Social learning in birds and its role in shaping a foraging niche

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1567, 2011, Pages 969-977

  Slagsvold, Tore ^a   Wiebe, Karen L ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Cultural transmission; Ecological niche; Foraging conservatism; Habitat preferences; Speciation

Indexed keywords

ANTIPREDATOR DEFENSE; AVIFAUNA; BIOLOGY; CAPTIVE POPULATION; EUSOCIALITY; FEEDING GROUND; FOOD PROVISIONING; FORAGING BEHAVIOR; HABITAT SELECTION; IMITATION; LEARNING; LITERATURE REVIEW; MATE CHOICE; PARENT-OFFSPRING INTERACTION; PASSERINE; SONG; SPECIATION (BIOLOGY);

AVES; CYANISTES CAERULEUS; PARUS MAJOR; PASSERI; PASSERIFORMES;

AGE DISTRIBUTION; ANIMAL; ARTICLE; ECOSYSTEM; FEEDING BEHAVIOR; LEARNING; PHYSIOLOGY; SOCIAL BEHAVIOR; SONGBIRD;

AGE DISTRIBUTION; ANIMALS; ECOSYSTEM; FEEDING BEHAVIOR; LEARNING; PASSERIFORMES; SOCIAL BEHAVIOR;

EID: 79959498870     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0343     Document Type: Review

References (98)

1. Borenstein, E., Feldman, M. W. & Aoki, K. 2008 Evolution of learning in fluctuating environments: when selection favors both social and exploratory individual learning. Evolution 62, 586-602. (doi:10.1111/j.1558-5646.2007.00313.x)
2. van der Post, D. J. & Hogeweg, P. 2009 Cultural inheritance and diversification of diet in variable environments. Anim. Behav. 78, 155-166. (doi:10.1016/j.anbehav.2009. 04.009)
3. Whiten, A., Hinde, R. A., Laland, K. N. & Stringer, C. B. 2011 Culture evolves. Phil. Trans. R. Soc. B 366, 938-948. (doi:10.1098/rstb.2010.0372)
4. Rieucau, G. & Giraldeau, L.-A. 2011 Exploring the costs and benefits of social information use: an appraisal of current experimental evidence. Phil. Trans. R. Soc. B 366, 949-957. (doi:10.1098/rstb.2010.0325)
5. Thornton, A. & Clutton-Brock, T. 2011 Social learning and the development of individual and group behaviour in mammal societies. Phil. Trans. R. Soc. B 366, 978-987. (doi:10.1098/rstb.2010.0312)
6. Boere, G. C., Galbraith, C. A. & Stroud, D. A. (eds) 2006 Waterbirds around the world. Edinburgh, UK: The Stationary Office.
7. Davis, J. M. 2008 Patterns of variation in the influence of natal experience on habitat choice. Quart. Rev. Biol. 83, 363-380. (doi:10.1086/592851)
8. Slagsvold, T. & Wiebe, K. L. 2007 Learning the ecological niche. Proc. R. Soc. B 274, 19-23. (doi:10.1098/rspb. 2006.3663)
9. Doligez, B., Danchin, E. & Clobert, J. 2002 Public information and breeding habitat selection in a wild bird population. Science 297, 1168-1170. (doi:10. 1126/science.1072838)
10. Gould, J. L. & Gould, C. G. 2007 Animal architects. Building and the evolution of intelligence. New York, NY: Basic Books.
11. Madden, J. R., Lowe, T. J., Fuller, H.V., Dasmahapatra, K. K. & Coe, R. L. 2004 Local traditions of bower decoration by spotted bowerbirds in a single population. Anim. Behav. 68, 759-765. (doi:10.1016/j.anbehav.2003.12.007)
12. Curio, E., Ernst, U. & Vieth, W. 1978 Cultural transmission of enemy recognition: one function of mobbing. Science 202, 899-901. (doi:10.1126/science. 202.4370.899)
13. Griffin, A. S. 2004 Social learning about predators: a review and prospectus. Learn. Behav. 32, 131-140.
14. Davies, N. B. & Welbergen, J. A. 2009 Social transmission of a host defence against cuckoo parasitism. Science 324, 1318-1320. (doi:10.1126/science.1172227)
15. Davies, N. B., Madden, J. R., Butchart, S. H. M. & Rutila, J. 2006 A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species. Proc. R. Soc. B 273, 693-699. (doi:10. 1098/rspb.2005.3324)
16. Hollén, L. I. & Radford, A. N. 2009 The development of alarmcall behaviour in mammals and birds. Anim. Behav. 78, 791-800. (doi:10.1016/j.anbehav.2009.07.021)
17. Slagsvold, T. & Hansen, B. T. 2001 Sexual imprinting and the origin of obligate brood parasitism in birds. Am. Nat. 158, 354-367. (doi:10.1086/321994)
18. Jarvis, E. D. 2006 Selection for and against vocal learning in birds and mammals. Ornithol. Sci. 5, 5-14. (doi:10. 2326/osj.5.5)
19. Catchpole, C. K. & Slater, P. J. B. 2008 Bird song. Biological themes and variations. Cambridge, UK: Cambridge University Press.
20. Hoppitt, W. & Laland, K. N. 2008 Social processes influencing learning in animals: a review of the evidence. Adv. Stud. Behav. 38, 105-165. (doi:10.1016/S0065-3454(08)00003-X)
21. Eriksen, A., Slagsvold, T. & Lampe, H. M. In press. Vocal plasticity-are pied flycatchers (Ficedula hypoleuca) open-ended learners? Ethology. (doi:10.1111/j.1439-0310.2010.01864.x)
22. ten Cate, C. & Vos, D. R. 1999 Sexual imprinting and evolutionary processes in birds: a reassessment. Adv. Stud. Behav. 28, 1-31. (doi:10.1016/S0065-3454(08)60214-4)
23. Freeberg, T. M. 2004 Social transmission of courtship behavior and mating preferences in brown-headed cowbirds, Molothrus ater. Learn. Behav. 32, 122-130.
24. Harris, M. P. 1970 Abnormal migration and hybridization of Larus argentatus and L. fuscus after interspecies fostering experiments. Ibis 112, 488-498. (doi:10.1111/ j.1474-919X.1970.tb00820.x)
25. Grant, P. R. & Grant, B. R. 1997 Hybridization, sexual imprinting, and mate choice. Am. Nat. 149, 1-18. (doi:10.1086/285976)
26. Slagsvold, T., Hansen, B. T., Johannessen, L. E. & Lifjeld, L. T. 2002 Mate choice and imprinting in birds studied by cross-fostering in the wild. Proc. R. Soc. Lond. B 269, 1449-1455. (doi:10.1098/rspb.2002.2045)
27. Hansen, B. T., Johannessen, L. E. & Slagsvold, T. 2008 Imprinted species recognition lasts for life in free-living great tits and blue tits. Anim. Behav. 75, 921-927. (doi:10.1016/j.anbehav.2007.07.023)
28. Slagsvold, T. 2004 Cross-fostering of pied flycatchers (Ficedula hypoleuca) to heterospecific hosts in the wild: a study of sexual imprinting. Behaviour 14, 1079-1102. (doi:10.1163/1568539042664614)
29. Sæther, S. A. et al. 2007 Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318, 95-97. (doi:10.1126/science. 1141506)
30. Eriksen, A., Lampe, H. M. & Slagsvold, T. 2009 Interspecific cross-fostering affects song acquisition but not mate choice in pied flycatchers, Ficedula hypoleuca. Anim. Behav. 78, 857-863. (doi:10.1016/j.anbehav.2009.07.005)
31. Swaddle, J. P., Cathey, M. G., Correll, M. & Hodkinson, B. P. 2005 Socially transmitted mate preferences in a monogamous bird: a non-genetic mechanism of sexual selection. Proc. R. Soc. B 272, 1053-1058. (doi:10. 1098/rspb.2005.3054)
32. White, D. J. 2004 Influence of social learning on matechoice decisions. Learn. Behav. 32, 105-113.
33. Freed-Brown, G. & White, D. J. 2009 Acoustic mate copying: female cowbirds attend to other females' vocalizations to modify their song preferences. Proc. R. Soc. B 276, 3319-3325. (doi:10.1098/rspb.2009.0580)
34. Galef, B. G. & White, D. J. 1998 Mate choice copying in Japanese quail, Coturnix coturnix japonica. Anim. Behav. 55, 545-552. (doi:10.1006/anbe.1997.0616)
35. Drullion, D. & Dubois, F. 2008 Mate choice copying by female zebra finches Taeniopygia guttata: what happens when model females provide inconsistent information? Behav. Ecol. Sociobiol. 63, 269-276. (doi:10.1007/ s00265-008-0658-5)
36. Slagsvold, T. & Viljugrein, H. 1999 Mate choice copying versus preference for actively displaying males by female pied flycatchers. Anim. Behav. 57, 679-686. (doi:10. 1006/anbe.1998.0996)
37. 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. Anim. Behav. 59, 1199-1207. (doi:10.1006/anbe.1999.1419)
38. Cloutier, S., Newberry, R. C., Honda, K. & Alldredge, R. 2002 Cannibalistic behaviour spread by social learning. Anim. Behav. 63, 1153-1162. (doi:10.1006/anbe.2002. 3017)
39. Nicol, C. J. 2004 Development, direction, and damage limitation: social learning in domestic fowl. Learn. Behav. 32, 72-81.
40. Clark, J. A. 2010 White-tailed ptarmigan food calls enhance chick diet choice: learning nutritional wisdom? Anim. Behav. 79, 25-30. (doi:10.1016/j.anbehav.2009. 09.021)
41. Kitowski, I. 2009 Social learning of hunting skills in juvenile marsh harriers Circus aeruginosus. J. Ethol. 27, 327-332. (doi:10.1007/s10164-008-0123-y)
42. Lefebvre, L. 1986 Cultural diffusion of a novel foodfinding behaviour in urban pigeons: an experimental field test. Ethology 71, 295-304. (doi:10.1111/j.1439-0310.1986.tb00594.x)
43. Boogert, N. J., Reader, S. M., Hoppitt, W. & Laland, K. N. 2008 The origin and spread of innovations in starlings. Anim. Behav. 75, 1509-1518. (doi:10.1016/j. anbehav.2007.09.033)
44. Holzhaider, J. C., Hunt, G. R. & Gray, R. D. 2010 Social learning in New Caledonian crows. Learn. Behav. 38, 206-219. (doi:10.3758/LB.38.3.206)
45. Norton-Griffiths, M. 1967 Some ecological aspects of the feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis. Ibis 109, 412-424. (doi:10.1111/j.1474-919X. 1967.tb04014.x)
46. Bouchard, J., Goodyer, W. & Lefebvre, L. 2007 Social learning and innovation are positively correlated in pigeons (Columba livia). Anim. Cogn. 10, 259-266. (doi:10.1007/s10071-006-0064-1)
47. Laland, K. N. 2004 Social learning strategies. Learn. Behav. 32, 4-14.
48. Cadieu, N., Fruchard, S. & Cadieu, J.-C. 2010 Innovative individuals are not always the best demonstrators: feeding innovation and social transmission in Serinus canaria. PLoS ONE 5, e8841. (doi:10.1371/journal. pone.0008841)
49. Giraldeau, L.-A. & Dubois, F. 2008 Social foraging and the study of exploitative behavior. Adv. Stud. Behav. 38, 59-104. (doi:10.1016/S0065-3454(08)00002-8)
50. Zentall, T. R. 2004 Action imitations in birds. Learn. Behav. 32, 15-23.
51. Heyes, C. & Saggerson, A. 2002 Testing for imitative and nonimitative social learning in the budgerigar using a two-object/two-action test. Anim. Behav. 64, 851-859. (doi:10.1006/anbe.2003.2002)
52. 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. Anim. Behav. 72, 1329-1343. (doi:10.1016/j.anbehav. 2006.04.007)
53. Holzhaider, J. C., Gunt, G. R. & Gray, R. D. 2010 The development of pandanus tool manufacture in wild New Caledonian crows. Behaviour 147, 553-586. (doi:10. 1163/000579510X12629536366284)
54. Heyes, C. M. 1993 Imitation, culture and cognition. Anim. Behav. 46, 999-1010. (doi:10.1006/anbe.1993. 1281)
55. van der Post, D. J. & Hogeweg, P. 2008 Diet traditions and cumulative cultural processes as side-effects of grouping. Anim. Behav. 75, 133-144. (doi:10.1016/j. anbehav.2007.04.021)
56. Claidière, N. & Sperber, D. 2010 Imitation explains the propagation, not the stability of animal culture. Proc. R. Soc. B 277, 651-659. (doi:10.1098/rspb.2009. 1615)
57. Thornton, A. & Raihani, N. J. 2010 Identifying teaching in wild animals. Learn. Behav. 38, 297-309. (doi:10. 3758/LB.38.3.297)
58. Raihani, N. J. & Ridley, A. R. 2008 Experimental evidence for teaching in wild pied babblers. Anim. Behav. 75, 1-11. (doi:10.1016/j.anbehav.2007.11.001)
59. Galef, B. G. J. 2004 Approaches to the study of traditional behaviors of free-living animals. Learn. Behav. 32, 53-61.
60. Kendal, R. L., Galef, B. G. & van Schaik, C. P. 2010 Social learning research outside the laboratory: how and why? Learn. Behav. 38, 187-194. (doi:10.3758/ LB.38.3.187)
61. Reader, S. M. & Biro, D. 2010 Experimental identification of social learning in wild animals. Learn. Behav. 38, 265-283. (doi:10.3758/LB.38.3.265)
62. Whiten, A. & Mesoudi, A. 2008 Establishing an experimental science of culture: animal social diffusion experiments. Phil. Trans. R. Soc. B 363, 3477-3488. (doi:10.1098/rstb.2008.0134)
63. Langen, T. A. 1996 Social learning of a novel foraging skill by white-throated magpie jays (Calocitta formosa, Corvidae): a field experiment. Ethology 102, 157-166. (doi:10.1111/j.1439-0310.1996.tb01113.x)
64. Lorenz, K. 1935 Der Kumpan in der Umwelt des Vogels. J. Ornithol. 83, 137-214 (289-413). (doi:10.1007/ BF01905355)
65. Verzijden, M. N. & ten Cate, C. 2007 Early learning influences species assortative mating preferences in Lake Victoria cichlid fish. Biol. Lett. 3, 134-136. (doi:10.1098/rsbl.2006.0601)
66. Laland, K. N., Atton, N. & Webster, M. M. 2011 From fish to fashion: experimental and theoretical insights into the evolution of culture. Phil. Trans. R. Soc. B 366, 958-968. (doi:10.1098/rstb.2010.0328)
67. Kendrick, K. M., Hinton, M. R. & Atkins, K. 1998 Mothers determine sexual preferences. Nature 395, 229-230. (doi:10.1038/26129)
68. Johannessen, L. E., Slagsvold, T. & Hansen, B. T. 2006 Song structure and repertoire size affected by social rearing conditions: experimental evidence from the field. Anim. Behav. 72, 83-95. (doi:10.1016/j.anbehav.2005. 09.019)
69. Lack, D. 1971 Ecological isolation in birds. London, UK: Blackwell Scientific Publications.
70. Dhondt, A. A. 2010 Effects of competition on great and blue tit reproduction: intensity and importance in relation to habitat quality. J. Anim. Ecol. 79, 257-265. (doi:10.1111/j.1365-2656.2009.01624.x)
71. Partridge, L. 1979 Differences in behaviour between blue and coal tits reared under identical conditions. Anim. Behav. 27, 120-125. (doi:10.1016/0003-3472(79)90132-5)
72. Slagsvold, T. & Wiebe, K. L. 2007 Hatching asynchrony and early nestling mortality: the feeding constraint hypothesis. Anim. Behav. 73, 691-700. (doi:10.1016/j. anbehav.2006.05.021)
73. Pinheiro, J. C. & Bates, D. M. 2000 Statistics and computing. Mixed-effects models in S and S-PLUS. New York, NY: Springer.
74. Fisher, J. & Hinde, R. A. 1949 The opening of milk bottles by birds. Br. Birds 42, 347-357.
75. Rowe, C., Linström, L. & Lyytinen, A. 2004 The importance of pattern similarity between Müllerian mimics in predator avoidance learning. Proc. R. Soc. Lond. B 271, 407-413. (doi:10.1098/rspb. 2003.2615)
76. Estók, P., Zsebok, S. & Siemers, B. 2010 Great tits search for, capture, kill and eat hibernating bats. Biol. Lett. 6, 59-62. (doi:10.1098/rsbl.2009.0611)
77. Krebs, J. R., MacRoberts, M. H. & Cullen, J. M. 1972 Flocking and feeding in the great tit Parus major: an experimental study. Ibis 114, 507-530. (doi:10.1111/j. 1474-919X.1972.tb00852.x)
78. Marples, N. M., Roper, T. J. & Harper, D. G. C. 1998 Responses of wild birds to novel prey: evidence of dietary conservatism. Oikos 83, 161-165. (doi:10.2307/3546557)
79. Thomas, R. J., Bartlett, L.A., Marples, N.M., Kelly, D. J. & Cuthill, I. C. 2004 Prey selection by wild birds can allow novel prey and conspicuous colour morphs to spread in prey populations. Oikos 106, 285-294. (doi:10.1111/j. 0030-1299.2004.13089.x)
80. Schaefer, H. M., Spitzer, K. & Bairlein, F. 2008 Longterm effects of previous experience determine nutrient discrimination abilities in birds. Front. Zool. 5, 4. (doi:10.1186/1742-9994-5-4)
81. Dall, S. R. X. & Cuthill, I. C. 1997 The information costs of generalism. Oikos 80, 197-202. (doi:10.2307/ 3546535)
82. Marples, N. M., Kelly, D. J. & Thomas, R. J. 2005 The evolution of warning coloration is not paradoxical. Evolution 59, 933-940.
83. Salva, O. R., Daisley, J. N., Regolin, L. & Vallortigara, G. 2010 Time-dependent lateralization of social learning in the domestic chick (Gallus gallus domesticus): effects of retention delays in the observed lateralization pattern. Behav. Brain Res. 212, 152-158. (doi:10.1016/j.bbr. 2010.04.004)
84. Danchin, E. & Wagner, R. H. 2010 Inclusive heritability: combining genetic and non-genetic information to study animal behavior and culture. Oikos 119, 210-218. (doi:10.1111/j.1600-0706.2009.17640.x)
85. Pfenning, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D. & Moczek, A. P. 2010 Phenotypic plasticity's impact on diversification and speciation. Trends Ecol. Evol. 25, 459-467. (doi:10. 1016/j.tree.2010.05.006)
86. Paenke, I., Sendhoff, B. & Kawecki, T. J. 2007 Influence of plasticity and learning on evolution under directional selection. Am. Nat. 170, E47-E58. (doi:10. 1086/518952)
87. Stevens, M. & Merilaita, S. 2009 Animal camouflage: current issues and new perspectives. Phil. Trans. R. Soc. B 364, 423-427. (doi:10.1098/rstb.2008.0217)
88. Begon, M., Townsend, C. R. & Harper, J. L. 2005 Ecology. From individual to ecosystem, 4th edn. Oxford, UK: Blackwell Publishing.
89. Stephens, D. W., Brown, J. S. & Ydenberg, R. C. 2007 Foraging, behavior and ecology. Chicago, IL: University of Chicago Press.
90. Davis, J. M. & Stamps, J. A. 2004 The effect of natal experience on habitat preferences. Trends Ecol. Evol. 19, 411-416. (doi:10.1016/j.tree.2004.04.006)
91. Tonnis, B., Grant, P. R., Grant, B. R. & Petren, K. 2005 Habitat selection and ecological speciation in Galápagos warbler finches (Certhidea olivacea and Certhidea fusca). Proc. R. Soc. B 272, 819-826. (doi:10.1098/rspb.2004. 3030)
92. Chevin, L.-M., Lande, R. & Mace, G. M. 2010 Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, 1-8. (doi:10.1371/journal.pbio.1000357)
93. Stamps, J. A., Krishnan, V. V. & Willits, N. H. 2009 How different types of natal experience affect habitat preferences. Am. Nat. 174, 623-630. (doi:10.1086/ 644526)
94. Beltman, J.B., Haccou, P. & tenCate, C. 2004 Learning and colonization of new niches: a first step toward speciation. Evolution 58, 35-46.
95. Grosch, K. 2003 Hybridization between two insectivorous bird species and the effect on prey-handling efficiency. Evol. Ecol. 17, 1-17. (doi:10.1023/A:1022451219527)
96. Slagsvold, T. & Lifjeld, J. T. 1985 Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. J. Zool. 206, 321-328. (doi:10.1111/j. 1469-7998.1985.tb05661.x)
97. Hill, G. E., Inouye, C. Y. & Montgomerie, R. 2002 Dietary carotenoids predict plumage coloration in wild house finches. Proc. R. Soc. Lond. B 269, 1119-1124. (doi:10. 1098/rspb.2002.1980)
98. McLoughlin, P. D., Coulson, T. & Clutton-Brock, T. 2008 Cross-generational effects of habitat and density on life history in red deer. Ecology 89, 3317-3326. (doi:10.1890/07-1044.1)