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CHAPTER Socio-Cognitive Specializations in Nonhuman : Evidence from 1 0 Gestural Communication

Erica Cartmill and Dario Maestripieri

Abstract This chapter reviews cognitive abilities in physical, social, and communicative realms and asks (1) whether primates exhibit abilities that diff er from those of other , and (2) what selective pressures primates face that may have led to the emergence of specifi c cognitive abilities. The authors focus on communication as the most likely realm for primate cognitive specialization and on the gestural communication of great as the modality in which primates exhibit the most advanced cognitive abilities. Findings from studies of natural communication systems of both wild and captive primates as well as studies involving communication with experimenters are presented and discussed. Apes demonstrate fl exibility, learning, and sensitivity to social cues in their gestural communication, but further studies are needed to determine how are acquired and how they are perceived. Studies of comparative development of gestural communication and social cognition have the greatest potential to reveal the cognitive abilities used during gesturing, and they will help to determine whether those abilities are truly specializations for communication. Key Words: Great , communication, , social cognition, development

Introduction fl exibly, with the individual organism making deci- Primate Cognitive sions among possible courses of action based on an Th e past 30 years have witnessed an explosion of assessment of the current situation in relation to its research on all aspects of . Much current goal; and (2) involve some kind of men- of this new research has been fueled by the cogni- tal representation that goes beyond the informa- tive revolution in and , which tion given to direct perception” (Tomasello & Call, prompted a shift from the study of learned behav- 1997, p. 8). ior to the study of mental representations of the Flexibility is central to cognition, because with- self and of the physical and social environment. A out some agency in choosing to perform an action further impetus is the framing of cognitive inves- or having a range of possible actions to confront tigations within and evolutionary biology. a problem or achieve a goal, an ’s response Th is framing has led to a new understanding of the would most likely be an automatic response to a ecological signifi cance and evolutionary origins of reoccurring environmental situation. Some complex cognitive adaptations. behaviors may seem like cognitive adaptations, but Primate cognitive adaptations can be of if the behaviors are infl exible responses to the envi- as complex “behavioral adaptations in which per- ronment, then they are considered behavioral adap- ceptual and behavioral processes (1) are organized tations, not cognitive ones. Th e idea that an animal

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has some agency over what variables of the environ- As in many areas of cognitive research, there is a ment it attends to and how it acts in response to wide gap between the abilities apes demonstrate in those variables is at the foundation of attributing experimental settings and those they employ dur- cognitive processes to animals, and fl exibility lies at ing conspecifi c communication in wild or captive the heart of agency. groups. We compare results from studies of wild Mental representation of some type is also a key and captive conspecifi c gesture, artifi cial- element in cognition. Complex, human-like repre- studies, and experiments in which captive apes sentation based on images or symbols is not required communicate with but by using their natu- or implied. Rather, this representation involves the ral communication systems. Taken together, these ability to make decisions based on perceptions of results demonstrate that the cognitive skills apes the external world by extracting relevant environ- use during gestural communication should be con- mental features, holding information in working or sidered cognitive adaptations, though many ques- long-term , comparing several things, cate- tions remain. Th e captive studies demonstrate the gorizing things, or recognizing similarities between importance of the developmental period in estab- the immediate environment and a previously solved lishing and encouraging the acquisition and use of problem. Animals that appear to display “intelli- both cognitive and communicative abilities. Com- gent” choices, generalized learning, or are all parative studies focusing on the role of ontogeny in employing mental representations that allow them the development of cognitive abilities and on the to learn or make decisions outside the context of tri- interaction between cognitive and communicative al-and-error learning (see Tomasello & Call, 1997). abilities during ontogeny hold the greatest poten- Cognitive adaptations and their underlying neu- tial for providing insight into whether the cognitive ral substrates evolve by in response abilities used in gestural communication evolved as to recurrent problems posed by the physical, ecolog- specializations for communication. ical, or social environment, but they are selected at the cognitive rather than the behavioral level. Th ey Physical Cognition involve the ability to make decisions about what to Th e study of primate cognitive adaptations has do in a particular situation based on the perception involved many aspects of physical and social cogni- or understanding of contextual variables rather than tion. Primate research in the domain of physical cog- precise behavioral responses to external stimuli. nition has addressed how monkeys and apes acquire Cognitive adaptations may be general abilities (e.g., information about the physical space in which they the ability to inhibit a behavior), or they may per- live and the inanimate objects in it, how this infor- tain to specifi c contexts or environmental problems mation is mentally represented and processed, and (e.g., the ability to make probing tools). how it is retrieved and used to make decisions. Free- In this chapter, we ask fi rst whether the primate ranging primates form spatial maps that represent order as a whole exhibits cognitive adaptations that the environment in which they live and use them to diff er from those of other animals, and second we make travel decisions as they search for food within ask what pressures primates face that may have led their home range (for a review see Janson & Byrne, to the emergence of specifi c cognitive abilities. In 2007). In the laboratory, primates exhibit knowledge the introduction, we discuss primates’ abilities in of movements of objects through space and under- the realms of physical cognition, social cognition, standing of object permanence, that is, the notion and communication. We focus on communication, that objects continue to exist and maintain their and on gestural communication in particular, as an features and properties if they have been moved or area in which there is great evidence for both fl ex- hidden from view (Barth & Call, 2006; Call, 2001). ibility and mental representation. In an attempt to For example, primates search for hidden objects, determine whether primates that are phylogeneti- and some can solve tasks that require the mental cally closest to humans show evidence of cognitive rotation of objects (Call, 2000; Vauclair, Fagot, & specializations similar to those of the human spe- Hopkins, 1993). Th ough primates are profi cient cies, we discuss facial expressions and body postures at these tasks, there is no evidence that primates in both apes and monkeys. We then concentrate have greater understanding of space and objects on the manual gestures of great apes as the type relative to other mammals, nor is there evidence of communication that demonstrates the greatest of signifi cant diff erences among primate fl exibility. (e.g., between monkeys and apes).

 socio-cognitive specializations in nonhuman primates

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Other research in the domain of physical cog- Social Cognition nition has involved object manipulation tasks, in Social cognition has been a topic of great interest which objects are used in relation to other objects, in primate research over the past 50 years, and there and which require an understanding of causality is now a growing focus on social cognition research (e.g., the relation between the use of the tool and in a wide range of nonprimate species. Th ese stud- the goal to be accomplished with it). Many spe- ies are driven in part by our desire to understand cies of primates, and especially capuchin monkeys the evolutionary pressures underlying the develop- and the great apes, are profi cient tool users and also ment of human social cognition, including the abil- show some evidence of understanding of causality ity to be aware of the self and others; to empathize, (although see Povinelli, 2000). However, primates’ cooperate, inform, create, and share symbols; and to tool using skills have been matched or even sur- hold collective beliefs. Many complex human abil- passed by the tool using skills of some corvid birds ities (including language and understanding oth- (e.g., Emery & Clayton, 2004; Hunt, 1996). Dis- ers’ beliefs) may have foundations in skills of social crimination learning studies have addressed whether awareness that evolved to keep track of, predict primates learn to discriminate particular features of the behavior of, and manipulate relationships with objects and assign these objects to categories on the other individuals in large social groups. Primates basis of similarities and diff erences in these features. have demonstrated advanced capabilities in many Th ese studies have shown that primates cannot areas of social awareness, including self-recognition, only discriminate and categorize objects but can awareness of knowledge, social learning, and under- also understand complex rules underlying catego- standing the social relationships of others. Some rization, for example, the notion that categories of nonhuman primate lineages (particularly birds objects can be formed on rules such as identity, and ) demonstrate comparable abilities in cer- oddity, sameness, or diff erence (Tomasello & Call, tain aspects of social cognition, but primates most 1997). Similar to birds and other mammals (e.g., consistently demonstrate cognitive adaptations for laboratory rats), primates also possess the ability to processing and benefi ting from social informa- make accurate estimates of small quantities of items tion. Primates may diff er most substantially from as well as the ability to solve simple tasks involv- nonprimates in the ability to represent other minds. ing quantity conservation or summation (Brannon In a recent review, Byrne and Bates (2010) draw a & Terrace, 1998; Cantlon & Brannon, 2006). Th e distinction between diff erences in social cognition exact perceptual or conceptual mechanisms under- based on degree (e.g., keeping track of more group lying these skills remain unclear. members or having more categories) and those based Taken together, studies of primate physical cogni- on a deeper understanding of the mind (e.g., aware- tion have shown that monkeys and apes possess the ness of the self or understanding of others as having ability to form mental representations of their space diff erent perceptions and knowledge). Th e authors and objects, including hidden ones, but they show argue that “particular skills such as insightful coop- little evidence of greater learning skills or greater eration or deception, perception of intent, imitation understanding of the physical world and its proper- of novel skills, and mirror self-recognition, signify a ties than other vertebrate animals do. Th e strongest qualitatively diff erent representation of mechanisms evidence for a potential primate cognitive special- and minds.” Th is diff erence probably relies on the ization in the realm of physical cognition involves presence of “specifi c cognitive architecture that the use of tools and the understanding of relational allows for behavior parsing and the formation of properties of objects including causality. Th is is par- hierarchically organized programs of action” (Byrne ticularly strong in large-brained primate species that & Bates, 2010, p. 825). Abilities relating to percep- face strong ecological pressures for complex food tion and representation of other minds are good processing, such as capuchin monkeys and all spe- candidates for primate cognitive specializations that cies of great apes. Comparative studies between the set them apart from other species. development and transmission of tool manufacture Th e ability to be aware of oneself may be one step and use in primates and corvids may reveal com- toward recognizing that other individuals are also mon social and environmental factors driving the “selves” with autonomous behavior and diff erent goals development of these abilities in both lineages (e.g., and beliefs. Researchers have conducted many studies Emery & Clayton, 2004; Emery, chapter fi ve of this of primates’ ability to recognize themselves in a mir- volume). ror, driven by the hypotheses that mirror self-recog-

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nition indicates self-awareness and that knowledge of through emulation, imitation, or teaching. Social self forms the basis for (Gallup, 1970; learning of complex behaviors has been demon- Gallup, Anderson, & Shillito, 2002). On the mark strated by many primate species in captivity, and test of self-recognition (which measures self-explor- behavioral diff erences between groups of wild pri- atory behavior in front of a mirror after subjects have mates are often considered to be the result of social been unknowingly marked with a salient paint), pri- learning. Primates’ demonstrated abilities to learn mates as a whole perform better than other animals from observing others along with observations of (but see Plotnik, de Waal, & Reiss, 2006; Reiss & naturally occurring regional behaviors provide evi- Marino 2001 for evidence of mirror self recognition dence for the origin and spread of behavioral tra- in and cetaceans). Apes outperform mon- ditions that may approximate elementary forms of keys on the mirror task (Gallup, Anderson, & Shil- human culture (van Schaik et al., 2003; Whiten et lito, 2002), but monkeys may have an intermediate al., 1999). Many other animals have demonstrated level of understanding where they do not recognize the ability to learn from observation of others in the refl ection as their own but still understand that it captive settings, and they sustained transmission of is not a stranger (de Waal, Dindo, Freeman, & Hall, behavioral traditions (e.g., guppies: Warner, 1988; 2005). Th e notion that learning how to use a mir- meerkats: Th ornton, Samson, Clutton-Brock, 2010; ror to inspect inaccessible aspects of one’s body nec- see further review in Laland & Galef, 2009). Species essarily entails possessing a concept of self has been capable of often have local “dialects” questioned (e.g., Hayes, 1993), but the tendency of that vary between locations (e.g., Deecke, Ford, & great apes to examine the face in detail, even when it Spong, 2006; Jenkins, 1978). Th ere is less evidence is not marked, provides support for a self-recognition for “material culture” (i.e., socially learned behav- interpretation (Gallup et al., 1995). iors involving the manufacture or manipulation of Metacognitive abilities (e.g., awareness of what objects) in nonprimate species, but some observed you do or do not know) may be a better indica- behaviors might comprise local traditions (e.g., dol- tor that an animal is aware of itself as a cognitive phins using sponges as tools Krützen et al., 2005). agent (able to make judgments or possess knowl- Unsurprisingly, regardless of whether culture can edge). Tests of metacognition typically involve dis- be considered a cognitive specialization unique to crimination or memory tasks in which animals have humans or shared by other primates (and/or other the option to participate in or opt out of the task animals) rests on how culture is defi ned and what on each trial (or in some cases to gamble on a trial operational criteria are used for its identifi cation based on their confi dence) (see chapter 15 of this across species (Byrne et al., 2004; Laland & Hop- volume). To succeed on a trial, an animal must usu- pit, 2003). ally either remember earlier stimuli or be able to cat- Although the question of whether nonhuman egorize a new stimulus correctly. If the animal opts primates have the ability to think about other indi- out of a trial, it might receive a smaller reward than viduals’ mental states remains unanswered, it is well it would if it had participated and chosen correctly recognized that they excel at the task of observ- or it might simply avoid a punishment incurred if ing other individuals’ behavior, remembering past a wrong answer is given. To maximize success on interactions, and making predictions about future these tests, animals should participate when they interactions. Primates form complex social relation- are confi dent they will succeed and opt out when ships with others and have knowledge and memory, they are unsure of their answer. Both primates and not only of their own relationships, but also of rela- cetaceans have performed well in these types of tionships between other individuals (e.g., Cheney tasks, indicating that they are aware of what they do & Seyfarth, 1999). Studies investigating this aspect and do not know (Hampton, 2001; Kornell, 2009; of social cognition have assessed primates’ ability to Kornell, Son, & Terrace, 2007; Smith, Shields, & recognize kinship, dominance-rank relationships, or Washburn, 2003; Smith & Washburn, 2005; Smith friendships among individuals that reside in their et al., chapter 15 of this volume). Th ough there are social group. Knowledge of social relationships is few comparative studies, monkeys appear to need used in complex cooperative and competitive strat- more training to perform these tasks than apes (see egies involving exchange of favors, alliance forma- Kornell, 2009; Suda-King, 2008). tion, opportunistic exploitation of social situations, Apes also outperform monkeys on tests involving and manipulation of other individuals with deceit- social learning (i.e., learning by observing others) ful tactics (Byrne & Whiten, 1988).

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Complex social strategies in group-living mon- It is now recognized, however, that this ability is keys and apes invariably entail the exchange of vocal shared by a number of birds and other mammals or visual signals between individuals. Communica- (Evans & Evans, 2007; Hauser, 1996; Macedonia tion can provide a window into the primate social & Evans, 1993). Food calls have also been given as mind, though it is unclear whether the cognitive examples of referential signals because, according to abilities that underlie communication are adapta- some researchers, they convey information about tions primarily for communication or whether they the type, quantity, and location of food to other evolved more generally for group living and simply conspecifi cs (e.g., Dittus, 1984). It is unlikely, how- provide an advantage to communication when they ever, that primate vocalizations about predators or are present. Studies of communication can pro- food require a higher degree of cognitive complexity vide into cognitive adaptations; however, than similar vocalizations used by other mammals they must fi rst demonstrate that the communica- or birds. Th is is because the problems faced by most tive signals studied are not involuntary reactions to primates during or escaping predators are the environment but, instead, meet the criteria of simply no diff erent in complexity from those faced fl exibility and mental representation. Many features by most other animal species. Th erefore, it is dif- of communication have the potential to shed light fi cult to argue that these activities posed a special on cognitive adaptations. Th ese include the role of pressure to evolve higher cognitive or communica- learning in the acquisition of signal production, tive abilities in primates. comprehension, and usage; the extent to which Vocalizations related to intragroup social inter- signals are under volitional control; the complex- actions are more likely to demonstrate increased ity in the structure of signals; and the information cognitive complexity in primates because of the content or meaning of signals. Th e features of the complexity of their social systems and their dem- environment that animals attend to when choosing onstrated abilities in the realm of social cognition. when or how to signal and the ways in which they Rather than being broadcast indiscriminately, social use communicative strategies to achieve their goals calls may be sensitive to the identity and social rank have great potential to reveal when and how animals of listeners. For example, the agonistic screams of make choices during communication. Studied fea- macaques appear to elicit diff erent responses from tures of communicative strategies include the extent other group members in relation to characteristics to which signals are combined with other signals of opponents, such as their dominance rank (Gou- within the same modality or across diff erent modal- zoules, Gouzoules, & Marler, 1984), and represen- ities to accomplish diff erent functions; the extent tational signaling in the context of recruitment of to which combinations of signals exhibit properties agonistic support is an ability that might have been of human , such as syntax; and the extent strongly selected for in the social environment of to which the production of signals is modifi ed in group-living primates. Social calls may be directed relation to the presence of particular individuals at a specifi c individual, but they are likely broad- (audience eff ects), their attentional states or current cast to at least several individuals, and they can behavior, and possibly also their mental states. be used to initiate or maintain group behavior. Vocalizations that are emitted in order to coordi- Cognitive Complexity in Natural Primate nate the behavior of group members during travel Communication or to facilitate affi liative and bonding interactions Investigations of complexity in primate com- are a particularly interesting area of investigation munication have mainly focused on vocalizations, because, unlike antipredator calls and recruitment in part because the shared modality aff ords direct screams, these signals are not obviously associated comparison between vocalizations and with states of high arousal (e.g.,, Rendall, Cheney, human speech. For example, great emphasis has & Seyfarth, 2000). Contact vocalizations that facil- been placed on the fi nding that vervet monkeys itate coordination of group movements and close- (Chlorocebus aethiops) possess diff erent alarm calls range interactions are particularly well developed for aerial and terrestrial predators and are, therefore, in arboreal species such as New World monkeys claimed to be capable of semantic communication (Boinski, 1993; Snowdon, 1989). Th e complex- (Cheney & Seyfarth, 1990; Gouzoules, Gouzoules, ity of vocal structure and vocal sequences in New & Ashley, 1995; Struhsaker, 1967; Zuberbühler, World monkeys, however, is likely to be the result 2000a; 2000b; 2003, chapter 17 of this volume). of the pressures of arboreal life rather than those of

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social variables (Snowdon, 1993). Moreover, the process involved in vocal communication (and in referential nature of agonistic screams, grunts, or information acquisition through listening to calls) other short-range contact calls has been questioned is thought to be the associative learning process by even for the Old World monkeys and apes (e.g., which a listener acquires the contingent relation Rendall, Owren & Ryan, 2009). Controversy over between two paired stimuli (a call and an object or the interpretation of the cognitive underpinnings of an event) (e.g., Seyfarth et al., 2010). primate vocalizations can be reduced to the contrast Both interpretations place the bulk of learn- between two fundamentally diff erent views of pri- ing in communication on the recipient, who must mate vocal communication: the “information” view quickly acquire associations between calls and exter- and the “infl uence” view. nal events (for a discussion of the diff erent pressures facing signalers and receivers see Seyfarth & Cheney, the “information” view and the “influence” 2003). Primates are adept at learning contingen- view of primate vocal communication cies between auditory stimuli and external events Th e “information” view of primate vocalizations and some species have even learned to respond to is grounded in a traditional view of animal commu- the alarm calls of other species (e.g., Zuberbühler, nication as a process of cooperation, which involves 2000b). Th ough both versions of the information the exchange of information through signals in a way view require the receivers to learn the relationships that benefi ts both the sender and the recipient of the between calls and the external world, the behaviorist signal (but see Lachmann, Szamado, & Bergstrom, approach does not require that the pairing between 2001; Scott-Phillips, 2008 for mechanisms to keep a call and stimulus be stored as a mental represen- signals honest even when interests do not coincide). tation of the external referent. Th is view has more Th e information view assumes that primate vocal- in common with the interpretation of vocalizations izations have meaning and that the speaker and the as tools to directly infl uence others’ behavior rather listener have similar representational processes that than to inform others’ minds. ensure corresponding coding and decoding of signal In contrast to the “information” view’s focus on meaning. In this view, primates use vocal signals in a shared representations, the “infl uence” view of pri- representational fashion, similar to the way humans mate vocal communication maintains that the func- use words. Implicit in this view is the assumption tion of calls is to infl uence the behavior of listeners that speaker and listener make attributions about rather than to transmit meaningful information each other’s mental states, such as their , through mental representations (Owren & Rendall, beliefs or knowledge, because these attributions 2001; Rendall, Owren & Ryan, 2009). Th is view are what motivate and sustain reciprocal semantic emphasizes that sender and recipient often have exchange. Given that primates, however, seem to be diff erent interests (hence communication involves unaware of the consequences their own vocal sig- manipulation) and play more distinct roles in the nals have on the behavior of the recipients, and do communication process (Dawkins & Krebs, 1978; not appear to intentionally transfer information to Owings & Morton, 1998). In this view vocaliza- them, the information view assumes that vocaliza- tions have acoustic features well suited to access and tions are functionally, but not intentionally, refer- exploit listeners’ basic perceptual sensitivities and ential (Seyfarth & Cheney, 2003). In other words, central nervous system refl exes (Owren & Rendall, recipients respond to vocalizations ‘as if’ they con- 2001). Th ey elicit predictable responses in listeners tained semantic information. through direct eff ects on the listener’s aff ective and In reality, proponents of the information view of motivational states and through learning processes primate vocalizations have often oscillated between by which the listener learns associations between two highly cognitive interpretations. On the one vocalizations and contexts. hand, are interpretations of vocalizations that Th e infl uence view explicitly excludes the notion emphasize their language-like properties such as that mental representations or any type of theory semanticity, syntax, and grammar and imply men- of mind cognitive processes are involved in the tal representations of call referents (e.g., Hauser, exchange of primate vocalizations. Th erefore, in 1996; Seyfarth & Cheney, 2003; Zuberbühler, this view, primate vocal communication is funda- 2002, 2003). On the other hand, recent interpre- mentally diff erent and evolutionarily discontinuous tations of the information view have taken a more from human language. For example, although com- behavioristic approach, in which the only cognitive munication through language entails similar and

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symmetrical cognitive processes in the speaker and (visual and tactile) signals in terrestrial species, and the listener, communication through primate calls (2) the increasing complexity of gestural signals may involve asymmetries in the mechanisms that from the prosimians to the great apes (Maestripieri, support signal production in senders versus recep- 1999; Parr & Maestripieri, 2003). tion in perceivers. Moreover, although the acous- It might be speculated that life in the open savan- tic structure of vocalizations is often arbitrary in nas after departure from the forests selected for the human language, the infl uence view maintains that physical characteristics, especially bipedalism, found the design of signals is central to the process of non- in Australopithecines and later species, as well as for human primate vocal communication. a further enhancement of the use of gestural com- munication. Furthermore, bipedalism probably had Evolutionary Trends in Primate a more profound infl uence in freeing the hands for Communication communication than in altering the vocal repertoire Primate vocal communication can be both refer- (Corballis, 1992; Hewes, 1973). Th e patterns of ges- ential and complex. However, call production does tural communication observed in extant species of not display much fl exibility and agency on the part primates suggest that gestures could have been used of the signaler and may therefore indicate a greater initially in primarily dyadic contexts to commu- reliance on behavioral rather than cognitive adap- nicate information moderating social interactions. tations. In addition, regardless of whether primate Gestures could fi rst have functioned to anticipate calls are interpreted according to an information or the signaler’s social actions and to request and com- infl uence view, there is little evidence that primates mand specifi c actions from others (see; Cartmill & show more complex cognitive specializations in Byrne; 2010; Genty, Breuer, Hobaiter, & Byrne, their vocal communication abilities when compared 2009; King, 2004). Subsequently, gestural commu- to other animals. Moreover, there is no trend toward nication could have expanded to reference aspects increasing complexity in the structure, function, and of the external environment such as food, predators, use of vocal signals from the prosimians to the New or tools. World monkeys, the Old World monkeys, and the In the rest of this chapter, we examine the cog- great apes, suggesting that the evolutionary increase nitive underpinnings of social communication, par- in that occurred in the Cercopithecoids ticularly with regard to nonvocal signals, because and the ape lineage was not associated with increas- we believe that the study of gestural communica- ing complexity in vocal exchanges or their cognitive tion can elucidate many aspects of primate cogni- substrates. Such an evolutionary trend, however, is tive adaptations to social life. We begin, in the next observable in the use of nonvocal signals (Parr & section, by reviewing and discussing how nonvocal Maestripieri, 2003). signals are used in Old World monkeys (especially In the Cercopithecidae and in the great apes, there macaques and ) and apes, and what social is a clear increase in the role played by facial expres- and communicative functions are accomplished sions (associated with the development of complex through them in the contexts of competition, mat- facial musculature) relative to vocalizations (e.g., ing, affi liation, and parental care. Maestripieri & Call, 1996; Parr & Maestripieri, 2003). Moreover, in the great apes, there is an Natural Gestural Communication of involvement of the arms and hands in making social Monkeys and Apes: Description of Patterns gestures to a degree that is not observed in other Primates frequently use nonvocal signals in com- nonhuman primates or other animals (Bard, 1992; munication. Many are involuntary responses to Berdecio & Nash, 1981; de Waal, 1988; Goodall, external stimuli or internal states of arousal (e.g., 1968; 1986; Hewes 1973; Kortlandt, 1962; Mae- piloerection or expanding the chest to seem larger). stripieri & Call, 1996; McGrew & Tutin, 1978; Th ough they can be eff ective signals, these invol- Plooij, 1978; 1979; Nishida, 1980; Tomasello, untary signals are not cognitive adaptations. Rather George, Kruger, Farrar, & Evans, 1985; Tomasello, they are behavioral adaptations selected for com- Call, Nagell. Olguin, & Carpenter, 1994; Toma- munication in reoccurring contexts (e.g., aggression sello, Gust, & Frost, 1989). Th us, if any evolution- or mating). Some signals, however, demonstrate ary trends are apparent in primate communication, both fl exibility and representation and thus repre- these are (1) the preponderance of vocal signals in sent cognitive adaptations. Primate gestural com- arboreal species versus the preponderance of gestural munication contains both involuntary responses

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and voluntary, fl exible signals. Th e fi rst challenge function appears to be to reduce the likelihood of for researchers is to distinguish one from the other; future aggression. Th e signal, however, may or may the second is to question whether communication not be eff ective in preventing aggression, depend- drove or benefi ted from the evolution of its under- ing on the circumstances. In some primates, the lying cognitive abilities. bared-teeth display may occur without any prior We review studies of nonvocal communication interaction between two individuals and may be in both monkeys and apes with an eye toward iden- followed by affi liation or mating (Petit & Th ierry, tifying behaviors that might indicate complex cog- 1992; Th ierry, Demaria, Preuschoft, & Desportes, nitive abilities. We present fi ndings from both wild 1989). Th erefore, the way in which the bared-teeth and captive groups, all involving conspecifi c com- display is used seems to vary across species. Another munication using the species’ own communicative common submissive signal is the hindquarter pre- systems. In this section, we contextualize the studies sentation. Similar to the bared-teeth display, sub- and present results, but we wait until the following ordinates present to dominants upon receiving section to discuss the potential implications of the aggression or in situations with high risk of aggres- fi ndings to the study of primate cognitive adapta- sion (Chadwick-Jones, 1989; Maestripieri, 1996a; tions. Maestripieri & Wallen, 1997). Th e presentation can also be displayed to initiate affi liative interactions. Facial Expressions and Body Postures in Old Bared-teeth and hindquarter presentation can occur World Monkeys and Apes in conjunction with other submissive signals such as Most species of Old World (OW) monkeys and lip-smacking and teeth-chattering (Altmann, 1962; apes live in either one-male groups, or in multimale- Dixson, 1977; Hadidian, 1979; Hinde & Rowell, multifemale groups. Group-living primates interact 1962). with one another on a daily basis and communicate in the context of both competitive and coopera- mating and affiliation tive interactions. Communication in the context of Facial expressions and body postures play an competition allows individuals to negotiate access important role also in mating interactions. Females to resources and reduces the probability of costly in estrus signal their readiness to mate by approach- fi ghts. Facial expressions of threats typically involve ing males and presenting their hindquarters to staring at the opponent with eyes wide open, them. Macaque males use facial expressions such as mouth open without showing the teeth, eyebrows the pucker, bared-teeth, lip-smack, or teeth-chatter raised, and ears fl attened (Altmann, 1962; Hinde while approaching an estrous female (Christopher & Rowell, 1962; Kaufman & Rosenblum, 1966; & Gelini, 1977; Goosen & Kortmulder, 1979; Mae- van Hooff , 1967). Competition over feeding and stripieri, 1996a). Once the distance between males mating, or simple proximity to another individual and females is reduced, males use tactile signals such can elicit a threat. Th e threat signals the individu- as hip-touches to induce the female to present her al’s potential, or motivation to engage in a confl ict. hindquarters. During copulation, the female often Th e relationship between threat and aggression, reaches back grasping the male’s fl ank or leg with however, is not ubiquitous. Aggression may not be her hand and lip-smacks while the male displays preceded by threats and, in most cases, threats are bared-teeth, squeaks, or teeth-chatters (Maestrip- not followed by aggression. Th reats, instead, elicit ieri, 1996a). In this context, facial expressions could the expression of submissive signals in the individ- simply refl ect an underlying orgasm-related emo- ual being threatened. tion (Goldfoot, Westerborg-Van Loon, Groeneveld, & Slob, 1980). submission Mating interactions are often preceded or fol- Submissive signals can include facial expres- lowed by affi liative behavior such as grooming and sions or postures that expose vulnerable regions of a range of signals are used to entice another indi- the body. Th e most common submissive signal in vidual to approach or to indicate affi liative intent OW monkeys and is the silent bared- during approach. An individual may use the pucker, teeth display, also referred to as “fear grin” or gri- lip-smack, teeth-chatter, the bared-teeth, or the mace. Th e bared-teeth display occurs primarily in hindquarter presentation while approaching, or to response to threats or aggression, or the approach induce another individual to come closer. Once of a dominant individual (Maestripieri, 1997). Th e distance is reduced, grooming is usually requested

 socio-cognitive specializations in nonhuman primates

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by lying on the ground and exposing the part of the and it most often occurs during contact play involv- body to be groomed. Postural changes are also used ing struggle (Preuschoft, 1992). Traditional explana- to signal the intention to terminate the interaction tions of play signals in monkeys and other animals (Boccia, 1986). Th e facial expressions and body maintain that they are a form of “metacommunica- postures used to reduce distance between adults tion,” that is, they communicate to the partner “I are also used between adults and infants. Macaque want you to know that this is only play” (Altmann, mothers retrieve their infants from a distance by 1962). Th is explanation, however, implies quite using the pucker, the bared-teeth, the lip-smack, or sophisticated cognitive processes, notably the abil- the presentation, depending on the species or the ity to attribute knowledge to others. It is also possi- circumstance (Ferrari, Paukner, Ionica, & Suomi, ble that the play face is produced spontaneously in 2009; Jensen & Gordon 1970; Maestripieri, 1996b; situations of ambiguous threat (when it is unclear Maestripieri & Wallen, 1997). Some of these signals whether a conspecifi c is being aggressive or playing). are used interchangeably and often occur in rapid In this scenario, the signaler does not produce the succession, that is, a mother will fi rst lip-smack or play face purposefully as a signal, but play partners bare-teeth to her infant and then turn around and learn to use the spontaneous expression as an indi- raise her tail (Maestripieri, 1995). Th ese interac- cation that the interaction will be affi liative and not tions are particularly frequent in the fi rst weeks of an aggressive (e.g., Pellis & Pellis, 1996). Some authors infant’s life when mothers display these expressions have hypothesized that the play face may simply be to their infants while walking backward as a way a form of play rather than a signal with a complex to encourage their infants’ independent locomotion meaning (Maestripieri, 1997; Pellis & Pellis, 1996; (Ferrari et al., 2009; Maestripieri, 1995; 1996b). Tanner & Byrne, 1999). In addition to the typical Affi liative communication between males often play face, chimpanzees, and involves hip-clasping, mounting, and genital manip- also exhibit “smile” and “laughter” (Chevalier-Skol- ulation (i.e.,, one individual reaches out and fondles nikoff , 1982; van Hooff , 1967). Th ese expressions the other’s genitalia). In contrast, females often are believed to be homologous in macaques, chim- embrace each other (Dixson, 1977; Maestripieri, panzees, and humans (Preuschoft & van Hooff , 1996a). Mounting, clasping, and embracing may 1995). Unlike monkeys, all great apes are reported be accompanied by lip-smacking or teeth-chatter- to frequently exhibit novel facial expressions, par- ing by one or both partners (Chevalier-Skolnikoff , ticularly in the context of play, in which the facial 1974; Maestripieri, 1996a). Th ese signals are most muscles are contorted in highly variable shapes likely expressions of excitement and might function and combinations (Chevalier-Skolnikoff , 1982; de to minimize risk of aggression and promote bond- Waal, 1988). ing. Particular affi liative interactions between adult males known as “greetings” probably serve to nego- development and use tiate dominance relationships, alliance formation, Although little research has been done on the and decision-making processes relative to the direc- mechanisms underlying communication through tion of travel (in baboons, see Colmenares, 1991; nonvocal signals in primates, it is very likely that Smuts & Watanabe, 1990; Whitham & Maestrip- many facial expressions and whole body postures ieri, 2003). in Old World monkeys and apes refl ect underlying emotional states or induce emotional changes in the play recipient (Parr & Maestripieri, 2003). Many of these Play is characterized by the occurrence of a dis- signals appear to be graded rather than discrete. Th e tinctive facial expression known as the “play face” fl exibility in the combination of elements in each (van Hooff , 1962; 1967). Th is expression consists signal (e.g., exposure of the teeth along with raising of a wide opening of the mouth, as if attempting the shoulders) would be an to refl ect the to bite, but without clenching the teeth. Th e top intensity of the emotion or motivation underlying teeth are typically covered but the bottom teeth may the signal. Similarly, the structural similarities among be visible. Play faces are usually displayed simulta- signals may allow the expression of rapid transi- neously by two play partners and may be associated tions in emotional or motivational states (Shirek- with soft vocalizations (Symons, 1978). Typically, Ellefson, 1972). Functionally, facial expressions the play face does not occur in contexts other than and body postures may communicate information play. It is not used to initiate play from a distance, about the signaler’s impending behavior, requests to

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approach and engage in affi liation, mating, or play, use this gesture to request food or agonistic support or requests to inhibit behaviors such as aggression more than bonobos do. Other gestures and postures or fl eeing. Unlike vocalizations, they are not used observed among chimpanzees and bonobos include to communicate about aspects of the external envi- wrist shaking, arm waving, arm up, stretch over, ronment, such as the presence of food or predators; hunch over, hand and foot clapping, chest beating, rather, they may convey information about a range and various types of rhythmic movements involv- of social activities occurring in the group, and pos- ing the hands and feet, and embraces (see Goodall, tures often also contain an indication of the location 1968). Some of these signals are presumably used where the activity will take place (e.g., grooming or as attention-getters (e.g., arm waving) whereas oth- direction of travel). ers are more explicit requests for sex or grooming. Facial expressions and body postures rarely show McGrew and Tutin (1978) reported a cultural tra- any context-specifi city linking them to the external dition involving a “hand-clasp” posture that occurs environment. Th e same signal is used in diff erent between wild chimpanzees engaged in allogroom- contexts and the same communicative function can ing, and this was later observed in a captive group as often be served by diff erent signals. Th is contex- well (de Waal & Seres, 1997). It is unclear, however, tual fl exibility is considered an important feature of if the posture has any communicative signifi cance manual gesture in great apes, but unlike gestures, to the individuals engaged in this behavior, or to facial expressions and body postures show little evi- other group members. A form of attention-getting dence that they are used in an intentionally com- behavior (“leaf clipping”), in which leaves are held municative way with the expectation of eliciting a and torn apart with the teeth producing an audi- particular response. Th e relation between the struc- ble sound, has been reported among chimpanzees ture of signals and their function seems to be prob- in the Mahale mountains, mostly in the context of abilistic rather than fi xed, with much information requesting sex or food (Nishida, 1980). being provided by the social context. Th ough facial expressions and body postures are likely spontane- intentional gestures ous expressions of internal emotional states, appro- Th e distinction between intentional and nonin- priate use and interpretation of signals in relation to tentional gestures in chimpanzees was fi rst explicitly social context probably requires some social learn- made by Plooij (1978, 1984). Plooij described sev- ing during development. eral gestures used by infants during interactions with their mothers or with their peers: a “hands around Manual Gestures in Great Apes the head” gesture to request tickling, an “arm-high” Although facial expressions and their contexts of gesture to initiate grooming; a “food-beg” gesture to occurrence are rather similar in Old World mon- request food; “leaf-grooming” and “running away keys and the great apes (see Berdecio & Nash, 1981; with an object” gestures to encourage social play. de Waal 1988; Goodall, 1968; 1986; van Hooff , Plooij identifi ed gestures as being intentional when 1973, for great apes), apes diff erentiate themselves they were used “fl exibly” and/or were accompanied when it comes to the use of manual gestures. Apes by gaze alternation. By fl exibly, he meant that the use gestures in a wide range of social contexts and same signal could be used to achieve diff erent goals, they appear to have a level of volitional control over and diff erent signals could be used for the same when and how to use them that sets both apes and goal. For example, Plooij observed a juvenile who, gesture apart from other primates and other types of in some cases, used an “arm-high” gesture to invite communication. Apes produce a range of gestural grooming under its arm, and in other cases used the forms that are not typically observed in monkeys same gesture in an appeasement context. Th is fl exi- and use many of them in ways that indicate a deeper bility in relation to goal indicates that the gesture is sensitivity to the minds of other individuals and, in not produced as an automatic response to an exter- many cases, an intention to communicate. nal stimulus. Gaze alternation involved monitoring Hand begging gestures, for instance, are rare or the response of another individual to the signal and nonexistent among Old World monkeys but have suggested that the sender had some understanding been reported in all four species of great apes. De of the eff ect of the signal on the recipient. For exam- Waal (1988) believes that bonobos use this ges- ple, Plooij observed that when begging for food, ture as an overture for reconciliation after a fi ght infants alternated their gaze between their mother’s more than chimpanzees do, whereas chimpanzees face and their hand (see also Bard, 1992, for similar

 socio-cognitive specializations in nonhuman primates

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interactions in orangutans). Plooij (1984) argued nursing, three to request carrying, and two to beg that some gestures develop ontogenetically from for food. Visual signals were used only if the recipi- goal-directed actions, but then become signals in ent was looking and tactile signals only if the recip- part due to the infl uence of social learning and shap- ient was attending to the behavior of the signaler. ing. He suggested that, at some point during devel- Many social interactions (e.g., play) were initiated opment, the infant understands that the mother is with an “attention-getter” gesture such as “throwing an independent agent with her own communicative chips,” “poking at,” or “ground slapping.” ability and, at this point, most gestures begin to be Th e comparison of gestures across time periods used intentionally. and generations showed that there was little over- Building upon Plooij’s work, Tomasello and lap among gestures either within or between groups, colleagues (Tomasello et al., 1985, 1989) focused indicating that the gestures were not acquired via on intentional gestures used by juvenile chimpan- social learning. Specifi cally, (1) some juveniles zees during interactions with their mother or other used gestures that no other group member used; group members. In addition to fl exibility in the use (2) some juveniles used gestures that had not been of signals and gaze alternation, response waiting and directed to them and that they had little opportu- audience eff ects were also included as evidence of nity to observe; (3) juveniles raised only with peers intentional gesture use. Response waiting meant ended up developing some of the same gestures as that the individual waited for a response from those raised with adults; (4) within-group variability another individual after sending the signal, thus in the use of gestures was very high. Th ese fi ndings suggesting that the goal of the gesture was to com- suggested that younger individuals were not acquir- municate. Finally, audience eff ects occurred when ing their gestures by watching older, more experi- an individual used a signal diff erently depending enced ones. To determine whether these fi ndings on the identity or attentional state of the recipient. were typical of the species, Tomasello and Camaioni Some of the intentional gestures studied by Toma- (1997) extended the longitudinal study of chim- sello and collaborators were used to get the mother’s panzee gestures to include additional groups. Th is attention and initiate nursing (e.g., touching her study replicated some of the earlier fi ndings, includ- body), solicit carrying (placing one arm on the back ing low concordance rates in gestures within groups of another individual or pulling another individual and generations. Two individuals in this study were along), request grooming (exposing the body part to taught new food begging gestures by human experi- be groomed or placing the other individual’s hand menters and then reintroduced into the group, but on this part), request food sharing (placing the hand the novel gestures did not spread within the group: under the adult’s mouth in a begging gesture), or other individuals kept using their own gestures and invite play (arm raising, ground slapping, head bob- did not adopt the new ones during the course of bing, hand clapping, foot stomping, running away the study. and looking back). Tomasello et al. (1985) reported Tomasello and Camaioni (1997) argued that that some gestures were used quite fl exibly in diff er- chimpanzees use two basic types of intentional ent contexts and that the older juveniles used some gestures with their conspecifi cs: “attractors” and novel behaviors not observed among other indi- “incipient actions.” Attractors are imperative ges- viduals. Tomasello et al. (1989) also reported the tures aimed at getting other individuals’ atten- creation of new gestures when new materials were tion, whereas incipient actions are also imperative introduced to the group (e.g.,, newly introduced gestures, but they are used to communicate infor- wood chips were used to initiate play by throwing mation about impending behavior or to request them at others). specifi c activities. According to Tomasello and Camaioni (1997), both attractors and incipient longitudinal study actions are mostly used in dyadic contexts and are In a follow-up to their original study of chimpan- never used for declarative purposes, that is, to share zee gestures, Tomasello and colleagues (Tomasello, interest in, or comment on, something or someone. Call, Nagell, Olguin, & Carpenter, 1994) returned Furthermore, many gestures rely on physical con- to the same group to see whether gesture repertoires tact between signaler and recipient or are incipient or use had changed over time. Th ey reported that movements that anticipate contact. Th us, in Toma- juvenile chimpanzees used eight diff erent gestures sello and Camaioni’s (1997) view, gestures are more to initiate play, three diff erent gestures to solicit closely related to the mechanical manipulation of

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another’s body than to the psychological manipu- choosing between tactile and visual gestural modali- lation of another’s mind. Tomasello and Camaioni ties: visual gestures were used more frequently when (1997) emphasized the diff erences between the the gesturer could be seen, whereas tactile gestures intentional gestures of chimpanzees and those of were used similarly regardless of gaze. Th e authors human children and adults. In their view, the lat- looked for group diff erences as well as species dif- ter are often used triadically and for declarative pur- ferences comparing gestural repertoires between poses, are often indexical or symbolic, are meant to conspecifi c individuals within and between diff er- infl uence others psychologically, not mechanically, ent groups. Th ey found that individual repertoires and are learned through social observation rather varied as much within as between groups. Th is was than individual learning (we discuss this distinction used as evidence against the possibility that gestures further in a later section). Tomasello and Camaioni are acquired through social learning and as support conclude that intentional gestures in chimpanzees for the theory of ontogenetic ritualization posited are probably learned by a process of ontogenetic rit- by Tomasello and Camaioni (1997). ualization and not by . Onto- One may argue that the characterization of genetic ritualization is a form of individual learning gestures as imperative signals acquired in which each individual learns the eff ects of its through individual learning that manipulate behav- behavior on the other’s behavior. Gestures described ior rather than transmit information used by Toma- as incipient actions support this proposed learning sello and Camaioni (1997) is overly strict, and that mechanism since the process of ritualization would the diff erences that Tomasello and colleagues draw naturally yield gestures that were comprised of the between ape and human gestures are overstated. For initial movements or other parts of actions. example, chimpanzees and other primates can use both attention getters and requests for action in tri- cross-species comparisons adic ways (e.g., alarm calls, food begs, or recruit- To determine whether the features of chim- ment solicitations). Furthermore, among both panzee gesture were typical of all apes, Tomasello human and nonhuman primates, many gestures are and his colleagues expanded their study to include used to manipulate behavior rather than either the , bonobos, orangutans, and siamangs (Call body or the mind. It is also likely that the gestural & Tomasello, 2007; Liebal, Call, & Tomasello, repertoires of both primates and humans are the 2004; Liebal, Pika, Call, & Tomasello, 2004; Lie- result of a combination of genetic expression and bal, Pika, & Tomasello, 2004, 2006; Pika, Liebal, & individual and social learning processes. Finally, Tomasello, 2003; Pika, Liebal, & Tomasello 2005). some of the distal and declarative (i.e., comment- Th e researchers gathered focal video data from two ing rather than requesting) uses of human gestures groups of each species and identifi ed intentional are strictly related to language, and there is evidence gestures according to the same criteria. In this way, that when great apes learn rudiments of human lan- the repertoires and gesture use of each species could guage, the use of indexical and symbolic gestures be directly compared. Somewhat surprisingly, the follows closely (see section on ape-human commu- authors found far more similarities than diff er- nication). ences between species in both the number and use of gestures. Th e authors identifi ed repertoires of iconic gestures between 20 and 30 gestures for each species, and One way in which ape and human gestures all of them involved a combination of visual and appear to diff er sharply from one another is their tactile elements. Notably, only the African apes use of representational elements. Humans use ( and ) used auditory gestures such as iconic gestures to represent objects or events by rec- clapping or banging objects. Th is inclusion of audi- reating an aspect of their referent’s shape, size, or tory elements may be related to the propensity for movement. Producing and interpreting this type of bimanual drumming, an ability found in only the gesture requires the ability to represent real-world African apes that some have claimed is linked to the referents by their salient aspects (e.g., using a round origins of music and language (Fitch, 2006). Aside gesture to refer to a ball). Iconic gestures are impor- from the diff erences in auditory gesture, all species tantly diff erent from incipient actions because included in the large comparative study appeared they represent actions through recreating a partic- to use gestures in very similar ways. For example, ular physical feature rather than indicate desired all species were sensitive to the gaze of others when actions by performing the initial movement of an

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uncompleted action. Th ere is scant evidence that similarities between the iconic gestures used by nonhuman primates are capable of spontaneously zoo gorillas and the signs used by language-trained producing signals with this type of representational gorillas, which often elaborated upon species-typ- relationship to objects or events in the world. Apes ical gestures in their symbolic communication. In can be specifi cally trained to make iconic gestures; their view, although certain aspects of gesture are however, a handful of studies have also reported use heritable (e.g., the predisposition to produce and of spontaneous iconic gestures with conspecifi cs in recognize certain movements as gestures), the cog- bonobos and gorillas. Savage-Rumbaugh, Wilker- nitive abilities great apes use during gestural com- son, and Bakeman (1977), and Savage-Rumbaugh munication (e.g., selection of appropriate gestures, and Wilkerson (1978) reported high variability in awareness of gaze, fl exible use of diff erent gestures) both copulation positions and the facial are not so diff erent from human communication. expressions and gestures that accompanied them, Th ey argue that the sharp distinction made by some including prolonged mutual gaze, and a number authors between the symbolic use of gestures in of diff erent gestural and postural signals. Savage- humans and the nonsymbolic nature of primate Rumbaugh et al. (1977) argued that some gestures gestures is not as dramatic as it could be (though were iconically related to the desired change in the Byrne’s later fi ndings support sharp contrasts in partner’s behavior. For example, they observed that acquisition and symbolic use of gesture; see Genty a male would often physically push the female’s et al., 2009; Hobaiter & Byrne, 2011). Th is issue is body into a desired copulatory position, but some- further explored in the next section. times he would move his hand across the female’s body rather than pushing her. Th is latter movement Natural Gestural Communication of Apes: was interpreted as an iconic indication of what he Implications for Cognition wanted the female to do (but see Tomasello & Call, Th e increased interest in primate gesture in the 1997 for a diff erent interpretation). last 30 years has been largely motivated by a desire Tanner and Byrne (1993; 1996; 1999) argued to identify complex, fl exible, and intentional commu- that some captive lowland gorillas use iconic ges- nication in great apes. Reacting to fi ndings that apes tures similar to those observed by Savage-Rum- are poor vocal learners and their vocal repertoire baugh et al. (1977) among bonobos. Most of the appears largely fi xed, researchers turned to gestural observed gestures occurred during play, a few in communication for clues to cognitive adaptations agonistic contexts, and none in feeding situations. underlying ape communication and possible ante- In the context of play, an adult male appeared to use cedents to human language. Here we review what his arms iconically to indicate to another individual great apes’ gestures reveal about their potential for the direction in which he wanted her to move or complex, fl exible, intentional communication, and the action he wanted her to perform. Many of these we discuss what cognitive mechanisms are involved gestures appeared interchangeable in function. Th e in gesture. authors observed individual diff erences in the use Th e fact that apes can acquire novel manual of gestures, including an increase in their expres- skills and movements through observation of oth- sion during development, as well as changes in the ers makes great ape gesture a likely candidate in the preferred types of gestures as individuals matured search for social-cognitive adaptations and prelin- (Tanner & Byrne, 1999). Although some of their guistic cognitive foundations of language. Because developmental data were consistent with the onto- the focus on the gestural modality was, in large part, genetic ritualization hypothesis, Tanner and Byrne a reaction to the growing understanding of the vocal (1999) also argued that some aspects of gestural modality as infl exible and unlearned, it is unsurpris- communication, notably the comprehension of ing that most of the research on and discussion of gestures, are not learned but somehow “biologi- ape gestures has focused on either the fl exibility cally encoded” (e.g., innate; Byrne and colleagues of gesture use or potential mechanisms of gesture have developed this hypothesis in subsequent work, acquisition. which we discuss in the section on acquisition mechanisms). Furthermore, they argued that goril- Flexibility las have the potential for symbolic communication Th e fl exibility with which apes use gestures is men- and are anatomically and cognitively preadapted to tioned in nearly every recent study (Arbib, Liebal, & use iconic gestures. For example, they noted some Pika, 2008; Call & Tomasello, 2007; Genty, Breuer,

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Hobaiter, & Byrne, 2009; Liebal et al., 2006; Pika et unlikely that they carry any meaning outside the al., 2003; Pika, Liebal, & Tomasello, 2005; Pollick context in which they are produced, and recipients & de Waal, 2007). Flexibility is usually defi ned as must, therefore, rely on the surrounding social con- the number of diff erent contexts in which a gesture text to respond appropriately. If gestures cannot be is used, but it may also refer to the number of “func- interpreted outside their social contexts, then they tional contexts” (i.e., social goal resulting from the are weak signals, and their relevance to human gesture rather than type of social interaction in which language origins is more questionable. Recently, the gesture occurs). Pollick and de Waal (2007) mea- Cartmill and Byrne (2010) proposed analyzing ape sured the relative fl exibility of gestures and vocaliza- gestures for “intentional meaning,” categorizing tions in captive groups of chimpanzees and bonobos them by how probabilistically they are associated and compared them within and among groups and with achieving specifi c social goals. By identifying species. Th ey observed that manual gestures were examples of gestures that have “goal-outcome used in a wide range of contexts both within and matches” (where the outcome of the interac- between groups, but that the use of vocalizations and tion matches the goal attributed to the signaler), facial expressions was limited to specifi c contexts and one can determine how often a particular gesture did not vary between groups. is associated with a particular goal. Cartmill and Pollick and de Waal (2007) also found that mul- Byrne argue that gestures used frequently with a timodal signals (gestures accompanied by vocal- single goal-outcome match have specifi c meanings. izations) were more likely to elicit responses in Th e authors applied this analysis to gestures made bonobos than in chimpanzees. Th is combination by three captive groups of orangutans and found of gesture with vocalization (which occurs rarely in that more than half of the gestures had predictable gorillas and orangutans) may have particular impor- meanings. Importantly, the authors attempted to tance in the origins of language. In adult humans validate their attributions of meaning by observing who are fl uent speakers of a language, gesture and whether gesturers persisted in their communica- speech are tightly linked in time (McNeill, 1992), tive attempts following diff erent types of recipient and synchronization of gesture and vocalization reactions, and found that orangutans were more occurs as early as 9–15 weeks of age (Fogel & Han- likely to persist when the reaction did not match nan, 1985). Th e extent to which apes are able to the gesture’s presumed meaning. Th eir persistence synchronize vocalizations with gestures when com- demonstrated that the gesturers’ goals had not been municating with conspecifi cs has not received much fulfi lled by the responses to the initial gestures and, attention, though it appears to occur only rarely thus, supported the experimenters’ attributions of (if at all in some species). Chimpanzees’ ability to meaning to those gestures. produce synchronous vocal and gestural signals to Th e balance between fl exibility and meaning communicate with humans is currently being stud- poses a problem for the discussion of gesture and ied (see later). its usefulness as a tool to understand the cognition underlying ape communication. On the one hand, Meaning if gestures have very specifi c meanings, then they Th e fact that apes use gestures in more than one should demonstrate a very tight correspondence context and use more than one gesture in each con- with specifi c contexts, and it might be diffi cult to text is often used as evidence that gestures are used determine whether they are used intentionally or intentionally. Th is lack of one-to-one correspon- refl exively in response to environmental stimuli. dence between stimulus and signal is often referred On the other hand, if gestures are too fl exible, they to as “means-ends disassociation” (Bruner, 1981) cannot be useful as communicative signals and their and provides evidence that gestures are not auto- function is unclear. One way in which gestures matic responses to specifi c external stimuli but are could demonstrate fl exibility without sacrifi cing rather employed voluntarily. Establishing that ape meaning is in apes’ ability to use them strategically gestures are not mechanical responses is important in response to various properties of the intended when comparing them to language or attributing recipients (e.g., attention, knowledge, social status). cognitive processes to signalers, but the focus on By investigating the behavior of the recipient prior establishing fl exibility has, in some cases, led to a to the gesture, it is possible to study what social fac- view in which all gestures are multifunctional. If tors are important in predicting the choice and use all gestures are truly multifunctional, then it is of a gesture.

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Strategic Communication 2003; Whiten et al., 1999). It is clear that apes have Because gestures are not broadcast openly like the potential to learn novel manual actions from vocalizations, it is often trivial to identify the ges- others, and they are able to use acquired actions to turer’s intended recipient (and indeed many stud- communicate when encouraged by human experi- ies use directedness as a criterion of intentional menters. Given this potential, one might expect use). Because the recipient is usually apparent, that ape communicative gestures would be socially researchers can ask more detailed questions about learned and would display cultural variation in their what aspects of the recipient the signaler takes into forms or uses between diff erent sites. account when gesturing. Several studies have indi- Local traditions involving the presence or varia- cated, for example, that apes are able to take the tion of manual actions, such as tool use, food pro- recipient’s visual attention into account, choosing cessing, and grooming, have been reported in wild appropriate modalities based on whether they can great apes (e.g., Whiten et al., 2001; van Schaik et or cannot be seen (Call & Tomasello, 2007; Tan- al, 2003; Hobaiter & Byrne, 2010; also see Byrne, ner & Byrne, 1993). Th ere is also some indication 2004; Byrne et al. 2004 for review and discussion that they may continue to monitor the other’s visual of studying nonhuman culture.). Th ere is no evi- attention throughout a communicative exchange dence, however, that manual gestures show simi- (Genty et al., 2009). Apes also combine gesture into lar levels of group specifi city. Studies consistently sequences or exchanges with others, and the tran- report that gestures are either highly idiosyncratic sitions between diff erent gestures may reveal more or highly shared by all individuals of a species and about communicative strategies than the specifi c that there are few (if any) group-specifi c gestures or gestures used. For example, apes might quickly esca- traditions involving gesture. Th e gestures of a gorilla late to a fully functional shove when trying to dis- in a Brazilian zoo are just as likely to resemble those place a subordinate individual, but attempt a wider of a gorilla in a Swedish zoo as they are those of range of gestures when attempting to coerce a dom- a gorilla in the same group. Because no local ges- inant individual to move from a choice spot. Such tural traditions have developed, there is no evidence strategies have the potential to reveal the decision that gestures are socially learned. Only two plausi- process underlying gesture use. It can be diffi cult, ble alternatives have been off ered: gestures are either however, to interpret the cognitive processes under- ritualized from the fi rst movements of functional lying communication with conspecifi cs because of actions (ontogenetic ritualization) or they are genet- the inability to control environmental and social ically inherited. factors. Because of this, many studies of strategic Ontogenetic ritualization of functional move- use of gesture are conducted using ape-to-human ments into communicative signals is exemplifi ed in communication (see section on human-directed human infants during the development of some early communication). gestures such as raising the arms to indicate a desire to be carried. In this process, what was once a func- Acquisition Mechanisms tional movement (raising both arms to grab onto One of the most important questions raised the mother while she picks up the infant) becomes by studies of ape gesture is the problem of acqui- stereotyped into only the fi rst part of the action (the sition. In nonhuman primates, gesture is regarded arm raise) as the recipient learns to respond to the as having greater potential for social learning and fi rst part of the action. Th is is an eff ective mecha- cultural transmission than vocalization. Both apes nism for creating gestures from actions, and it seems and monkeys are able to learn new manual actions a likely candidate for many ape gestures (Tomasello by observing others performing them (see review & Camaioni, 1997; Tomasello & Call, 2007), par- in Whiten, 2000), and apes can acquire novel ticularly for tactile gestures that resemble functional communicative signs and gestures from humans movements such as brushing, pulling, or pushing. (e.g., Gardner & Gardner, 1969; Shapiro & Galdi- It is more diffi cult, however, to attribute ontoge- kas, 1999; Tomasello & Camaioni, 1997). Addi- netic ritualization to gestures that do not resemble a tionally, most of the population-specifi c behaviors movement associated with a functional action (as in described in reports of culture in wild apes involve the case of clapping or performing a headstand). It manual tasks, such as tool use or grooming tech- is also important to note that ritualization is primar- niques, indicating that social learning of manual ily an individual learning process. No social learning actions occurs in wild populations (van Schaik et al., is implied and thus every individual must undergo

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the same process of reducing functional actions to canalization into physical forms and potential mes- ritualized gestures. sages that are species-typicalî (Hobaiter & Byrne, Th e theory of ontogenetic ritualization has 2011). Th is explanation does not imply that there been criticized recently by Byrne and his colleagues would be no individual diff erences in gesture form (Genty et al., 2009; Hobaiter & Byrne, 2011). Th ey or use, that social interactions would not infl uence argue that, because ontogenetic ritualization must the form and use of gestures, or that gestures would occur de novo with every individual and every ges- be used in a hardwired refl exive way, but rather that ture, the chances of each individual acquiring a sim- all members of a species are biologically predisposed ilar form for a gesture ritualized from an action are to use a certain set of gestural forms and meanings very low. Furthermore, although the conditioning given a typical rearing environment. inherent in ritualization might lead an individual to It may not be reasonable to assume that a sin- use an incipient movement as a gesture, it does not gle mechanism underlies the development of all require that either individual understand the ges- ape gestures. It seems most likely that gestures are ture as a means of communicating a particular desire acquired through a variety of mechanisms. Even the and, thus, would not necessarily lead to the ability gestures of prelinguistic human infants are probably for one individual to both produce and comprehend acquired through a range of mechanisms including the same gesture. Even assuming that the production ritualization (for incipient actions such as the arm or comprehension of a gesture could be generalized raise) and observation (for conventional gestures, from use with a specifi c individual to the rest of the such as nodding to mean yes). group, each individual must (at minimum) acquire A detailed longitudinal study early in develop- each gesture from the perspective of both signaler ment would be needed to determine whether apes and receiver through ontogenetic ritualization. acquire gestures through ontogenetic ritualization. Byrne and his colleagues stress that ontogenetic rit- If so, one would expect to see young infants begin ualization is a likely acquisition mechanism only with functional actions and slowly reduce down the for those gestures that resemble incipient actions size and eff ort of their gestures until they are ineff ec- of common species-typical actions, for which every tive and somewhat standardized. Th rough this type individual has frequently both initiated and been of study, one could also determine whether infants the recipient of the original actions. Furthermore, had to receive the same ritualization process to com- close analysis of two gorilla actions and gestures prehend the same gesture directed toward them. that seemed likely candidates for ontogenetic ritual- It might also be the case that an ontogenetic ritu- ization revealed little similarity between the specifi c alization process is combined with something like movements of the gestures and those that initiated imitation recognition (e.g., Nielsen, Collier-Baker, the actions, weakening the theory that the gestures Davis, & Suddendorf, 2005) such that once an ape were ritualized from the actions (Hobaiter & Byrne, had ritualized an action to a gesture, it could rec- 2011). Byrne and colleagues further argue that, for ognize similar movements produced by others and ontogenetic ritualization to result in the same gesture ascribe the same goals to the other ape. Th is com- in several individuals, the same ritualization process bination of individual learning and generalization is must have taken place for each individual in exactly attractive as a potential mechanism for gesture acqui- the same way; otherwise, we would expect that each sition and use, but it relies heavily on the assumption might use a diff erent gesture to initiate a particular that apes can attribute goals to one another. Th ough type of interaction, arising from diff erences in the the patterns of gesture use suggest that apes respond actions or responses during ritualization. to one another’s attention, gestures, and responses in Hobaiter and Byrne (2011) report high overlap a dynamic way, there is no evidence that they attrib- of gestural repertoires between groups of the same ute goals to gesturing individuals. Controlled labora- species studied at diff erent sites, and also between tory studies can assess the ability of apes to attribute species of great apes. Th e authors report a 60% over- goals to others, but whether they do so in their natu- lap between chimpanzee and gorilla gestural reper- ral communication is likely to remain a question for toires and an 80% overlap between chimpanzee and speculation and debate. repertoires. Th ey report 24 gesture types shared between the 3 genera and conclude that many Comparison to Human Gesture ape gestures are not only species-typical but are, It is clear that ape gestures are diff erent from indeed, ìfamily-typical.î Th ey propose that the nat- those used by humans. Human gestures are almost ural repertoire of ape gestures are a result of “genetic always framed within linguistic exchanges and

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reference external objects, events, or ideas through ing the path of a ball after it was thrown). Only symbolic, metaphoric, or iconic means. It is unclear, the fi rst type would directly resemble the action a however, exactly how the gestures of great apes dif- person would take when performing an action. fer. Tomasello and Camaioni (1997) characterized Th ough some ape gestures do bear resemblance to apes’ gestures as dyadic, imperative, and ritual- the actions an ape would take when directly manip- ized, and children’s gestures as triadic, declarative, ulating another (e.g., grabbing the air near another and learned. Th is distinction provides an excellent individual without coming into contact or shooing framework for comparison, but may be an oversim- another away), it is not apparent whether any of plifi cation: the diff erence might be one of degree these gestures “represent” objects or events. With- rather than kind. Th ere is some indication that apes out evidence that apes are using these gestures rep- use gesture triadically; for example, when they off er resentationally, it is unclear what can be gained by or request food or objects (e.g., Liebal et al., 2006). labeling some gestures “iconic.” If iconic gestures Th ese interactions are triadic in that they involve do, however, provide some indication that apes can an object external to both animals in the dyad, use, elicit, and share mental representations through but in all cases one of the animals is touching the gesture, then one would expect the strongest indi- object, so they could also be perceived as part of cations of intentional use (response waiting, per- the dyad. Something similar seems to occur when sistence, elaboration, etc.) to accompany these apes use gesture to indicate places they would like to gestures. Unfortunately, because iconic gestures are be groomed (Pika & Mitani, 2006). Chimpanzees described only rarely in great apes, it would be dif- use an exaggerated scratch on their own bodies to fi cult to fully answer this question beyond catalogu- indicate where they would like another to groom ing and describing anecdotal examples of iconic them. Th is gesture seems to have deictic and triadic gesture when they occur (but see Bates and Byrne, properties by drawing attention to a specifi c area, 2007 for a discussion of using anecdotes to study but it is diff erent from a human mother and infant complex cognition). sharing attention and gesturing toward an external Recently, Russon and Andrews (2010) addressed object. Again, the question remains whether it is a the issues of very rare events and iconicity by ana- diff erence of kind or degree. lyzing descriptions of extended iconic gesture Th e question of whether apes are capable of sequences used to elaborate a message (described by iconic gesture has also been the subject of some the authors as “pantomime”). Using observations debate. Th e cases of iconic gesture in captive gorillas of forest-living rehabilitant orangutans obtained that Tanner and Byrne (1993; 1996; 1999) reported from 20 years of descriptive data, they identifi ed 18 mainly consisted of indications of where one indi- cases of pantomime (14 of which were addressed vidual wanted another to travel or what position one to humans). Th ese extremely rare cases of elabo- wanted the other to take. Th ese types of gestures rated iconic gesture did display numerous markers are iconic because of their similarity to the move- of intentionality, and the signalers usually had clear ment the recipient would make when fulfi lling the goals. However, most of the events were taken from request. However, if these gestures began as direct written descriptions that had been initially recorded manipulation of the other’s body and were ritual- for other purposes, so systematic analysis of goals, ized into gestures that resembled either the start of types of elaboration, and measures of social cognition the manipulative action or an ineff ective smaller could not be performed. It is also notable that the version of the action, it is possible that they would vast majority of examples of pantomime described have much the same form as they would if the goril- were performed to humans, and all orangutans had las were representing the desired action iconically: prolonged contact with humans during the process moving the arm along the path that it would take if of rehabilitation. Given the paucity of observations manipulating the other. in this study and the orangutans’ extensive exposure In human gesture research, iconic gestures are to human culture, it remains unclear to what extent defi ned as “representational” gestures because they apes can use spontaneous gesture representationally refer to objects, actions, or relations by recreating with one another, or at all. an aspect of their referent’s shape or movement (McNeill, 1992). Moreover, in an iconic gesture, the Insights from Studies of Conspecifi c Gestures hand can represent either a hand grasping an object So what have studies of gesture revealed about or performing an action (e.g., throwing a ball), or the cognitive specializations of apes? It seems represent an object or action itself (e.g., indicat- that apes use at least some of their gestures inten-

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tionally with the expectation of a specifi c behavioral by the diffi culty of controlling for various social and response (as indicated by response waiting, persis- environmental variables. Attributing particular cog- tence, and elaboration). It is unclear whether apes nitive processes to either signaler or receiver in a gesture with the intention to communicate desires or communicative exchange is tricky, and it is diffi cult with the intention of eliciting particular behaviors to narrow down the range of possible explanations from others. Th ough the philosophical and cogni- for an animal signaling or responding to a signal in tive implications of these two possibilities diff er, the a particular way. Experiments performed on captive functional outcome is much the same: gestures are populations attempt to introduce environmental used to fulfi ll the gesturer’s goals by causing specifi c controls (e.g., by restricting visibility or introducing behaviors in others. Th e preferential use of visual specifi c items as a way to manipulate the probability gestures when the recipient is watching demon- of observing communication about a specifi c type strates that apes take the visual attention of others of stimulus (e.g., Barros, Boere, Mello, & Tomaz, into account before signaling. All studies indicate 2002; Cheney & Seyfarth, 1990). Observers then that apes are able to use gesture voluntarily (i.e., record subsequent changes in animals’ signaling they do not gesture automatically in response to or in how they respond. Th is can be an eff ective certain stimuli). Gestures also seem less likely than method for testing changes in animals’ actions in facial expressions or vocalizations to be designed to or reactions to a particular type of environment, elicit emotional reactions in recipients—they can but the behavior of other individuals in the group be subtle movements, are directed at specifi c indi- remains an essential but uncontrolled variable. Th is viduals, and often get no reaction whatsoever. Ape means that it is diffi cult to ask questions about how gestures may or may not have meanings that can be animals react to particular types of behavior. One interpreted outside of the context in which they are must either wait until the right animal produces produced. As with most primate signals, it is likely the desired behavior in exactly the right conditions, that the recipient learns to extract a gesture’s mean- or forgo the naturalness of the exchange and opt ing from a combination of signal form and context. instead to use a human experimenter as a commu- Only playback studies or carefully designed experi- nication partner. ments will allow us to determine whether gestures Experiments in which apes communicate with themselves are perceived as having meaning without human experimenters fall into two categories: those being contextualized in an ongoing interaction. in which the animals are taught to interact using Future studies should be designed to provide evi- a human-designed communication system (“artifi - dence for mechanisms of gesture acquisition and how cial” or “taught” language studies), and those that gestures are perceived. Gesture has thus far proven attempt to elicit the animals’ natural communicative itself a useful tool for studying the cognition of the signals or responses. Each contributes something to signaler prior to and during gesture use, but it has our understanding of the abilities and communica- not yet been used to address questions of the recipi- tive potential of diff erent species and, in turn, each ent’s perceptions or understanding. It is our hope that presents challenges and limitations on what can be future studies will attempt to determine how much learned about the scope and use of communicative apes understand about gesture events. For exam- abilities in apes. ple, do recipients attribute goals and/or intentions to the gesturer? Do gesturers have intent to inform “Artifi cial Language” Studies or merely to aff ect behavior? Because gesture often Artifi cial language studies attempt to teach occurs in bouts during which both parties produce infant apes to use and respond to symbolic commu- signals, there is great potential to investigate the nication with human caretakers. Usually, the apes changing dynamics during which a signaler becomes are reared with human caregivers in enriched, often recipient and then signaler again. One might also ask human-like, environments focusing on fostering whether gesture is used to “negotiate” or arrive at a communicative play and encouraging the apes to compromised outcome in extended interactions in use the taught linguistic medium to request treats which the goals of two individuals are competing. and activities. Th e earliest attempts used spoken English (Hayes & Hayes, 1951), but after discover- Human-Directed Gestural Communication ing that apes lack the ability to mimic vocal sounds, Observational studies of communication between researchers focused their attempts on systems of nonhuman primates are limited in their conclusions written or manual signs. Following the success of

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Gardner and Gardner (1969) in teaching an infant or the creation of new signs, however, has been sig- chimpanzee (ASL), inter- nifi cantly lacking. Th ere have been a few reports of est in exploring ape communication in the visual apes inventing or combining known signs to refer modality (using either American Sign Language or to novel ideas or objects (e.g., Fouts & Mills, 1997; visual symbols) took off . Patterson, 1980; Patterson & Cohn, 1990), but no ape habitually combined or created new signs learning and use to dramatically increase its vocabulary. Th is is an Artifi cial language studies have been conducted important observation because studies of primate on gorillas, chimpanzees, bonobos, and orang- communication have overwhelmingly focused on utans, and all have demonstrated extensive ability the search for syntactic rules in primate communi- in producing and comprehending manual signs or cation systems as clues to the origins of human lan- symbols (Gardner & Gardner, 1969; Miles, 1990; guage (e.g., Arnold & Zuberbühler, 2006; Genty & Patterson & Linden 1981; Savage-Rumbaugh, Byrne, 2010). It is notable, then, that even when Shanker, & Taylor, 1998). Th ese studies with signed provided with individual units that are analogous or symbolic languages revealed that great apes pos- to human words (i.e., referential, arbitrary, taught), sess many communicative abilities once attributed apes do not display any aptitude in combining the only to humans—most importantly, perhaps, the units in a systematic or meaningful way. Th e only ability to communicate using arbitrary symbols that consistent “syntactic” rule observed in taught lan- are not linked to internal states. guage studies was a modality ordering preference in Th ough techniques and successes have varied which an ape consistently used a keyboard symbol from study to study, all taught-language experi- fi rst followed by a gesture (Greenfi eld & Savage- ments have demonstrated that apes can learn to Rumbaugh, 1990). Th is ordering rule was likely map arbitrary symbols onto real world referents based on facilitating movement following commu- and to use these symbols to communicate their nication and it lacked the added meaning associ- desires. Moreover, several have indicated that apes ated with syntactic structure in human language. can acquire these symbols from passive observation Although their abilities to employ syntax during of others as well as from direct instruction (Fouts, language production appear very limited, apes in Fouts, & van Canfort, 1989; Gardner & Gardner, these studies have demonstrated great success at 1969; Savage-Rumbaugh et al., 1998). Th is ability perceiving and responding to syntactic changes in to acquire communicative signs through passive human language. Th e best example is the bonobo, observation is of great interest to those interested in , who was able to respond appropriately to comparisons between primate communication and a range of commands varying diff erent syntactic human language. Apes can be trained to associate properties (e.g., “place the X on the Y” and “place symbols with objects through conditioning or shap- the Y on the X in the Z”). Kanzi even responded ing (where an experimenter physically manipulates more appropriately than a two-year-old child to the ape’s hands to perform the desired behavior), commands containing recursive changes (Savage- but the acquisition of such symbols through obser- Rumbaugh et al., 1993). vation of others is a characteristic most often asso- Overall, the ape language studies have left us ciated with human language learning. However, it with more questions than answers (see also chap- is notable that at least some of the communicative ter 19 of this volume). As we become more aware abilities (using arbitrary symbols and learning these of the extent of apes’ ability to use complex sym- symbols from observation of others) have also been bolic communication in experimental settings, the shown in free- ranging apes when taught to request gap between their potential for such communica- specifi c foods at a feeding station (Shapiro & Galdi- tion and the apparent lack of such features in their kas, 1999). natural communication systems is widened. Artifi - cial language studies demonstrate what a species is syntax capable of given exactly the right confi guration of It was hoped that, once apes were given the environmental infl uences, but they cannot provide right environment and an arbitrary symbolic sys- much information about how the abilities would tem, they would show many elements of human have arisen in the fi rst place in a natural environ- language that were apparently lacking in their own ment without devoted teachers and a preexisting communication systems. Evidence for use of syntax linguistic framework.

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Spontaneous Human-Directed Hostetter, Wesley, & Hopkins, 2004; Liebal, Pika, Communication Call, et al., 2004). Studies in which apes are encouraged to com- Studies in which human experimenters respond municate with a human experimenter through their “inappropriately” or do not fulfi ll the desires of the own spontaneous (i.e.,, not taught) behavior attempt ape provide information about what apes do to over- to remove some of the artifi ciality from the taught come failed communicative attempts. Leavens, Rus- language studies and yet elicit behavior that might sell, and Hopkins (2005) designed an experiment be diffi cult to observe in conspecifi c interactions. in which chimpanzees that have requested one food By requiring apes to communicate with a human, item from an experimenter are then given only part researchers can more eff ectively control for social of the food or an undesirable food instead. Th ey variables such as the eye gaze, location, and response found that the chimpanzees persisted in their com- of the communication partner. In many of these municative attempts and elaborated the attempts paradigms, apes must communicate with humans in by using new gestures when they were not given order to obtain a food or another resource that they the entire desired food. Expanding on this analysis, cannot obtain directly. Th is design introduces what Cartmill and Byrne (2007) presented orangutans some have called the “problem space,” an artifi cially with a similar protocol and found that their strat- imposed distance between signaler and receiver that egies diff ered based on whether they had been par- elicits diff erent types of behaviors than those one tially successful in communicating (given part of the would see if the apes were free to act directly on desired food) or unsuccessful (given the undesirable their environment (e.g., Leavens, Hopkins & Bard, food). When partially successful, orangutans used 2005). In these situations, apes must fi gure out a previously attempted gestures and repeated each ges- way to cross the problem space by using the human ture more. When unsuccessful, orangutans avoided experimenter as a tool to obtain a result they can- failed signals and attempted more novel gestures, not achieve directly. Th ese types of experiments are trying each only once or twice. Because the orang- very eff ective at identifying the cognitive processes utans were not more likely to repeat the last signal underlying communication, but they tell us little they attempted following a partial reward, the results about how and whether these processes operate in cannot be explained by a simple operant condition- communicative interactions with conspecifi cs. ing account. Subjects remembered which gestures and actions they attempted; reattempting behaviors communicative strategies from the full set when they had been partially suc- Experimenters have used the problem space cre- cessful in obtaining the desired food and avoiding ated by the distance between ape and human to them when they had failed. Th is study demonstrated study the types and sequences of gestures apes pro- that apes have a greater sensitivity to the responses of duce when they cannot move freely in relation to the recipient and to the success of their own commu- their recipient. In these studies, experimenters are nication than had been previously thought. able to control the reactions and the attention of the human recipient and thus observe what apes pointing do in situations where recipients do not perceive Many ape-to-human communication experi- the communicative attempts or do not respond as ments have focused on the forms of communica- expected. Studies in which apes must request food tion rather than the strategies. Th ese studies mostly from human experimenters who are either looking address the questions of whether apes understand away or have their backs turned have largely sup- pointing and whether they themselves point. Point- ported the conclusions of observational studies that ing is one of the important milestones in child apes attend to the visual attention of others and use development (Bates, Camaioni, & Volterra, 1975; visual gestures more often when they can be seen Bruner 1983). It is thought to be important in (Liebal, Call et al., 2004; Liebal, Pika, Call, et al., allowing triadic communication, establishing join 2004; Poss, Kubar, Stoinski, & Hopkins, 2006). attention, and developing theory of mind (Akhtar Th ese studies have also gone beyond the fi ndings & Tomasello, 2000; Baldwin, 1993; Butterworth, of the observational work, concluding that, when 2003). Th e cognitive mechanism behind pointing the recipient is looking away, some apes use atten- in infants is hotly debated, with infant pointing hav- tion-getting behaviors (such as auditory gestures) or ing both “rich” and “lean” interpretations accord- move to locations where they can be seen (Leavens, ing to whether the researcher believes that infants

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are attempting to change the minds or merely the and cognitive abilities demonstrated by very young actions of others when they point (for a review see children and absent in captive apes. Apes reared in Tomasello, Carpenter, & Liszkowski, 2007). human enriched environments have opportunities to Pointing has gained prominence in debates about develop skills and motivations (e.g., desires to share what makes humans diff erent from apes (e.g., Toma- attention or cooperate) absent in the natural rearing sello, 2006), with some authors strongly claiming that environments of great apes. Abilities such as theory apes do not point (Povinelli, Bering, & Giambrone, of mind, shared intentionality, declarative commu- 2003). In response to these claims, Leavens, Hop- nication, and displaced reference might develop dur- kins and their colleagues conducted a large num- ing ontogeny only under ideal circumstances (i.e., ber of studies with captive chimpanzees specifi cally our own), and only then with the encouragement to elicit pointing (Leavens, Hopkins & Bard, 1996, and support of profi cient adult tutors. Th is might 2005; Leavens, 2004). In a range of studies, Leavens help to explain why language-trained apes (and and Hopkins have demonstrated that captive apes human-reared apes, in general) exhibit many cogni- will indicate distal objects to human experimenters by tive skills that naturally reared apes do not (Leavens, extending an arm or fi nger toward the object. Th ere Hopkins, & Bard, 2005; Lyn, Russell, & Hopkins, has been some disagreement about whether the form 2010). Th ese human-reared culturally-enriched apes of the gesture in apes (usually a whole hand exten- are often referred to as “enculturated,” and have sion) constituted pointing, but most researchers cur- demonstrated abilities both in comprehending and rently agree that captive apes can deictically indicate producing declarative pointing (Lyn et al., 2010). objects to humans when given the right environment. Studies with enculturated apes show that apes Th e focus then shifted to the motivation behind the have the capacity to acquire complex cognitive and act of pointing itself: whether the motivation of the communicative abilities when reared in the “right” gesturer is to change the behavior of the other individ- way. Th ese results shift the question from “Why ual (imperative pointing) or the contents of the other’s do apes lack these abilities?” to “Why don’t apes mind (declarative pointing). Some have claimed that develop these abilities outside human-constructed imperative gestures do not constitute intentional com- contexts?” It is clear that the early rearing environ- munication because they are not produced to change ment has an enormous eff ect on the development the knowledge state of another (Baron-Cohen, 1999). of the cognitive skills and motivations necessary for Tomasello and colleagues argue that apes may complex communication. Th e role of the develop- point to request objects, but they do not point to share mental environment in diff erent species and during interest or to inform others (Tomasello, Carpenter, evolutionary history must, therefore, be called on to & Liszkowski, 2007). Tomasello and colleagues con- help reconcile diff erences between the abilities and tend that such declarative pointing arises from and common practices of a species’ communication. helps to foster the collaborative culture-rich environ- ment in which humans are reared. Children point Th e Importance of Development to share attention, to indicate novel things, and to Monkeys, apes, and humans all mature slowly inform or help. Th ese abilities are all associated with and have an extremely long period of maternal human culture and are central to human social cog- dependence compared to most other mammals nition. It is possible that captive apes do not possess (Harvey & Clutton-Brock, 1985). It is likely that the same cognitive abilities for social intelligence as this period is needed to allow the acquisition and humans and, therefore, lack the understanding and development of social and material skills needed ability to perform declarative gestures (Herrmann, to survive in primates’ complex environments. Call, Hernanez-Lloreda, Hare, & Tomasello, 2007). Moreover, the slow rate of maturation in primates Others argue, however, that the ability is present provides a period of time during which the brain in apes, but diff erences in the rearing environment continues to grow, and the infants’ environment lead to a lack of motivation for declarative gesturing during this period can shape both brain structure (Lyn, Russell, & Hopkins, 2010). and brain function, including the development of cognitive skills. Enculturation Th e advantage of being raised from birth in the Social Environment enriched environment of a human culture may pro- Arguably, the complex social environments vide the motivation behind many communicative in which many primates live present the greatest

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cognitive challenges to the developing individual. benefi ts in many species of birds: females may prefer It is likely that even the development of material males with more complex songs, and territorial dis- and technological skills in primates requires the use putes may be won by the individual with the larg- of complex social skills, because many are acquired est repertoire of songs (e.g., Mountjoy & Lemon, through observation of knowledgeable individu- 1996; Searcy, 1992; for a review see Catchpole & als. Mastering the complexity of a primate society Slater, 2003). requires a great deal of learning, and this need for Instead of learning to produce new calls during learning was likely an important evolutionary force development, monkeys and apes mainly learn how in the extension of the human developmental period to interpret them. Primates may learn to narrow (Dunbar, 1995; Flinn et al., 2005). down the contexts in which they give a particular Social complexity is positively correlated with call so that they call only in response to a particular size in primates (Dunbar, 1995, chap- type of stimulus (Seyfarth & Cheney, 1986), but the ter 6 of this volume; Reader & Laland, 2002). Th is underlying motivation to call and the types of calls evolutionary increase in the part of the brain asso- used appear to be mainly innate. It is the receiv- ciated with executive function is most likely driven ers (rather than the senders) who have the most to by the need to understand social dynamics, forge learn in primate vocal communication (Seyfarth & alliances, and manage relationships with other indi- Cheney, 2003). Primates must learn how to respond viduals over many years. Longer juvenile periods are to specifi c calls—pairing particular sounds with also associated with increased brain size and social external events and learning to react appropriately complexity and all three likely co-evolved (Joff e, in each case. However, the structures of many types 1997). Bjorklund and colleagues have argued that of calls seem designed to elicit immediate physio- these three factors form the foundation from which logical responses in others (e.g., alarm calls and fear; human intelligence evolved (Bjorklund & Bering, see Rendall et al., 2009) and much of the learning 2003; Bjorklund & Rosenberg, 2005). that does occur can be accomplished in large part by Primates have a wide range of skills and relation- behavioral conditioning (Seyfarth et al., 2010). ships they must learn before they reach adult com- petency. All primates must be profi cient learners; Gestural Communication however, it is unclear whether the primary or only Great apes have slower and more extended peri- cognitive specialization of humans and other pri- ods of development and maturation than monkeys. mates is an amazing ability to learn, or whether they Th ey also use manual gestures to communicate to a are pre-adapted for learning, reasoning, and under- much greater extent than monkeys do. As we dis- standing in some particular domains. We argue that cussed earlier, there is no evidence that ape gestures primates have evolved many specifi c cognitive spe- are socially learned from others. However, the fl exi- cializations in the social domain and that some of bility with which apes use gestures in diff erent con- these cognitive adaptations are apparent in the way texts and in response to diff erent aspects of the social primates communicate with others. environment likely requires considerable develop- mental learning and experience. If gestures develop Vocal Communication through a process of ontogenetic ritualization, it In terms of vocal communication, nonhuman would require many exposures to and opportunities primates possess no extraordinary production skills. to perform a particular action before it became a ges- Th eir vocal repertoires are highly fi xed and it is ture. Infants would begin by attempting to manip- almost impossible for them to acquire new calls, ulate their partners directly, and as their partners even when cross-fostered by other species (includ- began to anticipate their desires, the infants would ing humans) (Gardner & Gardner, 1969; Owren, slowly learn that only part of the movement was nec- Dieter, Seyfarth, & Cheney,1992). It is clear that essary to elicit the desired response. Th is ritualization primates’ extended period of development is not process would allow an ape to learn which move- used to acquire a large repertoire of calls. In con- ments are eff ective indicators of desired actions, and trast, species that display remarkable vocal learning, also when these diff erent gestures are eff ective. If the such as songbirds or parrots, devote a considerable forms of gestures are largely innate, then a period amount of time during development to the acquisi- of learning when diff erent gestures are likely to be tion and practice of complex songs. Th e breadth and eff ective (e.g., use the visual modality only when vis- accuracy of the acquired repertoire has direct fi tness ible) would be required. Much like vervet monkey

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infants must learn which species deserve alarm calls only beginning to explore the role of the social envi- and which should be ignored (Seyfarth & Cheney, ronment in shaping the development of socio-cog- 1986), infant apes would learn which contexts and nitive and communicative abilities in primates. We social variables were important in determining how must also ask what external environmental pressures and when to gesture. We propose that primates, and led to rearing environments that could shape and especially great apes, have evolved cognitive special- develop these abilities. Comparative studies of both izations to attend to and learn to use social variables ontogeny and rearing hold great promise to provide (such as the identity, visual attention, and domi- insight into the relationships between the physical nance of communication partners) during commu- and social environment and the development of nication, and particularly during gesture. cognitive and communicative abilities. Cross-spe- cies studies comparing ontogenetic environments Comparative Development: Th e Future of and the development of cognitive and communica- the Field? tive abilities are essential to understand the unique Th e importance of development in shaping pri- combination of environmental, social, and ontoge- mate communication has been investigated in only netic factors that led to the capacity for culture and a limited number of studies, and most of them have language in the human lineage. focused on vocal communication (e.g., Hauser, 1996; Pistorio, Vintch, & Wang, 2006; Seyfarth Future Directions & Cheney, 1997, but see Tomasello et al., 1994). 1. What features of the rearing environment Additionally, little is known about the relationships infl uence the development of communicative and between socio-cognitive abilities (such as under- cognitive complexity? standing visual attention, gaze following, and rec- 2. What aspects of ape gesture systems (if any) ognizing individuals) and the structure and use of are learned? communication systems in nonhuman primates. 3. Do nonhuman primates process gesture and In humans, language develops alongside a whole vocalization in similar ways? range of cognitive abilities, building upon some and 4. Why do nonhuman primates so rarely providing the foundation for others. Th e relation- synchronize vocal and gestural modalities given ship between the emergence of language and other that it is so common in human communication? cognitive abilities is well studied in humans; sim- ilar work is needed to understand the relationship References between communication and cognition in nonhu- Akhtar, N., & Tomasello, M. (2000). Th e social nature of words man primates. and word learning. In R. Golinkoff . (Ed.), Becoming a word Comparative developmental studies are needed learner: A debate on lexical acquisition (pp. 115–135). 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Primates raised in human envi- Oxford, England: Oxford University Press. ronments fi lled with cooperation, tool use, symbolic Barros, M., Boere, V., Mello, E. L., & Tomaz, C. (2002). Reac- tions to potential predators in captive-born marmosets (Cal- communication, and teaching develop abilities that lithrix penicillata). International Journal of , 23, they do not naturally exhibit in the wild. We are 443–454.

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