Discussion post

Culture and Selective Social Learning in Wild and Captive Primates

Stuart K. Watson, Jennifer Botting, Andrew Whiten, and Erica van de Waal

Abstract Once thought to be a unique human trait, the presence of culture in non-human primates has been confirmed and studied by researchers for several decades. What has been discovered is evidence for between-group traditions in a wide range of primate taxa, including all of the great apes, macaques, capuchins and spider monkeys, as well as many non-primate species. The capacity to learn from others is a powerful means by which animals can acquire adaptive ways of interacting with their environment and each other without engaging in time- consuming and potentially risky trial-and-error learning. However, much remains to be understood about the exact mechanisms and processes that underpin social learning and how these lead to the cultures identified in wild populations of primates, including humans. In the current chapter, we review what is known about

The authors “Stuart K. Watson” and “Jennifer Botting” contributed equally. Order of authorship was determined by coin-toss.

S. K. Watson Centre for Social Learning and Cognitive Evolution, and Scottish Primate Research Group, School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK

J. Botting Centre for Social Learning and Cognitive Evolution, and Scottish Primate Research Group, School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK

Inkawu Vervet Project, Mawana Game Reserve, Swart Mfolozi, KwaZulu Natal, South Africa

Smithsonian National Zoological Park, Washington, DC, USA

A. Whiten Centre for Social Learning and Cognitive Evolution, and Scottish Primate Research Group, School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK

Inkawu Vervet Project, Mawana Game Reserve, Swart Mfolozi, KwaZulu Natal, South Africa e-mail: [email protected]

E. van de Waal (*) Inkawu Vervet Project, Mawana Game Reserve, Swart Mfolozi, KwaZulu Natal, South Africa

Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland e-mail: [email protected]

© Springer International Publishing AG, part of Springer Nature 2018 L. D. Di Paolo et al. (eds.), Evolution of Primate Social Cognition, Interdisciplinary Evolution Research 5, https://doi.org/10.1007/978-3-319-93776-2_14

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non-human primate culture with a particular emphasis on the emerging field of social learning biases. Theoreticians and field researchers alike have suggested that animals may exhibit biases in whom they obtain information from, either as by-products of social dynamics or as adaptive strategies that allow animals to selectively acquire the most useful information. Here, we review the theoretical arguments and current empirical evidence for proposed biases in social learning, including majority-based biases and model-based biases. We draw from field observations and experiments in both captive and wild populations to examine how information may be transferred between individuals and how this may affect the emergence of cultural behaviours across primate species.

Keywords Culture · Primates · Social learning biases · Social transmission mechanisms · Conformity · Model-based biases

1 Introduction

Culture pervades every aspect of human life, from the way we communicate and the values we hold to the way we think and shape our environment. The extent and complexity of human culture has created such a palpable gulf between us and other members of the animal kingdom that the capacity for culture has historically been argued to be unique to humans (e.g. Galef 1992). However, this depends on how culture is defined, operationalised and tested for. Here we adopt the definition offered by Reader and Laland (2003) that cultures are ‘group-typical behaviour patterns shared by members of a community that rely on socially learned and transmitted information’ (p. 151). This seems sufficiently broad to account for all instances which one might consider ‘cultural’ in humans, but it means that theoret- ically, culture might emerge in any species with sufficient propensity for social learning. We humans are pre-eminent (Dean et al. 2014) in our capacity for ‘cumu- lative culture’—the ability to modify learned behaviours to become more complex and/or efficient, which can be transmitted and further improved by others—but an increasingly large body of research shows that our fellow animals are also capable of a functionally significant degree of cultural inheritance and diversity.

The adaptive benefits of social learning appear clear; the alternative, individual innovation, is potentially costly as it may require a significant time or energy investment, produce only minor or non-existent rewards or be physically dangerous. Instead, the capacity to learn from others allows individuals to reap the benefits of others’ useful innovations whilst minimising the costs. Furthermore, this may benefit not only the learner but also any offspring or other kin to whom the behaviour subsequently spreads. In this sense, culture acts as nature’s ‘second inheritance system’ (Whiten 2005). However, social learning may not always be adaptive. An indiscriminate social learner runs the risk of copying costly or other suboptimal behaviours (Laland and Williams 1998; Kendal et al. 2005). To avoid these, the evolution of social learning ‘biases’ (or ‘strategies’ in some literature) has been

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predicted, to guide when to use social information and whom best to acquire it from (Giraldeau et al. 2002; Laland 2004).

This chapter reviews what is known about social learning in non-human primates, with particular emphasis on the cognitive biases that underpin it, and the important light it sheds on our understanding of the emergence, propagation and maintenance of culture. Studies of social learning in non-primate species will also be noted when pertinent, in order to situate the primate literature within a broader biological context.

2 Observations of Culture in the Wild

Early whispers of non-human primate culture were heard when, in 1953, a young Japanese macaque, Imo, carried pieces of sand-covered sweet potato to a stream and washed off the sand before eating them (Kawai 1965). In the months and years that followed, other macaques began using this technique, and it eventually became a common behaviour in Imo’s group, leading the researchers studying the macaques to label this behaviour as ‘pre-culture’. Whilst later scrutiny of the spread of sweet potato washing behaviour suggested it did not provide strong evidence for cultural transmission (e.g. due to factors such as human provisioning; Galef 1992), the case of the Japanese macaques established the study of social transmission and culture in wild primates, which led to a plethora of exciting discoveries in the animal kingdom.

A further influential finding came when, following observations of group differ- ences in chimpanzee behaviours across different sites (Goodall 1986; Boesch et al. 1994), Whiten et al. (1999, 2001) systematically collated data from seven long-term chimpanzee field sites across Africa and found evidence of multiple variations in behaviours between communities, inferred to be cultural. The researchers listed 39 behavioural traditions which were common (either customary or habitual) in some groups, yet absent in others, without obvious ecological explanation, ranging from handclasp grooming to different termite fishing and nut-cracking behaviours (see Fig. 1). The discovery of this large number of putative cultural variations in our closest relatives challenged the assumption of complex culture being uniquely human.

On the heels of these findings, researchers collated data from other great ape species. Van Schaik et al. (2003) conducted a similar analysis of behavioural traditions in orangutans across six different field sites and identified 24 cultural variants that were habitual or customary at some sites and absent at others. The authors concluded that orangutans also possess multiple-tradition cultures. A more recent analysis supports these earlier conclusions, finding that ecological and genetic differences accounted for only a small proportion of the variation seen between groups (Krützen et al. 2011). Emerging evidence has also been found for a number of traditions in wild gorillas (Robbins et al. 2016, but see Neadle et al. (2017) for a discussion on the ontogeny of food cleaning behaviours) and bonobos (Hohmann

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and Fruth 2003), although we have less information on bonobos than for chimpan- zees or orangutans.

Whilst the ‘exclusion’ method of inferring social learning where ecological or genetic explanations appear untenable can never be conclusively watertight (Laland and Janik 2006; Langergraber et al. 2011: Robbins et al. 2016, explicitly refer to the traditions they identify as ‘putative’), additional lines of evidence have more recently supported the role of social learning in the maintenance of the above behaviours. First, a series of diffusion experiments in which different foraging techniques are ‘seeded’ in different groups has shown that these will spread in ways that confirm a capacity to transmit and sustain multiple traditions (Whiten 2011; Whiten et al. 2016). Second, recent advances in statistical techniques have allowed researchers to assess the role of social learning in the spontaneous spread of a novel behaviour in the wild. For example, Hobaiter et al. (2014) used a dynamic form of network-based diffusion analysis (NBDA, Franz and Nunn 2009) to systematically chart the spread of a novel leaf-sponging behaviour in a group of wild chimpanzees via social transmission, providing the first direct evidence that at least some of the observed behavioural variation in wild chimpanzees is likely due to cultural learning. This conclusion is further supported by Lonsdorf (2006), who found a correlation between the amount of time infant chimpanzees spend with their mother and the rate at which they become proficient at termite fishing, as well as Luncz and Boesch (2014, see below) comparing neighbouring communities where neither genetic nor ecological appear able to explain behavioural variations. It is also worth noting that the exclusion method of identifying animal cultures has been criticised for being too conservative, as it precludes examination of ecologically driven cultural differences (Koops et al. 2014; Sanz and Morgan 2013).

Whilst the great apes, in particular chimpanzees, display the most diverse reper- toire of cultural behaviours documented thus far, the first candidates for cultural

Fig. 1 The putative cultures of wild chimpanzees (after Whiten 2005). ‘Customary’ acts are those typical in a community; ‘habitual’ are less frequent yet consistent with social learning. Each community displays its own profile of such local behavioural variants, providing evidence of a unique culture for each locality. Numbers identify behaviour patterns in the catalogue attached to Whiten et al. (1999). For a more recent and detailed version focused on nut-cracking variations, see Carvalho and McGrew (2012)

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behaviours came from monkeys. Evidence has since accrued that several monkey species exhibit their own forms of culture. Notably, Perry et al. (2003) described a number of ‘social customs’ found in some, but not all, groups of capuchins studied in Costa Rica. These included a number of social ‘games’ and other, seemingly bizarre, conventions such as poking fingers in each other’s nostrils and eyes. Whilst the functions of these conventions are difficult to pin down, the authors suggest that they may serve to enhance social bonds between participants and perhaps highlight them to others. Whatever the function, the distributions of conventions across groups are strongly suggestive of cultural transmission. Additionally, Santorelli et al. (2011) identified a number of behavioural traditions, many in the social domain, in wild spider monkeys, and peculiar stone-handling behaviours seen in numerous provi- sioned groups of Japanese macaques also appear to display the pattern of multiple, if narrowly constrained, cultural traditions (Leca et al. 2007).

Whilst it might be tempting for us to think of primates as distinctive in their capacity for cultural transmission, researchers have uncovered convincing evidence for culture in other animal taxa, notably in cetaceans and in birds. Whitehead and Rendell (2014) discuss evidence for a range of putative traditions in cetaceans, most notably in the domain of song transmission in the baleen whales (also well documented in birds; Slater 1986), but also including a number of foraging traditions (Krützen et al. 2005; Allen et al. 2013). Implementation of the aforementioned technique, NBDA, has provided some of the strongest evidence for social learning in the wild in any species, documenting the gradual spread of a particular foraging method, lob-tail feeding, in a population of over 600 humpback whales (Allen et al. 2013).

In addition to vocal culture, there may also be tentative evidence for tool-making traditions in birds. Hunt and Gray (2003) described evidence for sophisticated tool- making in wild New Caledonian crows and, finding that the distribution could not be linked to ecological correlates, suggested a role for social learning. They argued that the distribution of tool types across New Caledonia indicates cumulative technolog- ical culture. However, the extent to which the tool manufacture is necessarily socially learned remains in doubt, as hand-reared crows in captivity also display tool-making skills (Kenward et al. 2005, but see also Holzhaider et al. 2010), and experiments have failed to support social learning of alternative techniques (Logan et al. 2016). Recently, researchers also found that the experimental removal and replacement of individuals from a group of homing pigeons improved the efficiency of homing routes over successive generations through social learning and refine- ment, satisfying the main criteria for cumulative culture (Sasaki and Biro 2017). This finding is important not only for identifying a putative case of cumulative culture in a non-human species, a capacity many argue to be uniquely human, but also for emphasising that culture extends beyond foraging behaviour which is the primary focus of a majority of social learning studies.

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3 Mechanisms of Information Transmission

The study of the social learning processes that underlie culture can broadly be split into two main categories: mechanisms and biases. Mechanisms, or psychological processes, refer to the how of information transmission. Whereas biases (or strategies) refer to when and whom to copy (Laland 2004; Hoppitt and Laland 2013, but see Heyes (2016) for discussion of limitations in the identification of underlying cognitive mechanisms). Whilst this chapter focuses primarily upon the biases of social learning, here we provide a brief introduction to transmission mechanisms. Some researchers argued early on that only the (supposedly) more cognitively complex processes of imitation and teaching would allow for transmis- sion of sufficient fidelity to create stable, between-group traditions (Galef 1992, but see Claidiere and Sperber 2010). Thus, it was the study of mechanisms and partic- ularly the exploration of the process of imitation which formed the primary research focus in experiments on social learning that until recently were largely restricted to captive primates and other animals, where rigorous experimental and contrasting control conditions can be engineered.

Social learning mechanisms range from the simplest processes of local and stimulus enhancement (increased attention respectively towards locations and objects one observes others acting on) to more complex mechanisms such as teaching and copying (Heyes 1994). Experimenters have distinguished between two principal types of copying mechanisms: imitation, which refers to copying the actions (often conceived of a bodily actions) of another individual (Whiten et al. 2004), and emulation, which refers to learning focused only on desirable environ- mental results of other’s actions (Tomasello et al. 1987). Whilst initial tests with chimpanzees suggested they are capable of only emulation (Tomasello et al. 1987), later studies provided a diversity of evidence for imitation, including recognisable successes in ‘do-as-I-do’ games and other tests that require matching of bodily actions [Custance et al. (1995), Buttelmann et al. (2007), although it should be noted that some of these studies were conducted with hand-reared chimpanzees; see also Fuhrmann et al. (2014), but see Tomasello et al. (1997), Tennie et al. (2012) for evidence of marked limitations in copying arbitrary or novel gestures in untrained chimpanzees]. Other studies with captive chimpanzees (and children) found evi- dence for flexible use of imitation and emulation in chimpanzees (Hopper et al. 2008), with replication of a whole sequence of actions being preferred when a complex task was relatively opaque (“program-level imitation”, Byrne and Russon 1998) and a more emulative response made when it was sufficiently transparent that some actions could be seen to be redundant and were not copied (Horner and Whiten 2005). Other studies revealed some contexts where emulation does not enable chimpanzees to solve a complex task, whereas seeing another chimpanzee complete it allows success by copying (Hopper et al. 2007, 2015) and other contexts where chimpanzees are flexible enough to succeed by emulation when direct imitation is made impossible (Tennie et al. 2010).

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Limited evidence for bodily imitation in monkeys has also emerged, from species including marmosets (Voelkl and Huber 2000), vervet monkeys (van de Waal and Whiten 2012) and capuchins (Fragaszy et al. 2011, although see Dean et al. 2012). There is thus limited evidence in monkeys and apes for one of the two features that Galef emphasised as crucial to human culture: imitation. However, perhaps more important is that a range of cultural diffusion experiments have demonstrated that species of monkeys and apes can transmit and sustain traditions, whether or not these are driven by imitative or emulative copying processes (reviewed in Whiten et al. 2016, but see Bandini and Tennie 2017). By contrast, there is little evidence for Galef’s other factor, teaching, in non-human primates (although see Musgrave et al. 2016 for a recent example of tool transfer interpreted as teaching in chimpanzees). There is, however, evidence for teaching (defined in functional rather than inten- tional terms) in non-primate animals such as meerkats (Thornton and McAuliffe 2006), ants (Franks and Richardson 2006) and pied babblers (Raihani and Ridley 2008). It should be noted, however, that whilst we include teaching here to illustrate its importance in the study of cultural transmission, it is not a mechanism in the learner, but rather in the teacher, coupled with complementary social learning processes in the learner. For example, the teaching process of demonstration couples well with a capacity for imitation in the learner (Hoppitt and Laland 2008). For discussions on the evidence for teaching and its significance in non-human animals, see Thornton and Raihani (2010) and Hoppitt and Laland (2008).

4 Social Learning Biases

More recently, research has begun to tackle the potential biases or ‘strategies’ which influence when and from whom animals learn socially. Given that learning from others indiscriminately may result in the transmission of maladaptive behaviours (Laland and Williams 1998; Pongracz et al. 2003), Laland (2004) suggested that individuals should be selective in when and from whom they engage in social learning, highlighting a number of potential social learning strategies (or biases as we refer to them here). Indeed Coussi-Korbel and Fragaszy (1995) had earlier suggested that the social dynamics of groups would likely lead to biases in social learning. An adaptive bias may allow individuals to select the most productive behaviour between multiple options and overwrite pre-existing behaviours when innovations or a changing environment renders them inefficient. Whilst a number of such biases have been suggested by researchers, empirical investigation of many remains lacking, and Heyes (2016) points out that the underlying mechanisms remain largely unspecified. Here we limit our discussion to the social learning biases that have received the most research attention to date (Table 1), ranging from frequency-based copying (e.g. copying common behaviours) to model-based biases (e.g. copying high-ranked individuals). One of the most studied—and contentious— biases addressed in recent years, in both humans and animals, is that of conformity.

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4.1 Conformity and Majority Bias

In the 1950s, Solomon Asch (Asch 1951) showed that when people were faced with a unanimous majority giving incorrect answers on a line judgement task, roughly one third of individuals conformed to the group decision even though it was visibly wrong. These findings were replicated across cultures (Bond and Smith 1996) and more recently in children (Haun and Tomasello 2011), suggesting a powerful predisposition for humans to conform to the judgement of the majority.

Circumstantial evidence for conformist behaviour in primates arose in open diffusion studies such as that by Whiten et al. (2005) which utilised a puzzle box (the ‘panpipes’) that could be opened using either of two tool-based techniques (‘poke’ or ‘lift’). A high-ranking female from each of the two groups was trained in one of these methods and demonstrated it in front of the rest of their group, who later had opportunities to interact with the panpipes. After 2 months, it was found that although some individuals did open with the alternative method, there was a significant tendency for individuals to converge on the option most common in their group. Whiten et al. (2005) suggested this to be indicative of a conformity effect. A similar effect has since been recorded in capuchin monkeys (Dindo et al. 2008, 2009). Critics have pointed out that chimpanzees are often reluctant to give up a first-learned behaviour (Hopper et al. 2011; Marshall-Pescini and Whiten 2008; Hrubesch et al. 2009; Harrison and Whiten 2018), so it may be that individuals were simply returning to their original method after a period of exploration (van Leeuwen and Haun 2013). However, there are also several documented examples of flexible,

Table 1 Definitions and examples of selected social learning biases

Category Term Definition Selected examples

Frequency- based biases

Majority bias

A tendency to copy the behaviour of the majority when learning a task

Chimpanzees, Haun et al. (2012) Cf. van Leeuwen and Haun (2013)

Conformity A tendency to forgo one’s own behavioural preference in favour of that used by the majority

Fish, Pike and Laland (2010) Vervet monkeys, van de Waal et al. (2013) Chimpanzees, Luncz and Boesch (2014) Birds, Aplin et al. (2015a, b)

Model- based biases

Rank bias A tendency to copy individuals of high social rank

Chimpanzees, Horner et al. (2010); Kendal et al. (2015)

Sex bias A tendency to copy individuals of one sex over the other

Vervet monkeys, van de Waal et al. (2010)

Kin bias A tendency to copy one’s own kin

Chimpanzees, Matsuzawa et al. (2001) Vervet monkeys, van de Waal et al. (2012, 2014)

For a more exhaustive review, particularly of ‘when’ biases, see Laland (2004) and Rendell et al. (2011)

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non-conservative problem-solving by chimpanzees (Hopper et al. 2015; Yamamoto et al. 2013)

Subsequent evidence for conformity in chimpanzees has been mixed. No study has yet found an example of conformity in which an individual gives up a first- learned behaviour in favour of that used by the majority. However, Luncz and Boesch (2014), having earlier identified consistent differences between neighbouring groups in aspects of nut-cracking tool selection, found that females who transfer between these groups are as likely as males to match their local group preferences, suggesting they must have conformed to them since their arrival. A case study of one wild female chimpanzee that had recently migrated to a new group showed that, over time, her behavioural repertoire became progressively more similar to that of the group. However, without systematic testing we cannot be sure this was driven by majority influence, rather than other biases. Working with captive chimpanzees on a token exchange task, van Leeuwen and Haun (2013) found that individuals were motivated to switch methods by greater rewards, but not by the behaviour of the majority. This suggests other factors, such as maximising payoffs, may be more critical in motivating apparently conformist behaviour than majority influence. Moreover, Vale et al. (2017) found that captive chimpanzees who were trained to prefer one colour of food and then moved to a group with a strong preference for the alternative colour did not conform to the foraging prefer- ences of their new ‘host’ group, although they did feed from this food more frequently than before. Watson et al. (2018) found that lone minority individuals trained on a method of opening a puzzle box, whilst the rest of their group were trained on an alternative method, rapidly converged on the behavioural preference of the majority. However, this occurred after observing just one or two groupmates, meaning that they did not have first-hand knowledge of the majority preference. In contrast, dyads of chimpanzees trained on alternative methods never switched to using their partner’s preferred method. The authors argue that it is possible that, when in a group context, chimpanzees may make inferences about group-level behaviour preferences based on a limited sample and act accordingly, in a potentially conformist manner.

Arguably, the strongest evidence for conformist transmission in non-human animals has been found in non-primate species. In Pike and Laland (2010), nine- spined stickleback fish independently learned that one of the two feeders was richer in food than the other. The positions of the feeders were then reversed, and the fish could observe others feeding at the previously less rewarding location. When these demonstrator fish were removed and the observer was once again allowed to choose a feeding location, they preferentially used the one favoured by the majority. This effect increased disproportionately according to the relative size of the majority, thereby fulfilling the most stringent definitions of conformist bias. In another convincing example of conformity in a non-primate species, Aplin and colleagues (Aplin et al. 2015a, b) found that not only did experimentally induced innovations (alternative methods of operating a foraging box) spread throughout groups of great tits in a manner consistent with majority-biased transmission but they expressed an exaggerated tendency to do so. In addition, when individuals migrated between

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groups, if the local method was different from their own, then a majority of birds adopted the behaviour most common in their new community [but see van Leeuwen et al. (2015) and Aplin et al. (2015b) for further debate]. This echoes the results from an experiment that seeded alternative options in wild vervet monkeys (van de Waal et al. 2013). Four groups of wild vervet monkeys were repeatedly provided with two boxes of coloured corn, one pink and one blue. For each group, one of these colours was initially made to taste bitter and unpalatable. Then, after monkeys had learned to avoid one colour, no more bitter material was added to either colour of corn. When males later migrated between groups with different preferences, and once they were not outranked by residents at the boxes, nine of ten switched to eat the colour that was locally preferred, expressing an apparently striking degree of conformity. In a follow-up study, the preferences of low-ranking females who had permanently splintered from their natal group have been monitored. The low rank of these females meant that in their original group, they ate more of the previously bad-tasting food than others yet, after the split, they ate exclusively the colour preferred in the group from which they split, even though both colours were available and neither tasted bad, emphasising the potency and durability of socially learned behaviours (van de Waal et al. 2017). However, whether the individuals were influenced by the behaviour of the majority of individuals or by certain classes of individual within that group (as discussed below) remains unclear. The lack of clear experimental evidence for conformity in chimpanzees may suggest that other biases are more central to the transmission of information in this species or that it is only expressed by certain individuals. It is very possible that primates may display conformist transmission in only certain contexts, such as after a recent immigration to a new group. Further experimental research into these questions is required in order to better understand these distinctions (Fig. 2).

To date, only one primate study has directly and experimentally tested for majority-biased transmission. Haun et al. (2012) carried out a study in which human children, chimpanzees and orangutans were exposed to conspecific models depositing tokens in a receptacle in order to receive a reward. Three receptacles were on display, one of which was used by a single individual three times, another by three individuals a single time and another by none. Observers had no previous exposure to the task. When given a token to deposit for themselves, both children and chimpanzees (but not orangutans) showed a tendency to choose the receptacle used by the majority of demonstrators. Related findings have been reported in such distantly related species as rats (Chou and Richerson 1992), pigeons (Lefebvre and Giraldeau 1994), dogs (Kundey et al. 2012) and fruit flies (Battesti et al. 2012).

Most studies of majority influence have focussed on foraging behaviour, as this is relatively straightforward to model in experimental designs. A disadvantage of this approach is that cognition is being examined within a single behavioural context, when our understanding could be enriched by taking a broader approach (Watson and Caldwell 2009). For example, there is a wealth of evidence for the social learning of vocalisations in a wide range of species (e.g. bats, birds, bears, cetaceans and primates), which Janik and Slater (1997) argue serves (amongst other functions) the purpose of identifying oneself with the group, just as has been argued to motivate

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human conformist behaviour. Collecting data before and after wild group migrations to test for vocal conformity is inherently difficult, but this can be achieved in captivity. Watson et al. (2015a) examined the referential ‘food grunts’ of chimpan- zees moved from the Netherlands and integrated with a resident group at Edinburgh Zoo in Scotland. Over the period of time that it took for the two groups to socially integrate, so too did the referential food calls of the ‘Dutch’ chimps converge on that of the ‘local’ group, despite the arousal levels associated with the referent foods remaining constant. This draws an interesting parallel with examples of conformity in migrating animals (Luncz and Boesch 2014; van de Waal et al. 2013), although in this case the immigrant subgroup was equal in size to that which they converged on. This is suggestive of conformist behaviour in the vocal domain, although it is worth noting that there is debate over the extent of and likely motivations for this convergence (Fischer et al. 2015; Watson et al. 2015b).

The few studies purporting to have identified conformity or majority bias trans- mission in non-human animals have come under criticism in part for not adequately ruling out other types of social influence that might explain their findings, including biases towards certain individuals within the majority (van Leeuwen and Haun 2013; Haun et al. 2013). Rather than being attentive to the behaviour displayed by the majority of conspecifics, it is argued that animals may instead direct social learning towards specific individuals, perhaps an individual that is regarded as more success- ful or more knowledgeable or an individual who presents the learner with more opportunities for social learning.

Fig. 2 An illustration from the follow-up experiments of van de Waal et al. (2013) showing a group of vervets crowding around their preferred colour of corn (pink, left) and avoiding the other (blue, right)

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4.2 Model-Based Biases in Primates

Also termed ‘who strategies’ (Laland 2004), model-based biases (Wood et al. 2013) focus on characteristics of the model, for instance, the age, sex, rank or previous success of the model. Whilst there is a growing body of research with humans identifying a number of biases causing directed social learning [Mesoudi and Whiten 2008; Molleman et al. 2014; for reviews in children, see Wood et al. (2013) and Price et al. (2017)], research with non-human primates has only recently begun to gain momentum. Here we discuss the evidence gathered for these biases in non-human primates, both in captivity and the field, and discuss the implications of these biases for the social transmission of behaviours.

The initial models selected by experimenters in open diffusion paradigms with non-human primates are often dominant members in the group (Hopper et al. 2011; Whiten et al. 2005). This is often because a dominant individual has first access to new food/stimuli and can thus act as a model for the rest of the group without interference, particularly in captivity. But do non-human primates have a natural bias towards copying a dominant individual? If rank serves as a proxy for success, then animals may benefit from copying the behaviour of a high-ranking individual. However, whilst a high-ranking individual may be seen as successful in some regards, there is no guarantee that copying their behaviours in all domains would be an adaptive strategy. Such a bias could certainly have important implications for the spread of innovations and emergence of traditions. In chimpanzees, there is a relatively high level of innovation compared to the number of traditions observed (Nishida et al. 2009). A review of the primate literature found that most innovations are performed by low-ranking individuals (Reader and Laland 2001), and it has been suggested that a bias towards attending to and copying higher-ranking individuals may explain the discrepancy between innovation rates and the relatively low number of traditions that become established in chimpanzee groups (Kendal et al. 2015).

Whilst there remains a lack of data from the field to corroborate this assertion, two recent studies have found biases towards copying dominant and knowledgeable individuals in captive chimpanzees. Horner et al. (2010) investigated model biases in chimpanzees by training two females in each of two groups of captive chimpan- zees to deposit tokens in different receptacles in exchange for a reward. One of the models (Model A) was older than the other, higher-ranking and had previously introduced novel tasks to the group; a collection of traits labelled by the authors as ‘prestige’ (a term used by Henrich and Gil-White 2001 in discussing such phenom- ena in humans). In both groups, after the models had demonstrated their methods, naive observers dropped significantly more tokens into the receptacle demonstrated by Model A, thereby suggesting that the chimpanzees were biased towards copying the behaviour of this ‘prestigious’ female, over the non-prestigious female. This study, however, provides only limited support for a bias based upon dominance rank, since the models differed in age and previous success rates, either or both of which may have influenced the observer’s actions. Following this, Kendal et al. (2015) used an open diffusion method and sophisticated statistical techniques to

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investigate transmission biases in captive chimpanzees. Alternative sliding move- ments of the door on an artificial fruit (left or right) were first seeded into two groups by mid-ranking females. The diffusion of behaviours and patterns of observation revealed biases towards copying dominant and knowledgeable individuals. Any existing rank bias is unlikely to be totally rigid, however, as both Watson et al. (2017) and Hopper et al. (2013) report diffusion of social information from low-ranking chimpanzees and squirrel monkeys, respectively. In a field experiment with wild vervet monkeys, Botting, Whiten, Grampp and van de Waal (2018) found that monkeys showed no consistent preference for a foraging behaviour demon- strated by a high-ranking, rather than that displayed by a low-ranking, female. Similarly, examining model-based biases in captive capuchin monkeys, Dindo et al. (2011) found no effect of watching a high-ranking or low-ranking female model on an individual’s choice of action in a foraging task. However, in a subset of participants, there was a significant bias towards a related model (i.e. kin), which leads us to another bias which has been examined in non-human primates.

Observations from the field suggest that chimpanzee mothers act as the primary model in an infant’s early life and are highly tolerant of their offspring. It is suggested that this may allow young chimpanzees to learn such behaviours as nut-cracking through a ‘master-apprentice’ style relationship (Matsuzawa et al. 2001). Field experiments have shown that infants are significantly more likely than juveniles or adults to observe a related model nut-cracking (Biro et al. 2003), perhaps reflecting a ‘critical age’ (Matsusawa and Yamakoshi 1996) at which this bias may operate to allow infants to learn these skills. Similarly, wild orangutan infants engage in increased ‘peering’ towards their mother whilst she is performing difficult extractive foraging techniques (Jaeggi et al. 2010; Schuppli et al. 2016). Field experiments with wild vervet monkeys have provided further evidence of a bias towards copying the mother in a primate’s early life. Van de Waal et al. (2012) presented wild groups of vervet monkeys with grapes covered in sand and recorded the different techniques used by individuals to clean them prior to ingestion. It was found that individuals within the same matriline used similar techniques. This experiment was later extended to reveal that infants showed significant fidelity to their mother’s favoured technique (van de Waal et al. 2014), indicating a strong bias towards the mother as a model for social learning in infancy, as has also been reported for humans (Henrich and Broesch 2011). Preferring kin as models likely stems from the increased tolerance, and thus social learning opportunities, that they provide (Coussi-Korbel and Fragaszy 1995), although it has also been suggested that learning from kin may prove adaptive since they are more likely to have similar behaviours and reactions to the learner (Hoppitt and Laland 2013). With respect to the emergence of traditions, a kinship bias may promote between-group differences (Wrangham et al. 2016), but this will depend upon the dispersion patterns of the species and might also be affected by sex-based biases in social learning (e.g. Lonsdorf et al. 2004).

In addition to this kinship-based bias, a sex-based bias has also been found in wild vervet monkeys, highlighting the fact that different social learning biases may operate concurrently in a community. van de Waal et al. (2010) found that monkeys

Culture and Selective Social Learning in Wild and Captive Primates 223

who witnessed a dominant female model showed higher rates of participation and acted on the same part of an artificial fruit when compared with individuals who witnessed a dominant male model. The authors also found this to be associated with selective attention to female models, rather than a greater tolerance for observers from these models. Given this selective attention to females in a species with female philopatry, we might expect to see localised traditions between groups, as the migrating males would be far less likely to spread socially learned information. Lonsdorf et al. (2004) also found a bias in the acquisition of tool-use skills in juvenile chimpanzees, with females watching others termite fishing at an earlier age and becoming proficient at an earlier age than males. This highlights that the sex of the learner may also bias social learning processes (although it should be noted that the number of juveniles analysed here was relatively low).

Looking briefly beyond the primates, a handful of studies have examined model- based biases in other species. A bias towards copying dominant individuals was found in domestic hens (Nicol and Pope 1999), and biases towards copying older and larger individuals have been found in both fish (Duffy et al. 2009) and mice (Choleris et al. 1997). Biases towards copying from kin (ravens, Schwab et al. 2008) and a certain sex (finches, Katz and Lachlan 2003; hens, Nicol and Pope 1999) have also been reported. Thus, model biases appear to be a widespread adaptation in the animal kingdom, which suggests that they are an efficient way of obtaining infor- mation. Much more research is needed to discover when each bias is utilised, as the presence of multiple biases in a species suggests contextual implementation. Indeed, in humans, there is evidence that different individuals rely on different social learning strategies in the same contexts (Molleman et al. 2014). This highlights the individual variation seen in social learning and thus makes the task of elucidating which biases are utilised by animals and their role in cultural transmission all the more complex.

5 Conclusions

The last few decades have seen a huge leap forward in our understanding of non-human culture, with a particular intensity of research on primates. Phenomena once thought to be uniquely human have been found again and again amongst primates and, indeed, across the animal world. It seems that the more we examine social learning in non-human animals including our fellow primates, the less we find it to be limited to humans. This allows us not only to understand more of how and why cultural behaviours are present in modern humans but also to appreciate the richness of the cultural lives of these species and expand our conceptions of the role such second inheritance systems play in evolutionary processes.

There are, of course, many questions which remain unanswered. In particular, whilst research into social learning biases has yielded deeper understanding, it has also revealed the complexity of learning biases; how there may be several biases operating within a single species, or even within a single individual; and how a

224 S. K. Watson et al.

multitude of factors (context, sex, age, environment, etc.) can affect their subsequent expression. Only when we better understand how the range of social learning biases and mechanisms operate in different contexts can we fully understand how they function to contribute to the emergence and maintenance of traditions and culture. Our current knowledge is the result of an amalgamation of the complementary techniques of field observations, controlled captive experimentation and more recently, bringing these together, the more challenging achievement of field exper- iments. These methods all provide us with valuable complementary insights, for example, by using captive experimentation to test predictions based upon wild observation e.g. as in the case of wild chimpanzee traditions (Whiten et al. 1999) and the underlying role of social learning within these (Whiten et al. 2005). By continuing to utilise all of the methods that are available to us and in particular maintaining the inclusion of studies of free-ranging animals, which have provided some of the most exciting findings in recent years, we can expect to gain a clearer understanding of non-human and, indeed, human culture.

Acknowledgements JB, SKW and AW are grateful for the support of grant ID40128, ‘Exploring the evolutionary foundations of cultural complexity, creativity and trust’, from the John Templeton Foundation, and JB is grateful for the support of a grant from the David Bohnett Foundation during the writing of this paper. EW was supported by the Swiss National Science Foundation (P300P3_151187 and 31003A_159587) and Society in Science—Branco Weiss Fellowship. We thank two anonymous referees for discussion and comments on the manuscript.

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