The Amboseli Baboon Research Project: 40 Years of Continuity and Change

Chapter

Abstract

In 1963, Jeanne and Stuart Altmann traveled through Kenya and Tanzania searching for a baboon study site. They settled on the Maasai-Amboseli Game Reserve (later Amboseli National Park) and conducted a 13-month study that laid the groundwork for much future research. They returned for a short visit in 1969, and came again in July 1971 to establish a research project that has persisted for four decades. In July 1984 Susan Alberts joined the field team, later becoming a graduate student and eventually a director. Over the years, we have tackled research questions ranging from feeding ecology to behavioral endocrinology, from kin recognition to sexual selection, and from aging research to functional genetics. A number of our results have explicitly depended upon the longitudinal nature of the research. Without decades worth of individual-based data we would not have known, for instance, that the presence of fathers influenced the maturation rates of their offspring, that maternal dominance rank had pervasive effects on the physiology of sons, or that the social behavior of a female influenced her infants’ survival. Here we summarize the major research themes that have characterized each of the past four decades, and our directions for the future, emphasizing the scientific insights that the longitudinal nature of the study has made possible.

Notes

Acknowledgments

We gratefully acknowledge the National Science Foundation for generous support over the years, most recently through DEB 0846286 and DEB 0919200 to S.C. Alberts, DEB 0846532 to J. Altmann, and IOS 1053461 to E. Archie. We are also very grateful for support from the National Institute of Aging (R01AG034513-01 and P01AG031719). We also thank the Princeton Center for the Demography of Aging (funded through P30AG024361), the Chicago Zoological Society, the Max Planck Institute for Demographic Research, the L.S.B. Leakey Foundation and the National Geographic Society for support at various times over the years.

We thank the Kenya Wildlife Services, Institute of Primate Research, National Museums of Kenya, and members of the Amboseli-Longido pastoralist communities for their cooperation and assistance in Kenya. A number of people, too numerous to list here, have contributed to the long-term data collection over the years, and we are grateful to all of them for their dedication and contributions. Particular thanks go to Stuart Altmann, the late Amy Samuels, and the Amboseli Baboon Project long-term field team (Raphael S. Mututua, Serah N. Sayialel, and J. Kinyua Warutere), as well as to Vera Somen and Tim Wango for their untiring assistance in Nairobi.

Karl Pinc has provided expertise in database design and management for many years and we are grateful for his seminal contributions to the development of Babase. We also thank the database technicians who have provided assistance with Babase over the years, most recently D. Onderdonk, C. Markham, T. Fenn, N. Learn, and L. Maryott. Our Amboseli research is approved by the IACUC at Princeton University and at Duke University and has adhered to all the laws and guidelines of Kenya.

References

  1. Alberts SC (in press) Magnitude and sources of variation in male reproductive performance. In: Mitani J, Call J, Kappeler PM, Palombit R, Silk JB (eds) The evolution of primate societies. University of Chicago Press, ChicagoGoogle Scholar
  2. Alberts SC, Altmann J (1995a) Preparation and activation: determinants of age at reproductive maturity in male baboons. Behav Ecol Sociobiol 36:397–406CrossRefGoogle Scholar
  3. Alberts SC, Altmann J (1995b) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306CrossRefGoogle Scholar
  4. Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821–840CrossRefGoogle Scholar
  5. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196CrossRefGoogle Scholar
  6. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  7. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Syst 34:517–547CrossRefGoogle Scholar
  8. Altmann SA (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann NY Acad Sci 102:338–435PubMedCrossRefGoogle Scholar
  9. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266PubMedCrossRefGoogle Scholar
  10. Altmann J (1979) Age cohorts as paternal sibships. Behav Ecol Sociobiol 6:161–164CrossRefGoogle Scholar
  11. Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge, MAGoogle Scholar
  12. Altmann SA (1991) Diets of yearling female primates (Papio cynocephalus) predict lifetime fitness. Proc Natl Acad Sci USA 88:420–423PubMedCrossRefGoogle Scholar
  13. Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, ChicagoGoogle Scholar
  14. Altmann J (2000) Models of outcome and process: predicting the number of males in primate groups. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 236–247Google Scholar
  15. Altmann J, Alberts SC (2003) Intraspecific variability in fertility and offspring survival in a nonhuman primate: behavioral control of ecological and social sources. In: Wachter KW, Bulatao RA (eds) Offspring: human fertility behavior in biodemographic perspective. National Academies Press, Washington, DC, pp 140–169Google Scholar
  16. Altmann J, Alberts SC (2004) Monitoring guide for the Amboseli baboon research project: protocols for long-term monitoring and data collection. http://www.princeton.edu/~baboon/monitoring_guide.htm
  17. Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501CrossRefGoogle Scholar
  18. Altmann SA, Altmann J (1970) Baboon ecology: African field research. University of Chicago Press, ChicagoGoogle Scholar
  19. Altmann J, Muruthi P (1988) Differences in daily life between semiprovisioned and wild-feeding baboons. Am J Primatol 15:213–221CrossRefGoogle Scholar
  20. Altmann J, Samuels A (1992) Costs of maternal care: infant carrying in baboons. Behav Ecol Sociobiol 29:391–398CrossRefGoogle Scholar
  21. Altmann J, Hausfater G, Altmann SA (1985) Demography of Amboseli baboons, 1963-1983. Am J Primatol 8:113–125CrossRefGoogle Scholar
  22. Altmann J, Altmann SA, Hausfater G (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 403–418Google Scholar
  23. Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Bruford MW (1996) Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93:5797–5801PubMedCrossRefGoogle Scholar
  24. Altmann J, Gesquiere L, Galbany J, Onyango PO, Alberts SC (2010) Life history context of reproductive aging in a wild primate model. Ann NY Acad Sci 1204:27–138CrossRefGoogle Scholar
  25. Beehner JC, Nguyen N, Wango EO, Alberts SC, Altmann J (2006) The endocrinology of pregnancy and fetal loss in wild baboons. Horm Behav 49:688–699PubMedCrossRefGoogle Scholar
  26. Bercovitch FB, Widdig A, Nürnberg P (2000) Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons. Behav Ecol Sociobiol 48:1–11CrossRefGoogle Scholar
  27. Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130:103–115PubMedCrossRefGoogle Scholar
  28. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999) DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys. Proc R Soc Lond B 266:901–904CrossRefGoogle Scholar
  29. Bronikowski AM, Alberts SC, Altmann J, Packer C, Carey KD, Tatar M (2002) The aging baboon: comparative demography in a non-human primate. Proc Natl Acad Sci USA 99:9591–9595PubMedCrossRefGoogle Scholar
  30. Bronikowski AM, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey AE, Stoinski T, Morris WF, Strier KB, Alberts SC (2011) Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331:1325–1328PubMedCrossRefGoogle Scholar
  31. Brunet-Rossinni AK, Austad SN (2006) Senescence in wild populations of mammals and birds. In: Masoro EJ, Austad SN (eds) Handbook of the biology of aging. Elsevier, Amsterdam, pp 243–266Google Scholar
  32. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425:179–181PubMedCrossRefGoogle Scholar
  33. Buchan JC, Archie EA, Van Horn RC, Moss CJ, Alberts SC (2005) Locus effects and sources of error in noninvasive genotyping. Mol Ecol Notes 5:680–683CrossRefGoogle Scholar
  34. Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103CrossRefGoogle Scholar
  35. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC (2008a) Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci USA 105:1988–1992PubMedCrossRefGoogle Scholar
  36. Charpentier MJE, Tung J, Altmann J, Alberts SC (2008b) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17:2026–2040PubMedCrossRefGoogle Scholar
  37. Clutton-Brock TH, Harvey PH (1977) Primate ecology and social organization. J Zool Lond 183:1–39CrossRefGoogle Scholar
  38. Clutton-Brock TH, Sheldon BC (2010) The seven ages of Pan. Science 327:1207–1208PubMedCrossRefGoogle Scholar
  39. Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056CrossRefGoogle Scholar
  40. Crook JH, Gartlan JS (1966) Evolution of primate societies. Nature 210:1200–1203PubMedCrossRefGoogle Scholar
  41. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  42. Fossey D (1979) Development of the mountain gorilla (Gorilla gorilla beringei): the first thirty-six months. In: Hamburg DA, McCown E (eds) Perspectives on human evolution, vol 5, The great apes. Benjamin, Cummings, Menlo Park, CA, pp 139–184Google Scholar
  43. Galbany J, Dotras L, Alberts SC, Pérez-Pérez A (2010) Tooth size variation related to age in Amboseli baboons. Folia Primatol 81:348–359PubMedGoogle Scholar
  44. Galbany J, Altmann J, Pérez-Pérez A, Alberts SC (2011) Age and individual foraging behavior predict tooth wear in Amboseli baboons. Am J Phys Anthropol 144:51–59PubMedCrossRefGoogle Scholar
  45. Gerloff U, Schlötterer C, Rassmann K, Rambold I, Hohmann G, Fruth B, Tautz D (1995) Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living bonobos (Pan paniscus). Mol Ecol 4:515–518CrossRefGoogle Scholar
  46. Gesquiere LR, Wango EO, Alberts SC, Altmann J (2007) Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51:114–125PubMedCrossRefGoogle Scholar
  47. Gesquiere LR, Khan M, Shek L, Wango TL, Wango EO, Alberts SC, Altmann J (2008) Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 54:410–416PubMedCrossRefGoogle Scholar
  48. Gesquiere LR, Onyango PO, Alberts SC, Altmann J (2011) Endocrinology of year-round reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 144:169–176PubMedCrossRefGoogle Scholar
  49. Gesquiere LR, Learn NH, Simao MCM, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: Rank and stress in wild male baboons. Science 333:357–360PubMedCrossRefGoogle Scholar
  50. Hall KRL, DeVore I (1965) Baboon social behavior. In: DeVore I (ed) Primate behavior: field studies of monkeys and apes. Holt, Rinehardt, and Winston, New York, pp 53–110Google Scholar
  51. Hausfater G (1975) Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. Karger, BaselGoogle Scholar
  52. Hausfater G, Altmann J, Altmann SA (1982) Long-term consistency of dominance relations among female baboons (Papio cynocephalus). Science 217:752–755PubMedCrossRefGoogle Scholar
  53. Höss M, Kohn M, Pääbo S, Knauer F, Schröder W (1992) Excrement analysis by PCR. Nature 359:199PubMedCrossRefGoogle Scholar
  54. Hrdy SB (1977) The langurs of Abu: female and male strategies of reproduction. Harvard University Press, Cambridge, MAGoogle Scholar
  55. Jay P (1963) Mother-infant relations in langurs. In: Rheingold HL (ed) Maternal behavior in mammals. Wiley, New York, pp 282–304Google Scholar
  56. Jolly CJ (1993) Species, subspecies, and baboon systematics. In: Kimbel WH, Martin LB (eds) Species, species concepts, and primate evolution. Plenum Press, New York, pp 67–107Google Scholar
  57. Kappeler PM, Port M (2008) Mutual tolerance or reproductive competition? Patterns of reproductive skew among male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 62:1477–1488CrossRefGoogle Scholar
  58. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley TM, Schumacher-Stankey JC, Wroblewski EE, Mosser A, Raphael J, Kamenya S, Lonsdorf EV, Travis DA, Mlengeya T, Kinsel MJ, Else JG, Silvestri G, Goodall J, Sharp PM, Shaw GM, Pusey AE, Hahn BH (2009) Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460:515–519PubMedCrossRefGoogle Scholar
  59. Khan MZ, Altmann J, Isani SS, Yu J (2002) A matter of time: evaluating the storage of fecal samples fo steroid analysis. Gen Comp Endocrinol 128:57–64PubMedCrossRefGoogle Scholar
  60. Kingdon J (1997) The Kingdon field guide to African mammals. Academic, LondonGoogle Scholar
  61. Kummer H (1968) Social organization of hamadryas baboons: a field study. University of Chicago Press, ChicagoGoogle Scholar
  62. Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60:695–706CrossRefGoogle Scholar
  63. Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104:7786–7790PubMedCrossRefGoogle Scholar
  64. Launhardt K, Borries C, Hardt C, Epplen JT, Winkler P (2001) Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Anim Behav 61:53–64PubMedCrossRefGoogle Scholar
  65. Lehmann J, Fickenscher G, Boesch C (2006) Kin biased investment in wild chimpanzees. Behaviour 143:931–955CrossRefGoogle Scholar
  66. Lynch JW, Khan MZ, Altmann J, Njahira MN, Rubenstein N (2003) Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation. Gen Comp Endocrinol 132:264–271PubMedCrossRefGoogle Scholar
  67. Melnick DJ, Pearl MC (1987) Cercopithecines in multimale groups: genetic diversity and population structure. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 121–134Google Scholar
  68. Ménard N, von Segesser F, Scheffrahn W, Pastorini J, Vallet D, Gaci B, Martin RD, Gautier-Hion A (2001) Is male-infant caretaking related to paternity and/or mating activities in wild barbary macaques (Macaca sylvanus)? Neurosciences 324:601–610Google Scholar
  69. Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol 63:1471–1482PubMedCrossRefGoogle Scholar
  70. Muruthi P, Altmann J, Altmann SA (1991) Resource base, parity, and reproductive condition affect females’ feeding time and nutrient intake within and between groups of a baboon population. Oecologia 87:467–472CrossRefGoogle Scholar
  71. Nelson RJ (2005) An introduction to behavioral endocrinology. Sinauer Associates, New YorkGoogle Scholar
  72. Newman TK, Jolly CJ, Rogers J (2004) Mitochondrial phylogeny and systematics of baboons (Papio). Am J Phys Anthropol 124:17–27PubMedCrossRefGoogle Scholar
  73. Nguyen N, Gesquiere LR, Wango EO, Alberts SC, Altmann J (2008) Late pregnancy glucocorticoid levels predict responsiveness in wild baboon mothers (Papio cynocephalus). Anim Behav 75:1747–1756CrossRefGoogle Scholar
  74. Nguyen N, Van Horn RC, Alberts SC, Altmann J (2009) “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol 63:1331–1344CrossRefGoogle Scholar
  75. Noë R (1986) Lasting alliances among adult male savannah baboons. In: Else JG, Lee PC (eds) Primate ontogeny, cognition and social behaviour. Cambridge University Press, Cambridge, pp 381–392Google Scholar
  76. Noë R (1992) Alliance formation among male baboons: shopping for profitable partners. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 285–321Google Scholar
  77. Noë R, Sluijter AA (1990) Reproductive tactics of male savanna baboons. Behaviour 113:117–170CrossRefGoogle Scholar
  78. Noë R, Sluijter AA (1995) Which adult male savanna baboons form coalitions? Int J Primatol 16:77–105CrossRefGoogle Scholar
  79. Nunn CL, Altizer S (2006) Infectious disease and primate social systems. In: Nunn CL, Altizer S (eds) Infectious diseases in primates: behavior, ecology, and evolution. Oxford University Press, New York, pp 176–213CrossRefGoogle Scholar
  80. Onyango PO, Gesquiere LR, Wango EO, Alberts SC, Altmann J (2008) Persistence of maternal effects in baboons: mother’s dominance rank at son’s conception predicts stress hormone levels in subadult males. Horm Behav 54:319–324PubMedCrossRefGoogle Scholar
  81. Ostner J, Heistermann M, Schülke O (2011) Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis). Horm Behav 59:105–113PubMedCrossRefGoogle Scholar
  82. Packer C, Collins DA, Eberly LE (2000) Problems with primate sex ratios. Philos Trans R Soc Lond B 355:1627–1635CrossRefGoogle Scholar
  83. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614PubMedCrossRefGoogle Scholar
  84. Paul A, Kuester J, Arnemann J (1992) Maternal rank affects reproductive success of male Barbary macaques (Macaca sylvanus): evidence from DNA fingerprinting. Behav Ecol Sociobiol 30:337–341Google Scholar
  85. Paul A, Kuester J, Arnemann J (1996) The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170CrossRefGoogle Scholar
  86. Pereira ME (1988a) Agonistic interactions of juvenile savanna baboons. I. Fundamental features. Ethology 79:195–217CrossRefGoogle Scholar
  87. Pereira ME (1988b) Effects of age and sex on intra-group spacing behaviour in juvenile savannah baboons, Papio cynocephalus cynocephalus. Anim Behav 36:184–204CrossRefGoogle Scholar
  88. Pereira ME (1989) Agonistic interactions of juvenile savanna baboons. II. Agonistic support and rank acquisition. Ethology 80:152–171CrossRefGoogle Scholar
  89. Pinc KO, Altmann J, Alberts SC (2009) Babase: Technical specifications for the Amboseli Baboon Project Data Management System. http://papio.biology.duke.edu/babase_system.html
  90. Port M, Kappeler PM (2010) The utility of reproductive skew models in the study of male primates, a critical evaluation. Evol Anthropol 19:46–56CrossRefGoogle Scholar
  91. Post DG (1981) Activity patterns of yellow baboons (Papio cynocephalus) in the Amboseli National Park, Kenya. Anim Behav 29:357–374CrossRefGoogle Scholar
  92. Pusey AE (1978) Age-changes in the mother-offspring association of wild chimpanzees. In: Chivers DJ, Herbert J (eds) Recent advances in primatology. Academic, London, pp 119–123Google Scholar
  93. Ransom TW, Ransom BS (1971) Adult male-infant relations among baboons (Papio anubis). Folia Primatol 16:179–195PubMedCrossRefGoogle Scholar
  94. Samuels A, Altmann J (1986) Immigration of a Papio anubis male into a group of Papio cynocephalus baboons and evidence for an anubis-cynocephalus hybrid zone in Amboseli, Kenya. Int J Primatol 7:131–138CrossRefGoogle Scholar
  95. Samuels A, Altmann J (1991) Baboons of the Amboseli basin: demographic stability and change. Int J Primatol 12:1–19CrossRefGoogle Scholar
  96. Samuels A, Silk JB, Altmann J (1987) Continuity and change in dominance relations among female baboons. Anim Behav 35:785–793CrossRefGoogle Scholar
  97. Sapolsky RM, Altmann J (1991) Incidence of hypercortisolism and dexamethasone resistance increases with age among wild baboons. Biol Psychiatr 30:1008–1016CrossRefGoogle Scholar
  98. Sapolsky RM, Alberts SC, Altmann J (1997) Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatr 54:1137–1143PubMedCrossRefGoogle Scholar
  99. Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698PubMedCrossRefGoogle Scholar
  100. Silk JB (1987) Social behavior in evolutionary perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 318–329Google Scholar
  101. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234PubMedCrossRefGoogle Scholar
  102. Silk JB, Alberts SC, Altmann J (2004) Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim Behav 67:573–582CrossRefGoogle Scholar
  103. Silk JB, Altmann J, Alberts SC (2006a) Social relationships among adult female baboons (Papio cynocephalus). I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61:183–195CrossRefGoogle Scholar
  104. Silk JB, Altmann J, Alberts SC (2006b) Social relationships among adult female baboons (Papio cynocephalus). II. Variation in the quality and stability of social bonds. Behav Ecol Sociobiol 61:197–204CrossRefGoogle Scholar
  105. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104CrossRefGoogle Scholar
  106. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361PubMedCrossRefGoogle Scholar
  107. Smith K, Alberts SC, Altmann J (2003) Wild female baboons bias their social behaviour towards paternal half-sisters. Proc R Soc Lond B 270:503–510CrossRefGoogle Scholar
  108. Smuts BB (1985) Sex and friendship in baboons. Aldine, Hawthorne, NYGoogle Scholar
  109. Stein DM (1984) The sociobiology of infant and adult male baboons. Ablex, Norwood, NJGoogle Scholar
  110. Stoltz LP, Saayman GS (1970) Ecology and behaviour of baboons in the northern Transvaal. Ann Transvaal Mus 26:99–143Google Scholar
  111. Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990PubMedCrossRefGoogle Scholar
  112. Struhsaker TT (1973) A recensus of vervet monkeys in the Masai-Amboseli Game Reserve, Kenya. Ecology 54:930–932CrossRefGoogle Scholar
  113. Strum SC (1982) Agonistic dominance in male baboons: an alternative view. Int J Primatol 3:175–202CrossRefGoogle Scholar
  114. Surbeck M, Mundry R, Hohmann G (2011) Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc R Soc Lond B 278:590–598CrossRefGoogle Scholar
  115. Tung J, Charpentier MJE, Garfield DA, Altmann J, Alberts SC (2008) Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population. Mol Ecol 17:1998–2011PubMedCrossRefGoogle Scholar
  116. Tung J, Primus A, Bouley AJ, Severson TF, Alberts SC, Wray GA (2009) Evolution of a malaria resistance gene in wild primates. Nature 460:388–391PubMedGoogle Scholar
  117. Tung J, Alberts SC, Wray GA (2010) Evolutionary genetics in wild primates: combining genetic approaches with field studies of natural populations. Trends Genet 26:353–362PubMedCrossRefGoogle Scholar
  118. Tung J, Akinyi MY, Mutura S, Altmann J, Wray GA, Alberts SC (2011) Allele-specific gene expression in a wild nonhuman primate population. Mol Ecol 20:725–739PubMedCrossRefGoogle Scholar
  119. Van Horn RC, Buchan JC, Altmann J, Alberts SC (2007) Divided destinies: group choice by female savannah baboons during social group fission. Behav Ecol Sociobiol 61:1823–1837CrossRefGoogle Scholar
  120. van Noordwijk MA, van Schaik CP (2001) Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138:359–395CrossRefGoogle Scholar
  121. van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144CrossRefGoogle Scholar
  122. van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evol Anthropol 5:152–156CrossRefGoogle Scholar
  123. Walters JR (1987) Transition to adulthood. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 358–369Google Scholar
  124. Wasser SK, Risler L, Steiner RA (1988) Excreted steroids in primate feces over the menstrual cycle and pregnancy. Biol Reprod 39:862–872PubMedCrossRefGoogle Scholar
  125. Watts DP (1997) Agonistic interventions in wild mountain gorilla groups. Behaviour 134:23–57CrossRefGoogle Scholar
  126. Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP (2003) Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140:405–427CrossRefGoogle Scholar
  127. Western D (2007) A half a century of habitat change in Amboseli National Park, Kenya. Afr J Ecol 45:302–310CrossRefGoogle Scholar
  128. Western D, Maitumo D (2004) Woodland loss and restoration in a savanna park: a 20-year experiment. Afr J Ecol 42:111–121CrossRefGoogle Scholar
  129. Western D, Sindiyo DM (1972) The status of the Amboseli rhino population. East Afr Wildl J 10:43–57CrossRefGoogle Scholar
  130. Western D, van Praet C (1973) Cyclical changes in the habitat and climate of an East African ecosystem. Nature 241:104–106CrossRefGoogle Scholar
  131. Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB (2001) Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc Natl Acad Sci USA 98:13769–13773PubMedCrossRefGoogle Scholar
  132. Wroblewski EE (2010) Paternity and father-offspring relationships in wild chimpanzees, Pan troglodytes schweinfurthii. PhD thesis, University of Minnesota, MinneapolisGoogle Scholar
  133. Ziegler TE, Santos CV, Pissinatti A, Strier KB (1997) Steroid excretion during the ovarian cycle in captive and wild muriquis, Brachyteles arachnoides. Am J Primatol 42:311–321PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA

Personalised recommendations