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The Animal Cultures Debate Opinion TRENDS in Ecology and Evolution Vol.21 No.10 The animal cultures debate Kevin N. Laland and Vincent M. Janik Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, Bute Building, Queen’s Terrace, St. Andrews, Fife, UK, KY16 9TS Recent interest in animal cultures has been fuelled by relationships among culture-like phenomena in diverse high-profile reports of intra- and interpopulation differ- taxa. A broad definition is likely to be more stimulating ences in the behavioural repertoires of primates and and henceforth we refer to culture (or tradition) as all group- cetaceans, consistent with the existence of socially typical behaviour patterns, shared by members of animal learned traditions. Several studies have mapped spatial communities, that are to some degree reliant on socially differences in behaviour, revealing a mosaic of beha- learned and transmitted information [4]. Here, we criticize vioural phenotypes within species. The dominant cur- the dominant (‘ethnographic’) method for identifying animal rent approach attempts to determine whether this is cultures, which seeks to isolate cultural variation by ruling cultural variation by excluding asocial learning, ecologi- out alternative explanations for behavioural differences, cal or genetic factors. However, claims of animal cultures and instead advocate a more thorough consideration of remain controversial because such comparisons are sub- the interplay between genetics, ecology and culture. ject to weaknesses; thus, new approaches to isolating the influence of culture on behaviour are required. Here Animal cultures we suggest that, rather than attributing behaviour to The idea that animals might acquire components of their explanatory categories, researchers would often be bet- behavioural repertoire by copying others has a long his- ter advised to partition variance in behaviour to alter- tory, dating back to Aristotle. Several early evolutionists, native sources. including Wallace, Morgan and Baldwin, emphasised learned traditions as a source of adaptive behaviour [6]. Introduction More recently, researchers have documented vocal dialects The ‘inheritance of acquired behaviour’ has been a long- in bird song [7] and the diffusion of novel foraging beha- standing interest of biologists and psychologists alike, viour in animal populations [8–10]. Whereas some animal albeit tainted in the minds of many by its association with traditions might be specialised adaptations, a few animals Lamarckism. However, the social learning of knowledge, (e.g. some primates) appear to have a broad cultural skills and vocalisation is now a well-established and non- repertoire. For instance, building on earlier work of controversial aspect of the adaptive behaviour of verte- McGrew [1], Whiten et al. [11] synthesised behavioural brates. This social learning can take many forms, from information on chimpanzee Pan troglodytes populations social attraction to a location where individuals then learn collated from seven different sites across Africa. Their independently (local enhancement) to the close observation analysis revealed 65 categories of behaviour, 42 of which and copying of the behaviour of a conspecific (imitation). exhibited significant variability across sites. Some of this The largest body of evidence for social learning comes from variation could be attributed to differences in ecology. For vocal learning studies of birds and foraging specialisations instance, the absence of ground night-nesting at four sites in primates and, in some cases, the patterns observed are could be explained by high-predation risk from leopards evocative of human cultural variation. However, whether and lions. However, once ecological explanations had been this resemblance is superficial, indicative of convergent discounted, 39 variants, including tool usage, grooming selection acting on humans and animals, or a manifesta- and courtship behaviour, were absent at some sites but tion of homologous traits shared with humans, is highly common at others, and it is these that Whiten et al. contentious [1–5]. described as cultural. As in human societies, for which Debates have revolved around how to define culture, differences are constituted by multiple variations in tech- what kinds of social learning support it and how best to nology and conventions, the behavioural profiles of each interpret behavioural variation [1–5]. Even for humans, community were also distinctively different. Seemingly a culture has proven a difficult concept to pin down and there unique case could be made for the chimpanzee as a cultural exists little definitional consensus within the social sciences. animal. Whereas some researchers characterise species as cultural However, far from singling out chimpanzees, the study according to whether they exhibit ‘key characteristics’ of prompted a spate of articles arguing that geographical human culture, we suggest here that an anthropocentric differences in the behavioural repertoires of other large- perspective acts as a barrier to understanding the evolu- brained mammals were cultural [12–15]. The approach, tionary roots of culture, and jeopardises our ability to see commonly known as the ‘ethnographic method’ [16], has now become the standard means for detecting animal Corresponding author: Laland, K.N. ([email protected]). culture. For instance, van Schaik et al. [12] applied this Available online 27 June 2006 method to six orangutan Pongo spp. populations www.sciencedirect.com 0169-5347/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2006.06.005 Opinion TRENDS in Ecology and Evolution Vol.21 No.10 543 throughout Borneo and Sumatra. The authors identified 24 Box 1. Vocal cultures putative cultural variants, including feeding techniques and social signals, with each population characterised by a Vocal cultures can be found in numerous birds and mammals [7,17,38], and provide the largest body of evidence for cultural distinctive repertoire; for example, some populations of transmission of behavioural traits in the animal kingdom. However, orangutans make leaf-bundle ‘dolls’, whereas others use vocal learning is still seen as a special adaptation [6,39,40] and it has tools as sexual stimulants or blow raspberries at bedtime. not yet been fully integrated into discussions of animal culture. This Around the same time as van Schaik et al. were writing is largely because early studies of bird-song learning stressed the [12], a long-term collaborative study of capuchin monkeys importance of sensitive phases and the lack of flexibility once song had developed. Although this is true for some avian species (e.g. Cebus capucinus revealed behavioural variation in the zebra finch Taeniopygia guttata), further work has revealed a social conventions of 13 social groups throughout Costa remarkable variety of learning processes, including learning when Rica [13]. Several striking and often bizarre social conven- to use a copied sound [41] and learning new song throughout life tions were candidate cultural traditions, including hand [7]. Thus, there are many birds that appear to be no more or less sniffing, sucking of body parts and placing fingers in the genetically predisposed to learn a song than a chimpanzee is to learn how to use a tool. There is a difference in that vocal learning mouths of other monkeys. Variation in such conventions is does not occur in every avian species, whereas general associative not obviously attributable to differences in ecological learning can be found in all vertebrates. Although this is important if resource distribution across sites, and the monkeys might we are interested in learning mechanisms, it makes little sense to use group-specific social conventions to test the quality of exclude vocalisations if we are looking at animal culture, just like it their social relationships. would make little sense to exclude spoken language from human culture studies. Bird and mammal dialect studies have given us a Social learning in cetaceans had also been established more detailed understanding of mechanisms involved in diffusion long before the recent flurry of studies of culture. Much of and cultural drift than have any other culture studies. this research had been in the vocal domain of bottlenose Studies of humpback whale Megaptera novaeangliae song dolphins Tursiops truncatus and humpback whales Mega- demonstrate that studying culture is possible even with large and ptera novaeangliae relatively inaccessible mammals, and provide some of the most [17] (Box 1). Calls and songs are more compelling evidence for animal cultures (Figure I). All males in a easily recognised as a form of social learning because population share the same song at any one time, but the song communication signals can only be learnt from another changes gradually throughout the singing season. In Bermuda, animal. However, claims of social learning have been made humpback whales change, on average, 37% of their song each year, for other domains, particularly foraging and migratory too rapid a rate to be explained plausibly by genes. It took 15 years to change the entire song [42]. However, off the east coast of traditions, moving the topic of culture into the spotlight Australia, the entire song changed within two years to match that of cetacean research. A recent review [14] lists a broad found off the west coast [43], apparently triggered by the movement range of traits that are interpreted to be cultural, including of
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