Determinants of hyena participation in risky collective action.

Collective action problems arise when cooperating individuals suffer costs of cooperation, while the benefits of cooperation are received by both cooperators and defectors. We address this problem using data from spotted hyenas fighting with lions. Lions are much larger and kill many hyenas, so these fights require cooperative mobbing by hyenas for them to succeed. We identify factors that predict when hyena groups engage in cooperative fights with lions, which individuals choose to participate and how the benefits of victory are distributed among cooperators and non-cooperators. We find that cooperative mobbing is better predicted by lower costs (no male lions, more hyenas) than higher benefits (need for food). Individual participation is facilitated by social factors, both over the long term (close kin, social bond strength) and the short term (greeting interactions prior to cooperation). Finally, we find some direct benefits of participation: after cooperation, participants were more likely to feed at contested carcasses than non-participants. Overall, these results are consistent with the hypothesis that, when animals face dangerous cooperative dilemmas, selection favours flexible strategies that are sensitive to dynamic factors emerging over multiple time scales.

Long-distance vocalizations of spotted hyenas contain individual, but not group, signatures.

In animal societies, identity signals are common, mediate interactions within groups, and allow individuals to discriminate group-mates from out-group competitors. However, individual recognition becomes increasingly challenging as group size increases and as signals must be transmitted over greater distances. Group vocal signatures may evolve when successful in-group/out-group distinctions are at the crux of fitness-relevant decisions, but group signatures alone are insufficient when differentiated within-group relationships are important for decision-making. Spotted hyenas are social carnivores that live in stable clans of less than 125 individuals composed of multiple unrelated matrilines. Clan members cooperate to defend resources and communal territories from neighbouring clans and other mega carnivores; this collective defence is mediated by long-range (up to 5 km range) recruitment vocalizations, called whoops. Here, we use machine learning to determine that spotted hyena whoops contain individual but not group signatures, and that fundamental frequency features which propagate well are critical for individual discrimination. For effective clan-level cooperation, hyenas face the cognitive challenge of remembering and recognizing individual voices at long range. We show that serial redundancy in whoop bouts increases individual classification accuracy and thus extended call bouts used by hyenas probably evolved to overcome the challenges of communicating individual identity at long distance.

Measuring salivary cortisol in wild carnivores.

Salivary hormone analyses provide a useful alternative to fecal and urinary hormone analyses in non-invasive studies of behavioral endocrinology. Here, we use saliva to assess cortisol levels in a wild population of spotted hyenas (Crocuta crocuta), a gregarious carnivore living in complex social groups. We first describe a novel, non-invasive method of collecting saliva from juvenile hyenas and validate a salivary cortisol assay for use in this species. We then analyze over 260 saliva samples collected from nearly 70 juveniles to investigate the relationships between cortisol and temporal and social variables in these animals. We obtain some evidence of a bimodal daily rhythm with salivary cortisol concentrations dropping around dawn and dusk, times at which cub activity levels are changing substantially. We also find that dominant littermates have lower cortisol than singleton juveniles, but that cortisol does not vary with age, sex, or maternal social rank. Finally, we examine how social behaviors such as aggression or play affect salivary cortisol concentrations. We find that inflicting aggression on others was associated with lower cortisol concentrations. We hope that the detailed description of our methods provides wildlife researchers with the tools to measure salivary cortisol in other wild carnivores.

Applications of conceptual models from lifecourse epidemiology in ecology and evolutionary biology.

In ecology and evolutionary biology (EEB), the study of developmental plasticity seeks to understand ontogenetic processes underlying the phenotypes upon which natural selection acts. A central challenge to this inquiry is ascertaining a causal effect of the exposure on the manifestation of later-life phenotype due to the time elapsed between the two events. The exposure is a potential cause of the outcome-i.e. an environmental stimulus or experience. The later phenotype might be a behaviour, physiological condition, morphology or life-history trait. The latency period between the exposure and outcome complicates causal inference due to the inevitable occurrence of additional events that may affect the relationship of interest. Here, we describe six distinct but non-mutually exclusive conceptual models from the field of lifecourse epidemiology and discuss their applications to EEB research. The models include Critical Period with No Later Modifiers, Critical Period with Later Modifiers, Accumulation of Risk with Independent Risk Exposures, Accumulation of Risk with Risk Clustering, Accumulation of Risk with Chains of Risk and Accumulation of Risk with Trigger Effect. These models, which have been widely used to test causal hypotheses regarding the early origins of adult-onset disease in humans, are directly relevant to research on developmental plasticity in EEB.

Social alliances improve rank and fitness in convention-based societies.

Social hierarchies are widespread in human and animal societies, and an individual's position in its hierarchy affects both its access to resources and its fitness. Hierarchies are traditionally thought of in terms of variation in individual ability to win fights, but many are structured around arbitrary conventions like nepotistic inheritance rather than such traits as physical strength or weapon size. These convention-based societies are perplexing because position in the hierarchy appears to be gained irrespective of individual physical ability, yet social status strongly affects access to resources and fitness. It remains unclear why individuals abide by seemingly arbitrary conventions regarding social status when they stand to benefit by ignoring these conventions and competing for top positions or access to resources. Using data from wild spotted hyenas collected over 27 y and five generations, we show that individuals who repeatedly form coalitions with their top allies are likely to improve their position in the hierarchy, suggesting that social alliances facilitate revolutionary social change. Using lifetime reproductive success as a fitness measure, we go on to demonstrate that these status changes can have major fitness consequences. Finally, we show that the consequences of these changes may become even more dramatic over multiple generations, as small differences in social rank become amplified over time. This work represents a first step in reconciling the advantages of high status with the appearance of "arbitrary" conventions that structure inequality in animal and human societies.

The value of individual identification in studies of free-living hyenas and aardwolves.

From population estimates to social evolution, much of our understanding of the family Hyaenidae is drawn from studies of known individuals. The extant species in this family (spotted hyenas, Crocuta crocuta, brown hyenas, Parahyaena brunnea, striped hyenas, Hyaena hyaena, and aardwolves, Proteles cristata) are behaviorally diverse, presenting an equally diverse set of logistical constraints on capturing and marking individuals. All these species are individually identifiable by their coat patterns, providing a useful alternative to man-made markings. Many studies have demonstrated the utility of this method in answering a wide range of research questions across all four species, with some employing a creative fusion of techniques. Despite its pervasiveness in basic research on hyenas and aardwolves, individual identification has rarely been applied to the conservation and management of these species. We argue that individual identification using naturally occurring markings in applied research could prove immensely helpful, as this could further improve accuracy of density estimates, reveal characteristics of suitable habitat, identify threats to population persistence, and help to identify individual problem animals. Supplementary Information: The online version contains supplementary material available at 10.1007/s42991-022-00309-4.

Infanticide by Females Is a Leading Source of Juvenile Mortality in a Large Social Carnivore.

AbstractSocial animals benefit from their groupmates, so why do they sometimes kill each other's offspring? Using 30 years of data from multiple groups of wild spotted hyenas, we address three critical aims for understanding infanticide in any species: (1) quantify the contribution of infanticide to overall mortality, (2) describe the circumstances under which infanticide occurs, and (3) evaluate hypotheses about the evolution of infanticide. We find that infanticide, although observed only rarely, is in fact a leading source of juvenile mortality. Infanticide accounted for 24% of juvenile mortality, and one in 10 hyenas born in our population perished as a result of infanticide. In all observed cases of infanticide, killers were adult females, but victims could be of both sexes. Of four hypotheses regarding the evolution of infanticide, we found the most support for the hypothesis that infanticide in spotted hyenas reflects competition over social status among matrilines.

The effect of urbanization on innovation in spotted hyenas.

Urbanization represents a dramatic form of evolutionary novelty in the landscapes inhabited by many extant animals. The Cognitive Buffer Hypothesis suggests that innovation, the process by which animals solve novel problems or use novel behaviors, may be key for many animals when adapting to novel environments. If innovation is especially beneficial in urban environments, then we would expect urban animals to be more innovative than their non-urban counterparts. However, studies comparing innovative problem-solving between urban and rural habitats have produced mixed results. Here, we hypothesized that these findings result from comparing only two levels of urbanization when related research suggests that the stage of invasion of urban habitats likely has a strong effect on demand for innovation, with demand being highest during early establishment in a novel environment. To test this hypothesis, we assessed innovation in three locations where spotted hyenas experienced varying degrees of urbanization. Spotted hyenas are relatively innovative compared to other carnivores and, although many large carnivores in Africa are endangered, spotted hyenas remain abundant both inside and outside protected areas. We measured innovation with a multi-access puzzle box with four different doors through which hyenas could obtain a food reward. We predicted that hyenas in a transitional, rapidly urbanizing habitat would be more innovative, measured by the number of unique doors opened, than those in rural or fully urban habitats. Contrary to our predictions, hyenas in the rural habitat were the most innovative. These results challenge the idea that the evolutionary novelty associated with urbanization favors greater innovativeness.

Early-life relationships matter: Social position during early life predicts fitness among female spotted hyenas.

How social development in early-life affects fitness remains poorly understood. Though there is growing evidence that early-life relationships can affect fitness, little research has investigated how social positions develop or whether there are particularly important periods for social position development in an animal's life history. In long-lived species in particular, understanding the lasting consequences of early-life social environments requires detailed, long-term datasets. Here we used a 25-year dataset to test whether social positions held during early development predicted adult fitness. Specifically, we quantified social position using three social network metrics: degree, strength and betweenness. We determined the social position of each individual in three types of networks during each of three stages of ontogeny to test whether they predict annual reproductive success (ARS) or longevity among adult female spotted hyenas Crocuta crocuta. The social positions occupied by juvenile hyenas did predict their fitness, but the effects of social position on fitness measures differed between stages of early development. Network metrics when individuals were young adults better predicted ARS, but network metrics for younger animals, particularly when youngsters were confined to the communal den, better predicted longevity than did metrics assessed during other stages of development. Our study shows how multiple types of social bonds formed during multiple stages of social development predict lifetime fitness outcomes. We suggest that social bonds formed during specific phases of development may be more important than others when considering fitness outcomes.

Juvenile rank acquisition is associated with fitness independent of adult rank.

Social rank is a significant determinant of fitness in a variety of species. The importance of social rank suggests that the process by which juveniles come to establish their position in the social hierarchy is a critical component of development. Here, we use the highly predictable process of rank acquisition in spotted hyenas to study the consequences of variation in rank acquisition in early life. In spotted hyenas, rank is 'inherited' through a learning process called 'maternal rank inheritance.' This pattern is very consistent: approximately 80% of juveniles acquire the exact rank expected under the rules of maternal rank inheritance. The predictable nature of rank acquisition in these societies allows the process of rank acquisition to be studied independently from the ultimate rank that each juvenile attains. In this study, we use Elo-deviance scores, a novel application of the Elo-rating method, to calculate each juvenile's deviation from the expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition among juveniles, most of these juveniles come to attain the exact rank expected of them according to the rules of maternal rank inheritance. Nevertheless, we find that transient variation in rank acquisition in early life is associated with long-term fitness consequences for these individuals: juveniles 'underperforming' their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers, and this relationship is independent of both maternal rank and rank achieved in adulthood. We also find that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness. Future work is needed to determine if variation in rank acquisition directly affects fitness, or if some other variable, such as maternal investment or juvenile condition, causes variation in both of these outcomes.

Early life social and ecological determinants of global DNA methylation in wild spotted hyenas.

Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross-sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high- than low-ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.

Multispecies hierarchical modeling reveals variable responses of African carnivores to management alternatives.

Carnivore communities face unprecedented threats from humans. Yet, management regimes have variable effects on carnivores, where species may persist or decline in response to direct or indirect changes to the ecosystem. Using a hierarchical multispecies modeling approach, we examined the effects of alternative management regimes (i.e., active vs. passive enforcement of regulations) on carnivore abundances and group sizes at both species and community levels in the Masai Mara National Reserve, Kenya. Alternative management regimes have created a dichotomy in ecosystem conditions within the Reserve, where active enforcement of regulations maintains low levels of human disturbance in the Mara Triangle and passive enforcement of regulations in the Talek region permits multiple forms of human disturbance. Our results demonstrate that these alternative management regimes have variable effects on 11 observed carnivore species. As predicted, some species, such as African lions and bat-eared foxes, have higher population densities in the Mara Triangle, where regulations are actively enforced. Yet, other species, including black-backed jackals and spotted hyenas, have higher population densities in the Talek region where enforcement is passive. Multiple underlying mechanisms, including behavioral plasticity and competitive release, are likely causing higher black-backed jackals and spotted hyena densities in the disturbed Talek region. Our multispecies modeling framework reveals that carnivores do not react to management regimes uniformly, shaping carnivore communities by differentially producing winning and losing species. Some carnivore species require active enforcement of regulations for effective conservation, while others more readily adapt (and in some instances thrive in response) to lax management enforcement and resulting anthropogenic disturbance. Yet, high levels of human disturbance appear to be negatively affecting the majority of carnivores, with potential consequences that may permeate throughout the rest of the ecosystem. Community approaches to monitoring carnivores should be adopted as single species monitoring may overlook important intra-community variability.

Inferring longitudinal hierarchies: Framework and methods for studying the dynamics of dominance.

Social inequality is a consistent feature of animal societies, often manifesting as dominance hierarchies, in which each individual is characterized by a dominance rank denoting its place in the network of competitive relationships among group members. Most studies treat dominance hierarchies as static entities despite their true longitudinal, and sometimes highly dynamic, nature. To guide study of the dynamics of dominance, we propose the concept of a longitudinal hierarchy: the characterization of a single, latent hierarchy and its dynamics over time. Longitudinal hierarchies describe the hierarchy position (r) and dynamics (∆) associated with each individual as a property of its interaction data, the periods into which these data are divided based on a period delineation rule (p) and the method chosen to infer the hierarchy. Hierarchy dynamics result from both active (∆a) and passive (∆p) processes. Methods that infer longitudinal hierarchies should optimize accuracy of rank dynamics as well as of the rank orders themselves, but no studies have yet evaluated the accuracy with which different methods infer hierarchy dynamics. We modify three popular ranking approaches to make them better suited for inferring longitudinal hierarchies. Our three "informed" methods assign ranks that are informed by data from the prior period rather than calculating ranks de novo in each observation period and use prior knowledge of dominance correlates to inform placement of new individuals in the hierarchy. These methods are provided in an R package. Using both a simulated dataset and a long-term empirical dataset from a species with two distinct sex-based dominance structures, we compare the performance of these methods and their unmodified counterparts. We show that choice of method has dramatic impacts on inference of hierarchy dynamics via differences in estimates of ∆a. Methods that calculate ranks de novo in each period overestimate hierarchy dynamics, but incorporation of prior information leads to more accurately inferred ∆a. Of the modified methods, Informed MatReorder infers the most conservative estimates of hierarchy dynamics and Informed Elo infers the most dynamic hierarchies. This work provides crucially needed conceptual framing and methodological validation for studying social dominance and its dynamics.

Brain size predicts problem-solving ability in mammalian carnivores.

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.

The evolution of general intelligence in all animals and machines.

We strongly agree that general intelligence occurs in many animals but find the cultural intelligence hypothesis of limited usefulness. Any viable hypothesis explaining the evolution of general intelligence should be able to account for it in all species where it is known to occur, and should also predict the conditions under which we can develop machines with general intelligence as well.

Symbiotic bacteria appear to mediate hyena social odors.

All animals harbor beneficial microbes. One way these microbes can benefit their animal hosts is by increasing the diversity and efficacy of communication signals available to the hosts. The fermentation hypothesis for mammalian chemical communication posits that bacteria in the scent glands of mammals generate odorous metabolites used by their hosts for communication and that variation in host chemical signals is a product of underlying variation in the bacterial communities inhabiting the scent glands. An effective test of this hypothesis would require accurate surveys of the bacterial communities in mammals' scent glands and complementary data on the odorant profiles of scent secretions--both of which have been historically lacking. Here we use next-generation sequencing to survey deeply the bacterial communities in the scent glands of wild spotted and striped hyenas. We show that these communities are dominated by fermentative bacteria and that the structures of these communities covary with the volatile fatty acid profiles of scent secretions in both hyena species. The bacterial and volatile fatty acid profiles of secretions differ between spotted and striped hyenas, and both profiles vary with sex and reproductive state among spotted hyenas within a single social group. Our results strongly support the fermentation hypothesis for chemical communication, suggesting that symbiotic bacteria underlie species-specific odors in both spotted and striped hyenas and further underlie sex and reproductive state-specific odors among spotted hyenas. We anticipate that the fermentation hypothesis for chemical communication will prove broadly applicable among scent-marking mammals as others use the technical and analytical approaches used here.

Topological effects of network structure on long-term social network dynamics in a wild mammal.

Social structure influences ecological processes such as dispersal and invasion, and affects survival and reproductive success. Recent studies have used static snapshots of social networks, thus neglecting their temporal dynamics, and focused primarily on a limited number of variables that might be affecting social structure. Here, instead we modelled effects of multiple predictors of social network dynamics in the spotted hyena, using observational data collected during 20 years of continuous field research in Kenya. We tested the hypothesis that the current state of the social network affects its long-term dynamics. We employed stochastic agent-based models that allowed us to estimate the contribution of multiple factors to network changes. After controlling for environmental and individual effects, we found that network density and individual centrality affected network dynamics, but that social bond transitivity consistently had the strongest effects. Our results emphasise the significance of structural properties of networks in shaping social dynamics.

Socioecological variables predict telomere length in wild spotted hyenas.

Telomeres are regarded as important biomarkers of ageing and serve as useful tools in revealing how stress acts at the cellular level. However, the effects of social and ecological factors on telomere length remain poorly understood, particularly in free-ranging mammals. Here, we investigated the influences of within-group dominance rank and group membership on telomere length in wild adult spotted hyenas (Crocuta crocuta). We found large effects of both factors; high-ranking hyenas exhibited significantly greater mean telomere length than did subordinate animals, and group membership significantly predicted mean telomere length within high-ranking females. We further inquired whether prey availability mediates the observed effect of group membership on telomere length, but this hypothesis was not supported. Interestingly, adult telomere length was not predicted by age. Our work shows for the first time, to the best of our knowledge, the effects of social rank on telomere length in a wild mammal and enhances our understanding of how social and ecological variables may contribute to organismal senescence.

Do female hyaenas choose mates based on tenure?

In their investigation into whether female mate-choice drives male dispersal, Höner et al. argue that female spotted hyaenas (Crocuta crocuta) prefer mates whose tenure in the social group is less than the females' age, to avoid paternal incest, and suggest that male dispersal reflects this preference. However, we are not persuaded that females choose mates on the basis of tenure because Höner et al. overlook the alternative hypothesis that dispersal status itself is important in female mate-choice, such that females prefer immigrants over natal males. Like mate-choice based on tenure, choice based on dispersal status reduces the risk of incest.

Spotted Hyena skull size variation across geography favors the energetic equivalence rule over Bergmann's Rule.

Much historic work has focused on establishing geographical and ecological rules that broadly explain patterns in size variation. We examined geographic variation in Spotted Hyena skull size using geometric morphometrics and spatial statistics. We quantified size variation and sexual size dimorphism of the skull, and evaluated the influence of temperature, precipitation, land cover type, and population density on skull size. We found that female spotted hyenas are slightly larger on average than males. Our analysis of regional differences did not indicate geographic variation in sexual size dimorphism. Skull size of Spotted Hyenas varies with geography but does not adhere to Bergmann's Rule. The smallest individuals of both sexes occur between -5.00° and 10.00° latitude and east of 28.50° longitude, with larger individuals being found elsewhere. Although Spotted Hyena skull size co-varies in some views with such variables as habitat type and climate indicators, skull size in this species most strongly co-varies with population density. The highest population densities are associated with the smallest skull size, possibly reflecting a relationship between high population density and access to resources. These results suggest that geographic variation in Spotted Hyena skull size is better explained by the energetic equivalence rule than Bergmann's Rule.