Abstract
The quality, availability and distribution of food resources and their influence on types and levels of feeding competition play a central role in ecological models of female social structure in mammals. Here, we investigate the impact of social and ecological factors on rates of food-related aggression and the use of potential conflict avoidance mechanisms in wild Assamese macaques (Macaca assamensis) in northeastern Thailand. These questions were addressed by examining feeding competition at the level of individual food patches which provides detailed information on resource characteristics, aggression and feeding party composition. Results suggest that the frequency of aggression in food patches increases with increasing feeding group size and decreasing patch size but is not affected by ecological variables representing resource value (abundance and nutritional value of food items in a patch). Interestingly, females appear to employ several mechanisms to avoid direct conflicts, including the use of alternative feeding sites within food patches, delayed arrival at feeding sites, storing food in cheek pouches and co-feeding with individuals they share strong social bonds with. Conflict avoidance may be partially responsible for the absence of a rank-related skew in female energy intake in this population and may explain other cases where empirical data do not fit the predictions of socio-ecological theory. Our findings also inform the debate about the mechanisms generating fitness benefits from strong social bonds by suggesting that by increasing feeding tolerance, social bonds may enhance resource acquisition, reduce the risk of injuries and lower levels of agonism-related stress.
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Alberts S (2010) Primatology: “a faithful friend is the medicine of life”. Curr Biol 20:R632–R634
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Altmann J, Alberts S (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409
Aureli F (1992) Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis). Behav Ecol Sociobiol 31:329–337
Aureli F, van Schaik CP, van Hooff JARAM (1989) Functional aspects of reconciliation among captive long-tailed macaques (Macaca fascicularis). Am J Primatol 19:39–51
Aureli F, Cords M, van Schaik CP (2002) Conflict resolution following aggression in gregarious animals: a predictive framework. Anim Behav 64:325–343
Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, Cambridge
Baayen RH (2011) R package languageR. R package version 1.4, http://CRAN.R-project.org/package=languageR. Accessed 30 Dec 2011
Barton RA (1993) Sociospatial mechanisms of feeding competition in female olive baboons, Papio anubis. Anim Behav 46:791–802
Barton RA, Byrne RW, Whiten A (1996) Ecology, feeding competition and social structure in baboons. Behav Ecol Sociobiol 38:321–329
Bates D, Maechler M, Bolker B (2012) lme4 - linear mixed effects models using S4 classes. R package version 0.999999-0, http://CRAN.R-project.org/package=lme4. Accessed 23 June 2012
Berkman LF, Glass T (2000) Social integration, social networks, social support, and health. In: Berkman LF, Kawachi I (eds) Social epidemiology. Oxford University Press, New York, pp 137–173
Blumstein DT, Evans CS, Daniel JC (1999) An experimental study of behavioural group size effects in tammar wallabies, Macropus eugenii. Anim Behav 58:351–360
Boinski S (1999) The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol Anthropol 8:101–112
Borries C (1993) Ecology of female social relationships: hanuman langurs (Presbytis entellus) and the van Schaik model. Folia Primatol 61:21–30
Borries C, Larney E, Kreetiyutanont K, Koenig A (2002) The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, Northeast Thailand. Nat Hist Bull Siam Soc 50:75–88
Bradbury JW, Vehrencamp SL (1977) Social organization and foraging in emballonurid bats. III. Mating systems. Behav Ecol Sociobiol 2:1–17
Burnham KP, Anderson DR (2002) Model selection and multimodel Inference, 2nd edn. Springer, Berlin
Cameron E, Setsaas T, Linklater W (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci U S A 106:13850–13853
Carne C, Wiper S, Semple S (2011) Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. Am J Primatol 73:1127–1133
Chancellor RL, Isbell LA (2009) Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behav Ecol Sociobiol 63:1447–1458
Chapman C, Chapman L, Cords M, Gathua J, Gautier-Hion A, Lambert J, Rode K, Tutin C, White L (2002) Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In: Glenn ME, Cords M (eds) The guenons: diversity and adaptation in African monkeys. Kluwer Academic/Plenum Publishers, New York, pp 325–350
Clutton-Brock TH (1974) Primate social organization and ecology. Nature 250:539–542
Clutton-Brock TH, Janson C (2012) Primate socioecology at the crossroads: Past, present, and future. Evol Anthropol 21:136–150
Cords M (2000) Agonistic and afilliative relationships in a blue monkey group. In: Whitehead P, Jolly C (eds) Old world monkeys. Cambridge University Press, Cambridge, pp 453–479
Crook JH, Gartlan JC (1966) Evolution of primate societies. Nature 210:1200–1203
de Waal FBM (1991) Rank distance as a central feature of rhesus monkey social organization: a sociometric analysis. Anim Behav 41:383–395
Deutsch JC, Lee PC (1991) Dominance and feeding competition in captive rhesus monkeys. Int J Primatol 12:615–625
R Development Core Team (2012) A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria, http://www.R-project.org/. Accessed 22 Dec 2012
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Giraldeau L-A, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton
Goldberg JL, Grant JWA, Lefebvre L (2001) Effects of the temporal predictability and spatial clumping of food on the intensity of competitive aggression in the Zenaida dove. Behav Ecol 12:490–495
Gore MA (1993) Effects of food distribution on foraging competition in rhesus monkeys, Macaca mulatta, and hamadryas baboons, Papio hamadryas. Anim Behav 45:773–786
Goss-Custard JD (1980) Competition for food and interference among waders. Ardea 68:52
Hall CL, Fedigan LM (1997) Spatial benefits afforded by high rank in white-faced capuchins. Anim Behav 53:1069–1082
Hanya G (2009) Effects of food type and number of feeding sites in a tree on aggression during feeding in wild Macaca fuscata. Int J Primatol 30:569–581
Hayes VJ, Henzi SP, Freedman L, Gaynor D (1992) The differential use of cheek pouches in a troop of Papio ursinus. Primates 33:477–500
Heesen M (2014) Feeding competition in female Assamese macaques (Macaca assamensis). Georg-August-Universität Göttingen
Heesen M, Rogahn S, Ostner J, Schülke O (2013) Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67:1053–1066
Hemery GE, Savill PS, Pryor SN (2005) Applications of the crown diameter-stem diameter relationship for different species of broadleaved trees. Forest Ecol Manag 215:285–294
Hill WCO (1966) Primates: comparative anatomy and taxonomy (volume VI; Catarrhini, Cercopithecoidea, Cercopithecinae). Edinburgh University Press, Edinburgh
Hirsch BT (2007) Costs and benefits of within-group spatial position: a feeding competition model. Q Rev Biol 82:9–27
Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202
Isbell L, Pruetz J, Young T (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123–133
Janson CH (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138
Janson CH (1992) Evolutionary ecology of primate social structure. In: Smith EA, Winterhalder B (eds) Evolutionary ecology and human behavior. Aldine de Gruyter, New York, pp 95–130
Janson CH (2000) Primate socio-ecology: the end of a golden age. Evol Anthropol 9:73–86
Janson CH, Chapman CA (1999) Resources and primate community structure. In: Fleagle JG, Janson CH, Reed JM (eds) Primate communities. Cambridge University Press, Cambridge, pp 237–267
Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition: methods. Behaviour 105:165–186
Jarman PJ (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–256
King AJ, Isaac NJB, Cowlishaw G (2009) Ecological, social, and reproductive factors shape producer-scrounger dynamics in baboons. Behav Ecol 20:1039–1049
King AJ, Clark FE, Cowlishaw G (2011) The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks. Am J Primatol 73:768–774
Koenig A (2000) Competitive regimes in forest-dwelling hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109
Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783
Koenig A, Borries C (2006) The predictive power of socioecological models: a reconsideration of resource characteristics, agonism, and dominance hierarchies. In: Hohmann G, Robbins M, Boesch C (eds) Feeding ecology in apes and other primates—ecological, physical, and behavioral aspects. Cambridge University Press, Cambridge, pp 263–284
Koenig A, Borries C (2009) The lost dream of ecological determinism: time to say goodbye?…or a White Queen’s proposal? Evol Anthropol 18:166–174
Koenig A, Beise J, Chalise M, Ganzhorn J (1998) When females should contest for food—testing hypotheses about resource density, distribution, size, and quality with hanuman langurs (Presbytis entellus). Behav Ecol Sociobiol 42:225–237
Koenig A, Borries C, Suarez S, Kreetiyutanont K, Prabnasuk J (2004) Socio-ecology of Phayre’s leaf monkeys (Trachypithecus phayrei) at Phu Khieo wildlife sanctuary. J Wildlife Thail 12:150–163
Koenig A, Scarry CJ, Wheeler BC, Borries C (2013) Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain. Philos Trans R Soc Lond B Biol Sci 368(1618):20120348. doi: 10.1098/rstb.2012.0348
Lambert JE (2005) Competition, predation, and the evolutionary significance of the cercopithecine cheek pouch: the case of Cercopithecus and Lophocebus. Am J Phys Anthropol 126:183–192
Lambert JE, Whitham J (2001) Cheek pouch use in Papio cynocephalus. Folia Primatol 72:89–91
Lee PC (1987) Nutrition, fertility and maternal investment in primates. J Zool 213:409–422
Leighton M, Leighton DR (1982) The relationship of size of feeding aggregate to size of food patch: howler monkeys (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica 14:81–90
Lockhart BR, Robert C, Weih JR, Keith MS (2005) Crown radius and diameter at breast height relationships for six bottomland hardwood species. J Ark Acad Sci 59:110–115
Lomnicki A (1988) Population ecology of individuals. Princeton University Press, Princeton
Macdonald S, Schülke O, Ostner J (2013) The absence of grooming for rank-related benefits in female Assamese macaques (Macaca assamensis). Int J Primatol 34:571–584
Maynard Smith J (1974) The theory of games and the evolution of animal conflicts. J Theor Biol 47:209–221
Martin P, Bateson P (2007) Measuring Behaviour, Third edn. Cambridge University Press, Cambridge
Mitani JC (2006) Reciprocal exchange in chimpanzees and other primates. In: Kappeler P, van Schaik C (eds) Cooperation in primates and humans. Springer, Heidelberg, pp 107–120
Murray P (1973) The anatomy and functional significance of cheek pouches (Bursae buccales) in the Cercopithecinae, Cercopithecoidea. University of Chicago
Murray P (1975) The role of cheek pouches in cercopithecine monkey adaptive strategy. In: Tuttle RH (ed) Primate functional morphology and evolution. Mouton Publishers, The Hague, pp 151–194
Noldus (2003) MatMan 1.1.4. Noldus Information Technology, Inc. Sterling, USA, http://www.noldus.com/human-behavior-research/products/matman
Phillips KA (1995) Resource patch size and flexible foraging in white-faced capuchins (Cebus capucinus). Int J Primatol 16:509–519
Pruetz JD, Isbell LA (2000) Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behav Ecol Sociobiol 49:38–47
Ranta ESA, Peuhkuri N, Laurila A, Rita H, Metcalfe NB (1996) Producers, scroungers and foraging group structure. Anim Behav 51:171–175
Roberts S, Cords M (2013) Group size but not dominance rank predicts the probability of conception in a frugivorous primate. Behav Ecol Sociobiol 67:1995–2009
Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Anim Behav 51:967–980
Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 193–219
Schülke O, Chalise M, Koenig A (2006) The importance of ingestion rates for estimating food quality and energy intake. Am J Primatol 68:951–965
Seyfarth RM, Cheney DL (2012) The evolutionary origins of friendship. Annu Rev Psychol 63:153–177
Silk JB (2007) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559
Silk JB, Alberts S, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234
Silk JB, Alberts SC, Altmann J (2006a) Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds. Behav Ecol Sociobiol 61:197–204
Silk JB, Altmann J, Alberts SC (2006b) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 6:183–195
Silk JB, Beehner J, Bergman T, Crockford C, Engh A, Moscovice L, Wittig R, Seyfarth R, Cheney D (2010a) Female chacma baboons form strong, equitable, and enduring social bonds. Behav Ecol Sociobiol 64:1733–1747
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010b) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361
Smith KP, Christakis NA (2008) Social networks and health. Annu Rev Sociol 34:405–429
Smith LW, Link A, Cords M (2008) Cheek pouch use, predation risk, and feeding competition in blue monkeys (Cercopithecus mitis stuhlmanni). Am J Phys Anthropol 137:334–341
Snaith TV, Chapman CA (2005) Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behav Ecol Sociobiol 59:185–190
Snaith TV, Chapman CA (2007) Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol 16:94–106
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton
Sterck EHM, Steenbeek R (1997) Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour 134:749–774
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309
Strier KB (1989) Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatol 52:70–77
Su H, Birky W (2007) Within-group female-female agonistic interactions in Taiwanese macaques (Macaca cyclopis). Am J Primatol 69:199–211
Thierry B (2008) Primate socioecology, the lost dream of ecological determinism. Evol Anthropol 17:93–96
Tiddi B, Aureli F, Polizzi di Sorrentino E, Janson CH, Schino G (2011) Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin monkeys. Behav Ecol 22:663–669
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Heinemann, London, pp 136–179
van Noordwijk MA, van Schaik CP (1987) Competition among female long-tailed macaques, Macaca fascicularis. Anim Behav 35:577–589
van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology: the behavioural ecology of humans and other mammals. Blackwell Scientific Publications, Oxford, pp 195–218
Vander Wall SB, Longland WS, Pyare S, Veech JA (1998) Cheek pouch capacities and loading rates of heteromyid rodents. Oecologia 113:21–28
Ventura R, Majolo B, Koyama NF, Hardie S, Schino G (2006) Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. Am J Primatol 68:1138–1149
Vickery WL, Giraldeau L-A, Templeton JJ, Kramer DL, Chapman CA (1991) Producers, scroungers, and group foraging. Am Nat 137:847–863
Vogel E (2004) The ecological basis of aggression in white-faced capuchins monkeys, Cebus capucinus, in a Costa Rican dry forest. Stony Brook University
Vogel E (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344
Vogel E, Janson C (2007) Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method. Am J Primatol 69:533–550
Wheeler BC, Scarry CJ, Koenig A (2013) Rates of agonism among female primates: a cross-taxon perspective. Behav Ecol 24:1369–1380
Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5:139–159
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300
Yee JR, Cavigelli SA, Delgado B, McClintock MK (2008) Reciprocal affiliation among adolescent rats during a mild group stressor predicts mammary tumors and lifespan. Psychosom Med 70:1050–1059
Acknowledgments
We thank the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation (DNP) for permission (nos. 0004.3/3618 and 0002.3/2647) to conduct this study. We are grateful to J. Prabnasuk, K. Nitaya, M. Kumsuk and K. Kreetiyutanont (Phu Khieo Wildlife Sanctuary) for their cooperation and permission to carry out this research. We thank A. Koenig and C. Borries (Stony Brook University), who developed the field site at Huai Mai Sot Yai. We are very thankful to N. Juntuch, N. Ponganan, D. Bootros, S. Jomhlotwong, T. Kilawit, T. Wisate, P. Saisawatdikul and especially M. Swagemakers for their help in the field. We are also very grateful to W. Nuagchiy and A. Chunchaen for their help with data collection. We thank N. Bhumpakphan, W. Eiadthong (Kasetsart University) and W. Brockelman (Mahidol University) for their support and cooperation. Furthermore, we would like to thank Maria van Noordwijk and four anonymous reviewers for helpful comments on earlier drafts of this manuscript. This work was supported by the Max Planck Society and the University of Göttingen through funding from the German Initiative of Excellence.
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Approval and permission to conduct research was granted by the authorities of Thailand (permit no. 0004.3/3618 and 0002.3/2647), and all research was undertaken in strict accordance with the laws set forth by the National Research Council of Thailand and the regulations of the Department of National Parks, Wildlife and Plant Conservation, Bangkok, as well as the guidelines of the involved institutes.
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Heesen, M., Rogahn, S., Macdonald, S. et al. Predictors of food-related aggression in wild Assamese macaques and the role of conflict avoidance. Behav Ecol Sociobiol 68, 1829–1841 (2014). https://doi.org/10.1007/s00265-014-1792-x
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DOI: https://doi.org/10.1007/s00265-014-1792-x