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.
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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.
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- NSF-PAR ID:
- 10388664
- Date Published:
- Journal Name:
- Mammalian Biology
- ISSN:
- 1616-5047
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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 (
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. -
How social development in early-life affects fitness remains poorly understood. 2. 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. 3. 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. 4. 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. 5. 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.more » « less
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Abstract 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.
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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
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1007/s42991-022-00309-4
