Anthropogenic disturbance can have important influences on the fitness and behaviors of wild animals, including their boldness when exposed to risky conditions. We presented spotted hyenas (
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.
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- NSF-PAR ID:
- 10388676
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 289
- Issue:
- 1979
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Crocuta crocuta ) from two populations, each exposed to a different level of human activity, with a life‐size model hyena representing an intruder from another clan. The high‐disturbance population lived adjacent to human settlements, and the low‐disturbance population inhabited a relatively undisturbed part of the same national park in Kenya. The mock intruder was presented to individual hyenas to assess their reactions to an alien hyena, and to determine whether their reactions varied with their exposure to anthropogenic activity. We found that human disturbance was indeed associated with hyena risk‐taking behavior in response to the model intruder. Hyenas tested in the low‐disturbance area exhibited more risk‐taking behaviors by approaching the mock intruder more closely, and spending more time near it, than did their counterparts living in high‐disturbance areas. Hyenas that spent less time in close proximity to the model had greater survivorship than those that spent more time in close proximity to it, regardless of disturbance level. Furthermore, the individual differences in risk‐taking measured here were consistent with those obtained previously from the same animals using a different set of experimental manipulations. However, the experimentally induced behaviors were not consistent with naturally occurring risk‐taking behaviors in proximity to lions; this suggests that risk‐taking behaviors are consistent within individuals across experimental contexts, but that exposure to lions elicits different responses. Although our results are consistent with those from earlier tests of anthropogenic disturbance and boldness in spotted hyenas and other predators, they differ from results obtained from birds and small mammals, which are generally found to be bolder in areas characterized by human disturbance. -
Hird, Sarah M. (Ed.)The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specific and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas’ guts; 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. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. 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 not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis.more » « less
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Abstract Populations of large carnivores are declining in many parts of the world due to anthropogenic activity. Some species of large carnivores, however, are able to coexist with people by altering their behavior. Altered behaviors may be challenging to identify in large carnivores because these animals are typically cryptic, nocturnal, live at low densities, and because changes in their behavior may be subtle or emerge slowly over many years. We studied the effects of livestock presence on the movements of one large carnivore, the spotted hyena (Crocuta crocuta). We fit 22 adult female spotted hyenas with GPS collars to quantify their movements in areas with and without livestock or herders present, in and around a protected area in southwestern Kenya. We investigated anthropogenic, social, and ecological effects on the speed of movement, distances traveled, long-distance movements, and extraterritorial excursions by spotted hyenas. Hyenas living primarily within the protected area, but in the presence of livestock and herders, moved faster, traveled over longer distances, and were more likely to be within their territories than did conspecifics living in areas without livestock and herders. Hyenas of low social rank were more likely than hyenas of high social rank to engage in long-distance travel events, and these were more likely to occur when prey were scarce. The movement patterns of this large African carnivore indicate a flexibility that may allow them to persist in landscapes that are becoming increasingly defined by people.
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ABSTRACT Host-associated microbial communities, henceforth ‘microbiota’, can affect the physiology and behavior of their hosts. In mammals, host ecological, social and environmental variables are associated with variation in microbial communities. Within individuals in a given mammalian species, the microbiota also partitions by body site. Here, we build on this work and sequence the bacterial 16S rRNA gene to profile the microbiota at six distinct body sites (ear, nasal and oral cavities, prepuce, rectum and anal scent gland) in a population of wild spotted hyenas (Crocuta crocuta), which are highly social, large African carnivores. We inquired whether microbiota at these body sites vary with host sex or social rank among juvenile hyenas, and whether they differ between juvenile females and adult females. We found that the scent gland microbiota differed between juvenile males and juvenile females, whereas the prepuce and rectal microbiota differed between adult females and juvenile females. Social rank, however, was not a significant predictor of microbiota profiles. Additionally, the microbiota varied considerably among the six sampled body sites and exhibited strong specificity among individual hyenas. Thus, our findings suggest that site-specific niche selection is a primary driver of microbiota structure in mammals, but endogenous host factors may also be influential.more » « less
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Introduction Dominance relationships in which females dominate males are rare among mammals. Mechanistic hypotheses explaining the occurrence of female dominance suggest that females dominate males because (1) they are intrinsically more aggressive or less submissive than males, and/or (2) they have access to more social support than males. Methods Here, we examine the determinants of female dominance across ontogenetic development in spotted hyenas ( Crocuta crocuta ) using 30 years of detailed behavioral observations from the Mara Hyena Project to evaluate these two hypotheses. Results Among adult hyenas, we find that females spontaneously aggress at higher rates than males, whereas males spontaneously submit at higher rates than females. Once an aggressive interaction has been initiated, adult females are more likely than immigrant males to elicit submission from members of the opposite sex, and both adult natal and immigrant males are more likely than adult females to offer submission in response to an aggressive act. We also find that adult male aggressors are more likely to receive social support than are adult female aggressors, and that both adult natal and immigrant males are 2–3 times more likely to receive support when attacking a female than when attacking another male. Across all age classes, females are more likely than males to be targets of aggressive acts that occur with support. Further, receiving social support does slightly help immigrant males elicit submission from adult females compared to immigrant males acting alone, and it also helps females elicit submission from other females. However, adult females can dominate immigrant males with or without support far more often than immigrant males can dominate females, even when the immigrants are supported against females. Discussion Overall, we find evidence for both mechanisms hypothesized to mediate female dominance in this species: (1) male and female hyenas clearly differ in their aggressive and submissive tendencies, and (2) realized social support plays an important role in shaping dominance relationships within a clan. Nevertheless, our results suggest that social support alone cannot explain sex-biased dominance in spotted hyenas. Although realized social support can certainly influence fight outcomes among females, adult females can easily dominate immigrant males without any support at all.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2022.0548
