Abstract
In human societies, cultural norms arise when behaviours are transmitted through social networks via high-fidelity social learning1. However, a paucity of experimental studies has meant that there is no comparable understanding of the process by which socially transmitted behaviours might spread and persist in animal populations2,3. Here we show experimental evidence of the establishment of foraging traditions in a wild bird population. We introduced alternative novel foraging techniques into replicated wild sub-populations of great tits (Parus major) and used automated tracking to map the diffusion, establishment and long-term persistence of the seeded innovations. Furthermore, we used social network analysis to examine the social factors that influenced diffusion dynamics. From only two trained birds in each sub-population, the information spread rapidly through social network ties, to reach an average of 75% of individuals, with a total of 414 knowledgeable individuals performing 57,909 solutions over all replicates. The sub-populations were heavily biased towards using the technique that was originally introduced, resulting in established local traditions that were stable over two generations, despite a high population turnover. Finally, we demonstrate a strong effect of social conformity, with individuals disproportionately adopting the most frequent local variant when first acquiring an innovation, and continuing to favour social information over personal information. Cultural conformity is thought to be a key factor in the evolution of complex culture in humans4,5,6,7. In providing the first experimental demonstration of conformity in a wild non-primate, and of cultural norms in foraging techniques in any wild animal, our results suggest a much broader taxonomic occurrence of such an apparently complex cultural behaviour.
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References
Rogers, E. M. Diffusion of Innovations 4th edn (Free Press, 1995)
Claidière, N., Messer, E. J. E., Hoppitt, W. & Whiten, A. Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr. Biol. 23, 1251–1255 (2013)
Cantor, M. & Whitehead, H. The interplay between social networks and culture: theoretically and among whales and dolphins. Phil. Trans. R. Soc. B 368, 20120340 (2013)
Rendell, L. et al. Cognitive culture: theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15, 68–76 (2011)
van de Waal, E., Borgeaud, C. & Whiten, A. Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485 (2013)
Whiten, A., Hinde, R. A., Laland, K. N. & Stringer, C. B. Culture evolves. Phil. Trans. R. Soc. B 366, 938–948 (2011)
Whiten, A., Horner, V. & de Waal, F. B. Conformity to cultural norms of tool use in chimpanzees. Nature 437, 737–740 (2005)
Laland, K. N. & Janik, V. M. The animal cultures debate. Trends Ecol. Evol. 21, 542–547 (2006)
Warner, R. R. Traditionality of mating-site preferences in a coral reef fish. Nature 335, 719–721 (1988)
Coussi-Korbel, S. & Fragaszy, D. M. On the relation between social dynamics and social learning. Anim. Behav. 50, 1441–1453 (1995)
Dean, L. G., Kendal, R. L., Schapiro, S. J., Thierry, B. & Laland, K. N. Identification of the social and cognitive processes underlying human cumulative culture. Science 335, 1114–1118 (2012)
Laland, K. Social learning strategies. Learn. Behav. 32, 4–14 (2004)
Galef, B. G. & Laland, K. N. Social learning in animals: empirical studies and theoretical models. Bioscience 55, 489–499 (2005)
Whiten, A. & Mesoudi, A. Establishing an experimental science of culture: animal social diffusion experiments. Phil. Trans. R. Soc. B 363, 3477–3488 (2008)
Galef, B. G. in Oxford Handbook of Comparative Cognition (eds Zentall, T. R. & Wasserman, E. ) Ch. 40, 803–818 (Oxford Univ. Press, 2012)
Fisher, J. B. & Hinde, R. A. The opening of milk bottles by birds. Br. Birds 42, 347–357 (1949)
Sherry, D. F. & Galef, B. G. Cultural transmission without imitation: milk bottle opening by birds. Anim. Behav. 32, 937–938 (1984)
Aplin, L. M., Sheldon, B. & Morand-Ferron, J. Milk-bottles revisited: social learning and individual variation in the blue tit (Cyanistes caeruleus). Anim. Behav. 85, 1225–1232 (2013)
Morand-Ferron, J., Cole, E. F., Rawles, J. E. C. & Quinn, J. L. Who are the innovators? A field experiment with 2 passerine species. Behav. Ecol. 22, 1241–1248 (2011)
Slagsvold, T. & Wiebe, K. L. Social learning in birds and its role in shaping a foraging niche. Phil. Trans. R. Soc. B 366, 969–977 (2011)
Aplin, L. M. et al. Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol. Lett. 16, 1365–1372 (2013)
Psorakis, I., Roberts, S. J., Rezek, I. & Sheldon, B. C. Inferring social network structure in ecological systems from spatio-temporal data streams. J. R. Soc. Interface 9, 3055–3066 (2012)
Allen, J., Weinrich, M. T., Hoppitt, W. & Rendell, L. Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science 340, 485–488 (2013)
Thornton, A. & Malapert, A. The rise and fall of an arbitrary tradition: an experiment with wild meerkats. Proc. R. Soc. B 276, 1269–1276 (2009)
Morgan, T. J. H. & Laland, K. The biological bases of conformity. Front. Neurosci. 6, 87 (2012)
van Leeuwen, E. J. C. & Haun, D. B. M. Conformity in nonhuman primates: fad or fact? Evol. Hum. Behav. 34, 1–7 (2013)
Bouwhuis, S., Choquet, R., Sheldon, B. C. & Verhulst, S. The forms and fitness cost of senescence: age-specific recapture, survival, reproduction, and reproductive value in a wild bird population. Am. Nat. 179, E15–E27 (2012)
Haun, D. B. M., Rekers, Y. & Tomasello, M. Majority-biased transmission in chimpanzees and human children, but not orangutans. Curr. Biol. 22, 727–731 (2012)
de Waal, F. B. Animal conformists. Science 340, 437–438 (2013)
van Schaik, C. P. Animal culture: chimpanzee conformity? Curr. Biol. 22, R402–R404 (2012)
Aplin, L. M., Farine, D. R., Morand-Ferron, J. & Sheldon, B. C. Social networks predict patch discovery in a wild population of songbirds. Proc. R. Soc. B 279, 4199–4205 (2012)
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, 2002)
Farine, D. R. Animal social network inference and permutations for ecologist in R using asnipe. Methods Ecol. Evol. 4, 1187–1194 (2013)
Franks, D. W., Ruxton, G. D. & James, R. Sampling animal association networks with the gambit of the group. Behav. Ecol. Sociobiol. 64, 493–503 (2010)
Whitehead, H. Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis (Univ. Chicago Press, 2008)
Bejder, L., Fletcher, D. & Brager, S. A method for testing association patterns of social animals. Anim. Behav. 56, 719–725 (1998)
Franz, M. & Nunn, C. L. Network-based diffusion analysis: a new method for detecting social learning. Proc. R. Soc. B 276, 1829–1836 (2009)
Hoppitt, W., Boogert, N. J. & Laland, K. N. Detecting social transmission in networks. J. Theor. Biol. 263, 544–555 (2010)
Acknowledgements
This project was supported by grants from the BBSRC (BB/L006081/1) and the ERC (AdG 250164) to B.C.S., who was also supported by a visiting professorship at Uppsala University. L.M.A. was also supported by an Australian Postgraduate Award; and A.T., by a BBSRC David Phillips Fellowship (BB/H021817/1). The EGI social networks group, S. Lang and K. McMahon provided assistance in the field, and M. Whitaker produced electronic components for the puzzle boxes.
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Contributions
The study was initially conceived by L.M.A., J.M.-F. and B.C.S., with input from D.R.F., A.C. and A.T. in designing the experiments. Infrastructure to support the work was conceived and developed by B.C.S. The experimental work was led by L.M.A.; and the analysis, by L.M.A. and D.R.F. The manuscript was drafted by L.M.A. and B.C.S., and important contributions were made by all of the other authors.
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Extended data figures and tables
Extended Data Figure 1 Wytham Woods, UK, (51° 46′ N, 01° 20′ W), showing the location of replicates and puzzle boxes.
The total area of Wytham Woods is 385 ha; the location and size of the separate woodland areas within the woods are labelled on the map. The green points indicate the puzzle-box locations for the three control replicates, C1, C2 and C3: Broad Oak, Bean Wood and Singing Way, respectively. The blue points indicate the puzzle-box locations for the two option A replicates, T1 and T2: Common Piece and Brogden’s Belt, respectively. The red points indicate the puzzle-box locations for the three option B replicates, T3, T4 and T5: Great Wood, Marley Plantation and Pasticks, respectively. (d) indicates the locations where trained demonstrators were caught from and released to.
Extended Data Figure 2 Social network data collection.
a, Schematic of a feeding station (shut), with sunflower-seed feeder, RFID antennae and data-logging hardware. The cage is to restrict access to small passerines only. b, Map of the study area showing the placement of 65 feeding stations. The stations are approximately 250 m apart and open simultaneously from dawn to dusk on Saturday and Sunday over winter. c, Grouping events were inferred from the temporal data stream gained from the feeding stations, with individuals assigned to grouping events in a bipartite network. d, Repeated co-occurrences were used to create social networks22.
Extended Data Figure 3 Social networks showing the diffusion of innovation.
The red nodes represent individuals that acquired the novel behaviour after 20 days of exposure. The black nodes represent naive individuals. The yellow nodes represent trained demonstrators. The networks are heavily thresholded to show only the links above the average edge strength for each replicate (T1–T5, 0.09, 0.05, 0.08, 0.07 and 0.07, respectively). a, Network for the T1 replicate (n = 123). b, Network for the T2 replicate (n = 137). c, Network for the T3 replicate (n = 154). d, Network for the T4 replicate (n = 95). e, Network for the T5 replicate (n = 110).
Extended Data Figure 4 Individual trajectories (option A or B) for each replicate.
Only individuals that performed both options are included, and individuals that moved between replicates are excluded. The lines are running proportions of the seeded option for each individual over its last ten visits. a, T1 (option A), n = 30. b, T2 (option A), n = 10. c, T3 (option B), n = 19. d, T4 (option B), n = 15. e, T5 (option B), n = 4.
Extended Data Figure 5 Food preference trials.
The birds were presented with a freely available mix of 40 mealworms, 40 peanut granules and 40 sunflower seeds for 1 h on 2 days over 1 week at 6 sites (3 sites for T2 and 3 sites for T4). The trials were conducted 2 weeks after the end of the main experiment, in March 2014. Food choice was identified from video camera footage, and the trial was halted when all of one prey item was taken. Only great tits were included, but the birds could not be individually identified. The birds clearly preferred the live mealworms to peanut granules or sunflower seeds.
Supplementary information
Supplementary Information
This file contains Supplementary Text and Supplementary Table 1. (PDF 164 kb)
Two ways of solving the puzzle-box
First shows great tit using option A, pushing the door to the left from the blue side. The bird extracts a reward and the puzzle-box automatically resets 1sec after its departure. Second shows great tit using option B, pushing the door to the right from the red side. Again the bird gains access to the feeder, and the puzzle-box resets back to the middle 1 sec after its departure. (MP4 27734 kb)
Birds solving the task in a sequence of solves and scrounges
Footage shows great tits interacting at the puzzle-box over a 1 min period at a busy site, with multiple birds either solving the puzzle-box, scrounging from others, or visually observing the solves of others. Up to two scrounges in the 1 sec after a solve are permitted, and are registered as such at the puzzle-box before it shuts. (MP4 14203 kb)
: Diffusion of experimentally introduced behaviour through the social network
Foraging social network for T3 replicate as an example. Nodes represent individuals; lines are edges indicating the strength of connection between individuals. Yellow nodes are trained demonstrators, and nodes turn red in the order in which they first performed the new behavior (whether option A/B). (MP4 8344 kb)
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Aplin, L., Farine, D., Morand-Ferron, J. et al. Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518, 538–541 (2015). https://doi.org/10.1038/nature13998
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DOI: https://doi.org/10.1038/nature13998
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