Establishing an experimental science of culture: animal social diffusion experiments

A growing set of observational studies documenting putative cultural variations in wild animal populations has been complemented by experimental studies that can more rigorously distinguish between social and individual learning. However, these experiments typically examine only what one animal learns from another. Since the spread of culture is inherently a group-level phenomenon, greater validity can be achieved through ‘diffusion experiments’, in which founder behaviours are experimentally manipulated and their spread across multiple individuals tested. Here we review the existing corpus of 33 such studies in fishes, birds, rodents and primates and offer the first systematic analysis of the diversity of experimental designs that have arisen. We distinguish three main transmission designs and seven different experimental/control approaches, generating an array with 21 possible cells, 15 of which are currently represented by published studies. Most but not all of the adequately controlled diffusion experiments have provided robust evidence for cultural transmission in at least some taxa, with transmission spreading across populations of up to 24 individuals and along chains of up to 14 transmission events. We survey the achievements of this work, its prospects for the future and its relationship to diffusion studies with humans discussed in this theme issue and elsewhere.

[1]  K. Laland,et al.  Diffusion of foraging innovations in the guppy , 2000, Animal Behaviour.

[2]  Mark Lubell,et al.  Beyond existence and aiming outside the laboratory: estimating frequency-dependent and pay-off-biased social learning strategies , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  K. Laland,et al.  Shoaling generates social learning of foraging information in guppies , 1997, Animal Behaviour.

[4]  Louis Lefebvre,et al.  The social transmission of a food-finding technique in pigeons: what is learned? , 1985, Animal Behaviour.

[5]  K. Laland,et al.  The effects of group size, rate of turnover and disruption to demonstration on the stability of foraging traditions in fish , 2008, Animal Behaviour.

[6]  C. Caldwell,et al.  Studying cumulative cultural evolution in the laboratory , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  E. Thomas,et al.  Effects of group size. , 1963, Psychological bulletin.

[8]  Andrew Whiten,et al.  The second inheritance system of chimpanzees and humans , 2005, Nature.

[9]  Andrew Whiten,et al.  Transmission of Multiple Traditions within and between Chimpanzee Groups , 2007, Current Biology.

[10]  Ruth C. Newberry,et al.  Cannibalistic behaviour spread by social learning , 2002, Animal Behaviour.

[11]  Lydia M. Hopper,et al.  Experimental studies of traditions and underlying transmission processes in chimpanzees , 2007, Animal Behaviour.

[12]  Andrew Whiten,et al.  The evolution of animal ‘cultures’ and social intelligence , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  D. Paquette.  Discovering and learning tool-use for fishing honey by captive chimpanzees , 1992 .

[14]  K. Laland,et al.  Further experimental analysis of the social learning and transmission of foraging information amongst Norway rats , 1992, Behavioural Processes.

[15]  J. Cambefort.  A comparative study of culturally transmitted patterns of feeding habits in the chacma baboon Papio ursinus and the vervet monkey Cercopithecus aethiops. , 1981, Folia primatologica; international journal of primatology.

[16]  A. Whiten,et al.  How do apes ape? , 2004, Learning & behavior.

[17]  K. Laland,et al.  Social transmission of food preferences among norway rats by marking of food sites and by gustatory contact , 1993 .

[18]  A. Whiten,et al.  Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children , 2006, Proceedings of the National Academy of Sciences.

[19]  L. Lefebvre.  Cultural Diffusion of a Novel Food-finding Behaviour in Urban Pigeons: an Experimental Field Test , 2010 .

[20]  Kevin N. Laland,et al.  Social learning and social transmission of foraging information in Norway rats (Rattus norvegicus) , 1990 .

[21]  Perspectives on Imitation: From Mirror Neurons to Memes, Vol II , 2005 .

[22]  Kevin N. Laland,et al.  Familiarity facilitates social learning of foraging behaviour in the guppy , 2001, Animal Behaviour.

[23]  A. Whiten,et al.  Conformity to cultural norms of tool use in chimpanzees , 2005, Nature.

[24]  Andrew Whiten,et al.  Spread of arbitrary conventions among chimpanzees: a controlled experiment , 2007, Proceedings of the Royal Society B: Biological Sciences.

[25]  T. Matsuzawa,et al.  Acquisition and Transmission of Tool Making and Use for Drinking Juice in a Group of Captive Chimpanzees (Pan troglodytes) , 1997 .

[26]  W. McGrew.  CULTURE IN NONHUMAN PRIMATES , 1998 .

[27]  D. Campbell,et al.  The perpetuation of an arbitrary tradition through several generations of a laboratory microculture. , 1961, Journal of abnormal and social psychology.

[28]  F. D. de Waal,et al.  Modification of reconciliation behavior through social experience: an experiment with two macaque species. , 1993, Child development.

[29]  T. Matsuzawa.  Field experiments on use of stone tools by chimpanzees in the wild. , 1994 .

[30]  W. McGrew,et al.  Chimpanzees using stones to crack open oil palm nuts in Liberia , 2006, Primates.

[31]  Masao Kawai,et al.  Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet , 1965, Primates.

[32]  C. Heyes,et al.  Social learning in animals : the roots of culture , 1996 .

[33]  A. Whiten,et al.  The multiple roles of cultural transmission experiments in understanding human cultural evolution , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  A. Whiten,et al.  On the Nature and Evolution of Imitation in the Animal Kingdom: Reappraisal of a Century of Research , 1992 .

[35]  U. Ernst,et al.  The adaptive significance of avian mobbing: II. Cultural transmission of enemy recognition in blackbirds: Effectiveness and some constraints. , 2010 .

[36]  S. Hirata,et al.  An experimental study of leaf swallowing in captive chimpanzees: insights into the origin of a self-medicative behavior and the role of social learning , 2004, Primates.

[37]  I. Morrison.  Genuine imitation , 2002, Trends in Cognitive Sciences.

[38]  T. A. Langen.  Social Learning of a Novel Foraging Skill by White‐throated Magpie‐jays (Calocitta formosa, Corvidae): a Field Experiment , 2010 .

[39]  U. Ernst,et al.  Cultural Transmission of Enemy Recognition: One Function of Mobbing , 1978, Science.

[40]  J. Kitahara-Frisch,et al.  The acquisition of stone-tool use in captive chimpanzees , 1985, Primates.

[41]  Emma Flynn,et al.  Investigating children as cultural magnets: do young children transmit redundant information along diffusion chains? , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[42]  E. Price,et al.  Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis , 2007, Behavioural Processes.

[43]  D. Biro,et al.  Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments , 2003, Animal Cognition.

[44]  Cecilia Heyes,et al.  Special issue on social learning and imitation , 2004 .

[45]  L. Huber,et al.  Testing social learning in a wild mountain parrot, the kea (Nestor notabilis) , 2004, Learning & behavior.

[46]  B. Galef,et al.  A new model system for studying behavioural traditions in animals , 1995, Animal Behaviour.

[47]  E. Visalberghi,et al.  The Complete Capuchin: The Biology of the Genus Cebus , 2004 .

[48]  A. Whiten,et al.  Cultural panthropology , 2003 .

[49]  A. Whiten,et al.  Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella) , 2008, Proceedings of the Royal Society B: Biological Sciences.

[50]  A. King,et al.  Cultural transmission of vocal traditions in cowbirds (Molothrus ater) influences courtship patterns and mate preferences. , 2001, Journal of comparative psychology.

[51]  K. Laland,et al.  Social transmission of maladaptive information in the guppy , 1998 .

[52]  K. Laland,et al.  Social learning of a novel avoidance task in the guppy: conformity and social release , 2002, Animal Behaviour.

[53]  T. Freeberg.  The cultural transmission of courtship patterns in cowbirds,Molothrus ater , 1998, Animal Behaviour.

[54]  K. Laland,et al.  Towards a unified science of cultural evolution. , 2006, The Behavioral and brain sciences.

[55]  Cecilia Heyes,et al.  CHAPTER 17 – Genuine Imitation? , 1996 .

[56]  B. Galef.  The question of animal culture , 1992, Human nature.

[57]  E. Menzel,et al.  Protocultural aspects of chimpanzees' responsiveness to novel objects. , 1972, Folia primatologica; international journal of primatology.