Abstract
New Caledonian (NC) crows are the most sophisticated tool manufacturers other than humans. The diversification and geographical distribution of their three Pandanus tool designs that differ in complexity, as well as the lack of ecological correlates, suggest that cumulative technological change has taken place. To investigate the possibility that high-fidelity social transmission mediated this putative ratchet-like process, we studied the ontogeny of Pandanus tool manufacture and social organization in free-living NC crows. We found that juvenile crows took more than 1 year to reach adult proficiency in their Pandanus tool skills. Although trial-and-error learning is clearly important, juveniles have ample opportunity to learn about Pandanus tool manufacture by both observing their parents and interacting with artifactual material. The crows’ social system seems likely to promote the faithful social transmission of local tool designs by both favoring the vertical transmission of tool information and minimizing horizontal transmission. We suggest that NC crows develop their Pandanus tool skills in a highly scaffolded learning environment that facilitates the cumulative technological evolution of tool designs.
Article PDF
Similar content being viewed by others
References
Allison, P. D. (1992). Cultural relatedness under oblique and horizontal transmission rules. Ethology & Sociobiology, 13, 153–169.
Avital, E., & Jablonka, E. (2000). Animal traditions: Behavioural inheritance in evolution. Cambridge: Cambridge University Press.
Baker, M. C., & Cunningham, M. A. (1985). The biology of bird-song dialects. Behavioral & Brain Sciences, 8, 85–133.
Balda, R. P., & Bateman, G. C. (1971). Flocking and annual cycle of the piñon jay, Gymnorhinus cyanocephalus. Condor, 73, 287–302.
Bird, C. D., & Emery, N. J. (2009). Insightful problem solving and creative tool modification by captive nontool-using rooks. Proceedings of the National Academy of Sciences, 106, 10370–10375.
Bird, C. D., & Emery, N. J. (2010). Rooks perceive support relations similar to six-month-old babies. Proceedings of the Royal Society B, 277, 147–151.
Biro, D., Sousa, C., & Matsuzawa, T. (2006). Ontogeny and cultural propagation of tool use by wild chimpanzees at Bossou, Guinea: Case studies in nut cracking and leaf folding. In T. Matsuzawa, M. Tomonaga, & M. Tanaka (Eds.), Cognitive development in chimpanzees (pp. 476–508). Tokyo: Springer.
Bluff, L. A., Troscianko, J., Weir, A. A. S., Kacelnik, A., & Rutz, C. (2010). Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites. Proceedings of the Royal Society B, 277, 1377–1385.
Boesch, C., Head, J., & Robbins, M. M. (2009). Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon. Journal of Human Evolution, 56, 560–569.
Boserup, E. (1981). Population and technological change: A study of long-term trends. Chicago: University of Chicago Press.
Box, H. O. (1984). Primate behaviour and social ecology. London: Chapman & Hall.
Boyd, R., & Richerson, P. J. (1985). Culture and the evolutionary process. Chicago: University of Chicago Press.
Boyd, R., & Richerson, P. J. (1996). Why culture is common, but cultural evolution is rare. Proceedings of the British Academy, 88, 77–93.
Bugnyar, T. (2008). Animal cognition: Rooks team up to solve a problem. Current Biology, 18, R530-R532.
Caldwell, C. A., & Whiten, A. (2003). Scrounging facilitates social learning in common marmosets, Callithrix jacchus. Animal Behaviour, 65, 1085–1092.
Call, J., Carpenter, M., & Tomasello, M. (2005). Copying results and copying actions in the process of social learning: Chimpanzees (Pan troglodytes) and human children (Homo sapiens). Animal Cognition, 8, 151–163.
Call, J., & Tomasello, M. (1994). The social learning of tool use by orangutans (Pongo pygmaeus). Human Evolution, 9, 297–313.
Catchpole, C. K., & Slater, P. J. B. (1995). Bird song: Biological themes and variations. Cambridge: Cambridge University Press.
Cavalli-Sforza, L. L., & Feldman, M. W. (1981). Cultural transmission and evolution: A quantitative approach. Princeton, NJ: Princeton University Press.
Chappell, J., & Kacelnik, A. (2002). Tool selectivity in a non-primate, the New Caledonian crow (Corvus moneduloides). Animal Cognition, 5, 71–78.
Chappell, J., & Kacelnik, A. (2004). Selection of tool diameter by New Caledonian crows (Corvus moneduloides). Animal Cognition, 7, 121–127.
Claidière, N., & Sperber, D. (2010). Imitation explains the propagation, not the stability of animal culture. Proceedings of the Royal Society B, 277, 651–659.
Clayton, N. S., & Emery, N. J. (2007). The social life of corvids. Current Biology, 17, R652-R656.
Cnotka, J., Güntürkün, O., Rehkämper, G., Gray, R. D., & Hunt, G. R. (2008). Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides). Neuroscience Letters, 433, 241–245.
Connolly, K., & Dalgleish, M. (1989). The emergence of a tool-using skill in infancy. Developmental Psychology, 25, 894–912.
Coussi-Korbel, S., & Fragaszy, D. M. (1995). On the relation between social dynamics and social learning. Animal Behaviour, 50, 1441–1453.
de Resende, B. D., Ottoni, E. B., & Fragaszy, D. M. (2008). Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): A perception-action perspective. Developmental Science, 11, 828–840.
de Waal, F. B. M. (1989). Food sharing and reciprocal obligations among chimpanzees. Journal of Human Evolution, 18, 433–459.
Donald, M. (1991). Origins of the modern mind: Three stages in the evolution of culture and cognition. Cambridge, MA: Harvard University Press.
Doupe, A. J., & Konishi, M. (1991). Song-selective auditory circuits in the vocal control system of the zebra finch. Proceedings of the National Academy of Sciences, 88, 11339–11343.
Emery, N. J. (2004). Are corvids “feathered apes”?: Cognitive evolution in crows, jays, rooks and jackdaws. In S. Watanabe (Ed.), Comparative analysis of mind (pp. 181–213). Tokyo: Keio University Press.
Emery, N. J. (2006). Cognitive ornithology: The evolution of avian intelligence. Philosophical Transactions of the Royal Society B, 361, 23–43.
Emery, N. J., & Clayton, N. S. (2004). The mentality of crows: Convergent evolution of intelligence in corvids and apes. Science, 306, 1903–1907.
Emery, N. J., & Clayton, N. S. (2009). Tool use and physical cognition in birds and mammals. Current Opinion in Neurobiology, 19, 27–33.
Emery, N. J., Seed, A. M., von Bayern, A. M. P., & Clayton, N. S. (2007). Cognitive adaptations of social bonding in birds. Philosophical Transactions of the Royal Society B, 362, 489–505.
Findlay, C. S., Hansell, R. I. C., & Lumsden, C. J. (1989). Behavioral evolution and biocultural games: Oblique and horizontal cultural transmission. Journal of Theoretical Biology, 137, 245–269.
Fragaszy, D. M., & Visalberghi, E. (1996). Social learning in monkeys: Primate “primacy” reconsidered. In C. M. Heyes & B. G. Galef, Jr. (Eds.), Social learning in animals: The roots of culture (pp. 65–84). San Diego: Academic Press.
Galef, B. G., Jr. (1988). Imitation in animals: History, definition, and interpretation of data from the psychological laboratory. In T. R. Zentall & B. G. Galef, Jr. (Eds.), Social learning: Psychological and biological perspectives (pp. 3–28). Hillsdale, NJ: Erlbaum.
Giraldeau, L.-A., & Lefebvre, L. (1987). Scrounging prevents cultural transmission of food-finding behaviour in pigeons. Animal Behaviour, 35, 387–394.
Hernandez-Aguilar, R. A., Moore, J., & Pickering, T. R. (2007). Savanna chimpanzees use tools to harvest the underground storage organs of plants. Proceedings of the National Academy of Sciences, 104, 19210–19213.
Heyes, C. M. (1993). Imitation, culture and cognition. Animal Behaviour, 46, 999–1010.
Heyes, C. M. (1994). Social learning in animals: Categories and mechanisms. Biological Reviews, 69, 207–231.
Hirata, S., & Celli, M. L. (2003). Role of mothers in the acquisition of tool-use behaviours by captive infant chimpanzees. Animal Cognition, 6, 235–244.
Hirata, S., & Morimura, N. (2000). Naive chimpanzees’ (Pan troglodytes) observation of experienced conspecifics in a tool-using task. Journal of Comparative Psychology, 114, 291–296.
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.
Holzhaider, J. C., Sibley, M. D., Taylor, A. H., Singh, P. J., Gray, R. D., & Hunt, G. R. (in press). The social structure of New Caledonian crows. Animal Behaviour.
Horner, V., & Whiten, A. (2005). Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Animal Cognition, 8, 164–181.
Humle, T. (2006). Ant dipping in chimpanzees: An example of how microecological variables, tool use, and culture reflect the cognitive abilities of chimpanzees. In T. Matsuzawa, M. Tomonaga, & M. Tanaka (Eds.), Cognitive development in chimpanzees (pp. 452–475). Tokyo: Springer.
Hunt, G. R. (1996). Manufacture and use of hook-tools by New Caledonian crows. Nature, 379, 249–251.
Hunt, G. R. (2000a). Human-like, population-level specialization in the manufacture of Pandanus tools by New Caledonian crows Corvus moneduloides. Proceedings of the Royal Society B, 267, 403–413.
Hunt, G. R. (2000b). Tool use by the New Caledonian crow Corvus moneduloides to obtain Cerambycidae from dead wood. Emu, 100, 109–114.
Hunt, G. R., & Gray, R. D. (2002). Species-wide manufacture of stick-type tools by New Caledonian Crows. Emu, 102, 349–353.
Hunt, G. R., & Gray, R. D. (2003). Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proceedings of the Royal Society B, 270, 867–874.
Hunt, G. R., & Gray, R. D. (2004a). The crafting of hook tools by wild New Caledonian crows. Proceedings of the Royal Society B, 271, 88–90.
Hunt, G. R., & Gray, R. D. (2004b). Direct observations of Pandanus tool manufacture and use by a New Caledonian crow (Corvus moneduloides). Animal Cognition, 7, 114–120.
Hunt, G. R., & Gray, R. D. (2007). Parallel tool industries in New Caledonian crows. Biology Letters, 3, 173–175.
Hunt, G. R., Lambert, C., & Gray, R. D. (2007). Cognitive requirements for tool use by New Caledonian crows. New Zealand Journal of Zoology, 34, 1–7.
Inoue-Nakamura, N., & Matsuzawa, T. (1997). Development of stone tool use by wild chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 111, 159–173.
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.
Jerison, H. J. (1973). Evolution of the brain and intelligence. New York: Academic Press.
Kawai, M. (1965). Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet. Primates, 6, 1–30.
Kendal, R. L., Custance, D. M., Kendal, J. R., Vale, G., Stoinski, T. S., Rakotomalala, N. L., & Rasamimanana, H. (2010). Evidence for social learning in wild lemurs (Lemur catta). Learning & Behavior, 38, 220–234.
Kendal, R. L., Kendal, J. R., Hoppitt, W., & Laland, K. N. (2009). Identifying social learning in animal populations: A new “option-bias” method. PLoS ONE, 4, e6541. doi:10.1371/journal.pone.0006541
Kenward, B., Rutz, C., Weir, A. A. S., Chappell, J., & Kacelnik, A. (2004). Morphology and sexual dimorphism of the New Caledonian Crow Corvus moneduloides, with notes on its behaviour and ecology. Ibis, 146, 652–660.
Kenward, B., Rutz, C., Weir, A. A. S., & Kacelnik, A. (2006). Development of tool use in New Caledonian crows: Inherited action patterns and social influences. Animal Behaviour, 72, 1329–1343.
Kenward, B., Weir, A. A. S., Rutz, C., & Kacelnik, A. (2005). Behavioural ecology: Tool manufacture by naive juvenile crows. Nature, 433, 121.
Konishi, M. (1985). Birdsong: From behavior to neuron. Annual Review of Neuroscience, 8, 125–170.
Laland, K. N., & Hoppitt, W. (2003). Do animals have culture? Evolutionary Anthropology: Issues, News, & Reviews, 12, 150–159.
Laland, K. N., Odling-Smee, J., & Feldman, M. W. (2000). Niche construction, biological evolution, and cultural change. Behavioral & Brain Sciences, 23, 131–146.
Lind, J., & Lindenfors, P. (2010). The number of cultural traits is correlated with female group size but not with male group size in chimpanzee communities. PLoS ONE, 5, e9241. doi:10.1371/journal.pone.0009241
Lockman, J. J. (2000). A perception-action perspective on tool use development. Child Development, 71, 137–144.
Marler, P., & Tamura, M. (1964). Culturally transmitted patterns of vocal behavior in sparrows. Science, 146, 1483–1486.
Marzluff, J. M., & Balda, R. P. (1989). Causes and consequences of female-biased dispersal in a flock-living bird, the Pinyon Jay. Ecology, 70, 316–328.
Matsuzawa, T. (1994). Field experiments on use of stone tool by chimpanzees in the wild. In R. W. Wrangham, W. C. McGrew, F. B. M. de Waal, & P. Heltne (Eds.), Chimpanzee cultures (pp. 351–370). Cambridge, MA: Harvard University Press.
Matsuzawa, T., Biro, D., Humle, T., Inoue-Nakamura, N., Tonooka, R., & Yamakoshi, G. (2001). Emergence of culture in wild chimpanzees: Education by master-apprenticeship. In T. Matsuzawa (Ed.), Primate origins of human cognition and behavior (pp. 557–574). Tokyo: Springer.
McGrew, W. C. (1992). Chimpanzee material culture: Implications for human evolution. Cambridge: Cambridge University Press.
Mehlhorn, J., Hunt, G. R., Gray, R. D., Rehkämper, G., & Güntürkün, O. (2010). Tool-making New Caledonian crows have large associative brain areas. Brain, Behavior & Evolution, 75, 63–70.
Midford, P. E., Hailman, J. P., & Woolfenden, G. E. (2000). Social learning of a novel foraging patch in families of free-living Florida scrub-jays. Animal Behaviour, 59, 1199–1207.
Mundinger, P. C. (1980). Animal cultures and a general theory of cultural evolution. Ethology & Sociobiology, 1, 183–223.
Myowa-Yamakoshi, M., & Matsuzawa, T. (1999). Factors influencing imitation of manipulatory actions in chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 113, 128–136.
Nagell, K., Olguin, R. S., & Tomasello, M. (1993). Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). Journal of Comparative Psychology, 107, 174–186.
Nishida, T., & Hiraiwa, M. (1982). Natural history of a tool-using behavior by wild chimpanzees in feeding upon wood-boring ants. Journal of Human Evolution, 11, 73–99.
Noad, M. J., Cato, D. H., Bryden, M. M., Jenner, M.-N., & Jenner, K. C. S. (2000). Cultural revolution in whale songs. Nature, 408, 537.
Nottebohm, F. (1984). Birdsong as a model in which to study brain processes related to learning. Condor, 86, 227–236.
Odling-Smee, F. J., Laland, K. N., & Feldman, M. W. (2003). Niche construction: The neglected process in evolution. Princeton, NJ: Princeton University Press.
Ottoni, E. B., & Izar, P. (2008). Capuchin monkey tool use: Overview and implications. Evolutionary Anthropology: Issues, News, & Reviews, 17, 171–178.
Perry, S., Panger, M., Rose, L. M., Baker, M., Gros-Louis, J., Jack, K., et al. (2003). Traditions in wild white-faced capuchin monkeys. In D. M. Fragaszy & S. Perry (Eds.), The biology of traditions: Models and evidence (pp. 391–425). Cambridge: Cambridge University Press.
Reader, S. M., & Biro, D. (2010). Experimental identification of social learning in wild animals. Learning & Behavior, 38, 265–283.
Rehkämper, G., Frahm, H. D., & Zilles, K. (1991). Quantitative development of brain and brain structures in birds (galliformes and passeriformes) compared to that in mammals (insectivores and primates). Brain, Behavior & Evolution, 37, 125–143.
Reiner, A., Perkel, D. J., Bruce, L. L., Bulter, A. B., Csillag, A., Kuenzel, W., et al. (2004). Revised nomenclature for avian telencephalon and some related brainstem nuclei. Journal of Comparative Neurology, 473, 377–414.
Reisman, K. (2007). Is culture inherited through social learning? Biological Theory, 2, 300–306.
Rendell, L., & Whitehead, H. (2001). Culture in whales and dolphins. Behavioral & Brain Sciences, 24, 309–382.
Rutz, C., Bluff, L. A., Weir, A. A. S., & Kacelnik, A. (2007). Video cameras on wild birds. Science, 318, 765.
Sanz, C., Call, J., & Morgan, D. (2009). Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes). Biology Letters, 5, 293–296.
Sanz, C., Morgan, D., & Gulick, S. (2004). New insights into chimpanzees, tools, and termites from the Congo basin. American Naturalist, 164, 567–581.
Seed, A., Emery, N., & Clayton, N. (2009). Intelligence in corvids and apes: A case of convergent evolution? Ethology, 115, 401–420.
Sterelny, K. (2006). The evolution and evolvability of culture. Mind & Language, 21, 137–165.
Stevens, J. R., & Gilby, I. C. (2004). A conceptual framework for nonkin food sharing: Timing and currency of benefits. Animal Behaviour, 67, 603–614.
Taylor, A. H., Hunt, G. R., Holzhaider, J. C., & Gray, R. D. (2007). Spontaneous metatool use by New Caledonian crows. Current Biology, 17, 1504–1507.
Taylor, A. H., Hunt, G. R., Medina, F. S., & Gray, R. D. (2009). Do New Caledonian crows solve physical problems through causal reasoning? Proceedings of the Royal Society B, 276, 247–254.
Taylor, A. H., Medina, F. S., Holzhaider, J. C., Hearne, L. J., Hunt, G. R., & Gray, R. D. (2010). An investigation into the cognition behind spontaneous string pulling in New Caledonian crows. PLoS ONE, 5, e9345.
Taylor, A. H., Roberts, R., Hunt, G. R., & Gray, R. D. (2009). Causal reasoning in New Caledonian crows: Ruling out spatial analogies and sampling error. Communicative & Integrative Biology, 2, 311–312.
Tebbich, S., Seed, A. M., Emery, N. J., & Clayton, N. S. (2007). Non-tool-using rooks, Corvus frugilegus, solve the trap-tube problem. Animal Cognition, 10, 225–231.
Tebbich, S., Taborsky, M., Fessl, B., & Blomqvist, D. (2001). Do woodpecker finches acquire tool-use by social learning? Proceedings of the Royal Society B, 268, 2189–2193.
Terkel, J. (1996). Cultural transmission of feeding behavior in the black rat (Rattus rattus). In C. M. Heyes & B. G. Galef, Jr. (Eds.), Social learning in animals: The roots of culture (pp. 17–47). San Diego: Academic Press.
Thouless, C. R., Fanshawe, J. H., & Bertram, B. C. R. (1989). Egyptian vultures Neophron percnopterus and ostrich Struthio camelus eggs: The origins of stone throwing behavior. Ibis, 131, 9–15.
Tomasello, M. (1996). Do apes ape? In C. M. Heyes & B. G. Galef, Jr. (Eds.), Social learning in animals: The roots of culture (pp. 319–346). London: Academic Press.
Tomasello, M. (1999). The human adaptation for culture. Annual Review of Anthropology, 28, 509–529.
Tomasello, M. (2005). Uniquely human cognition is a product of human culture. In S. C. Levinson & P. Jaisson (Eds.), Evolution and culture: A Fyssen Foundation symposium (pp. 203–218). Cambridge, MA: MIT Press.
Tomasello, M., Davis-Dasilva, M., Camak, L., & Bard, K. (1987). Observational learning of tool-use by young chimpanzees. Human Evolution, 2, 175–183.
Tomasello, M., Kruger, A. C., & Ratner, H. H. (1993). Cultural learning. Behavioral & Brain Sciences, 16, 495–552.
Tomasello, M., Savage-Rumbaugh, S., & Kruger, A. C. (1993). Imitative learning of actions on objects by children, chimpanzees, and enculturated chimpanzees. Child Development, 64, 1688–1705.
van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., et al. (2003). Orangutan cultures and the evolution of material culture. Science, 299, 102–105.
van Schaik, C. P., Deaner, R. O., & Merrill, M. Y. (1999). The conditions for tool use in primates: Implications for the evolution of material culture. Journal of Human Evolution, 36, 719–741.
von Bayern, A. M. P., de Kort, S. R., Clayton, N. S., & Emery, N. J. (2007). The role of food- and object-sharing in the development of social bonds in juvenile jackdaws (Corvus monedula). Behaviour, 144, 711–733.
Want, S. C., & Harris, P. L. (2001). Learning from other people’s mistakes: Causal understanding in learning to use a tool. Child Development, 72, 431–443.
Want, S. C., & Harris, P. L. (2002). How do children ape? Applying concepts from the study of non-human primates to the developmental study of “imitation” in children. Developmental Science, 5, 1–14.
Weir, A. A. S., Chappell, J., & Kacelnik, A. (2002). Shaping of hooks in New Caledonian crows. Science, 297, 981.
Weir, A. A. S., & Kacelnik, A. (2006). A New Caledonian crow (Corvus moneduloides) creatively re-designs tools by bending or unbending aluminium strips. Animal Cognition, 9, 317–334.
Whiten, A. (2005). The second inheritance system of chimpanzees and humans. Nature, 437, 52–55.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., et al. (1999). Cultures in chimpanzees. Nature, 399, 682–685.
Whiten, A., Horner, V., Litchfield, C. A., & Marshall-Pescini, S. (2004). How do apes ape? Learning & Behavior, 32, 36–52.
Whiten, A., McGuigan, N., Marshall-Pescini, S., & Hopper, L. M. (2009). Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Philosophical Transactions of the Royal Society B, 364, 2417–2428.
Wimpenny, J. H., Weir, A. A. S., Clayton, L., Rutz, C., & Kacelnik, A. (2009). Cognitive processes associated with sequential tool use in New Caledonian crows. PLoS ONE, 4, e6471.
Author information
Authors and Affiliations
Corresponding author
Additional information
We thank William Wadrobert for kindly allowing us to work on his family’s land in Wabao District, Maré, and the Province des Iles Loyauté for permission to work on Maré. Mick Sibley prepared DVD versions of the video footage. Noel Andrews, Lindsey Davidson, Roland Rehm, Robert Ross, Mick Sibley, and Alex Taylor assisted with data collection. We thank Katie Palmer for help with the coding of video footage, Puja Singh for help with the coding and processing of the sociality data, Vivian Ward for drawing Figure 3, and Roland Rehm for the production of Figure 5. Jeff Galef provided many helpful comments that improved the manuscript. This research was funded by a grant from the New Zealand Marsden Fund (awarded to R.D.G. and G.R.H.). The research reported in this article was approved by the University of Auckland Animal Ethics Committee (approvals R231 and R375) and complies with the laws of New Caledonia.
Rights and permissions
About this article
Cite this article
Holzhaider, J.C., Hunt, G.R. & Gray, R.D. Social learning in new Caledonian crows. Learning & Behavior 38, 206–219 (2010). https://doi.org/10.3758/LB.38.3.206
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/LB.38.3.206