-
- Primate communication relies strongly on the
visual modality, notably through the production
of a wide range of expressive facial signals.
The authors investigated here the facial display
repertoire of a relatively little-studied
cercopithecid species, red-capped mangabeys
(Cercocebus torquatus), and questioned whether
their facial displays were dependent on social
contexts and accompanied by indices of
intentionality. Although the dual intentional
and emotional use of apes' facial expressions
has recently been suggested, the question of
whether monkeys produce facial expressions
intentionally to communicate remains open. They
described 6 facial displays produced by captive
red-capped mangabeys in social contexts. They
are based on movements of the mouth, eyebrows,
and ears, possibly graded in intensity and
produced independently or in combination. They
showed that most of the facial displays were
produced preferentially in specific social
contexts and that repertoires varied with
subjects' characteristics, highlighting the
communicative function of these displays.
Moreover, behavioral markers of intentionality
commonly used in gestural studies were found to
accompany the production of some of the facial
signals observed. Particularly, playful "open
mouth" appeared strongly associated with
intentionality indices, as previously noticed in
ape species. All other facial displays, except
yawns, did not exhibit all defined intentional
indices but were, at least, directed toward a
recipient. Interestingly, yawns presented
different variants of intensity associated
presumably with different social functions.
Altogether, these results emphasize the
communicative function of red-capped mangabeys'
facial displays and provide a basis for further
research on their intentional
communication.
-
- La communication des primates repose
fortement sur la modalité visuelle,
notamment à travers la production d'une
large gamme de signaux faciaux expressifs. Les
auteurs ont étudié ici le
répertoire d'affichage facial d'une
espèce de cercopithécides
relativement peu étudiée, les
mangabeys à tête rouge (Cercocebus
torquatus), et nous nous sommes demandé
si leurs affichages faciaux dépendaient
des contextes sociaux et étaient
accompagnés d'indices
d'intentionnalité. Bien que la double
utilisation intentionnelle et
émotionnelle des expressions faciales des
singes ait récemment été
suggérée, la question de savoir si
les singes produisent des expressions faciales
intentionnellement pour communiquer reste
ouverte. Ils décrivent 6 affichages
faciaux produits par des mangabeys à
tête rouge captifs dans des contextes
sociaux qui sont basés sur des mouvements
de la bouche, des sourcils et des oreilles,
éventuellement gradués en
intensité et produits
indépendamment ou en combinaison. Ils ont
montré que la plupart des affichages
faciaux étaient produits
préférentiellement dans des
contextes sociaux spécifiques et que les
répertoires variaient selon les
caractéristiques des sujets, mettant en
évidence la fonction communicative de ces
affichages. De plus, des marqueurs
comportementaux d'intentionnalité
couramment utilisés dans les
études gestuelles se sont
avérés accompagner la production
de certains des signaux faciaux observés.
En particulier, la "bouche ouverte" ludique est
apparue fortement associée aux indices
d'intentionnalité, comme cela a
été remarqué
précédemment chez les
espèces de singes. Tous les autres
affichages faciaux, à l'exception des
bâillements, ne présentaient pas
tous les indices intentionnels définis
mais étaient, au moins, dirigés
vers un receveur. Fait intéressant, les
bâillements présentaient
différentes variantes d'intensité
associées vraisemblablement à
différentes fonctions sociales. Dans
l'ensemble, ces résultats soulignent la
fonction communicative des affichages faciaux
des mangabeys à coiffe rouge et
fournissent une base pour d'autres recherches
sur leur communication intentionnelle.
- Introduction
- Primate communication strongly relies on the
visual modality (Liebal, Waller, Burrows, &
Slocombe, 2014b; Redican, 1975) through a
variety of gestural and postural signals.
Moreover, compared to other mammals, primates
produce a wide range of expressive facial
movements, owing to their complex facial
musculature (Burrows, 2008; Diogo, Wood, Aziz,
& Burrows, 2009). Facial expressions can
involve movements of the mouth and lips, eyelids
and eyebrows, forehead and ears (van Hooff,
1967; Waller & Micheletta, 2013).
Substantial variations are notable between
primate genera and species regarding facial
mobility (Santana, Dobson, & Diogo, 2014)
and facial expression repertoires (Marler, 1965;
van Hooff, 1967). Thus, the understanding of
visual communication in primate species needs
precise descriptions of their facial expression
repertoire and the context of production as
their communicative signals. Some authors
include facial displays in the gestural domain
(Altmann, 1962; Call & Tomasello, 2007;
Chalmers, 1968a; Dube, 2013; Hesler &
Fischer, 2007; Hinde & Rowell, 1962;
Hostetter, Cantero, & Hopkins, 2001;
Maestripieri, 1997, 2005; Poss, Kuhar, Stoinski,
& Hopkins, 2006; Wolfheim & Rowell,
1972), whereas others consider facial displays
as disen- tangled from gestures owing to
differences in the definitions of signal
intentionality (Byrne et al., 2017; Genty,
Breuer, Hobaiter, & Byrne, 2009; Graham,
Furuichi, & Byrne, 2017; Hobaiter &
Byrne, 2011a; Liebal, Call, Tomasello, &
Pika, 2004; Liebal, Pika, & Tomasello, 2006;
Pollick & de Waal, 2007; Roberts, Roberts,
& Vick, 2014). Indeed, the intentional use
of facial expressions in primates is still a
matter of debate (Arbib, Liebal, & Pika,
2008; Hopkins, Taglialatela, & Leavens,
2011; Slocombe, Waller, & Liebal,
2011).
-
- Nonhuman primates seem to have a voluntary
control of their facial movements, which is
required for the flexible use of facial
expressions. Regarding neuroanatomical data from
humans and great apes, facial expressions are
controlled by both voluntary and emotional
pathways acting in parallel within the facial
motor system that differs from the motor system
controlling limb movements (Cattaneo &
Pavesi, 2014; Mu_ri, 2016; Sherwood, Hollo- way,
Erwin, & Hof, 2004; Sherwood, Hof, et al.
2005; Sliwa, Takahashi, & Sheperd, 2018).
Moreover, some facial expression asymmetries are
associated with attention-getting calls in
chimpanzees, suggesting voluntary control of
these facial movements (Hopkins et al., 2011;
Reynolds-Losin, Russell, Freeman,
Meguerditchian, & Hopkins, 2008). This
possible voluntary con- trol may reveal that
primates could use facial expressions
intentionally as communication signals.
-
- The distinction between intentional
behaviors and intentional communication was
previously addressed by Bretherton and Bates
(1979) in their developmental studies in
children, based on the implication of social
agents within intentional sequences of behavior.
Then, the philosophical stance of intentional
communication as a goal-directed process was
formulated by Dennett (1983), who defined
different degrees of intentionality. The first
degree, as studied in animal communication,
supposes that an intentional signal would be
controlled and produced voluntarily by a
signaler and directed toward a recipient to
trigger the appropriate response by the receiver
(Hobaiter & Byrne, 2013; Roeder &
Gosset, 2001). The goal-directedness
discriminates intentional communicative signals
from mere informative signals, which convey
messages without being voluntarily emitted by
the signaler (Poggi & D'Errico, 2012). One
example of "informative signal" could be
piloerection, which conveys information about
the individual's internal state (Benedek &
Kaernbach, 2011; Dettling, Pryce, Mar- tin,
& Do_beli, 1998) without appearing
voluntarily emitted. Bard (1992) introduced
Bates' definition of intentional communication
to the study of primate communication,
distinguishing intentional communication from
other intentional behaviors in orangutan
mother-infant interactions. In the same line,
several behavioral indices of intentional
communication inherited from child devel-
opmental studies were then applied to nonhuman
gestural studies to assess intentionality (see,
for reviews, Byrne et al., 2017; Leavens,
Russell, & Hopkins, 2005; Liebal, Waller,
Burrows, & Slocombe, 2014c; Schel, Bono,
Aychet, Pika, & Lemasson, 2020; Townsend et
al., 2017). Townsend et al. (2017) recently
gathered these indices in a general framework
implying three main criteria to attribute
intentionality to communicative signals: The
signal has to be directed toward a recipient,
produced to reach a particular social goal, and
has to be followed by a response from the
recipient that is consistent with the goal that
is deduced for the signaler. This last
criterion, related to the communicative value of
the signal (Altmann, 1968; Green, 1975; Marler,
1967), would imply that the signal is followed
by a consistent change in the recipient's behav-
ior, consistency with signaler's intention
corresponding to an ac- ceptance or a refusal of
signaler's goal. Following this framework,
appropriate behavioral markers have thus to
accompany the pro- duction of the signal so that
it could be associated with intention- ality.
These behavioral markers may have validity
limitations to admit a signal's intentionality,
as each of them can also be ex- plained by
unintentional processes, such as learning or
changes in signaler's emotional state (Graham,
Wilke, Lahiff, & Slocombe, 2019; Liebal,
Waller, Burrows, & Slocombe, 2014a). It has
been argued that the more indices observed, the
more we get confidence that the criteria are
fulfilled and so that the signal might be
intentional (Schel, Townsend, Machanda,
Zuberbu_hler, & Slocombe, 2013), considering
that several convergent indices are more likely
to be explained by a single cognitive mechanism
(intentionality) rather than a series of lower
level cognition expla- nations (Byrne &
Bates, 2006; Liebal et al., 2014a; Townsend et
al., 2017). However, these markers have to be
used cautiously when studying animal signals,
with due consideration to all possible cognitive
mechanisms underlying signal production.
-
- A signal is considered as recipient-directed
if it is produced in the presence of potential
receivers (i.e., "socially used") and physically
directed to another individual (Call &
Tomasello, 2007; Leavens & Hopkins, 1998;
Leavens, Hopkins, & Bard, 1996; Leavens,
Hopkins, & Thomas, 2004; Liebal, Pika, &
Tomasello, 2004; Liebal et al., 2014a; Schel et
al., 2020; Tomasello et al., 1985; Tomasello,
Call, Nagell, Olguin, and Carpenter, 1994). To
discriminate socially dependent signals from
others, supplemen- tary indicators should be
taken into account, such as the fact that the
signaler first checked the audience's
attentional state before producing the display
(Genty et al., 2009; Graham et al., 2017;
Hobaiter & Byrne, 2011a; Schel et al.,
2020), at least in case of signals that have to
be perceived on the visual channel. Further-
more, the sensitivity to the attentional state
of the recipient, both regarding the rate or the
modality of the signal, is often studied as an
indicator of intentional use of gestures
(Bourjade, Meguerditchian, Maille, Gaunet, &
Vauclair, 2014; Demuru, Ferrari, & Palagi,
2015; Leavens, Hostetter, Wesley, & Hopkins,
2004; Liebal, Pika, et al., 2004; Maille,
Engelhart, Bourjade, & Blois- Heulin, 2012;
Meunier, Prieur, & Vauclair, 2013; Poss et
al., 2006). The second dimension of intentional
communication, that is, the goal-directedness of
the signal, could be checked by monitoring
response-waiting from the signaler after it
produced the display (Call & Tomasello,
2007; Cartmill & Byrne, 2010; Gra- ham et
al., 2017; Hobaiter & Byrne, 2011a; Liebal,
Pika, et al., 2004; Molesti, Meguerditchian,
& Bourjade, 2020; Pika, Liebal, &
Tomasello, 2003; Roberts et al., 2014; Roberts,
Vick, Roberts, Buchanan-Smith, &
Zuberbu_hler, 2012; Schel et al., 2020; Toma-
sello et al., 1985, 1994). Moreover,
goal-directedness is recognized when the
signaler stops producing the signal once the
presumed goal has been reached, and repeats
and/or elaborates the signals in case the goal
has not been met yet (Cartmill & Byrne,
2007, 2010; Genty, Clay, Hobaiter, &
Zuberbu_hler, 2014; Graham et al., 2017; Gupta
& Sinha, 2019; Hobaiter & Byrne, 2011b;
Hostetter et al., 2001; Leavens et al., 2005;
Liebal, Call, Tomesella, Pika, 2004; Liebal et
al., 2014a; Roberts, Vick, & Buchanan-Smith,
2013).
- Based on these indices, the intentionality
of great apes' com- munication gestures has been
admitted, notably from Tomasello et al. (1994)'s
work on chimpanzee sensitivity to the receiver's
attentional state when gesturing, followed by
numerous field and lab studies on great apes
(see, for reviews, Byrne et al., 2017; Call
& Tomasello, 2007; Liebal et al., 2014c).
Intentional gestures have been explored recently
in monkey species such as macaques (Macaca
mulatta, tonkeana, and radiata, Canteloup,
Bovet, & Meunier, 2015a, 2015b; Deshpande,
Gupta, & Sinha, 2018; Gupta & Sinha,
2019), olive baboons (Papio anubis, Bourjade et
al., 2014; Meunier et al., 2013; Molesti et al.,
2020), red-capped mangabeys (Cercocebus
torquatus, Aychet et al., 2020; Maille et al.,
2012; Schel et al., 2020), squirrel monkeys
(Saimiri sciureus, Anderson, Kuroshima, Hattori,
& Fujita, 2010). However, studies of
potential intentionality markers accompanying
the production of primates' facial expressions
are still rare.
-
- Some observational studies seem to indicate
the social dependency of apes' facial
expressions. The facial expressions of five
gibbon species were shown to last longer when
the signaler and the receiver were facing each
other in social contexts (Scheider, Waller,
On_a, Burrows, & Liebal, 2016). This social
directedness and sensitivity to receiver's
attentional state were also observed in
orangutans (Pongo pygmaeus) playful facial
expressions as they produce more intense play
faces when facing a visually attentive play
partner (Waller, Caeiro, & Davila-Ross,
2015), and in bono- bos (Pan paniscus), who
display this facial expression more during
social than solitary play, and more in the
presence of a visually attentive recipient
(Demuru et al., 2015). Thus, the audience effect
supports the communication function of the play
faces in these species and their
social-directedness may reveal both their emo-
tional and intentional use. Moreover, four of
siamangs' (Sympha- langus syndactylus) facial
expressions, mostly performed in combination
with tactile or visual gestures, were found to
be recipient-directed and accompanied by
response waiting or persistence (Liebal, Pika,
et al., 2004). Assumptions of intentional facial
displays were also made for orangutans (Pongo
pygmaeus), with the same recipient-directedness
and goal-directedness indices found for both
gestures and facial expressions (Cartmill &
Byrne, 2010).
-
- Although observations of apes suggest the
dual intentional and emotional use of facial
expressions, the question whether monkeys
produce facial expressions intentionally to
communicate remains open. To our knowledge, even
though the facial expressions of numerous
catarrhine and platyrrhine monkey species have
been described (e.g., Macaca genus: Hesler &
Fischer, 2007; Hinde & Rowell, 1962;
Maestripieri, 2005; Partan, 2002; Thierry et
al., 2000; gray-cheeked mangabeys: Lophocebus
albigena, Chalmers, 1968a; hamadryas baboons:
Papio hamadryas, Dube, 2013; Talapoins:
Miopithecus talapoin, Wolfheim & Rowell,
1972; capu- chin monkeys: Cebus apella, De Marco
& Visalberghi, 2007; Visalberghi, Valenzano,
& Preuschoft, 2006; Weigel, 1979; and see
comparative studies of Redican, 1975; van Hooff,
1967), there is no evidence that nonhominoid
monkeys produce facial expressions in
association with behavioral markers of
intentional communication, as reported for
gestures. The investigation of this topic is
necessary to fill the gap in understanding both
monkeys' facial signal functions and the
evolutionary history of intentional
communication, which is of prime interest in the
study of language origin (Fro_hlich, Sievers,
Townsend, Gruber, & van Schaik, 2019;
Hauser, 1996; Hauser, Chomsky, & Fitch,
2002).
-
- Here, we investigated the facial display
repertoire of a relatively little-studied
cercopithecid species, red-capped mangabeys
(Cercocebus torquatus), and questioned whether
these facial displays were dependent of social
contexts and accompanied by indices of
intentionality. Red-capped mangabeys are
semiterrestrial primates (Mitani, Call,
Kappeler, Palombit, & Silk, 2012) that
originate from West African rainforest coastal
regions (Cooke, 2012; Gautier-Hion, Colyn, &
Gautier, 1999; Jones & Sabater-Pi, 1968;
Orimaye, 2017). They have colored hair and skin
and white eyelids that contrast with their black
face (see Figure 1), presumably in accordance
with a communication function of facial
expressions (Gautier-Hion et al., 1999; Hill,
1974; Redican, 1975). Their gestural
communication has been described recently (Schel
et al., 2020), and suggests, together with data
on their multimodal inter- actions (Baraud,
Deputte, Pierre, & Blois-Heulin, 2016), a
wide use of visual signals for communication.
Experimental studies highlighted the ability of
red-capped mangabeys to use a learnt begging
gesture intentionally, as a function of visual
attentional state of a human receiver (Aychet et
al., 2020; Maille et al., 2012). Moreover,
spontaneous intraspecific gestures produced by
red- capped mangabeys were associated with
key-markers of intentional communication (Schel
et al., 2020). Thus, we hypothesized that the
intentional use of visual displays as
communication signals by this species would
encompass facial expressions. Our first aim was
to describe the repertoire of facial displays
produced by red-capped mangabeys in social
situations and test how this repertoire depends
on individual characteristics. Moreover, in
accor- dance with a presumed communication
function, we expected that facial displays would
be performed under particular social con- texts,
whereas their production in nonsocial contexts
would con- note a predominant emotional
component underpinning the dis play. Then, we
hypothesized that facial displays would be part
of this species' intentional dyadic
communication, and thus that they would be
accompanied by behavioral markers of
intentionality, similarly to gestures.
-
- Discussion
- This study explored the repertoire of six
facial displays of a captive population of
red-capped mangabeys, and tested whether these
displays were produced socially and accompanied
by indices of intentional communication. This
preliminary assessment of first-order
intentionality in mangabeys' facial displays was
based on behavioral markers similar to those
used in gestural studies, to evaluate whether
signals were (a) directed toward a recipient,
(b) produced in order to reach a specific goal,
and (c) led to a change in the recipient's
behavior (Townsend et al., 2017). The social
condition of mangabeys' facial displays, as well
as the effects of individual characteristics on
the repertoire, supports their communication
function. The playful "open mouth" displays were
produced exclusively in social contexts and in
most cases in the direction of an attentive
recipient, with all defined markers of
intentional communication. We discuss later the
significance of these results regarding the
potential intentionality of these dis- plays,
given the current limitations of the behavioral
method use to assess first-order intentionality
in animal communication (Graham et al., 2019).
Although other cognitive mechanisms may explain
our observations, the present results constitute
a first step to address the potential
intentionality of red-capped mangabeys' facial
displays, particularly the "open mouth."
Although not meeting criteria for goal-directed
signals for all occurrences, other facial
displays ("raise eyebrows," "ears back,"
lipsmacks and "stick tongue out"), except yawns
were at least recipient-directed in most cases.
Finally, yawns seemed not associated with dyadic
communication, and thus did not fulfill the
defined criteria for intentional communication.
Interestingly, these displays presented
different variants of intensity, which were
presumably associated with different
functions.
-
- We described six facial displays produced by
red-capped mang- abeys, which involve movements
of the ears, eyebrows or mouth, and can be
produced in combination or independently one
from the other. One noticeable point of the
present repertoire is the description of unitary
ear displays used socially by red-capped
mangabeys. Although nonhuman primates' ear
musculature is controlled by facial nerves
(Mu_ri, 2016), few studies of facial displays
describe ear movements (but see in rhesus and
long-tailed macaques, Macaca mulatta and
fascicularis: Chance, Emory, & Payne, 1977;
Hinde & Rowell, 1962; Partan, 2002).
Although most facial displays of the repertoire
are discrete, we distinguished variants for two
of them, corresponding to different intensities
of mouth displays. The repertoire size and this
possible gradualness of the morphology of some
facial displays suggest that red-capped
mangabeys' communication relies strongly on
complex visual cues (Dobson, 2012; Freeberg,
Dunbar, & Ord, 2012).
-
- Thus, the "open mouth" displays, highly
related to play con- texts, appeared graded.
Some facial displays are indeed graded signals
that can be associated with different
motivations of the signaler (Marler, 1965; Parr,
Cohen, & De Waal, 2005; Preuschoft & van
Hooff, 1996; Waller & Micheletta, 2013). In
primates, the variants "open mouth fully" and
"half" have been largely de- scribed as playful
facial displays (Chevalier-Skolnikoff, 1994; van
Hooff, 1967). Moreover, subjects' age influenced
the production of "open mouth fully" and "half,"
as younger subjects were in- volved in playful
interactions more frequently and were possibly
more emotionally involved in play than adults
(Demuru et al., 2015). Although primate gestures
are used in variable contexts (Byrne et al.,
2017; Call & Tomasello, 2007; Hobaiter &
Byrne, 2013; Liebal et al., 2014c), the fact
that facial displays are more context-specific
allows us to hypothesize that their function is
to help elucidate the meaning of associated
signals used in multi- modal communication.
These facial displays may act as "meta-
communicative signals" (Altmann, 1967; Bateson,
1955), notably because play might involve
agonistic-like gestures (Demuru et al., 2015;
Palagi, 2008; Waller & Cherry, 2012).
-
- Red-capped mangabeys generally produced
"open mouth fully" and "open mouth half" in
association with all previously defined
behavioral markers of intentionality, and
significantly more in situations when the
receiver was visually attentive. Therefore, our
results on red-capped mangabeys' directed "open
mouth" are con- sistent with previous
observations of great apes. Bonobos' (Pan
paniscus: Demuru et al., 2015) and orangutans'
(Pongo pygmaeus: Waller et al., 2015) homologous
facial displays were suggested to be dependent
on audience attentional state, indicating that
these facial expressions are not an automatic
response to play.
-
- However, we should be careful before drawing
the conclusion that these "open mouth" displays
are produced intentionally, given some
alternative explanations to audience effect. For
instance, the production of "open mouth"
preferentially in front of an attentive
recipient could be the result of a learnt
discrimination. Individuals may be more likely
to produce a facial display in these conditions
because they have learnt that seeing the face of
a recipient is necessary to obtain a response
from their signal (Graham et al., 2019).
Moreover, the social use of "open mouth" and the
sensi- tivity to the recipient's attentional
state cannot rule out an emotional-based
production of these displays. Eye gaze is an
emotional stimulus in primates (Emery, 2000),
and arousal is prone to be higher in the
presence of others compared to alone (Zajonc,
1965). Thus, these factors could induce changes
in the signaler's emotional state, resulting in
the production of the facial expressions.
Besides, observations in apes suggest that the
produc- tion of play faces has a strong
emotional component. This expres- sions can be
observed during bonobos' (Pan paniscus) solitary
play (Demuru et al., 2015), and the example of a
female gorilla (Gorilla gorilla) hiding her play
face (Tanner & Byrne, 1993) suggests that
she was not able to inhibit this facial display,
as it is the case of humans experiencing intense
emotions (Porter, ten Brinke, & Wallace,
2012). We found concomitant markers of other
criteria of intentional communication (i.e.,
waiting for a response from the signaler and
recipient's consistent behavioral response)
accompanying red-capped mangabeys' "open mouth,"
but one particular limit of the present
observations is that "response wait- ing" should
be cautiously interpreted as a goal-directedness
marker per se (Graham et al., 2019; Liebal et
al., 2014a). As a first insight in the
intentionality of facial displays in red-capped
mangabeys, the present framework about
"goal-direction" did not include markers related
to goal-dependent cessation of communication or
persistence and elaboration, because these
aspects of signal's "aboutness" require that the
observer is knowledgeable of the signal function
and thus presumed signaler's intention
displaying it. Thus, we must remain cautious
when concluding about the possible
intentionality of the signals studied, given
that criteria of recipient-directedness and
goal-directedness were both assessed based on
markers related to visual attention only.
Moreover, while analyzing intentionality at the
signal-level, this study did not address yet the
question of interindividual variability in
intentional communicative facial displays. In
this sense, the present results will need to be
supplemented by further investigations of the
goal-directedness of "open mouth fully" and
"half," which pre- sumably corresponds to an
invitation to play or to maintain a playful
interaction. We believe that a multimodal
approach would be beneficial in this regard,
addressing goal-persistence by taking into
account associated vocalizations and
gestures.
- Overall, there are current validity
limitations in the behavioral method used to
assess first-order intentionality in animal
commu- nication (see the abovementioned examples
of other cognitive processes possibly underlying
the behaviors identified as inten- tionality
markers). The framework proposed by Townsend et
al. (2017) has the advantage to be widely
applicable to diverse species and communication
modalities, although it does not permit to
conclude with certainty that signals are
intentionally produced. Graham and colleagues
(2019) suggested some perspectives in light of
this methodological problem, such as
experimentally ad- dress second-order
intentionality (which implies mental-state at-
tribution, see Dennett, 1983), or complete
observational studies with valid measures of
arousal during signal production. Until such
approaches are applicable, behavioral assessment
of first-order intentionality still permits to
gather meaningful information, such as the
present results, which we believe constitute a
first step in assessing the intentionality of
red-capped mangabey facial dis- plays,
particularly for "open mouth."
-
- Other facial displays "raise eyebrows,"
"ears back," lipsmacks and "stick tongue out"
appeared only partially accompanied by defined
behavioral markers of intentionality. However,
these dis- plays were at least
recipient-directed in most of the cases, thus
indicating their communicative function (Call
& Tomasello, 1994; Leavens et al., 1996).
Eyebrow-raising and ears back were exclusively
produced in social contexts, that is, agonistic
and affiliative contexts, respectively, and
mostly directed to a visually attentive
recipient. Lipsmacks were produced more in
social than nonsocial contexts, particularly in
affiliative and grooming situations, but not
more in front of an attentive than an
inattentive recipient, as found for "stick
tongue out." Although lipsmacks' production was
not dependent on recipient's visual attention,
we may hypothesize that this signal can also be
acoustically perceived (as the "audible smacking
sound" produced by macaques: Maestripieri, 2005;
Mae- stripieri & Wallen, 1997), and
therefore visual attention would not be
necessary. We note that most of the above-cited
facial displays described, except "stick tongue
out," were preferentially or exclusively
produced in social contexts. Lipsmacks were
produced in affiliative and grooming contexts,
as found for instance in olive baboons (Papio
anubis: Easley & Coelho, 1991), but also in
nonsocial contexts, especially during
auto-grooming. This enabled us to hypothesize
that lipsmacking may be an automatic response to
grooming actions and, as for nonsocial
production of yawns, might indicate a prominent
emotional component driving the pro- duction of
this facial display.
-
- Yawns, as opposed to the other facial
displays, seem to be disentangled from dyadic
interactions, as even in social contexts we
found almost no signs of recipient-directed use.
The high frequency of yawns in nonsocial context
is in agreement with the hypothesis that yawns
are strongly linked to internal states of the
signaler (Deputte, 1994). Moreover, regarding
their production in social conditions, yawns may
have an informative function, for conspecifics,
on the signaler's emotional state during
agonistic and alarm contexts (Bolwig, 1959;
Deputte, 1994). An interesting point concerning
this particular display lies in the relationship
between its form and function, as red-capped
mangabeys produced different types of yawns,
with regard to mouth opening and teeth uncover-
ing, in different contexts. These variations are
known and characterized for gray-cheeked
mangabeys (Lophocebus albigena: Deputte, 1994),
as well as for macaque species (Macaca fascicu-
laris: Deputte, 1994; Zannella, Stanyon, &
Palagi, 2017), geladas (Theropithecus gelada:
Palagi, Leone, Mancini, & Ferrari, 2009),
and chimpanzees (Pan troglodytes: Vick &
Paukner, 2010).
-
- Yawns of the first type, with mouth less
open, were used only in nonsocial contexts and
might correspond to physiological regulators
during transition between activity and resting
or during feed- ing anticipation (Deputte,
1978). Some yawns of the second and third types,
with mouth more open and teeth more visible were
associated with alarm calls, as described also
for gray-cheeked mangabeys (Lophocebus albigena:
Deputte, 1994), apparently be- cause of high
arousal and social tension. Moreover, yawns of
the third type were mainly produced in agonistic
contexts, as visible canines are hypothesized to
play the role of threat or prethreat (Altmann,
1967; Redican, 1975). Yawns of the third type
were produced more frequently by middle-aged and
old adult males, while individual
characteristics did not affect the production of
yawns of the first type. In our sample, the
males were not equally distributed in the social
groups, most of them living in all-male groups.
However, as sex influenced some variants of
yawns and not the others, we assume that male
group membership did not bias the analysis of
the effect of sex on facial display repertoire.
These results on sex effects are consistent with
the hypothesis of a threat value of the yawns
with visible canines (Leone, Ferrari, &
Palagi, 2015; Zannella et al., 2017),
particularly because red-capped mangabeys
exhibit an important sexual dimorphism in canine
size that becomes evident with sexual maturity
(Deputte, 1986; Hill, 1974). This hypothesis is
supported by similar sexual differences of yawn
production by macaque species (Macaca fuscata
and tonkeana: Zannella et al., 2017), taken that
this difference was not found for primate
species such as lemurs (Propithecus verreauxi
and Lemur catta: Zannella, Norscia, Stanyon,
& Palagi, 2015) or humans (Homo sapiens:
Schino & Aureli, 1989), with absent or
slight sexual dimorphism in canine-size.
Moreover, the age effect on yawn production may
be associated with testosterone level changing
with sexual maturity since testosterone was
correlated with yawn production in rhesus
macaques (Macaca mulatta: Phoe nix &
Chambers, 1982; Robinson, Scheffler, Eisele,
& Goy, 1975; Wallen & Goy, 1977). The
relationship between yawn morpho- logical
variability and function, highlighted by the
contexts of production and by the effect of
individual characteristics, is in agreement with
previous results for geladas (Theropithecus ge-
lada: Leone et al., 2015). In macaques, this was
associated with communication redundancy
observed in species showing more tolerant social
styles (Zannella et al., 2017), which also
exhibit larger meaningful communicative
repertoires (Dobson, 2012).
-
- Moreover, we found no dominance or kinship
effects on any of the facial expressions
displayed, presumably in relation with the
sociality of red-capped mangabeys, which have
been shown to adopt both despotic and
egalitarian behaviors (Dolado & Beltran,
2012). Despite a steep hierarchy within their
groups, red-capped mangabeys have indeed
relatively dynamic dominance relation- ships
(Dolado & Beltran, 2011) with some
propensity to counter- attack, as do tolerant
macaque species (De Waal & Luttrell, 1989;
Thierry, 2007).
-
- Conclusion
- In sum, the repertoire of red-capped
mangabeys' facial displays is composed by six
different displays that could be graded in
intensity. We characterized the social-dependent
production of facial expressions by red-capped
mangabeys, and brought to light behavioral
indices of intentionality accompanying facial
displays. Particularly, playful "open mouth"
appeared strongly associated with some
intentionality indices, as previously noticed in
ape species. We believe that the present
repertoire provides a basis for further research
on function and intentionality of red-capped
mangabeys' facial expressions. As the gestural,
vocal, and facial signals are now described in
this species, we also believe that it will
constitute a useful tool for a multimodal
approach for the study of catarrhine monkeys'
intentional communication, a key feature for
evolutionary research on language origins.
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