Competitive regimes and female bonding in two species of squirrel monkeys (Saimiri oerstedi and S. sciureus)

Summary Ecological and behavioral data from long-term field studies of known individuals in two closely related squirrel monkey species (Saimiri oerstedi and S. sciureus) were used to examine hypotheses about the source of variation in female bonding among group-living primates. Social relationships in species which live in cohesive groups are thought to depend on the nature of competition for resources. S. oerstedi and S. sciureus both live in large groups and are subject to intense predation. Direct feeding competition both between and within groups is extremely low in S. oerstedi; in this species female relationships are undifferentiated, no female dominance hierarchy is evident and females disperse from their natal group. S. sciureus also experiences very low levels of between-group competition, but within-group direct competition for resources is frequent; this species demonstrates differentiated female relationships, a female dominance hierarchy, and female philopatry. The correlated ecological and social variables found in these two congeners further minimize the minor effects of phylogenetic differences and emphasize the importance of food distribution in determining social characteristics. Offprint requests to: S. Boinski     

Socioecological influences on the reproductive success of female mountain gorillas (<Emphasis Type="Italic">Gorilla beringei beringei</Emphasis>)

Over the past few decades, socioecological models have been developed to explain the relationships between the ecological conditions, social systems, and reproductive success of primates. Feeding competition, predation pressures, and risk of infanticide are predicted to influence how female reproductive success (FRS) depends upon their dominance rank, group size, and mate choices. This paper examines how those factors affected the reproductive success of female mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes, Rwanda from 1967–2004. Reproductive success was measured through analyses of interbirth intervals, infant survival, and surviving infant birth rates using data from 214 infants born to 67 females. Mountain gorillas were predicted to have “within-group scramble” feeding competition, but we found no evidence of lower FRS in larger groups, even as those groups became two to five times larger than the population average. The gorillas are considered to have negligible “within-group contest” competition, yet higher ranked mothers had shorter interbirth intervals. Infant survival was higher in multimale groups, which was expected because infanticide occurs when the male dies in a one-male group. The combination of those results led to higher surviving birth rates for higher ranking females in multimale groups. Overall, however, the socioecological factors accounted for a relatively small portion of the variance in FRS, as expected for a species that feeds on abundant, evenly distributed foliage.     

Competition and group size in Thomas’s langurs (Presbytis thomasi): the folivore paradox revisited

Among primates, group size is highly variable. The standard ecological model assumes that better predation avoidance as group size increases favours living in larger groups, whereas increased travel costs and reduced net food intake due to within-group competition for resources set the upper limit. Folivorous primates, however, tend to defy this generalisation in that some live in small groups despite low costs of feeding competition. To resolve this ’folivore paradox’, it has been suggested that folivore group size is limited by social factors such as male harassment or infanticide, or that females can disperse more easily and thus maintain group size near optimum levels. In this paper, we examine the effects of group size on home range size, day-journey length, activity budget and diet in wild Thomas’s langurs (Presbytis thomasi), which live in one-male multi-female groups with a limited life cycle. We examined only data from the stable middle tenure phase when factors such as the strength of the breeding male or the way in which groups were formed did not influence ranging and activities. During this phase, group size affected day-journey length and home range size, and had a minor effect on diet, but did not influence time spent feeding or resting, allogrooming or birth rates. Hence the upper limit to group size during the middle tenure phase in Thomas’s langurs is not set by feeding competition. The folivore paradox is not due to frequent female dispersal in Thomas’s langurs. The timing of female dispersal is not as expected if it serves to keep group sizes near the ecological optimum, and groups seem to be below this optimum. Instead, female reproductive success is presumably maximised in small to mid-sized groups because larger groups show a clear trend to experience higher risk of take-over, often accompanied by infanticide. Because females can redistribute themselves among nearby groups when groups reorganise each time a new male starts up a new group, females can keep the group small. Thus, a social factor, risk of infanticide, seems to provide the selective advantage to small group size in Thomas’s langurs. Received: 29 July 1999 / Revised: 17 November 1999 / Accepted: 15 October 2000     

Ecology,feeding competition and social structure in baboons

Predictions of the model of van Schaik (1989) of female-bonding in primates are tested by systematically comparing the ecology, level of within-group contest competition for food (WGC), and patterns of social behaviour found in two contrasting baboon populations. Significant differences were found in food distribution (percentage of the diet from clumped sources), feeding supplant rates and grooming patterns. In accord with the model, the tendencies of females to affiliate and form coalitions with one another, and to be philopatric, were strongest where ecological conditions promoted WGC. Group fission in the population with strong WGC was “horizontal” with respect to female dominance rank, and associated with female-female aggression during a period of elevated feeding competition. In contrast, where WGC was low, females’ grooming was focused on adult males rather than other females. Recent evidence suggests that group fission here is initiated by males, tends to result in the formation of one-male groups, and is not related to feeding competition but to male-male competition for mates. An ecological model of baboon social structure is presented which incorporates the effects of female-female competition, male-male competition, and predation pressure. The model potentially accounts for wide variability in group size, group structure and social relationships within the genus Papio. Socio-ecological convergence between common baboons and hamadryas baboons, however, may be limited in some respects by phylogenetic inertia. Received: 22 April 1994/Accepted after revision: 9 December 1995     

Females go where the food is: does the socio-ecological model explain variation in social organisation of solitary foragers?

The socio-ecological model (SEM) links ecological factors with characteristics of social systems and allows predictions about the relationships between resource distribution, type of competition and social organisation. It has been mainly applied to group-living species but ought to explain variation in social organisation of solitary species as well. The aim of this study was to test basic predictions of the SEM in two solitary primates, which differ in two characteristics of female association patterns: (1) spatial ranging and (2) sleeping associations. Beginning in August 2002, we regularly (re-)captured and marked individuals of sympatric populations of Madame Berthe's and grey mouse lemurs (Microcebus berthae, Microcebus murinus) in Kirindy Forest (Madagascar). We recorded data on spatial patterns, feeding and social behaviour by means of direct observation of radio-collared females. The major food sources of M. berthae occurred in small dispersed patches leading to strong within-group scramble competition and over-dispersed females with a low potential for female associations. In contrast, M. murinus additionally used patchily distributed, high-quality (large) resources facilitating within-group contest competition. The combined influence of less strong within-group scramble and contest as well as between-group contest over non-food resources allowed females of this species to cluster in space. Additionally, we experimentally manipulated the spatial distribution of food sources and found that females adjusted their spatial patterns to food resource distribution. Thus, our results support basic predictions of the SEM and demonstrated that it can also explain variation in social organisation of solitary foragers.     

On the evolutionary stability of female infanticide

Territoriality among female rodents may have evolved as an adaptation to intraspecific competition for resources or, alternatively, to defend pups against infanticide. In order to evaluate the latter, we analyse the conditions that allow an infanticidal strategy to invade a population of non-infanticidal females, and the circumstances under which infanticide may become an evolutionarily stable strategy (ESS). Our game theoretical analyses indicate that infanticide has to be associated with some direct (cannibalism) or indirect (reduced competition) resource benefits in order to invade a non-infanticidal population. We also expect that females will primarily kill litters of nearby neighbors, thereby removing the closest competitors while keeping costs at a low level. However, once established in a population, infanticide may be an ESS, even if females do not gain any resource benefits. This is theoretically possible if a female through infanticide can reduce the possibility that other, potentially infanticidal, females establish and/or stay close to her nest. While behavioral data indicate that these special circumstances sometimes occur, they may be too specific to apply generally to small rodents. Therefore, we expect that the evolutionary stability of infanticide often requires resource benefits, and that female infanticide in small rodents may, in fact, be a consequence rather than a cause of territoriality. Received: 27 June 1996 / Accepted after revision: 28 December 1996     

Vigilance in wild Thomas's langurs (Presbytis thomasi ): the importance of infanticide risk

This study examines vigilance as a behavioural indicator of the importance of infanticide risk by comparing the infanticide avoidance hypothesis with the predation avoidance and mate defence hypotheses for wild Thomas's langurs (Presbytis thomasi) in Sumatra. We found that all individuals were more vigilant in situations of high predation risk, i.e. lower in the trees and in the absence of neighbours. Females were also more vigilant on the periphery of the group. However, there were variations in vigilance levels that could not be accounted for by the predation avoidance hypothesis. Males without infants showed higher levels of vigilance in areas of home range overlap than in non-overlap areas during the early phase of their tenure, strongly suggesting mate defence. In these areas of home range overlap where Thomas's langur groups can interact, males may attack females and infants, and so the infanticide risk for males and females with infants is likely to be high in these areas. Only females with infants, but not males with infants or females without infants, showed higher vigilance levels in overlap areas than in non-overlap areas; in addition, in overlap areas, females with an infant were more vigilant than females without an infant, while this was not the case in non-overlap areas. Both females and males with infants were more vigilant high in the trees than at medium heights in overlap areas but not elsewhere. These findings can only be explained by the infanticide avoidance hypothesis. In contrast to predator attacks, infanticidal male attacks come from high in the canopy, and only occur in overlap areas. There was a significant sex difference in vigilance, but males were only more vigilant than females without an infant, and not more vigilant than females with an infant. We conclude that vigilance varied mainly in relation to the risk of predation and infanticide. Mate competition only played a role for males during the early phase of their tenure. Predation risk seems to offer the best explanation for vigilance for all individuals in the absence of infants. Both predation risk and infanticide risk played a role for females and males with infants. Received: 4 April 1998 / Accepted after revision: 6 September 1998     

Ecological sexual segregation in fallow deer (Dama dama): a multispatial and multitemporal approach

We questioned the different interpretations of ecological sexual segregation from a novel perspective, i.e., by carrying out diverse temporal and spatial scale analyses within a long-term study (1984–2003). Thus we combined spatial (small/large) and temporal (small/large) scale analyses to identify the factors generating sexual segregation in fallow deer in San Rossore, Italy. The study site was divided into an eastern sector characterized by human disturbance (DS) and a western undisturbed sector (US). According to census data, human presence increased in DS from 1984, and while females gradually abandoned it, males remained—thus supporting the predation risk hypothesis (large spatial and temporal scale)—and actually increased their presence in DS, where they seemingly benefited from a lower female density. This supported the indirect competition hypothesis. The analysis of data on a large temporal and small spatial scale confirmed that intersexual competition, in particular for grass, was higher in a crowded pasture in US. Observations by means of radio-telemetry of 23 adult females and 25 adult males (1997–2001, reduced temporal and large spatial scale) showed that large scale segregation was relevant during the day and disappeared at night, when disturbance was absent and also the females reached DS. This also supported the predation risk hypothesis. Moreover, sexes showed different habitat choices inside DS at night, thus supporting the forage selection hypothesis (small spatial and temporal scale). In conclusion, failure to address the whole set of combinations of spatial and temporal scale analyses would have led to monocausal explanations of ecological sexual segregation.     

Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus)

Van Schaik’s socioecological model predicts interrelations among food distribution, competitive regimes, and female social relationships. To test the internal consistency of the model, feeding competition was examined in three differently sized groups of a forest-dwelling population of Hanuman langurs (Semnopithecus entellus). The nutritional condition of females was used as a direct indicator of feeding competition and related to the seasonal variation in resource distribution and abundance. Female dominance hierarchies were characterized by displacements. Dominance hierarchies were significantly linear and relatively stable, but less so with increasing group size. Physical condition correlated with dominance rank and high-ranking females were in the best condition, indicating within-group contest competition. The strength of this relationship became less pronounced with increasing group size. The females of the medium-sized group were in the best physical condition indicating between-group contest plus within-group scramble competition. Closer examination revealed variable costs and benefits of group foraging with a predominance of within-group scramble competition when food was more abundant. The results support some basic predictions of the model. Limiting food abundance was bound to ubiquitous within-group scramble competition. The use of clumped resources translated into differences in net energy gain based on dominance. In contrast to the predictions, group-size-related costs and benefits were related to food abundance instead of food distribution. As predicted, within-group contest competition was linked to a linear dominance hierarchy. The absence of nepotism and coalitions in Hanuman langurs may be attributed to dominance hierarchies that are unstable through time, probably minimizing fitness gain via kin support. Received: 25 May 1999 / Received in revised form: 18 February 2000 / Accepted: 25 February 2000     

Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups – defence pattern, paternity and sexual behaviour

Hypotheses about the evolution of gregariousness and social organisation in primates are based on ecological explanations as well as on social factors such as conspecific threat (especially infanticide by males). The social explanation fits well with the conditions found in strepsirrhine primates and furthermore explains why infanticide in anthropoid primates living in one-male groups mainly occurs when the resident male (protector) is replaced. However, whether it likewise fits to the conditions in multimale groups will depend on the role of resident males as infant protectors, which has rarely been examined. We investigated long-term data of wild Hanuman langurs (Presbytis entellus) inhabiting a forest near the village of Ramnagar (southern Nepal). Twenty-two eye-witnessed attacks on infants by males were analysed in connection with male residency, paternity (DNA analyses) and sexual behaviour. Adult males played a major role in infant defence (65%). Only the genetic father or males who had been residents when the infant was conceived were observed to protect infants. Males who immigrated after a female had conceived may later attack her infant and were never observed to defend it. lt seems that the males took only copulations with potentially fertile females but not with pregnant females as clues for paternity. In the light of these results it seems likely that the risk of infanticide is an important determinant in female-male associations even in anthropoid primate multimale groups. Received: 22 December 1998 / Received in revised form: 30 April 1999 / Accepted: 1 May 1999     

Female philopatry and its social benefits among Bornean orangutans

Female philopatry in mammals is generally associated with ecological and sometimes social benefits, and often with dispersal by males. Previous studies on dispersal patterns of orangutans, largely non-gregarious Asian great apes, have yielded conflicting results. Based on 7?years of observational data and mitochondrial and nuclear DNA analyses on fecal samples of 41 adult Bornean orangutans (Pongo pygmaeus wurmbii) from the Tuanan population, we provide both genetic and behavioral evidence for male dispersal and female philopatry. Although maternally related adult female dyads showed similar home-range overlap as unrelated dyads, females spent much more time in association with known maternal relatives than with other females. While in association, offspring of maternally related females frequently engaged in social play, whereas mothers actively prevented this during encounters with unrelated mothers, suggesting that unrelated females may pose a threat to infants. Having trustworthy neighbors may therefore be a social benefit of philopatry that may be common among solitary mammals, thus reinforcing female philopatric tendencies in such species. The results also illustrate the diversity in dispersal patterns found within the great-ape lineage.     

Variance in the male reproductive success of western gorillas: acquiring females is just the beginning

Variance in male reproductive success is expected to be high in sexually dimorphic mammals, even when it is modulated by the costs and benefits of group living. Here, we investigate the variance in reproductive success of male western gorillas (Gorilla gorilla), a highly dimorphic primate with long-term male–female associations, using 12.5 years of data collected at Mbeli Bai in northern Congo. Access to mates and offspring survival were both major sources of variance in male reproductive success. Males with larger harems had lower offspring mortality with no apparent reduction in female fertility or observed tenure length, so the size of harems did not seem to be limited by female feeding competition or by the risk of takeovers and infanticide by outsider males. The lower mortality in larger harems may reflect improved vigilance against predators, and females may cluster around males that enhance offspring survival. Thus, this study illustrates how a detailed analysis of the components of male reproductive success can shed light on the interrelated social and ecological aspects that affect it.     

Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus

Among social animals, group size is constrained by competition over resources. Because female reproductive success is limited by access to food resources, and that of males by access to fertile females, chimpanzee females are proposed to be less social than males and to maintain weak intrasexual relations. Findings from Taï National Park, Côte d’Ivoire, challenged this view, as chimpanzee females were described as generally gregarious, and close intrasexual bonds were common. Here, in a new analysis that focuses on the South Group of chimpanzees in Taï forest, we reevaluate the proposed differences in female association patterns between the Taï and East African populations. We find that mean party size and dyadic association index between females has decreased in Taï, although the level of dyadic associations remains high compared with East African chimpanzees. We attribute the decrease in female gregariousness to the decline in community size over the last 10 years. In addition, we use a multivariate approach to analyze social and ecological factors influencing party size in females. We show that female gregariousness increased when the fruit resources were more clumped and with increased number of females in estrus present. Party size of mothers with sons, however, was smaller with increasing number of sexually receptive females. The results of our model and the reviewed findings of other studies support the socioecological model because food distribution affects female gregariousness, but social and demographic aspects are equally influencing female grouping tendencies.     

When females should contest for food – testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus)

Predictions of ecological models on female social relationships (van Schaik 1989) and their links with food distribution and the potential competitive regime are used to analyze the feeding and spatial behavior, and resource density, size, distribution, and quality in a forest population of Hanuman langurs (Presbytis entellus). In contrast to other populations, and assumptions on folivorous primates, the females of this population exhibit a linear dominance hierarchy. The langurs concentrated their feeding on three key resources with a low density and clumped distribution. Two out of the three key resources contained significantly higher levels of extractable protein and soluble sugar than other food plants, indicating high spatial variability of food quality. Even the mature leaves of the most preferred food plant were about twice as nutritious as those from other food plants. Group spread was small and only a single high-quality resource was used at a time. Finally, even rich resources could accommodate only a subset of a group. These findings fit predictions made for the prevalence of within-group contest competition. Given the observed food distribution and phytochemical heterogeneity of mature foliage, even females of folivorous species should contest for food. The effect of female dominance rank on size and composition of feeding parties also agrees with this prediction. A comparison with data from another forest population, where female dominance relations are weakly developed, revealed a clear-cut difference in the use and abundance of resources. It is argued that between-population differences in female social relationships within a species may be viewed as adaptive responses to local habitat conditions. Received: 1 August 1997 / Accepted after revision: 7 December 1997     

Why male orangutans do not kill infants

Infanticide is widespread among mammals, is particularly common in primates, and has been shown to be an adaptive male strategy under certain conditions. Although no infanticides in wild orangutans have been reported to date, several authors have suggested that infanticide has been an important selection pressure influencing orangutan behavior and the evolution of orangutan social systems. In this paper, we critically assess this suggestion. We begin by investigating whether wild orangutans have been studied for a sufficiently long period that we might reasonably expect to have detected infanticide if it occurs. We consider whether orangutan females exhibit counterstrategies typically employed by other mammalian females. We also assess the hypothesis that orangutan females form special bonds with particular “protector males” to guard against infanticide. Lastly, we discuss socioecological reasons why orangutan males may not benefit from infanticide. We conclude that there is limited evidence for female counterstrategies and little support for the protector male hypothesis. Aspects of orangutan paternity certainty, lactational amenorrhea, and ranging behavior may explain why infanticide is not a strategy regularly employed by orangutan males on Sumatra or Borneo.     

Female bank voles (Clethrionomys glareolus) prefer dominant males; but what if there is no choice?

Both intra-sexual competition between males and female mate choice have been found to affect mating behaviour in rodents. We studied female choice in the bank vole (Clethrionomys glareolus) under circumstances where male-male competition was excluded and the female could interact and mate freely with the males. Mating behaviour was observed in two situations: (1) the female encountered two males with a clear dominance relationship; and (2) the two males were equal in their social status. In all tests where a female in postpartum oestrus had a choice between males of different social rank she mated with the dominant one. When choosing between an even pair of males there was no difference in the frequency of lordotic responses, mounts or intromissions the female exhibited with either male before mating with one of them. The mean ejaculation latency was significantly longer in the tests with an even pair of males than in the tests where male hierarchy was clear. These results show that bank vole females are able to discriminate males according to their social status and strongly prefer dominant males as mating partners. However, when the females were presented with two equal males, they seemed to be unable to make a choice. The ability to choose the mating partner when the males are clearly different may be an important direct benefit for the female in terms of time saved during mating and thus decreased risk of predation and infanticide. Received: 16 March 1995/Accepted after revision: 11 February 1996     

Sex-biased dispersal in a long-lived polygynous reptile (Crocodylus johnstoni )

We compared natal dispersals of freshwater crocodiles (Crocodylus johnstoni) against the prediction of male dispersal bias for a polygynous mating system. The crocodiles inhabited a linear series of pools and we calculated the net distances from natal pools to recapture locations some 12–18 years later, at maturity. Philopatry was assessed in terms of adult social distances. A female social distance was 0.46 pools and a male social distance was 1.0 pool. By these criteria, both sexes showed low levels of philopatry (7–12%). However, individuals of both sexes dispersed from the natal site long before they were sexually mature. Divergence in dispersal patterns by sex occurred after the maturity threshold, as males dispersed two to three times farther than females. Intrasexual competition by males is resolved by a size-based hierarchy. The displacement of small males from local mating access is a probable cause of the longer dispersals undertaken by males. Competition, rather than inbreeding avoidance, is driving dispersal in this population of freshwater crocodiles. Received: 8 May 1998 / Accepted after revision: 26 June 1998     

Local genetic structure and relatedness in a solitary mammal, Neotoma fuscipes

We used DNA microsatellites to investigate temporal and spatial patterns of local genetic differentiation and relatedness in a solitary mammal, the dusky-footed woodrat (Neotoma fuscipes). Patterns of genetic variation were measured relative to spatial clusters, or neighborhoods, of woodrats. We detected significant genetic differentiation among woodrat neighborhoods in two populations spanning multiple habitat types and densities. Estimates of θ _ST among neighborhoods ranged 0.034–0.075 and were comparable to levels reported in social mammals. Genetic differentiation at such a local scale is noteworthy because it occurred in the absence of any physical barriers to gene flow, suggesting that the patterns observed are linked to the nonrandom patterns of mating and dispersal that characterize woodrat social structure. Genetic differentiation and relatedness among neighborhoods were even higher when only resident females were analyzed. These results are consistent with a pattern of female philopatry and male-biased dispersal in woodrats. Geographic distance and relatedness were inversely correlated in adult females at intermediate densities, but not at low densities. Nonetheless, matrilineal genetic structure was apparent even at low woodrat densities based on estimates of θ _ST among neighborhoods of resident females that were significantly greater than zero and consistently greater than estimates including all individuals. In summary, this study demonstrates a matrilineal genetic structure in dusky-footed woodrats. In addition, our results support the idea that intermediate densities may be better at facilitating the formation of spatial kin clusters than either extreme. An erratum to this article can be found at     

Seasonal variation in feeding behavior, competition and female social relationships in a forest dwelling guenon, the blue monkey (Cercopithecus mitis stuhlmanni), in the Kakamega Forest, Kenya

Socioecological models relate differences in feeding strategies to variation in the nature of female social relationships. Among the African forest guenons, females consume large quantities of fruit and other plant reproductive parts, resources which are thought to promote contest competition, yet these monkeys have been characterized as having agonistically undifferentiated relationships in which rank, if discernible at all, does not correlate with fitness benefits. To determine whether female relationships become more hierarchical under relevant ecological conditions, we monitored the adult females of two blue monkey groups (Cercopithecus mitis stuhlmanni) over a complete annual cycle in the Kakamega Forest, Kenya. Females competed aggressively for plant reproductive parts more often than any other resource type, and in both groups we detected linear dominance hierarchies. Nonetheless, agonism rates remained low throughout our study, and did not vary with changes in ecological conditions. Rather, when plant reproductive parts were scarce, subordinate females spent more time feeding and less time resting in an apparent attempt to compensate for a reduced efficiency of food intake. The effects of rank and food abundance were not reflected, however, in the distribution of grooming. The use of alternative feeding strategies appeared to blunt competition – females of all ranks were unlikely to be near others while feeding and spent more time consuming alternative resources when plant reproductive parts were scarce. The diverse diet of this species may allow females to avoid conflict so that dominance has only subtle effects that are difficult to detect. While socioecological models often simplify the connection between resources and female interactions, our results emphasize that the behavior of animals consuming particular resources, and not the resources themselves, are critical predictors of social patterns.