Kay E. Holekamp

Fission-Fusion Dynamics: New Research Frameworks

Renewed interest in fission‐fusion dynamics is due to the recognition that such dynamics may create unique challenges for social interaction and distinctive selective pressures acting on underlying communicative and cognitive abilities. New frameworks for integrating current knowledge on fission‐fusion dynamics emerge from a fundamental rethinking of the term “fission‐fusion” away from its current general use as a label for a particular modal type of social system (i.e., “fission‐fusion societies”). Specifically, because the degree of spatial and temporal cohesion of group members varies both within and across taxa, any social system can be described in terms of the extent to which it expresses fission‐fusion dynamics. This perspective has implications for socioecology, communication, cognitive demands, and human social evolution.

Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas

Within any hierarchical society, an individuals social rank can have profound effects on its health and reproductive success, and rank-related variation in these traits is often mediated by variation in endocrine function. Maternal effects mediated by prenatal hormone exposure are potentially important for non-genetic inheritance of phenotypic traits related to social rank, and thus for shaping individual variation in behaviour and social structure. Here we show that androgen concentrations in wild female spotted hyaenas (Crocuta crocuta) are higher during late gestation in dominant females than in subordinate females. Furthermore, both male and female cubs born to mothers with high concentrations of androgens in late pregnancy exhibit higher rates of aggression and mounting behaviour than cubs born to mothers with lower androgen concentrations. Both behaviours are strongly affected in other mammals by organizational effects of androgens, and both have important effects on fitness in hyaenas. Therefore, our results suggest that rank-related maternal effects of prenatal androgen exposure can adaptively influence offspring phenotype in mammals, as has previously been shown to occur in birds. They also suggest an organizational mechanism for the development of female dominance and aggressiveness in spotted hyaenas, traits that may offset the costs of extreme virilization.

Patterns of Association among Female Spotted Hyenas (Crocuta crocuta)

We examined subgroup association patterns among adult female members of a clan of free-living spotted hyenas ( Crocuta crocuta ) and between adult females and their juvenile offspring during three consecutive stages of development of offspring. These stages represented the approximate periods of residence of offspring at the communal den, from 1 to 8 months of age, between leaving the communal den and weaning, from 8 to 14 months, and between weaning and reproductive maturity or dispersal, from 14 to 36 months of age. Mean association indices among adult female dyads varied with social rank, with the highest mean association index observed for the alpha female. Adult females associated more closely with their adult female kin than with unrelated adult females. Female kin from high-ranking matrilines associated more closely than did kin from lower-ranking matrilines. Within mother-offspring pairs, association patterns were strongly influenced by the mothers social rank during all three stages of development of offspring, with high-ranking mother-offspring dyads associating more tightly than low-ranking dyads at each stage. Mean mother-offspring association indices declined as offspring grew older, but we found no significant differences based on sex of offspring during any of the developmental stages examined.

Innovative problem solving by wild spotted hyenas

Innovative animals are those able to solve novel problems or invent novel solutions to existing problems. Despite the important ecological and evolutionary consequences of innovation, we still know very little about the traits that vary among individuals within a species to make them more or less innovative. Here we examine innovative problem solving by spotted hyenas (Crocuta crocuta) in their natural habitat, and demonstrate for the first time in a non-human animal that those individuals exhibiting a greater diversity of initial exploratory behaviours are more successful problem solvers. Additionally, as in earlier work, we found that neophobia was a critical inhibitor of problem-solving success. Interestingly, although juveniles and adults were equally successful in solving the problem, juveniles were significantly more diverse in their initial exploratory behaviours, more persistent and less neophobic than were adults. We found no significant effects of social rank or sex on success, the diversity of initial exploratory behaviours, behavioural persistence or neophobia. Our results suggest that the diversity of initial exploratory behaviours, akin to some measures of human creativity, is an important, but largely overlooked, determinant of problem-solving success in non-human animals.

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.

Dispersal Status Influences Hormones and Behavior in the Male Spotted Hyena

Male spotted hyenas (Crocuta crocuta) reach puberty at 24 months of age and then invariably emigrate from their natal clans 1 to 38 months later. Thus there are two classes of reproductively mature males in every Crocuta clan: adult natal males born in the clan and adult immigrant males born elsewhere. In one free-living hyena population in Kenya, these two groups of males were compared with respect to measures of aggression, social dominance, sexual behavior, and circulating hormone levels. Adult natal males engaged in higher hourly rates of aggression than did immigrants, won all fights with immigrants, and were socially dominant to immigrants. In addition, adult natal males engaged in far lower hourly rates of sexual behavior with resident females than did immigrants, and natal males were never observed to copulate with natal females. Mean basal plasma cortisol values did not differ between the two groups of adult males, but cortisol concentrations in immigrants were positively correlated with tenure in the clan and with immigrant male social rank. Adult natal males had plasma testosterone levels significantly lower than those of immigrants. Social rank and plasma testosterone values were positively correlated among immigrant males. Thus two different relationships appear to exist between circulating testosterone and social rank in male Crocuta: one apparent in immigrants and the other in natal adult males. Our results suggest that dispersal might disinhibit testosterone secretion in postpubertal male hyenas.

Altered behaviour in spotted hyenas associated with increased human activity

To investigate how anthropogenic activity might affect large carnivores, we studied the behaviour of spotted hyenas (Crocuta crocuta) during two time periods. From 1996 to 1998, we documented the ecological correlates of space utilization patterns exhibited by adult female hyenas defending a territory at the edge of a wildlife reserve in Kenya. Hyenas preferred areas near dense vegetation but appeared to avoid areas containing the greatest abundance of prey, perhaps because these were also the areas of most intensive livestock grazing. We then compared hyena behaviour observed in 1996‐98 with that observed several years earlier and found many differences. Female hyenas in 1996‐98 were found farther from dens, but closer to dense vegetation and to the edges of their territory, than in 1988‐90. Recent females also had larger home ranges, travelled farther between consecutive sightings, and were more nocturnal than in 1988‐90. Finally, hyenas occurred in smaller groups in 1996‐98 than in 1988‐90. We also found several changes in hyena demography between periods. We next attempted to explain differences observed between time periods by testing predictions of hypotheses invoking prey abundance, climate, interactions with lions, tourism and livestock grazing. Our data were consistent with the hypothesis that increased reliance on the reserve for livestock grazing was responsible for observed changes. That behavioural changes were not associated with decreased hyena population density suggests the behavioural plasticity typical of this species may protect it from extinction.

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.

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.

Brain size predicts problem-solving ability in mammalian carnivores

Significance Intelligence presents evolutionary biology with one of its greatest challenges. It has long been thought that species with relatively large brains for their body size are more intelligent. However, despite decades of research, the idea that brain size predicts cognitive abilities remains highly controversial; little experimental support exists for a relationship between brain size and the ability to solve novel problems. We presented 140 zoo-housed members of 39 mammalian carnivore species with a novel problem-solving task and found that the species’ relative brain sizes predicted problem-solving success. Our results provide important support for the claim that brain size reflects an animal’s problem-solving abilities and enhance our understanding of why larger brains evolved in some species. Despite considerable interest in the forces shaping the relationship between brain size and cognitive abilities, it remains controversial whether larger-brained animals are, indeed, better problem-solvers. Recently, several comparative studies have revealed correlations between brain size and traits thought to require advanced cognitive abilities, such as innovation, behavioral flexibility, invasion success, and self-control. However, the general assumption that animals with larger brains have superior cognitive abilities has been heavily criticized, primarily because of the lack of experimental support for it. Here, we designed an experiment to inquire whether specific neuroanatomical or socioecological measures predict success at solving a novel technical problem among species in the mammalian order Carnivora. We presented puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species from nine families housed in multiple North American zoos. We found that species with larger brains relative to their body mass were more successful at opening the boxes. In a subset of species, we also used virtual brain endocasts to measure volumes of four gross brain regions and show that some of these regions improve model prediction of success at opening the boxes when included with total brain size and body mass. Socioecological variables, including measures of social complexity and manual dexterity, failed to predict success at opening the boxes. Our results, thus, fail to support the social brain hypothesis but provide important empirical support for the relationship between relative brain size and the ability to solve this novel technical problem.