Creativity and experience in nonhuman primate communication

Full text

!
1!
In: Cognition, Experience and Creativity (Eds Manjaly J A and Indurkhya B)
Orient Blackswan, Hyderabad, India, in press
Creativity and Experience in Nonhuman Primate Communication!
Shreejata Gupta1, Rajesh Kasturirangan2 and Anindya Sinha1,3,4!
!
1School!of!Natural!Sciences!and!Engineering,!National!Institute!of!Advanced!Studies,!Indian!
Institute!of!Science!Campus,!Bangalore!560012,!India!
2School!of!Humanities,!National!Institute!of!Advanced!Studies,!Indian!Institute!of!Science!
Campus,!Bangalore!560012,!India!
3Centre!for!Neuroscience,!Indian!Institute!of!Science,!Bangalore!560012,!India!
4Nature!Conservation!Foundation,!3076/5,!4th!Cross,!Gokulam!Park,!Mysore!570002,!India!
!
!
!
Creativity and experience in nonhuman species: State of the art!
The word creativity, coined undoubtedly for human achievement, has perhaps never
been applied to the behaviour of nonhuman species. Whether this was simply to avoid
the threat of anthropomorphism or whether there are qualitative differences between
the innovative behaviours of nonhuman and human animals that would preclude the
former from being included in the category of creative beings remains an open
question. There has, however, been a growing interest in creative behaviours in
nonhuman species since Lloyd Morgan (1912). Morgan observed that the behavioural
repertoire of every animal consisted of two kinds of behaviour, some repetitive and a
small proportion of novel behaviours, which were distinctly different from the former
regular behaviours. It is this second kind of behaviour that interests us here.!
!
Innovative behaviour in animals has been long investigated under various titles such as
neophilia (attraction for the new), exploration, or learning (see Reader and Laland 2003)

!
2!
but it had neither been shown much academic interest in terms of its functional
importance nor considered analogous to human creativity until as recently as twenty
years ago (Reader and Laland 2003). Some comprehensive accounts reported
tendencies of innovation in certain animal taxa (Thorpe 1956; Cousteau 1958;
Cambefort 1981; Lefebvre et al. 1997), and argued for a phylogenetic trend of more
innovative behaviours being preferentially associated with ‘higher organisms’ with larger
brain sizes (Morgan 1912; McDougall 1936; Wyles et al. 1983; Lefebvre et al. 1997).!
!
One of the pioneering papers that first drew attention to novel behaviours in animals
was a review of primate innovations by Hans Kummer and Jane Goodall (1985). They
not only discussed the striking variety of behavioural innovations possible but also
highlighted the functional importance of such behaviours. More functional explanations
of novel behavioural responses to ecological change have been provided over the years
in a wide range of taxa including fish, birds and primates (Fisher and Hinde 1949; Hinde
and Fisher 1951; Goodall 1964; Beck 1980; McGrew 1994; Laland and van Bergen
2003). Subsequently, attention was drawn to the psychological and cognitive processes
that could underlie innovative behaviours, as, for example, the positive correlation of
forebrain size with innovation frequency in birds (Lefebvre et al. 1997), which opened up
a new approach to study innovation in animals. Such an approach provides an
opportunity to carry out investigations regarding the psychological processes underlying
innovative behaviour as well as the role of innovation in evolutionary processes (Reader
and Laland 2003). With these developments in animal innovation or creativity studies,
another area of research has gained more attention, perhaps independently or in
conjunction with these endeavours - that of animal social traditions or cultures. These
include behaviours that nonhuman animal species develop through their own
experience in everyday life or learn from others by observation. During the 1990s, some
path-breaking work reported and explained the phenomenon of animal behavioural
traditions in a few mammalian species, particularly nonhuman primates (Quiatt and
Reynolds 1993; King 1994; Quiatt and Itani 1994; Wrangham et al. 1994; McGrew et al.
1996). Soon other innovative studies, some conducted even earlier, began to attract
attention; these documented social traditions in various other taxa including birds

!
3!
(Lefebvre and Palameta 1988; Lefebvre et al. 1997), fish (Warner 1988) and cetaceans
(Rendell and Whitehead 2001).!
!
The notion of culture in nonhuman animals has, however, been challenged, primarily
on the basis of the nature of the cognitive mechanisms underlying the inter-individual
transmission of behaviours (Green 1975; Visalberghi and Fragaszy 1990; Galef 1991;
Whiten and Ham 1992). This controversy mainly emerged from a human-centric
definition of ‘culture’ wherein ‘imitation’ was supposed to be the only socially learnt
process that could transmit behaviours (see Boesch 1995). Further work has, however,
shown that social mechanisms other than imitation can underlie even human cultures
and raised the idea that narrowing down the definition of ‘cultures’ too much would
lead to ignoring crucial information. Other social learning processes such as emulation,
social enhancement and trial-and-error learning were thus subsequently included in
the definition of socially transmitted behaviours and what has now variously been
called behavioural traditions, social traditions or arguably, culture in both human and
nonhuman species (McGrew 1992; Boesch 1993; Wynn 1993; Galef 2004).!
!
In more recent years, research in the field of animal creativity or innovation has focused
on the connections between behaviours that are primarily socially learnt through
individual experiences in daily life and the inception and establishment of these novel
behaviours in the repertoire of the population to which such experienced individuals
belong (Galef 2003; van Bergen et al. 2004; Boogert et al. 2008; see also Reader and
Laland 2003).!
!
In this paper, we digress from the usual model of discussions on the innovation-social
learning links in animal creativity and examine a range of novel communicative
behaviours that nonhuman primates adopt under certain ecological or social conditions
(Kummer and Goodall 1985; Goodall 1986; Rowe 1996). An investigation of the
variation in nonhuman primate gestures and vocal signals, typically employed in social
contexts, both affiliative and agonistic, might throw light, at the proximate level, on the
flexibility of both, the production and usage of such signals. Such an analysis should
prove insightful not only in understanding the behavioural plasticity underlying

!
4!
communication modalities in nonhuman primates, but also the creativity that typifies
these communicative processes. Ultimately, we might be able to understand the
mechanisms with which individual primates learn, if they do, the use of social
communicative behaviours and discover whether these could contribute to the
establishment of potential social or behavioural traditions akin to human language. We
also consider the possibility that such an analysis could finally illuminate the processes
underlying the evolution of human language.!
!
Defining creativity and experience in nonhuman species!
Creativity in humans has been defined mostly as ‘an idea, practice or object that is
perceived as new by an individual’ (Rogers 1995) or simply as a creative process
(Simonton 2003). The definition of creativity or innovation, thus, takes into account the
final product of or a process involved in a new behaviour. There are, however, two
distinct approaches in defining innovative behaviours in nonhuman species, which
hardly overlap, unlike the definitions of human creativity. The common feature of both
these perspectives is that they regard innovation as a novel behaviour pattern
previously unobserved in the population. One school considers innovative behaviour as
a product, which could be a solution to a novel problem or a new solution to an old
problem (Kummer and Goodall 1985). The other school defines creative behaviour as a
process that includes the inception of a new behaviour, its use in solving a problem,
and its subsequent spread in the population (Wyles et al.1983; Lee 1991).!
Innovation can, thus, be regarded as a new or modified behaviour (innovation sensu
product) or as a process that leads to the establishment of such a novel or modified
behaviour (innovation sensu process; see Reader and Laland 2003). As the
interchangeable use of innovation as product or process can be quite ambiguous, it is
essential that a proper analysis be conducted of what is actually involved when an
innovation is operationally defined in a particular context. The process of acquiring a
new behaviour cannot, by itself, be considered an innovation unless the behaviour is
newly created or an existing behaviour is modified in a novel manner. Usually,
innovation also requires that this novel behaviour be then incorporated into the
behavioural repertoire of the individual and used, possibly, in a novel context as well.

!
5!
For example, when a bird learns a song from its tutor, it is social learning, but if it adds a
different note from another adult bird into its song and sings a complete new song, such
an end result, the new song in this case, would be considered an innovative behaviour
rather than just a process of social learning (Slater and Lachlan 2003). Thus, innovation
is a new behaviour ‘invented’ by an individual (Reader and Laland 2003) or a group of
individuals (Laland and Plotkin 1990; Paquette 1992) and it could develop by chance or
by individual- or group learning.!
!
The appearance of a novel behaviour may then be followed by a mechanism that would
introduce the variant behaviour, now a stable component of the innovator’s behavioural
profile, into the population’s behavioural repertoire. The process of diffusion of this new
behaviour to the learning audience could occur through the processes of imitation,
emulation, stimulus enhancement, observational conditioning or, more indirectly, by the
immigration of new individuals into the group (Whiten and Ham 1993; for a discussion,
see McGrew 1998). In a nutshell, all these processes can be perceived as being the
experience of an individual embedded in a group. An individual in isolation would not
experience the process of social learning although it can be argued that such
experiences are not essential for the expression of creativity. An innovative behaviour
that has developed by chance or trial-and-error learning in an individual in isolation
could also be reinforced by repetition and could contribute to individual experience of a
different nature. Although such behaviours could then spread through the group by
mechanisms of social learning, there might be instances where the creative novel
behaviour does not diffuse to the other members of the group. Rather, it remains
restricted to the ‘inventor’s’ repertoire, and the behaviour exists as long as the inventor
uses it. In this case, individual learning alone underlies the inception of a novel
behaviour, one that never becomes a tradition in the group (Whiten and Ham 1993).!
!
To summarise, we need to distinguish an innovative product from the process that
generated it while defining creativity. The product could consist of the final form of a
novel behaviour, which either arises de novo or by modification of a pre-existing
behaviour, but which enables an individual animal to solve a new problem or an old
problem in a new way. Such a behavioural innovation sensu product has been

!
6!
considered evidence of creativity by Reader and Laland (2003). This product may or
may not then be followed by social learning mechanisms through which another
individual experiences the invented behaviour and adopts it in its own repertoire, thus
giving rise to a cultural or behavioural tradition in the population, and this has been
considered innovation sensu process. It can, therefore, be concluded that innovation
sensu product is a necessary condition for innovative behaviour or creativity while
innovation sensu process or experience may not always be.!
!
Innovation in nonhuman primate communication!
Both innovation and cultural traditions possibly reach their pinnacle in humans, more
specifically in a behavioural attribute that is almost uniquely human: organised
language. A search for the evolutionary roots of human language and culture should
thus involve a close understanding of nonhuman primates (henceforth referred to as
primates), with whom we share our closest ancestors. Like us, nonhuman primates
lead rather complex lives – and this is often reflected in the intriguing diversity
presented by their behaviour. Primates typically live under ecologically unpredictable
conditions. Individual primates are thus often called upon to develop innovative
behavioural responses to meet the challenges of their physical and social
environments and effectively adapt to them. For example, experiences of food scarcity
could favour the development of creative foraging strategies while an abundance of
food could lead to novel ways of exploring these resources (Knott 1998). Moreover,
most species usually live in complex social groups that may change over time and this
uncertainty of the social environment also requires individual primates to be
behaviourally flexible and innovative in order to survive and reproduce successfully
(Reader and Laland 2001; Sinha 2005). Crucial survival strategies, often involving
creative behaviour, thus occasionally emerge and these could spread both within and
without the group as effective problem-solving abilities that influence the behaviour of
succeeding generations as well.!
!
Although nonhuman primate communication has been explored extensively in the wild
and in captivity, what continues to remain controversial is the extent of flexibility in vocal
communication displayed by individual primates. For example, it has long been debated

!
7!
whether the development of primate vocalisations is completely hardwired or whether
there is a certain flexibility in their production and usage, influenced by social learning
processes during early ontogeny (Janik and Slater, 1997, 2000; Hammerschmidt and
Fischer 2008). What is more accepted, however, is the significant flexibility of primate
gestural communication, which appears to stem from a social learning process of
ontogenetic ritualisation during development (Tomasello 1996; Tomasello and Call
2007). The spread of some novel gestures as a group-specific tradition, however,
apparently needs different learning processes (see Pika 2007).!
!
A close analysis of innovations in nonhuman primate vocal and gestural repertoires
may unveil the role of individual creativity in generating some of these behaviours.
Moreover, they might reveal whether novel social learning processes other than the
usually understood ontogenetic ritualisation could be responsible for their further
development and establishment as behavioural traditions within certain primate groups.
We now present some examples of apparently novel nonhuman primate vocalisations
and gestures that allow us to understand the level of plasticity underlying such
communicative behaviour.!
!
Creativity in nonhuman primate vocalisations!
In direct contrast to the widely held belief that most primate vocalisations are
involuntary responses, there have emerged, in recent times, studies that report a
certain level of plasticity in the production of specific calls (reviewed in Snowdon 2009).
We stress on vocal production because the usage and comprehension of vocalisations
have already been accepted to show clear signs of flexibility (Seyfarth and Cheney
1997). Such lability is usually reflected in the developmental processes that allow naïve
individuals to learn the apt usage of specific calls rather than to produce them
perfectly, and more explicitly manifest in the generation of novel calls or in creative
modifications and usage of pre-existing calls (see also Sinha 2003, 2005).!
!
Examples of creative vocal production from the wild are quite rare. Although there are
examples of behavioural traditions in call structure within populations of chimpanzees,
tarsiers and other species, the point of inception of such variant calls remains unknown.

!
8!
The possibility of genetic drift giving rise to such differences, for example, cannot be
easily ruled out (Mitani et al. 1992; Mitani and Brandt 1994; Burton and Nietsch 2010).
There does exist a single report, however, which confirms the failure of genetic drift to
explain inter-population differences in the structure of pant-hoot vocalisations in
chimpanzees (Crockford et al. 2004). Such differences in vocal production might
contribute to the ability of individuals to distinguish between group and non-group
members and these could, therefore, rapidly establish themselves as cultural traditions
between groups. Similar observations have been reported in populations of pygmy
marmosets, where individuals modified their J-calls and trill vocalisations depending on
the habitat conditions (De la Torre and Snowdon 2009). Ecological conditions also
seem to affect the vocal production of wild olive baboons, similar to that reported for
pygmy marmosets, with baboons in forested areas producing calls of relatively lower
frequency and longer durations than those in populations inhabiting open fields (Ey et
al. 2009).!
!
More creativity in the production of vocalisations has, however, been observed in
captive groups of several species of nonhuman primates. For instance, two female
juvenile Japanese macaques, who had been conditioned to respond to their names,
given by the food provider, differently improvised the coo-calls in their repertoire
(Masataka 1992). These responses were distinct to each individual and were described
as ‘idiosyncratic’ improvisations, although they definitely fit into the category of creative
production of vocal signals. Barbary and Japanese macaque groups arising, in each
case, from an original founder population and separated subsequently for 20-30 years,
were observed to develop novel variations of social shrill-bark vocalisations and coo-
calls, respectively, in captivity (Fischer et al. 1998; Tanaka et al. 2006). These
differences could only!be attributed to flexible inventions peculiar to each group as the
short time of separation of these groups from the founder populations precluded the
appearance of significant genetic differences between them. The coo-call variation
displayed by the captive Japanese macaques was reported in adults alone while infants
only developed the variant calls after experiencing a certain level of exposure to the
calls – a clear example of innovative behaviour diffused by social learning. What,
however, remains unknown is whether these novel calls were products of individual

!
9!
creativity or of group innovation. Pygmy marmoset captive populations have also been
experimentally shown to modify their calls under changed social conditions (Snowdon
2009).!
!
The relatively higher levels of innovation in vocal production displayed by primates in
captivity than in the wild could be an artefact of the lower number of studies in the wild
and the greater amount of time spent on captive populations for experiments. More
investigations of primate communication in the wild have also been carried out to
understand the referentiality of individual calls with significantly less attention paid to
contextual social calls of the study species. It is, however, social calls that appear to
exhibit a relatively greater potential of plasticity than do other calls that are involved in
more survival-related functions like the avoiding of predators or the finding of food. It
should, however, also be borne in mind that there are also instances where novel vocal
production has been observed in typically costly situations such as predator attacks. A
Japanese macaque individual, for example, once invented an alarm call for a
rattlesnake, a novel predator for the species (see Reader and Laland 2003). A more
holistic approach to involving a greater variety of vocalisations is thus called for if one
wishes to understand the inherent flexibility of primate communication systems.!
!
Creativity in nonhuman primate gestural communication!
Gestural communication in nonhuman primates, particularly the great apes, appear
to be more creative and shows considerable flexibility in the production and usage of
gestures both in the wild and under captivity. Comparative studies on prosimians and
monkeys are, however, rare and present an urgent need for the future.!
Examples of truly innovative gestures, generated in the wild, however, continue to be
exceptions rather than the rule, even in apes. A pioneering paper on genuine gestural
innovation in wild chimpanzees by Kummer and Goodall (1985) reported a classic
example of males in a single group that repeatedly rattled and banged on empty
kerosene cans in order to generate loud noises during aggressive interactions.
Although many individuals of the group used the gesture, there was one particular
individual who succeeded in actually threatening his group members through this

!
10!
newly found gesture, thus retaining his dominant position in the group. In the same
group, another novel gesture – that of inviting an infant to be carried – was repeatedly
used and soon established itself as a group specific communicative behaviour as it was
able to achieve its intended goal. Certain gestural innovations, however, may not
succeed in establishing themselves as traditions in the group although they could have
been used by more than one individual for a certain length of time. A female
chimpanzee, for example, invented a gesture of wrist-shaking in an aggressive context
(Goodall 1973) but though this practice was adopted by another female of the same
group, it was eventually lost from the repertoire of the inventor as well as that of the
adopter.!
!
As in the case of vocal communication, captive primate groups typically show a
relatively greater number of innovative gestures. Zoo-living orangutans, for example,
were observed to modify their sequence of gestures to receive their desired food
according to the level of understanding of the food provider (Cartmill and Byrne 2007). If
they perceived the individual to have only partly understood their desire, they displayed
the same gestures repeatedly while, in cases of complete misunderstanding, they
created a new sequence consisting of novel gestures in order to achieve their goal.
Another group of rehabilitated, captive orangutans adopted different types of novel
gestures, amongst which an adult female invented a signal, arguably an iconic one, to
communicate nursing behaviour to her infant while a juvenile female of the same group
created a gesture to request her desired processing of a coconut to a food provider
(Russon 2003).!
!
The creative development and use of novel gestures appear to be more rarely reported
among monkeys, especially in the wild. Sinha (2005) reported a number of innovative
gestures used in communicative contexts in two populations of wild bonnet macaques
in southern India. Three!adult individuals of a troop, for example, systematically begged
for food from people with their hands outstretched while standing bipedally on their
hindlimbs – an interesting form of inter-species communication between two primate
species. This appears to be an example of the rapid spread of a novel behaviour within
a segment of a population implying the involvement of a largely horizontal, within-

!
11!
generation cultural process (Cavalli-Sforza and Feldman 1981). These three individuals
were amongst the highest ranked of all the adult males and females in the group and
least shy of humans, implying a possible underlying role for temperament in such
behavioural innovation. Only individuals that were motivated strongly to approach
people and beg food from them were perhaps able to learn and/or display this
behaviour!
!
A different example of a group-specific behavioural tradition that also apparently arose
from a creative innovation in a communicative context was demonstrated by the adult
females of a troop in another population. Six of the nine adult females of the troop
shook branches very frequently at human observers and less frequently towards other
troop females during agonistic interactions; this is a behaviour regularly shown by
dominant bonnet macaque males but rarely by females. Remarkably, not once did any
of the adult females of a neighbouring troop display this behaviour under any
circumstance. It is noteworthy that these two troops shared the same habitat and
frequently interacted with one another – thus ruling out environmental causation for
these behavioural variants (Sinha 2005).!
!
A classic example of a novel gesture among monkeys, evolved under captive
conditions, was that developed by female hamadryas baboons in Basel Zoo, who
expressed affiliative interest for one another by walking in parallel with their tails
intertwined and held erect (Kummer 1995). A captive group of mandrills invented a
gesture of hand extension directed towards other adults in social contexts (Laidre
2008),. The juveniles of the same group not only learnt this behaviour from the adults
but used it in a completely different context – to solicit play from the adults as there
were very few other juveniles in the group. This is not only an example of innovative
behaviour diffusing through a group but also its adoption for a novel use in a different
context by a different subset of individuals within the same group. Innovation can thus
take on different forms, fuelled by individual creativity and experience. There are also
occasional examples of!idiosyncratic gestures, performed by single individuals,
observed in several species, as for example, bonobos (Pika 2007). Although such
records have not been given much importance, such gestures could, in future, mark

!
12!
the beginnings of novel behavioural traditions in these groups; initial reports of the
inception of these behaviours could immensely help in re-constructing the whole
process.!
!
Creativity and experience in nonhuman primate communication: Clues to the
evolution of!language!
Creative innovations in nonhuman primate communication that often spread within
groups through social learning, reinforced by individual experience, and give rise to
group-specific behavioural traditions or cultures, present some interesting issues. First,
virtually all the documented examples of such creativity seem to be related to calls and
gestures in the social context, rather than, for instance, predator avoidance. One
explanation for this could be that, evolutionarily speaking, social contexts are less
critical in terms of the basic survival of individuals. Thus, individuals can afford to take
the risk of behavioural flexibility in such situations. Another possible explanation could
be that the social environments that primates live in are far more unpredictable.
Individuals of a particular macaque species, for example, usually face similar kinds of
predators in their natural habitats. The social environment for any individual of this
species, in contrast, is often not as predictable. One could, therefore, expect that an
alarm call is likely to be more stereotyped for the species while social calls, as for
example those used in affiliative contexts, could be naturally selected to be flexible and
innovative, depending on the contexts that the individual finds itself in.!
!
Of greater interest, however, are the insights that could potentially be drawn from such
examples into the evolutionary roots of human language. The dominant paradigm today
argues for human language being categorically distinct, which could have evolved either
gradually or suddenly (Chomsky 2007; Ghazanfar 2008). The suggested uniqueness of
human language is believed to stem from the innate human capacities of innovation and
social learning, with ‘traditional transmission’ by learning being a hallmark of human
communication (Hockett 1960). A child!thus learns socially to combine innate sounds or
phonemes to form words and sentences (Vygotsky 1986). This ability to create an
infinite set of words and sentences from a finite source of phonemes or, in other words,
this ‘double articulation’ or ‘duality of patterning’ is considered to be yet another

!
13!
exclusive feature of human language (Hockett 1960). Additionally, humans can invent
new words and add meanings to them by improvising and creating new utterances
(Hockett 1960).!
!
The creation of novel communicative behaviours by nonhuman primates and their
acquisition by naïve individuals through social learning, some instances of which were
discussed above, however, suggests that the generation of human language may not
truly be unique. Transmission of newly discovered communicative behaviours and their
establishment as social traditions have now been well documented in Japanese
macaques (Masataka 1992), Barbary macaques (Fischer et al. 1998), chimpanzees
(Crockford et al. 2004), bonnet macaques (Sinha 2005) and orangutans (Cartmill and
Byrne 2007). Nonhuman primates also combine different gestures to form sequences,
(Poss et al. 2006; Call and Tomasello 2007; Cartmill and Byrne 2007), similar to the
duality of patterning displayed by humans. Although we are still far from deciphering the
meaning (semantics) and organisation (syntax) of such sequences, the fact that
different modifications elicit different behavioural responses is proof enough of their
differential information content. Finally, there is now increasing evidence of the capacity
of monkeys and apes to produce new calls in novel contexts, both in the wild and in
captivity (Japanese macaques, Masataka 1992; orangutans, Russon 2003; Campbell’s
monkey, Ouattara et al. 2009; see also Reader and Laland 2003).!
!
Some of the characteristic features of human language, traditionally considered unique
to our species, thus, appear to be present in nonhuman primate communication
systems to varying degrees. This capacity to innovate and learn novel communicative
behaviours socially, therefore, could be a general ability of nonhuman primates
although it does not appear to manifest itself too commonly in the wild. This could be
due to two possible reasons. First, as described above, creativity is not as critical for an
animal’s survival as are the immediate needs of survival (Kummer and Goodall 1985).
More importantly, creative communicative behaviours could fail to be effective in
groups that are not typically cohesive or where inter-individual behavioural!coordination
is weak. In captivity, however, where individuals live under energetically relaxed
conditions, nonhuman primates do evolve innovations in novel situations. Systematic

!
14!
investigations into creative innovations in nonhuman primate communication and their
cultural transmission through social learning, usually accompanied by individual
reinforcement learning, could thus further our understanding of the evolutionary
pathways that have shaped human language.!
!
Acknowledgements!
Rajesh Kasturirangan and Anindya Sinha would like to acknowledge a research grant
on Language and Brain Organization in Normative Multilingualism from the Cognitive
Science Research Initiative of the Department of Science and Technology, Government
of India that made this study possible. We also thank Debapriyo Chakraborty and Rolla
Das for illuminating discussions.!
References!
!
Beck B.B. 1980. Animal Tool Behavior: The Use and Manufacture of Tools by Animals.
New York: Garland.!
Boesch C. 1993. Toward a new image of culture in chimpanzees. Behavior and Brain
Sciences 16: 514-515.!
Boesch C. 1995. Innovation in wild chimpanzees (Pan troglodytes). International
Journal of Primatology 16: 1-14.!
Boogert N.J., Reader S.M., Hoppitt W.J.E and Laland K.N. 2008. The origin and spread
of innovations in starlings. Animal Behaviour 75: 1509-1518.!
Burton J.A. and Nietsch A. 2010. Geographical variation in duet songs of Sulawesi
tarsiers: Evidence for new cruptic species in South and Southwest Sulawesi.
International Journal of Primatology 31: 1123-1146.!
Call J. and Tomasello M. 2007. The Gestural Communication of Apes and Monkeys.
Mahwah, New Jersey: Lawrence Erlbaum Associates.!
Cambefort J.P. 1981. A comparative study of culturally transmitted patterns of feeding
habits in the chacma baboon Papio ursinus and the vervet monkey
Cercopithecus aethiops. Folia Primatologica 36: 243-263.!
Cartmill E.A. and Byrne R.W. 2007. Orangutans modify their gestural signalling
according to their audience’s comprehension. Current Biology 17: 1345-1348.!

!
15!
Cavalli-Sforza L. L. and Feldman M. W. 1981. Cultural Transmission and Evolution: A
Quantitative Approach. Princeton: Princeton University Press.!
Chomsky N. 2007. Of minds and language. Biolinguistics 1: 9-27.!
Cousteau J.Y. 1958. The Silent World. Harmondsworth, UK: Penguin Books and
Hamish Hamilton.!
Crockford C., Herbinger I., Vigilant L. and Boesch C. 2004. Wild chimpanzees produce
group-specific calls: A case for vocal learning? Ethology 110 : 221-243.!
De La Torre S. and Snowdon C. T. 2009. Dialects in pygmy marmosets? Population
variation in call structure. Animal Journal of Primatology 71: 333-342.!
Ey E., Rahn C., Hammerschmidt K. and Fischer, J. 2009. Wild female olive baboons
adapt their grunt vocalizations to environmental conditions. Ethology 118: 493-
503.
Fischer J., Hammerschmidt K. and Todt D. 1998. Local variation in Barbary macaque
shrill barks. Animal Behavior 56: 623-629.!
Fisher J. and Hinde R.A. 1949. The opening of milk bottles by birds. British Birds 42:
347-357.
Galef B.J. Jr. 1991. Tradition in animals: field observations and laboratory analyses. In:
Bekoff!M. and Jamieson D. (eds), Interpretation and Explanation in the Study of
Behaviour, Vol. 1: Interpretation, Intentionality and Communication, pp. 74-95,
Boulder, Colorado: Westview Press.!
Galef B.G. Jr. 2003. Social learning: Promoter or inhibitor of innovation? In: Reader
S.M. and Laland K.N. (eds), Animal Innovation, pp. 137-154, Oxford: Oxford
University Press.!
Galef, B.G. Jr. 2004. Approaches to the study of traditional behaviors of free-living
animals. Learning and Behavior 32: 53-61.!
Ghazanfar A. A. 2008. Language evolution: Neural differences that make a difference.
Nature Neuroscience 11: 382-384.!
Goodall J. 1964. Tool-using and aimed throwing in a community of free-living
chimpanzees. Nature 201: 1264-1266.!
Goodall J. 1986. The Chimpanzees of Gombe: Patterns of Behaviour. Cambridge,
Mass.: Belknap Press.!
Goodall J. 1973. Cultural elements in a chimpanzee community. Symposium, 4th
International Congress of Primatology. In Manzel E. (ed), Precultural Primate
Behaviour, Vol. 1, pp. 144-184, Basel: Karger.!

!
16!
Green S. 1975. Dialects in Japanese monkeys: Vocal learning and cultural transmission
of locale-specific vocal behaviour. Zeitschrift für Tierpsychologie 38: 304-314.!
Hammerschmidt K. and Fischer J. 2008. Constraints on primate vocal production. In:
Oller D.K. and Griebel U. (eds.), Evolution of Communicative Flexibility, pp. 93-
119, Cambridge, Mass.: MIT Press.!
Hinde R.A. and Fisher J. 1951. Further observations on the opening of milk bottles by
birds. British Birds 44: 393-396.!
Hockett C.F. 1960. The origin of speech. Scientific American 203: 89-96.!
Janik V. M. and Slater P. J. B. 1997. Vocal learning in mammals. Advances in the Study
of Behavior 26: 59-99.!
Janik V. M. and Slater P. J. B. 2000. The different roles of social learning in vocal
communication. Animal Behaviour 60: 1-11.!
King B.J. 1994. The Information Continuum: Evolution of Social Information Transfer in
Monkeys, Apes and Hominids. Santa Fe, New Mexico: School of American
Research Press.!
Knott C.D. 1998. Changes in orang-utan caloric intake, energy balance, and ketones in
response to fluctuating fruit availability. International Journal of Primatology 19:
1061-1079.!
Kummer H. 1995. In Quest of the Sacred Baboon: A Scientist’s Journey. Princeton:
Princeton University Press.!
Kummer H. and Goodall J. 1985. Conditions of innovative behaviour in primates.
Philosophical Transactions of the Royal Society of London Series B 308: 203-
214.!
Laidre M.E. 2008. Do captive mandrills invent new gestures? Animal Cognition 11: 179-
187.
Laland K.N. and Plotkin H.C. 1990. Social learning and social transmission of digging
for buried!food in Norway rats. Animal Learning and Behavior 18: 246-251.!
Laland K.N. and van Bergen Y. 2003. Experimental studies of innovation in guppy. In:
Reader S.M. and Laland K.N. (eds), Animal Innovation, pp. 155-174, Oxford:
Oxford University Press.!
Lee P. 1991. Adaptations to environmental change: An evolutionary perspective. In: Box
H.O. ed), Primate Responses to Environmental Change, pp. 39-56, London:
Chapman and Hall.!
Lefebvre L. and Palameta B. 1988. Mechanisms, ecology and population diffusion of
socially-learned food-finding behaviour in feral pigeons. In Zentall T.R and Galef

!
17!
B. G. Jr. (eds), Social Learning: Psychological and Biological Perspectives, pp.
141-164, Hillsdale, New Jersey: Lawrence Erlbaum Associates.!
Lefebvre L., Whittle P., Lascaris E. and Finkelstein A. 1997. Feeding innovation and
forebrain size in birds. Animal Behaviour 53: 549-560.!
Lloyd Morgan C. 1912. Instinct and Experience. London: Methuen.!
Marler P. 1970. Bird song and speech development: Could there be parallels? American
Scientist 58: 669-673.
Masataka N. 1992. Attempts by animal caretakers to condition Japanese macaque
vocalizations result inadvertently in individual-specific calls. In: Nishida T.,
McGrew W.C., Marler M., Pickford M. and de Waal F.B.M. (eds), Topics in
Primatology, Vol. 1: Human Origins, pp. 271-278, Tokyo: University of Tokyo
Press.
McDougall W. 1936. An Outline of Psychology, 7th Edition. London: Methuen. McGrew
W. 1992. Chimpanzee Material Culture: Implications for Human Evolution.!
Cambridge: Cambridge University Press.
McGrew W.C, Marchant L.F. and Nishida T. (eds). 1996. Great Ape Societies.
Cambridge: Cambridge University Press.!
McGrew W.C. 1994. Tools compared: The material of culture. In: Wrangham R.W.,
McGrew W.C., de Waal F.B.M. and Heltne P. (eds), Chimpanzee Cultures, pp.
25-39, Cambridge, Mass.: Harvard University Press.!
McGrew W.C. 1998. Culture in nonhuman primates? Annual Review of Anthropology
27: 301-328.!
Mitani J.C., Hasegawa T., Gros-Louis J., Marler P. and Byrne R. 1992. Dialects in wild
chimpanzees? American Journal of Primatology 27: 233-243.!
Mitani, J.C. and Brandt K. 1994. Social factors influence the acoustic variability in the
long-range distance calls of male chimpanzees. Ethology 96: 233-252.!
Ouattara K., Lemasson, A. and Zuberbühler, K. 2009. Campbell’s monkeys use
affixation to alter call meaning. PLoS One 4: e7808.!
Paquette D. 1992. Discovering and learning tool-use for fishing honey by captive
chimpanzees. Human Evolution 7: 17-30.!
Pika S. 2007. Gestures in subadult bonobos (Pan paniscus). In: Call J. and Tomasello
M. (eds), The Gestural Communication of Apes and Monkeys, pp. 41-67,
Mahwah, New Jersey: Lawrence Erlbaum Associates.!
Poss S., Kuhar C., Stoinski T.S. and Hopkins W.D. 2006. Differential use of attentional
and visual communicative signaling by orangutans (Pongo pygmaeus) and

!
18!
gorillas (Gorilla gorilla) in response to the attentional status of a human.
American Journal of Primatology 68: 978-992.!
Quiatt D. and Itani J. (eds). 1994. Hominid Culture in Primate Perspective. Niwot,
Colorado: University Press of Colorado.!
Quiatt D. and Reynolds V. 1993. Primate Behaviour: Information, Social Knowledge,
and the Evolution of Culture. Cambridge: Cambridge University Press.!
Reader S.M. and Laland K.N. 2001. Primate innovation: Sex, age and social rank
differences. International Journal of Primatology 22: 787-805.!
Reader S.M. and Laland K.N. 2003. Animal innovation: An introduction. In: Reader S.M.
and Laland K.N. (eds), pp. 3-33, Oxford: Oxford University Press.!
Rendell L. and Whitehead H. 2001. Culture in whales and dolphins. Behaviour and
Brain Sciences 24: 309-324.!
Rogers E.M. 1995. Diffusion of Innovations, 4th Edition. New York: Free Press.!
Rowe N. (ed.). 1996. The Pictorial Guide to the Living Primates. New York: Pogonias
Press. !
Russon A.E. 2003. The nature and evolution of orangutan intelligence. Primates 39:
485-503.
Seyfarth R.M. and Cheney D.L. 1997. Vocal development in nonhuman primates. In:
Snowdon,!C.T. and Hausberger, M. (eds), Social Influences on Vocal
Development, pp. 249-273, Cambridge: Cambridge University Press.!
Simonton D.K. 2003. Human creativity: Two Darwinian analyses. In: Reader S.M. and
Laland K.N. (eds), Animal Innovation, pp. 309-328, Oxford: Oxford University
Press.!
Sinha A. 2003. A beautiful mind: Attribution and intentionality in wild bonnet macaques.
Current Science 85: 1021-1030.!
Sinha A. 2005. Not in their genes: Phenotypic flexibility, behavioural traditions and
cultural evolution in wild bonnet macaques. Journal of Biosciences 30: 51-64.!
Slater P.J.B. and Lachlan R.F. 2003. Is innovation in bird song adaptive? In: Reader
S.M. and Laland K.N. (eds), Animal Innovation, pp. 117-136, Oxford: Oxford
University Press.!
Snowdon C. T. 2009. Plasticity of communication in nonhuman primates. In: Naguib M.
and Janik V.M. (eds), Advances in the Study of Behavior, Vol. 40, pp. 239-276,
Burlington, Mass.: Academic Press.!

!
19!
Tanaka T., Sugiura H. and Masataka N. 2006. Cross-sectional and longitudinal studies
of the development of group differences in acoustic features of coo calls of two
groups of Japanese macaques. Ethology 112: 7-21.!
Thorpe W.H. 1956. Learning and Instinct in Animals. London: Methuen.!
Tomasello M. 1996. Do apes ape? In: Galef J. and Heyes C. (eds), Social Learning in
Animals: The Roots of Culture, pp. 319-346, San Diego: Academic Press.!
Van Begen Y., Hoppitt W. and Laland K.N. 2004. Social learning , innovation and
intelligence in fish. In: Rogers L.J. and Kaplan G. (eds), Comparative Vertebrate
Cognition: Are Primates Superior to Non-primates? pp. 141-168, New York:
Kluwer Academic/Plenum Publishers.!
Visalberghi E. and Fragaszy D.M. 1990. Do monkeys ape? In: Parker S. and Gibson K.
(eds), Language and Intelligence in Monkeys and Apes: Comparative
Developmental Perspectives, pp. 247-273, Cambridge: Cambridge University
Press.!
Vygotsky L.S. 1986. Thought and Language. Cambridge, Mass.: MIT Press!
Warner R.R. 1988. Traditionality of mating-site preferences in a coral reef fish. Nature
335: 719-721.!
Whiten A. and Ham R. 1992. On the nature and evolution of imitation in the animal
kingdom: Reappraisal of a century of research. In: Slater P.J.B., Rosenblatt J.S.,
Beer C. and Milinski M. (eds), Advances in the Study of Behaviour, Vol. 21, pp.
239-283, New York: Academic Press.!
Wrangham R.W., McGrew W.C., de Waal F.B.M. and Heltne P.G. (eds). 1994.
Chimpanzee Cultures. Cambridge, Mass.: Harvard University Press.!
Wyles J.S., Kunkel J.G. and Wilson A.C. 1983. BIrds, behaviour, and anatomical
evolution. Proceedings of the National Academy of Sciences, USA 80: 4394-
4397.!
Wynn T. 1993. Layers of thinking in tool behaviour. In: Ingold T. and Gibson K. (eds),
Tools, Language and Intelligence: Evolutionary Implications, pp. 389-406,
Cambridge: Cambridge University Press.