David A. Leavens & Timothy P. Racine Joint Attention in Apes and Humans Are Humans Unique? Abstract: Joint attention is the ability to intentionally co-orient towards a common focus. This ability develops in a protracted, mosaic fashion in humans. We review evidence of joint attention in humans and great apes, finding that great apes display every phenomenon described as joint attention in humans, although there is considerable variation among apes of different rearing histories. We conclude that there is little evidence for human species-unique cognitive adaptations in the non-verbal communication of humans in the first 18 months of life. This conclusion is consistent with the Narrative Practice Hypothesis (NPH) because the NPH posits training in folk psychological narratives as a basis for folk psychological competence. Humans communicate before they can speak. As far as we know, all other animals communicate without speech or any communicative system analogous to speech. There are points of comparison between language and non-human animal systems of communication (e.g., Burling, 1993; Hauser et al., 2002), but there is no evidence that any other organism tells stories, with or without language. Even in humans, storytelling is an advanced communicative skill, which takes years to develop. Yet, as Hutto (2009 [this issue]) points out, mainstream theory in cognitive developmental psychology interprets the pre-speech communicative behaviour of human infants as evidence for the early acquisition, in our species, of a complex, if tacit, Correspondence: David A. Leavens, Psychology Department, School of Life Sciences, University of Sussex, Falmer, East Sussex, BN1 9QH. Email: davidl@sussex.ac.uk Journal of Consciousness Studies, 16, No. 6–8, 2009, pp. 240–67 Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 241 story-like understanding of mental processes in others. This is especially apparent in discussions of joint attention, which, in humans, is widely taken as evidence for a nascent theory of mind (ToM). Joint attention is the intentional co-orientation of two or more organisms to the same locus. By ‘intentional’ we mean that at least one of the organisms displays a pattern of behaviour that defines a sequence as goaldirected: the signaller might point to a distant locus, alternate his or her gaze between that locus and an interlocutor, and, in the face of miscommunication, attempt to repair that communication by persisting in its signalling or elaborating upon the initial signal (Bard, 1992; Bates et al., 1975; Leavens, 2004; Leavens et al., 2005a). Thus, joint attention is a class of distinctively patterned sequences of behaviour defined by objective, publicly available behavioural measures of visual orienting, and the deployment of visual, auditory, and tactile signals (Leavens, 2004; Leavens et al., 2005a). According to a variety of theoretical perspectives on human cognitive development, joint attention is diagnostic of the acquisition of complex representations that mediate young infants’ social interactions (reviewed by, e.g., Hutto, 2008a; Racine & Carpendale, 2007; Reddy, 1996; Reddy & Morris, 2004). According to these kinds of theoretical perspectives, later linguistic competence simply gives symbolic expression to pre-existing, but previously unspoken, representations of what are taken to be the invisible causes of the behaviour of babies’ social partners. Even when granting that epistemic concepts, such as beliefs and knowledge, might be co-constituted by linguistic input, it is nevertheless widely argued that infants as young as 12 months of age, who manifestly lack the linguistic competence to verbally express pre-epistemic mental states pertaining to intentionality, somehow construe others as psychological agents with mental stances vis-à-vis events in the world (e.g., Tomasello, 1995; among many others). In making his case, Hutto focuses on a form of narrative practice that makes use of certain kind of narrative, which he calls a folk psychological (FP) narrative: FP narratives are a specific sub-type of narrative; distinguished by their content — they are about people (or their analogues) who act for reasons of the kind that minimally implicates beliefs and desires (Hutto, 2008b, p. 178). These narratives assist children in integrating their initial, practical capacities to attribute intentions, desires and beliefs so that they become able to produce and understand accounts of why we and Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 242 D.A. LEAVENS AND T.P. RACINE others act for reasons. Importantly, Hutto does not claim that engaging in such practices is the origin of children’s first understanding of desires and beliefs. The Narrative Practice Hypothesis (NPH) is an account of the human development of ‘FP-competence’, which situates this competence in the narrative experiences of human children. According to this view, organisms that lack exposure to these FP narratives will not develop FP-competence (see, esp., Hutto, 2008a, ch. 6–8). Thus, by extension, non-linguistic or pre-linguistic organisms could not display FP-competence, even in an incipient form. This is the proposal examined, here. In this article, we review joint attentional skills in human primates and consider whether speciesunique kinds of social cognition are required in order for such behaviours to emerge. We then turn to a consideration of these skills in nonhuman primates and conclude that on empirical and logical grounds there is little evidence for qualitatively different cognitive capacities operating in humans and their nearest living relatives, the great apes. If this is the case, it favours Hutto’s proposal (that it is only through engaging in narrative practices that one comes by full FP-competence) because we also deny that the social cognitive abilities shared by humans and other primates rest on their possessing bona fide ‘Theory of Mind’ abilities. As such, our findings may lend some much needed ammunition to Hutto’s cause since a standard complaint against the NPH is that it depends on children already having a theory of mind if they are to engage in the kind of narrative practice that Hutto describes. Joint Attention in Humans According to a widely used descriptive scheme by Mundy and his colleagues (e.g., Mundy & Gomes, 1998), the development of joint attention in humans can be charted by measuring their increasing skills in initiating behaviour regulation (IBR), initiating joint attention (IJA), and responding to joint attention (RJA). Examples of these developmental milestones include reaching out the hand in the apparent request for delivery of an object (IBR), pointing to a distant dog (IJA), and following a caregiver’s head turn so that the child is looking in the same direction as the caregiver (RJA). Some researchers restrict the term ‘joint attention’ to RJA, or to IJA plus RJA, but we use the term, here, in a more inclusive sense, including IBR, RJA, IJA and related triadic phenomena such as social referencing (use of emotional information about novel objects to regulate one’s own reaction to those Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 243 objects) and imitation (Bard & Leavens, 2008; Leavens et al., 2008; Striano & Bertin, 2005). As IBR skills develop, infants become increasingly competent at manipulating adults into acting on the world for them, for example, by raising their arms to be picked up and cuddled or, later, pointing to dropped toys or out-of reach bottles, until an adult retrieves them. IBR is conceptually the same sort of thing as protoimperative signalling, a term introduced by Bates and her colleagues (Bates et al., 1975). Considered in many theoretical perspectives to be an important developmental milestone, IBR describes the onset of intentional use of ritualized or conventionalized gestures in our species. Again, by ‘intentional’ we simply mean that babies exhibiting IBR are working toward a contextually appropriate end. For example, Blake, O’Rourke, and Borzellino (1994) reported that ‘reaching out’ gestures displayed in the context of out-of-reach items were displayed by 8-month-old infants with accompanying vocalizations, but the same gestures by 4-month-old infants in the same eliciting contexts were not accompanied by vocalizations; they interpreted this bimodal elaboration at 8 months as evidence for the onset of intentional, gestural communication. Similarly, Bates and her colleagues (1975) noted that only in the latter part of the first year of life do babies begin to visually monitor adult caregivers during goal-directed sequences, as though they are beginning to perceive the relevance of the adults for achieving their aims. Pointing with the index finger in apparent requests for object delivery (protoimperative pointing) appears at about 12 months of age, although reaching out with all fingers extended occurs several months earlier (Blake et al., 1992; 1994; Leung & Rheingold, 1981; Lock et al., 1994). For many years developmental psychologists thought that pointing (for any reason) was a uniquely human activity (see, e.g., Butterworth & Grover, 1988; Povinelli et al., 2003), and therefore even IBR was widely taken to signify human species-unique psychological processes. However, as we will see, great apes and other animals that depend upon humans or conspecifics for provisioning also develop signalling strategies that meet the same objective criteria for IBR, so IBR is a widespread mammalian phenomenon (Arbib et al., 2008; Bard, 1992; Leavens, 2004; Leavens & Hopkins, 1999; Leavens et al., 2008; 2009). Although IBR is subject to a variety of theoretical interpretations, few would dispute that, empirically, sometime near the end of the first year of life, human children, in Western and some other cultures, begin to point and otherwise use manual gestures in apparent attempts to manipulate others to act on the world for them. Few Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 244 D.A. LEAVENS AND T.P. RACINE researchers have assessed the degree to which babies respond to requests (RBR — but see, e.g., Mundy & Gomes, 1998); rather surprisingly, the comprehension of protoimperative pointing, per se, has not been well-studied in experimental and naturalistic contexts (see Colonnesi et al., 2008, for a recent corrective). Psychologists do traditionally distinguish IJA from RJA. Developmentally, these skills seem to be distinct, in so far as they are only rarely found to be significantly correlated competencies either at the same age or longitudinally (e.g., Desrochers et al., 1995; Mundy & Gomes, 1998; Striano & Bertin, 2005). At some risk of over-simplification, RJA seems to have an earlier onset than IJA and is more frequently associated with later language skills (e.g., Baldwin, 1993; 1995; Morales et al., 1998; Mundy & Gomez, 1998; but see Carpenter et al., 1998, for the opposite pattern; and Flom et al., 2007, for a review of the development of RJA). RJA has a complex developmental profile, which has been studied in human infancy with two primary eliciting contexts: either an experimenter turns his or her gaze (with or without head turns) or the experimenter points (to near and far targets). The development of RJA has been reviewed by Adamson (Adamson, 1996; Adamson & Bakeman, 1991), Butterworth (e.g., Butterworth, 2001; Butterworth & Grover, 1988), Doherty (2006), and Reddy (2003), among many others. Although even 6-month-old human infants will turn their heads in the same direction as an adult’s head turn, it is not until about 10 months of age that babies turn their heads to the correct side more than the opposite side (e.g., Corkum & Moore, 1995; 1998). Not until about 18 months of age will babies follow an adult’s gaze to a specific target behind themselves (e.g., Butterworth & Grover, 1988). Beginning at about 10 months of age, babies in cultures that use manual pointing will follow pointing gestures to close objects, and then, as with gaze-following, to ever more distant targets (e.g., Adamson, 1996). In terms of IJA, babies in most cultures studied, to date, evince a developmental sequence from exhibition of self at about 10 months of age, followed by exhibition of objects, giving objects to others and, finally, at about a year of age, pointing to objects and events (e.g., Adamson, 1996; Miles, 1990). This kind of pointing is referred to as protodeclarative pointing (e.g., Baron-Cohen, 1995; Bates et al., 1975). Bates and her colleagues (1975) originally portrayed protoimperative and protodeclarative signalling as types of non-verbal requests: protoimperatives were requests to deliver objects, to pick up a child, or to convey the child somewhere (use of adults to obtain Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 245 objects or objectives), whereas protodeclaratives were requests to engage with the child (use of objects to obtain adult attention). Although many contemporary writers construe protodeclarative pointing as springing from a different motivational or conceptual structure than protoimperative pointing (e.g., Baron-Cohen, 1989; 1995; Franco & Butterworth, 1996; Tomasello, 2006; Tomasello et al., 2007), numerous others have noted that there is no empirical evidence that forces the interpretation that protodeclarative pointing is anything other than the use of objects to obtain the attention or an affective response from a caregiver (Leavens, 2004; Leavens et al., 2005a; Moore & Corkum, 1994); indeed, Bates and her colleagues (1975), in introducing these terms, were explicit in defining protodeclaratives as a subset of imperative signals — these points were described as the use of objects to elicit some kind of adult behavioural response (reviewed by Leavens et al., 2009), and it is in this sense of the term that we will evaluate evidence for protodeclarative behaviour in nonhumans (we take as an example of protodeclarative pointing, the ‘informative’ pointing described by Liszkowski et al., 2006). Joint Attention and the Mind Infants as young as 12 months of age are widely believed to appreciate the invisible mental causes of the behaviour of their caregivers (e.g., Baron-Cohen, 1989; 1995; Meltzoff, 1995; Tomasello, 1995; 1999; 2006; see reviews in Colonnesi et al., 2008; Racine & Carpendale, 2007; among others). In particular, protodeclarative pointing, which emerges early in the second year of life (in Western populations), is taken to be the quintessential sign of mental state awareness in humans: why would one point to change the knowledge state of an observer, the argument goes, if one does not appreciate that there are minds with mental contents? Thus, when babies point to events or objects in their environments, in apparent attempts to share attention to these objects with their social partners, this is taken as evidence that infants are attempting to influence the state of mind of their interlocutors, which entails that they have at least a tacit understanding of others as mental beings (e.g., Baron-Cohen, 1995; Camaioni et al., 2004; Legerstee & Barillas, 2003; Liszkowski et al., 2004; Tomasello, 1995). Developmental psychologists rely on a number of mental process models in which mental states (a) exist; (b) reside entirely within the cranium; (c) are available to introspection; (d) cause behaviour; and therefore can be (e) indexed by overt behaviour. Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 246 D.A. LEAVENS AND T.P. RACINE Although a full review is beyond the scope of this paper, in recent years these kinds of mentalistic interpretations of infant behaviour have been increasingly criticized on epistemological and empirical grounds by numerous researchers, including ourselves (e.g., Leavens, 1998; 2002; 2004; 2006; Leavens et al., 2005a; 2008; 2009; Racine & Carpendale, 2007; 2008; Racine et al., 2008; Susswein & Racine, 2008; 2009) and many others (e.g., Boesch, 2007; Doherty, 2006; Hutto, 2008a; 2008b; 2008c; Leudar & Costall, 2004; Moore & Corkum, 1994; Reddy, 1996; Reddy & Morris, 2004). For example, Moore and Corkum (1994) pointed out that there is no compelling evidence that young babies cannot learn, through experience, the typical consequences of their own signalling behaviour — so that babies with mothers who respond with positive and intense emotional displays to the babies’ points, could learn the socially embedded, contingent structure of communication in the absence of any mental state representation. Indeed, Corkum and Moore (1998) demonstrated that babies could be trained to follow gaze two months earlier than is typical, simply by exposing babies to a training regimen; hence, this aspect of RJA can be learned through relevant experience. Because we are unaware of any set of empirical findings that unambiguously rules out learning from experience as a route into the development of joint attention, a brief digression on principles of learning is warranted. A training regimen is nothing more nor less than life experience that is intentionally manipulated; if a behaviour is acquired, yet not explicitly trained, this does not imply that the behaviour was not learned. A fortiori, this would not imply that the capacity was innate (see Bateson & Mameli, 2007). Examples are legion in which human babies display some behavioural competency at joint attention, and researchers conclude that there is a ‘poverty’ of environmental stimuli to account for this novel skill (see Leudar & Costall, 2004, for a critique of this argument). This cannot follow from the present state of knowledge in which we do not know nearly enough, in terms of natural history, about how parents respond to babies’ communicative signals to conclude that babies have not been differentially reinforced to display such joint attentional skills as gaze-following and pointing. If, for example, positive affective displays are reliable consequences of children’s pointing, then pointing to elicit positive emotion can be both untrained and learned (e.g., Leavens, 2004; Leavens et al., 2005a). There are few empirical data on parents’ responses to infant pointing behaviour, but what few studies have been performed are consistent with a learning model. For example, Masataka (1995; 2003) reported that parents respond more positively to speech-like infant Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 247 vocalizations; because index-finger extensions more frequently accompany speech-like vocalizations than non-speech-like vocalizations, index-finger extensions are, thus, subject to what he terms ‘inadvertent conditioning of index-finger extension’ (2003, p. 74). There is no aspect of human joint attention in infancy (IBR, RJA & IJA) that simply could not have been acquired through experience (i.e., learned). An astonishingly large number of contemporary researchers seem to believe, incorrectly, that any behaviour acquired as a result of reinforcement must be cognitively uninteresting, or, as Reddy and Morris (2004) concisely observed in a related context, ‘that anything learned from reinforcement cannot constitute genuine knowledge’ (p. 650). What is acquired through learning, trained or incidental, is knowledge — real knowledge, in real organisms, operating in the real world. Thus, to suggest that humans might learn to exhibit joint attention skills through experience is to simply assert that we have no a priori basis to promulgate a theoretical perspective that human infants, alone among vertebrates, are so appallingly obtuse that evolution had to come up with human species-specific cognitive modules to do the same things that, as we shall see, other animals manage to do without such modules. Others have noted that social engagement is suffused with intense subjective awareness that can only be experienced in participation, and is only weakly caricatured in any objective, third-party analysis; without the rapport that characterizes the experience of self-other engagement (e.g., Reddy, 2003). As Reddy and Morris poignantly put it, Such definitions [of intentional communication] presume the existence of a prior script, the isolation of the communicator from the receiver, and a separation of the act of communication from its content, and make the loneliness of the subject almost insurmountable (2004, p. 653). Leudar and Costall (2004) discussed how the use of an informationtheoretic model of communication — in which previously existing messages are encoded, transmitted through some channel, received in some sensory modality, then decoded, appraised, and finally responded to — force a telementational view of even early human communication: individuals must infer the meaning of communicative acts. In the telementational perspective, the possibility of directly perceiving meaning in the shared sensory space of interactants, outside their crania, is not permissible (see also, e.g., Johnson, 2001; King, 2004; Leavens et al., 2008; 2009; Racine & Carpendale, 2007; 2008; Savage-Rumbaugh et al., 1998; Susswein & Racine, 2009). Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 248 D.A. LEAVENS AND T.P. RACINE Thus, the reliance of psychology on telementational models to interpret human infant communication creates the illusion of a chasm between babies and their caregivers that can only be bridged through a computational process involving either inference or simulation. Such a perspective is belied by the experience of any parent who has held their young babies in their arms, played peek-a-boo, tickled their young child, etc.; in these contexts we do not doubt that we are directly engaged with our children, long before the ages at which they might start to point to distant objects or reliably follow our gaze to distant events. Communication in early infancy is emotionally intense, vibrantly dynamic, and, as far as we can tell, non-inferential. The earliest communication of human infants is not a meeting of minds across an epistemological abyss, but a direct interdigitation of feeling in which it is often difficult to point out an ownership of separate feelings at specific times. If we can engage so directly with our children before they achieve joint attentional skills, then telementational accounts of joint attention impose a wholly unnecessary psychical cleavage upon infancy at approximately one year of age. There is developmental change in communicative abilities at approximately this age, but there is no empirical evidence that this involves the kind of psychological re-birth into a state of extreme solipsism required by telementational perspectives, which can only be bridged through computational processes; rather, the common ground simply expands, with novel opportunities to apply the emotional routines of early infancy to increasingly disparate elements in a common sphere of experience (e.g., Adamson & Bakeman, 1991; Bard, 1998; Bard & Leavens, 2008; Reddy, 2003; Striano & Bertin, 2005).1 As Gregory Bateson pointed out years ago, mentality is a distributed phenomenon, reaching out across the transductive envelope of the neuromuscular and neurosensory junctions: … we may say that ‘mind’ is immanent in those circuits of the brain which are complete within the brain. Or that mind is immanent in circuits that are complete within the system, brain plus body. Or, finally, that mind is immanent in the larger system — man plus environment (1972, p. 317, emphasis in original). [1] One of the greatest intellectual tragedies of the present age is that scientists often assess the communicative behaviour of animals that have never experienced these kinds of early communion and conclude that these animals lack basic joint attention skills because of their evolutionary histories, rather than their specific, impoverished or very different species-typical developmental histories (Bard & Leavens, 2008; Leavens, 1998; 2004; Leavens et al., 2008; Racine et al., 2008). Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 249 Recently, numerous researchers from different traditions have independently converged upon a view of cognition as ‘embodied’ (e.g., Clark, 1997; De Jaegher & Di Paolo, 2007; Gallagher, 2001; 2008; Griffiths & Stotz, 2000; Johnson, 2001; Lakoff & Johnson, 1999; Leavens et al., 2008; Lickliter, 2008; Leudar & Costall, 2004; King, 2004; Racine & Carpendale, 2008; Reddy & Morris, 2004). The central significance of these emerging perspectives on cognition, at least for the purposes of the present article, is that increasing numbers of researchers are taking seriously the notion that minds, meanings and even evolutionary adaptations are properties of systems, with specific histories, embedded in particular sociocultural contexts. If communication between caregiver and child (of any species) crucially involves parameters outside the participating neural systems, then a full scientific understanding of the development of joint attention (in any species) must take into account the specific learning histories of the interactants, the emotional tones of the engagements, the quality of the relationships between the interactants; everything, in short, that influences what babies and their caregivers might come to expect in the specific unfolding of their interactions (Bard & Leavens, 2008; Boesch, 2007; Leavens et al., 2008). These expectations form the warp through which the weft of creative performance is drawn — surprise, a key essential of rudimentary humour, can only exist against the less variant properties of the familiar (e.g., King, 2004; SavageRumbaugh, 1991). This kind of dynamic engagement is referred to as intersubjectivity (Trevarthen, 1977; 1998; Trevarthen & Hubley, 1978). Earlier dyadic engagement is referred to as primary intersubjectivity, and the suite of triadic skills comprising joint attentional competence is known as secondary intersubjectivity. Thus, while Hutto and many others argue that FP-competence is ‘socioculturally grounded’ (Hutto, 2008a, p. x) — with Hutto making the specific case that this is because FP-competence is acquired through narrative practice — it is nevertheless widely believed that the much earlier human capacity for secondary intersubjectivity involves species-unique competencies for engagement with others (e.g., Hutto, 2008a, ch. 6; Tomasello, 1999; Tomasello et al., 2007; Zlatev, 2008).2 If this is true, [2] Arguments are also made for human-unique aspects of primary intersubjectivity, but there is little empirical support for this idea; however, this lies beyond the scope of the present article (see, e.g., Bard, 1998; 2007; Bard et al., 2005; Susswein & Racine, 2008; reviewed by Tomonaga, 2007). Generally speaking, human infants stand out from the other ape infants in their slower development of locomotor competence and their unusual vocal behaviour, including babbling and the development of phonation over the first year of life. Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 250 D.A. LEAVENS AND T.P. RACINE then we might expect to find fundamental behavioural discontinuities between humans and the other apes in their joint attentional competencies; we now briefly review the empirical data to determine whether this is indeed the case (see Gómez, 1998, for an earlier review of joint attention in apes). Intersubjective Primates Gallagher and Hutto (2008) explored a triad of competencies to account for developmental precursors to FP-competencies. These were (a) intersubjective perception; (b) pragmatically contextualized (i.e., secondary) intersubjectivity; and (c) narrative competency (Gallagher & Hutto, 2008, p. 20). Here we briefly examine the evidence for the second of these competencies, pragmatically contextualized joint attention, in nonhuman primates and other animals in each of the three domains reviewed above. Initiating behavioural regulation There are many examples of manual gestures used by both wild and captive great apes in which they manipulate the behaviour of others. Here we list a few illustrative examples. Begging gestures. Chimpanzees and orangutans exhibit apparent ‘request’ gestures in dyadic contexts, both in the wild and in captivity. Systematic studies have demonstrated that ape infants initiate nursing and play bouts and, later, both infants and adults display begging gestures, in which the palm is supinated, oriented towards their mothers or other social partners, and often with outstretched arm, typically beginning between 9 and 12 months of age (e.g., Bard, 1990; 1992; Goodall, 1986; Leavens & Hopkins, 1998; Leavens et al., 2004a; Plooij, 1978; Teleki, 1973; see Figure 1). Directed scratching (touching). Chimpanzees in the Kibale National Park, Uganda, have been recently reported to scratch parts of their own bodies in apparent requests for their grooming partners to groom that area (Pika & Mitani, 2006). Other systematic studies have shown that apes often touch parts of their own bodies in apparent requests for another ape or a human to direct tickles or other activities at the location indicated (e.g., Plooij, 1978; Tanner et al., 2006; Otherwise, at least in the domains studied to date, early competencies of human and ape infants are remarkably similar: early in infancy, representatives of both species display neonatal imitation (Bard, 2007; Myowa-Yamakoshi et al., 2004), face-recognition (Myowa-Yamakoshi et al., 2005), and recognition of direct gaze (Bard et al., 1992; Myowa-Yamakoshi et al., 2003). Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 251 Figure 1 A juvenile chimpanzee displays a typical begging gesture through cage mesh. Palm is supinated (facing up), hand held in a slightly ‘cupped’ posture, and the arm is outstretched towards the experimenter. Photograph by David A. Leavens. Tomasello et al., 1985). Included in this category might be points to oneself, in apparent requests to elicit action directed at a particular place on the signaller’s body. For example, Yerkes (1943) described an episode in which a caregiver had examined the oral cavity of a chimpanzee named Booey, who had gone off his food. After a fruitless search for dental problems, Booey pointed to one of its own teeth, where the caretaker then found an abscess, upon further scrutiny. Pointing to request.3 There are hundreds of published examples of apes pointing in apparent requests for food or other object delivery [3] There has been a debate over the structural aspects of pointing, with some researchers limiting the category of pointing to ‘canonical’ pointing with an outstretched arm and index finger only (e.g., Butterworth, 2003; Povinelli & Davis, 1994; Povinelli et al., 2003). We simply note, here, that (a) not all humans always point with their index fingers (e.g., Enfield, 2001; Wilkins, 2003); (b) researchers who study infant communication have generally failed to find significant differences between ‘reaching-to-request’ and ‘[index-finger] pointing-to-request’ in terms of accompanying visual checking towards caregivers or vocalizations, and therefore it is often quite ambiguous whether children are iconically reaching or indexically pointing with their whole hands (e.g., Leung & Rheingold, 1981; Masur, 1983; reviewed by Leavens & Hopkins, 1999); and (c) some infancy researchers now include pointing with the whole hand as part of their coding scheme for pointing (e.g., O’Neill, 1996; Brooks and Meltzoff, 2002). See Leavens (2004) for extended discussion of this point. Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 252 D.A. LEAVENS AND T.P. RACINE Figure 2 Merv, a young adult chimpanzee, points with his index finger to a juice bottle, located on the ground, just out of camera view. Photograph by David A. Leavens, used with permission from the American Psychological Association (from Leavens & Hopkins, 1998). (reviewed by Leavens, 2004; Leavens & Hopkins, 1999; Leavens et al., 2009; see Figure 2). Although other forms of gesturing may be frequent in wild populations (Pika, 2008), pointing of any form seems almost nonexistent. Nevertheless, pointing is very frequently displayed by captive apes, and occasionally displayed by more distantly related monkeys (e.g., Hess et al., 1993; Mitchell & Anderson, 1997).4 Apes point in apparent requests for food delivery, but also to request other objects, such as shoes (e.g., Leavens et al., 1996), tools required to open containers containing desirable food (e.g., Call & Tomasello, 1994; Russell et al., 2005; Whiten, 2000), and to manipulate sexual partners to assume different positions for copulation (Savage-Rumbaugh et al., 1977). There are also reports of pointing by dolphins (through orientation of their bodies, Xitco et al., 2001) and, of course, many hunting dogs (‘pointers’) are routinely trained to orient towards fallen prey, by capitalizing upon some breeds’ propensities to freeze in the presence of prey. Very occasionally, researchers report training apes to point (e.g., Call & Tomasello, 1994; Woodruff [4] Intriguing claims to the effect that explicitly training monkeys to point results in generalized facilitation in other domains of social cognition have been reported by Blaschke and Ettlinger (1987) and Kumashiro and his colleagues (Kumashiro et al., 2002; 2003). Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 253 & Premack, 1979), but the vast majority of pointing by captive apes emerges ‘spontaneously’ (that is to say, in the absence of any explicit training). Numerous researchers have remarked on the apparent paucity of manual pointing in wild populations of apes (e.g., Butterworth, 2003; Povinelli et al., 2003; Tomasello et al., 2007). We have argued that the reason wild apes do not point manually is that they simply have no need (cf. Menzel, 1973): unlike human children and captive apes, wild apes virtually never experience a ‘Referential Problem Space’ in which they are dependent upon others to act on the world for them (e.g., Leavens et al., 2008; 2009). This is because wild apes achieve locomotor independence at approximately 5 months of age, and therefore can directly locomote to and manipulate any object that takes their interest. In contrast, both human children, by virtue of the large proportion of time they spend in restraints (car seats, feeding chairs, cots, papooses, etc.), and captive apes in cages, very frequently encounter desirable, but out-of-reach objects; in this Referential Problem Space, pointing to request delivery of these objects develops in both humans and captive apes (see Leavens, 2004; Leavens et al., 1996; 2005b; 2008; Leavens et al., 2009, for elaboration). Although apes frequently gesture between themselves (Pika, 2008), it is sometimes stated that apes do not point between themselves (e.g., Povinelli et al., 2003; Tomasello, 2006); in fact, this is rather far from the truth. Although infrequent, pointing between apes has been reported in the wild (Inoue-Nakamura & Matsuzawa, 1997; Veà & Sabater-Pi, 1998), among captive apes in zoo environments (de Waal, 1982), and among language-trained apes (Savage-Rumbaugh, 1986). For example, Savage-Rumbaugh (1986) described 37 instances of pointing between two chimpanzees, Sherman and Austin, who were working on a food-sharing task. In this task, the first chimpanzee selected a lexigram (an arbitrary visual symbol, representing a type of food), from a panel of lexigrams. The second chimpanzee was charged with retrieving the food from a tray, delivering half to the first chimpanzee, and then consuming the second half of that food item. The first chimpanzee frequently augmented his selection of the lexigram with a point to the food in the tray. According to the Referential Problem Space hypothesis, it is to be expected that this behaviour will be rare between apes, because, they usually do not depend upon other apes to act on the world for them (e.g., Leavens, 2004); in the example involving Sherman and Austin, they were explicitly trained to take turns and to share food, and ape-ape pointing emerged in this specific context. In terms of joint attention, successful pointing to request delivery of Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 254 D.A. LEAVENS AND T.P. RACINE objects requires the capture and re-direction of a caregiver’s attention to a specific locus, and the further conveyance of the expectancy that the caregiver will deliver that object to the signaller. Responding to joint attention There are also numerous demonstrations of RJA among the great apes, and other animals. Here we selectively concentrate on a few illustrative examples. Gaze- and point-following. Following the gaze of social partners, both ape and human, is well-demonstrated in great apes (reviewed by Leavens et al., 2008). It is well-demonstrated by systematic studies that apes follow humans’ gaze shifts (e.g., Itakura, 1996; Itakura & Tanaka, 1998; Povinelli & Eddy, 1996; Tomasello et al., 1999) and gaze-shifting of conspecifics (e.g., Tomasello et al., 1998) and that some great apes will also follow pointing and other deictic gestures (e.g., Call & Tomasello, 1994; Peignot & Anderson, 1999; Povinelli et al., 1990; Warneken & Tomasello, 2006), although, as with humans, this takes some time and experience to develop. Some apes that have experienced less day-to-day interaction with humans, such as those raised in institutional settings such as zoos and biomedical research centres, or animals raised in the wild and taken into institutional settings as juveniles, have displayed either a reluctance or an incapacity to follow human points (e.g., Hermann et al., 2007; Povinelli et al., 1997). However, we are unaware of any language-trained or homeraised ape who does not follow pointing; this pattern, taken together with the observations of ape-ape pointing, clearly demonstrates that, empirically, many great apes do easily follow pointing gestures. There is, thus, no evidence for a species-level incapacity for RJA.5 [5] There are numerous recent demonstrations of apes failing to follow pointing on initial presentation of experimental conditions (e.g., Hermann et al., 2007; Povinelli et al., 1997). Tomasello and his colleagues (e.g., 2007) interpret these kinds of findings as evidence to the effect that apes cannot recognize altruistic intentions in others; however, we note that it takes humans at least 9 to 12 months to acquire point-following, and some perfectly normal humans, evidently, make it to adulthood without understanding the referential significance of the pointing gesture (see Wilkins, 2003). One of us (Leavens) recalls a strange pursing of the lips displayed by his then fiancée towards food at a dinner — he failed utterly to follow what is the canonical pointing gesture for millions of people, worldwide: pointing with the lips (Enfield, 2001; Wilkins, 2003). We submit that his failure does not implicate a profound cognitive deficit in Leavens’s (much less the human species’) ability to recognize communicative intentions of one sort or another, but simply a lack of familiarity with this particular gesture. (A reviewer confused this logical argument with an anecdote: to be clear, Leavens really did fail to comprehend the canonical lip-pointing gesture — that is an empirical fact; logically, the incomprehension cannot be attributed to Leavens’s evolutionary history). Because so many apes (and other animals, including Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 255 Tactical communication. Great apes also alter the modality of their signalling, depending upon whether an observer is looking at them (i.e., they spontaneously discriminate visual attention; it was not explicitly trained). Thus, apes will display visual signals if an observer is looking at them, but switch to auditory or tactile signalling if the observer is facing away. This has been demonstrated in ape-ape communication (e.g., Liebal et al., 2006; Pika et al., 2003; 2005; Tomasello et al., 1994), as well as in communication with humans (Cartmill & Byrne, 2007; Hostetter et al., 2001; Leavens et al., 2004b; in press). Initiating joint attention Exhibition of self. This behaviour is commonplace in both wild and captive populations of great apes, and would include the kinds of self-directed gestures described above, as examples of initiating behavioural regulation (Pika & Mitani, 2006). In addition, apes and many other primates present their hindquarters in sexual solicitation and to signal submission (e.g., Goodall, 1986, for chimpanzees). Plooij (1978) describes infant chimpanzees presenting their backs to their mothers, accompanied by arms raised above their heads, in an exhibition of self that initiates tickling. Showing and giving objects. Systematic studies have demonstrated showing of objects in a variety of environmental and rearing contexts. For example, Plooij (1978) described the use of objects to elicit attention in wild chimpanzees, for example, grabbing an object and running away with it, while looking back at another ape. These kinds of behaviours are commonplace in apes, particularly juvenile apes. Russell, Bard and Adamson (1997) reported showing of a novel object to a favourite caregiver. Savage-Rumbaugh (1986) noted that while showing objects is a common part of both captive and wild ape repertoires, giving these objects to another is very atypical in captive populations. However, both showing and giving objects was reported for a sign-language-trained orangutan by Miles (1990) and languagetrained chimpanzees by Savage-Rumbaugh (1986), and Carpenter, Tomasello, and Savage-Rumbaugh (1995), among others. Moreover, bartering, the offering of low-quality food (e.g., peanut shells) for more desirable food (e.g., grapes) has been reported by Hyatt and Hopkins (1998) in laboratory chimpanzees at a biomedical research humans) clearly do follow pointing gestures, given adequate experience, failures to follow pointing are not diagnostic of any cognitive implication beyond a lack of either motivation or sufficient task-relevant experience to use the gesture. Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 256 D.A. LEAVENS AND T.P. RACINE facility; these apes differ from language-trained apes in having very reduced frequencies and durations of communicative engagement with humans. Protodeclarative pointing. Pointing with no apparent motivation to manipulate the observer to act on the indicated locus is a relatively rare behaviour among both wild and captive apes, but such acts are far from non-existent. The only well-described example of pointing that we have been able to find by a wild ape involved a bonobo pointing to hidden human observers, and looking back towards his troop — a quintessentially protodeclarative point (Veà & Sabater-Pi, 1998). Among captive apes, Witmer (1909) reported that Peter, a circus chimpanzee, would point to himself when asked where Peter was, and point to the indicated person (for example, one of his trainers) when asked where they were. In a systematic study of language comprehension spanning many months, Gua, a home-raised chimpanzee, pointed to her nose when asked where her nose was (Kellogg & Kellogg, 1933, see Figure 3). Systematic studies have demonstrated that virtually all great apes who have undergone language training can easily point informatively when asked to indicate the location of somebody or something and, also, to point to a picture of a named object (e.g., Gardner et al., 1989; Kellogg & Kellogg, 1933; Miles, 1990; SavageRumbaugh et al., 1998). Carpenter et al. (1995) reported a single instance of possible declarative pointing by a language-trained chimpanzee. It is important to emphasize that these examples are relatively rare and limited, for the most part, to language-trained apes operating in particular task environments. Even in these rare populations of language-trained apes, protodeclarative pointing is not nearly as frequent as in typical Western human infants, after about a year of age. However, as noted by Leavens and his colleagues (Leavens, 2004; Leavens et al., 2008; 2009), these apes, who have unusually rich exposure to language-using human communities, do sometimes point protodeclaratively. Leavens and his colleagues (Leavens, 2004; Leavens et al., 2005a; 2008; 2009) have speculated that protodeclarative pointing requires a social environment in which such acts reliably receive positive emotional responses — very few apes experience these kinds of social contingencies. As noted above, pointing to request the delivery of an object and pointing to request positive affect or attention are both instrumental acts (e.g., Leavens et al., 2005a; 2009); if this view is correct, then it can be only the rarest of circumstance in which human smiles, laughter and attention gain reinforcing properties for great apes. Because humans who develop protodeclarative pointing also have emotionally rich exposures to language-using Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 257 Figure 3 Gua pointed to her nose in response to the query ‘Where is your nose?’ (informative point) and also in response to the command, ‘Show me your nose’ (declarative point). Photograph from Kellogg and Kellogg (1933), courtesy of Jeff Kellogg. human communities, it is not logically possible to determine whether human protodeclarative pointing is best viewed as (a) an interaction of mammalian, primate, ape or human psychological adaptations with particular human sociocultural contexts or (b) an interaction of uniquely human psychological adaptations with particular human sociocultural contexts, the latter of which is the dominant perspective in psychology, today. However, the empirical data clearly show that it is not impossible for great apes to display protodeclarative pointing; thus, what we do not know is which experiences foster protodeclarative pointing in apes (or humans). Conclusion This brief review demonstrates that no element of joint attention in humans is beyond the reach of our nearest living relatives, the great apes. Some of these aspects, such as exhibition of self, use of objects to elicit attention, and requesting behaviours through manual gestures, are characteristic of apes in all environments, whereas some elements, such as pointing with the fingers, are largely (although not Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction 258 D.A. LEAVENS AND T.P. RACINE exclusively) restricted to captive environments, and other elements, such as apparently declarative behaviours, are primarily restricted to apes that have had, like human children, intensive exposure to human sociocultural environments. If representatives of closely related species display similar behavioural repertoires, and if these behavioural repertoires are even more similar after cross-fostering of one or both species, then this implicates epigenetic processes in behavioural acquisition (Leavens, 2004; Leavens et al., 2005b). In other words, apes display every major category of joint attention, including IBR, IJA and RJA; differences that exist between groups of apes with radically different rearing histories result in only minor differences in sub-categories of these major motivations. Great apes are ontogenetically flexible in their accommodation to different communicative environments (e.g., Bard, 1998; Bard & Leavens, 2008). Thus, wild apes, in contrast to captive apes, only rarely point with their hands, but they routinely display IBR (e.g., begging) and IJA (e.g., using objects to gain attention); RJA has been less systematically studied in wild populations, perhaps because of the difficulty in imposing the kinds of controls that characterize captive ape studies, but it would be very surprising, indeed, if captive apes but not wild apes displayed RJA. RJA has been well-documented in both ape-ape and ape-human communication by apes of large variety of different rearing histories. For another example, apes of virtually every background (barring isolation-reared animals) display IJA, although only a few display protodeclarative pointing. With respect to the NPH, the fact that apes display joint attention with and without exposure to humans does not either challenge or directly support the hypothesis. It does receive indirect support from the necessary entailments of our claim that great apes acquire most types of joint attention with no special training, presumably because, like humans, they learn from experience what are the usual consequences of their signals. People who study human children do not need to invoke qualitatively different modes of explanation to account for human communicative development; indeed, to the degree that apes display joint attention, the exercise is fraught with logical pitfalls and potential mythmongering (endless creation of causative entities that cannot be empirically verified, in principle). A particularly egregious example of this seems to be the claim by Povinelli and his colleagues that similar behaviour displayed by individuals of different species does not implicate similar mental processes in humans and non-humans (e.g., Povinelli & Giambrone, 2001; Povinelli et al., 2003). Yet, ironically, they support this claim by purporting to show Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction JOINT ATTENTION IN APES AND HUMANS 259 that apes and human children, in fact, behave dissimilarly, which — even if it were true — obviously cannot speak to the premise. The weaknesses of telementational approaches (summarized above) apply equally to the understanding of human infant and great ape cognition. What we have tried to show in the present review is that (a) either FP-competence is a necessary foundation for joint attention, and therefore it is a shared cognitive trait of humans and apes or (b) FP-competence is not a necessary foundation for joint attention in apes or humans. If the former is implausible, then the latter is a far stronger starting point for theory-building than the currently fashionable idea that humans require FP-competence to display joint attention, whereas other animals achieve joint attention through oldfashioned learning or, to put this another way, that joint attention in humans indexes FP-competence, but joint attention in animals indexes mere learning. The similarities between humans and apes in joint attention behaviours that we have reviewed, here, argue for psychological continuity between humans and their nearest living relatives, the great apes. Importantly for the NPH, it is by no means necessary to attribute a ‘Theory of Mind’ of any kind to great apes in accounting for their joint attentional skills, and it would be, besides, impossible to confirm this through experiment, even if we made such an attribution, because, like human infants, great apes cannot tell us about their mental functioning (e.g., Leavens et al., 2004a; 2004b). Thus, that great apes readily display every major category of joint attention described for human infants can be interpreted as being fully consistent with the NPH, which also denies to preverbal or nonverbal organisms the capacity to account for the behaviour of others in terms of folk psychological concepts such as intention and belief. Acknowledgements We thank our collaborators, especially Kim A. Bard, Jeremy I.M. Carpendale, William D. Hopkins, Jamie L. Russell, Noah Susswein, Brenda K. 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