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The Influence of Dominance Rank on the Reproductive Success of Female Chimpanzees

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Science  08 Aug 1997:
Vol. 277, Issue 5327, pp. 828-831
DOI: 10.1126/science.277.5327.828

Abstract

Female chimpanzees often forage alone and do not display obvious linear dominance hierarchies; consequently, it has been suggested that dominance is not of great importance to them. However, with the use of data from a 35-year field study of chimpanzees, high-ranking females were shown to have significantly higher infant survival, faster maturing daughters, and more rapid production of young. Given the foraging behavior of chimpanzees, high rank probably influences reproductive success by helping females establish and maintain access to good foraging areas rather than by sparing them stress from aggression.

In many species of group-living mammals, especially those that feed on monopolizable foods, such as spotted hyenas and many primates, females have frequent dominance interactions and are ranked in stable linear hierarchies (1-4). These hierarchies result from, and are maintained by, a pattern of alliances in which close relatives support each other against more distant relatives and high-ranking matrilines support each other against low-ranking matrilines (5). In most studies, high rank is associated with higher reproductive success (3, 6), although this relation is often weak, perhaps because of counterbalancing costs of high rank (7). There is debate over the extent to which the effects of rank on reproductive success are due to better access to food for high-ranking individuals or to protection from stress that results from aggression toward individuals at the bottom of the hierarchy (7, 8).

Chimpanzees resemble these species in that they live in permanent social groups and feed predominantly on ripe fruit that often occurs in monopolizable patches (9). However, they differ in that females in some populations spend more than half their time feeding alone, and most females disperse to other groups before breeding, with the result that they are usually not surrounded by relatives (9). Compared to female macaques and baboons, it is difficult to detect linear hierarchies among female chimpanzees. Although some female chimpanzees clearly dominate others (10-13), dominance behavior in stable groups or stable pairs of females is uncommon and is never observed between some dyads (10, 13). In addition, when aggressive behavior does occur within a dyad, it is sometimes two-sided with no clear winner (14). These observations have led some to believe that female dominance is unimportant for reproductive success (13, 15). However, others have suggested that dominant females may gain advantages (10, 16). Here we present data from a 35-year study of the chimpanzees of Gombe National Park, Tanzania.

The chimpanzees of Gombe have been studied since 1960 (10). The 48.7-km2 park consists of a series of steep valleys running from the eastern rift escarpment (1600 m elevation) to Lake Tanganyika (775 m). The valley bottoms contain evergreen forest that gives way to semi-deciduous forest on the valley sides and grassland on the ridges (17). Since 1963, the chimpanzees of the central area of the park have been provisioned with bananas at an artificial feeding station in order to habituate them and to facilitate regular observation (10). The feeding station has been likened to an unusually long-term natural food source and, since 1970, has been estimated to provide less than 2% of the chimpanzees' diet (18, 19). Daily observations are made of the presence, reproductive state, and social interactions of individuals at the feeding station and, since 1975, during daily all-day follows of individuals throughout their range (10). Since 1970, the habituated community has consisted of 4 to 13 adult males, 10 to 18 adult females, and 18 to 31 immatures and has occupied a range of 6.75 to 14.5 km2 spanning three to six main valleys in the middle of the park (10, 20). Adult females spend about 65% of their time alone with only their dependent offspring, foraging in distinct but overlapping core areas of about 2 km2 (19, 21), whereas adult males are more social, travel over the whole community range, and jointly patrol and defend its borders (10, 19). Whereas almost all males born in the community remain in the community as adults, most or all natal females visit other communities during adolescence, and about 50% emigrate permanently (22).

We assessed dominance relationships among females by examining the direction of all pant-grunts between females recorded from 1970 to 1992. Pant-grunts are the most reliable measure of submission in chimpanzees and correlate with the reception of aggressive behavior (13, 14). When we constructed dyadic matrices, many cells were empty, but by assessing 2-year blocks we were able to assign 88% of the females that were observed more than 10 days per year (23) as high-, middle-, or low-ranking in each block (24). Dominance rank was not related to body weight (R 2 = 0.01, n = 15) (25, 26), but individual dominance rank increased with age (27) as observed in the chimpanzees of the Mahale Mountains (11). However, a female's rank at age 21 strongly predicts her rank a decade later (R 2 = 0.80,P = 0.001, n = 9), suggesting that early rank acquisition is important.

Dominance rank has a marked effect on several measures of reproductive success. First, offspring survival was significantly related to mother's rank at the birth of her offspring. Infants of low-ranking females showed much higher mortality than those of high-ranking females over the first 7 years of life (Fig. 1). Second, the age at which daughters reached sexual maturity was significantly related to their mother's dominance rank (Fig.2). Daughters of low-ranking females experienced their first full anogenital swelling during which adult males mated with them (28) as much as 4 years later than daughters of high-ranking females. Age at first full swelling was strongly correlated with age at first birth (R 2= 0.67, P = 0.01, n = 8 regularly observed females). Third, there was a tendency for high-ranking females to live longer (29). Finally, the annual production of offspring surviving to weaning age (5 years) was correlated with rank for mature females that were observed for at least 12 years (Fig.3), indicating that low-ranking females were unable to compensate for the higher mortality of their offspring by reproducing more quickly. All these factors combined to produce higher lifetime reproductive success in females of higher rank (30). In the analyses concerning reproduction, we excluded the female GG, because she was sterile. GG was an aggressive, masculine-looking female who occupied the highest rank and cycled regularly for 28 years but never became pregnant. If she is included in the analyses, the relation of the rate of production of surviving infants and life-time reproductive success with rank ceases to be significant (Fig. 3) (30).

Figure 1

Kaplan-Meier cumulative survival plot of offspring at ages 0 to 7 for females of high, middle, and low rank at the birth of the offspring. Dashed line indicates high rank (n = 10 infants of 4 mothers), dotted line, middle rank (n = 39 infants of 13 mothers), and solid line, low rank (n = 16 infants of 11 mothers). In a single Cox-proportional hazards regression with multiple variables (38), mother's rank and age at birth were both significant factors. The exponentiated coefficients estimate the proportional increase in infant mortality rates as a function of unit change in rank, such as from middle to low, or increase in age; Exp(coeff.rank) = 4.3, P = 0.001, Exp(coeff.age) = 1.09, P = 0.01.

Figure 2

Age of daughter's reproductive maturity plotted against mother's rank at the birth of her daughter (R 2 = 0.59, P = 0.02,n = 9 females). For the one mother with two mature daughters, we used the mean age of maturity. Mother's average rank over the daughter's lifetime was also a significant indicator of daughter's age of maturity (R 2 = 0.58,P = 0.02).

Figure 3

Annual production of infants surviving to age 5 plotted against mother's average rank during her childbearing years (R 2 = 0.36, P = 0.02,n = 14, excluding GG; R 2 = 0.02, not significant, n = 15, including GG). Analysis includes all females whose rank was known during their childbearing years who were observed for at least 12 years as adults.

Dominance probably exerts its effects in several ways. First, the high mortality of infants of low-ranking females in the first few months of life was partly due to the infanticidal behavior of the high-ranking female, PS, and her daughter, PM, who snatched and ate the infants of several females in the 1970s (10, 31). Since then, high-ranking females FF and GG were observed trying to snatch the newborn infant of middle-ranking female GM, and females of unknown rank in an adjacent community were seen eating another female's infant (20). These observations suggest that female infanticide may be a significant, if sporadic, threat, rather than the pathological behavior of one female. However, infants are vulnerable to infanticide for only a few weeks, and rank-related effects on offspring mortality continue well beyond that age (Fig. 1). Second, the younger age at which daughters of high-ranking females reach sexual maturity reflects their higher rates of weight gain (20), suggesting that high-ranking females have better nutrition. Better nutrition might also account for better survival of high-ranking females and their offspring. In species living in permanent groups, reduced reproductive success of low-ranking females has been attributed to chronic stress due to frequent aggression from other females (8). Because female chimpanzees spend so much time alone, often going for a day or longer without seeing another female, this is unlikely to be important in this species.

High rank may confer better access to food, both by enabling a female to acquire and maintain a core area of high quality and by affording her priority of access to food in overlap areas (32). Because of the mosaic distribution of vegetation at Gombe, some female core areas are likely to contain higher quality food than others. In addition, because core areas overlap almost completely, a high-ranking female may gain priority of access to preferred food sites in an overlap area. These modes of competition might explain why dominance behavior is less frequent in this species than in some others and why linear dominance hierarchies are hard to detect. If core areas are stable, competition is likely to be most intense when new or maturing females are attempting to establish their own core areas (16). This idea is consistent with the frequent observations of aggressive interactions from resident females to newly immigrant females at Gombe (33) and the Mahale mountains (11), the fact that PS and PM killed the infants of neighboring females as PM reached maturity (31,34), and observations of more frequent dominance interactions during the establishment of a new female group in captivity (16). In addition, clear dominance relationships may only be established between females whose core areas overlap, thus explaining the general lack of clearly defined linear dominance hierarchies. The stability of core areas, the acquisition of core areas, and the relationships of females whose core areas overlap are the focus of current research at Gombe.

More research is needed to understand how female chimpanzees achieve high rank. Some females, such as GG, acquired high rank by their own aggressive behavior. Other females, such as PM, have gained high rank through their mother's support. The fact that alliances with kin are sometimes important makes it all the more striking that young female chimpanzees often disperse to other communities. This underscores the suggestion that they are “forced” to do so in order to avoid inbreeding because their male relatives do not disperse, perhaps because of even stronger advantages to males from cooperation with relatives (35, 36). More information on the relative importance of alliances in the acquisition of female dominance rank and the influence of dominance on reproductive success in other populations of chimpanzees might clarify why only half the females at Gombe disperse, whereas almost 100% do so in other populations (9). Finally, if the considerable degree of reproductive skew observed in the Gombe chimpanzees also occurs in other populations, this has implications for the future genetic diversity of this endangered species. As populations become small and isolated, there is a greater chance for the genetic diversity of the population to be reduced by the successful reproduction of a few dominant individuals (37).

  • * To whom correspondence should be addressed. E-mail: pusey001{at}maroon.tc.umn.edu

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