Experimental evidence for the co-evolution of hominin tool-making teaching and language.

Hominin reliance on Oldowan stone tools-which appear from 2.5 mya and are believed to have been socially transmitted-has been hypothesized to have led to the evolution of teaching and language. Here we present an experiment investigating the efficacy of transmission of Oldowan tool-making skills along chains of adult human participants (N=184) using five different transmission mechanisms. Across six measures, transmission improves with teaching, and particularly with language, but not with imitation or emulation. Our results support the hypothesis that hominin reliance on stone tool-making generated selection for teaching and language, and imply that (i) low-fidelity social transmission, such as imitation/emulation, may have contributed to the ~700,000 year stasis of the Oldowan technocomplex, and (ii) teaching or proto-language may have been pre-requisites for the appearance of Acheulean technology. This work supports a gradual evolution of language, with simple symbolic communication preceding behavioural modernity by hundreds of thousands of years.

The impact of moving to a novel environment on social networks, activity and wellbeing in two new world primates.

Among the stressors that can affect animal welfare in zoos, the immediate effect of relocation to a novel environment is one that has received little attention in the literature. Here, we compare the social network, daily activity and the expression of stress-related behavior in capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) before and just after they were relocated to a new enriched enclosure. Results showed similar immediate responses to the move in the two species. Both showed a substantial increase in the time spent resting and spent more time in the highest and "safest" part of their enclosure after relocation. Both capuchins and squirrel monkeys spent significantly more time in close proximity to other group members after relocation, compared to before. In squirrel monkeys, the structure of the social network, which was initially correlated to affiliation, was no longer so after the move. In capuchins, the network analysis showed that individuals regrouped by age, with the youngsters who were potentially more affected by stress being in the center of the network. Social network analysis helped to achieve a more complete picture of how individuals were affected by relocation. We suggest that this type of analysis should be used alongside traditional methods of observation and analysis to encompass the most complex aspects of animal behavior in times of stress and to improve welfare.

Imitative learning by captive western lowland gorillas (Gorilla gorilla gorilla) in a simulated food-processing task.

Although field studies have suggested the existence of cultural transmission of foraging techniques in primates, identification of transmission mechanisms has remained elusive. To test experimentally for evidence of imitation in the current study, we exposed gorillas (Gorilla gorilla gorilla) to an artificial fruit foraging task designed by A. Whiten and D. M. Custance (1996). Gorillas (n=6) watched a human model remove a series of 3 defenses around a fruit. Each of the defenses was removed using 1 of 2 alternative techniques. Subsequent video analysis of gorillas' behavior showed a significant tendency to copy the observed technique on 1 of the individual defenses and the direction of removal on another defense. This is the first statistically reliable evidence of imitation in gorillas. Sequence of defense removal was not replicated. The gorillas' responses were most similar to those of chimpanzees.

Mental evolution and development: evidence for secondary representation in children, great ages, and other animals.

Recent interest in the development and evolution of theory of mind has provided a wealth of information about representational skills in both children and animals. According to J. Perner (1991), children begin to entertain secondary representations in the 2nd year of life. This advance manifests in their passing hidden displacement tasks, engaging in pretense and means-ends reasoning, interpreting external representations, displaying mirror self-recognition and empathic behavior, and showing an early understanding of "mind" and imitation. New data show a cluster of mental accomplishments in great apes that is very similar to that observed in 2-year-old humans. It is suggested that it is most parsimonious to assume that this cognitive profile is of homologous origin and that great apes possess secondary representational capacity. Evidence from animals other than apes is scant. This analysis leads to a number of predictions for future research.

Imitation, mirror neurons and autism.

Various deficits in the cognitive functioning of people with autism have been documented in recent years but these provide only partial explanations for the condition. We focus instead on an imitative disturbance involving difficulties both in copying actions and in inhibiting more stereotyped mimicking, such as echolalia. A candidate for the neural basis of this disturbance may be found in a recently discovered class of neurons in frontal cortex, 'mirror neurons' (MNs). These neurons show activity in relation both to specific actions performed by self and matching actions performed by others, providing a potential bridge between minds. MN systems exist in primates without imitative and 'theory of mind' abilities and we suggest that in order for them to have become utilized to perform social cognitive functions, sophisticated cortical neuronal systems have evolved in which MNs function as key elements. Early developmental failures of MN systems are likely to result in a consequent cascade of developmental impairments characterised by the clinical syndrome of autism.

Testing for social learning in the "artificial fruit" processing of wildborn orangutans (Pongo pygmaeus), Tanjung Puting, Indonesia.

Social learning about actions, objects and sequencing was investigated in a group of 14 wildborn orangutans (four adult females and ten 3- to 5-year-old juveniles). Human models showed alternative methods and sequences for dismantling an artificial fruit to groups of participants matched by gender and age. Each participant received three to six 2-min trials in which they were given access to the artificial fruit for manipulation. Independent coders, who were unaware of which method each participant had seen, gave confidence ratings and collected action frequencies from watching video recordings of the experimental trials. No significant differences were found between groups in terms of the coders' confidence ratings, the action frequencies or the sequence of manipulations. These negative results may at least partly reflect the immaturity of a large proportion of the participants. A positive correlation was found between age and the degree of matching to the method shown. Although none of the juveniles succeeded in opening the "fruit", two out of the four adults did so and they also seemed to match more closely the sequence of elements touched over successive trials. The results are compared with similar data previously collected from human children, chimpanzees, gorillas, capuchin monkeys and common marmosets.

Social complexity and social intelligence.

When we talk of the 'nature of intelligence', or any other attribute, we may be referring to its essential structure, or to its place in nature, particularly the function it has evolved to serve. Here I examine both, from the perspective of the evolution of intelligence in primates. Over the last 20 years, the Social (or 'Machiavellian') Intelligence Hypothesis has gained empirical support. Its core claim is that the intelligence of primates is primarily an adaptation to the special complexities of primate social life. In addition to this hypothesis about the function of intellect, a secondary claim is that the very structure of intelligence has been moulded to be 'social' in character, an idea that presents a challenge to orthodox views of intelligence as a general-purpose capacity. I shall outline the principal components of social intelligence and the environment of social complexity it engages with. This raises the question of whether domain specificity is an appropriate characterization of social intelligence and its subcomponents, like theory of mind. As a counter-argument to such specificity I consider the hypothesis that great apes exhibit a cluster of advanced cognitive abilities that rest on a shared capacity for second-order mental representation.

Social anxiety, relationships and self-directed behaviour among wild female olive baboons.

Self-directed behaviour (SDB) can be used as a behavioural indicator of stress and anxiety in nonhuman primates (Maestripieri et al. 1992, Animal Behaviour, 44, 967-979). We investigated the effect of nearest neighbours' relative dominance status on the SDB of sexually mature female olive baboons, Papio anubis. When the animal nearest to (within 5 m of) a female was a dominant individual, SDB rates (a combined measure of self-scratching, self-grooming, self-touching, body shaking and yawning) increased by ca. 40% over those observed when the nearest neighbour was a subordinate. The results indicate that (1) SDB can be used as a measure of uncertainty during the social interactions of cercopithecine primates and (2) as there was considerable variation in SDB response according to the nature of the dominant individual, SDB can be used to assess relationship security (i.e. the perceived predictability of a relationship for one partner). Finally, in combination with measures of affiliation rate, SDB may provide insight into relationship value. Copyright 1999 The Association for the Study of Animal Behaviour.

Cultures in chimpanzees.

As an increasing number of field studies of chimpanzees (Pan troglodytes) have achieved long-term status across Africa, differences in the behavioural repertoires described have become apparent that suggest there is significant cultural variation. Here we present a systematic synthesis of this information from the seven most long-term studies, which together have accumulated 151 years of chimpanzee observation. This comprehensive analysis reveals patterns of variation that are far more extensive than have previously been documented for any animal species except humans. We find that 39 different behaviour patterns, including tool usage, grooming and courtship behaviours, are customary or habitual in some communities but are absent in others where ecological explanations have been discounted. Among mammalian and avian species, cultural variation has previously been identified only for single behaviour patterns, such as the local dialects of song-birds. The extensive, multiple variations now documented for chimpanzees are thus without parallel. Moreover, the combined repertoire of these behaviour patterns in each chimpanzee community is itself highly distinctive, a phenomenon characteristic of human cultures but previously unrecognised in non-human species.

Imitation of the sequential structure of actions by chimpanzees (Pan troglodytes).

Imitation was studied experimentally by allowing chimpanzees (Pan troglodytes) to observe alternative patterns of actions for opening a specially designed "artificial fruit." Like problematic foods primates deal with naturally, with the test fruit several defenses had to be removed to gain access to an edible core, but the sequential order and method of defense removal could be systematically varied. Each subject repeatedly observed 1 of 2 alternative techniques for removing each defense and 1 of 2 alternative sequential patterns of defense removal. Imitation of sequential organization emerged after repeated cycles of demonstration and attempts at opening the fruit. Imitation in chimpanzees may thus have some power to produce cultural convergence, counter to the supposition that individual learning processes corrupt copied actions. Imitation of sequential organization was accompanied by imitation of some aspects of the techniques that made up the sequence.

Imitative learning of artificial fruit processing in children (Homo sapiens) and chimpanzees (Pan troglodytes).

Observational learning in chimpanzees and young children was investigated using an artificial fruit designed as an analog of natural foraging problems faced by primates. Each of 3 principal components could be removed in 2 alternative ways, demonstration of only one of which was watched by each subject. This permitted subsequent imitation by subjects to be distinguished from stimulus enhancement. Children aged 2-4 years evidenced imitation for 2 components, but also achieved demonstrated outcomes through their own techniques. Chimpanzees relied even more on their own techniques, but they did imitate elements of 1 component of the task. To our knowledge, this is the first experimental evidence of chimpanzee imitation in a functional task designed to simulate foraging behavior hypothesized to be transmitted culturally in the wild.

Chemical composition of baboon plant foods: implications for the interpretation of intra- and interspecific differences in diet.

Information on the chemical composition of baboon foods from the Laikipia Plateau, Kenya, is presented. Despite some differences in methods, results of analyses performed on the same foods at different sites were found to be extremely consistent, encouraging the view that meaningful intra- and interspecific comparisons of diet selection are feasible. Contrary to assumptions in the literature, no relationship between the abundance of food types and their chemical composition was found, nor was the foliage eaten by the baboons found to be a low-quality or high-fibre item in comparison with fruits and storage organs. Emphasis is placed on the need for caution in the use of simplistic dietary taxonomies which imply phytochemical and ecological homogeneity within broad food categories. Comparisons between three species revealed marked differences in the chemical composition of their diets; in particular, baboon diets were found to be higher in protein and lower in fibre than those of either lowland gorillas or Malaysian leaf monkeys, and differences in condensed tannin levels were also found. The relationship between these differences and the socio-ecology of the three species is discussed.

Dietary and foraging strategies of baboons.

As large-bodied savannah primates, baboons have long been of special interest to students of human evolution: many different populations have been studied and dietary comparisons among them are becoming possible. Baboons' foraging strategies can be shown to combine high degrees of flexibility and breadth with selectivity. In this paper we develop and test multivariate models of the basis of diet selection for populations of montane and savannah baboons. Food selection is positively related to protein and lipid content and negatively to fibre, phenolics and alkaloids. Seasonal changes in dietary criteria predicted by these rules are tested and confirmed. Although nutritional bottlenecks occur at intervals, a comparison between long-term nutrient intakes in four different populations indicates convergence on lower degrees of variation than exist in superficial foodstuff profiles.

Social relationships of mountain baboons: Leadership and affiliation in a non-female-bonded monkey.

Instead of close and differentiated relationships among adult females, the accepted norm for savanna baboons, groups of Drakensberg mountain baboons (Papio ursinus) showed strong affiliation of females towards a single male. The same male was usually the decision-making animal in controlling group movements. Lactating or pregnant females focused their grooming on this "leader" male, producing a radially patterned sociogram, as in the desert baboon (P. hamadryas); the leader male supported young animals in the group against aggression and protected them against external threats. Unlike typical savanna baboons, these mountain baboons rarely displayed approach-retreat or triadic interactions, and entirely lacked coalitions among adult females. Both groups studied were reproductively one-male; male-female relationships in one were like those in a unit of a hamadryas male at his peak, while the other group resembled the unit of an old hamadryas male, who still leads the group, with a male follower starting to build up a new unit and already monopolizing mating. In their mountain environment, where the low population density suggests conditions as harsh for baboons as in deserts, adults in these groups kept unusually large distances apart during ranging; kin tended to range apart, and spacing of adults was greatest at the end of the dry, winter season. These facts support the hypothesis that sparse food is responsible for convergence with hamadryas social organization. It is suggested that all baboons, though matrilocal, are better categorized as "cross-sex-bonded" than "female bonded".

Social relationships of mountain baboons: Leadership and affiliation in a non-female-bonded monkey.

Instead of close and differentiated relationship among adult females, the accepted norm for savanna baboons, groups of Drakensberg mountain baboons (Papio ursinus) showed strong affiliation of females towards a single male. The same male was usually the decision-making animal in controlling group movements. Lactating or pregnant females focused their grooming on this "leader" male, producing a radially patterned sociogram, as in the desert baboon (P. hamadryas); the leader male supported young animals in the group against aggression and protected them against external threats. Unlike typical savanna baboons, these mountain baboons rarely displayed approach-retreat or triadic interactions, and entirely lacked coalitions among adult females. Both groups studied were reproductively one-male; male-female relationships in one were like those in a unit of hamadryas male at his peak, while the other group resembled the unit of an old hamadryas male, who still led the group, with a male follower starting to build up a new unit and already monoplizing mating. In their mountain environment, where the low population density suggests conditions as harsh for baboons as in deserts, adults in these groups kept unusually large distances apart during ranging; kin tended to range apart, and spacing of adults was greatest at the end of the dry, winter season. These facts support the hypothesis that sparse food is responsible for convergence with hamadryas social organization. It is suggested that all baboons, though matrilocal, are better categorized as "cross-sex-bonded" than "female bonded".

Demise of the checksheet: Using off-the-shelf miniature hand-held computers for remote fieldwork applications.

Laboratory-based researchers have increasingly reaped the benefits of entering data directly into a computer; those concerned with behaviour often using specially designed keyboards. However, many ecologists and ethologists doing fieldwork in remote places have been reluctant to abandon paper checksheets because of worries about unreliability, lack of electrical supply and sheer weight of computer equipment, adding to more general drawbacks such as the need for considerable expertise in purpose-built hardware and software. Having used commercially available hand-held computers extensively for our own fieldwork on baboons in Africa, we are confident that these worries are unfounded. As some researchers have already discovered, field computerization is not something to be distrusted, but in fact offers several important benefits.