Abstract
Primates show life history traits similar to those of cetaceans, such as small litter size, long gestation, long lactation, and long lifespan, in spite of striking contrasts in habitats, diet, mobility, and range size between them. Ecological factors (food and predation) may influence their life history traits in various ways, but social factors (social structure and reproductive strategies) may be more important for the life history of primates, in which both sexes live together even outside the breeding season. Group-living primates are classified into female-bonded species and female-dispersal species, based on the patterns of female dispersal after maturity. A comparison of life history parameters shows that female-dispersal species have a slower life history (gestation length, weaning age, age at first reproduction, and interbirth interval) than the female-bonded species, except for neonatal weight and weaning weight, which may be determined in relationship to female body weight. To elucidate factors promoting the slow life history, we focus on Atelinae and Hominidae (female-dispersal species) and examine their interspecific and intraspecific variation in social structure and male reproductive tactics in relationship to life history traits. Most Atelinae species form multimale and multifemale groups, and variation in their life history features may reflect relationships among males and their reproductive tactics. In howler monkeys, both males and females disperse, and infanticide by males may lead to a fast life history. In other Atelines, infanticide rarely occurs, although it has the effect of reducing interbirth interval. Forcible copulation by males occasionally occurs in spider monkeys. Variations in grouping among females reflecting their flexible foraging efforts according to distribution of high-quality foods may have some effects on the fast–slow continuum in the life history features of female Atelinae. Hominidae exhibit larger variations in life history features than Atelinae, probably because of their diverse social structure. Solitary nature and male reproductive tactics may have great influences on the life history of female great apes. Female orangutans, who usually live a solitary life, show the slowest life history. Maturing female orangutans need a longer time to establish their own home range and relationships with reproductive mates than female chimpanzees and gorillas, who transfer into other groups immediately after emigration. Female gorillas show the lowest age at first reproduction and the shortest interbirth interval. Intensive caretaking of the immature by male gorillas may facilitate early weaning, and infanticide by males may promote a prolonged bonding between a protector male and females to shorten the interbirth interval. Similar life history traits have been found in four long-term study sites of chimpanzees. Only females at Bossou show a fast life history, probably the result of high-quality foods and single male group composition under isolated conditions. The more frequent and stable association between females and males and more promiscuous mating in bonobos may facilitate the search for mating partners and lead to a shorter interbirth interval than chimpanzees. Frugivorous orangutans and chimpanzees may suffer more costs of female dispersal through decreased foraging efficiency than folivorous gorillas, and chimpanzees with fission–fusion grouping may suffer more social stress than gorillas in highly cohesive groups. Such differences may generally shape the fast–slow continuum of life history in female-dispersal primate species.
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References
Agoramoorthy G, Rudran R (1995) Infanticide by adult and subadult males in free-ranging red howler monkeys of Venezuela. Ethology 99:75–88
Allman JM, McLaughlin T, Hakeem A (1993) Brain weight and life-span in primate species. Proc Natl Acad Sci USA 90:118–122
Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409
Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savanna baboons. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 403–418
Anderson HB, Emery Thompson M, Knott M, Perkins CD (2008) Fertility and mortality patterns of Bornean and Sumatran orangutans: is there a species difference in life history? J Hum Evol 54:34–42
Arcadi AC, Wrangham RW (1999) Infanticide in chimpanzees: review of cases and a new within-group observation from the Kanyawara study group in Kibale National Park. Primates 40:337–351
Barton RA, Byrne RW, Whiten A (1996) Ecology, feeding competition, and social structure in baboons. Bahav Ecol Sociobiol 38:321–329
Bermejo M (2004) Home-range use and intergroup encounters in western gorillas (Gorilla g. gorilla) at Lossi Forest, North Congo. Am J Primatol 64:223–232
Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour 117:220–242
Boesch C, Boesch-Achermann H (2000) The chimpanzees of Tai Forest. Cambridge University Press, Cambridge
Borries C, Koenig A, Winkler P (2001) Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behav Ecol Sociobiol 50:391–402
Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L (2004) Dispersed male networks in western gorillas. Curr Biol 14:510–513
Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N, Boesch C, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102:9418–9423
Breuer T, Breuer-Ndoundou Hockemba M, Olejniczak C, Parnell RJ, Stokes EJ (2009) Physical maturation, life-history classes and age estimates of free-ranging western gorillas: insights from Mbeli Bai, Republic of Congo. Am J Primatol 71:106–119
Campbell CJ (2003) Female directed aggression in free-ranging Ateles geoffroyi. Int J Primatol 24:223–238
Campbell (2006) Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi). Am J Primatol 68:1197–1201
Charnov EL (1991) Evolution of life history variation among female mammals. Proc Natl Acad Sci USA 88:1134–1137
Charnov EL (1993) Life history invariants: some explorations of symmetry in evolutionary ecology. Oxford University Press, Oxford
Cheney DL, Seyfarth RM, Andleman S, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago
Connor RC, Wells R, Mann J, Read A (2000) The bottlenose dolphin: social relationships in a fission–fusion society. In: Mann J, Connor R, Tyack P, Whitehead H (eds) Cetacean societies: field studies of whales and dolphins. University of Chicago Press, Chicago, pp 91–126
Constable JL, Ashley MV, Goodall J, Pusey AE (2001) Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279–1300
Crockett CM, Janson CH (2000) Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 75–98
Crockett CM, Pope TR (1993) Consequences of sex differences in dispersal for juvenile red howler monkeys. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, Oxford, pp 104–118
Crockett CM, Rudran R (1987) Red howler monkey birth data. II: Interannual, habitat, and sex comparisons. Am J Primatol 13:369–384
Crockett CM, Seklic R (1984) Infanticide in red howler monkeys (Alouatta seniculus). In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine De Gruyter, New York, pp 173–191
Delgado R, van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218
Doran DM, Jungers WL, Sugiyama Y, Fleagle JG, Heesy CP (2002) Multivariate and phylogenetic approaches to understanding chimpanzee and bonobo behavioral diversity. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 14–34
Drickamer LC (1974) A ten-year summary of reproductive data for free ranging Macaca mulatta. Folia Primatol 21:61–80
Dunbar RIM (1988) Primate social system. Helm, London
Eisenberg JF (1981) The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. Chicago University Press, Chicago
Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 40:553–562
Fedigan LM, Rose LM (1995) Inter-birth interval variation in three sympatric species of Neotropical monkey. Am J Primatol 37:9–24
Fletcher A (2001) Development of infant independence from the mother in wild mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, London, pp 153–182
Fossey D (1979) Development of the mountain gorilla (Gorilla gorilla beringei): the first thirty-six months. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 138–184
Fossey D (1984) Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine, Hawthorne, pp 217–236
Furuichi T (1987) Sexual swelling, receptivity and grouping of wild pygmy chimpanzee females at Wamba, Zaire. Primates 28:309–318
Furuichi T (1997) Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 18:855–875
Furuichi T, Hashimoto C (2002) Why female bonobos have a lower copulation rate during estrus than chimpanzees. In: Boesch C, Hohmann G, Marchant LF (eds) Behavioral diversity in chimpanzees and bonobos. Cambridge University Press, New York, pp 156–167
Furuichi T, Idani G, Ihobe H, Kuroda S, Kitamura K, Mori A, Enomoto T, Okayasu N, Hashimoto C, Kano T (1998) Population dynamics of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 19:1029–1043
Galdikas BMF (1984) Adult female sociality among wild orangutans at Tanjung Putting Reserve. In: Small MF (ed) Female primates: studies by women primatologists. Liss, New York, pp 217–235
Galdikas BMF (1985) Orangutan sociality at Tanjung Putting, Central Borneo. Int J Primatol 9:1–35
Gibson KN, Vick LG, Palma AC, Carrasco FM, Taub D, Ramos-Fernandez G (2008) Intra-community infanticide and forced copulation in spider monkeys: a multi-site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico. Am J Primatol 70:485–489
Goldsmith ML (1999) Ecological constraints on the foraging effort of western gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Int J Primatol 20:1–23
Goodall J (1977) Infant killing and cannibalism in free-living chimpanzees. Folia Primatol (Basel) 28:259–282
Goodall J (1986) The chimpanzees of Gombe. Belknap, Cambridge
Goodall J, Bandora A, Bergmann E, Busse C, Matama H, Mpongo E, Pierce A, Riss D (1979) Intercommunity interactions in the chimpanzee population of the Gombe National Park. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 13–53
Gouzoules H, Gouzoules S, Fedigan LM (1982) Behavioral dominance and reproductive success in female Japanese monkeys (Macaca fuscata). Anim Behav 30:1138–1190
Hamai M, Nishida T, Takasaki H (1992) New records of within-group infanticide and cannibalism in wild chimpanzees. Primates 33:151–162
Harcourt AH (1992) Coalitions and alliances: are primates more complex than non-primates? In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in human and other animals. Oxford University Press, Oxford, pp 445–472
Harcourt AH, Stewart KJ (2007) Gorilla society: conflict, compromise and cooperation between the sexes. University of Chicago Press, Chicago
Harvey PH, Purvis A (1999) Understanding the ecological and evolutionary reasons for life history variation: mammals as a case study. In: McGlade J (ed) Advanced ecological theory: principles and applications. Blackwell, Oxford, pp 232–248
Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 181–196
Hasegawa T (1989) Sexual behavior of immigrant and resident female chimpanzees at Mahale. In: Heltne PG, Marquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 90–103
Hasegawa T, Hiraiwa-Hasegawa M (1983) Opportunistic and restrictive mating among wild chimpanzees in the Mahale Mountains, Tanzania. J Ethol 1:75–85
Hashimoto C, Tashiro Y, Hibino E, Mulabwa M, Yangonze K, Furuichi T, Idani G, Takenaka O (2008) Longitudinal structure of a unit-group of bonobos: male philopatry and possible fusion of unit-groups. In: Furuichi T, Thompson J (eds) The bonobos: behavior, ecology, and conservation. Springer, New York, pp 107–119
Henzi P, Barrett L (1999) The value of grooming to female primates. Primates 40:47–59
Henzi P, Barrett L (2003) Evolutionary ecology, sexual conflict, and behavioral differentiation among baboon populations. Evol Anthropol 12:217–230
Herbinger L, Boesch C, Rothe H (2001) Territory characteristics among three neighboring chimpanzee communities in the Tai National Park, Ivory Coast. Int J Primatol 32:143–167
Hohmann G, Gerloff U, Tautz D, Fruth B (1999) Social bonds and genetic ties: kinship, association, and affiliation in a community of bonobos (Pan paniscus). Behaviour 136:1219–1235
Idani G (1990) Relations between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions. Afr Stud Monogr 11:153–186
Idani G (1991) Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol (Basel) 57:83–95
Inoue E, Inoue-Murayama M, Vigilant L, Takenaka O, Nishida T (2008) Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors. Am J Phys Anthropol 137:256–262
Itoigawa N, Tanaka T, Ukai N, Fujii H, Kurokawa T, Koyama T, Ando A, Watanabe Y, Imakawa S (1992) Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) in Katsuyama. Primates 33:49–68
Janson CH, van Schaik CP (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: development and behavior. Oxford University Press, Oxford, pp 57–74
Jones KE, MacLarnon A (2001) Bat life histories: testing models of mammalian life history evolution. Evol Ecol Res 3:465–476
Kano T (1989) The sexual behavior of pygmy chimpanzees. In: Heltne PG, Marcquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 176–183
Kano T (1992) The last ape: pygmy chimpanzee behavior and ecology. Stanford University Press, Stanford
Kappeler PM, Pereira ME (eds) (2003) Primate life history and socioecology. University of Chicago Press, Chicago
Kappeler PM, Pereira ME, van Schaik CP (2003) Primate life histories and socioecology. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. Chicago University Press, Chicago, pp 1–23
Kasuya T (1995) Overview of cetacean life histories. In: Blix AS, Walløe, Ulltang Ø (eds) Whales, seals, fish and man: proceedings of the international symposium on the biology of marine mammals in the northeast Atlantic, Tromsø, Norway, 29 November–1 December 1994. Elsevier, Amsterdam, pp 481–497
Kasuya T, Jones LL (1984) Behavior and segregation of the Dall’s porpoise in the northwestern North Pacific Ocean. Sci Rep Whales Res Inst 35:107–128
Kasuya T, Balcomb K, Brownell RL Jr (1997) Life history of Baird’s whales off the Pacific coast of Japan. Rep Int Whaling Comm 47:969–979
Kirschofer R (1987) International studbook of the gorilla, Gorilla gorilla, 1985. Frankfurt Zoological Garden, Frankfurt
Kitamura K (1989) Genito-genital contacts in the pygmy chimpanzee (Pan paniscus). Afr Stud Monogr 10:46–67
Knott CD (2001) Female reproductive ecology of the apes: implications for human evolution. In: Ellison PT (ed) Reproductive ecology and human evolution. de Gruyter, New York, pp 429–463
Knott CD, Kahlenberg SM (2007) Orangutans in perspective. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Beader SK (eds) Primates in perspective. Oxford University Press, New York, pp 290–305
Knott CD, Thompson ME, Wich SA (2009) The ecology of female reproduction in wild orangutans. In: Wich SA, Utami SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographical variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 171–188
Kuroda S (1980) Social behavior of the pygmy chimpanzees. Primates 21:181–197
Kuroda S (1989) Developmental retardation and behavioral characteristics of pygmy chimpanzees. In: Heltne PG, Marquardt AE (eds) Understanding chimpanzees. Chicago Academy of Sciences, Chicago, pp 184–193
Kuze N, Sipangkui S, Malim T, Bernard H, Ambu L, Kohshima S (2008) Reproductive parameters over a 37-year period of free-ranging female Borneo orangutans at Sepilok Orangutan Rehabilitation Centre. Primates 49:126–134
Kuze N, Dellatore D, Banes GL, Pratje P, Tajima T, Russon AE (2012) Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval. Primates 53:181–192
Lee PC (1996) The meaning of weaning: growth, lactation, and life history. Evol Anthropol 5:87–96
Lee PC, Majluf P, Gordon IJ (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool 225:99–114
Lehman J, Boesch C (2003) Social influences on ranging patterns among chimpanzees (Pan troglodytes verus) in the Tai National Park, Cote d’Ivoire. Behav Ecol 14(5):642–649
Lehmann J, Boesch C (2008) Sexual differences in chimpanzee sociality. Int J Primatol 29:65–81
Mann J, Smuts BB (1999) Behavioral development of wild bottlenose dolphin newborns. Behaviour 136:529–566
Mann J, Connor RC, Barre LM, Heithaus MR (2000) Female reproductive success in wild bottlenose dolphins (Tursiops sp.): life history, habitat, provisioning, and group size effects. Behav Ecol 11:210–219
Marsden BS, Marsden D, Thompson EM (2006) Demographic and female life history parameters of free-ranging chimpanzees at the chimpanzee rehabilitation project, River Gambia National Park. Int J Primatol 27:391–410
Martin RD (1995) Phylogenetic aspects of primate reproduction: the context of advanced maternal care. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 16–26
Martin RD (1996) Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:149–156
Martin AR, Rothery P (1993) Reproductive parameters of female long-finned pilot whales (Globicephala melas) around the Faroe Islands. In: Donovan GP, Lockyer CH, Martin AR (eds) Biology of northern hemisphere pilot whales: a collection of papers. Reports of the International Whaling Commission, Special Issue 14. International Whaling Commission, Cambridge, pp 263–304
Miyazaki N, Nishiwaki M (1978) School structure of the striped dolphin off the Pacific coast of Japan. Sci Rep Whales Res Inst 30:65–115
Muller MN (2007) Chimpanzee violence: femmes fatales. Curr Biol 17:365–366
Newton-Fisher NE, Thompson ME, Reynolds V, Boesch C, Vigilant L (2010) Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. Am J Phys Anthropol 142:417–428
Nishida T (1979) The social structure of chimpanzees of Mahale Mountains. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 73–121
Nishida T, Hiraiwa-Hasegawa M, Hasegawa T, Takahata Y (1985) Group extinction and female transfer in wild chimpanzees in the Mahale Mountains. Z Tierpsychol 67:284–301
Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59:99–121
Nishimura A (1994) Social interaction patterns of woolly monkeys (Lagothrix lagothricha): a comparison among the atelines. Sci Eng Rev Doshisha Univ 35(2):235–254
Nishimura A (2003) Reproductive parameters of wild female Lagothrix lagotricha. Int J Primatol 24:707–722
Nunn CL, Pereira ME (2000) Group histories and offspring sex ratios in ringtailed lemurs (Lemur catta). Behav Ecol Sociobiol 48:18–28
Oftedal OT (1997) Lactation in whales and dolphins: evidence of divergence between baleen- and toothed-species. J Mamm Gland Biol Neoplasia 2:205–230
Parish AR (1994) Sex and food control in the “uncommon chimpanzee:” how bonobo females overcome a phylogenetic legacy of male dominance. Ethol Sociobiol 15:157–179
Paul A, Kuester J (1996) Differential reproduction in male and female Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 293–317
Paul A, Preuchoft S, van Schaik CP (2000) The other side of the coin: infanticide and the evolution of affiliative male–infant interactions in Old World primates. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 269–292
Printes RC, Strier KB (1999) Behavioral correlates of dispersal in female muriquis (Brachyteles arachnoides). Int J Primatol 20:941–960
Purvis A, Harvey PH (1995) Mammalian life history evolution: a comparative test for Charnov’s model. J Zool 237:259–283
Purvis A, Webster AJ, Agapow P-M, Jones KE, Isaac NJB (2003) Primate life histories and phylogeny. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. Chicago University Press, Chicago, pp 25–40
Pusey AE (1980) Inbreeding avoidance in chimpanzees. Anim Behav 28:543–552
Read AF, Harvey PH (1989) Life history differences among the eutherian radiations. J Zool 219:329–353
Robbins MM (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47
Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020
Robbins MM (2001) Variation in the social system of mountain gorillas: the male perspective. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 29–58
Robbins AM, Robbins MM (2005) Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 58:295–309
Robbins MM, Bermejo M, Cipolletta C, Magliocca F, Parnell RJ, Stokes E (2004) Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol 64:145–159
Robbins AM, Stoinski TS, Fawsett KA, Robbins MM (2009) Socioecological influences on the dispersal of female mountain gorillas: evidence of a second folivore paradox. Behav Ecol Sociobiol 63:477–489
Rodman PS, Mitani JC (1987) Orangutans: sexual dimorphism in a solitary species. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 146–154
Rosenberger AL, Strier KB (1989) Adaptive radiation of the ateline primates. J Hum Evol 18:717–750
Ross C (1992) life history patterns and ecology of macaque species. Primates 33:207–215
Ross C (1998) Primate life histories. Evol Anthropol 6:54–63
Ross C, MacLarnon A (1995) Ecological and social correlates of maternal expenditure on infant growth in haplorhine primates. In: Pryce C, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates: biological and social determinants. Karger, Basel, pp 37–46
Schaller GB (1963) The mountain gorilla: ecology and behavior. University of Chicago Press, Chicago
Shane SH, Wells RS, Wursig B (1986) Ecology, behavior and social organization of the bottlenose dolphin: a review. Mar Mamm Sci 2:34–63
Shimooka Y (2005) Sexual differences in ranging of Ateles belzebuth belzebuth at La Macarena, Colombia. Int J Primatol 26:385–406
Shimooka Y, Campbell CJ, Di Fiore A, Felton AM, Izawa K, Link A, Nishimura A, Ramos-Fernandez G, Wallace RB (2008) Demography and group composition of Ateles. In: Campbell CJ (ed) Spider monkeys: behavior, ecology, and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 329–348
Silk J (1982) Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour 79:162–168
Silk J (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 318–329
Sivert J, Karesh WB, Sunde V (1991) Reproductive intervals in captive female western lowland gorillas with a comparison to wild mountain gorillas. Am J Primatol 24:227–234
Stanford CB (1992) Costs and benefits of allomothering in wild capped langurs (Presbytes pileata). Behav Ecol Sociobiol 30:29–34
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Steenbeck R (2000) Infanticide by males and female choice in wild Thomas’s langurs. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 153–177
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309
Stewart KJ (2001) Social relationships of immature gorillas and silverbacks. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, London, pp 183–214
Stewart KJ, Harcourt AH (1987) Gorillas: variation in female relationships. In: Smuts B, Cheney D, Seyfarth R, Wrangham RW, Struhsaker T (eds) Primate societies. University of Chicago Press, Chicago, pp 155–164
Stokes EJ (2004) Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol 64:233–246
Stokes EJ, Parnell RJ, Olejniczak C (2003) Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav Ecol Sociobiol 54:329–339
Strier KB (1992) Ateline adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524
Strier KB (1999a) The atelines. In: Dolhinow P, Fuentes A (eds) The nonhuman primates. Mayfield, Mountain View, pp 109–122
Strier KB (1999b) Why is female kin bonding so rare? Comparative sociality of neotropical primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 300–319
Strier KB, Ziegler TE (2000) Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides. Anim Behav 59:849–860
Sugardjito J, te Boekhorst IJA, van Hooff JARAM (1987) Ecological constraints on the grouping of wild orangutans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. Int J Primatol 8:17–41
Sugiyama Y (1988) Grooming interactions among adult chimpanzees at Bossou, Guinea, with special reference to social structure. Int J Primatol 9:393–407
Sugiyama Y (1997) Social tradition and the use of tool-composites by wild chimpanzees. Evol Anthropol 6:23–27
Sugiyama Y (1999) Socioecological factors of male chimpanzee migration at Bossou, Guinea. Primates 40:61–68
Sugiyama Y (2004) Demographic parameters and life history of chimpanzees at Bossou, Guinea. Am J Primatol 124:154–165
Symington MM (1988) Demography, ranging patterns, and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru. Am J Primatol 15:45–67
Symington MM (1990) Fission–fusion social organization in Ateles and Pan. Int J Primatol 11:47–61
Takahata Y, Huffmann MA, Suzuki S, Koyama N, Yamagiwa J (1999) Why dominants do not consistently attain high mating and reproductive success: a review of longitudinal Japanese macaque studies. Primates 40:143–158
Townsend SW, Slocombe KE, Emery Thompson ME, Zuberbühler K (2007) Female-led infanticide in wild chimpanzees. Curr Biol 17:355–356
Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38
Tutin CEG (1994) Reproductive success story: variability among chimpanzees and comparisons with gorillas. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, pp 181–194
Tutin CEG (1996) Ranging and social structure of lowland gorillas in the Lopé Reserve, Gabon. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 58–70
Tutin CEG, McGinnis PR (1981) Chimpanzee reproduction in the wild. In: Graham CE (ed) Reproductive biology of the great apes. Academic Press, New York, pp 239–264
Udono T, Sasaoka S, Inoue M, Takenaka A, Takenaka O (1989) Breeding of the chimpanzee in Sanwakagaku Kenkyusho Reichorui Center and paternity discrimination. Primate Res 5:157 (in Japanese)
Valeo A, Schaffner CM, Vick L, Aureli F, Ramos-Fernandez G (2006) Intragroup lethal aggression in wild spider monkeys. Am J Primatol 68:732–737
Van Noodwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94
Van Noordwijk MA, van Schaik CP (2000) Reproductive patterns in eutherian mammals: adaptations against infanticide? In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 322–360
van Schaik CP (1999) The socioecology of fission–fusion sociality in orangutans. Primates 40:73–90
van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60
van Schaik CP, Deaner RO (2002) Life history and cognitive evolution in primates. In: Tyack PL, de Waal FBM (eds) Animal social complexity. Harvard University Press, Cambridge
van Schaik CP, van Hooff JARAM (1996) Toward an understanding of the orangutan’s social system. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 3–15
van Schaik CP, Preuschoft S, Watts DP (2004) Great ape social systems. In: Russon AE, Begun DR (eds) The evolution of thought: evolutionary origins of great ape intelligence. Cambridge University Press, Cambridge, pp 190–209
Watanabe K (1979) Alliance formation in a free-ranging troop of Japanese macaques. Primates 20:459–474
Watts DP (1989) Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology 81:1–18
Watts DP (1991a) Harassment of immigrant female mountain gorillas by resident females. Ethology 89:135–153
Watts DP (1991b) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225
Watts DP (1994) Agonistic relationships between female mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 34:347–358
Watts DP (1996) Comparative socio-ecology of gorillas. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 16–28
Watts DP (1997) Agonistic interventions in wild mountain gorilla groups. Behaviour 134:23–57
Watts DP (1998) Long-term habitat use by mountain gorillas (Gorilla gorilla beringei). 1. Consistency, variation, and home range size and stability. Int J Primatol 19:651–680
Watts DP (2000) Causes and consequences of variation in male mountain gorilla life histories and group membership. In: Kappeler P (ed) Primate males. Cambridge University Press, Cambridge, pp 169–179
Watts DP (2003) Gorilla social relationships: a comparative overview. In: Taylor AB, Goldsmith ML (eds) Gorilla biology: a multidisciplinary perspective. Cambridge University Press, Cambridge, pp 302–327
Watts DP, Mitani JC (2000) Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda. Primates 41:357–365
Watts DP, Muller M, Amsler S, Mbabazi G, Mitani JC (2006) Lethal intergroup aggression by chimpanzees in the Kibale National Park, Uganda. Am J Primatol 68:161–180
Whitehead H (1998) Cultural selection and genetic diversity in matrilineal whales. Science 282:1708–1711
Whitehead H, Mann J (2000) Female reproductive strategies of cetaceans: life histories and calf care. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 219–246
Whitehead H, Weilgart L (2000) The sperm whale: social females and roving males. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 154–172
Wich SA, Sterck EHM, Utami SS (1999) Are orangutan females as solitary as chimpanzee females? Folia Primatol (Basel) 70:23–28
Wich SA, Utami-Atmoko SS, Mitra Setia T, Rijksen HD, Schurmann C, van Hooff JARAM, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398
Wich SA, de Vries H, Ancrenaz M, Perkins L, Shumaker RW, Suzuki A, van Schaik CP (2009) Orangutan life history variation. In: Wich SA, Utami SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographical variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 65–75
Williams J, Pusey AE, Carlis JV, Farm BP, Goodall J (2002) Female competition and male territorial behaviour influence female chimpanzees’ ranging patterns. Anim Behav 63:347–360
Williams-Blangero S, Blangero J (1995) Heritability of age at first birth in captive olive baboons. Am J Primatol 37:233–239
Wilson ML, Wrangham RW (2003) Intergroup relations in chimpanzees. Annu Rev Anthropol 32:363–392
Wittig RM, Boesch C (2003) Food competition and linear dominance hierarchy among female chimpanzees in the Tai National Park. Int J Primatol 24:847–867
Wrangham RW (1979) Sex differences in chimpanzee dispersion. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 480–489
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300
Wrangham RW (1986) Ecology and social relationships in two species of chimpanzees. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution: birds and mammals. Princeton University Press, Princeton, pp 352–378
Wrangham RW (1987) Evolution of social structure. In: Smuts BB, Wrangham RW, Cheney DL, Struhsaker TT, Seyfarth RM (eds) Primate societies. University of Chicago Press, Chicago
Wrangham RW, Smuts B (1980) Sex differences in the behavioral ecology of chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil Suppl 28:13–31
Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, Pusey AE (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77:873–885
Yamagiwa J (1999) Socioecological factors influencing population structure of gorillas and chimpanzees. Primates 40:87–104
Yamagiwa J (2004) Diet and foraging of the great apes: ecological constraints on their social organizations and implications for their divergence. In: Russon AE, Begun DR (eds) The evolution of thought: evolutionary origins of great ape intelligence. Cambridge University Press, Cambridge, pp 210–233
Yamagiwa J, Kahekwa J (2001) Dispersal patterns, group structure and reproductive parameters of eastern lowland gorillas at Kahuzi in the absence of infanticide. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, London, pp 89–122
Yamagiwa J, Mwanza N, Spangenberg A, Maruhashi T, Yumoto T, Fischer A, Steinhauer BB (1993) A census of the eastern lowland gorillas Gorilla gorilla graueri in Kahuzi-Biega National Park with reference to mountain gorillas G. g. beringei in the Virunga region, Zaire. Biol Conserv 64:83–89
Yamagiwa J, Maruhashi T, Yumoto T, Mwanza N (1996) Dietary and ranging overlap in sympatric gorillas and chimpanzees in Kahuzi-Biega National Park, Zaire. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 82–98
Yamagiwa J, Kahekwa J, Basabose AK (2003) Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates 44:359–369
Yamagiwa J, Kahekwa J, Basabose AK (2009) Infanticide and social flexibility in the genus Gorilla. Primates 50:293–303
Yamagiwa J, Basabose AK, Kahekwa J, Bikaba D, Ando C, Matsubara M, Iwasaki N, Sprague DS (2011) Long-term research on Grauer’s gorillas in Kahuzi-Biega National Park, DRC: life history, foraging strategies, and ecological differentiation from sympatric chimpanzees. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, New York, pp 385–412
Yamakoshi G (1998) Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106:283–295
Yoshihara K (1999) Present situation of chimpanzees in Japan. Primate Res 15:267–271 (in Japanese)
Acknowledgments
This study was financed in part by Grants-in-Aid for Scientific Research by the Ministry of Education, Culture, Sports, Science, and Technology, Japan (No. 162550080, No. 19107007, and No. 24255010 to J. Yamagiwa), by Grant-in-Aid for Young Scientists (B) 19770213 to Shimooka. the Global Environmental Research Fund by Japanese Ministry of Environment (F-061 to T. Nishida, Japan Monkey Centre), the Kyoto University Global COE Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research,” and Science and Technology Research Partnership for Sustainable Development of JST/JICA, and was conducted in cooperation with CRSN and ICCN. We appreciate to Dr. Kosei Izawa for his kind permission for the usage of a picture.
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Yamagiwa, J., Shimooka, Y., Sprague, D.S. (2014). Life History Tactics in Monkeys and Apes: Focus on Female-Dispersal Species. In: Yamagiwa, J., Karczmarski, L. (eds) Primates and Cetaceans. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54523-1_9
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