C. P. van Schaik

The evolution of female social relationships in nonhuman primates

Abstract Considerable interspecific variation in female social relationships occurs in gregarious primates, particularly with regard to agonism and cooperation between females and to the quality of female relationships with males. This variation exists alongside variation in female philopatry and dispersal. Socioecological theories have tried to explain variation in female-female social relationships from an evolutionary perspective focused on ecological factors, notably predation and food distribution. According to the current “ecological model”, predation risk forces females of most diurnal primate species to live in groups; the strength of the contest component of competition for resources within and between groups then largely determines social relationships between females. Social relationships among gregarious females are here characterized as Dispersal-Egalitarian, Resident-Nepotistic, Resident-Nepotistic-Tolerant, or Resident-Egalitarian. This ecological model has successfully explained differences in the occurrence of formal submission signals, decided dominance relationships, coalitions and female philopatry. Group size and female rank generally affect female reproduction success as the model predicts, and studies of closely related species in different ecological circumstances underscore the importance of the model. Some cases, however, can only be explained when we extend the model to incorporate the effects of infanticide risk and habitat saturation. We review evidence in support of the ecological model and test the power of alternative models that invoke between-group competition, forced female philopatry, demographic female recruitment, male interventions into female aggression, and male harassment. Not one of these models can replace the ecological model, which already encompasses the between-group competition. Currently the best model, which explains several phenomena that the ecological model does not, is a “socioecological model” based on the combined importance of ecological factors, habitat saturation and infanticide avoidance. We note some points of similarity and divergence with other mammalian taxa; these remain to be explored in detail.

Why Are Diurnal Primates Living in Groups

There are two main competing theories on the evolution of group living in diurnal nonhuman primates. The first theory claims that predation avoidance favours group living, whereas there are only disadvantages to feeding in a group and feeding competition increases with group size. The second theory claims that there is a feeding advantage to group living deriving from communal defence of high-quality food patches and that predation is not important. These theories have not yet been rigorously tested. In this paper a critical test is proposed: the theories differ in the predicted relationship between a females birth rate and the size of the group in which she lives (Fig. 1). An additional test is concerned with the predicted relationship between population density relative to food availability and average group size. Finally, a critical test is proposed of the hypothesis that increasing group size should lead to reduced predation risk by comparing demographic patterns between areas where predators are still present and where they have disappeared. A total of 23 data sets on 13 species were extracted from the literature and supplemented with four unpublished data sets. In all three tests the results provide strong support for the predation-feeding competition theory and are clearly unfavourable for the theory postulating feeding advantages to group living. Such feeding advantages may, however, gain prominence under some conditions.

THE EVOLUTION OF MONOGAMY IN LARGE PRIMATES: A NEW HYPOTHESIS AND SOME CRUCIAL TESTS

Monogamy among the large primates is not accompanied by high levels of male care for infants. The selective pressures that have led to its evolution in this case are far from clear. In this paper, we evaluate and test four different hypotheses. Monogamy in these species did not evolve because males are unable to defend access to more than one female. Hence, it must be related to behavioural services provided by the male which substantially increase the females reproductive output. Existing data argue against the suggestion that these services involve protection against predators or defence of an exclusive feeding area. We propose that the males service consists primarily in protecting the female against infanticide by other males. Tests that would differentiate this hypothesis unequivocally from other hypotheses are suggested. To the extent that these predictions can be tested with the data currently available, the evidence supports the infanticide hypothesis. We speculate that infanticide avoidance is also responsible for the near-universal occurrence among primates of male-female bonds.

The special role of male Cebus monkeys in predation avoidance and its effect on group composition

SummaryVigilance behavior, predator detection abilities, and responses to real and model predators were studied in two species of capuchin monkeys (Cebus albifrons and C. apella) in a Peruvian lowland rain forest. Adult males were more vigilant than adult females in both species, mainly because the males spent less time feeding and foraging and partly because they were at the periphery more often than the females. The increased vigilance of adult males is reflected in their superior performance in the detection of (model) predators. Adult and subadult males were also far more likely to approach and mob real and model predators. Adults that were outside the center of the group increased foraging activities but cut back an feeding, much of which was done in exposed tree crowns. Current theory suggests that primate groups are multi-male when a single male is unable to defend sexual access to the group of females. In these small capuchin groups, which are multimale, the enhanced safety of females and young provided by extra adult males furnishes a more plausible explanation. A comparison of the two capuchins with the ecologically similar Southeast Asian Macaca fascicularis suggests that the high predation risk outside the group may also have caused the unusual male career profile in capuchins, which have a long tenure of dominants and a very long potential lifespan. Further predictions of this hypothesis are developed.

Phenological changes in a Sumatran rain forest

Phenological observations were made in a Sumatran rain forest during three years (1980–1982). Phenological changes followed a consistent seasonal pattern. The abundance of young leaves and the fall of leaf litter peaked between December and February (first dry season); flowers were most abundant between January and April (first dry and first wet sea son), and ripe fruits in July-August (the second dry season). The fruit of strangling fig trees showed peaks in April and October, both wet season months. Within the study area there was variation in both the phase and the amplitude of the phenological cycles. One year, 1981, displayed mast flowering and fruiting. The observations indicate that the conditions for production were better during the mast year, a finding that facilitates our understanding of the evolution of mast fruiting.

Cyclicity in the structure of female baboon social networks

There is an established and very influential view that primate societies have identifiable, persistent social organizations. It assumes that association patterns reflect long-term strategic interests that are not qualitatively perturbed by short-term environmental variability. We used data from two baboon troops in markedly different habitats over three consecutive seasons to test this assumption. Our results demonstrate pronounced cyclicity in the extent to which females maintained differentiated relationships. When food was plentiful, the companionships identified by social network analysis in the food-scarce season disappeared and were replaced by casual acquaintanceships more representative of mere gregariousness. Data from the fourth, food-scarce, season at one site indicated that few companions were re-united. It is likely that this reflected stochastic variation in individual circumstances. These results suggest that attention could profitably be paid to the effects of short-term local contingencies on social dynamics, and has implications for current theories of primate cognitive evolution.

The evolutionary origin of human hyper-cooperation

Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.

The impact of El Nino on mast fruiting in Sumatra and elsewhere in Malesia

Long-term data on flower and fruit production of the forest commun- ity in two lowland tropical rain forests in north-western Sumatra are presented. The proportion of years with mast fruiting was found to be similar to that found elsewhere in Malesia. However, masting at the two sites, 70 km apart, did not coincide, and showed no correlation with the El Nifio-Southern Oscillation phe- nomenon (ENSO). Comparisons with other sites in Malesia suggest a general waning of ENSOs impact toward western Malesia. Spatial variation at various scales in the timing of masting events was noted in Sumatra and elsewhere. This suggests that additional factors to ENSO play a role in determining forest-level mast fruiting, and we hypothesize that frugivorous animals have the opportunity to track mast fruiting. It is hypothesized that asynchrony between nearby areas in masting increases toward the western edge of Malesia.

A pilot study of the social correlates of levels of urinary cortisol, prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis)

Urine samples were collected from individuals in a wild population of Sumatran long-tailed macaques (Macaca fascicularis), and the levels of cortisol, immunoreactive prolactin, and (for males) testosterone were determined. The amount of foraging during the 2 hr preceding urine collection were found to affect the levels of urinary cortisol, but not those of the other hormones. Immigration into a new group and having ones infant kidnapped led to increased levels of cortisol. Levels of cortisol and testosterone were correlated both within and between individuals, whereas prolactin varied independently. The effects of age, reproductive status, and social rank on the mean values of individuals were also examined. Lactating females had higher prolactin levels than non-lactating ones; reproductive state interacted with the age effect on prolactin and possibly cortisol. No effects of social status were found in spite of a small, but consistent effect of rank on birth rate in this population. Among males, age and rank are strongly linked. The low ranking old males had increased levels of cortisol, even though the younger high-ranking males were involved in the fiercest conflicts.

Manufacture and use of tools in wild Sumatran orangutans

The manufacture and use of tools in great apes may provide insights into the evolution of hominid cognitive abilities [1] and technology [2]. So far, the common chimpanzee (Pan troglodytes) is the only nonhuman species known to show extensive manufacture and flexible use of tools in nature [2], suggesting that these skills arose only in the chimpanzee-hominid clade [2, 3], around 7 million years ago [4]. Here we report on the habitual manufacture and use of tools in wild Sumatran orangutans (Pongo pygmaeus abelii) to extract social insects and their products from tree holes, and edible seeds from a fruit. These observations strongly suggest that the capacity to produce simple stone tools was already present in the last common ancestor of orangutans and the African hominoids. Orangutans present a paradox. Although virtually no tool use has been seen in the wild, that of captives and rehabilitants is at least as complex as that of chimpanzees [5-7] . One interpretation is that wild orangutans possess the cognitive capacity to make and use tools for foraging, but simply do not need tools in their current habitat [7, 8]. However, wild orangutans also show much less tool use than chimpanzees in nonforaging contexts [8, 9]. Another, equally plausible, interpretation is that the technological skills displayed in captivity reflect a combination of exposure to human tool use, a high capacity for imitation or emulation, and strong exploratory tendencies