Cooperative relationships among male primates are emerging as an important aspect of primate social behavior. What remains unclear is the extent to which male associations with coresident males vary within species, and what social and demographic factors drive these associations. This information provides an important contribution to our understanding of how cooperative relationships play an adaptive role in the evolution of male social and reproductive strategies. To examine the nature of male associations and the influence of social and demographic factors, including rank and age, we collected 1751Â h of focal behavioral data on adult males in two large multimaleâmultifemale groups of mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. Both groups inhabited upland forest area, were of similar size and sex ratio, and exhibited strongly linear male hierarchies. Based on observed spatial associations within 3Â m proximity, dyadic patterns varied from strongly preferred to strongly avoided associations that were largely consistent among dyads over the study period. In contrast to reports from other mantled howler study sites, neither rank nor age differences among males predicted whether dyads spent any time in proximity to one another, nor the amount of time in proximity. However, higher-ranked males within dyads were more likely to maintain close proximity than their lower-ranked counterparts. Our results provide important data on the nature of male associations within mantled howler groups with linear dominance relationships, and are suggestive of the adaptive value of cooperative relationships.
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Adiseshan A., Adiseshan T., Isbell L.A. (2011). Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India. â Am. J. Primatol. 73: 1107-1113.
Altmann J. (1974). Observational study of behavior: sampling methods. â Behaviour 49: 227-267.
Altmann S. (1962). A field study of the sociobiology of the rhesus monkey, Macaca mulatta. â Ann. NY Acad. Sci. 102: 338-435.
Appleby M.C. (1983). The probability of linearity in hierarchies. â Anim. Behav. 31: 600-608.
Arroyo-RodrÃguez V., Asensio N., Cristóbal-Azkarate J. (2008). Demography, life history and migrations in a Mexican mantled howler group in a rainforest fragment. â Am. J. Primatol. 70: 114-118.
Bejder L., Fletcher D., Bräger S. (1998). A method for testing association patterns of social animals. â Anim. Behav. 56: 719-725.
Bercovitch F.B. (1988). Coalitions, cooperation and reproductive tactics among adult male baboons. â Anim. Behav. 36: 1198-1209.
Bezanson M., Garber P.A., Murphy J.T., Premo L.S. (2008). Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata). â Am. J. Primatol. 70: 282-293.
Breslow N.E., Clayton D.G. (1993). Approximate inference in generalized linear mixed models. â J. Am. Stat. Assoc. 88: 9-25.
Bshary R. (2010). Cooperation between unrelated individuals â a game theoretical approach. â In: Animal behaviour: evolution & mechanisms ( Kappeler P., ed.). Springer, Berlin, p. 213-240.
Carpenter C.R. (1965). The howlers of Barro Colorado Island. â In: Primate behavior: field studies of monkeys and apes ( DeVore I., ed.). Holt, Rinehart and Winston, New York, NY, p. 250-291.
Cheney D., Seyfarth R., Smuts B. (1986). Social relationships and social cognition in nonhuman primates. â Science 234: 1361-1366.
Chiarati E., Canestrari D., Vera R., Marcos J.M., Baglione V. (2010). Linear and stable dominance hierarchies in cooperative carrion crows. â Ethology 116: 346-356.
Clarke M.R. (1983). Infant-killing and infant disappearance following male takeovers in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. â Am. J. Primatol. 5: 241-247.
Clarke M.R. (1990). Behavioral development and socialization of infants in a free-ranging group of howling monkeys (Alouatta palliata). â Folia Primatol. 54: 1-15.
Clarke M.R., Glander K.E. (1984). Female reproductive success in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. â In: Female primates: studies by women primatologists ( Small M.F., ed.). Alan R. Liss, New York, NY, p. 111-126.
Clarke M.R., Glander K.E. (2005). Male tenure and reproductive success in single-male vs. multi-male groups of free-ranging howling monkeys in Costa Rica. â Neotrop. Prim. 13: 23-27.
Clarke M.R., Glander K.E. (2008). Natal emigration by both sexes in the La Pacifica population of mantled howlers: when do some stay? â Am. J. Primatol. 70: 195-200.
Clarke M.R., Glander K.E. (2010). Secondary transfer of adult mantled howlers (Alouatta palliata) on Hacienda La Pacifica, Costa Rica: 1975â2009. â Primates 51: 241-249.
Clarke M.R., Zucker E.L. (1994). Survey of the howling monkey population at La Pacifica: a seven-year follow-up. â Int. J. Primatol. 15: 61-73.
Clarke M.R., Zucker E.L., Scott N.J. (1986). Population trends of the mantled howler groups of La Pacifica, Guanacaste, Costa Rica. â Am. J. Primatol. 11: 79-88.
Clarke M.R., Zucker E.L., Glander K.E. (1994). Group takeover by a natal male howling monkey (Alouatta palliata) and associated disappearance and injuries of immatures. â Primates 35: 435-442.
Clarke M.R., Glander K.E., Zucker E.L. (1998). Infant-nonmother interactions of free-ranging mantled howlers (Alouatta palliata) in Costa Rica. â Int. J. Primatol. 19: 451-472.
Clutton-Brock T.H. (2009). Cooperation between non-kin in animal societies. â Nature 462: 51-57.
Colvin J. (1983). Familiarity, rank and the structure of rhesus male peer networks. â In: Primate social relationships: an integrated approach ( Hinde R.A., ed.). Blackwell Scientific, Oxford, p. 190-200.
Cooper M.A., Bernstein I.S. (2008). Evaluating dominance styles in Assamese and rhesus macaques. â Int. J. Primatol. 29: 225-243.
Corewyn L.C., Clarke M.R. (2012). Dominance in male mantled howlers (Alouatta palliata): association with age, immigration patterns and group history in two social groups at Hacienda La Pacifica, Costa Rica. â Am. J. Phys. Anthropol. 147(S34): 120.
Corewyn L.C., Clarke M.R., Glander K.E. (2011). Variation in male dominance relationships in two multimaleâmultifemale groups of mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. â Am. J. Primatol. 73(S1): 98.
Crockett C.M., Eisenberg J.F. (1987). Howlers: variations in group size and demography. â In: Primate societies ( Smuts B.B., Cheney D.L., Seyfarth R.W., Wrangham R.W., Struhsaker T.T., eds). University of Chicago Press, Chicago, IL, p. 54-68.
Crook J.H. (1970). The socio-ecology of primates. â In: Social behaviour in birds and mammals: essays on the social ethology of animals and man ( Crook J.H., ed.). Academic Press, London, p. 103-166.
Darwin C. (1859). On the origin of species by means of natural selection. â John Murray, London.
de Vries H. (1995). An improved test of linearity in dominance hierarchies containing unknown or tied relationships. â Anim. Behav. 50: 1375-1389.
de Vries H. (1998). Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. â Anim. Behav. 55: 827-843.
de Waal F.B.M. (2000). Primates â a natural heritage of conflict resolution. â Science 289: 586-590.
de Waal F.B.M., Brosnan S.F. (2006). Simple and complex reciprocity in primates. â In: Cooperation in primates and humans: mechanisms and evolution ( Kappeler P.M., van Schaik C.P., eds). Springer, Berlin, p. 85-105.
de Waal F.B.M., Luttrell L.M. (1988). Mechanisms of social reciprocity in three primate species: symmetrical relationship characteristics or cognition? â Ethol. Sociobiol. 9: 101-118.
de Waal F.B.M., Luttrell L.M. (1989). Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptail monkeys. â Am. J. Primatol. 19: 83-109.
Dias P.A.D., RodrÃguez Luna E.R. (2006). Seasonal changes in male associative behavior and subgrouping of Alouatta palliata on an island. â Int. J. Primatol. 27: 1635-1651.
Dias P.A.D., RodrÃguez Luna E., Canales Espinosa D. (2008). The functions of the âgreeting ceremonyâ among male mantled howlers (Alouatta palliata) on Agaltepec Island, Mexico. â Am. J. Primatol. 70: 621-628.
Dias P.A.D., Rangel-Negrin A., Vea J.J., Canales-Espinosa D. (2010). Coalitions and maleâmale behavior in Alouatta palliata. â Primates 51: 91-94.
Duffy K.G., Wrangham R.W., Silk J.B. (2007). Male chimpanzees exchange political support for mating opportunities. â Curr. Biol. 17: R686-R687.
Dugatkin L.A. (2002). Animal cooperation among unrelated individuals. â Naturwissenschaften 89: 533-541.
Emlen S.T., Oring L.W. (1977). Ecology, sexual selection, and the evolution of mating systems. â Science 197: 215-223.
Fedigan L.M., Fedigan L., Chapman C. (1985). A census of Alouatta palliata and Cebus capucinus in Santa Rosa National Park, Costa Rica. â Brenesia 23: 309-322.
Ford R.T. (2010). Sexual selection in mantled howling monkeys (Alouatta palliata), with an emphasis on the role of female mate choice. â PhD dissertation, Duke University, Raleigh/Durham, NC.
Garber P.A., Kowalewski M.K. (2011). Collective action and male affiliation in howler monkeys (Alouatta caraya). â In: Origins of altruism and cooperation ( Sussman R.W., Cloninger C.R., eds). Springer, New York, NY, p. 145-165.
Gardner W., Mulvey E.P., Shaw E.C. (1995). Regression analyses of counts and rates: Poisson, overdispersed Poisson, and negative binomial models. â Psychol. Bull. 118: 392-404.
Gilby I.C., Wrangham R.W. (2008). Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. â Behav. Ecol. Sociobiol. 62: 1831-1842.
Glander K.E. (1978). Howling monkey feeding behavior and plant secondary compounds: a study of strategies. â In: The ecology of arboreal folivores ( Montgomery G.G., ed.). Smithsonian Institution Press, Washington, DC, p. 561-574.
Glander K.E. (1981). Feeding patterns in mantled howling monkeys. â In: Foraging behavior: ecological, ethological, and psychological approaches ( Kamil A.C., Sargent T.D., eds). Garland, New York, NY, p. 231-257.
Glander K.E. (2006). Average body weight for mantled howling monkeys (Alouatta palliata): an assessment of average values and variability. â In: New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation ( Estrada A., Garber P.S., Pavelka M., Luecke L., eds). Springer, New York, NY, p. 247-263.
Glander K.E. (1980). Reproduction and population growth in free-ranging mantled howling monkeys. â Am. J. Phys. Anthropol. 53: 25-36.
Glander K.E. (1992). Dispersal patterns in Costa Rican mantled howling monkeys. â Int. J. Primatol. 13: 415-436.
Glander K.E., Nisbett R.A. (1996). Community structure and species density in tropical dry forest associations at Hacienda La Pacifica in Guanacaste Province, Costa Rica. â Brenesia 45-46: 113-142.
Glander K.E., Fedigan L.M., Fedigan L., Chapman C. (1991). Field methods for capture and measurement of three monkey species in Costa Rica. â Folia Primatol. 57: 70-82.
Grinnell J., Packer C., Pusey A.E. (1995). Cooperation in male lions: kinship, reciprocity or mutualism? â Anim. Behav. 49: 95-105.
Hamilton W.D. (1964). The genetical evolution of social behaviour. II. â J. Theor. Biol. 7: 17-52.
Hedeker D. (2005). Generalized linear mixed models. â In: Encyclopedia of statistics in behavioral science ( Everitt B.S., Howell D.C., eds). Wiley, Chichester, p. 729-738.
Henzi P., Barrett L. (2003). Evolutionary ecology, sexual conflict, and behavioral differentiation among baboon populations. â Evol. Anthropol. 12: 217-230.
Hinde R.A., Atkinson S. (1970). Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. â Anim. Behav. 18: 169-176.
Holdridge L.R. (1967). Life zone ecology. â Tropical Science Center, San Jose.
Jack K.M. (2003). Explaining variation in affiliative relationships among male white-faced capuchins (Cebus capucinus). â Folia Primatol. 74: 1-16.
Janzen D.H. (1986). Guanacaste National Park: tropical, ecological and cultural restoration. â Editorial Universidad Estatal A Distancia, San Jose.
Jones C.B. (1979). Grooming in the mantled howler monkey, Alouatta palliata Gray. â Primates 20: 289-292.
Jones C.B. (1985). Reproductive patterns in mantled howler monkeys: estrus, mate choice and copulation. â Primates 26: 130-142.
Jones C.B. (1995). Alternative reproductive behaviors in the mantled howler monkey (Alouatta palliata Gray): testing Carpenterâs hypothesis. â Bol. Primatol. Lat. 5: 1-5.
Jones C.B. (1980). The functions of status in the mantled howler monkey, Alouatta palliata Gray: intraspecific competition for group membership in a folivorous Neotropical primate. â Primates 21: 389-405.
Jones C.B., Cortés-Ortiz L. (1998). Facultative polyandry in the howling monkey (Alouatta palliata): Carpenter was correct. â Bol. Primatol. Lat. 7: 1-7.
Kelaita M., Dias P.A.D., Aguilar-Cucurachi M.D.S., Canales-Espinosa D., Cortés-Ortiz L. (2011). Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. â Am. J. Phys. Anthropol. 146: 179-187.
Kitchen D.M., Horwich R.W., James R.A. (2004). Subordinate male black howler monkey (Alouatta pigra) responses to loud calls: experimental evidence for the effects of intra-group male relationships and age. â Behaviour 141: 703-723.
Kummer H. (1971). Spacing mechanisms in social behavior. â Soc. Sci. Inform. 9: 109-122.
Landau H.G. (1951). On dominance relations and the structure of animal societies: I. Effect of inherent characteristics. â B. Math. Biophys. 18: 1-19.
Langengraber K.E., Mitani J.C., Vigilant L. (2007). The limited impact of kinship on cooperation in wild chimpanzees. â Proc. Natl. Acad. Sci. USA 104: 7786-7790.
Lehner P.N. (1996). Handbook of ethological methods, 2nd edn. â Cambridge University Press, Cambridge.
Lott D.F. (1984). Intraspecific variation in the social systems of wild vertebrates. â Behaviour 88: 266-325.
Martin P., Bateson P. (1993). Measuring behaviour: an introductory guide, 2nd edn. â Cambridge University Press, Cambridge.
Massen J.J.M., Overduin-de Vries A.M., de Vos-Rouweler A.J.M., Spruijt B.M., Doxiadis G.G.M., Sterck E.H.M. (2012). Male mating tactics in captive rhesus macaques (Macaca mulatta): the influence of dominance, markets, and relationship quality. â Int. J. Primatol. 33: 73-92.
Milton K. (1998). Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. â Int. J. Primatol. 19: 513-548.
Milton K. (1980). The foraging strategy of howler monkeys: a study in primate economics. â Columbia University Press, New York, NY.
Milton K., Lozier J.D., Lacey E.A. (2009). Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. â Conserv. Genet. 10: 347-358.
Mitani J.C. (2009). Male chimpanzees form enduring and equitable social bonds. â Anim. Behav. 77: 633-640.
Mitani J.C., Watts D.P., Pepper J.W., Merriwether D.A. (2002). Demographic and social constraints on male chimpanzee behaviour. â Anim. Behav. 64: 727-737.
Newton-Fisher N.E. (1999). Association by male chimpanzees: a social tactic? â Behaviour 136: 705-730.
Nunn C.L. (1999). The number of males in primate groups: a comparative test of the socioecological model. â Behav. Ecol. Sociobiol. 46: 1-13.
Nunn C.L. (2000). Collective benefits, free-riders, and male extra-group conflict. â In: Primate males: causes and consequences of variation in group composition ( Kappeler P.M., ed.). Cambridge University Press, Cambridge, p. 192-204.
Olendorf R., Getty T., Scribner K. (2004). Cooperative nest defence in red-winged blackbirds: reciprocal altruism, kinship or by-product mutualism? â Proc. Roy. Soc. Lond. B: Biol. Sci. 271: 177-182.
Pepper J.W., Mitani J.C., Watts D.P. (1999). General gregariousness and specific social preferences among wild chimpanzees. â Int. J. Primatol. 20: 613-632.
Perry S. (1998). Maleâmale social relationships in wild white-faced capuchins, Cebus capucinus. â Behaviour 135: 139-172.
Plavcan J.M. (2001). Sexual dimorphism in primate evolution. â Yb. Phys. Anthropol. 44: 25-53.
Pope T.R. (1990). The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers. â Behav. Ecol Sociobiol. 27: 439-446.
Riley E.P. (2010). Maleâmale affiliation in Sulawesi tonkean macaques. â In: Indonesian primates ( Gursky-Doyen S., Supriatna J., eds). Springer, New York, NY, p. 257-268.
Schülke O., Bhagavatula J., Vigilant L., Ostner J. (2010). Social bonds enhance reproductive success in male macaques. â Curr. Biol. 20: 2207-2210.
Silk J.B. (1994). Social relationships of male bonnet macaques: male bonding in a matrilineal society. â Behaviour 130: 271-291.
Silk J.B. (2002). Using the âFâ-word in primatology. â Behaviour 139: 421-446.
Silk J.B. (2007). The adaptive value of sociality in mammalian groups. â Philos. Trans. Roy. Soc. B 362: 539-559.
Sokal R.R., Rohlf F.J. (1995). Biometry, 3rd edn. â W.H. Freeman, New York, NY.
Strier K.B. (1994). Brotherhoods among atelins: kinship, affiliation, and competition. â Behaviour 130: 151-167.
Strier K.B. (2009). Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. â Curr. Anthropol. 50: 213-228.
Strier K.B. (2011). Social plasticity and demographic variation in primates. â In: Origins of altruism and cooperation ( Sussman R.W., Cloninger C.R., eds). Springer, New York, NY, p. 179-192.
Sussman R.W., Cloninger C.R. (2011). Introduction: cooperation and altruism. â In: Origins of altruism and cooperation ( Sussman R.W., Cloninger C.R., eds). Springer, New York, NY, p. 1-7.
Sussman R.W., Garber P.A. (2011). Cooperation, collective action, and competition in primate social interactions. â In: Primates in perspective, 2nd edn. ( Campbell C.J., Fuentes A., MacKinnon K.C., Bearder S.K., Stumpff R.M., eds). Oxford University Press, New York, NY, p. 587-599.
Sussman R.W., Garber P.A., Cheverud J.M. (2005). Importance of cooperation and affiliation in the evolution of primate sociality. â Am. J. Phys. Anthropol. 128: 84-97.
Trivers R.L. (1972). Parental investment and sexual selection. â In: Sexual selection and the descent of man, 1871â1971 ( Campbell B., ed.). Aldine, Chicago, IL, p. 136-179.
Van Belle S., Estrada A., Strier K.B. (2008). Social relationships among male Alouatta pigra. â Int. J. Primatol. 29: 1481-1498.
van Hooff J.A.R.A.M., van Schaik C.P. (1992). Cooperation in competition: the ecology of primate bonds. â In: Coalitions and alliances in humans and other animals ( Harcourt A.H., de Waal F.B.M., eds). Oxford University Press, New York, NY, p. 357-389.
van Hooff J.A.R.A.M., van Schaik C.P. (1994). Male bonds: affiliative relationships among nonhuman primate males. â Behaviour 130: 309-337.
van Schaik C.P. (1989). The ecology of social relationships amongst female primates. â In: Comparative socioecology: the behavioral ecology of humans and other mammals ( Standen V., Foley R.A., eds). Blackwell, Oxford, p. 195-218.
van Schaik C.P. (1996). Social evolution in primates: the role of ecological factors and male behavior. â Proc. Br. Acad. 88: 9-31.
van Schaik C.P., Kappeler P.M. (2006). Cooperation in primates and humans: closing the gap. â In: Cooperation in primates and humans: mechanisms and evolution ( Kappeler P.M., van Schaik C.P., eds). Springer, Berlin, p. 3-21.
Wang E., Milton K. (2003). Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. â Int. J. Primatol. 24: 1227-1243.
West S.A., Griffin A.S., Gardner A. (2007). Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. â J. Evol. Biol. 20: 415-432.
Whitehead H. (2009). SOCPROG programs: analyzing animal social structures. â Behav. Ecol. Sociobiol. 63: 765-778.
Wiszniewski J., Brown C., Müller L.M. (2012). Complex patterns of male alliance formation in a dolphin social network. â J. Mammal. 93: 239-250.
Zucker E.L., Clarke M.R. (1992). Developmental and comparative aspects of social play of mantled howling monkeys in Costa Rica. â Behaviour 123: 144-171.
Zucker E.L., Clarke M.R. (1998). Agonistic and affiliative relationships of adult female howlers (Alouatta palliata) in Costa Rica over a 4-year period. â Int. J. Primatol. 19: 433-449.
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Cooperative relationships among male primates are emerging as an important aspect of primate social behavior. What remains unclear is the extent to which male associations with coresident males vary within species, and what social and demographic factors drive these associations. This information provides an important contribution to our understanding of how cooperative relationships play an adaptive role in the evolution of male social and reproductive strategies. To examine the nature of male associations and the influence of social and demographic factors, including rank and age, we collected 1751Â h of focal behavioral data on adult males in two large multimaleâmultifemale groups of mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. Both groups inhabited upland forest area, were of similar size and sex ratio, and exhibited strongly linear male hierarchies. Based on observed spatial associations within 3Â m proximity, dyadic patterns varied from strongly preferred to strongly avoided associations that were largely consistent among dyads over the study period. In contrast to reports from other mantled howler study sites, neither rank nor age differences among males predicted whether dyads spent any time in proximity to one another, nor the amount of time in proximity. However, higher-ranked males within dyads were more likely to maintain close proximity than their lower-ranked counterparts. Our results provide important data on the nature of male associations within mantled howler groups with linear dominance relationships, and are suggestive of the adaptive value of cooperative relationships.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 433 | 40 | 6 |
| Full Text Views | 222 | 5 | 0 |
| PDF Views & Downloads | 91 | 12 | 0 |