Biology subjects

Holekamp, K. E.

Publications and source records attributed to Holekamp, K. E..

12 recordsLinked to original sources

bioRxiv2026

HyenaSET: Hyena Sound Event Transcripts and benchmark animal2vec performance for parsing animal communication

Here, we present HyenaSET, a large (~1640 hours) bioacoustic dataset derived from collar-mounted audio recorders deployed on 19 spotted hyenas in the Maasai Mara National Reserve, Kenya. Within this dataset, 243 hours have been strongly labeled by identifying the onset and offset of all vocalizations as well as their types, and the labels have been validated by experts on hyena vocalizations and behavior. Within the strongly labeled data, the total amount of time hyenas were vocalizing was 9.5 hours (3.9%). Furthermore, each vocalization has been manually identified as "focal" (emitted by the hyena wearing the collar) or "non-focal" (emitted by a nearby conspecific), making use of information from collar-mounted accelerometers that picked up vibrations of the animals throat when it produced vocalizations. In addition to the labeled data, we also provide a large corpus of unlabeled data from the same recordings, which can be used for un- or self-supervised machine learning tasks. To ensure reproducibility of this dataset as a benchmark in machine learning studies, we present it alongside five stratified cross-validation train/test splits to enable accurate comparisons, and we also provide a train/test split in which specific individuals are left out of the training set to assess generalizability across individuals. Finally, as a performance benchmark, we present baseline results for this dataset using animal2vec, a recently developed transformer-based model optimized for bioacoustic data.

animal behavior and cognition↗

bioRxiv2024

Behavioral sequences across multiple animal species in the wild share common structural features

Animal behavior can be decomposed into a sequence of discrete activity bouts over time. Analyzing the statistical structure of such behavioral sequences can provide insights into the drivers of behavioral decisions. Laboratory studies, predominantly in invertebrates, have suggested that behavioral sequences exhibit multiple timescales and long-range memory, but whether these results can be generalized to other taxa and to animals in natural settings remains unclear. By analyzing accelerometer-inferred predictions of behavioral states in three species of social mammals (meerkats, white-nosed coatis, and spotted hyenas) in the wild, we discovered surprisingly consistent structuring of behavioral sequences across all behavioral states, all individuals, and all study species. Behavioral bouts were characterized by decreasing hazard functions, wherein the longer a behavioral bout had progressed, the less likely it was to end within the next instant. The predictability of an animals future behavioral state as a function of its present state always decreased as a truncated power-law for predictions made farther into the future, with very similar estimates for the power law exponent across all species. Finally, the distributions of bout durations were also heavy-tailed. Why such shared structural principles emerge remains unknown, and we explore multiple plausible explanations, including environmental non-stationarity, behavioral self-reinforcement, and the hierarchical nature of behavior. The existence of highly consistent patterns in behavioral sequences across our study species suggests that these phenomena could be widespread in nature, and points to the existence of fundamental properties of behavioral dynamics that could drive such convergent patterns. Significance statementThe study of animal behavior seeks to understand how and why animals do what they do. This pursuit of general principles governing behavior across species can be approached by first understanding when animals choose to change their behavioral states (e.g., switching from walking to standing, or to running). Using accelerometer-inferred behaviors of three social mammals, we uncover common structural long timescale patterns in their sequences of behavior. We explore two explanations, involving either positive feedbacks or the interaction of several independent time-scales, about how such common patterns arise.

animal behavior and cognition↗

bioRxiv2023

Accelerometer-based predictions of behaviour elucidate factors affecting the daily activity patterns of spotted hyenas

Animal activity patterns are highly variable and influenced by internal and external factors, including social processes. Quantifying activity patterns in natural settings can be challenging, as it is difficult to monitor animals over long time periods. Here, we developed and validated a machine-learning based classifier to identify behavioural states from accelerometer data of wild spotted hyenas (Crocuta crocuta), social carnivores that live in large fission-fusion societies. By combining this classifier with continuous collar-based accelerometer data from five hyenas, we generated a complete record of activity patterns over more than one month. We used these continuous behavioural sequences to investigate how past activity, individual idiosyncrasies, and social synchronisation influence hyena activity patterns. We found that hyenas exhibit characteristic crepuscular-nocturnal daily activity patterns. Time spent active was independent of activity level on previous days, suggesting that hyenas do not show activity compensation. We also found limited evidence for an effect of individual identity on activity, and showed that pairs of hyenas who spent more time together synchronised their activity patterns. This study sheds light on the patterns and drivers of activity in spotted hyena societies, and also provides a useful tool for quantifying behavioural sequences from accelerometer data.

animal behavior and cognition↗

bioRxiv2022

Taxonomic, genomic, and functional variation in the gut microbiomes of wild spotted hyenas across two decades of study

The gut microbiome provides vital functions for mammalian hosts, yet research on the variability and function of the microbiome across adult lifespans and multiple generations is limited in large mammalian carnivores. Here we use 16S rRNA gene and metagenomic sequencing to profile the taxonomic composition, genomic diversity, and metabolic function of the gut microbiome of 12 wild spotted hyenas (Crocuta crocuta) residing in the Masai Mara National Reserve, Kenya over a 23-year period spanning three generations. We determined the extent to which host factors predict variation in the gut microbiome and identify the core microbes present in the guts of hyenas. We also investigate novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition was highly variable across the two decades of sampling, but despite this, a core set of 14 bacterial genera and 19 amplicon sequence variants were identified. The strongest predictors of microbiome alpha and beta-diversity were host identity and age, suggesting that hyenas possess individualized microbiomes, and that these may change with age during adulthood. Gut microbiome functional profiles were also individual-specific, and were moderately correlated with antelope prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyena gut, spanning 25 bacterial orders and 51 genera. Some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species level matches to genomes in existing reference databases. ImportanceThere is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a hosts lifespan and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we demonstrate that although gut microbiomes are individualized and temporally variable among hyenas, they correlate similarly to large-scale changes in their hosts ecological environment. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores but over 80% of MAGs were novel and from species previously not represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of non-model wild hosts, using multiple sequencing methods and computational approaches, and at distinct scales of analysis.

microbiology↗

bioRxiv2022

Determinants of hyena participation in risky collective action

Many species engage in risky cooperative behaviors, which pose a challenge to evolutionary theory: participants take on all the costs of cooperation, yet even non-participants benefit from success in these encounters. So, why participate in these risky behaviors? We address this question 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: (1) when hyena groups engage in cooperative fights with lions, (2) which individuals choose to participate, and (3) how the benefits of victory are distributed among cooperators and non-cooperators. We find that cooperative mobbing is more strongly influenced 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 suggest that, when animals play dangerous cooperative games, selection favors flexible strategies that are sensitive to dynamic factors emerging over multiple time-scales.

animal behavior and cognition↗

bioRxiv2021

Daily ranging and den usage patterns structure fission-fusion dynamics and social associations in spotted hyenas

Environment structure often shapes social interactions. Spatial attractors that draw multiple individuals may play a particularly important role in dispersed groups, where individuals must first encounter one another to interact. We use GPS data recorded simultaneously from five spotted hyenas (Crocuta crocuta) within a single clan to investigate how communal dens and daily ranging patterns shape fission-fusion dynamics (subgroup splits and merges). We introduce a species-general framework for identifying and characterizing dyadic fission-fusion events and describe a taxonomy of ten possible configurations of these events. Applying this framework to the hyena data illuminates the spatiotemporal structure of social interactions within hyenas daily routines. The most common types of fission-fusion events involve close approaches between individuals, do not involve co-travel together, and occur at the communal den. Comparison to permutation-based reference models suggests that den usage structures broad-scale patterns of social encounters, but that other factors influence how those encounters unfold. We discuss the dual role of communal dens in hyenas as physical and social resources, and suggest that dens are an example of a general "social piggybacking" process whereby environmental attractors take on social importance as reliable places to encounter conspecifics, causing social and spatial processes to become fundamentally intertwined.

animal behavior and cognition↗

bioRxiv2021

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 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 either subordinate littermates or singletons, 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. HIGHLIGHTSO_LIWe validated methods for collecting and analyzing saliva from wild carnivores. C_LIO_LIWe documented a bimodal daily rhythm in juvenile spotted hyena salivary cortisol. C_LIO_LICortisol varied among juvenile hyenas based on litter size and intra-litter rank. C_LIO_LIInflicting aggression on others was associated with lower cortisol concentrations. C_LI

zoology↗

bioRxiv2020

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

The gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host dietary guild in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders. We found that gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity among gut microbiotas increased with host phylogenetic relatedness (r=0.73), yet this relationship was not consistent among seven closely related Bovid host species (r=0.21 NS). Within bovids, host dietary guild explained more of the variation in the gut microbiota than did host species. Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota, but these gut microbial communities could be furthered modified by host ecology, especially among closely related host species.

ecology↗

bioRxiv2020

Toxoplasma gondii infections are associated with boldness towards lions in wild hyena hosts

Toxoplasma gondii is widely reported to manipulate the behavior of its non-definitive hosts in ways that promote lethal interactions with the parasites definitive feline hosts. Nonetheless, there is a lack of data on the association between T. gondii infection and costly behavioral interactions with felids in nature. Here, we report that three decades of field observations reveal T. gondii infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality. Our findings support the hypothesis that T. gondiis manipulation of host boldness is an extended phenotype that promotes parasite transmission from intermediate hosts to feline predators. While upregulating hyena boldness toward lions might achieve this, it may also reflect a collateral influence of manipulative traits that evolved in other hosts (e.g., rodents). In either case, our findings corroborate the potential impacts of a globally distributed and generalist parasite (T. gondii) on fitness-related interaction with felids in a wild host. One Sentence SummaryWild hyenas infected with the parasite T. gondii show evidence of costly behavioral manipulation when interacting with lions.

animal behavior and cognition↗

bioRxiv2020

Associations of early social experience with offspring DNA methylation and later life stress phenotype

In a wild population of spotted hyenas, we tested the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development lead to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. We found that although maternal care and social connectedness during the communal den dependent period were not associated with fGCMs, greater social connectedness after hyenas leave their communal den is associated with lower adult fGCMs. Additionally, more maternal care and social connectedness after leaving the communal den corresponded with higher global (%CCGG) DNA methylation. Finally, we identified multiple DNA methylation biomarkers near genes involved in inflammation that may link maternal care and stress phenotype. Our findings suggest that both maternal care during the first year of life and social connections after leaving the den influence DNA methylation and contribute to a developmentally plastic stress response.

animal behavior and cognition↗

bioRxiv2020

Rank-dependent social inheritance determines social network structure in a wild mammal population

The structure of animal social networks influences survival and reproductive success, as well as pathogen and information transmission. However, the general mechanisms determining social structure remain unclear. Using data on 73,767 social interactions among wild spotted hyenas over 27 years, we show that a process of social inheritance determines how offspring relationships are formed and maintained. The relationships of offspring with other hyenas are similar to those of their mothers over up to six years, and the degree of similarity increases with maternal social rank. The strength of mother-offspring relationship affects social inheritance and is positively correlated with offspring longevity. These results confirm the hypothesis that social inheritance of relationships can structure animal social networks and be subject to adaptive tradeoffs.

animal behavior and cognition↗

bioRxiv2019

Juvenile rank acquisition influences fitness independent of adult rank

Social rank has been identified as 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 social 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 highly predictable: ~80% of juveniles acquire the exact rank predicted by the rules of maternal rank inheritance. This 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 a novel application of the Elo-rating method to calculate each juveniles deviation from expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition in 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 predicts long term fitness consequences for these individuals: juveniles underperforming their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers. Finally, we present evidence that this variability in rank acquisition in early life represents a source of early life adversity, and that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness.

animal behavior and cognition↗