Gesture Use in Communication between Mothers and Offspring in Wild Orang-Utans (Pongo pygmaeus wurmbii) from the Sabangau Peat-Swamp Forest, Borneo

Nonhuman great apes’ (hereafter great apes) use of 60–80 gestures in intentional communication remains the only broad system of communication outside of human language in which there is evidence for widespread and flexible use of goal-directed signals to communicate language-like meaning in everyday social interaction (Graham et al.2018; Hobaiter and Byrne 2014, 2017; Moore 2014). Great apes employ diverse repertoires of vocal, gestural, and facial signals to communicate a wide range of nuanced information (e.g., bonobos, Pan paniscus: Graham et al.2017; Pika et al.2005; chimpanzees, Pan troglodytes: Bard et al.2017; Fröhlich et al.2016a, 2016b; Hobaiter and Byrne 2011a, 2011b, 2014; Plooij 1978; Roberts et al.2012; Tomasello et al.1985, 1989; gorillas, Gorilla gorilla: Genty et al.2009; Perlman et al.2012; Pika et al.2003; Tanner and Byrne 1999; orang-utans, Pongo: Liebal et al.2006; cross-species: Bard and Vauclair 1984; Pollick and de Waal 2007). Recently, researchers have started to describe the way in which apes combine their signals; with gestures, vocalizations, and facial expressions, among other signals, employed in a single communicative system. These studies have highlighted the importance of considering communication holistically (Hobaiter et al.2017; Liebal et al.2011; Wilke et al.2017), as well as blurring the boundary between signal categories (e.g., orang-utans’ use of their hands to modify the acoustic properties of some vocalizations: Lameira et al.2013; Peters 2001).

Vocal behavior has been studied across great ape species in both captive and wild populations (e.g., chimpanzees: Crockford and Boesch 2005; Goodall 1986; Hauser and Wrangham 1987; bonobos: Bermejo and Omedes 1999; de Waal 1988; gorillas: Salmi et al.2013; orang-utans: Lameira et al.2015; Wich et al.2012). However, gestural research efforts have focused mostly on the African great apes, with detailed repertoires described for the gesturing of both captive and wild chimpanzees (e.g., Bard et al.2014; Hobaiter and Byrne 2011a; Pollick and de Waal 2007; Roberts et al.2012; Tomasello et al.1985, 1989), bonobos (e.g., Genty et al.2014, 2015; Graham et al.2017; Halina et al.2013; Pika et al.2005), and gorillas (Byrne and Tanner 2006; Genty et al.2009; Pika et al.2003; Tanner et al.2006), while gestural research on orang-utans is limited to a few captive studies (Cartmill 2008; Cartmill and Byrne 2007, 2010; Liebal et al.2006; although cf. Mackinnon 1974 for descriptions of wild orang-utan signals, Bard 1992 for gesture use in free-ranging reintroduced individuals, and Waller et al.2015 for facial displays).

Great apes show substantial flexibility in the production of their signals, for example showing nuanced audience effects in their vocalizations (audience composition: Crockford et al.2012; Schel et al.2013a, 2013b; Slocombe and Zuberbühler 2007) and facial expressions (audience attention: Waller et al.2015). Unlike either vocal or facial signal repertoires, gestural repertoires contain signals with a range of information modalities (e.g., in the case of gesture: audible, visual, and tactile). All vocal and facial signals contain, respectively, either audiovisual or visual information. However, gestural signals offer signalers flexibility in signal selection relative to the visual attention of their recipient. Great apes can adjust their selection of gesture types to take into account other individuals’ ability to receive the information (e.g., Cartmill and Byrne 2007; Cudmore and Galdikas 2012; Hobaiter and Byrne 2011a; Liebal et al.2004a, 2004b; Poss et al.2006; Tomasello et al.1994), including potential eavesdroppers (Hobaiter et al.2017).

Studies of communication in captive great apes have provided unique insights into their cognitive capacities, for example, selecting the appropriate modality for their audience’s visual attention, showing understanding of the physical basis of gestural communication (e.g., Tomasello et al.1985, 1989), and showing understanding of recipients’ knowledge states (Cartmill and Byrne 2007). However, a captive environment impacts the expression of species-typical behavior (e.g., Hobaiter and Byrne 2011a; Seyfarth and Cheney 2017), and can lead to the regular spontaneous production of behavior rarely, if ever, seen in the wild (chimpanzee pointing: Hobaiter et al. 2013; Leavens et al.2005b; tool use in gorillas: Fontaine et al.1995; Lonsdorf et al.2009).

The study of gestural communication in wild orang-utans provides a general point of broader comparison for an exploration of the evolutionary origins of gestural communication. Current estimates place the last common ancestor of the African apes and orang-utans at around 17 million yr. ago (Pozzi et al.2014). However, and of more interest, orang-utans also occupy a very different socioecological niche from that of their African cousins. Communication, like other behaviors, is adapted to the niche of the species employing it (Cheney and Seyfarth 2018). The semisolitary and arboreal niche occupied by wild orang-utans provides a unique point of comparison for the communicative usage of their gestures, as compared to African apes. Chimpanzees and bonobos live in large multimale–multifemale groups of between 20 and > 200 individuals, in a fission–fusion social structure (Aureli et al.2008; Nishida 1968). While gorilla groups are typically much smaller, they also typically include multiple adult males and females, as well as immature individuals (Robbins and Robbins 2018). Play, sex, and display are among the most prolific contexts for gestural communication in wild or captive African apes (Fröhlich et al.2016a; Genty and Zuberbühler 2014; Goodall 1986; Graham et al.2017; Hobaiter et al.2017; Plooij 1978; Schneider et al.2012; Tomasello et al.1997). In contrast, the most regular social partners in wild orang-utans are mothers and their offspring (Mitani et al.1991; van Schaik 1999). While siblings do interact, the long interbirth intervals of 6–8 yr. (Wich et al.2004) limit sibling interactions to the first few years of life, with a large age difference. With no known long-distance audible gestures (cf. chimpanzee drumming: Arcadi et al.1998, 2004), orang-utan signaling outside of mother–offspring is typically vocal (e.g., male long calls: Delgado et al.2009; Mitani 1985). Recent studies have highlighted the importance of early socialization on African ape communication (Bard et al.2014; Fröhlich et al.2016a, 2017; Laporte and Zuberbühler 2011), but the impact of the social environment on the development of wild orang-utan gesture remains unknown.

Their ecological niche presents physical and cognitive challenges that also distinguish them from African apes. Their diet requires the acquisition of complex food-processing techniques (Galdikas 1988; Jaeggi et al.2008; van Adrichem et al.2006; Van Noordwijk and Van Schaik 2005; Wich et al.2004) and their lifestyle is more arboreal (Thorpe and Crompton 2006). As a result, orang-utan hands and feet are employed simultaneously in locomotion more often than seen in African apes (chimpanzees and gorillas: Gebo 1992), perhaps limiting their availability for gesturing.

The socioecological environment of captive orang-utans differs strikingly from those in the wild. They are often housed socially with several adult individuals and offspring (Price and Stoinski 2007). As well as differences in the social partners and behavioral contexts available, the physical environment impacts signal selection and transmission (Hobaiter et al.2017; Mitani et al.1999). Captive habitats are limited in size, but also in form – with typically open enclosures that allow for longer lines of sight and more terrestrial behavior (Hebert and Bard 2000; Manduell et al.2011). As a result, the expression of gestural communication in wild orang-utans may differ substantially from that recorded in captive groups (Cartmill 2008; Cartmill and Byrne 2010; Liebal et al.2006). Given increasing anthropogenic pressures, many populations of wild primates are decreasing in numbers (Estrada et al.2017). As all three species of orang-utan are considered Critically Endangered in the wild (Ancrenaz et al.2016; Goossens et al., 2006; Nowak et al.2017), there is also an urgent need for both research and conservation in their natural habitat.

Here, we provide an initial description of the gestural and vocal signal repertoire used in mother–offspring pairs of wild Southwest Bornean orang-utans. The largely arboreal lifestyle of wild orang-utans may impact both the expression of gestural forms, for example limb use, and the range of gesture types available in a particular interaction. We examine the selection of signals and their adjustment to recipient attention. We further explore the responsiveness of orang-utans to gestural communications and describe the range of goals for which gestures are employed between mother–offspring pairs.

We collected data during focal follows (Altmann 1974) of mothers and dependent offspring orang-utans within the Sabangau peat-swamp forest in Borneo, Indonesia, at the Borneo Nature Foundation (BNF) research site in conjunction with the Centre for International Co-operation in Management of Tropical Peatland (CIMTROP). The study site is a 500-km² protected area known as the Natural Laboratory of Peat Swamp Forest (NLPSF), which is managed by the University of Palangkaraya for the purposes of scientific research. A base camp is located at 2°19′S and 114°00′E, 20 km SW of Palangkaraya. Unlike most forests in Kalimantan, the Sabangau forest is not impacted by high levels of fragmentation, making it one of the largest continuous areas of peat-swamp forests left on the island (Morrogh-Bernard et al.2003). This forest supports the largest population of orang-utans in the world at a density of two or three individuals per km² (Husson et al.2009; Morrogh-Bernard et al.2003; Singleton et al.2004; Wich et al.2008).

This was an observational study that did not contain any interventions. All research adhered to the ethical ASAB/ABS Guidelines for the Use of Animals in Research and followed the IPS Code of Best Practices for Field Primatology. Permission for the study was granted by RISTEK. The authors declare they have no conflict of interest.

Video coding yielded 1299 communicative signals: 858 vocal signals and 441 gestural signals. The majority of signals in our dataset were produced while in the canopy (signaler location canopy: N = 1267, ground: N = 17, unclear N = 15). Where a recipient could be identified, signaling was typically between mothers and infants (N = 412). Signaling between other individuals in our dataset (e.g., siblings, unrelated individuals) was relatively rare (N = 19; see Table SIII). Signals apparently directed toward human observers (N = 295), unknown recipients (N = 530), and other species (N = 41) were excluded from all further analyses.

We found no difference in the proportion of signal types used between adult (N = 7; mean proportion of gestural signals = 32.4% ± SD 22.5, range: 0–58.9) and juvenile signalers (N = 6; mean proportion of gestural signals = 24.3% ± SD 12.8, range: 13.3–49.3; t-test, t = 0.778; df = 11, P = 0.453). There were too few infant or adolescent signalers to compare the use of signal types in these age groups.

Gestural Communication

We recorded 441 instances of gestural signals that met criteria for intentional use. Gestures were produced individually (N = 131), and in sequence with other gestures (N = 30 instances; N = 15 sequences). Twenty-six distinct gesture types were provisionally identified; however, five of these were recorded on only a single occasion, and so do not, so far, meet the criteria for inclusion in individual or species repertoires (Table IV). When plotted cumulatively against the total number of gesture tokens coded, neither the total, nor the individual adult or offspring repertoires reached asymptote (Fig. 1), suggesting that further gesture types remain to be identified. Fourteen gesture types were used by adult female orang-utans, and 22 gesture types by their immature offspring. The gestures ‘Push,” “Protrude lower lip,” “Beckon,” and “Tap” were observed being used only by the adult females; and the gestures: “Swing arm,” “Swing leg,” “Swing object,” “Hand on,” “Dangle,” “Reach palm,” “Throw object,” “Hit object/ground,” “Fling,” “Stomp,” “Object move,” and “Object in mouth” were observed being used only by immature individuals. Signalers were more likely to gesture when the recipient was in close proximity: 84% of all gestures were executed when the recipient was <1 m from the signaler. Gestures carried out when the recipient was 2 or more m away were exclusively silent-visual “Present” gestures.

Table IV

Wild Bornean orang-utan gesture types recorded in this study

Gesture	Descriptiona	#G	#ind	Previously recordedb		Newly recorded
				Captive	Wild	Wild	Any
Beckon	Hand (or footb) moved in a sweep from elbow or wrist (knee or ankle) toward the signaler.	3	1	+ 2		+
Bite	Recipient’s body is held between or against lips or teeth of the signaler.	13	8	+ 1–4		+
Dangle	Signaler hands from arm(s) (or arm and legb) above another; may shake feet/legs.	10	3	+ 1–4		+
Fling	Rapid movement of hand or arm from the signaler toward the recipient.	2	1	+ 1,2		+
Grab	Signaler hand(s) (or foot/feeta) is firmly closed over part of the recipient’s body.	3	2	+ 1,2,5		+
Grab-hold	As “Grab” but contact is held for >2 s.	30	9	+ 1,2		+
Grab-pull	As “Grab” but closed hand(s) (or foot/ft.*) contact maintained and a force exerted to move the recipient from the current position.	26	7	+ 1–4		+
Hand on	Hand—typically palm or knuckles— placed on recipient with contact lasting >2 s.	8	5	+ 1		+
Hit object/ground	Movement of the arm(s) from the shoulder with hard short contact of the palm(s) to an object or the ground.	1	1	+ 1,3		+
Object in mouth	Signaler approaches recipient while carrying object (e.g., small branch) in the mouth.	1	1				+
Object move	Object is displaced in one direction; contact is maintained with the object throughout.	1	1	+ 1		+
Object shake	Repeated back-and-forth movement of an object (held in hand(s) or foot/feeta).	23	5	+ 1–4,6	+ 7
Poke	Firm, brief, push of one or more fingers (or toesa) into the recipient’s body; may be repeated.	2	2	+ 1–2		+
Present body part	Body part is moved to deliberately expose an area to the recipient’s attention.	105	6	+ 1,2,4		+
Protrude lower lip	A facial gesture in which the signaler pushes out just its lower lip while the top lip remains taut, creating an open shelf in the direction of the recipient.	5	2	+ 2		+
Push	Palm (or solea) in contact with the recipient’s body and force is exerted in an attempt to displace the recipient.	4	3	+ 1–4		+
Push— directed	A light short noneffective “Push” that indicates a direction of desired movement, immediately followed by the recipient moving as indicated.	74	7	+ 1–4		+
Reach palm	Arm is extended to the recipient with hand in open, palm exposed position (no contact).	19	3	+ 1,2,5,6		+
Reach wrist	As “Reach palm” but wrist or back of hand extended toward the recipient with the palm in sheltered position.	3	2	+ 1–6		+
Stomp	Sole of the foot/feet is lifted vertically and brought into short hard contact with the surface being stood upon.	1	1				+
Stroke	Stroking another individual with gentle back-and-forth movement of the palm(s) or fingers (or foot/toesa).	13	2	+ 1–6		+
Swing	Large back-and-forth movement of arm(s) or leg(s)a from shoulder (or hip).	41	5				+
Swing (with object)	As “Swing” but signaler holds a detached object in hand/ft.	21	2	+ 8	+ 7
Tapping other	Movement of the arm from the wrist or elbow with firm short rhythmic repeated contact of the fingers to the recipient’s body.	1	1	+ 1,2		+
Throw object	Object is moved and released so that there is displacement through the air after release.	11	5	+ 4,6	+ 7	+
Touch other	Light contact of the palm and/or other body part of the recipient, for <2 s.	14	4	+ 1–5		+

Data were collected in the Sabangau peat-swamp forest in Borneo, Indonesia (2014–2016). Descriptions taken from ¹ Byrne et al. (2017; updated in Hobaiter and Byrne 2017). Example videos are available at http://www.greatapedictionary.com

^aGesture previously described as used by the hand or arm, but here recorded with the foot or leg. #G = number of instances of a gesture’s use; #ind = number of individuals recorded as using gesture type. We note where gesture types were previously recorded in either Captive or Wild groups, or as newly recorded for a wild, or for any group; ² Cartmill (2008); ³ Cartmill and Byrne (2010); ⁴ Liebal et al. (2006); ⁵ Gruber (2014); ⁶ Smith (2009); ⁷ Mackinnon (1974); ⁸Personal observation, A. Knox. Italicized gestures were observed and coded in only one instance

^bRijksen (1978) recorded several gestures from Sumatran orang-utans in the wild, but these were from rehabilitated individuals and have been omitted from this list because of possible human enculturation

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Adults deployed a similar proportion of tactile gestures (N = 6; mean proportion = 54.3% ± SD 23.9, range: 33.3–85.7) as visual (audible or silent: mean proportion = 45.7% ± SD 23.9, range: 14.3–66.7; paired t-test: t = 0.440, df = 5, SE = 0.195, P = 0.679), whereas juveniles employed fewer tactile gestures (N = 6; mean proportion: 13.9% ± SD 16.3, range: 0–37.7) than visual (audible or silent: mean proportion = 86.1% ± SD 16.3, range: 62.3–100; paired t-test: t = 5.44, df = 5, SE = 0.133, P = 0.003). There were too few infant or adolescent signalers to compare the use of modalities in these age groups.

Twenty-one gesture types and 11 call types were identified in the signaling of wild mother and offspring orang-utans in the Sabangau peat-swamp forest in Borneo. All call types had previously been identified, but our ability to discriminate call types was limited by our use of video data and by our focus on mother–offspring communication, and as a result we likely underestimate the call repertoire. In addition to the 21 gestures included in the repertoire, an additional five gesture types were observed on a single occasion. Three of these have been described in the gestural repertoires of captive populations, and the two gesture types new to descriptions of orang-utan gesture use have been described in other ape repertoires (see Table IV and Byrne et al.2017). Our criteria for inclusion as a case of gesture are strict, and can lead to the exclusion of 20–40% of potential cases (e.g., Genty et al.2009; Kersken et al.2018). Given our small dataset we suggest that these gesture types, and others that remained unobserved, would likely meet criteria for inclusion with additional observations, also extending the total gestural repertoire size. Of the gesture types observed, 3 were previously unreported in orang-utans, and 20 were previously unrecorded in wild orang-utans. Eleven of these gesture types were employed with a higher degree of physical versatility than in previous descriptions, for example, the same action being used with the foot or leg, where previously only the hand or arm had been described (e.g., Byrne et al.2017). Combinations of gestural and vocal signals occurred as both simultaneous and sequential combinations, but both forms were rare.

Orang-utan signalers were very responsive to gestural requests, with ca. 90% of all successful communications occurring with either an overlapping or immediate (<1 s) response. This fluid “style” of communication more closely resembles that described for bonobos (Fröhlich et al.2016c), as compared to chimpanzees, where delayed responses (≥2 s) were observed as frequently as more responsive behavior (Fröhlich et al.2016c). Previous studies from both captive and wild groups of apes suggest that apes’ use of gesture is impacted by their early social experience (e.g., Bard et al.2014; Fröhlich et al.2016a, b; 2017; Hobaiter and Byrne 2011b; Schneider et al.2012; Tomasello et al.1989). The extended period of dependency, necessary for orang-utans to occupy a cognitively demanding ecological niche (Galdikas 1988; Jaeggi et al.2008; van Adrichem et al.2006; Van Noordwijk and Van Schaik 2005; Wich et al.2004), as well as their very restricted number of social partners as compared to African apes (Mitani et al.1991; van Schaik 1999), likely influence their understanding of the communicative intentions of their partners, perhaps increasing their responsiveness.

Orang-utans are highly flexible in their use of limbs in order to exploit their arboreal niche (Manduell et al.2011; Thorpe and Crompton 2005, 2006). In comparison with chimpanzee gesturing, we found that orang-utans were more likely to employ leg/ft. forms of gestures that had both a hand/arm and leg/ft. variant, and that orang-utans were more likely to use hand/ft. or leg/arm combinations in gesture forms that involved the use of two or more limbs. As a result, where only the limb use varied from existing descriptions of gesture types in other apes, we were conservative in listing them as variants of the same gesture type, rather than as novel gesture types. While we provide an initial description of gesture types employed by wild orang-utans, our analyses show no asymptote in the repertoire, strongly suggesting that additional gesture types remain to be described. Similarly, while we found low levels of overlap in the gestural repertoires of mothers and their offspring (10 of 26 gesture types), no age-class repertoire reached asymptote, and so further study is needed to properly describe any variation in the use of different gesture types within the repertoire across development. We found that the proportion of tactile to visual gesture types varied between adult and juvenile signalers, with a bias toward visual gestural signal use in younger signalers. Previous studies have found either similar proportions of use (Schneider et al.2012), or a bias toward the use of tactile gestures in infant apes (Fröhlich et al.2016a); however, the use of tactile signals decreased with increasing independence from the mother (Fröhlich et al.2016b; Plooij 1978), and so the variation in our data may reflect the comparison of juvenile, rather than infant, to adult signalers. Furthermore, as our data were collected across a wide range of behavioral contexts, and specific gesture types are associated with specific signaler goals (Cartmill and Byrne 2010; Hobaiter and Byrne 2014), the variation in signal selection may reflect a variation in adult and juvenile signaler goals, rather than a specific shift in modality of gesturing with age. The semisolitary social environment of wild orang-utans not only limits the frequency of social interactions in general, but particularly limits the frequency of contexts, such as play or sexual solicitation, that are among the most prolific for gesture use in wild African apes and captive orang-utans (Cartmill 2008; Fröhlich et al.2016a; Genty and Zuberbühler 2014; Goodall 1986; Graham et al.2017; Hobaiter et al.2017; Plooij 1978; Schneider et al.2012; Tomasello et al.1997). As a result, gestures employed only rarely and gestures associated with goals typically expressed in play or sexual contexts are likely absent from our data.

Supporting previous findings from captive groups (Cartmill and Byrne 2007; Liebal et al.2004a; Poss et al.2006; Waller et al.2015) and across other ape species (e.g., Hobaiter and Byrne 2011a; Leavens et al.2005a; Tomasello et al.1994), orang-utan signalers vary their production of intentional gestures depending on the visual attention of their audience, adjusting the modality of their signal (visual or tactile) to match the visual attention of their recipient (attending or not attending). These findings suggest that apes understand the physical basis of their gestural signals and that the gaze of the recipient is important in successfully deploying a visual gesture. Adjusting signaler behavior to match recipients’ visual attention can be achieved either by moving position so that the visual gesture is produced within the recipient’s line of sight, or by selecting a gesture type that includes information encoded in the auditory or tactile modalities. While evidence for both methods has been found in captive signalers (Liebal et al.2004a, 2004b), we very rarely observed wild orang-utan signalers adjusting the position from which they signaled, instead finding that they employed tactile gestures toward out-of-sight recipients. This bias may reflect the constraints of their arboreal niche, in which repositioning may be more costly than in more open terrestrial habitat typical of captive environments (Hebert and Bard 2000; Manduell et al.2011).

While a much larger dataset is needed to systematically define the gestural meanings of specific gesture types, we could describe the goals for which the orang-utans used their gestures and the relative flexibility of gesture types. Gestures were employed to achieve eight distinct goals, including six positive requests (Acquire object; Climb on me; Climb on you; Climb over; Play change; Play continue) and two negations (Move away; Stop behavior). As found in chimpanzees and bonobos (Graham et al.2018; Hobaiter and Byrne 2014), gestures were employed flexibly toward multiple goals, but the majority of gesture types were used to achieve at least one play-related goal; thus, flexibility decreased (to an average of two goals per gesture type) when play data were removed. These findings suggest that orang-utans also show means–ends dissociation in their gesturing, with individual gesture types used to achieve several distinct goals and several gestures employed to express an individual goal. While there is increasing evidence for signaler control over and intentional use of some ape vocalizations (Crockford et al.2012, 2015, 2017; Schel et al.2013a, 2013b), these tend to be one or two signals each tightly associated with specific information, such as danger or food. Ape gestural communication remains distinct, outside of human language, in the scope and flexibility of the gestural signals and their meanings.

The exploration of gestural communication in wild orang-utans is not straightforward. Orang-utans experience fewer social interactions than other nonhuman ape species (Delgado Jr. and van Schaik 2000; Galdikas 1985; van Schaik 1999). In combination with their arboreal lifestyle in a dense, high-canopy habitat (Thorpe and Crompton 2006), this makes video data collection of communicative signals particularly challenging: almost 700 h of video footage were required to provide even a modest first description. Nevertheless, within this we could provide confirmation of gesture types never previously recorded for orang-utans, and not previously recorded in wild populations, and that some aspects of their gesturing—for example, an apparent difference in the diversity of limb use—may reflect specific adaptations to their natural habitat. Given the rapid decline in orang-utan populations across all species (Davis et al.2013; Goosens et al. 2006; Meijaard et al.2010, 2011; Nowak et al.2017), and the occurrence of cultural variation between groups in their signaling (Lamiera et al. 2013), further research on understudied areas of their behavior, such as their gestural communication, is urgently needed..