The chimps fight culture wars, too

Jessica Flack welcomes a survey of how and why animal societies operate successfully.

" ...nevertheless the difference in mind between man and the higher animals, great as it is, certainly is one of degree and not of kind. We have seen that the senses and intuitions, the various emotions and faculties, such as love, memory, attention, curiosity, imitation, reason, etc., of which man boasts, may be found in an incipient, or even sometimes in a well-developed condition, in the lower animals ." Charles Darwin, The Descent of Man .

" Nikkie, the leader of the group, has slapped Hennie during a passing charge. Hennie, a young adult female of nine years, sits apart for a while feeling with her hand the spot on the back of the neck where Nikkie hit her. Then she seems to forget about the incident; she lies down in the grass, staring in the distance. More than 15 minutes later, Hennie slowly gets up and walks straight to a group that includes Nikkie and the oldest female, Mama. Hennie approaches Nikkie with a series of soft pant grunts. Then she stretches out her arm to offer Nikkie the back of her hand for a kiss. Nikkie's hand-kiss consists of taking Hennie's whole hand rather unceremoniously into his mouth. This contact is followed by a mouth-to-mouth kiss ."

Frans de Waal , Peacemaking among Primates , describing a conflict and reconciliation between two chimpanzees.

Few of us have had the opportunity to observe animals interacting in their social groups. Even fewer of us have had the opportunity to observe the behaviour and interactions, exemplified in the above anecdote, of long-lived, large-brained, highly social species, such as chimpanzees, killer whales, elephants and parrots. So it is no surprise that humans have historically been rather dismissive of non-human animal social complexity.

The publication of Darwin's On the Origin of Species (1859), The Descent of Man (1871) and The Expression of the Emotions in Man and Animals (1898) and George Romanes' Animal Intelligence (1882) and Mental Evolution in Animals (1883) laid the groundwork for a more informed and sophisticated debate about the question of human uniqueness and animal behaviour. In the first half of the 20th century, the debate found its centre in behaviourism - the study of observable behaviour and its underlying learning processes, made famous by the work of J. B. Watson, Edward Thorndike, Ivan Pavlov and B. F. Skinner.

Developing in parallel with behaviourism was ethology, which then focused on how so-called innate and species-specific behaviour patterns contributed to survival and reproduction, and was made famous by the work of Niko Tinbergen and Konrad Lorenz.

Neither school emphasised animal cognition or social behaviour. Animal cognition - primate cognition, in particular - was pursued by Wolfgang Kohler and Robert Yerkes, who performed some of the first problem-solving experiments with great apes and generally served as the antidote to behaviourism. The study of social behaviour and organisation developed somewhat independently through the work of Thorleif Schjelderup-Ebbe and W.

C. Allee, who studied the emergence of dominance hierarchies in chickens and other vertebrates to understand how stability was maintained in social groups.

The second half of the 20th century brought with it increasing attention to animal cognition, social behaviour and communication. This trend was most identifiable in the development of the field of primatology, which began with studies of free-ranging rhesus monkeys by C. R. Carpenter and of Japanese macaques by Kinji Imanishi in the 1940s and 1950s, but did not take off until the fieldwork on apes and lemurs of Jane Goodall, Birute Galdikas, Alison Jolly and Dian Fossey. Whereas their research jump-started the study of animal behaviour and communication in naturalistic, rather than laboratory, settings, the study of how cognition and social behaviour interact to produce social complexity was sparked by two seminal books - The Question of Animal Awareness: Evolutionary Continuity of Mental Experience , by Donald Griffin, and Chimpanzee Politics , by Frans de Waal, one of the editors of Animal Social Complexity .

This book, edited by De Waal and Peter Tyack, a biologist who studies dolphins and whales, is the latest contribution to the debate over what animals understand about their social environments and how this influences their behaviour and organisation. It comprises 18 papers and several case studies by 52 prominent scientists or promising young researchers. The topics covered range from life history and cognitive evolution in primates, laughter and smiling in mammals, and vocal communication in wild parrots, to questions of emotional recognition in chimpanzees and the possibility of culture in killer whales. The volume's most notable contribution is that it brings together a collection of studies on a wide range of species and topics in an effort to provide the groundwork for future synthetic work on the organising principles underlying complex animal societies.

The central theme is the exploration of the relationship between social intelligence and social behaviour in relatively large-brained, long-lived species characterised by triadic awareness - that is, the awareness of third parties and their influence on the outcome of dyadic interactions.

The editors' intention is to debunk the popular notion that animals are "gene machines, programmed to act in particular ways". Rather, they propose that future research will reveal animal societies to be flexible systems moulded by social learning. Indeed, this is the contributors' consensus, although there is, as in any field, substantial disagreement over the details.

One of the most important advances in the study of animal social complexity, advocated in the 1960s and 1970s by psychologist Robert Hinde, is that to understand social behaviour we must consider it in the relationship context. This might seem obvious, but at the time aggression was thought to be the product of a frustrated internal state, and little thought was given to the way in which social environment affected its expression. Even now, different types of interaction patterns, for example, conflict and affiliation, are typically studied independently, although individuals participate in multiple overlapping social networks, and the structure of any of these networks is likely to affect the structure of others.

This type of issue underlies many of the discussions throughout Animal Social Complexity . For example, biologists Anne Engh and Kay Holekamp suggest in their case study, "Maternal rank inheritance in the spotted hyena", that mothers, by providing effective coalitionary support in disputes between their offspring and others, can influence the rank a cub obtains by causing it to "win" conflicts against all opponents of lower rank than the mother. This simple process allows a cub to occupy the dominance rank just below its mother's. This is a good example of how a kinship network and two aggression networks (the mother's and the cub's) interact to influence the emergence of dominance hierarchies.

Emile Durkheim, one of the founders of sociology, stressed that social behaviour is shaped by "social facts", which are external to individuals (except in the sense of being realised through them) and persist when individuals die. This issue is a central but rarely discussed problem in the study of animal social complexity: how do we account for the persistence of animal social organisations despite components that are subject to development and senescence? An interesting discussion of this topic can be found in biologist Katy Payne's chapter, which details how the development and persistence of multiple and many-layered social relationships in elephant society results from the ability of the elephant to recognise and track individuals over long periods based on their age, condition and social status. Payne suggests that these factors, in combination with learning in the context of overlapping generations, promote a highly flexible social system.

Closely related to the question of how social organisations persist through time, despite perturbations and changing components, with only partly overlapping interests, is the question of animal culture. Animal culture has traditionally been approached from the anthropological perspective, where the primary question has been one of human uniqueness. Much of the debate has focused on what constitutes evidence of culture and, correspondingly, how "culture" should be defined, rather than on the implications culture has for animal social organisation or animal social complexity. Primatologist Bill McGrew provides a nice overview of the positions characterising both sides of the debate in "Ten dispatches from the chimpanzee culture wars". Meredith West and colleagues discuss how social interaction and feedback play a major role in song learning in cowbirds and starlings. They stress that understanding the extent to which culture is present in animal societies requires studying how developmental processes, interacting with the social environment, make organismal behaviour more or less modifiable.

A primary concern of the philosopher and semiotician Charles Sanders Peirce was the question of how meaning is produced and assigned by receivers and observers. Although Peirce was thinking mainly of human systems, this problem is also a fundamental issue in the study of animal social complexity. Peirce is particularly relevant to questions of whether primates and other cognitively sophisticated animals are capable of using symbols or only indices. Symbols are a class of signal that are arbitrarily connected to the object they stand for, as a word typically is to its referent. In animal behaviour, indices are connected to their referents through underlying physiological or genetic substrate (characteristics), as the "stotting" behaviour - a series of stiff-legged, vertical leaps performed with the head down and the back arched - of the springbok antelope is presumed to be to its physical fitness, thus signalling to predators that the antelope will be difficult to catch. Issues related to symbolic and proto-symbolic communication, typically called representational signalling in animal behaviour, are discussed in the sections of Animal Social Complexity on communication and on cognition.

Particularly interesting reports include Ronald Schusterman and colleagues' chapter "Equivalence classification as an approach to social knowledge: From sea lions to simians", and Klaus Zuberbuhler's case study, "Natural semanticity in primates".

Although the culmination of years of work, Animal Social Complexity marks only the beginning of determined investigation of animal social organisations. That is, their mechanics, how social structure emerges from communication networks, how, despite changing components, they persist in time by virtue of social learning and socialisation processes, and how cognition interacts with, and helps produce, social structure to make possible complex forms of sociality.

To accomplish this ambitious goal, animal behaviour researchers will have to look to other fields with a history of asking these questions. Credit is due to De Waal and Tyack for putting together this book, the product of an academic meeting held in 2000 in Chicago. It should be of interest to anyone curious about animal behaviour.

Jessica Flack is a postdoctoral fellow at the Santa Fe Institute, Santa Fe, New Mexico, US.