Primates (2004) 45:41–57 DOI 10.1007/s10329-003-0063-7
ORIGINAL ARTICLE
Katja Liebal Æ Simone Pika Æ Michael Tomasello Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions
Received: 18 September 2002 / Accepted: 2 September 2003 / Published online: 4 December 2003 Japan Monkey Centre and Springer-Verlag 2003
Abstract The current study represents the first system- Keywords Communication Æ Facial expressions Æ atic investigation of the social communication of cap- Gestures Æ Intentional signals Æ Symphalangus tive siamangs (Symphalangus syndactylus). The focus syndactylus was on intentional signals, including tactile and visual gestures, as well as facial expressions and actions. Fourteen individuals from different groups were observed and the signals used by individuals were Introduction recorded. Thirty-one different signals, consisting of 12 tactile gestures, 8 visual gestures, 7 actions, and Very little is known about the communicative and 4 facial expressions, were observed, with tactile gestures social-cognitive abilities of the various species of smaller and facial expressions appearing most frequently. The apes (Hylobatidae) (Tomasello and Call 1997). Although range of the signal repertoire increased steadily until a variety of studies concerning their complex singing the age of six, but declined afterwards in adults. The behavior exists (e.g., Haimoff 1986; Geissmann 1993), proportions of the different signal categories used there are only a few systematic studies of their com- within communicative interactions, in particular actions municative behavior more generally, or of the ways they and facial expressions, also varied depending on age. might use communicative signals to achieve social goals Group differences could be traced back mainly to social (Fox 1977; Orgeldinger 1999). factors or housing conditions. Differences in the rep- The largest species of the smaller apes is the siamang ertoire of males and females were most obvious in the (Symphalangus syndactylus). On the basis of a compre- sexual context. Overall, most signals were used flexibly, hensive field study, Chivers (1974) concluded that this with the majority performed in three or more social species has a very limited communicative repertoire of contexts and almost one-third of signals used in com- facial expressions and gestures. This conclusion is con- bination with other signals. Siamangs also adjusted sistent with predictions based on ecological, social, and their signals appropriately for the recipient, for exam- cognitive criteria. Thus, siamangs and other gibbons live ple, using visual signals most often when the recipient almost exclusively arboreally in relatively dense vegeta- was already attending (audience effects). These obser- tion. The resulting low visibility would seem by most vations are discussed in the context of siamang ecology, accounts to be more conducive to vocal rather than social structure, and cognition. to visual-gestural communication (Maestripieri 1999). With respect to sensory modalities of signals, gibbon ecology might be most conducive to tactile rather than to visual gestures compared to ground dwelling primates using a variety of visual postures and facial expressions To see video sequences of signals described here, please go to (Hinde and Rowell 1962; van Hooff 1962, 1967; Kummer http://email.eva.mpg.de/liebal/index.html and Kurt 1965). The monogamous social structure of siamangs and other gibbons is also not especially & K. Liebal ( ) Æ M. Tomasello conducive to a considerable repertoire of gestures and Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany facial expressions. The small family groups, consisting E-mail: [email protected] usually of an adult pair and its offspring, are composed Tel.: +49-341-3550422 of only familiar individuals. Thus, Maestripieri (1999) S. Pika proposed, on the basis of his analysis of the gestural University of Alberta, Edmonton T6G2E9, Canada communication and social structure of three macaque 42 species, that primate species in which most social inter- would show very little in the way of gestural commu- actions take fairly predictable forms—for example, nication or facial expressions. However, Fox (1977) and based on rigid dominance structures and wide-ranging Orgeldinger (1999) report a variety of different signals and fixed kinship structures—need very few communi- produced by siamangs observed in captive settings. Both cative signals. On the other hand, primate species in of these studies, however, only documented some ges- which individuals must do much negotiation—for tures and facial expressions as produced by members of example, more egalitarian species with a smaller range of the species in general. Thus, the aims of the current weaker kinship structures—need a wider repertoire of study were: (1) to document all intentional signals used communicative signals. Moreover, siamangs and other by different individuals in several captive groups of gibbons have many relatively predictable social inter- siamangs (S. syndactylus) including adults and their actions, with group members synchronizing their offspring of different age classes, and to document the behavior and engaging in the same activity as much as social context of each signal; (2) to compare those sig- 60–75% of their waking time, which is mainly main- nals and their social function with previous publications tained by observing other group members rather than by of communication in siamangs and other gibbon species, communicating with each other (Chivers 1974). Since to summarize the variety of terms used as a baseline for the monogamous mating system of smaller apes lacks an further research; (3) to establish individual differences in explicit dominance hierarchy but is characterized by a gestural communication with respect to group, age and strong bonding between the adult male and female sex; and (4) to provide some account of the cognitive (Kleiman 1977), the communicative repertoire of siam- processes involved, focusing on flexible use and combi- angs is assumed to be very limited and to contain only nation of those signals and adaptability for specific very simple structured signals (Chivers 1976). communicative circumstances. Finally, what little research there is on gibbon cog- nition has not revealed particularly complex cognitive skills (Tomasello and Call 1997). A number of theorists Methods have opposed the relatively modest cognitive skills of monkeys to the more complex cognitive skills of great Subjects apes (e.g., Byrne 1995; Chadwick-Jones 1998), and by all Subjects were 14 siamangs of four captive groups observed in June appearances siamangs and other gibbons are more like 2000, at the Zoo Krefeld (Germany) and in July and August 2000, monkeys (Grigor eva and Deriagina 1987). This might at the Howletts Wild Animal Park in Bekesbourne (United King- lead to the prediction that social communication of dom). Table 1 shows the individuals according to their affiliation to group and location, along with their age, date and place of birth, siamangs and other gibbons should be more like that of and sex. Following Geissmann (1991), age classes were defined as: monkeys, which means more tactile gestures, fewer infants 0–2 years; juveniles 2–4 years; subadults 4–6 years; and manual gestures, and perhaps less flexible usage overall adults >6 years. Thus, seven adult, two subadult and three juvenile in different social contexts (Tomasello and Zuberbuehler siamangs as well as two infants were observed. Six were males and 2002). Flexibility can be considered in two ways: (1) So- eight were females. Group 1 at the Zoo Krefeld lived in an indoor enclosure mea- called means-end dissociation is the use of a particular suring about 9 m·5.5 m·3 m where it was possible to observe the signal in different functional contexts and/or diverse siamangs during the whole day. Group 2 was housed in an outdoor signals for one functional context. Therefore the sig- enclosure measuring 8 m·4m·3 m with a small indoor area not naling individual uses different means to reach a par- visible to the observer, to which they could retreat at any time. Groups A and B at Howletts Wild Animal Park lived in cages ticular social goal. Those communicative strategies can measuring about 15 m·7m·8 m and 12 m·10 m·8 m, respec- be varied depending on previous interactions with the tively, with access to adjoining sleeping cages. All cages were recipient (Tomasello et al. 1997). (2) The audience effect equipped with stems and branches supplemented by wooden plat- is defined as the sender s sensitivity to the presence/ab- forms and varying ropes and nets. All groups were fed twice a day: once in the morning and once in the late afternoon, with a wide sence of a potential recipient as well as the choice of variety of different types of fruits and vegetables. Foliage, bran- signals depending on the attentional state of the re- ches, or grass were also given as additional enrichments. cipient. To prompt a recipient s reaction, tactile gestures and most of the actions could be performed either to- wards an attending recipient or a non-attending re- Procedure cipient, whereas visual gestures and facial expressions A digital video camera (Sony DCR-TRV900E) was used to record could only cause a reaction if the recipient was already all interactions between the siamangs. Focal-animal sampling attending. Simultaneous and successive combinations of (Altmann 1974) was used to calculate total frequencies of particular signals also seem to represent a possibility for increasing signals and therefore enabled comparisons across individuals, groups, age classes and sex. The total observation time was 10 h for the flexibility of the siamang s signal repertoire. They each of the 14 siamangs. Every focal animal was selected in a may enable the sender to consider previous interactions random order and was videotaped in 15-min bouts. If a subject with a particular recipient and to adjust the signal moved outside the range of vision, the recording was stopped, and depending on the recipient s state of attention as well as if it did not return within 5 min, the next session with a new focal animal was started. Daily observations took place between to force a response by repeating or substituting signals. 7.30 a.m. and 6 p.m. In each zoo, one group was observed in the So for ecological, social, and cognitive reasons, it morning and the other in the afternoon and the next day this order might be expected that siamangs and other gibbons was alternated. 43
Table 1 Location and group affiliation of each siamang Zoo Group Name Date of birth Place of birth Age Age class Sex along with individual features. In every group, parents are Krefeld 1 Ringo ca. 1974 Wild-born ca. 26 years Adult Male shown first followed by their Ellen ca. 1974 Wild-born ca. 26 years Adult Female offspring ordered by age (at the Helge 31 October 1994 Krefeld 5 years, 7 months Subadult Male beginning of the observation Alice 3 May 1997 Krefeld 3 years, 1 month Juvenile Female period). Of group A only the 2 Elvis ca. 1974 Wild-born ca. 26 years Adult Male infant individual was observed Kathrin ca. 1974 Wild-born ca. 26 years Adult Female and is therefore listed without Karen 18 August 1995 Krefeld 4 years, 9 months Subadult Female its parents and siblings Guildo 15 January 1998 Krefeld 2 years, 4 months Juvenile Male Howletts A Xhali 25 March 1999 Howletts 1 year, 3months Infantile Female B Gog ca. 1979 Wild-born ca. 21 years Adult Male Kuku-Gog 23 April 1991 Howletts 9 years, 2months Adult Female Jogog 5 July 1993 Howletts 6 years, 11months Adult Male Agog 17 June 1997 Howletts 3 years Juvenile Female Demagogue 3 May 1999 Howletts 1 years, 3 months Infantile Female
The videotapes were analyzed on a digital video recorder (Sony a. attending, if the recipient had direct eye contact with the sig- MiniDV) with a slow-playback function. All signals sent by the naling individual or if his body oriented towards the sender and focal animal or directed towards it were transferred into a the recipient had him in his field of vision; or spreadsheet-coding scheme. Furthermore, all signals that did not b. not attending, when the recipient s head was turned away from include the focal animal as sender or recipient, but another inter- the sender or if his attention was not directed towards the sen- acting pair of individuals present on the videotape, were also der, but distracted by other social partners or incidents in his recorded. Signals that occurred during an ongoing interaction environment. (e.g. within a play sequence) were not coded. However, if a signal appeared after an interruption of an interaction for at least 5 s it 3. Response of the recipient (within a time interval of 5 s), classi- was included in the further analysis. fied as follows: Intentional communication was defined as a motor act a. No reaction of the recipient; or directed to a recipient via body orientation, eye gaze or physical b. A change of the recipient s state of attention from not attend- contact with the sender expecting a response as evidenced by ing to attending without a further reaction to the preceded looking to the recipient, waiting for a response or persisting in signal; or the communicative interaction (Tomasello et al. 1985, 1994; c. The signal causes a reaction of the recipient, which can be Sarimski 2002). An observed behavior was thus defined as an classified into a particular functional context such as play or intentional signal if it conformed to the following three criteria: aggression. (1) it was observed at least three times over the whole observa- tion period to make sure that it served to reach a recurrent social 4. Functional context: affiliative, agonistic, ingestion, parental goal; (2) it was directed at a particular recipient ( social refer- care, play, social grooming, sexual behavior, singing, and sub- ence ); and (3) it was used flexibly in different social contexts, or missive behavior; signals that could not be connected with a else several signals were all used in the same context [ means-end particular context were labeled as unknown. dissociation Bruner (1981)]. In other words, intentional com- 5. Combinations: a signal could be performed as follows: munication implies that the sender considers the recipient as a social agent and adjusts its communicative mean by augmenta- a. As single signal; or tion, addition or substitution of the signal until the social goal is b. Simultaneously together with another signal at the same time; or obtained (Bates 1979; Bard 1992). Inflexible expressions of the c. As part of a successive combination (=sequence), which was subject s emotional state as well as the stereotyped songs—that is, defined as one sender performing two or more signals towards not accompanied by response-waiting, persistence, or means-ends the same recipient in the same context and within 5 s of one dissociation—were not recorded. another. To label the observed signals, new terms were established to provide an objective description of the communicative behavior instead of applying already existing definitions from other studies. Statistics The signals were classified into three signal categories: For every individual the cumulative number of signals as a function 1. Gestures: expressive movements of limbs or head and body of observation days was plotted to make sure that an asymptote postures; tactile gestures, including physical contact of the was achieved at the end of the observation period, indicating that interacting animals, were distinguished from visual gestures, most probably all signals of each animal s current repertoire were which were distant signals and represented movements of dif- recorded. ferent body parts or specific body postures. To assess the reliability of observations, the observer coded all 2. Facial expressions: expressive movements of different parts of videotapes and 20% of the data were coded by a second person. the face, such as mouth, lips and eyes, were classified as a special Cohen s kappa was used to measure their agreement in the defini- kind of visual signal. tion of signals, which was 0.71 [ good level of agreement (Altman, 3. Actions: as opposed to gestures, actions did not represent a 1991)]. particular, delimited expressive movement or body posture, but Because of the small sample size of 14 individuals, only non- rather a complex series of movements for which it was not parametric tests were applied. All tests were two-tailed and a possible to determine which particular component of this series null-hypothesis was rejected at an alpha-level of 5%. If not was initiating a recipient s response. described differently, medians of individual performance were For every recorded signal the following was coded: calculated. For group comparison, only three of the four groups were considered, because in Group A only the infant was ob- 1. Focal animal, sender, recipient. served, reflecting only a part of the whole group s communicative 2. Attention state of the recipient, defined as repertoire. 44
In determining the distribution of signals, the degree of con- – Slap: sender hits the recipient with a flat hand, rarely cordance of the signal repertoire was analyzed within each group as with a foot, at any body part. well as between groups, applying Cohen s kappa as described in Bakeman and Gottman (1986) and Tomasello et al. (1997). To measure within-group agreement in signal performance, the median Visual gestures kappa was calculated for each dyad of individuals based on the total number of signals that each individual performed and how many of them were also present in the other individual s repertoire – Direct positioning: sender positions himself close to in the compared dyad. Finally these median kappas were divided the recipient without touching him, but following by the number of dyads within this group. Analogously, between- him slowly but closely ( hot on his trail ) in case the group kappas were calculated out of all median kappas between recipient is moving away. each individual of one group and each individual of the other group and divided by the number of all dyads between the two groups. – Jerking body movements: sender hangs in front of the The Wilcoxon test was applied to compare each individual s med- recipient and moves the body up and down by angling ian kappa within group and with members of the other group. his arms repeatedly; this can also be performed in a Spearman s correlations were used to analyze the degree of sitting position with the sender supporting his body by relationship between two different variables. Friedman tests were putting his arms on the ground in front of him and applied to compare more than two variables followed by Wilcoxon tests for pair-wise comparison in case the Friedman test found producing the same jerking body movements by significant differences. Mann-Whitney U-tests were used to analyze bending his arms. two independent variables. – Offer body part: sender lies down on his belly in front of the recipient or offers another body part for grooming; sometimes the sender sits with his body Results oriented towards the recipient and lowers his head as an invitation for grooming (rare). Signals observed – Present genitals: sender sits or is hanging in front of the recipient and raises his posterior to present his Thirty-one different intentional signals were identified genital region. across individuals. This pooled signal repertoire con- – Extend arm: sender extends his arm towards the tained 12 tactile and 8 visual gestures, 7 actions, and recipient. 4 facial expressions. These signals are listed below (with – Shake object: sender shakes an object. a short description), according to signal category. – Throwback head: sender moves his head with a short movement repeatedly back and forth. – Wrist offer: sender approaches the recipient with ex- Tactile gestures tended arm and offers him his bent wrist by holding it in front of the face of the recipient. – Embrace: sender approaches recipient frontally or laterally and puts one or two of his arms around the body of the recipient. Actions – Embrace with feet: sender seizes the recipient ventrally or dorsally with both legs. – Biting: sender bites the recipient on any body part; as – Formal bite: sender touches recipient with its open opposed to the formal bite this is not just a hinted mouth on any body part and bites it with a low intensity. signal but is performed with higher intensity. – Gentle touch: sender touches the social partner softly – Bluff-chase: sender runs towards the recipient, stops with hand or foot on any body part. suddenly and bluffs a forward motion without run- – Hold tight: sender seizes the hand or foot of the re- ning away but waiting for the recipient to follow. cipient. – Chasing: sender approaches the recipient by rapid – Nudge: sender touches the recipient by a fast move- brachiation or running. ment of hand or foot; as opposed to slap , nudge is – Jump at: sender jumps at the recipient or drops on not the flat hand, but single fingers or a fist are used. him out of a hanging position. – Pull: sender grasps any body part of the recipient by – Somersault: sender tumbles towards the recipient. hand or foot and then performs a short, forceful – Swinging: sender hangs in front of the recipient and movement with it. rocks his body to and fro with rapid movements. – Push: sender pushes any body part of the recipient – Wrestling: sender approaches the recipient and starts with a short, vigorous movement away. to tussle with him; this action can be accompanied by – Rub under arms: sender touches the recipient, who biting or slapping and is performed in a lying, sitting turns his back towards the sender, under his arms and or hanging position. moves his hands along the lateral trunk up and down. – Rub with feet: sender touches the bottom or back of the Facial expressions recipient with his feet and moves them gently to and fro. – Shake body part: sender seizes arm or leg of the re- – Grin: mouth of the sender is slightly opened and the cipient and moves it to and fro with short, vigorous corners of the mouth are withdrawn with the teeth movements. scarcely visible between the lips. 45
– Mouth-open: this graduated facial expression occurred (324), nudge (308) or gentle touch (255), were also in a wide variety depending on the extent of opening the frequently used as opposed to rub under arms (4) and mouth; to deal with this situation only two variations embrace with feet (12). Offer body part was the most have therefore been distinguished: frequent visual gesture (211). The most common actions were jump at (329) and wrestling (315). • – Mouth-open half: mouth is opened slightly, so that the canine teeth are almost completely covered by lips; the shape of the mouth is oval with the corners Individual differences of the mouth withdrawn very little. • – Mouth-open full: mouth is opened to the full extent Table 3 shows the distribution of all signals among with the canine teeth and the palate visible. individuals and the total number of signals used by each individual. None of the 14 individuals showed the en- – Pull a face: upper and lower jawbones are closed; the tirety of the 31 observed signals. The size of individual lips are protruded and slightly opened, forming an signal repertoires ranged from 12 to 21 different signals; elliptical shape. the median number of signals used out of the total repertoire was 16 (51.6%). Some signals, such as the tactile gestures gentle touch , nudge , pull , and slap as Comparison with other studies well as the facial expression mouth-open full were dis- played by all siamangs, whereas shake body part or Table 2 provides a summary of the variety of terms used extend arm were used by few animals. Other signals, for some signals including the results of the present study such as wrist offer or direct positioning , were per- and other studies of wild and captive siamangs in formed by only one individual. comparison to other gibbon species. This is supplemented Table 4 shows, for each signal, the proportion of by the functional contexts the signals were used for. individuals that performed it as a function of the total Most of the signals observed in the present study number of siamangs as well as group, age class and sex. were also described in other studies concerning sia- mang s social behavior (Fox 1977; Orgeldinger 1999). The majority of signals observed in siamangs was also Group differences found in white-handed gibbons (Carpenter 1940; Ellefson 1967; Baldwin and Teleki 1976; Palombit There was no signal that was shown by all individuals of 1992). Differences became obvious when comparing one group, but not in other groups. The somersault was studies of captive and wild siamangs. For example, a only observed in Group 2 because of the tendency of its number of signals observed in captivity, such as grab , members to include the ground in their play activities slap or kick , were not observed in wild siamangs. (Table 4). Direct positioning in Group B was related to Furthermore the wrist offer and extend arm found in agonistic interactions because of the group composition the present study were not described in other publica- containing two adult males. Wrist offer was used by tions. The very few facial expressions of both siamangs only one subadult individual of Group 2 in the sub- and white-handed gibbon were often labeled using a missive context, e.g., after aggressive interactions with number of different terms (Ellefson 1967; Baldwin and her parents or when she was approaching them. Teleki 1976; Chivers 1976; Fox 1977; Palombit 1992). To analyze whether the signal repertoire was more Even for the agile gibbon (Hylobates agilis) a corre- uniform within a group than between groups, a Cohen s sponding open mouth stare and grimace were kappa was calculated. Kappas within groups were sim- described (Gittins 1979). The very few other signals ilar to those between groups (Table 5) and represented a known for this species seem to be arise from the lack of general good level of agreement (Altman 1991) sug- studies compared to siamangs and white-handed gib- gesting that the same degree of a relative concordance bons. among individuals existed both within and between groups. The comparison of each individual s median kappa Distribution of signals with all of its group members with its median kappa with each member of another group yielded no signifi- A central concern was to describe differences in the cant differences (values for the Wilcoxon test were number of signals used by individuals, and whether there Z=)0.314, P=0.753, n=13). were systematic differences as a function of social groups, age classes, or sex. Age differences
Frequency In terms of age differences (Table 4), there were some signals performed only by adults, such as the facial A total of 3,655 signals was observed. Table 3 shows expressions grin and pull a face as well as the tactile that the most common signal was the facial expression gestures embrace with feet , rub under arms , and rub mouth-open full (667). Tactile gestures, such as pull with feet , which are all signals used in the sexual 46 Table 2 Signals used by siamangs in the present study in comparison to other publications concerning siamangs as well as other gibbon species. For each signal, the corresponding reference and its functional contexts are shown. Underlined references indicate studies on captive individuals. Signals are ordered alphabetically within their corresponding signal category
Siamgang (Symphalangus syndactylus) White-handed gibbon (Hylobates lar) Agile gibbon (Hylobates agilis)
Liebal, Pika and Tomasello Other authors Signal (reference) Functional Signal Functional context (reference) context Signal Functional Signal [translation] (reference) Functional context context
Tactile gestures Embrace Affiliative, Frontal embrace (Fox 1977) Nursing/ Embrace (Carpenter 1940) Greeting grooming carrying infant Embrace (Palombit 1992) Affiliative Embrace (Ellefson 1967) Submissive Umarmen [embrace] Reassurance, Embrace (Baldwin and Teleki 1976) Vocalizing, (Orgeldinger 1999) greeting arousal Embrace (Palombit 1992) Affiliative Formal bite Agonistic, Gehemmt Beißen [inhibited bite] Play, nursing, grooming (Orgeldinger 1999) sexual Gentle touch Play, affiliative Kurzzeitig beru¨ hren [short touch] Play, aggressive, Touch (Baldwin and Teleki 1976) Play (Orgeldinger 1999) affiliative Hold tight Play, agonistic Festhalten [hold] (Orgeldinger 1999) Play Holding (Ellefson 1967) Play Nudge Play Grab (Fox 1977) Play Pull Play, grooming Heranziehen [pull] (Orgeldinger 1999) Play Push Grooming, Wegstoßen [push] (Orgeldinger 1999) Play Push (Ellefson 1967) Play agonistic Shake body Play Shaking (Fox 1977) Play part Slap Play, agonistic Slap, kick, jerk, hit (Fox 1977) Play, agonistic Slap, cuff (Baldwin and Teleki 1976) Play Schlagen [slap] (Orgeldinger 1999) Play, aggressive Hit, kick, jerk (Ellefson 1974) Play Strike (Baldwin and Teleki 1976) Agonistic, play Visual gestures Jerking body Sexual, play Upward thrusts (Palombit 1992) Sexual movements Ruckartiges Ko¨ rperbewegen Play, sexual, [jerking body movements] follow (Orgeldinger 1999) Offer body Grooming Anbieten des Ko¨ rperteiles Grooming Lowering head (Ellefson 1967) Grooming Present Grooming part [offer body part] (Gittins (Orgeldinger 1999) 1979) Present (Palombit 1992) Grooming Body present (Baldwin Grooming and Teleki 1976) Present (Palombit 1992) Grooming Present Sexual, Genitales pra¨ sentieren Sexual, Posterior present (Baldwin Reassurance genitals submissive [present genitals] reassurance and Teleki 1976) (Orgeldinger 1999) Present genitals (Fox 1977) Aggressive Genital present (Baldwin Sexual and Teleki 1976) Sexual crouch (Baldwin Sexual, and Teleki 1976) submissive Sexual crouch (Ellefson 1967) Sexual Throwback Play Kopf hochreißen [throwback head] Follow, sexual Head tilt (Baldwin and Teleki 1976) Play, travel head (Orgeldinger 1999) Throwing back head (Carpenter 1940) Antagonistic Facial expressions Grin Sexual, play Grimace (Fox 1977) Reassurance Grimace (Baldwin and Teleki 1976) Fear, Grimace Appeasement uncertainty (Gittins 1979) Grimace/bare-teeth (Palombit 1992) Appeasement Grimace (Ellefson 1967) Submissive Angespanntes Grinsen [grin] Play, submissive, Grimace/bare-teeth (Palombit 1992) Appeasement (Orgeldinger 1999) arousal Mouth-open Agonistic, Intense open-mouth threat Open-mouth toward (Ellefson 1967) full grooming (Fox 1977) Staring open-mouth face Open-mouth threat (Palombit 1992) Aggression Open mouth Aggression (Chivers 1976) stare (Gittins 1979) Open-mouth threat (Palombit 1992) Aggression Gerichtetes Drohen [Directed threat] Aggression (Orgeldinger 1999) Mouth-open Agonistic, Mild open-mouth threat (Fox 1977) half grooming, play Relaxed open-mouth face (Chivers 1974) Pull a face Grooming, Schnute [pull a face] Sexual sexual (Orgeldinger 1999) Actions Biting Play, Biting (Fox 1977) Play, antagonistic Bite (Baldwin and Teleki 1976) Play, agonistic agonistic Beißen [bite] (Orgeldinger 1999) Play, aggressive Chasing Play, Chasing (Fox 1977) Play Chase (Baldwin and Teleki 1976) Play, agonistic agonistic Verfolgen [pursue] (Orgeldinger 1999) Play, aggressive Chase (Ellefson 1974) Aggressive Pursue (Fox 1977) Play, antagonistic Jump at Play Anspringen [Jump at] Play, aggressive (Orgeldinger 1999) Somersault Play Purzelbaum [somersault] Play (Orgeldinger 1999) Somersault (Fox 1977) Play Wrestling Play Wrestling (Fox 1977) Play Grapple (Baldwin and Teleki 1976) Agonistic Rough-and tumble (Palombit 1992) Play Grapple (Ellefson 1967) Play 47 48
Table 3 Distribution of signals among individuals (arranged in alphabetical order), total number of signals per individual depending on signal category and total frequency of each signal
Agog Alice Dema- Ellen Elvis Guildo Gog Helge Jogog Karen Kathrin Kuku- Ringo Xhali Frequency gogue Gog
Tactile gestures Embrace X – X X X X – X X – X X X – 32 Embrace with feet – – – – – – X – – – – – X – 12 Formal bite X X – X X X X X X X X X X – 84 Gentle touch X X X X X X X X X X X X X X 255 Hold tight – X – X X – X X X – – – X – 23 Nudge X X X X X X X X X X X X X X 308 Pull X X X X X X X X X X X X X X 324 Push X – X X – X X X X – – X – – 45 Rub under arms – – – – – – – – X – – – – – 4 Rub with feet – – – – – – – – X – – – – – 6 Shake body part – – – – – X – X – – – – – – 3 Slap X X X X X X X X X X X X X X 242 Total for tactile gestures 1,338 Visual gestures Direct positioning – – – – – – – – X – – – – – 26 Jerking body movements – X – – – – – – – X X X – X 32 Offer body part X X X X X X X X X X X X – X 211 Present genitals – – X – – X – – – X X X – – 43 Extend arm – – – – – – – – – – – X X – 5 Shake object – X – – X X X X – X X X X X 60 Throwback head X – X – – X – – – – – X – X 63 Wrist offer – – – – – – – – – X – – – – 7 Total for visual gestures 447 Actions Biting X X X – – X – X X X – X X X 82 Bluff-chase X – – – – X – – – X – – – – 23 Chasing X X X – – X X X X X X – X X 85 Jump at X X X – X X X X X X X – X X 329 Somersault – – – – – X – – – X – – – – 5 Swinging X X X – – X – – – X – – – X 34 Wrestling X X X – X X X X X X – X X X 315 Total for actions 873 Facial expressions Grin – – – – X – X – X – – – – – 5 Mouth-open half X X X X X X X X X X X X X – 315 Mouth-open full X X X X X X X X X X X X X X 667 Pull a face – – – X – – – – – – – X – – 10 Total for facial expressions 997 Total of signals 17 16 16 12 14 21 16 17 19 19 14 18 16 14 context. Furthermore only adults performed the visual facial expressions with increasing age, whereas the gestures direct positioning and extend arm .Incon- number of actions declined (for facial expressions, trast, young siamangs showed a wider repertoire of values for Spearman s correlation were rs=0.758, actions used primarily in the play context. Shake body P=0.002, n=14; for actions, rs=)0.783, P=0.001, part , bluff-chase and somersault were observed in n=14). subadults and juveniles, but not in adults and infants. With respect to functional context, Fig. 2 shows the Furthermore infants did not use gestures such as for- median number of signals used depending on the age mal bite or hold tight . Figure 1 shows, for each age class of the sender. There was a significant positive class, the total number of signals as well as the number correlation between age and the number of signals used of tactile and visual gestures, actions and facial in agonistic context (for the agonistic context, Spear- expressions calculated as medians out of all individuals man s correlation values were rs=0.878, P<0.001, per age class. No correlation was found between the n=14). For the sexual context this correlation was total number of signals and age classes (for Spearman s marginally above significance level (rs=0.528, P=0.052, correlation, rs=)0.153, P=0.602, n=14). The number n=14). In contrast, a significant negative correlation of signals increased from 15 in infants to 17 in juveniles was found with respect to play context (for Spearman s and 18 in subadults and dropped to 16 in adult siam- correlation, rs=)0.670, P=0.009, n=14), where the angs. However, when considering signal categories median number of signals decreased from 13 in juveniles there was a positive correlation between the number of to 7 in adults. 49
Table 4 Use of each signal as proportion of all individuals and of individuals per group, age class and sex. For each signal category, the pooled numbers of different signals for each group, age class and sex are shown
Signal category Individuals Groups Age classes Sexes
(n=14) Krefeld 1 Krefeld 2 Howletts B Infantile Juvenile Subadult Adult Male Female
Tactile gestures Embrace 71.4 75 75 80 50 67 50 85.7 83.3 62.5 Embrace with feet 14.3 25 0 25 0 0 0 28.6 33.3 0 Formal bite 85.7 100 100 80 0 100 100 100 100 75 Gentle touch 100 100 100 100 100 100 100 100 100 100 Hold tight 50 100 25 40 0 33.3 50 71.4 83.3 25 Nudge 100 100 100 100 100 100 100 100 100 100 Pull 100 100 100 100 100 100 100 100 100 100 Push 57.1 50 25 100 50 66.7 50 57.1 66.7 50 Rub under arms 7.1 0 0 20 0 0 0 14.3 16.7 0 Rub with feet 7.1 0 0 20 0 0 0 14.3 16.7 0 Shake body part 14.3 25 25 0 0 33.3 50 0 33.3 0 Slap 100 100 100 100 100 100 100 100 100 100 Total number of tactile gestures 12 10 9 11 6 9 9 11 12 8 Visual gestures Direct positioning 7.1 0 0 20 0 0 0 14.3 16.7 0 Jerking body movements 35.7 25 50 20 50 33.3 50 28.6 0 62.5 Offer body part 92.9 75 100 100 100 100 100 85.7 83.3 100 Present genitals 35.7 0 75 40 50 33.3 50 28.6 16.7 50 Extend arm 14.3 25 0 20 0 0 0 28.6 16.7 12.5 Shake object 71.4 75 100 40 50 33.3 50 71.4 83.3 62.5 Throwback head 35.7 0 25 60 100 66.7 0 14.3 16.7 50 Wrist offer 7.1 0 25 0 0 0 50 0 0 12.5 Total number of visual gestures 8 4 6 7 5 5 5 7 6 7 Actions Biting 71.4 75 50 80 100 100 100 42.9 66.7 75 Bluff-chase 21.4 0 50 20 0 66.7 50 0 66.7 50 Chasing 78.6 75 75 80 100 100 100 57.1 83.3 75 Jump at 85.7 75 100 80 100 100 100 71.4 100 75 Somersault 14.3 0 50 0 0 33.3 50 0 16.7 12.5 Swinging 42.9 25 50 40 100 100 50 0 16.7 62.5 Wrestling 85.7 75 75 100 100 100 100 71.4 100 75 Total number of actions 7 5 7 6 5 7 7 4 7 7 Facial expressions Grin 21.4 0 25 20 0 0 0 42.8 50 0 Mouth-open half 92.9 100 100 100 50 100 100 100 100 87.5 Mouth-open full 100 100 100 100 100 100 100 100 100 100 Pull a face 14.3 25 0 20 0 0 0 28.6 0 25 Total number of facial expressions: 4 3 3 4 2 2 2 4 3 3
Table 5 Concordance of signal repertoires: Cohen s kappas within sexual context, whereas females initiated a copulation and between the three groups through visual gestures such as jerking body move- Group Within Between ments and throwback head , although the latter was displayed from young siamangs of both sexes (Table 4). 12BIt might be that the function of this gesture depended on age: young siamangs used this visual signal to ini- 1 0.65 – 0.65 0.66 tiate play or to get the attention of their parents, 2 0.65 0.65 – 0.65 B 0.66 0.66 0.65 – whereas adult females displayed the throwback head as a sexual solicitation. With regard to facial expres- sions, grin was only performed by males, as opposed Sex differences to pull a face observed only in females.
Sex differences were obvious in the higher number of tactile gestures used by males (for the Mann-Whitney Functional context U-test, Z=)2.700, P=0.005, n=14). For example, embrace with feet , rub with feet and rub under arms The use of signals was analyzed with respect to how were tactile signals used exclusively by males in the often they were performed within the nine different 50
Fig. 1 Total of signals and numbers of tactile gestures, visual gestures, actions and facial expressions shown as medians of all individuals according to their age class
Fig. 2 Median number of signals used in the different functional contexts depending on age
functional contexts, calculated as medians of individual Differences in the proportion of signal categories proportions. Most of the interactions took place in the performed were obvious between age classes. There was play context (51.9%) whereas the grooming and ago- a positive correlation between increasing age and the use nistic contexts were represented in 19% and 12.7%, of facial expressions, whereas the use of actions respectively. All other contexts occurred in less than 5% decreased with age (for actions, Spearman s correlation (in 4.2% of the cases it was not possible to identify the gave rs=)0.894, P<0.001, n=14; for facial expressions context of the interaction). rs=0.875, P<0.001, n=14). Figure 3 shows that infants and juveniles communicated most often by actions (46.9% and 40.4%, respectively), but in particular Signal category infants only rarely used facial expressions (2.4%). Subadults interacted mostly by tactile gestures (35.5%), Individuals performed tactile gestures (36.9%) and facial whereas adults most often used facial expressions expressions (32.1%) significantly more often than visual (38.1%) but only rarely engaged in actions (3.6%). gestures (13.0%) (for the Friedman test v2=12.367, With respect to functional context, tactile and df=3, P=0.006; for the Wilcoxon test for tactile visual gestures were typically used within play behavior gestures versus visual gestures, Z=)3.296, P=0.001, (19% and 11.2%, respectively). Facial expressions were n=14; for facial expressions versus visual gestures observed most often in the context of grooming (35.3%) Z=)2.229, P=0.03, n=14). Actions were performed in whereas the majority of actions (94.6%) were performed 19.2% of all interactions. in the play context. 51
Fig. 3 Proportions of signal categories used depending on age class. Since median proportions are shown, percentages per age class do not add up to 100%
Flexibility of use performance, a significantly higher number of signals was used in play behavior compared to each other One signal in different functional contexts functional context except agonistic behavior (for the Friedman test, v2=68.046, df=8, P<0.001; in the Wil- For every signal, its proportional distribution across the coxon test, P<0.05 for all pair comparisons other than functional contexts was calculated (Table 6). Nine sig- agonistic behavior). nals (29.0%) were observed in only one context whereas all other signals were used in at least three or more State of attention functional contexts. Embrace with feet , rub under arms , rub with feet and grin were only observed Figure 4 shows the percentage of signals the sender within sexual behavior, whereas shake body part , performed when the recipient was either attending or not bluff-chase and somersault were exclusively used in a depending on the signal category. play context. Direct positioning was related to ago- Individuals used visual gestures and facial expres- nistic interactions and wrist offer only to the submis- sions almost exclusively towards an attending recipient sive context. In contrast, gentle touch ,and nudge as (98.2% and 96.6%, respectively). Tactile gestures were well as mouth-open full occurred in all functional performed towards an attending recipient in 66.9% of contexts. cases, whereas actions were used in 70.2% of the time Considering medians of all signals per category, facial when the recipient was attending. The comparison of expressions were used in a significantly higher number of medians of individual proportions of signals directed different contexts (6.5) than tactile (5) and visual ges- towards an attending versus a non-attending recipient tures (4) as well as actions (3) (for the Friedman test, revealed that all signal categories were performed 2 v =23.537, df=3, P<0.001; for the Wilcoxon test for significantly more often towards an attending facial expressions versus tactile gestures, Z=)2.506, recipient (for the Wilcoxon test for tactile gestures, P=0.012, n=10; for facial expressions versus visual Z=)2.731, P=0.006, n=14; for visual gestures Z=)3.32, gestures Z=)3.239, P=0.001, n=14; for facial expres- P=0.001, n=14; for facial expressions Z=)3.299, sions versus actions Z=)2.949, P=0.003, n=11). Fur- P=0.001, n=14; for actions Z=)3.297, P=0.001, thermore, tactile gestures were used in a significantly n=14). Here, visual gestures and facial expressions higher number of contexts than visual gestures and were directed significantly more often towards an actions (for the Wilcoxon test for tactile gestures versus attending recipient than tactile gestures and actions visual gestures Z=)2.721, P=0.006, n=14; for tactile (for the Friedman test, v2=32.644, df=3, P<0.001; for gestures versus actions Z=)2.059, P=0.04, n=10). the Wilcoxon test for visual versus tactile gestures, Z=)3.296, P=0.001, n=14; for visual gestures versus actions Z=)3.061, P=0.002, n=12; for facial expres- One functional context with different signals sions versus tactile gestures Z=)3.296, P=0.001, n=14; for facial expressions versus actions Z=)3.110, When analyzing the use of different signals within one P=0.002, n=13). functional context, in general most of the 31 signals were observed within play behavior (77.4%) followed by sexual and agonistic behavior (61.3% and 58.1%, Combinations respectively). The lowest number of six signals (19.5%) was used within the submissive and singing context, Both simultaneous and successive combinations were respectively (Table 6). When considering individual investigated with regard to the number and categories 52
Table 6 Proportional distribution of signals across functional contexts. For each signal, the total number of contexts in which it was used as well as the total number of signals performed in each context is shown
Affiliative Agonistic Grooming Ingestion Parental care Play Sexual Singing Submissive Unknown Total number of contexts (unknown excluded)
Tactile gestures Embrace 40.5 6.2 12.4 9.4 3 3 25 6 Embrace with feet 100 1 Formal bite 2.6 37.2 29.5 3.8 11.5 2.6 3.8 8.9 7 Gentle touch 14.5 8.4 31.2 4.0 6.0 24 5.6 0.4 0.4 5.6 9 Hold tight 8.8 17.3 69.6 4.3 3 Nudge 12.7 12.1 8.4 0.7 3 45.5 4.4 2.0 4.4 7 9 Pull 3.7 7.4 21.3 2 1.8 52.6 1.3 0.6 8.7 8 Push 2.3 27.3 50 2.3 9.1 2.3 2.3 4.5 7 Rub under arms 100 1 Rub with feet 100 1 Shake body part 100 1 Slap 4.2 21.1 1.7 5.0 62.1 0.4 3.3 2.1 7 Visual gestures Direct positioning 100 1 Jerking body 3.2 6.5 32.3 58.1 4 movements Offer body part 0.5 89.5 0.9 4.2 0.9 3.7 5 Present genitals 9.4 2.3 81.3 7 4 Extend arm 33.3 33.3 33.3 3 Shake object 1.7 5.2 1.7 82.2 6.9 1.7 5 Throwback head 3.2 1.6 3.2 84.1 6.3 1.6 5 Wrist offer 100 1 Actions Biting 7.3 3.7 85.4 3.7 3 Bluff-chase 91.3 8.7 1 Chasing 10 1.2 88.7 3 Jump at 4.4 0.3 0.3 92.5 2.9 4 Somersault 100 1 Swinging 5.9 2.9 84.7 5.9 3 Wrestling 1 0.6 97.7 0.6 3 Facial expressions Grin 100 1 Mouth-open full 0.2 50.9 33.7 3.6 0.3 7.1 0.5 0.3 0.3 2.4 9 Mouth-open half 1.6 36.3 34.4 3.5 1.3 16.6 0.6 5.7 7 Pull a face 9.9 50.2 39 3 Total number 16 18 16 11 10 24 19 6 6 of gestures
Fig. 4 Performance of signal categories shown as median proportions depending on the recipient s state of attention 53 of signals combined. For successive combinations, the state of the recipient and whether he responded or not choice of signal category was analyzed depending on were known. Two patterns were possible: (1) the sender the recipient s state of attention and whether he repeated the same signal or (2) chose a different signal of responded or not. It was expected that in case there the same or another signal category as the second signal. was no response to the first signal, the sender would Here, the latter behavior seems to indicate a higher choose a different signal more often than simply degree of flexibility assuming that the sender tries to repeating the same signal again. vary the signal to force a response instead of simply repeating the same signal. Therefore it was expected that Simultaneous combinations the sender would choose a different signal more often than simply repeating the same signal in case the The number of simultaneous combinations recorded recipient did not respond to the first signal. (197) represented 5.8% of all interactions. The two Overall, the sender repeated the same signal in 38.9% combined signals could either belong to the same or of the interactions and chose a different signal of the different signal categories, but most frequently a tactile same or another signal category in 61.1%, representing gesture was performed together with a facial expression medians of individual proportions. If the recipient (67.5%) as well as an action combined with a facial responded to the first signal, as was the case in 32% of expression (28.9%). A response of the recipient was successive combinations, no significant differences were caused by 65.1% of all simultaneous combinations of a found between proportions of repetitions compared to tactile gesture with facial expression and 84.5% of the choice of a different signal (for the Wilcoxon test, action with facial expression . Those values were similar Z=)1.505, P=0.132, n=13). In contrast, if there was to the median proportions of response to single tactile no response to the first signal, the sender chose a dif- gestures (64.4%) and single actions (84.0%). ferent signal significantly more often than repetitions of the same signal (for the Wilcoxon test, Z=)2.983, Successive combinations P=0.003, n=14).
The number of successive combinations (=signal sequences) recorded (355) represented 26.5% of all Sender-recipient-interactions as a function of age observed signals. Figure 5 shows that the sender most often combined two signals (74.6%) followed by It was of interest to determine which age classes inter- sequences of three signals (18.0%) and four signals acted with each other and who was acting as sender and (4.5%). Combinations of five and more signals mostly recipient, respectively. In general, only 5.7% of all represented single instances. The highest number of interactions within one group took place between adults, successively combined signals was nine. A simultaneous whereas most interactions occurred between the combination was part of a sequence at the same time offspring. With respect to functional context, 65.9% of in 9.6% of all successive combinations, mostly in a all agonistic interactions occurred between adults in combination of two signals (79.4%). Group B because of the presence of two adult males, as To examine types of signal combination, the sender s opposed to only 13% and 6.5% in Groups 1 and 2, behavior depending on the recipient s response to the respectively. In the context of grooming, most interac- first signal was investigated. Of the total of 355 succes- tions were also observed between adults (Groups B and 2) sive combinations, 309 were included where both the or between an adult and subadult individual (Group 1).
Fig. 5 Proportion of successive combinations as a function of the number of signals combined 54
In the play context, interactions between adults were was reacting towards aggressive behavior—primarily either not observed (Groups 1 and 2) or were very rare from her mother—by performing the wrist offer . (1.4% in Group B). In all groups, most interactions She also used this gesture when she approached her within this context took place between young siamangs, father who still seemed to be an important social with the youngest offspring acting more frequently as a partner for her. sender than its older sibling. Although interactions in In siamangs, the offer body part was the most fre- the sexual context were only rarely observed in Groups 1 quent visual gesture, primarily used in the context of and 2, there was a wide variety of interactions between grooming; in most instances the sender would lie down different ages classes, in particular in Groups 2 and B. on his belly in front of the recipient and therefore offer Only 18.6% and 46% of sexual interactions, respec- his back for grooming. In contrast, white-handed gib- tively, were observed between adults. Hetero- as well as bons initiate grooming by taking up a sitting position homosexual interactions between siblings were more and then lowering the head (Ellefson 1967), something frequent, in contrast to some rare sexual interactions that was only rarely observed in the present study. The between the adult male and its offspring (of both sexes) visual gestures present genitals , jerking body move- in those two groups. ments and throwback head were signals performed by females to initiate copulation. In contrast to adults, young siamangs used the jerking body movement and throwback head to initiate play or to get the attention Discussion of their parents. Orgeldinger (1999) referred to the use of present genitals in conflict situations, which was also This study is the first systematic analysis of the social observed in the present study. After agonistic interac- communication of siamangs that considers both quali- tions with her mate, the female used this signal as a tative and quantitative aspects of their signal repertoire. reassurance gesture. Fox (1977) described this signal as The results clearly show that siamangs have a multi- the subadult daughter s reaction to aggressive behavior faceted and variable signal repertoire of several tactile of her father directed towards her, whereas no special and visual gestures as well as some more complex gestures serving to initiate copulation between the actions and a few facial expressions. adults were observed. Orgeldinger (1999) suggested that Siamangs performed a variety of different tactile females use visual signals to invite their partner to mate, gestures, which formed the most frequently used signal whereas males immediately start with pelvic thrusts or to category in general, although this varied depending on mount females without using any particular signals. age. Fox (1977) also observed slaps , kicks , and jerks Palombit (1992) observed upward thrust , which was in agonistic and play behavior. For white-handed gib- only performed by female siamangs. For white-handed bons (H. lar) gestures such as touch , strike , slap and gibbons Ellefson (1974) and Baldwin and Teleki (1976) cuff have been described as different tactile gestures described a sexual crouch gesture as invitation for (Baldwin and Teleki 1976). Embrace was also observed mating which was also used as a humility gesture by Fox (1977), who named it frontal embrace , which between young and adult siamangs, or subordinate and occurred in the context of nursing or carrying between dominant individuals, respectively. They also mentioned the infant and an adult siamang, whereas Orgeldinger a head tilt used in the play context resembling the (1999) described it as a reassurance and greeting gesture. throwback head observed in the present study. Palombit (1992) observed a rare, stereotyped embrace With respect to facial expressions, both variants of between adults. Ellefson (1974) considered embrace as mouth-open face in the present study have often a submissive signal of an individual when approaching a been mentioned in the literature, although they have dominant one. Baldwin and Teleki (1976) mentioned the been named in many different ways. Fox (1977) same signal, but extended its meaning as a reassurance described a mild and intense open-mouth-threat , gesture. respectively, whereas Chivers (1976) mentioned a A very noticeable visual gesture was the wrist offer relaxed open-mouth face and staring open-mouth performed by one subadult individual to her parents face . For white-handed gibbons Ellefson (1967) during aggressive interactions. This gesture, not previ- described an open-mouth-toward . Different descrip- ously described for siamangs, is an important signal tions have been used for the grin expression: some in the communicative repertoire of chimpanzees: authors mention a corresponding grimace , functioning approaching a dominant individual with an extended as a signal of reassurance (Fox 1977), whereas it was arm and offering the back of the flexed hand is an observed only in play and sexual context in this study. expression of submissiveness and serves as a reassur- Baldwin and Teleki (1976) described a grimace for ance gesture in conflict situations (Goodall 1986). In white-handed gibbons as an expression of fear or the present study the wrist offer of the subadult uncertainty, whereas Ellefson (1967) mentioned it in siamang was observed in the same context. Since the context with submissive behavior. As in this study, peripheralization of the maturing daughter—a natural Orgeldinger (1999) observed the pull a face performed prelude to the emigration of the oldest offspring of its by females in the context of sexual behavior, but here natal group—had already started, the young siamang it was also performed in the grooming context. 55
Actions such as chasing , biting and wrestling have expressions and tactile gestures were used most flexibly. been observed in both siamangs (Chivers 1974) and Furthermore, a variety of different signals was used white-handed gibbons (Baldwin and Teleki 1976). Pal- within play and also within agonistic and sexual ombit (1992) described a rough-and-tumble behavior to behavior. This suggests that the signals were used in a initiate play. In contrast to the highly arboreal wild flexible way and do not represent stereotyped behavior siamangs, captive individuals of the present study linked to a particular social context. sometimes involved the ground in play or grooming Combinations of signals may represent a possible sessions. Therefore somersault was only observed in way to increase the flexibility of a limited signal reper- captive siamangs (Orgeldinger 1999). toire and to create new functions or meanings by com- With respect to the qualitative aspects of signal rep- bining different signals. In the present study, facial ertoires, both siamangs and white handed gibbons seem expressions were most often performed simultaneously to use very similar gestures and facial expressions. Since with either tactile gestures or actions. Those combina- most of the existing studies focus on those two species it tions elicited responses in similar proportion to singly would be very interesting to see if a similar signal rep- performed tactile gestures and actions. It seems that ertoire is also representative for other species of smaller facial expressions were combined with those signals to apes, reflecting their uniform social structure and arbo- increase the likelihood of a recipient s response, since real lifestyle characteristic. single facial expressions caused a response less than 50% The current study is the first that systematically of the time. Another explanation might be that facial documented which individuals used which signals. expressions are involuntary displays accompanying Therefore it was possible to identify differences in signal gestures that express the emotional state of the recipient use as a function of group, age, and sex. In terms of (Caldecott 1986). However, their flexible use in most of group, all differences could be traced back to one of the the social contexts in the present study seems to support following: housing conditions (e.g., using the ground in their intentional nature. Although combinations con- play activities); special social situations (e.g., process of taining facial expressions as well as simultaneous com- peripheralizing subadults); atypical group composition binations of two signals were not considered in the study causing agonistic interactions; or the pregnancy of the of Tomasello et al. (1994), they found that chimpanzees adult female and the consequent low number of sexual combined gestures successively in about 30% of com- interactions. In terms of age, there was an increase in municative interactions, similar to siamangs in the tactile gestures as well as in facial expressions with age. present study. Also, sequences consisting of two signals Adults also used a higher number of visual gestures than were most frequently used in both species, but siamangs their offspring, but performed a lower number of ac- performed fewer repetitions of the same signal compared tions, mainly because they rarely engaged in playful to chimpanzees. Nevertheless, successive combinations interactions. The increase in facial expressions in adults seemed to emerge because there was no response after can be explained by the use of grin and pull a face , the first signal, and the sender therefore persisted in both gestures observed primarily in the sexual context signaling; this resembles findings for chimpanzees between adults. Considering the total number of signals, (Liebal, in preparation). This is supported by the fact there was an increase up to 6 years of age, whereas in that combinations were used equally often within the adults the number of signals dropped. A long-term study same functional contexts as single signals, as well as the investigating the development of gestural communica- rather high number of repetitions. As with the chim- tion in young chimpanzees yielded similar findings panzees (Liebal, in preparation) no new information (Tomasello et al. 1997). The increase in gestures up to content was created by combining two or more signals, the age of 6 years was explained by the distinct play but if the recipient did not respond to the first signal, behavior of young chimpanzees. Consistent with the siamangs more often chose a different signal rather than present results for siamangs, adult chimpanzees used simply repeating the same gesture, suggesting that they some additional gestures in the context of agonistic and consider the recipient s behavior when choosing the sexual behavior, which were not part of the gestural next signal to force a response. This reflects their ability repertoire of younger animals, but they performed a to use their signal repertoire flexibly and to vary their lower number of signals compared to the youngsters communicative behavior depending on the behavior of overall. In contrast, Pika et al. (2003) found that young the recipient. gorillas peaked in the number of gestures performed at The gestural communication of siamangs thus shows the age of 2–3 years, which was explained by their rather some similarities to that of monkeys, and other simi- short maturation period compared to other great ape larities to that of great apes. For example, great apes, species. Differences in signal repertoire of siamang males but not monkeys, use a number of manual gestures and females were not very distinct except for the use of (including visually based ones) to solicit play and other different gestures in sexual behavior. activities from group mates, and on occasion they even The current recording of discrete communicative incorporate objects into their gestures (Tomasello et al. events also enabled an analysis of flexibility of use. The 1994). In this respect, siamangs appear more like mon- majority of signals were performed in at least three or keys since they use neither manual nor object-based more different functional contexts, whereby facial gestures. Also like monkeys, but not great apes, siam- 56 angs use more tactile and fewer visual gestures in Chadwick-Jones J (1998) Developing a social psychology of mon- general. (It might be that the captive groups studied in keys and apes. Psychology Press, East Sussex Chivers DJ (1974) The siamang in Malaya: a field study of a pri- the current research use more visual gestures than their mate in tropical rain forest. Karger, Basel wild conspecifics, and that might be explained by their Chivers DJ (1976) Communication within and between family more visually open captive environment.) On the other groups of siamang (Symphalangus syndactylus). Behaviour hand, siamangs used most of their gestures very flexibly 57:116–135 Ellefson JO (1967) A natural history of gibbons in the Malay in terms of both adjustments for the state of the recipient Peninsula. University of California, Berkeley and means-ends dissociation as described for chimpan- Ellefson JO (1974) A natural history of white-handed gibbons in zees (Tomasello et al. 1994, 1997), but unfortunately the Malayan peninsula. In: Rumbaugh DM (ed) Gibbon and there are no studies using comparable methodologies to siamang, vol 3. Karger, Basel, pp 1–136 establish the flexibility of gesture use by any monkey Fox GJ (1977) Social dynamics in siamang. University of Wisconsin, Milwaukee species. Siamangs also seem to use fewer facial expres- Geissmann T (1991) Reassessment of age of sexual maturity in sions than the most-studied monkey species such as gibbons (Hylobates spp.). Am J Primatol 23:11–22 baboons and macaques; pig-tail macaques (Macaca Geissmann T (1993) Evolution of communication in gibbons nemestrina), for example, use a variety of facial expres- (Hylobates spp.). Unpublished PhD thesis, University of Zu¨ rich sions when expressing a dominant or submissive Gittins SP (1979) The behaviour and ecology of the agile gibbon status within their social hierarchy system (Maestripieri (Hylobates agilis). Unpublished PhD thesis, University of 1996). Cambridge It is likely that the special ecology of siamangs and Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge other gibbons, as well as their special social structure, Grigor eva OM, Deriagina MA (1987) Gestural forms of commu- have contributed to this unique profile of gesture use. nication in primates: development of gestural communication in Thus, using more tactile gestures is consistent with their ontogenesis and phylogenesis. Biol Nauki 1:45–50 arboreal habitat, and perhaps with their small social Haimoff EH (1986) Acoustic and organizational features of groups containing only highly familiar individuals who gibbons songs. In: Preuschoft HC, Chivers DJ, Brockelmann WY, Creel N (eds) The lesser apes: evolutionary and all engage in most activities together. However, to behavioural biology. Edinburgh University Press, Edinburgh, determine the role of ecology and social structure more pp 333–353 clearly, future studies of other gibbon species, as well as Hinde RA, Rowell TE (1962) Communication by postures and other great apes and monkeys, are needed in order to facial expressions in the rhesus monkey, Macaca mulatta. Proc Zool Soc Lond 138:1–21 allow appropriate comparisons. Hooff JARAM van (1962) Facial expressions in higher primates. Symp Zool Soc Lond 8:97–125 Acknowledgements Special thanks to the staff of Zoo Krefeld and Hooff JARAM van (1967) The facial displays of the catarrhine Howletts Wild Animal Park, in particular to Dr. W. Dressen and monkeys and apes. In: Morris D (ed) Primate ethology. E. Thetford, for their support and hospitality. Many thanks also to Weidenfeld and Nicolson, London, pp 7–68 Daniel Stahl, Josep Call and Keith Jensen for discussion and Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52: comments on the manuscript. 39–69 Kummer H, Kurt F (1965) A comparison of social behavior in captive and wild hamadryas baboons. In: Vagtborg H (ed) The baboon in medical research. University of Texas, Austin References Maestripieri D (1996) Gestural communication and its cognitive implications in pig-tail macaques (Macaca nemestrina). Behav- Altman D (1991) Practical statistics for medical research. CRC/ iour 133:997–1022 Chapman and Hall Maestripieri D (1999) Primate social organization, gestural reper- Altmann J (1974) Observational study of behavior: sampling toire size, and communication dynamics: a comparative study methods. Behaviour 49:227–267 of macaques. In: King BJ (ed) The evolution of language: Bakeman R, Gottman J (1986) Observing interaction: an intro- assessing the evidence from nonhuman primates. School of duction to sequential analysis. Cambridge University Press, American Research, Santa Fe, pp 55–77 Cambridge Orgeldinger M (1999) Paarbeziehungen beim Siamang-Gibbon Baldwin LA, Teleki G (1976) Patterns of gibbon behavior on Hall s (Hylobates syndactylus) im Zoo: Untersuchungen u¨ ber Island, Bermuda: a preliminary ethogram for Hylobates lar. den Einfluß von Jungtieren auf die Paarbindung. Schu¨ ling, In: Rumbaugh D (ed) Gibbon and siamang, vol 4. Karger, Mu¨ nster Basel, pp 21–105 Palombit RA (1992) Pair bonds and monogamy in wild siamang Bard K (1992) Intentional behaviour and intentional communica- (Hylobates syndactylus) and white-handed gibbon (Hylobates tion in young free-ranging orangutans. Child Dev 63:1186–1197 lar). University of California, Davis Bates E (1979) The emergence of symbols: cognition and commu- Pika S, Liebal K, Tomasello M (2003) Gestural communication in nication in infancy. Academic, New York young gorillas (Gorilla gorilla): gestural repertoire, learning and Bruner JS (1981) Intention in the structure of action and interac- use. Am J Primatol 60:95–111 tion. In: Lipsitt L (ed) Advances in infancy research, vol 1. Sarimski K (2002) Analysis of intentional communication in se- Ablex, Norwood, New Jersey pp 41–56 verely handicapped children with Cornelia-de-Lange syndrome. Byrne RW (1995) The thinking ape: evolutionary origins of intel- J Commun Disord 35:483–500 ligence. Oxford University Press, New York Tomasello M, Call J (1997) Primate cognition. Oxford University Caldecott JO (1986) An ecological and behavioural study of the Press, New York pig-tailed macaque. Karger, Basel Tomasello M, Zuberbuehler K (2002) Primate vocal and gestural Carpenter CR (1940) A field study in Siam of the behavior and communication. In: Bekoff M, Allen CS, Burghardt G (eds) social relations of the gibbon (Hylobates lar). Comp Psychol The cognitive animal: empirical and theoretical perspectives on Monogr 16:1–212 animal cognition. MIT Press, Cambridge, pp 293–29 57
Tomasello M, George BL, Kruger AC, Farrar MJ, Evans A (1985) Tomasello M, Call J, Warren J, Frost T, Carpenter M, Nagell K The development of gestural communication in young chim- (1997) The ontogeny of chimpanzee gestural signals: panzees. J Hum Evol 14:175–186 a comparison across groups and generations. Evol Commun Tomasello M, Call J, Nagell, K, Olguin R, Carpenter M (1994) The 1:223–253 learning and the use of gestural signals by young chimpanzees: a trans-generational study. Primates 35:137–154