Anne L. Engh

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.

Female chacma baboons form strong, equitable, and enduring social bonds

Analyses of the pattern of associations, social interactions, coalitions, and aggression among chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana over a 16-year period indicate that adult females form close, equitable, supportive, and enduring social relationships. They show strong and stable preferences for close kin, particularly their own mothers and daughters. Females also form strong attachments to unrelated females who are close to their own age and who are likely to be paternal half-sisters. Although absolute rates of aggression among kin are as high as rates of aggression among nonkin, females are more tolerant of close relatives than they are of others with whom they have comparable amounts of contact. These findings complement previous work which indicates that the strength of social bonds enhances the fitness of females in this population and support findings about the structure and function of social bonds in other primate groups.

Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons

Female baboons (Papio hamadryas spp.) must contend with myriad potential stressors on a daily basis. In a previous study on female chacma baboons, Papio hamadryas ursinus, living in the Okavango Delta of Botswana, increases in glucocorticoid (GC) concentrations were associated with female reproductive stage, male immigration and the threat of infanticide. Here, we extend this previous analysis to a larger data set with several additional potential stressors, including actual infanticide and instability in the female dominance hierarchy. A general linear mixed model showed that reproductive state, male immigration, infanticide, female rank instability and predation all had significant effects on GC levels. Lactating females’ GC levels increased in response to the arrival of immigrant males and increased even further when infanticide occurred. In contrast, cycling and pregnant females’ GC levels did not change. Females also showed elevated GCs in response to instability within their own dominance hierarchy, especially if their own ranks were at risk. Females’ stress responses were frequent, but specific to events that threatened their own lives, the lives of their offspring, or their dominance ranks.

Patterns of alliance formation and postconflict aggression indicate spotted hyaenas recognize third-party relationships

The social complexity hypothesis posits that natural selection has favoured the evolution of intelligence in animals living in challenging social environments. Although several primate species have been shown to use information about the social relationships between conspecifics in activities such as recruiting allies or reconciling after fights, this ability to recognize third-party relationships has never been demonstrated in nonprimate mammals. However, the social complexity hypothesis predicts that nonprimates should show some of the same cognitive abilities as primates when many features of their social lives resemble those of primates. Here we tested this prediction with data from a group of free-living spotted hyaenas, Crocuta crocuta, which are gregarious carnivores that live in primate-like societies. First, we examined whether hyaenas consistently supported dominant animals over subordinates when they joined in dyadic fights. The hyaenas overwhelmingly supported the dominant animal in each fight, even when both fighting animals ranked below the supporter, and even when the dominant individual was losing the fight. Next, we examined whether hyaenas preferentially attacked relatives of their opponents after a fight. We found that they were more likely to attack relatives of their opponents after a fight than during a control period, and that they were also more likely to attack relatives of their opponents than to attack low-ranking animals unrelated to their opponents. These results suggest that hyaenas can recognize third-party relationships, and support the idea that social complexity drives the evolution of intelligence in phylogenetically disparate taxa.

Behavioural structuring of relatedness in the spotted hyena ( Crocuta crocuta ) suggests direct fitness benefits of clan-level cooperation

Spotted hyenas (Crocuta crocuta) are gregarious carnivores that live in multigenerational social groups, called clans, containing one to several matrilines. Members of multiple matrilines within a clan cooperate during dangerous interactions with inter‐ and intraspecific competitors. The evolution of cooperation may be influenced by relatedness between individuals, which in turn is influenced by reproductive skew and mate choice, dispersal and territorial behaviours. Behavioural data exist for spotted hyenas, but corresponding data on patterns of relatedness are unavailable; this lack of data makes it difficult to assess the relative importance of selection pressures favouring cooperative behaviour within and among groups. Therefore we conducted a longitudinal analysis of relatedness within a single large clan of spotted hyenas, as well as a cross‐sectional analysis of relatedness among hyenas from multiple clans. Within a clan, patterns of relatedness reflected known pedigree relationships, and relatedness was higher within than among matrilines, even across generations. Although mean within‐matriline relatedness varied among matrilines, it did not decline with matriline rank. On average, clan members were not related closely, due to high levels of male‐mediated gene flow among clans, and relatedness declined very slightly across clan borders. Low mean relatedness within clans suggests that spotted hyenas cooperate with unrelated clan‐mates against close paternal kin in other clans. Our data also suggest that spotted hyenas must derive large net direct fitness benefits from group living and cooperation.

Association patterns among male and female spotted hyenas (Crocuta crocuta) reflect male mate choice

Abstract. Although female animals tend to be choosier than males in selecting mates, sexual selection theory predicts that males should also be choosy when female fecundity varies. Reproductive success among female spotted hyenas varies greatly with social rank. Our goals were therefore to determine whether male hyenas preferentially associate with high-ranking females, and whether male preferences are affected by female reproductive state. Interactions between adult males and females were observed intensively, and association indices calculated for all male-female pairs, over a 7-year period in one population of free-living hyenas. Males initiated most affiliative interactions with females, and males associated most closely with females that were likeliest to be fertile. High- and middle-ranking males associated most closely with high-ranking females, but low-ranking males associated equally closely with females in all rank categories. We used molecular markers to determine the paternity of cubs born during the study period, and found that sires associated more closely with the mothers of those cubs than did non-sires, particularly during the last months before conception. These association data indicate that male spotted hyenas do indeed exhibit selective mate choice, and that they prefer females likeliest to maximize male reproductive success.

Antibodies to canine and feline viruses in spotted hyenas (Crocuta crocuta in the masai mara national reserve

Spotted hyenas (Crocuta crocuta) are abundant predators in the Serengeti ecosystem and interact with other species of wild carnivores and domestic animals in ways that could encourage disease transmission. Hyenas also have a unique hierarchical social system that might affect the flow of pathogens. Antibodies to canine distemper virus (CDV), feline immunodeficiency virus (FIV), feline panleukopenia virus/canine parvovirus (FPLV/CPV), feline coronavirus/feline infectious peritonitis virus (FECV/FIPV), feline calicivirus (FCV), and feline herpesvirus 1 (FHV1) have been detected in other Serengeti predators, indicating that these viruses are present in the ecosystem. The purpose of this study was to determine whether spotted hyenas also had been infected with these viruses and to assess risk factors for infection. Serum samples were collected between 1993 and 2001 from 119 animals in a single clan for which behavioral data on social structure were available and from 121 hyenas in several other clans. All animals resided in the Masai Mara National Reserve. Antibodies to CDV, FIV, FPLV/CPV, FECV/FIPV, FCV, and FHV1 were present in 47%, 35%, 81%, 36%, 72%, and 0.5% of study hyenas, respectively. Antibody prevalence was greater in adults for FIV and FECV/FIPV, and being a female of high social rank was a risk factor for FIV. Hyenas near human habitation appeared to be at lower risk to have CDV, FIV, and FECV/FIPV antibodies, whereas being near human habitation increased the risk for FPLV/CPV antibodies. Canine distemper virus and FECV/FIPV antibody prevalence varied considerably over time, whereas FIV, FPLV/CPV, and FCV had a stable, apparently endemic temporal pattern. These results indicate that hyenas might play a role in the ecology of these viruses in the Serengeti ecosystem. The effect of these viruses on hyena health should be further investigated. The lower prevalence of CDV antibody–positive hyenas near human habitation suggests that reservoirs for CDV other than domestic dogs are present in the Serengeti ecosystem.

Why do female Belding's ground squirrels disperse away from food resources?

Abstract We examined the effects of food provisioning on the natal dispersal behavior of Beldings ground squirrels (Spermophilus beldingi). We provided extra food to adult and yearling females in their maternal territories during pregnancy and lactation, and to offspring of these females in their natal areas for 6 weeks after weaning. We used unprovisioned young of unprovisioned mothers as controls. Provisioning influenced the probability of dispersal from the natal area by female but not male S. beldingi. All surviving male S.␣beldingi dispersed by 55 weeks of age, regardless of whether they and their mothers received extra food. By contrast, we observed a significant trend, beginning 3 weeks after weaning and continuing through the yearling year, for a greater proportion of provisioned than control female S. beldingi to emigrate from the natal area. Competition for food did not appear to influence natal dispersal of females. However, overall population density, density of females weaning litters, and rates of aggression and vigilance among these females, were higher in provisioned than control areas, suggesting that competition for non-food resources was unusually intense in provisioned areas. We propose that juvenile female, but not juvenile male, S. beldingi may emigrate from the natal site to increase access to areas with low densities of conspecifics. Together with findings of earlier workers, our results suggest that spatial and temporal distributions of environmental resources are important influences on the dispersal behavior of female ground squirrels.

Courtship and mating in free-living spotted hyenas

Summary Female spotted hyenas (Crocuta crocuta) are larger and more aggressive than males, and their genitalia are heavily ‘masculinized’. These odd traits in females pose unusual challenges for males during courtship and copulation. Here our goals were to describe and quantify the behavior patterns involved in courtship and copulation in Crocuta, and determine whether rates of affiliative behavior directed toward females by males vary with female age, social rank, or time to conception. We also inquired whether consort formation with a particular female was necessary for a male to sire that female’s cubs. Behavioral observations and paternity data based on 12 microsatellite loci were collected over 11 years from free-ranging hyenas in Kenya. Several of the courtship displays exhibited by male hyenas differed from those found in other carnivores, and appeared to reflect intense motivational conflict between tendencies to approach and flee from females. Most male advances were either ignored by females or elicited aggression from females toward males. Rates of male affiliative behavior toward females peaked around the time of conception. Although males behaved similarly toward young and old females in the highest social rank category, males directed more affiliative behavior toward older than younger females that were mid- and low-ranking. Multiple short mounts usually preceded a long mount, but intromission and ejaculation appeared to occur only during long mounts. Female receptivity was indicated by inhibited aggression toward the male and assumption of a distinctive receptive stance. The only behavior indicative of female proceptivity was following of the male by the female in mating contexts. Some males who sired cubs formed consortships with females whereas others did not, suggesting that individual male hyenas may adopt alternative reproductive tactics to attract and acquire mates. Our results also suggest that low fertility may be an important cost of female virilization in this species.

Coprologic survey of parasites of spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya.

Seventy fecal samples from spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya were examined for parasite eggs and oocysts using sugar flotation. A total of nine parasite genera were identified, and all samples were positive for at least one parasite species. Most individuals were infected with Ancylostoma sp. and Spirometra sp., and these species had the highest median intensity of infection. Other parasites identified include Isospora sp., Taeniidae, Spirurida, Toxocara sp., Mesocestoides sp., Dipylidium sp., and Trichuris sp.