour of wild chimpanzees in threatening contexts have suggested sophisticated social cognitive abilities in adults. How do these behaviours develop in ontogeny? We addressed this question using a field experiment with 8 infants and 8 juveniles exposed to a novel and potentially threatening object in their natural habitat. We found that gaze alternations are present in some of the youngest individuals, potentially revealing early social awareness in chimpanzees. Age did not have an effect on the presence of gaze alternation. We also found that alarm calling was more common in older

Communicated by A. Widdig

This article is a contribution to the Topical Collection An evolutionary perspective on the development of primate sociality – Guest Editors: Federica Amici and Anja Widdig

**Electronic supplementary material** The online version of this article (https://doi.org/10.1007/s00265-019-2716-6) contains supplementary material, which is available to authorized users.

✉ Guillaume Dezecache
guillaume.dezecache@gmail.com

¹ Institut Jean Nicod, Département d'études cognitives, ENS, EHESS, CNRS, PSL Research University, Paris, France

² Budongo Conservation Field Station, Masindi, Uganda

³ Department of Experimental Psychology, University College London, London, UK

⁴ Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

⁵ Institute of Biology, Université de Neuchâtel, Neuchâtel, Switzerland

⁶ School of Psychology and Neuroscience, University of St Andrews, St Andrews, Scotland, UK
individuals, suggesting that call production and context of usage must be learnt. We discuss our results in light of developmental theories of social cognition and the role of social learning in the primate lineage.

**Keywords** Social learning · Social cognition · Alarm calling · Gaze · *Pan troglodytes*

Introduction

As a general rule, developmental patterns of anti-predatory
behaviours appear to depend on a species' life history, with
rapidly maturing species showing fully functional behaviours
earlier than slowly maturing ones (Lea and Blumstein 2011).
One well-studied anti-predator behaviour is 'alarm calling', a
type of signal whose main function is to warn others of the
presence of danger (Zuberbühler 2009; Klump and Shalter
2010). Alarm calls have been documented in many social
animals where they lower the predation risk, not just for the
actor, but often also for other group members (Caro 2005).

Whilst much research has examined its mechanisms and func-
tion, relatively less has been devoted to its development. Here,
the majority of studies has focused on how individuals acquire
appropriate responses to other group members' alarm calls
(reviewed in Hollen and Radford 2009; Lea and Blumstein
2011), with comparably less known about the acquisition of call
production and context-dependent usage. One influential devel-
opmental model has emerged from field observations on free-
ranging vervet monkeys (*Cercopithecus aethiops*). In this pri-
mate, individuals from a very early age produce acoustically
distinct calls, albeit to a much broader set of events than adults.
For instance, less than 12-month old infants can give aerial alarm
calls to geese, pigeons or falling leaves, suggesting that any type
of object from above initially triggers these calls. With experi-
ence, infants then learn to ignore events that do not pose a direct
threat and will eventually only alarm call to a small range of
dangerous predator species (Seyfarth and Cheney 1980). This
developmental process is adaptive insofar as it enables individ-
uals to develop habitat-specific anti-predator responses, whilst
reducing the likelihood of costly false positives (Owings and
Loughry 1985; Lea and Blumstein 2011). Although gradual
changes in alarm call usage during infancy have also been re-
ported in meerkats (*Suricata suricatta*) (Hollén and Manser
2006; Hollén et al. 2008), an alternative developmental model
suggests that age-related differences in alarm calling behaviour
reflect age differences in susceptibility to predation rather than
individual experience (Hollén et al. 2008; Hollen and Radford
2009; Lea and Blumstein 2011).

Chimpanzees (*Pan troglodytes*) produce alarm calls to a
range of disturbances, but previous studies have mainly fo-
cussed on a single class of threats—snakes. Chimpanzees emit
three alarm call types to snakes: acoustically variable hoo
alarm calls (different from hoos in non-predatory contexts;
Crockford et al. 2018) (Schel et al. 2013), waa-barks and

SOS screams (Goodall 1986; Zuberbühler 2000; Crockford and Boesch 2003; Schel et al. 2013; Crockford et al. 2018; Crockford 2019). The current literature suggests that these three call types are not strictly predator-specific, as demonstrated in various monkey species (e.g. Stephan and Zuberbühler 2016) but may reflect the degree of danger. Young chimpanzees show somewhat different vocal behaviours to dangers, by producing ‘hoo’ and ‘whimper’ calls (Plooij 1984; Plooij et al. 2015). Although the vocal behaviour of chimpanzees in threatening contexts has been the topic of much recent research (Crockford and Boesch 2003; Crockford et al. 2018; Crockford 2019), we are not aware of any systematic efforts to investigate the vocal behaviour of immature individuals. In adult chimpanzees, alarm call production is known to depend on a number of social parameters, such as presence of specific group members and their attentional and epistemic states (Crockford et al. 2012, 2017; Schel et al. 2013), suggesting that social competence (i.e. the history of social activities) is critical for the production of alarm calls. It is also undeniable that competence in alarm calling requires more basic cognitive competences, such as the ability to process and correctly identify predators and other dangers.

Another reason why chimpanzees are relevant for develop-
mental studies is that they often complement alarm calling
with conspicuous visual behaviour, gaze alternation, in ways
that suggest awareness of their audience (e.g. Liebal et al.
2013; Schel et al. 2013). For example, adult chimpanzees
can engage in gaze alternation between a danger and other
group members (Schel et al. 2013; Crockford et al. 2017)
often combined with alarm calling. Related to this, they have
been observed to actively position themselves such that they
can maintain visual contact to both the threat and other group
members, a behaviour that has been termed ‘marking’
(Crockford et al. 2017), in line with a social referencing inter-
pretation of gaze alternation (see also for positioning in other
contexts; Liebal et al. 2004). It may function to obtain infor-
mation from more experienced group members, as social
referencing, allowing others to detect the threat (Schel et al.
2013; Crockford et al. 2017; Townsend et al. 2017), or as a
means to establish joint attention, a necessary precondition for
joint action, such as group-level predator mobbing or travel-
ling (Gruber and Zuberbühler 2013). Gaze alternation has
been documented both in captivity (Leavens and Hopkins
1998) and in the wild (Gruber and Zuberbühler 2013; Schel
et al. 2013; Crockford et al. 2017). The alarm behaviour of
chimpanzees may thus be considered to involve multimodal
signals combinations, i.e., the coupling of two otherwise in-
dependent signals using distinct modalities (sensu Fröhlich
and Hobaiter 2018).

In humans, gaze alternation has been studied extensively in
the context of language acquisition, where it becomes frequent
by 9 months. It is said to facilitate joint attention with adults and
as such ease the acquisition of meaning (Carpenter et al. 1998).
The behaviour may also facilitate social learning and provide a
basis for more complex social interactions, such as gaze follow-
ing, social referencing and joint attention (Evans and Tomasello
1986; Baldwin and Moses 1996; Striano and Rochat 2000;
Slaughter and McConnell 2003; Tomasello et al. 2005).

In chimpanzees, gaze alternation has already been seen in
5-month-old infants (Bard et al. 2014) (but see Lucca et al.
2018). More generally, infant chimpanzees are socially re-
sponsive from 1 to 2 months of age (mutual gaze with moth-
er), show sensitivity to gaze direction from 2 months, employ
audience-checking (i.e. gazes at social partners) when produc-
ing communicative signals from 9 months and follow others'
gaze around 12 months of age (see Tomonaga et al. 2004 for a
review; Fröhlich et al. 2018).

Although the presence of gaze alternations is undisputed in
chimpanzees, their function is less clear, particularly in young
individuals. Three competing hypotheses can be spelled out.
One is that gaze alternations are not communicative devices
but momentary shifts of attention driven directly by the envi-
ronment. For example, an individual's focus of attention may
be momentarily disrupted by a novel event but then redirected
back to the original focus. A second possibility (which also
does not imply that their function is communication) is that
gaze alternations allow one individual to check the availability
of social partners. A last possibility is that the function of gaze
alternations is communication, i.e. gaze alternations help di-
rect the attention of audience members to an object worth of
attention. In adults at least, and when interacting with dangers,
gaze alternations appear to fulfil a communicative function
(Schel et al. 2013; Crockford et al. 2017; Townsend et al.
2017), as they are more likely to occur in cooperative contexts,
i.e. when audience members have most to gain (e.g. when
those are not aware of a presence of a threat).

In this study, we were interested in the emergence of alarm
calling and gaze alternation in young chimpanzees exposed to
a threat. We studied the development of both behaviours in
N = 16 young Eastern chimpanzees (Pan troglodytes
schweinfurthii) (N = 8 infants, N = 8 juveniles) of the Sonso
community of Budongo Forest, Uganda. To systematically
examine the development in natural circumstances, we con-
ducted controlled presentations of a model spider. This re-
search contributes to our understanding of the development
of social cognition, as alarm contexts represent situations
where chimpanzees typically recruit their social partners,
using visual and vocal signals (Crockford et al. 2012, 2017;
Schel et al. 2013) and where call production is sensitive to

audience affects due to the presence of kin or bond partners,
especially if they are ignorant of the snake.

Methods

Study site

The study was carried out in the Budongo Forest Reserve, a
moist, semi-deciduous, tropical forest in Western Uganda, cov-
ering 428 km² at an altitude of 1100 m between 1° 35' and 1° 55'
N and 31° 08' and 31° 42' E (Eggeling 1947). Data were collect-
ed on the Sonso chimpanzee community (Reynolds 2005) be-
tween January and April 2017. At the start of the study, the Sonso
community was composed of 35 adults (> 15 years) (24 fe-
males), 7 subadults (> 11 years) (6 females), 14 juveniles (>
4 years) (10 females) and 11 infants (< 4 years) (2 females).

Subjects

In chimpanzees, infancy is marked by physical dependence on
the mother. Weaning begins at around 3–4 years when phys-
ical independence from the mother tends to increase. When
weaned (at around 5 years), individuals are considered to be
juveniles (Reynolds 2005; Laporte 2011). Although they may
frequently travel with their mothers, juveniles gain physical
independence and no longer ride their mothers dorsally, a
behaviour seen in infants by 3 m.

In this study, we included all infants (individuals younger
than 4 years) and juveniles (individuals older than 4 years and
younger than 11 years) that were regularly seen. We were able
to carry out experimental trials with 16 individuals (N = 8
infants; N = 8 juveniles; see Table 1 for details).

Experimental procedure

A mechanical object representing a spider (see Fig. 1a; 10.5 cm
wide; 12 cm long) was presented to elicit alarm behaviour (see
Fig. 1b). Motor-driven leg movements could be triggered by
remote control. In a pilot experiment, we established that adult
chimpanzees perceived the model as potentially hazardous.
Presentation of the spider to four adult males elicited hoo alarm
calls in all. The fact that there are no natural arachnoid species in
Budongo Forest that even closely resembled the model, beyond
its general spider-like physical appearance, was a deliberate de-
sign feature with two advantages. First, since subjects had never
interacted with this particular device, they were unable to rely on
previous experience to make predictions about its behaviour or
potential dangerousness, regardless of age. Second, due to its
unfamiliarity, the potential danger may have been interesting
enough to be worth communicating about. The Sonso commu-
nity occupies a home range that includes a dysfunctional former
sawmill with a hamlet of houses that now serve as the base of the
<table><caption>**Table 1** List of subjects, sex, age (in months) and age class on the day of the experiment and responses: presence of an alarm call and gaze alternation</caption><thead><tr><th>ID</th><th>Sex</th><th>Age (in months)</th><th>Age class</th><th>Alarm call (1 = yes)</th><th>Gaze alternation (1 = yes)</th></tr></thead><tbody><tr><td>MZ</td><td>M</td><td>15</td><td>Infant</td><td>0</td><td>0</td></tr><tr><td>KV</td><td>M</td><td>25</td><td>Infant</td><td>0</td><td>1</td></tr><tr><td>OZ</td><td>M</td><td>28</td><td>Infant</td><td>1</td><td>1</td></tr><tr><td>KO</td><td>M</td><td>29</td><td>Infant</td><td>0</td><td>0</td></tr><tr><td>KF</td><td>M</td><td>36</td><td>Infant</td><td>0</td><td>0</td></tr><tr><td>HM</td><td>F</td><td>40</td><td>Infant</td><td>0</td><td>1</td></tr><tr><td>RY</td><td>M</td><td>41</td><td>Infant</td><td>1</td><td>1</td></tr><tr><td>KJ</td><td>M</td><td>44</td><td>Infant</td><td>0</td><td>1</td></tr><tr><td>HR</td><td>F</td><td>87</td><td>Juvenile</td><td>1</td><td>1</td></tr><tr><td>MB</td><td>M</td><td>97</td><td>Juvenile</td><td>0</td><td>0</td></tr><tr><td>KH</td><td>F</td><td>103</td><td>Juvenile</td><td>1</td><td>1</td></tr><tr><td>RF</td><td>F</td><td>115</td><td>Juvenile</td><td>1</td><td>0</td></tr><tr><td>KB</td><td>F</td><td>122</td><td>Juvenile</td><td>1</td><td>1</td></tr><tr><td>FA</td><td>F</td><td>124</td><td>Juvenile</td><td>1</td><td>1</td></tr><tr><td>KC</td><td>M</td><td>124</td><td>Juvenile</td><td>1</td><td>1</td></tr><tr><td>JS</td><td>M</td><td>129</td><td>Juvenile</td><td>1</td><td>1</td></tr></tbody></table>

Budongo Conservation Research Station (Reynolds 2005). As a consequence, all individuals regularly encounter human artefacts, suggesting that our manipulation was within the natural range of experiences. To avoid habituation, we only performed one trial per subject. As subjects, we only accepted individuals that had never seen the model previously and were not within earshot of previous trials. We also tried to avoid that former subjects witnessed the model a second time as audience members. No human was ever seen interacting with the model by a chimpanzee.

In each trial, the spider was set at around 7 m from potential focal individuals by an experienced field assistant (Sam Adue), provided nearby chimpanzees were not attending. We could elicit detection (defined as a visual inspection of the spider) by remotely operating the model. The detecting infant or juvenile then became the subject. In all but one trial, infants or juveniles detected the spider before other audience members (i.e. individual OZ—see Table 1, detected the spider second, after following the gaze of his mother but nonetheless alarm called before the mother did). We videotaped the behaviour and commented on the focal individual until it moved

away from and could no longer see the spider. We noted all other individuals present within 5, 10, 20 and 30 m of the focal animal and their relative position as left front, right front, right back and left back. Note that, in every trial, there was at least one individual (usually the mother or older sibling) within a radius of 30 m from the subject.

## Data coding and analysis

The presence or absence of the following behavioural elements were coded using BORIS (Friard and Gamba 2016) and Windows Media Player software, from the moment the spider was detected by the focal and up to 10 min after detection: (a) production of alarm call (yes/no), defined as calls resembling the hoo alarm call of adults, albeit sometimes softer. Young chimpanzees also produce whimpers (distress calls) when threatened (Plooij 1984), but those were not considered (see Fig. 2 for examples of alarm and distress calls in juveniles). We also considered (b) gaze alternation (yes/no), defined as alternating gaze between the spider, the direction of

<figure><img src="image_3.png" /><figcaption>**Fig. 1** a The spider model used as unfamiliar, potentially hazardous experimental stimulus. b Usual setting of the experiment: individual OZ (infant) discovering a spider after following the gaze of his mother OK.</figcaption></figure>

He later approached the spider (far right), retreated suddenly and after re-establishing contact with the mother, emitted a soft alarm call
<figure><img src="image_4.png" /><figcaption>**Fig. 2** **a** Alarm call produced by individual JS (juvenile). Alarm call of young individuals resembles hoo alarm calls produced by adults: they are soft, tonal and low in frequency (Schel et al. 2013; Crockford 2019). In adults, repetition rates for hoo alarm calls are relatively slow (Crockford et al. 2018). **b** Series of distress calls produced by individual HR</figcaption></figure>

other group members and back to the spider, with no obvious breaks between gaze shifts (see Crockford et al. 2017).

All measures were coded by GD. Fourteen of the 16 trials were double-coded by an observer blind to the hypotheses. To distinguish alarm calls and whimpers, the double coder was trained on a set of calls before coding the data. We obtained 100% agreement on whether any of the following occurred: (a) alarm calling and (b) gaze alternation between spider and audience (κ = 1). Two of 16 trials (12.5%) could not be completely videotaped due to technical failure. However, both trials could be reconstructed in terms of the sequence of behaviour undertaken by the focal animal due to detailed records provided by the field assistant naïve to the hypotheses.

## Statistical analysis

We conducted logistic regression analyses. The presence or absence of alarm call and gaze alternation was used as dependent variables in two separate models. To check whether age influenced the outcome of the dependent variables, we used age in months as a predictor in our models. To control for unbalanced sex distributions (1 out of 8 infants is a female; 5 out of 8 juveniles are females), we also used sex as an independent variable in our models. We compared full models (including age and sex) to a corresponding null model (sex only), using likelihood ratio tests (LRT) (lrtest function of package lmtest, Version 0.9-36; Zeilis and Hothorn 2002). Age was entered in months. Note that since we only collected 1 trial per individual, ID was not considered as a random effect. We fitted all models in R (Version 3.5.1) (R Core Team 2018) with R Studio (Version 1.1.453) (RStudio Team 2016), using the glm function. Note that the following assumptions were met: the dependent variable in both models is dichotomous (presence or absence of alarm call or gaze alternation), there was linear relationships between the predictor (age) and logit of both outcomes and there were no influential values (i.e. data points with absolute standardized residuals above 3).

<figure><img src="image_5.png" /></figure>

(juvenile). By contrast to hoo alarm calls, distress calls are higher in frequency and are produced at higher rate. Note difference in frequency scale on y-axis for **a** and **b**. The calls presented in **a** and **b** can be listened to at https://bit.ly/2J07yRs and https://bit.ly/2UIId0s, respectively

## Results

### Alarm calling

Age had a positive effect on the likelihood of producing an alarm call (alarm call emission 7 of 8 juveniles (87.5%) vs. 2 of 8 infants (25%); see Table 1; LRT $\chi^2(1) = 5.24$, P = 0.022) with individuals over 80 months more likely to emit alarm calls than younger individuals (Fig. 3).

### Gaze alternation

Age did not have an effect on the likelihood of producing at least one gaze alternation after detecting the stimulus (LRT $\chi^2(1) = 0.25$, P = 0.620) and was common in both infants and juveniles (5 of 8 infants (62.5%) and 6 of 8 juveniles (75%)).

<figure><img src="image_6.png" /><figcaption>**Fig. 3** Alarm calling (y-axis; 1 = yes) as function of age in months (x-axis), with the predicted logistic curve (in red), using the R package popBio (version 2.4.4) and logi.hist.plot function (Stubben and Milligan 2007)</figcaption></figure>
Discussion

Our study examined the ontogeny of anti-predator behaviour in
wild chimpanzees using cross-sectional data. N = 16 individuals
were exposed to a spider model that did not have a natural coun-
terpart in their habitat but represented a generalized type of arach-
noid. In a pilot experiment, the model trigged aversive reactions
in adult males. As predicted, infants and juveniles reacted to the
object in a manner that suggested they considered it to be a threat,
by giving alarm and/or distress calls.

We were interested in the role of age in the development of alarm calling and gaze alternation. We found that older individuals were more likely to alarm call than others, suggesting that, in slowly maturing species, antipredator behaviour can be subject to learning. This may be in contrast to rapidly maturing species, such as certain species of sciurids, where infant anti-predator behaviour appears early and in an adult-like fashion (Lea and Blumstein 2011).

Why was alarm calling not observed more frequently in infants? One hypothesis is that infant chimpanzees can produce alarm calls from early on but that, in our experiment, the motivation to alarm call in younger individuals (who are usually in close proximity to their mothers) could have been hindered. When offspring are physically closer to the mother, a threat may trigger less arousal, or mothers may be more likely to see and react to the threat before the offspring.

Another hypothesis is that young infant chimpanzees do not regularly produce alarm calls because they rely on other vocal strategies, such as distress calling (Plooij 1984; Lingle et al. 2012), in order to devolve any antipredator actions to their mothers. Through development, as the physical proximity between mothers and their offspring increases and the choice of travel parties differs, juveniles are no longer able to rely on maternal assistance and will have to take a more active role when dealing with threats.

Also, the absence of alarm calling in younger individuals
may reflect their inability to produce this particular vocal
structure. Whilst hoo calls are present in the repertoire of very
young chimpanzee infants (Plooij 1984), it remains unclear
whether there exists context-specific hoo call variants as seen
in adults (Crockford et al. 2018).

A last hypothesis is that infants lack the necessary knowl-
edge to engage competently with unfamiliar objects, that is, a
delay in what has been called ‘usage learning’ (Janik and
Slater 2000). Here, the prediction is that young individuals
first need to have experienced others calling in order to cate-
gorize the object as a threat. Although we employed a model
that was equally novel to all individuals (including juveniles),
it is undeniable that older individuals will have more experi-
ence allowing them to make generalizations based on shared
physical features with other dangerous objects.

In environments that are degraded by human presence
(Hockings et al. 2015), traits associated with wariness with

novel objects may be beneficial, especially as many items
associated with human activities (such as snares) represent a
threat to chimpanzees in Budongo and elsewhere (Waller and
Reynolds 2001; Quiatt et al. 2002). In Budongo, chimpanzees
sometimes produce alarm calls upon encountering snares
(Crockford et al. 2012). Flexibility and learning in the usage
of alarm calls appear essential in chimpanzees, a species that
live in a range of habitats, with specific predator fauna.

Our study also looked at the use of gaze alternations in infants and juveniles. For gaze alternation, we used a strict definition requiring that animals engaged in at least three sequential looks (to the spider, to the social partner, and back to the spider), whereas most previous studies typically required only two gazes (Bard et al. 2014). Nevertheless, we found that infants engaged regularly in gaze alternation (> 50% of trials), in contradiction to previous findings, which reported gaze alternation in late juveniles but not infants (Lucca et al. 2018). This highlights the importance of task type (danger vs. food), social partner (conspecific vs. human caretaker), living condition (wild vs. captivity) and behavioural definition of gaze alternation. Our results are more in line with another study that reports frequent gaze alternations by 5 months of age (Bard et al. 2014).

Which function does gaze alternations fulfil in infants and juveniles? In previous work (Schel et al. 2013; Crockford et al. 2017), it was proposed that gaze alternation in chimpanzees is a communicative behaviour, which helps audience members to acquire information about a potential danger in the environment. In our own study, the use of gaze alternation in younger individuals is equally consistent with a non-communicative function. It is indeed possible that gaze alternations help individuals check the availability of social partners for comfort seeking or for gaining information about the threat. By gaze alternating between the threat and audience members, younger individuals may gain information from the reactions of more experienced individuals about the nature of a threat, enabling social learning. This behaviour, in the human literature usually referred to as social referencing (Klinnert et al. 1983) is common and emerges in the first 2 years of life in humans (Walden and Ogan 1988), suggesting that it is evolutionarily old with counterparts in closely related non-human primates. Social referencing interpretations of gaze alternation, audience checking or audience monitoring has been invoked in chimpanzees (Ueno and Matsuzawa 2005), common marmosets (Callithrix jacchus; Kemp and Kaplan 2013), Barbary macaques (Macaca sylvanus; Roberts et al. 2008), domestic dogs (Canis lupus familiaris; Merola et al. 2012) and cats (Felis catus; Merola et al. 2015). In infant chimpanzees, social referencing has also been reported in interactions with human caregivers during exposure to a novel object (Russell et al. 1997). The social referencing hypothesis predicts that infants should look more towards older and mature individuals, including the mother, than younger
and less knowledgeable individuals. A second prediction is
that the subject’s reaction to the threat should be similar to
the social referent’s reaction to the threat.

Another possibility is that gaze alternations in infants
and juveniles are mere shifts in attention allocation caused
by changes in the close environment (e.g. movements of
another individual). Due to the density of the vegetation
and the poor visibility, it is difficult to rule out this hy-
pothesis with confidence. In two trials, however, visibility
was good and there was no sign of movement or any other
behavioural change in the audience that could have
caused the gaze shift.

Regardless of its actual function in infants and juveniles,
we found that gaze alternation is present from an early age in
chimpanzees. Future studies should clarify its function.

Limitations

Our research has provided new insights into the develop-
mental unfolding of social behaviour in a threatening con-
text in wild chimpanzees, whilst still under the care of
their mothers. We found evidence for an effect of age on
alarm calling but little influence of age on the emergence
of gaze alternation, as this behaviour appears to emerge
earlier in development (Bard et al. 2014). However, we
see limitations to this research. Regarding statistical pow-
er, and although our sample size is comparable with other
field experimental studies in great apes, replication in oth-
er sites appears important to secure the effect of age on
the emergence of alarm calling.

Additionally, the sex ratios are not comparable between
the infant and juvenile age classes (m/f infants 7/1 (9/2
possible); m/f juveniles 3/5 (4/10 possible)), to the effect
that any sex-specific developmental differences are un-
likely to be captured by our data. They yet matter, partic-
ularly in chimpanzees (Lonsdorf et al. 2018). Also, gaze
alternation data from individuals younger than 15 months
are missing to further evaluate the ontogenetic trajectory
of this trait. With our methodology, however, it would
probably be impossible to attract the attention of such
young infants before that of the mother, suggesting that
a new study design would be needed.

Another limitation is that we were not able to collect
reliable data on the behaviour of the audience during the
trials. In particular, it would have been very informative
to investigate whether subjects looked more towards in-
fluential, experienced or familiar group members than
other individuals. Mature individuals are more competent
in assessing threat, suggesting that inexperienced individ-
uals should preferentially seek visual contact with such
individuals to gain valuable information. Also, as in other
studies, the presence of kin and bond partners may have

had a strong influence on the motivation to alarm call or
to monitor other’s behaviour (Crockford et al. 2012, 2017;
Schel et al. 2013). Additionally, coding others’ behaviour
could clarify the function of gaze alternations, by
assessing whether gaze alternation promotes correspond-
ing shifts in the attentional state of audience members.

Similarly, it was also not possible to actively keep track of
the behaviour of mothers upon detecting the spider. In pri-
mates, adult behaviour influences infants’ learning of preda-
tors, for example by sanctioning incorrect usage of alarm calls
(Seyfarth and Cheney 1980), but we were not able to system-
atically investigate this here. On the contrary, in order to in-
crease the probability that the focal animal discovered the
object first (detectors are often the first to commit to the role
of alarm caller in chimpanzees), we waited for audience mem-
bers to be as far as possible from the focal (within a limit of
30 m) to start a trial.

Conclusion

Despite its limitations, this study is a first experimental
investigation of the ontogeny of alarm calling and gaze
alternations in wild chimpanzees. It demonstrates that
gaze alternations probably play a role in threat contexts
in chimpanzees as young as 25 months old, although its
function needs to be clarified. Our research also suggests
that recognition of dangerous objects and associated alarm
calling production may be subjected to social learning in
chimpanzees. Finally, and beyond complementing new
and important research on the development of communi-
cation in chimpanzees (Fröhlich et al. 2017, 2018; Lucca
et al. 2018) and the reliance on social learning in the
primate lineage (Maestripieri 2018; Whiten and van de
Waal 2018), it represents a missing piece in an underde-
veloped research area, that of the ontogeny of anti-
predator behaviour.

**Acknowledgments** We would like to thank Associate Editors Anja Widdig and Federica Amici for considering our manuscript. Critical inputs provided by Anja Widdig and two anonymous reviewers have been a great help in improving our manuscript. We would also like to thank the UWA and UNCST for permission to conduct the study and Geoffrey Muhanguzi, Caroline Asiimwe and Sam Adue for their support in the field. GD is indebted to Philippe Schlenker, Emmanuel Chemla and Lucie Ravaux for their financial, intellectual and logistic supports.

**Funding** The Royal Zoological Society of Scotland provided core funding to the Budongo Conservation Field Station. This research was financially supported by FP7-IDEAS-ERC (324115), by the Agence Nationale de la Recherche (ANR-10-LABX-0087 IEC and ANR-10-IDEX-0001-02 PSL) and by the Swiss National Science Foundation (31003A_166458).

**Data availability** The raw data is presented in Table 1.
## Compliance with ethical standards

**Ethical approval** Permission and ethical approval to conduct the study was received from the Ugandan Wildlife Authority (UWA) (permit number: COD/96/02) and the Uganda National Council for Science and Technology (UNCST) (permit number: NS 599). All applicable international, national, and institutional guidelines for the care and use of animals were followed.

**Conflict of interest** The authors declare that they have no conflict of interest.

**Open Access** This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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