Negotiations over Grooming in Wild Vervet Monkeys (Chlorocebus pygerythrus)

International Journal of Primatology

Volumn 34, Issue 6, 2013, Pages 1153-1171

  van de Waal, Erica ^a,b,c   Spinelli, Martina ^a,b   Bshary, Redouan ^a,b   Ros, Albert Frank Huascar ^a   Noë, Ronald ^b,d  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b UNIVERSITY OF SOUTH AFRICA   (South Africa)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Allogrooming; Chlorocebus pygerythrus; Negotiation; Signaling; Wild Vervet Monkeys

Indexed keywords

COOPERATIVE BEHAVIOR; GROOMING; PRIMATE; SIGNALING; WILD POPULATION;

LOSKOP DAM; MPUMALANGA; SOUTH AFRICA;

ANIMALIA; CERCOPITHECUS; CERCOPITHECUS PYGERYTHRUS; PRIMATES;

EID: 84890115515     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-013-9729-1     Document Type: Article

References (94)

1. Akçay, E., & Roughgarden, J. (2007). Negotiation of mutualism: Rhizobia and legumes. Proceedings of the Royal Society of London B: Biological Sciences, 274(1606), 25-32.
2. Akçay, E., & Simms, E. L. (2011). Negotiation, sanctions, and context dependency in the legume-rhizobium mutualism. The American Naturalist, 178(1), 1-14.
3. Balasubramaniam, K. N., Berman, C. M., Ogawa, H., & Li, J. (2011). Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana. American Journal of Primatology, 73(12), 1269-1279.
4. Barelli, C., Reichard, U. H., & Mundry, R. (2011). Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar? Animal Behaviour, 82(4), 801-809.
5. Barrett, L., Gaynor, D., & Henzi, S. P. (2002). A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Animal Behaviour, 63, 1047-1053.
6. Barrett, L., & Henzi, S. P. (2006). Monkeys, markets and minds: Biological markets and primate sociality. In P. M. Kappeler & C. P. van Schaik (Eds.), Cooperation in primates and humans (pp. 209-232). Berlin: Springer Science+Business Media.
7. Barrett, L., Henzi, S. P., Weingrill, T., & Hill, R. A. (1999). Market forces predict grooming reciprocity in female baboons. Proceedings of the Royal Society of London B: Biological Sciences, 266, 665-670.
8. Bell, M. B. V., Radford, A. N., Smith, R. A., Thompson, A. M., & Ridley, A. R. (2010). Bargaining babblers: Vocal negotiation of cooperative behaviour in a social bird. Proceedings of the Royal Society of London B: Biological Sciences, 277(1698), 3223-3228.
9. Binmore, K. (2010). Bargaining in biology? Journal of Evolutionary Biology, 23(7), 1351-1363.
10. Bshary, R., & Noë, R. (2003). Biological markets: The ubiquitous influence of partner choice on the dynamics of cleaner fish-client reef fish interactions. In P. Hammerstein (Ed.), Genetic and cultural evolution of cooperation (pp. 167-184). Cambridge: MIT Press.
11. Bulmer, E., Celis, P., & Gil, D. (2008). Parent-absent begging: Evidence for sibling honesty and cooperation in the spotless starling (Sturnus unicolor). Behavioral Ecology, 19(2), 279-284.
12. Carne, C., Wiper, S., & Semple, S. (2011). Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. American Journal of Primatology, 73(11), 1127-1133.
13. Chancellor, R. L., & Isbell, L. A. (2009). Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena). Behavioral Ecology, 20(1), 79-86.
14. de Waal, F. B. M. (2000). Attitudinal reciprocity in food sharing among brown capuchin monkeys. Animal Behaviour, 60, 253-261.
15. Doake, S., & Elwood, R. W. (2011). How resource quality differentially affects motivation and ability to fight in hermit crabs. Proceedings of the Royal Society of London B: Biological Sciences, 278(1705), 567-573.
16. Dreiss, A., Lahlah, N., & Roulin, A. (2010). How siblings adjust sib-sib communication and begging signals to each other. Animal Behaviour, 80(6), 1049-1055.
17. Dunbar, R. I. M. (1991). Functional significance of social grooming in primates. Folia Primatologica, 57(3), 121-131.
18. Dunbar, R. I. M. (2010). The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms. Neuroscience & Biobehavioral Reviews, 34, 260-268.
19. Dunbar, R. I. M., & Sharman, M. (1984). Is social grooming altruistic? Zeitschrift für Tierpsychologie, 64, 163-173.
20. Dunbar, R. I. M., & Thelma, E. (2001). Guenons, macaques, and baboons. In D. MacDonald (Ed.), The new encyclopedia of mammals (pp. 356-375). Oxford: Oxford University Press.
21. Fedurek, P., & Dunbar, R. I. M. (2009). What does mutual grooming tell us about why chimpanzees groom? Ethology, 115(6), 566-575.
22. Frank, R. E., & Silk, J. B. (2009). Grooming exchange between mothers and non-mothers: The price of natal attraction in wild baboons (Papio anubis). Behaviour, 146, 889-906.
23. Fraser, B. (2013). False advertising in biological markets: partner choice and the problem of reliability. In K. Sterelny, R. Joyce, B. Calcott, & B. Fraser (Eds.), Evolution, cooperation and complexity. Cambridge: MIT Press.
24. Fruteau, C., Lemoine, S., Hellard, E., van Damme, E., & Noë, R. (2011a). When females trade grooming for grooming: Testing partner control and partner choice models of cooperation in two primate species. Animal Behaviour, 81(6), 1223-1230.
25. Fruteau, C., van de Waal, E., van Damme, E., & Noë, R. (2011b). Infant access and handling in sooty mangabeys and vervet monkeys. Animal Behaviour, 81(1), 153-161.
26. Ginther, A. J., & Snowdon, C. T. (2009). Expectant parents groom adult sons according to previous alloparenting in a biparental cooperatively breeding primate. Animal Behaviour, 78(2), 287-297.
27. Grafen, A. (1990a). Biological signals as handicaps. Journal of Theoretical Biology, 144, 517-546.
28. Grafen, A. (1990b). Sexual selection unhandicapped by the Fisher Process. Journal of Theoretical Biology, 144, 473-516.
29. Gumert, M. D. (2007a). Grooming and infant handling interchange in Macaca fascicularis: The relationship between infant supply and grooming payment. International Journal of Primatology, 28(5), 1059-1074.
30. Gumert, M. D. (2007b). Payment for sex in a macaque mating market. Animal Behaviour, 74(6), 1655-1667.
31. Hamilton, W. D. (1964a). The genetical evolution of social behaviour I. Journal of Theoretical Biology, 7, 1-16.
32. Hamilton, W. D. (1964b). The genetical evolution of social behaviour II. Journal of Theoretical Biology, 7, 17-52.
33. Hazlett, B. A. (1978). Shell exchanges in hermit crabs-aggression, negotiation, or both. Animal Behaviour, 26, 1278-1279.
34. Hazlett, B. A. (1996). Assessments during shell exchanges by the hermit crab Clibanarius vittatus: The complete negotiator. Animal Behaviour, 51, 567-573.
35. Henzi, S. P., & Barrett, L. (2002). Infants as a commodity in a baboon market. Animal Behaviour, 63(5), 915-921.
36. Henzi, S. P., Barrett, L., Gaynor, D., Greeff, J., Weingrill, T., & Hill, R. A. (2003). Effect of resource competition on the long-term allocation of grooming by female baboons: Evaluating Seyfarth's model. Animal Behaviour, 66, 931-938.
37. Hinde, C., & Kilner, R. (2007). Negotiations within the family over the supply of parental care. Proceedings of the Royal Society of London B: Biological Sciences, 274(1606), 53-60.
38. Johnson, D. D. P., Stopka, P., & Macdonald, D. W. (2004). Ideal flea constraints on group living: Unwanted public goods and the emergence of cooperation. Behavioral Ecology, 15(1), 181-186.
39. Johnstone, R. A., & Roulin, A. (2003). Sibling negotiation. Behavioral Ecology, 14(6), 780-786.
40. Keverne, E. B. (1989). Beta-endorphin concentrations in cerebrospinal-fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology, 14(1-2), 155-162.
41. Kosztolanyi, A., Cuthill, I. C., & Szekely, T. (2009). Negotiation between parents over care: Reversible compensation during incubation. Behavioral Ecology, 20(2), 446-452.
42. Lazaro-Perea, C., de Fátima Arruda, M., & Snowdon, C. T. (2004). Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets. Animal Behaviour, 67(4), 627-636.
43. Leinfelder, I., de Vries, H., Deleu, R., & Nelissen, M. (2001). Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons. American Journal of Primatology, 55, 25-42.
44. Lendvai, A. Z., Barta, Z., & Chastel, O. (2009). Conflict over parental care in house sparrows: Do females use a negotiation rule? Behavioral Ecology, 20(3), 651-656.
45. Lessells, C. M., & McNamara, J. M. (2012). Sexual conflict over parental investment in repeated bouts: Negotiation reduces overall care. Proceedings of the Royal Society of London B: Biological Sciences, 279(1733), 1506-1514.
46. Lewis, R. J. (2002). Beyond dominance: The importance of leverage. Quarterly Review of Biology, 77(2), 149-164.
47. Löttker, P., Huck, M., Zinner, D. P., & Heymann, E. W. (2007). Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax). American Journal of Primatology, 69, 1-14.
48. Macdonald, S., Schülke, O., & Ostner, J. (2013). The absence of grooming for rank-related benefits in female Assamese macaques (Macaca assamensis). International Journal of Primatology, 34, 571-584.
49. McNamara, J. M., Gasson, C. E., & Houston, A. I. (1999). Incorporating rules for responding into evolutionary games. Nature, 401(6751), 368-371.
50. Meade, J., Nam, K.-B., Lee, J.-W., & Hatchwell, B. J. (2011). An experimental test of the information model for negotiation of biparental care. PLoS ONE, 6(5), e19684.
51. Melis, A. P., Hare, B., & Tomasello, M. (2009). Chimpanzees coordinate in a negotiation game. Evolution and Human Behavior, 30(6), 381-392.
52. Nakamichi, M. (2003). Age-related differences in social grooming among adult female Japanese monkeys (Macaca fuscata). Primates, 44(3), 239-246.
53. Nash, J. F., Jr. (1950). The bargaining problem. Econometrica, 18(2), 155-162.
54. Newton-Fisher, N. E., & Lee, P. C. (2011). Grooming reciprocity in wild male chimpanzees. Animal Behaviour, 81(2), 439-446.
55. Noë, R. (2006). Cooperation experiments: Coordination through communication versus acting apart together. Animal Behaviour, 71(1), 1-18.
56. Noë, R., & Hammerstein, P. (1994). Biological markets: Supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology, 35, 1-11.
57. Noë, R., & Hammerstein, P. (1995). Biological markets. Trends in Ecology and Evolution, 10, 336-339.
58. Noë, R., van Schaik, C. P., & van Hooff, J. A. R. A. M. (1991). The market effect: An explanation for pay-off asymmetries among collaborating animals. Ethology, 87, 97-118.
59. Norscia, I., Antonacci, D., & Palagi, E. (2009). Mating first, mating more: Biological market fluctuation in a wild prosimian. PLoS ONE, 4(3), e4679.
60. Patricelli, G. L., Krakauer, A. H., & McElreath, R. (2011). Assets and tactics in a mating market: Economic models of negotiation offer insights into animal courtship dynamics on the lek. Current Zoology, 57, 225-236.
61. Payne, H. F. P., Lawes, M. J., & Henzi, S. P. (2003). Competition and the exchange of grooming among female samango monkeys (Cercopithecus mitis erythrarchus). Behaviour, 140(4), 453-471.
62. Port, M., Clough, D., & Kappeler, P. M. (2009). Market effects offset the reciprocation of grooming in free-ranging redfronted lemurs, Eulemur fulvus rufus. Animal Behaviour, 77(1), 29-36.
63. Raihani, N. J., & Bshary, R. (2011). Resolving the iterated prisoner's dilemma: Theory and reality. Journal of Evolutionary Biology, 24(8), 1628-1639.
64. Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43, 223-225.
65. Roberts, G. (1998). Competitive altruism: from reciprocity to the handicap principle. Proceedings of the Royal Society of London B: Biological Sciences, 265, 427-431.
66. Roberts, G. (2005). Cooperation through interdependence. Animal Behaviour, 70(4), 901-908.
67. Roulin, A., Kolliker, M., & Richner, H. (2000). Barn owl (Tyto alba) siblings vocally negotiate resources. Proceedings of the Royal Society of London B: Biological Sciences, 267(1442), 459-463.
68. Rubinstein, A. (1982). Perfect equilibrium in a bargaining model. Econometrica, 50(1), 97-109.
69. Sachs, J. L., Mueller, U. G., Wilcox, T. P., & Bull, J. J. (2004). The evolution of cooperation. Quarterly Review of Biology, 79(2), 135-160.
70. Sade, D. S. (1972). Sociometrics of Macaca mulatta-linkages and cliques in grooming matrices. Folia Primatologica, 18(3-4), 196-223.
71. Saunders, C. D., & Hausfater, G. (1988). The functional-significance of baboon grooming behavior. Annals of the New York Academy of Sciences, 525, 430-432.
72. Schino, G. (2007). Grooming and agonistic support: a meta-analysis of primate reciprocal altruism. Behavioral Ecology, 18(1), 115-120.
73. Schino, G., Di Giuseppe, F., Visalberghi, E. (2009). The Time Frame of Partner Choice in the Grooming Reciprocaon of Cebuspaella. Ethology, 115, 70-76.
74. Seyfarth, R. M. (1977). A model of social grooming among adult female monkeys. Journal of Theoretical Biology, 65, 671-698.
75. Singh, M., Krishna, B. A., & Singh, M. (2006). Dominance hierarchy and social grooming in female lion-tailed macaques (Macaca silenus) in the Western Ghats, India. Journal of Biosciences, 31(3), 369-377.
76. Sirot, E. (2012). Negotiation may lead selfish individuals to cooperate: The example of the collective vigilance game. Proceedings of the Royal Society of London B: Biological Sciences, 279(1739), 2862-2867.
77. Slater, K. Y., Schaffner, C. M., & Aureli, F. (2007). Embraces for infant handling in spider monkeys: Evidence for a biological market? Animal Behaviour, 74(3), 455-461.
78. Smiseth, P., Musa, S., & Moore, A. (2006). Negotiation between parents: Does the timing of mate loss affect female compensation in Nicrophorus vespilloides? Behaviour, 143(3), 293-301.
79. Tanaka, I., & Takefushi, H. (1993). Elimination of external parasites (lice) is the primary function of grooming in free-ranging Japanese macaques. Anthropological Science, 101(2), 187-193.
80. Tiddi, B., Aureli, F., Polizzi di Sorrentino, E., Janson, C. H., & Schino, G. (2011). Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin monkeys. Behavioral Ecology, 22(3), 663-669.
81. Tiddi, B., Aureli, F., & Schino, G. (2010). Grooming for infant handling in tufted capuchin monkeys: A reappraisal of the primate infant market. Animal Behaviour, 79(5), 1115-1123.
82. Tiddi, B., Aureli, F., & Schino, G. (2012). Grooming up the hierarchy: The exchange of grooming and rank-related benefits in a new world primate. PLoS ONE, 7(5), e36641.
83. Trnka, A., & Grim, T. (2013). To compensate or not to compensate: Testing the negotiation model in the context of nest defense. Behavioral Ecology, 24(1), 223-228.
84. van de Waal, E. (2006) How to negotiate without language? Grooming markets in vervet monkeys. University of Neuchâtel.
85. van de Waal, E., Renevey, N., Favre, C. M., & Bshary, R. (2010). Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proceedings of the Royal Society of London B: Biological Sciences, 277(1691), 2105-2111.
86. van Hooff, J. A. R. A. M. (1967). The facial displays of the catarrhine monkeys and apes. In D. Morris (Ed.), Primate ethology (pp. 7-68). London: Weidenfeld & Nicolson.
87. Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). Berlin: Springer-Verlag.
88. Wei, W., Qi, X.-G., Guo, S.-T., Zhao, D.-P., Zhang, P., Huang, K., et al. (2012). Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana). PLoS ONE, 7(5), e36802.
89. Xia, D.-P., Li, J.-H., Garber, P. A., Matheson, M. D., Sun, B.-H., & Zhu, Y. (2013). Grooming reciprocity in male Tibetan macaques. American Journal of Primatology, 75, 1009-1020.
90. Xia, D.-P., Li, J., Garber, P. A., Sun, L., Zhu, Y., & Sun, B. (2012). Grooming reciprocity in female Tibetan macaques Macaca thibetana. American Journal of Primatology, 74(6), 569-579.
91. Zahavi, A. (1975). Mate selection-a selection for a handicap. Journal of Theoretical Biology, 53, 205-214.
92. Zahavi, A. (1977a). The cost of honesty (further remarks on the handicap principle). Journal of Theoretical Biology, 67, 603-605.
93. Zahavi, A. (1977b). Reliability in communication systems and the evolution of altruism. In B. Stonehouse & C. Perrins (Eds.), Evolutionary ecology (pp. 253-259). London: Macmillan.
94. Zahavi, A. (1995). Altruism as a handicap-the limitations of kin selection and reciprocity. Journal of Avian Biology, 26, 1-3.