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Benson-Amram, S., & Holekamp, K. E. (2012). Innovative problem solving by wild spotted hyenas. Proc R Soc B, 279, 4087–4095.
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Benson-Amram, S., Weldele, M. L., & Holekamp, K. E. (2013). A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta. Animal Behaviour, 85(2), 349–356.
Abstract: Innovative problem solving enables individuals to deal with novel social and ecological challenges. However, our understanding of the importance of innovation for animals in their natural habitat is limited because experimental investigations of innovation have historically focused on captive animals. To determine how captivity affects innovation, and whether captive studies of animal innovation suffer from low external validity, we need experimental investigations of innovation in both wild and captive populations of the same species in diverse taxa. Here we inquired whether wild and captive spotted hyaenas differ in their ability to solve the same novel technical problem, and in the diversity of exploratory behaviours they exhibit when first interacting with the problem. Our results suggest that wild and captive populations show important differences in their innovative problem-solving abilities. Captive hyaenas were significantly more successful at solving the novel problem, and significantly more diverse in their initial exploratory behaviour, than were wild hyaenas. We were able to rule out hypotheses suggesting that these differences result from excess energy or time available to captive animals. We conclude that captive hyaenas were more successful because captive individuals were less neophobic and more exploratory than their wild counterparts. These results have important implications for our interpretation of studies on innovative problem solving in captive animals and aid our attempts to gain a broader understanding of the importance of innovation for animals in their natural habitat.
Keywords: Crocuta crocuta; innovation; neophobia; problem solving; spotted hyaena
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Engh, A. L., Esch, K., Smale, L., & Holekamp, K. E. (2000). Mechanisms of maternal rank 'inheritance' in the spotted hyaena, Crocuta crocuta. Anim. Behav., 60(3), 323–332.
Abstract: Maternal rank [`]inheritance', the process by which juveniles attain positions in the dominance hierarchy adjacent to those of their mothers, occurs in both cercopithecine primates and spotted hyaenas. Maternal rank is acquired in primates through defensive maternal interventions, coalitionary support and unprovoked aggression ([`]harassment') directed by adult females towards offspring of lower-ranking individuals. Genetic heritability of rank-related traits plays a negligible role in primate rank acquisition. Because the social lives of Crocuta and cercopithecine primates share many common features, we examined whether the same mechanisms might operate in both taxa to promote maternal rank [`]inheritance'. We observed a large clan of free-living spotted hyaenas in Kenya to test predictions of four mechanistic hypotheses. Hyaena rank acquisition did not appear to be directly affected by genetic heritability. Unprovoked aggression from adult female hyaenas was not directed preferentially towards low-ranking cubs. However, high-ranking mothers intervened on behalf of their cubs more frequently and more effectively than low-ranking mothers. Maternal interventions and supportive coalitions appeared to reinforce aggression directed at [`]appropriate' conspecific targets, whereas coalitionary aggression directed at cubs apparently functioned to extinguish their aggressive behaviour towards [`]inappropriate' targets. Young hyaenas and primates thus appear to [`]inherit' their mothers' ranks by strikingly similar mechanisms.
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Holekamp, K. E. (2006). Questioning the social intelligence hypothesis. Trends. Cognit. Sci., 11(2), 65–69.
Abstract: The social intelligence hypothesis posits that complex cognition and enlarged [`]executive brains' evolved in response to challenges that are associated with social complexity. This hypothesis has been well supported, but some recent data are inconsistent with its predictions. It is becoming increasingly clear that multiple selective agents, and non-selective constraints, must have acted to shape cognitive abilities in humans and other animals. The task now is to develop a larger theoretical framework that takes into account both inter-specific differences and similarities in cognition. This new framework should facilitate consideration of how selection pressures that are associated with sociality interact with those that are imposed by non-social forms of environmental complexity, and how both types of functional demands interact with phylogenetic and developmental constraints.
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Holekamp, K. E., Sakai, S. T., & Lundrigan, B. L. (2007). Social intelligence in the spotted hyena (Crocuta crocuta). Philos Trans R Soc Lond B Biol Sci, 362(1480), 523–538.
Abstract: 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.
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Smith, J. E., Kolowski, J. M., Graham, K. E., Dawes, S. E., & Holekamp, K. E. (2008). Social and ecological determinants of fission-fusion dynamics in the spotted hyaena. Anim. Behav., 76(3), 619–636.
Abstract: Theory predicts that individuals living in fission-fusion societies, in which group members frequently change subgroups, should modify grouping patterns in response to varying social and environmental conditions. Spotted hyaenas, Crocuta crocuta, are long-lived carnivores that reside in permanent social groups called clans. Clans are complex, fission-fusion societies in which individual members travel, rest and forage in subgroups that frequently change composition. We studied two clans in Kenya to provide the first detailed description of fission-fusion dynamics in this species. Because social and ecological circumstances can influence the cohesiveness of animal societies, we evaluated the extent to which specific circumstances promote the formation of subgroups of various sizes. We found that cooperative defence of shared resources during interclan competition and protection from lions were cohesive forces that promoted formation of large subgroups. We also tested hypotheses suggesting factors limiting subgroup size. Mothers with small cubs avoided conspecifics, thereby reducing infanticide risk. Victims of aggression either reconciled fights or separated from former opponents to reduce the immediate costs of escalated aggression in the absence of food. As predicted by the ecological constraints hypothesis, hyaenas adjusted their grouping patterns over both short and long time scales in response to feeding competition. Crocuta were most gregarious during periods of abundant prey, joined clanmates at ephemeral kills in numbers that correlated with the energetic value of the prey and gained the most energy when foraging alone because cooperative hunting attracted numerous competitors. Overall, our findings indicate that resource limitation constrains grouping in this species.
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Smith, J. E., Van Horn, R. C., Powning, K. S., Cole, A. R., Graham, K. E., Memenis, S. K., et al. (2010). Evolutionary forces favoring intragroup coalitions among spotted hyenas and other animals. Behav. Ecol., 21(2), 284–303.
Abstract: Coalitionary support in agonistic interactions represents cooperation because intervening in a fight is potentially costly to the donor of support but benefits the recipient. Here, we first review the characteristics of, and evolutionary forces favoring, intragroup coalitions in 49 species and find that patterns of intragroup coalition formation are remarkably similar between primates and nonprimates. We then test hypotheses suggesting kin selection, reciprocal altruism, and direct benefits as adaptive explanations for coalitionary interventions among adult female spotted hyenas (Crocuta crocuta) belonging to a large social group in Kenya. As predicted by kin selection theory, females supported close kin most often, and the density (connectedness) of cooperation networks increased with genetic relatedness. Nevertheless, kinship failed to protect females from coalitionary attacks. We found no evidence of enduring alliances based on reciprocal support among unrelated adult females. Instead, donors generally minimized costs to themselves, intervening most often during low-intensity fights and when feeding opportunities were unavailable. Females also gained direct benefits from directing coalitionary attacks toward subordinates. Finally, females monitored the number of dominant bystanders in the “audience” at fights and modified their level of cooperation based on this knowledge. Overall, hyenas made flexible decisions regarding whether or not to intervene in fights, modifying their tendency to cooperate based on multiple types of information about their immediate social and ecological environments. Taken together, these findings indicate that the combined evolutionary forces of kin selection and direct benefits derived from reinforcing the status quo drive coalitionary interventions among adult female spotted hyenas.
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