Social influences on the development of ringtailed lemur feeding ecology

Animal Behaviour

Volumn 84, Issue 6, 2012, Pages 1547-1555

  O'Mara, M Teague ^a,b,c   Hickey, Cathriona M ^d,e  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b ARIZONA STATE UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^d UNIVERSITY OF YORK   (United Kingdom)

^e Flamingo Land Ltd   (United Kingdom)

Author keywords

Co feeding; Lemur catta; Ontogeny; Ringtailed lemur; Social learning; Stimulus enhancement

Indexed keywords

COMPLEXITY; DIET; FEEDING ECOLOGY; LEARNING; ONTOGENY; PHYLOGENETICS; PRIMATE;

BEZA MAHAFALY SPECIAL RESERVE; MADAGASCAR; TOLIARA;

HAPLORHINI; LEMUR; LEMUR CATTA; LEMURIDAE; PRIMATES; VERTEBRATA;

EID: 84870413195     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2012.09.032     Document Type: Article

References (86)

1. Altmann J. Observational study of behavior: sampling methods. Behaviour 1974, 49:227-265.
2. Altmann J. Baboon Mothers and Infants 1980, Harvard University Press, Cambridge, Massachusetts.
3. Altmann S.A. Diet of yearling female primates (Papio cynocephalus) predicts lifetime fitness. Proceedings of the National Academy of Sciences, U.S.A. 1991, 88:420-423.
4. Anderson J.R., Fornasieri I., Ludes E., Roeder J.J. Social processes and innovative behavior in changing groups of Lemur fulvus. Behavioural Processes 1992, 27:101-112.
5. Begon M., Harper J., Townsend C. Ecology 1996, Blackwell Science, Oxford.
6. Biro D., Inoue-Nakamura N., Tonooka R., Yamakoshi G., Sousa C., Matsuzawa T. Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. Animal Cognition 2003, 6:213-223.
7. Carter A.J., Marshall H.H., Heinsohn R., Cowlishaw G. How not to measure boldness: novel object and antipredator responses are not the same in wild baboons. Animal Behaviour 2012, 84:603-609.
8. Cheney D.L., Seyfarth R.M. Vervet monkey alarm calls: manipulation through shared information. Behaviour 1985, 94:150-166.
9. Choleris E., Guo C., Liu H., Mainardi M., Valsecchi P. The effect of demonstrator age and number on duration of socially-induced food preferences in house mouse (Mus domesticus). Behavioural Processes 1997, 41:69-77.
10. Coelho A.M., Bramblett C.A. Interobserver agreement on a molecular ethogram of the genus Papio. Animal Behaviour 1981, 29:443-448.
11. Dagosto M. Testing positional behavior of Malagasy lemurs: a randomization approach. American Journal of Physical Anthropology 1994, 94:189-202.
12. Dean L.G., Hoppitt W., Laland K.N., Kendal R.L. Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata and Varecia rubra). American Journal of Primatology 2011, 73:1210-1221.
13. Dewar R., Richard A. Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences, U.S.A. 2007, 104:13723-13727.
14. Dindo M., Whiten A., de Waal F. Social facilitation of exploratory foraging behavior in capuchin monkeys (Cebus apella). American Journal of Primatology 2009, 71:419-426.
15. Duffy G.A., Pike T.W., Laland K.N. Size-dependent directed social learning in nine-spined sticklebacks. Animal Behaviour 2009, 78:371-375.
16. Emery N.J., Clayton N.S. The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 2004, 306:1903-1907.
17. Feldman D.W., Klopfer P.H. A study of observational learning in lemurs. Zeitschrift für Tierpsychologie 1972, 30:297-304.
18. Galef B.G., Giraldeau L.-A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Animal Behaviour 2001, 61:3-15.
19. Godin J.G.J., Herdman E.J.E., Dugatkin L.A. Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Animal Behaviour 2005, 69:999-1005.
20. Gosset D., Roeder J.J. Factors affecting feeding decisions in a group of black lemurs confronted with novel food. Primates 2001, 42:175-182.
21. Gould L. The social development of free-ranging infant Lemur catta at Berenty Reserve, Madagascar. International Journal of Primatology 1990, 11:297-318.
22. Hauser M.D. Ontogeny of foraging behavior in wild vervet monkeys (Cercopithecus aethiops): social interactions and survival. Journal of Comparative Psychology 1993, 107:276-282.
23. Heinsohn R.G. Slow learning of foraging skills and extended parental care in cooperatively breeding white-winged choughs. American Naturalist 1991, 137:864-881.
24. Heyes C. Social learning in animals: categories and mechanisms. Biological Reviews of the Cambridge Philosophical Society 1994, 69:207-231.
25. Hilborn A., Pettorelli N., Orme C.D.L., Durant S.M. Stalk and chase: how hunt stages affect hunting success in Serengeti cheetah. Animal Behaviour 2012, 84:701-706.
26. Hoppitt W., Laland K. Social processes influencing learning in animals: a review of the evidence. Advances in the Study of Behavior 2008, 38:105-165.
27. Hosey G.R., Jacques M., Pitts A. Drinking from tails: social learning of a novel behaviour in a group of ring-tailed lemurs (Lemur catta). Primates 1997, 38:415-422.
28. Huchard E., Canale C., Le G.C., Perret M., Henry P., Kappeler P. Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate. Proceedings of the Royal Society B 2012, 279:1371-1379.
29. Humle T., Snowdon C.T. Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins, Saguinus oedipus. Animal Behaviour 2008, 75:267-277.
30. Irwin M. Feeding ecology of Propithecus diadema in forest fragments and continuous forest. International Journal of Primatology 2008, 29:95-115.
31. Jaeger T. Categorical data analysis: away from ANOVAs (transformation or not) and towards logit mixed models. Journal of Memory and Language 2008, 59:434-446.
32. Joffe T.H. Social pressures have selected for an extended juvenile period in primates. Journal of Human Evolution 1997, 32:593-605.
33. Jolly A. Lemur Behavior, a Madagascar Field Study 1966, University of Chicago Press, Chicago.
34. Jolly A. Lemur social behavior and primate intelligence. Science 1966, 153:501-506.
35. Kappeler P.M. The acquisition process of a novel behavior pattern in a group of ring-tailed lemurs (Lemur catta). Primates 1987, 28:225-228.
36. Kawai M. Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 1965, 6:1-30.
37. Kendal J., Giraldeau L.-A., Laland K. The evolution of social learning rules: payoff-biased and frequency-dependent biased transmission. Journal of Theoretical Biology 2009, 260:210-219.
38. Kendal R.L., Custance D.M., Kendal J.R., Vale G., Stoinski T.S., Rakotomalala N.L., Rasamimanana H. Evidence for social learning in wild lemurs (Lemur catta). Learning & Behavior 2010, 38:220-234.
39. King B.J. Social information transfer in monkeys, apes, and hominids. Yearbook of Physical Anthropology 1991, 34:97-115.
40. King B.J. Primate infants as skilled information gatherers. Pre- and Perinatal Psychology Journal 1994, 8:287-307.
41. Krakauer, E. B. 2005. Development of aye-aye (Daubentonia madagascariensis) foraging skills: independent exploration and social learning. Ph.D. thesis, Duke University.
42. Laland K.N. Social learning strategies. Learning & Behavior 2004, 32:4-14.
43. Laland K., Janik V. The animal cultures debate. Trends in Ecology & Evolution 2006, 21:542-547.
44. Lawler R., Caswell H., Richard A., Ratsirarson J., Dewar R., Schwartz M. Demography of Verreaux's sifaka in a stochastic rainfall environment. Oecologia 2009, 161:491-504.
45. Lewis F., Butler A., Gilbert L. A unified approach to model selection using the likelihood ratio test. Methods in Ecology and Evolution 2011, 2:155-162.
46. Luncz L., Mundry R., Boesch C. Evidence for cultural differences between neighboring chimpanzee communities. Current Biology 2012, 22:922-926.
47. Machlis L., Dodd P., Fentress J. The pooling fallacy: problems arising when individuals contribute more than one observation to the data set. Zeitschrift für Tierpsychologie 1985, 68:201-214.
48. Matsuzawa T., Biro D., Humle T., Inoue-Nakamura N., Tonooka R., Yamakoshi G. Emergence of culture in wild chimpanzees: education by master-apprenticeship. Primate Origins of Human Cognition and Behavior 2001, 557-574. Springer, Berlin. T. Matsuzawa (Ed.).
49. Mersmann D., Tomasello M., Call J., Kaminski J., Taborsky M. Simple mechanisms can explain social learning in domestic dogs (Canis familiaris). Ethology 2011, 117:675-690.
50. Mery F., Kawecki T.J. An operating cost of learning in Drosophila melanogaster. Animal Behaviour 2004, 68:589-598.
51. Nicholson, N. 1982. Weaning and the development of independence in olive baboons. Ph.D. thesis, Harvard University.
52. O'Mara, M. T. 2012. Development of feeding in ring-tailed lemurs. Ph.D. thesis, Arizona State University.
53. Page R., Ryan M. Flexibility in assessment of prey cues: frog-eating bats and frog calls. Proceedings of the Royal Society B 2005, 272:841-847.
54. Pereira M.E., Kappeler P.M. Divergent systems of agonistic behaviour in lemurid primates. Behaviour 1997, 134:225-274.
55. Perry S. Social traditions and social learning in capuchin monkeys (Cebus). Philosophical Transactions of the Royal Society B 2011, 366:988-996.
56. Pianka E.R. The structure of lizard communities. Annual Review of Ecology and Systematics 1973, 4:53-74.
57. Pinheiro J.C., Bates D.M. Mixed-effects Models in S and S-plus 2009, Springer, Berlin.
58. R: a Language and Environment for Statistical Computing 2011, R Development Core Team, R Foundation for Statistical Computing, Vienna.
59. Rapaport L., Brown G. Social influences on foraging behavior in young nonhuman primates: learning what, where, and how to eat. Evolutionary Anthropology 2008, 17:189-201.
60. Rendell L., Boyd R., Cownden D., Enquist M., Eriksson K., Feldman M., Fogarty L., Ghirlanda S., Lillicrap T., Laland K. Why copy others? Insights from the social learning strategies tournament. Science 2010, 328:208.
61. Richerson P., Boyd R. Not by Genes Alone: How Culture Transformed Human Evolution 2005, University of Chicago Press, Chicago.
62. Ross C., Jones K. Socioecology and the evolution of primate reproductive rates. Comparative Primate Socioecology 1999, 73-110. Cambridge University Press, Cambridge. P.C. Lee (Ed.).
63. Sandel A.A., Maclean E.L., Hare B. Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Animal Behaviour 2011, 81:925-931.
64. Sauther M.L. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. American Journal of Physical Anthropology 1991, 84:463-477.
65. Sauther, M. L. 1992. The effect of reproductive state, social rank and group size on resource use among free-ranging ringtailed lemurs (Lemur catta) of Madagascar. Ph.D. thesis, Washington University.
66. van Schaik C.P. Animal culture: chimpanzee conformity?. Current Biology 2012, 22:R402-R404.
67. van Schaik C.P., Burkart J. Social learning and evolution: the cultural intelligence hypothesis. Philosophical Transactions of the Royal Society B 2011, 366:1008-1016.
68. Sherwin C.M., Heyes C.M., Nicol C.J. Social learning influences the preferences of domestic hens for novel food. Animal Behaviour 2002, 63:933-942.
69. Slagsvold T., Wiebe K. Learning the ecological niche. Proceedings of the Royal Society B 2007, 274:19-23.
70. Slagsvold T., Wiebe K.L. Social learning in birds and its role in shaping a foraging niche. Philosophical Transactions of the Royal Society B 2011, 366:969-977.
71. Stoinski T., Drayton L., Price E. Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata). Biology Letters 2011, 7:376-379.
72. Sussman R.W., Ratsirarson J. Beza Mahafaly Special Reserve: a research site in southwestern Madagascar. Ringtailed Lemur Biology: Lemur catta in Madagascar 2006, 43-51. Springer, Berlin. A. Jolly, R.W. Sussman, N. Koyama, H. Rasamimanana (Eds.).
73. Tarnaud L. Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte. International Journal of Primatology 2004, 25:803-824.
74. Thornton A., Clutton-Brock T. Social learning and the development of individual and group behaviour in mammal societies. Philosophical Transactions of the Royal Society B 2011, 366:978-987.
75. Thornton A., McAuliffe K. Teaching in wild meerkats. Science 2006, 313:227-229.
76. Thornton A., Raihani N.J. The evolution of teaching. Animal Behaviour 2008, 75:1823-1836.
77. Toelch U., Van Delft M.J., Bruce M., Donders R., Meeus M., Reader S. Decreased environmental variability induces a bias for social information use in humans. Evolution and Human Behavior 2009, 30:32-40.
78. Ueno A. Development of co-feeding behavior in young wild Japanese macaques (Macaca fuscata). Infant Behavior & Development 2005, 28:481-491.
79. van de Waal E., Bshary R. Social-learning abilities of wild vervet monkeys in a two-step task artificial fruit experiment. Animal Behaviour 2011, 81:433-438.
80. van de Waal E., Renevey N., Favre C., Bshary R. Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proceedings of the Royal Society B 2010, 277:2105-2111.
81. van de Waal E., Krützen M., Hula J., Goudet J., Bshary R. Similarity in food cleaning techniques within matrilines in wild vervet monkeys. PLoS One 2012, 7:e35694.
82. Warton D., Hui F. The arcsine is asinine: the analysis of proportions in ecology. Ecology 2011, 92:3-10.
83. West M.J., King A.P., White D.J. The case for developmental ecology. Animal Behaviour 2003, 66:617-622.
84. Whiten A. Primate culture and social learning. Cognitive Science 2000, 24:477-508.
85. Whiten A. The scope of culture in chimpanzees, humans and ancestral apes. Philosophical Transactions of the Royal Society B 2011, 366:997-1007.
86. Whiten A., Goodall J., Mcgrew W., Nishida T., Reynolds V., Sugiyama Y., Tutin C., Wrangham R., Boesch C. Cultures in chimpanzees. Nature 1999, 399:682-685.