2 Department of Anthropology, University of California San Diego, La Jolla, CA 92093, USA and .... on captive and wild primates to suggest how rank might.
Behav Ecol Sociobiol (1993) 33:313-318
Behavioral Ecology and Sociobiology © Springer-Verlag 1993
Dominance rank, resource availability, and reproductive maturation in female savanna baboons Fred B. Bercovitch 1, Shirley C. Strum 2 1 Caribbean Primate Research Center, University of Puerto Rico - Medical Sciences Campus, P.O. Box 1053, Sabana Seca, PR 00952, USA 2 Department of Anthropology, University of California San Diego, La Jolla, CA 92093, USA and Institute of Primate Research, P.O. Box 24481, Karen, Nairobi, Kenya Received September 24, 1992 / Accepted after revision July 3, 1993
Summary. Ten years of data collected from a population of savanna baboons, Papio cynoeephalus anubis, residing near Gilgil, Kenya were analyzed to ascertain the extent to which social and ecological factors influence reproductive maturation in females. First sexual swelling occurred at an average age of 4.79 years and first birth occurred at an average age of 6.92 years. Age at first menses was significantly correlated with age at first sexual swelling, but age at first sexual swelling was not a good predictor of age at first birth. The amount of rainfall in the 6 months preceding first sexual swelling and resource availability were significantly correlated with age at first sexual swelling. When ecological factors were taken into account, dominant females had an earlier age at onset of puberty, but not an earlier age at first birth, than did subordinate females. We suggest that nutritional and social stress operate at the same physiological level to disrupt GnRH pulsatility and retard reproductive maturation in some females. Given that socioecological variables modify the timing of life history events related to fitness in female baboons, the task for the future is to unravel how socioecological factors influence different life history components and generate variation in lifetime reproductive success. Key words: Dominance - Puberty - First birth - Savanna baboons - Food availability Nest
Introduction Length of the reproductive lifespan is the main factor responsible for variation in lifetime reproductive success among a number of vertebrates (Clutton-Brock 1988; Newton 1989). One means of potentially increasing reproductive lifespan is to reduce age at production of first offspring. Yet age at first birth is not correlated with lifetime reproductive success in elephant seals, Mirounga anoustrisos, (LeBoeuf and Reiter 1988), Japanese maCorrespondence to: F.B. Bercovitch
caques, Macacafuseata, (Fedigan et al. 1986), or rhesus macaques, M. mulatta (Bercovitch and Berard 1993). The tempo of reproductive maturation appears to be partly a function of ecological conditions. For example, among wild horses, Equus caballus, rapid reproductive maturation characterizes individuals residing in better quality home ranges (Berger 1982). Cheney et al. (1988) reported a trend towards lower age at first birth in areas of better quality in three troops of vervet monkeys, Cercopithecus aethiops. Menarche in captive savanna baboons occurs between 3 and 4 years of age (Gilbert and Gillman 1960; Glassman et al. 1984; Coelho 1985) or about 1-2 years earlier than among wild savanna baboons (Altmann et al. 1981; Strum and Western 1982; Scott 1984). Savanna baboons within a population demonstrate a facultative response to resource availability by augmenting weight and fat under more plentiful conditions (Strum 1991 ; Altmann et al. 1993). When foods are clumped or restricted in distribution, high-ranking female primates tend to have a greater reproductive success (Harcourt 1987; Silk 1987; Bercovitch 1991). Dominant female primates have priority of access to limited food items, often monopolizing critical resources (Whitten 1983; Iwamoto 1987; Barton 1989). Because enhanced nutrition boosts growth rates and improves body condition (Strum 1991), we would expect that rank effects on female reproductive maturation would be most likely to occur under conditions of restricted or seasonal food distribution or availability. Three studies of food-enhanced primate populations have found that high-ranking females are more likely to reproduce at a young age than are their lower-ranking peers. Among rhesus macaques in the Cayo Santiago population (Bercovitch and Berard 1993) and living at La Parguera (Drickamer 1974), high-rank females are more likely to have their first offspring at 3 years of age than are low-rank females. Food provisioning accelerates age at first birth among high-ranking female Japanese macaques, but not among low-ranking females (Sugiyama and Ohsawa 1982). A rank-related acceleration in age at first birth among female primates is often assumed to
314 be a h a r b i n g e r o f greater lifetime r e p r o d u c t i v e success ( D r i c k a m e r 1974; Sade 1991), b u t d a t a collected over 30 years f r o m the C a y o S a n t i a g o p o p u l a t i o n c o n t r a d i c t this a s s u m p t i o n (Bercovich a n d Berard 1993). I n o n e o f few reports available f r o m u n p r o v i s i o n e d p r i m a t e p o p u l a tions, A l t m a n n et al. (1988) f o u n d t h a t d o m i n a n t female s a v a n n a b a b o o n s u n d e r w e n t p u b e r t y a n d h a d their first b i r t h at y o u n g e r ages t h a n s u b o r d i n a t e females, b u t they did n o t assess the effect o f resource availability o n sexual maturation. I n this r e p o r t we scrutinize b o t h social a n d ecological factors t h a t affect the t i m i n g o f r e p r o d u c t i v e m a t u r a t i o n i n a wild p o p u l a t i o n o f primates. W e identify h o w food a v a i l a b i l i t y c a n alter the t i m i n g o f life-history events a n d demonstrate how a variable environment can obviate differences in c o m p e t i t i v e ability. W e e x p a n d u p o n a n earlier analysis o f r e p r o d u c t i v e characteristics o f female s a v a n n a b a b o o n s ( S t r u m a n d W e s t e r n 1982) a n d link o u r findings f r o m the field with physiological d a t a o b t a i n e d o n captive a n d wild p r i m a t e s to suggest h o w r a n k m i g h t influence r e p r o d u c t i v e m a t u r a t i o n via a c o m m o n p a t h w a y u n d e r l y i n g n u t r i t i o n a l a n d social stress.
Methods Subjects and study location. The study subjects were born into Pumphouse troop, a social unit of baboons that has been the subject of behavioral observations almost continuously since 1970 (Strum 1987). The study site is about 1800 m above sea level near the town of Gilgil (0°30, S.) in the Central African Rift Valley of Kenya, 115 km northwest of Nairobi. All members of the troop were completely habituated to human observers and were recognized individually. Demographic information was compiled into the Gilgil Baboon Project Records. The information included daily census records on the reproductive cycle state of all females and birth dates, usually known to within a few days. Data analyzed in this report were collected between October 1971 and August 1981, but the key analyses are restricted to 1975-1981 due to the length of time required for female baboons to become adolescent. Birth dates were known for 16 of 19 females who traversed puberty between 1975 and 1981. The remaining three subjects have been assigned a birthdate corresponding to the first day of the month in which they were born. Births occur throughout the year at Gilgil (Bercovitch and Harding, in prep.). Between 1971 and 1981, troop size has ranged from about 50 to over 100 individuals, with between 18 and 23 adult females present at any one time. The study site is an open country, patchy scrub environment punctuated by nearly parallel outcroppings of volcanic cliffs. The flora is largely grassland, dotted with groves of acacia (Acacia • xanthophloea, A. drepanolobium, A. seyal), sandpaper (Cordia ovalis), and grewia (Grewia similis) trees, thickets of leleshwa bushes (Tarehonanthus camphoratus), and clumps of succulent plants (Opuntia spp., Aloe spp.). The baboons drank from cattle troughs, broken pipes, or temporary ponds and puddles. A variety of large mammals inhabited the troop's home range, including zebra (Equus burchelli), eland (Taurotragus oryx), Thomson's gazelle (Gazella thomsonii), impala (Aepycerus melampus), warthogs (Phacochoerus aetheiopicus), and domestic cattle and sheep. Poisonous snakes (puff adders, Bitis arietus; Egyptian cobra, Naja nigricollis) were regularly encountered and spotted hyena (Crocuta croeuta), were heard on occasion. Cheetah (Acinonyx jubatus) were sporadically sighted and left alone, but leopards (Panthera pardus) that were sighted were removed to protect domestic stock. Rainfall patterns vary from year to year, but the study site generally has a long rainy season (April to June), a short rainy
season (around November), and two intervening dry seasons. Annual variability in temperature is limited (Harding 1976).
Menstrual cycles in savanna baboons. Female savanna baboons have a perineal sexual skin that increases in size during the follicular phase of the menstrual cycle (Zuckerman 1930; Zuckerman and Parkes 1932; Gillman and Gilbert 1946). Swelling of the sexual skin is estrogen-dependent, but not necessarily indicative of ovulation (Zuckerman 1930; Zuckerman and Parkes 1932; Saayman 1972; Gillman and Gilbert 1946), and nulliparous female baboons have prolonged and irregular menstrual cycles (Scott 1984). Currently available techniques are inadequate to ascertain age at first ovulation in wild populations of primates. Menstruation in savanna baboons is visible to human observers, but it is not nearly as noticeable as are sexual swellings. Age at first sexual swelling, but not age at first menses, is available from a number of savanna baboon research sites, but many laboratory investigations of nonhuman primates use age at first menses to designate the beginning of puberty. When possible, we examine both life-history traits. We operationally define the onset of puberty as the day of first sexual swelling because (a) this is the first external sign of an increase in systemic estrogen associated with female adolescent development, (b) it is a common feature used in studies of wild baboons, and (c) it provides for a more in-depth analysis of a larger sample. Dominance rank and resource availability. Dominance hierarchies among female savanna baboons are extremely stable over a number of years (Hausfater et al. 1982; Samuels et al. 1987; Strum 1987). Daughters usually occupy a rank position immediately below that of their mothers, with older daughters subordinate to younger daughters and immature daughters of high-ranking females dominant to adult females of low rank. Nulliparous females were classified as high-, middle-, or low-ranking based upon their mothers' relative status as determined from the agonistic interactions that were contained within the long-term data base. Between 1971 and 1981, no profound alterations occurred in the female dominance hierarchy, indicating that mother's relative position within the dominance hierarchy was a reliable guide to relative rank of daughter. Resource availability was assessed in two ways. First, rainfall measurements were taken almost daily from a rain gauge located near the edge of the home range of Pumphouse troop. Although baboons have a very diverse diet, the major component of the diet among the Pumphouse troop is grass (Harding 1976). The amount of rainfall reflects primary productivity in African grassland environments (Walter 1973 ; Whittaker 1975). Food competition tends to be most severe among baboons at the end of the dry season (Post et al. 1980). Adult females in Pumphouse troop spent significantly more time feeding, and less time in social behavior, during the dry season (Bercovitch 1983). We have used the amount of rainfall in the 6 months prior to first sexual swelling as a means of gauging resource availability during the probable growth spurt in females. Among captive rhesus macaques, a limited growth spurt precedes menarche by about 2-6 months (Tanner et al. 1990). A pronounced growth spurt is not characteristic of wild female savanna baboons (Altmann and Alberts 1987; Strum 1991), but a growth spurt has been documented in captive female savanna baboons (Glassman et al. 1984). The second index of resource availability used was the food competition index, or FCI (Strum and Western 1982). Whereas rainfall provides an estimate of forage production, the resources actually available to baboons are less than this. As noted earlier, the savanna baboons at Gilgil are part of a wildlife community and share their ecosystem with many browzing and grazing ungulates that compete for the same food items. The FCI adjusts for both inter- and intra-specific food competition and yields a value estimating food availability to baboons in lieu of actual measurements of baboon food items in the environment (see Strum and Western 1982 for details). Estimates of ungulate grazing pressure and the impact
315 of conspecifics (i.e., troop size and home range area) are incorporated into the FCI. In sum, the FCI estimates the trough in food availability over the year while rainfall in the previous 6 months estimates the peak in food availability in the period immediately preceding the onset of puberty.
6.00
3O 25
(Z
0.50).
Discussion
Greater food availability and more rainfall were associated with a younger age at first sexual swelling, with rank effects superimposed upon ecological variables. Daughters of high-ranking females had accelerated onset of reproductive maturation only when resource availability was taken into account. However, rank effects on production of first offspring were not evident even when resource availability was considered. Although age at first birth was independent of dominance rank among the Gilgil baboons, age at first birth was younger among high-ranking female baboons at Amboseli Park compared to low-ranking females (Altmann et al. 1988). We suggest that the most likely explanation for the discrepancy between study locations resides in differential resource availability at the two sites. Amboseli is an arid environment with a mean annual rainfall of 280 mm (1973-1981; Western, pers. comm.), while mean annual rainfall at Gilgil is 700 mm. The more arid environment at Amboseli is characterized by extreme seasonality, periods of low biomass, and patchy food distribution of some important dietary elements, e.g., Acacia trees. The restricted distribution of food items in terms of both season and location creates conditions that are conducive to resource monopolization by higher-ranking females. Such patterns of resource availability and differential acquisition foster rank-related differences in reproductive output (Harcourt 1987; Bercovitch 1991). In contrast,.even when biomass is at its lowest at Gilgil, baboon food items are dispersed and indefensible,
yielding a situation that partly ameliorates rank-related effects on age at first birth. Differences reported between locations in Africa in the effect of rank on the timing of first birth may be the result of differences in habitat characteristics and the potential for resource monopolization by dominant individuals. Comparative data on the timing of reproductive maturation among savanna baboons is available from several research sites in Africa. Ransom (1981) suggested that some females had first sexual swellings at 3.5 years at the Gombe Reserve (Tanzania), but Packer (1979) reported a range from 4.5 years to 5.6 years at the same site, with a median age for onset of cycling of 4.96 years. At Amboseli National Park (Kenya), the onset of puberty is from 4.0 to 5.75 years, with an average age at first sexual swelling of 4.8 years (Altmann et al. 1981). The data from Gilgil are virtually identical to the data from Amboseli (range: 4.1-5.5 years; average=4.8 years). First birth at all three field sites usually occurs between 6.5 and 7.0 years (Packer 1979; Altmann et al. 1981, 1988; this study), but, in very rare cases, repeated menstrual cycling occurs without successful production of offspring (Hausfater 1975; Strum, unpubl, data). Among. the 60 females who have been observed in Pumphouse troop since 1970, only one has failed to produce offspring. For a given female savanna baboon, the timing of reproductive maturation will be molded by variation in ecological conditions, and constrained by physiological mechanisms. The earliest age at onset of puberty among wild female savanna baboons is about the same as the latest age at onset of puberty among captive baboons. Growth patterns and physical condition of female baboons at Gilgil under sustained plentiful conditions are essentially identical to those of captive female baboons (Strum 1991). The data from field and laboratory studies of savanna baboons concur in pinpointing the upper and lower bounds for life history events associated with reproductive maturation. Depending upon resource availability, the onset of puberty has a floor of about 3 years and a ceiling of about 6 years. No baboons have been reported to exceed this age without commencement of menstrual periods. The age at first birth has a floor of about 5 years, but no ceiling effect. Hence, regardless of food availability, eventually all females sustain first sexual swelling, but some females are barren throughout life. Puberty in primates commences with the appropriate timing of hypothalamic release of GnRH triggering regular pulsatile outbursts of gonadotropins (Plant 1988; Terasawa et al. 1983; Wilson 1989). Gonzalotropia releasing hormone (GnRH) is a polypeptide produced by th e hypothalamus and which provokes the anterior pitvitary to discharge luteinizing hormone (LH) and follicle stimulating hormone (FSH) into the circulation. The ratio of these two gonzalotropias, as well as their pulse frequency and amplitude, regulate ovulation. The pulsatile activity of GnRH is modulated by both nutritional (i.e., food type, quality, and quantity) and metabolic (i.e., food utilization and activity level) factors in captive primates (Cameron 1989). Severe food restriction has a strong suppressive effect on GnRH pulsatility and enhances negative feedback sensitivity to estradiol (Dubey
317 et al. 1986; Bronson 1989). Among male baboons in Kenya, testosterone concentrations during a drought declined by about 60% (Sapolsky 1986) and estradiol is a metabolite of testosterone (Martin 1985). Social factors also interfere with G n R H output in nonhuman primates. In captive marmosets, Callithrix jacchus, reproductive suppression of subordinate individuals is associated with stifled hypothalamic G n R H release and altered sensitivity to gonadal steroids (Abbott et al. 1988, 1990). Cortisol is the major glucocorticoid released in nohuman primates in response to stressful situations, and hyperactivity of the C R H - A C T H - g l u c o corticoid axis is linked with reproductive disorders, including depressed G n R H secretion, nonpulsatility of LH, and anovulation (Hagino 1972; Moberg et al. 1982; Martin 1985; Bronson 1989). In captive rhesus macaques, high-ranking females ovulate at younger ages than low-ranking females in the absence of differences in feeding time (Schwartz et al. 1985), and females who have their first ovulation at relatively young ages have lower cortisol levels than do peers who have their first ovulation at later ages (Schwartz, pers. comm.). The precursor to both cortisol and estradiol is pregnenolone (Martin 1985), so substrate limitations favoring enhanced production of corticosteroids would be likely to decrease production of sex steroids. It seems likely that reduced food availability arising from subordinate social status delays the onset of puberty among wild primates by interfering with G n R H profiles. Both nutritional stress and social stress are key entities influencing primate reproductive success (Dunbar (1988), but disentangling the impact of each factor may prove extremely difficult because both factors may interact under specific conditions in the wild. Inadequate nutrition and subordinate social status can both have a negative impact on reproduction due to the same physiological mechanism. F r o m an evolutionary perspective, age at first birth has a greater impact on fitness than does age at onset of puberty (Rowell 1977), but lengthy primate lifespans hinder collection of data on the relationship between the timing of these two life-history events. Our data indicated that age at first birth was not predictable on the basis of age at onset of puberty, whereas Altmann (1991) found that age at onset of puberty was predictive of age at first conception in the Amboseli population (r = 0.939, n = 5 , P < 0 . 0 5 ; from Table 1). In captive hamadryas baboons, P. hamadryas, neither age at onset of sexual swelling nor age at first birth were determined by dominance rank and early puberty was not associated with a younger age at first birth (Chalyan et al. 1991). A similar disassociation between the timing of first sexual swelling and age at onset of reproduction has been found among wild chimpanzees, Pan troglodytes (Pusey 1990), and first menses is not predictive of first ovulation in captive rhesus macaques (Schwartz et al. 1988; Bercovitch and G o y 1990). First birth is affected by the number of adolescent cycles, length of cycles, probability of ovulation, likelihood of conception, and chances o f early abortion. We suggest that socioecological variables directly influence neuroendocrine mechanisms responsible for reproductive cycling in females and that critical variables influenc-
ing the onset of reproductive maturation are likely to differ from those determing the age at first reproduction and the length o f the interbirth interval. Despite the evidence indicating that both dominance rank and resource availability influence the timing of reproductive events in a female's lifetime, we still confront large difficulties in deciphering how dominance rank impacts variation in female fitness. Advancements in this area will depend upon developing models integrating complex interactions among physiology, nutrition, longevity, ecology, and dominance status, as well as collecting longitudinal data to test the models.
Acknowledgements. We thank R.S.O. Harding, D. Harding, W. Malmi, H. Gilmore, P. Gilmore, L. Scott, M. Demment, D. Manzolillo, D. Bercovitch, J. Musau, D. Forthman, and H. Quick for contributing data to the Gilgil Baboon Project. Research has been funded by grants from the NSF, NIMH, L.S.B. Leakey Foundation, and the University of California. Occupancy at Kekopey Ranch was permitted through the graciousnessof A. and T. Cole and R. Dansie. Local sponsorship has been provided by the National Museums of Kenya and the Institute of Primate Research. Current financial support is provided by NIH Grant RR03640 to the Caribbean Primate Research Center (FBB), the L.S.B. Leakey Foundation (SCS), and Wildlife Conservation International (SCS). We appreciate the comments and suggestions made by R.I.M. Dunbar, R.S.O. Harding, S.M. Schwartz, and T.E. Rowell.
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