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  1. Abstract

    As fecal steroid methods increasingly are used by researchers to monitor the physiology of captive and wild populations, we need to expand our validation protocols to test the effects of procedural variation and to identify contamination by exogenous sources of steroid hormones. Mammalian carnivore feces often contain large amounts of hair from the prey they consume, which itself may contain high concentrations of hormones. In this study, we report first a validation of two steroid hormone antibodies, corticosterone and progesterone, to determine fecal concentrations of these hormones in wild spotted hyenas (Crocuta crocuta). Next, we expand on these standard validation protocols to test two additional metrics: (i) whether hair from consumed prey or (ii) the specific drying method (oven incubation vs. lyophilization) affect steroid hormone concentrations in feces. In the first biological validation for the progesterone antibody in this species, progesterone concentrations met our expectations: (i) concentrations of plasma and fecal progesterone were lowest in immature females, higher in lactating females, and highest in pregnant females; (ii) across pregnant females, fecal progesterone concentrations were highest during late pregnancy; and (iii) among lactating females, fecal progesterone concentrations were highest after parturition. Our additional validation experiments indicated that contamination with prey hair and drying method are hormone-specific. Although prey hair did not release hormones into samples during storage or extraction for either hormone, its presence appeared to “dilute” progesterone (but not corticosterone) measures indirectly by increasing the dry weight of samples. In addition, fecal progesterone, but not corticosterone, values were lower for lyophilized than for incubated samples. Therefore, in addition to the standard analytical and biological validation steps, additional methodological variables need to be tested whenever we measure fecal hormone concentrations, particularly from predatory mammals.

     
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  2. Abstract

    Individual differences in behavior are the raw material upon which natural selection acts, but despite increasing recognition of the value of considering individual differences in the behavior of wild animals to test evolutionary hypotheses, this approach has only recently become popular for testing cognitive abilities. In order for the intraspecific approach with wild animals to be useful for testing evolutionary hypotheses about cognition, researchers must provide evidence that measures of cognitive ability obtained from wild subjects reflect stable, general traits. Here, we used a multi-access box paradigm to investigate the intra-individual reliability of innovative problem-solving ability across time and contexts in wild spotted hyenas (Crocuta crocuta). We also asked whether estimates of reliability were affected by factors such as age-sex class, the length of the interval between tests, or the number of times subjects were tested. We found significant contextual and temporal reliability for problem-solving. However, problem-solving was not reliable for adult subjects, when trials were separated by more than 17 days, or when fewer than seven trials were conducted per subject. In general, the estimates of reliability for problem-solving were comparable to estimates from the literature for other animal behaviors, which suggests that problem-solving is a stable, general trait in wild spotted hyenas.

     
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  3. 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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  4. 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. 
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  5. 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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  6. 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. 
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  7. 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. 
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