MALE REPRODUCTIVE STRATEGIES IN NEW WORLD PRIMATES
K a r e n B. S t r i e r
University of Wisconsin-Madison
Patterns of three variables of r e p r o d u c t i v e strategies in m a l e N e w World primates are examined: (i) h o w males obtain access to p o t e n t i a l mates; (ii) h o w males o b t a i n actual m a t i n g o p p o r t u n i t i e s ; a n d (iii) h o w males affect infant survival a n d female reproductive success. M a l e opportunities to associate with females, w h e t h e r b y r e m a i n i n g in their natal groups, d i s p e r s i n g and f o r m i n g n e w groups, or d i s p e r s i n g and t a k i n g over or j o i n i n g e s t a b l i s h e d g r o u p s , are strongly influenced b y local p o p u lation densities a n d correlate w i t h female r e p r o d u c t i v e rates a n d the extent of female reproductive seasonality a n d synchrony. Differences in male m a t i n g success are affected b y female accessibility, w h e t h e r malemale and male-female r e l a t i o n s h i p s are hierarchical or egalitarian, a n d w h e t h e r female reproduction is seasonally restricted. Patterns of m a l e behavior toward infants, characterized as active assistance, overt interference, or b e n i g n tolerance, a p p e a r to co-vary w i t h differences in the degree to w h i c h males can affect female reproductive rates. These qualitative analyses suggest that the reproductive strategies of male N e w World primates can be classified along a c o n t i n u u m r a n g i n g from conservative to daring d e p e n d i n g on w h e t h e r female r e p r o d u c t i v e rates are relatively slow or fast a n d w h e t h e r r e p r o d u c t i o n is s t r o n g l y or w e a k l y l i n k e d to seasonal ecological variables. M a l e s a d o p t the conservative strategy of staying in their natal groups, forfeiting exclusive m a t i n g opportunities, a n d treating infants w i t h tolerance w h e n female r e p r o d u c -
Received September 29, 1995; accepted December 7, 1995.
Address all correspondence to Karen B. Strier, Department of Anthropology, University of Wisconsin-Madison, 1180 Observatory Drive, Madison, WI 53706. E-mail: strier@macc,wisc.edu Copyright 9 1996 by Walter de Gruyter, Inc., New York Human Nature, Vol. 7, No. 2, pp. 105-123. 105
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tion is constrained by ecological factors. Conversely, males adopt the more daring strategy of dispersing and competing when potential payoffs through their ability to affect female reproduction are high. KEYWORDS:New World primates; Reproductive strategies; Dispersal patterns; Mating success; Infant care; Reproductive seasonality.
Studies from captivity and the wild have provided insights into the diverse reproductive strategies of female New World primates. At one extreme are the rapid reproductive rates of female callitrichids, which may involve the production of twins, or more rarely triplets, at intervals as short as six months, and limited breeding opportunities, including the inhibition of ovulation for subordinate females (Dietz et al. 1994; Garber 1994). At the other extreme are the single infants produced at roughly three-year intervals by the larger-bodied atelins such as spider monkeys (Ateles: Chapman and Chapman 1990) and muriquis (Brachyteles arachnoides: Strier 1991). Single births at one- or two-year intervals characterize most of the other New World monkeys (Ross 1991), but even these primates vary considerably in the degree to which reproduction is constrained by seasonal ecological conditions (Lindburg 1987). Such marked differences in female reproductive biology should interact with ecological and social variables to influence the reproductive strategies of males. Yet, little is known about these interactions, or about more general characteristics of reproductive strategies in New World primate males. Fundamental differences between New World and some well-studied Old World monkeys make it difficult to extrapolate about male reproductive strategies without first understanding the range of behaviors that New World primate males exhibit. For example, in the majority of New World primates, by contrast to most cercopithecines, it is females or both males and females that disperse from their natal groups (Moore 1992; Strier 1994a). New World primates also exhibit striking intra- and interspecific variability in their grouping patterns (Kinzey and Cunningham 1994) and in whether relationships among males and between males and females are hierarchical or egalitarian (Boinski and Mitchell 1994; Strier 1994b). This paper explores the patterning of reproductive strategies among male New World primates by focusing on the interactions among three variables: (i) how males obtain access to potential mates; (ii) h o w males obtain actual mating, and presumably fertilization, opportunities; and (iii) how males affect infant survival and female reproductive success. The distributions of these key variables of male reproductive strategies are examined qualitatively because the paucity of comparative long-term
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field data (spanning at least one generation) precludes more rigorous quantitative analyses for most species. Nonetheless, identifying consistent interacting effects that emerge from this preliminary overview can contribute to hypotheses about the correlates or determinants of N e w World primate male reproductive strategies and provide comparative insights across the Primate order.
VARIABLES OF MALE REPRODUCTIVE STRATEGIES Opportunities to Associate with Females
Rationale. Males require opportunities to associate with one or more females, however briefly, in order to reproduce. At a behavioral level, these opportunities can be distinguished along a continuum ranging from insecure to secure depending on the degree to which males must actively seek out female associates. Dispersal patterns that affect male access to female associates thus provide a first approximation of the degree to which male reproductive strategies involve differential access to potential mates. Opportunities to associate with females are least secure for males that emigrate from their natal groups to establish their own reproductive units, and most secure for philopatric males, which remain in their natal groups throughout life. In long-term studies of Costa Rican mantled howler monkeys (Alouatta palliata) and Venezuelan red howler monkeys (A. seniculus) for example, most males emigrated from their natal groups (Crockett and Pope 1993; Glander 1992), whereas all male muriquis (Brachyteles arachnoides) born during one study since 1982 have remained in their natal group, where they mature into sexually active adults (Strier 1991). Other primates fall along the continuum between these extremes, either as emigrant males that must work their w a y into established female groups or as males that are tolerated in their natal groups until they either inherit the role of breeding male or are able to disperse and establish their own reproductive units. Patterns. Despite some clustering among close phylogenetic relatives (Strier 1994a), N e w World primates are represented across the continuum of dispersal patterns (Table 1). Except in the case of male philopatry, the success of each strategy in terms of opportunity for males to associate with females is strongly influenced by local population densities and demography (e.g., Crockett and Pope 1993; Emlen and Vehrencamp 1983; Sussman 1992), which in turn are affected by ecological factors (Goldizen 1990) and stochastic events (Dunbar 1979). Several genera
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exhibit flexible dispersal patterns that correspond to these local conditions. For example, among the marmosets (Callithrix), tamarins (Saguinus), and howler monkeys (Alouatta), males may wait in their natal groups for mating opportunities or emigrate from their natal groups, either to form new groups or to join established groups (Crockett and Eisenberg 1987; Garber 1994; Garber et al. 1993; Glander 1992; Goldizen 1987). Among squirrel monkeys, male philopatry characterizes one Costa Rican population (Saimiri oerstedi) whereas male dispersal characterizes a Peruvian population (S. sciureus: Mitchell et al. 1991). In most capuchins (Cebus), males disperse from their natal groups, but occasional female migrations and multi-male influxes have been reported (Robinson and Janson 1987; Fedigan 1993). Variability in dispersal patterns among squirrel monkeys has been attributed to differences in the distribution of food resources. Mitchell and colleagues (1991) suggest that differences in the size of preferred food patches are responsible for differences in Peruvian and Costa Rican squirrel monkey dispersal patterns. Large food patches available to Peruvian squirrel monkeys offer advantages for cooperation among female kin in resource defense, and consequently, males disperse to avoid inbreeding. The absence of cooperative advantages to defend the smaller food patches exploited by Costa Rican squirrel monkeys, by contrast, favors female-biased dispersal and male philopatry. Among the callitrichids, variability in the timing and pattern of dispersal has been attributed to whether or not breeding opportunities beyond the natal group exist (Baker et al. 1993; Goldizen 1990; Sussman and Garber 1987). More consistent dispersal patterns appear to occur among species that exhibit obligate monogamy and in which both sexes disperse (Aotus and Callicebus [owl and titi monkeys]: Garber 1994), and among some polygamous atelins where females disperse and males are philopatric (Strier 1994b). However, further studies on these taxa at a greater number of sites may ultimately reveal populational differences associated with local conditions similar to those found in other N e w World primate genera for which comparative data are available. Opportunities to Mate with Females
Rationale. Males that associate with females are not necessarily assured of opportunities to mate, and male mating success correlates imperfectly with actual or probable fertilization success (Gray 1985). Nevertheless, in the absence of genetic paternity tests or reliable data on the precise timing of female ovulation relative to copulations, examining the variance in male mating success can provide a rough estimate of the degree to which males are able to monopolize sexual, and potentially reproductive, access to females.
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Variance in male mating success is determined by a number of factors, including the number and ratio of breeding females to males, whether females reproduce seasonally or in synchrony, and whether males employ aggression to compete among themselves for access to females or to coerce females into mating with them (Cowlishaw and Dunbar 1991; van Hooff and van Schaik 1992; Strier 1994b). When males are able to monopolize access to females, either by forming exclusive liaisons or by interrupting the sexual liaisons females establish with other males, the variance in male mating success should be high. Conversely, the variance in male mating success should be low w h e n the ability of males to maintain exclusive mating privileges is limited, either because of the number of simultaneously receptive females or because egalitarian relationships between the sexes prevent males from overriding female mate choices. The range of strategies males employ to monopolize mating opportunities, and therefore increase variance in mating success, can thus be characterized along a continuum in which variance is highest when one male is able to monopolize all copulations, intermediate w h e n copulations are biased in favor of one male, and lowest when copulations are shared among males. Patterns. Variance in male mating success is distributed predictably across the New World primates (Figure 1). In those genera that routinely
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form pair bonds (e.g., Aotus, Callicebus), the greatest variance in male mating success occurs between mated and unmated males. Among those males that succeed in securing mates, however, the intraspecific variance in mating success is presumably low. In taxa with polygamous mating systems, the lowest variance in mating success occurs in the egalitarian societies of muriquis (Strier 1992, 1994b) and some callitrichids (e.g., Saguinusfuscicollis: Goldizen 1990; S. mystax: Garber et al. 1993) where all or most males have been observed to mate. In the hierarchical societies of other polygamous taxa, whether copulations are restricted to the dominant male, defined as the consistent winner of agonistic contests, or only biased in his favor appears to d e p e n d on the extent to which female choice parallels or deviates from the outcome of male-male competition for rank. Although male golden lion tamarins (Leontopithecus rosalia) frequently migrate in pairs, the dominant male has most often been observed to copulate with estrous females (Baker et al. 1993). In some capuchins (e.g., Cebus apella: Janson 1984; C. olivaceus: O'Brien 1991), receptive females solicit copulations almost exclusively from the dominant male despite the presence of subordinate males. In C. albifrons (Janson 1986) and C. capucinus (Fedigan 1993), however, there is no evidence that females mate preferentially or exclusively with the dominant male. Paternity studies of multi-male red howler monkey troops (Alouatta seniculus) reveal strong rank effects on male reproductive success (Pope 1990), despite the fact that alliances between red howler monkey males facilitate their ability to establish or remain in association with females (Crockett and Pope 1993). Copulations appear to be strongly biased in Costa Rican squirrel monkeys (Saimiri oerstedi), with the dominant male accounting for roughly 70% of all copulations observed during one mating season (Boinski 1987a), and somewhat biased in favor of dominant male woolly monkeys (Lagothrix: Nishimura 1990) and spider monkeys (Ateles: Symington 1987). However, contrary to predictions that strong reproductive seasonality should make it difficult for dominant males to monopolize sexual access to multiple receptive females (e.g., van Hooff and van Schaik 1992), the effects of male rank on mating success appear to be more pronounced in the seasonally breeding squirrel monkeys (Boinski 1987a, 1987b) than they are in the less seasonal polygamous spider m o n k e y s (Chapman and Chapman 1990) and muriquis (Strier 1996a). Indeed, among capuchin monkeys, mating success is strongly biased in favor of the dominant male in populations with pronounced birth peaks (Cebus apella: Janson 1984; Robinson and Janson 1987; and C. olivaceus: O'Brien 1991) but more evenly distributed across males in populations in which births occur during an extended (six-month) period (C. capucinus: Fedigan 1993; Fedigan and Rose 1995).
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Male Influence on Infant Survival and Female Reproduction
Rationale. Male reproductive strategies, like those of females, extend beyond mating opportunities to include their relationships with infants (Sussman and Garber 1987; Whitten 1987). Male behavior toward infants can be categorized along a continuum ranging from active assistance to benign tolerance to overt interference, expressed most extremely by infanticidal tendencies (Small 1990). Whether males help or hinder infant survival may correspond to the degree of genetic relatedness between a male and an infant, with fathers and kin more likely to promote than interfere with infants that share some common genetic interests (Trivers 1972). However, factors such as body size energetics (Wright 1990), social benefits (Smith and Whitten 1988; Small 1990), future reproductive opportunities (Baker et al. 1993), and the value of experience with infant care (Snowdon 1990) may be better predictors of male behavior toward infants than paternity or degree of relatedness. An alternative way of evaluating male behavior toward infants is to consider how differences in the ability of males to affect future female reproductive success correlate with male strategies. Female reproductive potential is determined by at least two factors: intrinsic reproductive rates (Ross 1991) and the degree to which the timing of reproduction can be altered. For N e w World primate females with high reproductive rates, males bear a large share of the energetic costs of infant care, thereby helping females recover their energy reserves for subsequent reproduction (Leutenegger 1980; Wright 1990). When female reproductive rates are intrinsically low, but not tightly linked to seasonal ecological conditions, males may benefit by interfering with the survival of unrelated infants because doing so will bring females, w h o s e lactation has been interrupted, into estrus more quickly (Hrdy 1979). Male tolerance toward infants, by contrast, should reflect low female reproductive rates coupled with seasonally restricted reproduction, because neither assistance nor interference by males will enable females to reproduce sooner than they would in the appropriate season. Patterns. As predicted, the clustering of infant care by male N e w World primates corresponds to male ability to affect female reproduction (Figure 2). High levels of male infant care have been observed in the callitrichids (Dietz and Baker 1993; Garber 1994; Goldizen 1990; Sussman and Garber 1987) and in the monogamous owl monkey (Aotus) and tiff monkey (Callicebus), where assistance by males helps females to recover their energy to reproduce again (Wright 1990) and increases infant survivorship (Sussman and Garber 1987). In howler monkeys, where female reproductive rates are relatively low, and in at least some popula-
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Figure 2. Continuum of male behavior toward infants, shown as axes for subsequent comparisons, and male effect on female reproduction. Arrows represent variation in behavior; curves represent overlapping domains. References cited in text. tions not tightly seasonal (Alouatta seniculus, A. palliata), overt interference in the form of suspected infanticide by unrelated males has been reported (Crockett and Eisenberg 1987). In other genera in which female reproductive rates are similarly slow, and reproduction is to varying degrees confined to particular seasons, the behavior males display toward infants corresponds to the effects male assistance or interference can have on female reproductive biology. The fact that infanticide by males has been reported in both seasonal Cebus olivaceus (O'Brien 1991) and aseasonal C. capucinus (Fedigan 1993) is therefore consistent with evidence that capuchin monkey interbirth intervals generally range between one and two years depending on infant survivorship (Robinson and Janson 1987; Fedigan and Rose 1995).
INTERACTING EFFECTS BETWEEN PARAMETERS Dispersal Patterns and Variance in Male Mating Success
N e w World primate dispersal patterns correspond imperfectly with male mating success (Figure 1). Although philopatric males tend to have
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lower variance in mating success than do males that disperse from their natal groups, there are nonetheless marked differences in male mating success across taxa with similar dispersal systems. Thus, although malebiased dispersal has been reported in all capuchin monkeys, variance in male mating success is high in Peruvian Cebus apella and relatively low in sympatric C. albifrons (Janson 1986). Conversely, although male philopatry occurs in both woolly monkeys (Lagothrix), spider monkeys (Ateles), and muriquis (Brachyteles arachnoides), the higher variance in male woolly monkey and spider monkey mating success is consistent with the more hierarchical relationships that exist among males and b e t w e e n males and females (Strier 1994b). Egalitarian relationships among muriquis prevent males from overtly competing for sexual access to females or from coercing females into undesirable liaisons (Strier 1992), and female choice of multiple mates maintains low variance in male mating success (Strier 1994b). Male mating success is biased in favor of dominant males in both philopatric male squirrel monkeys (Saimiri oerstedi) and dispersing male squirrel monkeys (S. sciureus: Boinski and Mitchell 1994). However, unlike the stable egalitarian relationships that persist year-round in muriquis, affiliative relationships among philopatric male S. oerstedi in Costa Rica appear to become more hierarchical during the restricted mating season (Baldwin 1992; Boinski 1987a), resulting in skewed mating opportunities that resemble those among unrelated male S. sciureus.
Variance in Male Mating Success and Reproductive Seasonality Differences in the degree of reproductive seasonality that affect female mate choice may account for some of the differences in the variance in male mating success among N e w World primates (Figure 3). Strong reproductive seasonality imposes high costs on females that fail to conceive and reproduce at the appropriate time and should therefore favor either strong male-male competition (e.g., Leontopithecus rosalia: Dietz et al. 1994) or strong female mate choice for males that are most likely to succeed at fertilization (e.g., Saimiri oerstedi: Boinski 1987a) or provide access to preferred foods (e.g., Cebus apella: Janson 1986). When reproduction is less seasonally constrained, however, females that fail to conceive can continue to cycle until conception occurs. These females may still discriminate among potential mates for any number of other attributes, and may benefit by earlier conceptions. Nonetheless, lower variance in male mating success may be a consequence of more relaxed time constraints on female reproduction (e.g., Cebus capucinus: Fedigan 1993).
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Effects o f F e m a l e R e p r o d u c t i o n P o t e n t i a l
Male ability to affect female reproduction maps on to other components of male reproductive strategies, such as dispersal patterns (Figure 4). It may be no coincidence, for example, that male philopatry and tolerance toward infants occurs when female reproduction is most strongly constrained by low reproductive rates or seasonality, while male dispersal and potential interference with infant survival appears to be more prevalent when males can affect the timing of female reproduction. The reproductive strategies employed by male N e w World primates can thus be distinguished as conservative w h e n female reproduction is constrained by ecological or endocrinological factors, and daring w h e n female reproduction can be altered. Males appear to adopt the conservative strategy of staying in their natal groups and potentially forfeiting exclusive mating opportunities when there is little they can do to increase the intrinsic reproductive rates of females9 Conversely, males adopt the riskier strategy of dispersing and competing when the potential pay-offs through their ability to affect female reproduction are high. In each strategy, seasonal constraints on reproduction appear to determine h o w selective females are in their choice of mates and thus h o w variable male mating success will be.
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PREDICTIONS
Such divergent alternatives, like all other components of New World primate male behavior reviewed here, represent extremes along a continuum. The patterns emphasize, however, the importance of female reproductive biology and ecology to male reproductive strategies. Simplifying the interacting effects between these variables also leads to testable predictions that may explain some of the diversity in behavior exhibited by New World primate males. For example, the prediction that more restricted breeding seasonality should occur among philopatric male squirrel monkeys than among squirrel monkeys in which males routinely disperse can be evaluated with comparative data on the timing of reproduction in populations with different dispersal systems. Similarly, the related predictions that infanticide should be prevalent only in those populations where females can reproduce throughout all or most of the year, whereas male tolerance toward infants should be m o r e prevalent in populations that inhabit highly seasonal environments where reproduction is temporally restricted, could be evaluated with comparative data on reproductive seasonality across different populations and species of howler monkeys and capuchin monkeys.
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EXTENDING THE MODEL Future Directions
The apparent relationships between female reproductive ecology and male reproductive strategies emphasize the importance of extending our knowledge of primate reproductive physiology from captive studies to the wild, where the effects of seasonal dietary correlates of reproduction can be assessed. Several possible mechanisms may be responsible for whether reproduction is seasonal or aseasonal, including differential responses to changes in photoperiod, rainfall patterns that affect food availability and consequently both female nutritional condition and the timing of weaning, and social pressures favoring reproductive synchrony (Clarke et al. 1992; Lindburg 1987). Yet, understanding how female reproductive hormones respond to these environmental pressures has been limited because measuring female endocrinological condition in the wild has been difficult. The recent development of noninvasive fecal steroid assays for New World primates now makes it possible to monitor reproductive hormones in wild monkeys, and to correlate subtle changes in female reproductive physiology with seasonality in diet and behavior (Strier and Ziegler 1994). These techniques permit more precise evaluations of the timing of mating behavior relative to ovulation, and of the timing of conception relative to ovulatory cycles. Such precision may be especially important to understanding the onset of ovulation and the postpartum resumption of ovulation in species in which nonreproductive sexual activity is common (Hrdy 1981). Noninvasive techniques can also be applied to monitor the effects of seasonality and female reproductive biology on male behavior and reproductive physiology. For example, male weight gain just prior to the breeding season has been reported from field studies of both Saimiri (Baldwin 1992) and Leontopithecus (Dietz et al. 1994). Little is currently known, however, about similar metabolic responses in other New World primates or about how such weight changes interact with social behavior and ecology to affect male reproductive strategies. Further Comparative Perspectives
Some of the apparent patterns in the reproductive strategies of male New World primates may be relevant to understanding the diversity of male reproductive strategies in other primates, including humans. For example, the association between tight reproductive seasonality, high metabolic costs of reproduction for females, and female dominance in lemurs (Richard and Dewar 1991) is consistent with two corollaries of
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the model. First, the tolerance and occasional help male lemurs exhibit toward infants are consistent with their seasonal breeding and the limits it imposes on the ability of males to affect female reproduction (Morland 1990). Second, males of at least some lemur species (e.g., Varecia variegata) resemble Costa Rican squirrel monkeys both in their low rates of aggressive competition outside of the breeding season and in the choices females express for particular males (Morland 1993). Male-biased dispersal in lemurs, like male philopatry in many New World primates, is not sufficient to predict consistent patterns of social relationships and behavior. Furthermore, the fact that male lemurs may disperse as cohorts and emigrate repeatedly depending on local sex ratios (Sussman 1992) is consistent with a strategy that minimizes risks to both male survival and male associations with females because the timing of female reproduction in these primates cannot be substantially altered. Despite marked differences in ecology and social organizations, the low reproductive rates of female hominoids lead to some predictable patterns in male reproductive strategies that correspond to the degree of reproductive seasonality. For example, the evidence that relationships among philopatric male chimpanzees are more hierarchical than those among male bonobos corresponds to more constrained reproductive seasonality in chimpanzees (Nishida et al. 1990; Wallis 1995) and prolonged female receptivity in bonobos (Furuichi 1989; Ihobe 1992). The variability described in male gorilla dispersal patterns, which encompass every possible alternative from emigration to philopatry (Robbins 1995), resembles that reported for New World callitrichids. However, the higher variance in male gorilla mating success and the lack of active assistance by male gorillas toward infants are consistent with predictions based on their less seasonal reproduction and lower reproductive rates. Changes in the reproductive biology of female hominids have figured prominently in many scenarios of h u m a n social evolution. While these models differ from one another concerning attribution of changes in female reproductive patterns to selection pressures favoring the inclusion of meat in the diet, larger brains, or correspondingly longer periods of infant dependency (e.g., Foley and Lee 1991; Lovejoy 1981; Martin 1981), they uniformly recognize the pivotal role of female reproductive biology on male behavior (e.g., Alexander and Noonan 1979). The present analysis of variables involved in the reproductive strategies of male New World primates also leads to specific predictions about how female reproductive biology may have influenced male hominids. Indeed, m a n y contemporary h u m a n foraging societies conform to the predictions that link birth seasonality, which is widespread in h u m a n s (Ellison 1994), with the prevalence of patrilocal residence and cooperation in subsistence efforts (Strier 1996b). Knowledge of the ecological
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conditions that m a y h a v e affected f e m a l e r e p r o d u c t i v e s e a s o n a l i t y in early h o m i n i d s w o u l d be instructive in p e r m i t t i n g us to e s t i m a t e w h e n a n d to w h a t d e g r e e h o m i n i d m a l e s a d o p t e d such c o n s e r v a t i v e r e p r o d u c tive strategies, a n d h o w variable s u c h strategies m a y h a v e b e e n across h o m i n i d species a n d p o p u l a t i o n s . I am grateful to Dr. Ben Campbell for inviting me to present a version of this paper at the symposium he organized on Reproduction in Males: Physiology, Ecology and Behavior for the 65th annual meeting of the American Association of Physical Anthropologists. Participation at this meeting and the associated research were supported by funds from NSF grant BNS 8959298. P. A. Garber, J. W. Lynch, and C. T. Snowdon provided valuable comments on an earlier draft of this manuscript. Karen B. Strier (B.A., 1980, Swarthmore College; M.A., 1981 and Ph.D., 1986, Harvard University) is Professor and Chair of the Department of Anthropology, University of Wisconsin-Madison. She is interested in primate behavioral ecology and conservation and has been studying the endangered muriqui monkeys of Brazil since 1982. She is the author of Faces in the Forest (Oxford University Press, New York, 1992).
REFERENCES Alexander, R. D., and K.M. Noonan 1979 Concealment of Ovulation, Parental Care, and Human Social Evolution. In Evolutionary Biology and Human Social Behavior, N. A. Chagnon and W. Irons, eds. Pp. 436-453. North Scituate, Massachusetts: Duxbury. Baker, A. J., J. M. Dietz, and D. G. Kleiman 1993 Behavioural Evidence for Monopolization of Paternity in Multi-Male Groups of Golden Lion Tamarins. Animal Behaviour 46:1091-1103. Baldwin, J. P. 1992 Determinants of Aggression in Squirrel Monkeys (Saimiri). In Aggression and Peacefulness in Humans and Other Primates, J. Silverberg and J. P. Gray, eds. Pp. 72-99. New York: Oxford University Press. Boinski, S. 1987a Mating Patterns in Squirrel Monkeys (Saimiri oerstedi). Behavioral Ecology and Sociobiology 21:13-21. 1987b Birth Synchrony in Squirrel Monkeys (Saimiri oerstedi). Behavioral Ecology and Sociobiology 21: 393-400. Boinski, S., and C. L. Mitchell 1994 Male Residence and Association Patterns in Costa Rican Squirrel Monkeys (Saimiri oerstedi). American Journal of Primatology 34: 157-169. Chapman, C. A., and L. J. Chapman 1990 Reproductive Biology of Captive and Free-Ranging Spider Monkeys. Zoo Biology 9:1-9.
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Clarke, A. S., N. C. Harvey, and D. G. Lindburg 1992 Reproductive Coordination in a Nonseasonally Breeding Primate Species, Macaca silenus. Ethology 91:46-58. Cowlishaw, G., and R. I. M. Dunbar 1991 Dominance Rank and Mating Success in Male Primates. Animal Behaviour 41:1045-1056. Crockett, C. M., and J. F. Eisenberg 1987 Howlers: Variations in Group Size and Demography. In Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds. Pp. 54-68. Chicago: University of Chicago Press. Crockett, C. M., and T. R. Pope 1993 Consequences of Sex Differences in Dispersal for Juvenile Red Howler Monkeys. In Juvenile Primates, M. E. Pereira and L. A. Fairbanks, eds. Pp. 104-118. New York: Oxford University Press. Dietz, J. M, and A. J. Baker 1993 Polygyny and Female Reproductive Success in Golden Lion Tamarin (Leontopithecus rosalia). Animal Behaviour 46:1067-1078. Dietz, J. M., A. J. Baker, and D. Miglioretti 1994 Seasonal Variation in Reproduction, Juvenile Growth, and Adult Body Mass in Golden Lion Tamarins (Leontopithecus rosalia). American Journal of Primatology 34:115-132. Dunbar, R. I. M. 1979 Population Demography, Social Organization, and Mating Strategies. In Primate Ecology and Human Origins, I. S. Bernstein and E. O. Smith, eds. Pp. 67-88. New York: Garland Press. Ellison, P. T. 1994 Advances in Human Reproductive Ecology. Annual Review of Anthropology 23:255-275. Emlen, S. T., and S. L. Vehrencamp 1983 Cooperative Breeding Strategies among Birds. In Perspectives in Ornithology, A, H. Brush and G. A. J. Clark, eds. Pp. 93-120. Cambridge: Cambridge University Press. Fedigan, L. 1993 Sex Differences and Intersexual Relations in Adult White-Faced Capuchins (Cebus capucinus). International Journal of Primatology 14:853-878. Fedigan, L. M., and L. M. Rose 1995 Interbirth Interval Variation in Three Sympatric Species of Neotropical Monkey. American Journal of Primatology 37:9-24. Foley, R. A., and P. C. Lee 1991 Ecology and Energetics of Encephalization in Hominid Evolution. Philosophical Transactions of the Royal Society of London B 334:223-232. Furuichi, T. 1989 Social Interactions and the Life History of Female Pan paniscus in Wamba, Zaire. International Journal of Primatology 10:173-197. Garber, P. A. 1994 Phylogenetic Approach to the Study of Tamarin and Marmoset Social Systems. American Journal of Primatology 34:199-219.
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Garber, P. A., F. Encarnaci6n, L. Moya, and J. P. Pruetz 1993 Demography and Reproductive Patterns in Moustached Tamarin Monkeys (Saguinus mystax): Implications for Reconstructing Platyrrhine Mating Systems. American Journal of Primatology 29:235-254. Glander, K. E. 1992 Dispersal Patterns in Costa Rican Mantled Howling Monkeys. International Journal of Primatology 13:415-436. Goldizen, A. W. 1987 Tamarins and Marmosets: Communal Care of Offspring. In Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds. Pp. 34-42. Chicago: University of Chicago Press. 1990 A Comparative Perspective on the Evolution of Tamarin and Marmoset Social Systems. International Journal of Primatology 11:63-83. Gray, J. P. 1985 Primate Sociobiology. New Haven, Connecticut: HRAF Press. Hrdy, S. B. 1979 Infanticide among Animals: A Review, Classification, and Examination of the Implications for Reproductive Strategies. Ethology and Sociobiology 1:13-40. 1981 The Woman That Never Evolved. Cambridge: Harvard University Press. Ihobe, H. 1992 Male-Male Relationships among Wild Bonobos (Pan paniscus) at Wamba, Republic of Zaire. Primates 33:163-179. Janson, C. H. 1984 Female Choice and Mating System of the Brown Capuchin Monkey Cebus apella (Primates: Cebidae). Zeitschrift fur Tierpsychologie 65:177200. 1986 The Mating Systems as a Determinant of Social Evolution in Capuchin Monkeys (Cebus). In Primate Ecology and Conservation, Vol. 2, J. G. Else and P. C. Lee, eds. Pp. 169-179. Cambridge: Cambridge University.Press. Kinzey, W. G., and E. P. Cunningham 1994 Variability in Platyrrhine Social Organization. American Journal of Primatology 34:185-198. Leutenegger, W. 1980 Monogamy in Callitrichids: A Consequence of Phyletic Dwarfism. International Journal of Primatology 1:95-98. Lindburg, D. G. 1987 Seasonality of Reproduction in Primates. In Behavior, Cognition, and Motivation, G. Mitchell and J. Erwin, eds. Pp. 167-218. Comparative Primate Biology, Vol. 2B. New York: Alan R. Liss. Lovejoy, C. O. 1981 The Origin of Man. Science 211:341-350. Martin, R. D. 1981 Relative Brain Size and Basal Metabolic Rate in Terrestrial Vertebrates. Nature 293:57-60. Mitchell, C. L., S. Boinski, and C. P. van Schaik 1991 Competitive Regimes and Female Bonding in Two Species of Squirrel
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Monkeys (Saimiri oerstedi and S. sciureus). Behavioral Ecology and Sociobiology 28:55-60. Moore, J. 1992 Dispersal, Nepotism, and Primate Social Behavior. International Journal of Primatology 13:361-378. Morland, H. S. 1990 Parental Behavior and Infant Development in Ruffed Lemurs (Varecia variegata) in a Northeast Madagascar Rain Forest. American Journal of Primatology 20:253-265. 1993 Reproductive Activity of Ruffed Lemurs (Varecia variegata variegata) in a Madagascar Rain Forest. American Journal of Physical Anthropology 91:71-82. Nishida, T., H. Takasaki, and Y. Takahata 1990 Demography and Reproductive Profiles. In The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies, T. Nishida, ed. Pp. 63-98. Tokyo: University of Tokyo Press. Nishimura, A. 1990 Mating Behavior of Woolly Monkeys (Lagothrix lagotricha) at La Macarena, Colombia (II): Mating Relationships. Field Studies of New World Monkeys, La Macarena, Colombia 3:7-12. O'Brien, T. G. 1991 Female-Male Social Interactions in Wedge-Capped Capuchin Monkeys: Benefits and Costs of Group Living. Animal Behaviour 41:555-567. Pope, T. 1990 The Reproductive Consequences of Male Cooperation in the Red Howler Monkey: Paternity Exclusion in Multi-Male and Single-Male Troops Using Genetic Markers. Behavioral Ecology and Sociobiology 27:439-446. Richard, A. F., and Dewar, R. E. 1991 Lemur Ecology. Annual Review of Ecology and Systematics 22:145-175. Robbins, M. M. 1995 A Demographic Analysis of Male Life History and Social Structure of Mountain Gorillas. Behaviour 132:21-47. Robinson, J. G. and C. H. Janson 1987 Capuchins, Squirrel monkeys, and Atelines: Socioecological Convergence. In Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, T. T. Struhsaker, eds. Pp. 69-82. Chicago: University of Chicago Press. Ross, C. 1991 Life History Patterns of New World Monkeys. International Journal of Primatology 12:481-502. Small, M. F. 1990 Alloparental Behavior in Barbary Macaques, Macaca sylvanus. Animal Behaviour 39:297-306. Smith, E. O., and P. L. Whitten 1988 Triadic Interactions in Savanna-Dwelling Baboons. International Journal of Primatology 9:409-424. Snowdon, C. T. 1990 Mechanisms Maintain Monogamy in Monkeys. In Contemporary Issues
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in Comparative Psychology, D. A. Dewsbury, ed. Pp. 225-251. Sunderland, Massachusetts: Sinauer Associates. Strier, K. B. 1991 Demography and Conservation of an Endangered Primate, Brachyteles arachnoides. Conservation Biology 5:214-218. 1992 Causes and Consequences of Nonaggression in Woolly Spider Monkeys. In Aggression and Peacefulness in Humans and Other Primates, J. Silverberg and J. P. Gray, eds. Pp. 100-116. New York: Oxford University Press. 1994a Myth of the Typical Primate. Yearbook of Physical Anthropology 37:233271. 1994b Brotherhoods Among Atelins: Kinship, Affiliation, and Competition. Behaviour 130:151-167. 1996a Reproductive Ecology of Female Muriquis (Brachyteles arachnoides). In Adaptive Radiations of Neotropical Primates, M. A. Norconk, A. L. Rosenberger, and P. A. Garber, eds. New York: Plenum Press, in press. 1996b Subtle Cues of Social Relations in Male Muriqui Monkeys (Brachyteles arachnoides). In New World Primates: Evolution, Ecology and Behavior, W. G. Kinzey, ed. New York: Aldine de Gruyter, in press. Strier, K. B., and T. E. Ziegler 1994 Insights into Ovarian Function in Wild Muriqui Monkeys (Brachyteles arachnoides). American Journal of Primatology 32:31-40. Sussman, R. W. 1992 Male Life History and Intergroup Mobility among Ringtailed Lemurs (Lemur catta). International Journal of Primatology 13:395-413. Sussman, R. W., and P. A. Garber 1987 A New Interpretation of the Social Organization and Mating System of the Callitrichidae. International Journal of Primatology 8:73-92. Symington, M. M. 1987 Ecological and Social Correlates of Party Size in the Black Spider Monkey, Ateles paniscus chamek. Ph.D. dissertation, Department of Anthropology, Princeton University. Trivers, R. L. 1972 Parental Investment and Sexual Selection. In Sexual Selection and the Descent of Man 1871-1971, B. Campbell, ed. Pp. 136-179. Chicago: Aldine. van Hooff, J. A. R. A. M., and C. P. van Schaik 1992 Cooperation in Competition: the Ecology of Primate Bonds. In Coalitions and Alliances in Humans and Other Animals, H.A. Harcourt and F.B.M. de Waal, eds. Pp. 357-389. New York: Oxford University Press. Wallis, J. 1995 Seasonal Influence on Reproduction in Chimpanzees of Gombe National Parks. International Journal of Primatology 16:435-451 Whitten, P. L. 1987 Infants and Adult Males. In Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds. Pp. 343-357. Chicago: University of Chicago Press. Wright, P. C. 1990 Patterns of Paternal Care in Primates. International Journal of Primatology 11:89-102.
K a r e n B. S t r i e r
University of Wisconsin-Madison
Patterns of three variables of r e p r o d u c t i v e strategies in m a l e N e w World primates are examined: (i) h o w males obtain access to p o t e n t i a l mates; (ii) h o w males o b t a i n actual m a t i n g o p p o r t u n i t i e s ; a n d (iii) h o w males affect infant survival a n d female reproductive success. M a l e opportunities to associate with females, w h e t h e r b y r e m a i n i n g in their natal groups, d i s p e r s i n g and f o r m i n g n e w groups, or d i s p e r s i n g and t a k i n g over or j o i n i n g e s t a b l i s h e d g r o u p s , are strongly influenced b y local p o p u lation densities a n d correlate w i t h female r e p r o d u c t i v e rates a n d the extent of female reproductive seasonality a n d synchrony. Differences in male m a t i n g success are affected b y female accessibility, w h e t h e r malemale and male-female r e l a t i o n s h i p s are hierarchical or egalitarian, a n d w h e t h e r female reproduction is seasonally restricted. Patterns of m a l e behavior toward infants, characterized as active assistance, overt interference, or b e n i g n tolerance, a p p e a r to co-vary w i t h differences in the degree to w h i c h males can affect female reproductive rates. These qualitative analyses suggest that the reproductive strategies of male N e w World primates can be classified along a c o n t i n u u m r a n g i n g from conservative to daring d e p e n d i n g on w h e t h e r female r e p r o d u c t i v e rates are relatively slow or fast a n d w h e t h e r r e p r o d u c t i o n is s t r o n g l y or w e a k l y l i n k e d to seasonal ecological variables. M a l e s a d o p t the conservative strategy of staying in their natal groups, forfeiting exclusive m a t i n g opportunities, a n d treating infants w i t h tolerance w h e n female r e p r o d u c -
Received September 29, 1995; accepted December 7, 1995.
Address all correspondence to Karen B. Strier, Department of Anthropology, University of Wisconsin-Madison, 1180 Observatory Drive, Madison, WI 53706. E-mail: strier@macc,wisc.edu Copyright 9 1996 by Walter de Gruyter, Inc., New York Human Nature, Vol. 7, No. 2, pp. 105-123. 105
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tion is constrained by ecological factors. Conversely, males adopt the more daring strategy of dispersing and competing when potential payoffs through their ability to affect female reproduction are high. KEYWORDS:New World primates; Reproductive strategies; Dispersal patterns; Mating success; Infant care; Reproductive seasonality.
Studies from captivity and the wild have provided insights into the diverse reproductive strategies of female New World primates. At one extreme are the rapid reproductive rates of female callitrichids, which may involve the production of twins, or more rarely triplets, at intervals as short as six months, and limited breeding opportunities, including the inhibition of ovulation for subordinate females (Dietz et al. 1994; Garber 1994). At the other extreme are the single infants produced at roughly three-year intervals by the larger-bodied atelins such as spider monkeys (Ateles: Chapman and Chapman 1990) and muriquis (Brachyteles arachnoides: Strier 1991). Single births at one- or two-year intervals characterize most of the other New World monkeys (Ross 1991), but even these primates vary considerably in the degree to which reproduction is constrained by seasonal ecological conditions (Lindburg 1987). Such marked differences in female reproductive biology should interact with ecological and social variables to influence the reproductive strategies of males. Yet, little is known about these interactions, or about more general characteristics of reproductive strategies in New World primate males. Fundamental differences between New World and some well-studied Old World monkeys make it difficult to extrapolate about male reproductive strategies without first understanding the range of behaviors that New World primate males exhibit. For example, in the majority of New World primates, by contrast to most cercopithecines, it is females or both males and females that disperse from their natal groups (Moore 1992; Strier 1994a). New World primates also exhibit striking intra- and interspecific variability in their grouping patterns (Kinzey and Cunningham 1994) and in whether relationships among males and between males and females are hierarchical or egalitarian (Boinski and Mitchell 1994; Strier 1994b). This paper explores the patterning of reproductive strategies among male New World primates by focusing on the interactions among three variables: (i) how males obtain access to potential mates; (ii) h o w males obtain actual mating, and presumably fertilization, opportunities; and (iii) how males affect infant survival and female reproductive success. The distributions of these key variables of male reproductive strategies are examined qualitatively because the paucity of comparative long-term
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field data (spanning at least one generation) precludes more rigorous quantitative analyses for most species. Nonetheless, identifying consistent interacting effects that emerge from this preliminary overview can contribute to hypotheses about the correlates or determinants of N e w World primate male reproductive strategies and provide comparative insights across the Primate order.
VARIABLES OF MALE REPRODUCTIVE STRATEGIES Opportunities to Associate with Females
Rationale. Males require opportunities to associate with one or more females, however briefly, in order to reproduce. At a behavioral level, these opportunities can be distinguished along a continuum ranging from insecure to secure depending on the degree to which males must actively seek out female associates. Dispersal patterns that affect male access to female associates thus provide a first approximation of the degree to which male reproductive strategies involve differential access to potential mates. Opportunities to associate with females are least secure for males that emigrate from their natal groups to establish their own reproductive units, and most secure for philopatric males, which remain in their natal groups throughout life. In long-term studies of Costa Rican mantled howler monkeys (Alouatta palliata) and Venezuelan red howler monkeys (A. seniculus) for example, most males emigrated from their natal groups (Crockett and Pope 1993; Glander 1992), whereas all male muriquis (Brachyteles arachnoides) born during one study since 1982 have remained in their natal group, where they mature into sexually active adults (Strier 1991). Other primates fall along the continuum between these extremes, either as emigrant males that must work their w a y into established female groups or as males that are tolerated in their natal groups until they either inherit the role of breeding male or are able to disperse and establish their own reproductive units. Patterns. Despite some clustering among close phylogenetic relatives (Strier 1994a), N e w World primates are represented across the continuum of dispersal patterns (Table 1). Except in the case of male philopatry, the success of each strategy in terms of opportunity for males to associate with females is strongly influenced by local population densities and demography (e.g., Crockett and Pope 1993; Emlen and Vehrencamp 1983; Sussman 1992), which in turn are affected by ecological factors (Goldizen 1990) and stochastic events (Dunbar 1979). Several genera
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exhibit flexible dispersal patterns that correspond to these local conditions. For example, among the marmosets (Callithrix), tamarins (Saguinus), and howler monkeys (Alouatta), males may wait in their natal groups for mating opportunities or emigrate from their natal groups, either to form new groups or to join established groups (Crockett and Eisenberg 1987; Garber 1994; Garber et al. 1993; Glander 1992; Goldizen 1987). Among squirrel monkeys, male philopatry characterizes one Costa Rican population (Saimiri oerstedi) whereas male dispersal characterizes a Peruvian population (S. sciureus: Mitchell et al. 1991). In most capuchins (Cebus), males disperse from their natal groups, but occasional female migrations and multi-male influxes have been reported (Robinson and Janson 1987; Fedigan 1993). Variability in dispersal patterns among squirrel monkeys has been attributed to differences in the distribution of food resources. Mitchell and colleagues (1991) suggest that differences in the size of preferred food patches are responsible for differences in Peruvian and Costa Rican squirrel monkey dispersal patterns. Large food patches available to Peruvian squirrel monkeys offer advantages for cooperation among female kin in resource defense, and consequently, males disperse to avoid inbreeding. The absence of cooperative advantages to defend the smaller food patches exploited by Costa Rican squirrel monkeys, by contrast, favors female-biased dispersal and male philopatry. Among the callitrichids, variability in the timing and pattern of dispersal has been attributed to whether or not breeding opportunities beyond the natal group exist (Baker et al. 1993; Goldizen 1990; Sussman and Garber 1987). More consistent dispersal patterns appear to occur among species that exhibit obligate monogamy and in which both sexes disperse (Aotus and Callicebus [owl and titi monkeys]: Garber 1994), and among some polygamous atelins where females disperse and males are philopatric (Strier 1994b). However, further studies on these taxa at a greater number of sites may ultimately reveal populational differences associated with local conditions similar to those found in other N e w World primate genera for which comparative data are available. Opportunities to Mate with Females
Rationale. Males that associate with females are not necessarily assured of opportunities to mate, and male mating success correlates imperfectly with actual or probable fertilization success (Gray 1985). Nevertheless, in the absence of genetic paternity tests or reliable data on the precise timing of female ovulation relative to copulations, examining the variance in male mating success can provide a rough estimate of the degree to which males are able to monopolize sexual, and potentially reproductive, access to females.
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Variance in male mating success is determined by a number of factors, including the number and ratio of breeding females to males, whether females reproduce seasonally or in synchrony, and whether males employ aggression to compete among themselves for access to females or to coerce females into mating with them (Cowlishaw and Dunbar 1991; van Hooff and van Schaik 1992; Strier 1994b). When males are able to monopolize access to females, either by forming exclusive liaisons or by interrupting the sexual liaisons females establish with other males, the variance in male mating success should be high. Conversely, the variance in male mating success should be low w h e n the ability of males to maintain exclusive mating privileges is limited, either because of the number of simultaneously receptive females or because egalitarian relationships between the sexes prevent males from overriding female mate choices. The range of strategies males employ to monopolize mating opportunities, and therefore increase variance in mating success, can thus be characterized along a continuum in which variance is highest when one male is able to monopolize all copulations, intermediate w h e n copulations are biased in favor of one male, and lowest when copulations are shared among males. Patterns. Variance in male mating success is distributed predictably across the New World primates (Figure 1). In those genera that routinely
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form pair bonds (e.g., Aotus, Callicebus), the greatest variance in male mating success occurs between mated and unmated males. Among those males that succeed in securing mates, however, the intraspecific variance in mating success is presumably low. In taxa with polygamous mating systems, the lowest variance in mating success occurs in the egalitarian societies of muriquis (Strier 1992, 1994b) and some callitrichids (e.g., Saguinusfuscicollis: Goldizen 1990; S. mystax: Garber et al. 1993) where all or most males have been observed to mate. In the hierarchical societies of other polygamous taxa, whether copulations are restricted to the dominant male, defined as the consistent winner of agonistic contests, or only biased in his favor appears to d e p e n d on the extent to which female choice parallels or deviates from the outcome of male-male competition for rank. Although male golden lion tamarins (Leontopithecus rosalia) frequently migrate in pairs, the dominant male has most often been observed to copulate with estrous females (Baker et al. 1993). In some capuchins (e.g., Cebus apella: Janson 1984; C. olivaceus: O'Brien 1991), receptive females solicit copulations almost exclusively from the dominant male despite the presence of subordinate males. In C. albifrons (Janson 1986) and C. capucinus (Fedigan 1993), however, there is no evidence that females mate preferentially or exclusively with the dominant male. Paternity studies of multi-male red howler monkey troops (Alouatta seniculus) reveal strong rank effects on male reproductive success (Pope 1990), despite the fact that alliances between red howler monkey males facilitate their ability to establish or remain in association with females (Crockett and Pope 1993). Copulations appear to be strongly biased in Costa Rican squirrel monkeys (Saimiri oerstedi), with the dominant male accounting for roughly 70% of all copulations observed during one mating season (Boinski 1987a), and somewhat biased in favor of dominant male woolly monkeys (Lagothrix: Nishimura 1990) and spider monkeys (Ateles: Symington 1987). However, contrary to predictions that strong reproductive seasonality should make it difficult for dominant males to monopolize sexual access to multiple receptive females (e.g., van Hooff and van Schaik 1992), the effects of male rank on mating success appear to be more pronounced in the seasonally breeding squirrel monkeys (Boinski 1987a, 1987b) than they are in the less seasonal polygamous spider m o n k e y s (Chapman and Chapman 1990) and muriquis (Strier 1996a). Indeed, among capuchin monkeys, mating success is strongly biased in favor of the dominant male in populations with pronounced birth peaks (Cebus apella: Janson 1984; Robinson and Janson 1987; and C. olivaceus: O'Brien 1991) but more evenly distributed across males in populations in which births occur during an extended (six-month) period (C. capucinus: Fedigan 1993; Fedigan and Rose 1995).
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Male Influence on Infant Survival and Female Reproduction
Rationale. Male reproductive strategies, like those of females, extend beyond mating opportunities to include their relationships with infants (Sussman and Garber 1987; Whitten 1987). Male behavior toward infants can be categorized along a continuum ranging from active assistance to benign tolerance to overt interference, expressed most extremely by infanticidal tendencies (Small 1990). Whether males help or hinder infant survival may correspond to the degree of genetic relatedness between a male and an infant, with fathers and kin more likely to promote than interfere with infants that share some common genetic interests (Trivers 1972). However, factors such as body size energetics (Wright 1990), social benefits (Smith and Whitten 1988; Small 1990), future reproductive opportunities (Baker et al. 1993), and the value of experience with infant care (Snowdon 1990) may be better predictors of male behavior toward infants than paternity or degree of relatedness. An alternative way of evaluating male behavior toward infants is to consider how differences in the ability of males to affect future female reproductive success correlate with male strategies. Female reproductive potential is determined by at least two factors: intrinsic reproductive rates (Ross 1991) and the degree to which the timing of reproduction can be altered. For N e w World primate females with high reproductive rates, males bear a large share of the energetic costs of infant care, thereby helping females recover their energy reserves for subsequent reproduction (Leutenegger 1980; Wright 1990). When female reproductive rates are intrinsically low, but not tightly linked to seasonal ecological conditions, males may benefit by interfering with the survival of unrelated infants because doing so will bring females, w h o s e lactation has been interrupted, into estrus more quickly (Hrdy 1979). Male tolerance toward infants, by contrast, should reflect low female reproductive rates coupled with seasonally restricted reproduction, because neither assistance nor interference by males will enable females to reproduce sooner than they would in the appropriate season. Patterns. As predicted, the clustering of infant care by male N e w World primates corresponds to male ability to affect female reproduction (Figure 2). High levels of male infant care have been observed in the callitrichids (Dietz and Baker 1993; Garber 1994; Goldizen 1990; Sussman and Garber 1987) and in the monogamous owl monkey (Aotus) and tiff monkey (Callicebus), where assistance by males helps females to recover their energy to reproduce again (Wright 1990) and increases infant survivorship (Sussman and Garber 1987). In howler monkeys, where female reproductive rates are relatively low, and in at least some popula-
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Figure 2. Continuum of male behavior toward infants, shown as axes for subsequent comparisons, and male effect on female reproduction. Arrows represent variation in behavior; curves represent overlapping domains. References cited in text. tions not tightly seasonal (Alouatta seniculus, A. palliata), overt interference in the form of suspected infanticide by unrelated males has been reported (Crockett and Eisenberg 1987). In other genera in which female reproductive rates are similarly slow, and reproduction is to varying degrees confined to particular seasons, the behavior males display toward infants corresponds to the effects male assistance or interference can have on female reproductive biology. The fact that infanticide by males has been reported in both seasonal Cebus olivaceus (O'Brien 1991) and aseasonal C. capucinus (Fedigan 1993) is therefore consistent with evidence that capuchin monkey interbirth intervals generally range between one and two years depending on infant survivorship (Robinson and Janson 1987; Fedigan and Rose 1995).
INTERACTING EFFECTS BETWEEN PARAMETERS Dispersal Patterns and Variance in Male Mating Success
N e w World primate dispersal patterns correspond imperfectly with male mating success (Figure 1). Although philopatric males tend to have
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lower variance in mating success than do males that disperse from their natal groups, there are nonetheless marked differences in male mating success across taxa with similar dispersal systems. Thus, although malebiased dispersal has been reported in all capuchin monkeys, variance in male mating success is high in Peruvian Cebus apella and relatively low in sympatric C. albifrons (Janson 1986). Conversely, although male philopatry occurs in both woolly monkeys (Lagothrix), spider monkeys (Ateles), and muriquis (Brachyteles arachnoides), the higher variance in male woolly monkey and spider monkey mating success is consistent with the more hierarchical relationships that exist among males and b e t w e e n males and females (Strier 1994b). Egalitarian relationships among muriquis prevent males from overtly competing for sexual access to females or from coercing females into undesirable liaisons (Strier 1992), and female choice of multiple mates maintains low variance in male mating success (Strier 1994b). Male mating success is biased in favor of dominant males in both philopatric male squirrel monkeys (Saimiri oerstedi) and dispersing male squirrel monkeys (S. sciureus: Boinski and Mitchell 1994). However, unlike the stable egalitarian relationships that persist year-round in muriquis, affiliative relationships among philopatric male S. oerstedi in Costa Rica appear to become more hierarchical during the restricted mating season (Baldwin 1992; Boinski 1987a), resulting in skewed mating opportunities that resemble those among unrelated male S. sciureus.
Variance in Male Mating Success and Reproductive Seasonality Differences in the degree of reproductive seasonality that affect female mate choice may account for some of the differences in the variance in male mating success among N e w World primates (Figure 3). Strong reproductive seasonality imposes high costs on females that fail to conceive and reproduce at the appropriate time and should therefore favor either strong male-male competition (e.g., Leontopithecus rosalia: Dietz et al. 1994) or strong female mate choice for males that are most likely to succeed at fertilization (e.g., Saimiri oerstedi: Boinski 1987a) or provide access to preferred foods (e.g., Cebus apella: Janson 1986). When reproduction is less seasonally constrained, however, females that fail to conceive can continue to cycle until conception occurs. These females may still discriminate among potential mates for any number of other attributes, and may benefit by earlier conceptions. Nonetheless, lower variance in male mating success may be a consequence of more relaxed time constraints on female reproduction (e.g., Cebus capucinus: Fedigan 1993).
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Patterns of male dispersal, mating success, and behavior toward infants. Dotted lines represent axes of male behavior toward infants s h o w n in Figure 2. Initials as in Figures 1 and 2; data on reproductive seasonality in Peruvian Saimiri are unavailable.
Effects o f F e m a l e R e p r o d u c t i o n P o t e n t i a l
Male ability to affect female reproduction maps on to other components of male reproductive strategies, such as dispersal patterns (Figure 4). It may be no coincidence, for example, that male philopatry and tolerance toward infants occurs when female reproduction is most strongly constrained by low reproductive rates or seasonality, while male dispersal and potential interference with infant survival appears to be more prevalent when males can affect the timing of female reproduction. The reproductive strategies employed by male N e w World primates can thus be distinguished as conservative w h e n female reproduction is constrained by ecological or endocrinological factors, and daring w h e n female reproduction can be altered. Males appear to adopt the conservative strategy of staying in their natal groups and potentially forfeiting exclusive mating opportunities when there is little they can do to increase the intrinsic reproductive rates of females9 Conversely, males adopt the riskier strategy of dispersing and competing when the potential pay-offs through their ability to affect female reproduction are high. In each strategy, seasonal constraints on reproduction appear to determine h o w selective females are in their choice of mates and thus h o w variable male mating success will be.
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Human Nature, Vol. 7, No. 2, 1996 r c @ o Q.
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PREDICTIONS
Such divergent alternatives, like all other components of New World primate male behavior reviewed here, represent extremes along a continuum. The patterns emphasize, however, the importance of female reproductive biology and ecology to male reproductive strategies. Simplifying the interacting effects between these variables also leads to testable predictions that may explain some of the diversity in behavior exhibited by New World primate males. For example, the prediction that more restricted breeding seasonality should occur among philopatric male squirrel monkeys than among squirrel monkeys in which males routinely disperse can be evaluated with comparative data on the timing of reproduction in populations with different dispersal systems. Similarly, the related predictions that infanticide should be prevalent only in those populations where females can reproduce throughout all or most of the year, whereas male tolerance toward infants should be m o r e prevalent in populations that inhabit highly seasonal environments where reproduction is temporally restricted, could be evaluated with comparative data on reproductive seasonality across different populations and species of howler monkeys and capuchin monkeys.
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EXTENDING THE MODEL Future Directions
The apparent relationships between female reproductive ecology and male reproductive strategies emphasize the importance of extending our knowledge of primate reproductive physiology from captive studies to the wild, where the effects of seasonal dietary correlates of reproduction can be assessed. Several possible mechanisms may be responsible for whether reproduction is seasonal or aseasonal, including differential responses to changes in photoperiod, rainfall patterns that affect food availability and consequently both female nutritional condition and the timing of weaning, and social pressures favoring reproductive synchrony (Clarke et al. 1992; Lindburg 1987). Yet, understanding how female reproductive hormones respond to these environmental pressures has been limited because measuring female endocrinological condition in the wild has been difficult. The recent development of noninvasive fecal steroid assays for New World primates now makes it possible to monitor reproductive hormones in wild monkeys, and to correlate subtle changes in female reproductive physiology with seasonality in diet and behavior (Strier and Ziegler 1994). These techniques permit more precise evaluations of the timing of mating behavior relative to ovulation, and of the timing of conception relative to ovulatory cycles. Such precision may be especially important to understanding the onset of ovulation and the postpartum resumption of ovulation in species in which nonreproductive sexual activity is common (Hrdy 1981). Noninvasive techniques can also be applied to monitor the effects of seasonality and female reproductive biology on male behavior and reproductive physiology. For example, male weight gain just prior to the breeding season has been reported from field studies of both Saimiri (Baldwin 1992) and Leontopithecus (Dietz et al. 1994). Little is currently known, however, about similar metabolic responses in other New World primates or about how such weight changes interact with social behavior and ecology to affect male reproductive strategies. Further Comparative Perspectives
Some of the apparent patterns in the reproductive strategies of male New World primates may be relevant to understanding the diversity of male reproductive strategies in other primates, including humans. For example, the association between tight reproductive seasonality, high metabolic costs of reproduction for females, and female dominance in lemurs (Richard and Dewar 1991) is consistent with two corollaries of
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the model. First, the tolerance and occasional help male lemurs exhibit toward infants are consistent with their seasonal breeding and the limits it imposes on the ability of males to affect female reproduction (Morland 1990). Second, males of at least some lemur species (e.g., Varecia variegata) resemble Costa Rican squirrel monkeys both in their low rates of aggressive competition outside of the breeding season and in the choices females express for particular males (Morland 1993). Male-biased dispersal in lemurs, like male philopatry in many New World primates, is not sufficient to predict consistent patterns of social relationships and behavior. Furthermore, the fact that male lemurs may disperse as cohorts and emigrate repeatedly depending on local sex ratios (Sussman 1992) is consistent with a strategy that minimizes risks to both male survival and male associations with females because the timing of female reproduction in these primates cannot be substantially altered. Despite marked differences in ecology and social organizations, the low reproductive rates of female hominoids lead to some predictable patterns in male reproductive strategies that correspond to the degree of reproductive seasonality. For example, the evidence that relationships among philopatric male chimpanzees are more hierarchical than those among male bonobos corresponds to more constrained reproductive seasonality in chimpanzees (Nishida et al. 1990; Wallis 1995) and prolonged female receptivity in bonobos (Furuichi 1989; Ihobe 1992). The variability described in male gorilla dispersal patterns, which encompass every possible alternative from emigration to philopatry (Robbins 1995), resembles that reported for New World callitrichids. However, the higher variance in male gorilla mating success and the lack of active assistance by male gorillas toward infants are consistent with predictions based on their less seasonal reproduction and lower reproductive rates. Changes in the reproductive biology of female hominids have figured prominently in many scenarios of h u m a n social evolution. While these models differ from one another concerning attribution of changes in female reproductive patterns to selection pressures favoring the inclusion of meat in the diet, larger brains, or correspondingly longer periods of infant dependency (e.g., Foley and Lee 1991; Lovejoy 1981; Martin 1981), they uniformly recognize the pivotal role of female reproductive biology on male behavior (e.g., Alexander and Noonan 1979). The present analysis of variables involved in the reproductive strategies of male New World primates also leads to specific predictions about how female reproductive biology may have influenced male hominids. Indeed, m a n y contemporary h u m a n foraging societies conform to the predictions that link birth seasonality, which is widespread in h u m a n s (Ellison 1994), with the prevalence of patrilocal residence and cooperation in subsistence efforts (Strier 1996b). Knowledge of the ecological
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conditions that m a y h a v e affected f e m a l e r e p r o d u c t i v e s e a s o n a l i t y in early h o m i n i d s w o u l d be instructive in p e r m i t t i n g us to e s t i m a t e w h e n a n d to w h a t d e g r e e h o m i n i d m a l e s a d o p t e d such c o n s e r v a t i v e r e p r o d u c tive strategies, a n d h o w variable s u c h strategies m a y h a v e b e e n across h o m i n i d species a n d p o p u l a t i o n s . I am grateful to Dr. Ben Campbell for inviting me to present a version of this paper at the symposium he organized on Reproduction in Males: Physiology, Ecology and Behavior for the 65th annual meeting of the American Association of Physical Anthropologists. Participation at this meeting and the associated research were supported by funds from NSF grant BNS 8959298. P. A. Garber, J. W. Lynch, and C. T. Snowdon provided valuable comments on an earlier draft of this manuscript. Karen B. Strier (B.A., 1980, Swarthmore College; M.A., 1981 and Ph.D., 1986, Harvard University) is Professor and Chair of the Department of Anthropology, University of Wisconsin-Madison. She is interested in primate behavioral ecology and conservation and has been studying the endangered muriqui monkeys of Brazil since 1982. She is the author of Faces in the Forest (Oxford University Press, New York, 1992).
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