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The Ecology of Social Learning in Animals and its Link with Intelligence

Published online by Cambridge University Press:  09 January 2017

Carel van Schaik ,
Sereina Graber ,
Caroline Schuppli  and
Judith Burkart
Carel van Schaik*
Affiliation:
University of Zurich (Switzerland)
Sereina Graber
Affiliation:
University of Zurich (Switzerland)
Caroline Schuppli
Affiliation:
University of Zurich (Switzerland)
Judith Burkart
Affiliation:
University of Zurich (Switzerland)
*
*Correspondence concerning this article should be addressed to Carel van Schaik. University of Zurich – Anrthropology. Winterthurerstrasse, 190. CH-8125. Zurich (Switzerland). Phone: +41–446355411. E-mail: [email protected]
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Abstract

Classical ethology and behavioral ecology did not pay much attention to learning. However, studies of social learning in nature reviewed here reveal the near-ubiquity of reliance on social information for skill acquisition by developing birds and mammals. This conclusion strengthens the plausibility of the cultural intelligence hypothesis for the evolution of intelligence, which assumes that selection on social learning abilities automatically improves individual learning ability. Thus, intelligent species will generally be cultural species. Direct tests of the cultural intelligence hypothesis require good estimates of the amount and kind of social learning taking place in nature in a broad variety of species. These estimates are lacking so far. Here, we start the process of developing a functional classification of social learning, in the form of the social learning spectrum, which should help to predict the mechanisms of social learning involved. Once validated, the categories can be used to estimate the cognitive demands of social learning in the wild.

Keywords

culturedomain-generalintelligencelearning
Type
Research Article
Information
The Spanish Journal of Psychology , Volume 19 , 2016 , E99
Copyright
Copyright © Universidad Complutense de Madrid and Colegio Oficial de Psicólogos de Madrid 2017 

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References

Allen, T., & Clarke, J. A. (2005). Social learning of food preferences by white-tailed ptarmigan chicks. Animal Behaviour, 70, 305–310. https://doi.org/10.1016/j.anbehav.2004.10.022 CrossRefGoogle Scholar
Alonso, J. A., & Alonso, J. C. (1993). Age-related differences in time budgets and parental care in wintering common cranes. The Auk, 110, 78–88.Google Scholar
Anderson, M. L., & Finlay, B. L. (2014). Allocating structure to function: The strong links between neuroplasticity and natural selection. Frontiers in Human Neuroscience, 7, 918. https://doi.org/10.3389/fnhum.2013.00918 CrossRefGoogle ScholarPubMed
Behrens, T. E. J., Hunt, L. T., Woolrich, M. W., & Rushworth, M. F. S. (2008). Associative learning of social value. Nature, 456, 245–249. https://doi.org/10.1038/nature07538 CrossRefGoogle ScholarPubMed
Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C., & Matsuzawa, T. (2003). Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. Animal Cognition, 6, 213–223. https://doi.org/10.1007/s10071-003-0183-x CrossRefGoogle ScholarPubMed
Burger, J., & Gochfeld, M. (1981). Age-related differences in piracy behaviour of four species of Gulls, Larus. Behaviour, 77, 242–266. https://doi.org/10.1163/156853981X00400 CrossRefGoogle Scholar
Burkart, J. M., Kupferberg, A., Glasauer, S., & van Schaik, C. P. (2012). Even simple forms of social learning rely on internation attribution in marmoset monkeys (Callithrix jacchus). Journal of Comparative Psychology 126, 129–138.CrossRefGoogle Scholar
Byrne, R. W. (1995). The thinking ape: Evolutionary origins of intelligence. Oxford, UK: University Press.CrossRefGoogle Scholar
Byrne, R. W., & Russon, A. E. (1998). Learning by imitation: A hierarchical approach. Behavioral and Brain Sciences, 21, 667–684. https://doi.org/10.1017/S0140525X98001745 CrossRefGoogle ScholarPubMed
Coelho, C. G., Falótico, T., Izar, P., Mannu, M., Resende, B. D., Siqueira, J. O., & Ottoni, E. B. (2015). Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.). Animal Cognition, 18, 911–919. https://doi.org/10.1007/s10071-015-0861-5 CrossRefGoogle ScholarPubMed
Custance, D. M., Whiten, A., & Fredman, T. (2002). Social learning and primate reintroduction. International Journal of Primatology, 23, 479–499.CrossRefGoogle Scholar
de Waal, F. B. M., & Johanowicz, D. L. (1993). Modification of reconciliation behavior through social experience: An experiment with two macaque species. Child Development, 64, 897–908. https://doi.org/10.2307/1131225 CrossRefGoogle ScholarPubMed
Deaner, R. O., Isler, K., Burkart, J., & van Schaik, C. (2007). Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behavior, Evolution, 70, 115–124. https://doi.org/10.1159/000102973 CrossRefGoogle Scholar
Deaner, R. O., van Schaik, C. P., & Johnson, V. (2006). Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology, 4, 149–196. https://doi.org/10.1177/147470490600400114 CrossRefGoogle Scholar
Estes, J. A., Riedman, M. L., Staedler, M. M., Tinker, M. T., & Lyon, B. E. (2003). Individual variation in prey selection by sea otters: Patterns, causes and implications. Journal of Animal Ecology, 72(1), 144–155. https://doi.org/10.1046/j.1365-2656.2003.00690.x CrossRefGoogle Scholar
Fabricius, E. (1991). Interspecific mate choice following cross-fostering in a mixed colony of greylag geese (Anser anser) and canada geese (Branta canadensis) - a study on development and persistence of species preferences. Ethology, 88, 287–296.CrossRefGoogle Scholar
Forss, S. I. F., Schuppli, C., Haiden, D., Zweifel, N., & van Schaik, C. P. (2015). Contrasting responses to novelty by wild and captive orangutans. American Journal of Primatology, 77, 1109–1121. https://doi.org/10.1002/ajp.22445 CrossRefGoogle ScholarPubMed
Galef, B. G. (2015). Laboratory studies of imitation/field studies of tradition: Towards a synthesis in animal social learning. Behavioural Processes, 112, 114–119. https://doi.org/10.1016/j.beproc.2014.07.008 CrossRefGoogle ScholarPubMed
Gamero, A., & Kappeler, P. M. (2015). Slow development of foraging skills and parental costs of family-living in a semi-precocial, non-cooperatively breeding bird. Behavioral Ecology and Sociobiology, 69, 1301–1309. https://doi.org/10.1007/s00265-015-1943-8 CrossRefGoogle Scholar
Geertz, C. (1973). The interpretation of cultures: Selected essays. New York, NY: Basic Books.Google Scholar
Gilmer, W. S., & McKinney, W. T. (2003). Early experience and depressive disorders: Human and non-human primate studies. Journal of Affective Disorders, 75, 97–113. https://doi.org/10.1016/S0165-0327(03)00046-6 CrossRefGoogle ScholarPubMed
Göth, A., & Evans, C. S. (2005). Life history and social learning: Megapode chicks fail to acquire feeding preferences from conspecifics. Journal of Comparative Psychology, 119, 381–386. https://doi.org/10.1037/0735-7036.119.4.381 CrossRefGoogle ScholarPubMed
Griesser, M., & Suzuki, T. N. (2016). Kinship modulates the attention of naive individuals to the mobbing behaviour of role models. Animal Behaviour, 112, 83–91. https://doi.org/10.1016/j.anbehav.2015.11.020 CrossRefGoogle Scholar
Guinet, C., & Bouvier, J. (1995). Development of intentional stranding hunting techniques in killer whale (Orcinus orca) calves at crozet archipelago. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 73(1), 27–33. https://doi.org/10.1139/z95-004 CrossRefGoogle Scholar
Heinsohn, R. G. (1987). Age-dependent vigilance in winter aggregations of cooperatively breeding white-winged choughs (Corcorax melanorhamphos). Behavioral Ecology and Sociobiology, 20, 303–306. https://doi.org/10.1007/BF00292183 CrossRefGoogle Scholar
Heyes, C. (2012). What’s social about social learning? Journal of Comparative Psychology, 126, 193–202. https://doi.org/10.1037/a0025180 CrossRefGoogle ScholarPubMed
Hoppitt, W., & Laland, K. N. (2013). Social learning: An introduction to mechanisms, methods, and models. Princeton, NJ: Princeton University Press.Google Scholar
Holzhaider, J. C., Hunt, G. R., & Gray, R. D. (2010). The development of pandanus tool manufacture in wild New Caledonian crows. Behaviour, 147, 553–586. https://doi.org/10.1163/000579510X12629536366284 Google Scholar
Ingolfsson, A., & Estrella, B. T. (1978). The development of shell-cracking behavior in herring gulls. The Auk, 95, 577–579.CrossRefGoogle Scholar
Jaeggi, A. V., Dunkel, L. P., van Noordwijk, M. A., Wich, S. A., Sura, A. A. L., & van Schaik, C. P. (2010). Social learning of diet and foraging skills by wild immature Bornean orangutans: Implications for culture. American Journal of Primatology, 72, 62–71. https://doi.org/10.1002/ajp.20752 CrossRefGoogle ScholarPubMed
Jaeggi, A. V., van Noordwijk, M. A., & van Schaik, C. P. (2008). Begging for information: Mother-offspring food sharing among wild Bornean orangutans. American Journal of Primatology, 70, 533–541. https://doi.org/10.1002/ajp.20525 CrossRefGoogle ScholarPubMed
Kacelnik, A. (2012). Putting mechanisms into behavioral ecology. In Hammerstein, P. & Stevens, J. R. (Eds.), Evolution and the mechanisms of Decision Making (pp. 21–38). Cambridge, MA: MIT Press.CrossRefGoogle Scholar
Kendal, R. L., Galef, B. G., & van Schaik, C. P. (2010). Social learning research outside the laboratory: How and why? Learning & Behavior, 38, 187–194. https://doi.org/10.3758/LB.38.3.187 CrossRefGoogle ScholarPubMed
Kitchener, A. C. (1999). Watch with mother: A review of social learning in the Felidae. Symposia of the Zoological Society of London, 72, 236–258.Google Scholar
Kitowski, I. (2009). Social learning of hunting skills in juvenile marsh harriers Circus Aeruginosus . Journal of Ethology, 27, 327–332. https://doi.org/10.1007/s10164-008-0123-y CrossRefGoogle Scholar
Krakauer, E. B. (2005). Development of Aye-Aye (Daubentonia madagascariensis) foraging skills: Independent exploration and social learning. (Published PhD Dissertation). Duke University, Durham NC.Google Scholar
Krebs, J. R., & Davies, N. B. (1978). Behavioural Ecology. Oxford, UK: Blackwell Scientific Publications.Google Scholar
Krützen, M., Mann, J., Heithaus, M. R., Connor, R. C., Bejder, L., & Sherwin, W. B. (2005). Cultural transmission of tool use in bottlenose dolphins. Proceedings National Academy of Sciences USA, 102, 8939–8943. https://doi.org/10.1073/pnas.0500232102 CrossRefGoogle ScholarPubMed
Kullberg, C., & Lind, J. (2002). An experimental study of predator recognition in great tit fledglings. Ethology, 108, 429–441. https://doi.org/10.1046/j.1439-0310.2002.00786.x CrossRefGoogle Scholar
Lefebvre, L. (2011). Taxonomic counts of cognition in the wild. Biology Letters 7, 631–633. https://doi.org/10.1098/rsbl.2010.0556 CrossRefGoogle ScholarPubMed
Lefebvre, L., & Bolhuis, J. J. (2003). Positive and negative correlates of feeding innovations in birds: Evidence for limited modularity. In Reader, S. M. & Laland, K. N. (Eds.), Animal Innovation (pp. 39–61). New York, NY: Oxford University Press.CrossRefGoogle Scholar
Lefebvre, L., Reader, S. M., & Sol, D. (2004). Brains, innovations and evolution in birds and primates. Brain, Behavior, Evolution, 63, 233–246. https://doi.org/10.1159/000076784 CrossRefGoogle ScholarPubMed
Lehmann, L., Wakano, J. Y., & Aoki, K. (2013). On optimal learning schedules and marginal value of cumulative cultural evolution. Evolution, 67, 1435–1445. https://doi.org/10.1111/evo.12040 Google ScholarPubMed
Lonsdorf, E. V. (2005). Sex differences in the development of termite-fishing skills in the wild chimpanzees, Pan troglodytes schweinfurthii, of Gombe National Park, Tanzania. Animal Behaviour, 70, 673–683. https://doi.org/10.1016/j.anbehav.2004.12.014 CrossRefGoogle Scholar
Lorenz, K. Z. (1981). The Foundations of Ethology. New York, NY: Touchstone books (Simon and Schuster).CrossRefGoogle Scholar
MacLean, A. A. E. (1986). Age-specific foraging ability and the evolution of deferred breeding in three species of gulls. Wilson Bulletin, 98, 267–279.Google Scholar
Mann, J., Sargeant, B. L., & Minor, M. (2007). Calf inspections of fish catches in bottlenose dolphins (Tursiops sp.): Opportunities for oblique social learning? Marine Mammal Science, 23(1), 197–202. https://doi.org/10.1111/j.1748-7692.2006.00087.x CrossRefGoogle Scholar
Mann, J., & Sargent, B. (2003). Like mother, like calf: The ontogeny of foraging traditions in wild Indian Ocean bottlenose dolphins (Tursiops sp.). In Fragaszy, D. & Perry, S. (Eds.), The biology of traditions: Models and evidence (pp. 236–266). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Matzel, L. D., Wass, C., & Kolata, S. (2011). Individual differences in animal intelligence: Learning, reasoning, selective attention and inter-species conservation of a cognitive trait. International Journal of Comparative Psychology, 24, 36–59.CrossRefGoogle Scholar
Mazur, R., & Seher, V. (2008). Socially learned foraging behaviour in wild black bears, Ursus americanus. Animal Behaviour, 75, 1503–1508. https://doi.org/10.1016/j.anbehav.2007.10.027 CrossRefGoogle Scholar
McDonald, D. L., & Forslund, L. G. (1978). Development of social preferences in voles Microtus montanus and Microtus canicaudus - effects of cross-fostering. Behavioral Biology, 22, 497–508. https://doi.org/10.1016/s0091-6773(78)92637-8 CrossRefGoogle ScholarPubMed
McGuire, B. (1988). Effects of cross-fostering on parental behavior of meadow voles (Microtus pennsylvanicus). Journal of Mammalogy, 69, 332–341. https://doi.org/10.2307/1381383 CrossRefGoogle Scholar
Norton-Griffiths, M. N. (1969). The organization, control and development of the feeding behavior of the oystercatcher, Haematropus ostralegus, on the edible mussel. Mytilus edulis. Behaviour, 34, 55–114.CrossRefGoogle Scholar
O’Mara, M. T., & Hickey, C. M. (2012). Social influences on the development of ringtailed lemur feeding ecology. Animal Behaviour, 84, 1547–1555. https://doi.org/10.1016/j.anbehav.2012.09.032 CrossRefGoogle Scholar
Ottoni, E. B., de Resende, B. D., & Izar, P. (2005). Watching the best nutcrackers: What capuchin monkeys (Cebus apella) know about others’ tool-using skills. Animal Cognition, 8, 215–219. https://doi.org/10.1007/s10071-004-0245-8 CrossRefGoogle ScholarPubMed
Rapaport, L. G., & Brown, G. R. (2008). Social influences on foraging behavior in young nonhuman primates: Learning what, where, and how to eat. Evolutionary Anthropology, 17, 189–201. https://doi.org/10.1002/evan.20180 CrossRefGoogle Scholar
Reader, S. M., Hager, Y., & Laland, K. N. (2011). The evolution of primate general and cultural intelligence. Philosophical Transactions Royal Society B, 366, 1017–1027. https://doi.org/10.1098/rstb.2010.0342 CrossRefGoogle ScholarPubMed
Reader, S. M., & Laland, K. N. (2002). Social intelligence, innovation, and enhanced brain size in primates. Proceedings of the National Academy of Sciences, 99, 4436–4441. https://doi.org/10.1073/pnas.062041299 CrossRefGoogle ScholarPubMed
Richardson, H., & Verbeek, N. A. (1987). Diet selection by yearling northwestern crows (Corvus caurinus) feeding on littleneck clams (Venerupis japonica). The Auk, 104, 263–269.CrossRefGoogle Scholar
Rowley, I., & Chapman, G. (1986). Cross-fostering, imprinting and learning in two sympatric species of cockatoo. Behaviour, 96, 1–16. https://doi.org/10.1163/156853986X00180 Google Scholar
Schuppli, C., Isler, K., & van Schaik, C. P. (2012). How to explain the unusually late age at skill competence among humans. Journal of Human Evolution, 63, 843–850. https://doi.org/10.1016/j.jhevol.2012.08.009 CrossRefGoogle ScholarPubMed
Schuppli, C., Meulman, E. J. M., Forss, S. I. F., Aprilinayati, F., van Noordwijk, M. A., & van Schaik, C. P. (2016). Observational social learning and socially induced practice of routine skills in wild immature orang-utans. Animal Behaviour, 119, 87–98. https://doi.org/10.1016/j.anbehav.2016.06.014 CrossRefGoogle Scholar
Schuppli, C., Zweifel, N., Forss, S. I. F., van Noordwijk, M. A., & van Schaik, C. P. (2016). Development of feeding skills in relation to life history in two populations of wild orangutans. (Manuscript in preparation)Google Scholar
Shettleworth, S. J. (2010). Cognition, evolution, and behavior (2 nd Ed.). New York, NY: Oxford University Press.Google Scholar
Slagsvold, T., & Wiebe, K. L. (2007). Learning the ecological niche. Proceedings Royal Society B, 274, 19–23. https://doi.org/10.1098/rspb.2006.3663 CrossRefGoogle ScholarPubMed
Slagsvold, T., & Wiebe, K. L. (2011). Social learning in birds and its role in shaping the foraging niche. Philosophical Transactions of the Royal Society of London, 366, 969–977. https://doi.org/10.1098/rstb.2010.0343 CrossRefGoogle ScholarPubMed
Smith, S. M. (1973). A study of prey-attack behaviour in young loggerhead shrikes. Lanius ludovicianus L. Behaviour, 44(1), 113–140. https://doi.org/10.1163/156853973X00355 CrossRefGoogle Scholar
Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P., & Lefebvre, L. (2005). Big brains, enhanced cognition, and response of birds to novel environments. Proceedings National Academy of Sciences, 102, 5460–5465. https://doi.org/10.1073/pnas.0408145102 CrossRefGoogle ScholarPubMed
Subiaul, F. (2007). The imitation faculty in monkeys: Evaluating its features, distribution and evolution. Journal of Anthropological Sciences, 85, 35–62.Google Scholar
Taggart, D. A., Schultz, D. J., Fletcher, T. P., Friend, J. A., Smith, I. G., Breed, W. G., & Temple-Smith, P. D. (2010). Cross-fostering and short-term pouch young isolation in macropodoid marsupials: Implications for conservation and species management. In Coulson, G. & Eldridge, M. (Eds.), Macropods: The biology of Kangaroos, Wallabies and Rat-Kangaroos (pp. 263–278). Collingwood, Canada: CSIRO Publishing.Google Scholar
Tebbich, S., Griffin, A. S., Peschl, M. F., & Sterelny, K. (2016). From mechanisms to function: An integrated framework of animal innovation. Philosophical Transactions of the Royal Society B, 371, 20150195. https://doi.org/10.1098/rstb.2015.0195 CrossRefGoogle ScholarPubMed
Thornton, A., & Raihani, N. J. (2008). The evolution of teaching. Animal Behaviour, 75, 1823–1836. https://doi.org/10.1016/j.anbehav.2007.12.014 CrossRefGoogle Scholar
Timmermans, S., Lefebvre, L., Boire, D., & Basu, P. (2000). Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behavior and Evolution, 56, 196–203. https://doi.org/10.1159/000047204 CrossRefGoogle ScholarPubMed
Tinbergen, N. (1951). The Study of Instinct. Oxford, NY: Oxford University Press.Google Scholar
Tomasello, M. (1999). The cultural origins of human cognition. Cambridge MA: Harvard University Press.Google Scholar
van Schaik, C. P. (2006). Why are some animals so smart? Scientific American, 294, 64–71. https://doi.org/10.1038/scientificamerican0406-64 CrossRefGoogle ScholarPubMed
van Schaik, C. P., Burkart, J., Damerius, L., Forss, S. I. F., Koops, K., van Noordwijk, M. A., & Schuppli, C. (2016). The reluctant innovator: Orangutans and the phylogeny of creativity. Philosophical Transactions of the Royal Society B, 371, 1690. https://doi.org/10.1098/rstb.2015.0183 CrossRefGoogle ScholarPubMed
van Schaik, C. P., & Burkart, J. M. (2011). Social learning and evolution: The cultural intelligence hypothesis. Philosophical Transactions of the Royal Society B, 366, 1008–1016. https://doi.org/10.1098/rstb.2010.0304 CrossRefGoogle ScholarPubMed
van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., … Merrill, M. Y. (2003). Orangutan cultures and the evolution of material culture. Science, 299, 102–105. https://doi.org/10.1126/science.1078004 CrossRefGoogle ScholarPubMed
van Schaik, C. P., Isler, K., & Burkart, J. M. (2012). Explaining brain size variation: From social to cultural brain. Trends in Cognitive Sciences, 16, 277–284. https://doi.org/10.1016/j.tics.2012.04.004 CrossRefGoogle ScholarPubMed
Verzijden, M. N., & ten Cate, C. (2007). Early learning influences species assortative mating preferences in Lake Victoria cichlid fish. Biology Letters, 3, 134–136. https://doi.org/10.1098/rsbl.2006.0601 CrossRefGoogle ScholarPubMed
Videan, E. N. (2006). Bed-building in captive chimpanzees (Pan troglodytes): The importance of early rearing. American Journal of Primatology, 68, 745–751. https://doi.org/10.1002/ajp.20265 CrossRefGoogle ScholarPubMed
Vygotsky, L. (1978). Interaction between learning and development. Readings on the Development of Children, 23, 34–41.Google Scholar
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York, NY: Oxford University Press.CrossRefGoogle Scholar
Whiten, A. (2015). Experimental studies illuminate the cultural transmission of percussive technologies in Homo and Pan. Philosophical Transactions of the Royal Society B, 370, 1682.CrossRefGoogle ScholarPubMed
Whiten, A., Horner, V., Litchfield, C. A., & Marshall-Pescini, S. (2004). How do apes ape? Animal Learning & Behavior, 32, 36–52. https://doi.org/10.3758/BF03196005 CrossRefGoogle ScholarPubMed
Whiten, A., & van Schaik, C. P. (2007). The evolution of animal “cultures” and social intelligence. Philosophical transactions of the Royal society B, 362, 603–620. https://doi.org/10.1098/rstb.2006.1998 CrossRefGoogle ScholarPubMed
Wilkinson, A., Kuenstner, K., Mueller, J., & Huber, L. (2010). Social learning in a non-social reptile (Geochelone carbonaria). Biology Letters, 6, 614–616. https://doi.org/10.1098/rsbl.2010.0092 CrossRefGoogle Scholar
Yoerg, S. I. (1998). Foraging behavior predicts age at independence in juvenile Eurasian dippers (Cinclus cinclus). Behavioral Ecology, 9, 471–477. https://doi.org/10.1093/beheco/9.5.471 CrossRefGoogle Scholar