Endocrine Correlates of Musth in Free-Ranging Asian Elephants (Elephas maximus) Determined by Non-Invasive Faecal Steroid Hormone Metabolite Measurements

Ghosal, Ratna; Ganswindt, André; Seshagiri, Polani B.

doi:10.1371/journal.pone.0084787

Cited by 26 publications

(20 citation statements)

References 32 publications

(77 reference statements)

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“…A similar finding was presented in a recent study on giraffes, where the oldest bulls also showed significantly higher fAM levels, when sexually active (Seeber et al, 2013). For a number of species, times of sexual activity are often correlated with elevated androgen levels, as for example shown in bison (Mooring et al, 2004) or African and Asian elephant (Ganswindt et al, 2005;Ghosal et al, 2013), with already minor changes in fAM levels being related to male sexual activity in elephants (Rasmussen et al, 2008). In contrast, elephant bulls in musth show much higher androgen levels than necessary to stimulate sexual behavior and therefore appear more likely to be linked to intra-sexual competition and mate guarding (Rasmussen et al, 2008).…”

Section: Discussionsupporting

confidence: 85%

“…Such alterations in androgen levels have even been described in non-seasonally breeding species such as chimpanzee (Pan troglodytes schweinfurthii), with males showing elevated androgen levels when parous females are present and therefore male-male aggression increases (Muehlenbein et al, 2004;Muller and Wrangham, 2004). Furthermore, a temporal increase in aggression related to male 4 reproductive activity appears to be androgen mediated in African (Loxodonta africana) and Asian elephants (Elephas maximus) (Ganswindt et al, 2005;Ghosal et al, 2013;Rasmussen et al, 2008).…”

Section: Introductionmentioning

confidence: 90%

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Age and socially related changes in fecal androgen metabolite concentrations in free-ranging male giraffes

Wolf

Schaebs

Bennett

et al. 2018

General and Comparative Endocrinology

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In many mammal species, androgen levels in males are elevated during periods of mating activity, often to facilitate aggressive behavior between males over access to fertile females. However, this pattern might be less obvious in species with a rather low male-male aggression rate, or in those that are not strictly seasonal breeders. A complex social structure, as well as additional social and environmental factors, might add more to the complexity. Here, we applied a non-invasive method to monitor fecal androgen metabolite (fAM) levels in free-ranging giraffe bulls over a period of months to examine longitudinal patterns of androgen metabolite concentrations in relation to observed male sexual behavior in different age classes. Giraffes are non-seasonal breeders, living in a fission-fusion social system and males show a roaming strategy to search for fertile females. Our results show that season has an impact on fAM levels in free-ranging giraffes, with respective steroid concentrations being higher in summer. In the presence of females, fAM levels of bulls are significantly higher compared to when found in all-male groups, with old adult bulls showing the highest fAM levels. In contrast, young adult bulls have overall slightly higher fAM levels compared to old adult bulls when residing in all male groups. Sexual behavior increases fAM levels only in old adult bulls.

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Section: Discussionsupporting

confidence: 85%

Section: Introductionmentioning

confidence: 90%

Age and socially related changes in fecal androgen metabolite concentrations in free-ranging male giraffes

Wolf

Schaebs

Bennett

et al. 2018

General and Comparative Endocrinology

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“…We used the protocol described in Ganswindt et al (2003) for African elephants, which has been successfully validated for Asian elephants (Ghosal et al, 2013;Pokharel et al, 2017), to extract steroid and analyse the fGCM levels. The faecal extraction and analysis for measuring immunoreactive fGCM (lg g À1 ) have been explained in detail in Pokharel et al (2017).…”

Section: Steroid Analysesmentioning

confidence: 99%

Lower levels of glucocorticoids in crop‐raiders: diet quality as a potential ‘pacifier’ against stress in free‐ranging Asian elephants in a human‐production habitat

Pokharel

Singh

Seshagiri

2018

Animal Conservation

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Overlapping habitats and sharing of resources between elephants and people has led to intense elephant-human conflicts, especially crop depredation by elephants, across elephant-range countries. While raiding agricultural crops, elephants face numerous threats from people through chase, injury and the risk of death which could enhance the associated energetic costs, ultimately elevating their stress levels. We hypothesized that crop-raiders (in the human-production habitat) would show higher faecal glucocorticoid metabolite (fGCM) levels, a proxy of stress-response, as compared to nonraiders (in protected forests). To study this, 208 faecal samples were collected from crop-raiding elephants in a human-production habitat and 394 samples from nonraiding elephants in protected forests during 2013 and 2015. Contrary to our expectation, fGCM levels were significantly higher in nonraiding than in crop-raiding elephants of both sexes. As one of the possible factors for lower fGCM in elephants inhabiting the human-production habitat, the influence of benefits obtained from foraging here was assessed. For this, the difference in vegetation greenness (standing biomass) between the human-production habitat and the protected forests was analysed from remotely-sensed Normalized Differential Vegetation Index (NDVI), and further confirmed by measuring dietary quality (faecal nitrogen (N) content and C:N ratio as proxies for crude protein). Interestingly, higher NDVI values (greater biomass availability), higher N content and lower faecal C:N ratio (indicating higher protein content in the diet) of elephants in the human-production habitat suggested enhanced nutritional levels here as compared to protected forests. Further, there were significant correlations between faecal C:N ratio (positive) or N content (negative) and fGCM levels. These findings suggest that crop-raiding comes with the benefits of a superior quality diet which may help in reducing human-induced stress-response in elephants inhabiting or foraging within human-production habitats.

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“…The results of our radiometabolism studies confirmed that the epi-A EIA detected immunoreactive, radiolabelled fTM in both an adult male and female. EIAs using antibodies directed against epi-A have also been validated for monitoring the gonadal status of other mammals, including the African and Asian elephant, Loxodonta africana and Elephas maximus [ 58 , 59 ] and the sun bear, Helarctos malayanus [ 60 ]. Epi-A is also a major testosterone metabolite in faeces of macaques [ 19 , 61 ].…”

Section: Discussionmentioning

confidence: 99%

Measuring Faecal Epi-Androsterone as an Indicator of Gonadal Activity in Spotted Hyenas (Crocuta crocuta)

et al. 2015

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Enzyme immunoassays (EIA) that measure faecal testosterone metabolites (fTM) are useful tools to monitor gonadal activity. The aim of this study was to validate an “in-house” epiandrosterone EIA to monitor fTM in spotted hyenas. FTM were characterised in a male and a female hyena that each received an injection of 3H-testosterone. High-performance liquid chromatography (HPLC) analyses revealed a cluster of highly polar enzyme-hydrolysable hormone metabolite conjugates. We performed hydrolysis using β-glucuronidase to deconjugate metabolites and improve sensitivity of the assay. Because β-glucuronidase from Helix pomatia has been reported to bias testosterone measurements in some species, we compared the enzymatic activity of the commonly used β-glucuronidase extracted from H. pomatia with the same enzyme from Escherichia coli. Our results showed that β-glucuronidases from both sources produced similar results from spotted hyena faeces. We therefore hydrolysed samples with H. pomatia enzymes. HPLC analyses also demonstrated that following hydrolysis the epiandrosterone EIA measured significant amounts of immunoreactive metabolites corresponding to radiolabelled metabolites in both sexes. Additionally, HPLC and GC-MS analyses confirmed the presence of epiandrosterone in faeces of spotted hyenas. The biological relevance of the epiandrosterone EIA was validated by demonstrating (1) a significant increase in fTM levels in response to a testosterone injection within 16 h, (2) no biological responsiveness to an adrenocorticotropic hormone (ACTH) injection and (3) significant differences in fTM levels between juvenile males and adult immigrant males in a free-ranging wild population. Our results clearly demonstrate that the epiandrosterone EIA is a reliable non-invasive method to monitor gonadal activity in spotted hyenas.

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Endocrine Correlates of Musth in Free-Ranging Asian Elephants (Elephas maximus) Determined by Non-Invasive Faecal Steroid Hormone Metabolite Measurements

Cited by 26 publications

References 32 publications

Age and socially related changes in fecal androgen metabolite concentrations in free-ranging male giraffes

Age and socially related changes in fecal androgen metabolite concentrations in free-ranging male giraffes

Lower levels of glucocorticoids in crop‐raiders: diet quality as a potential ‘pacifier’ against stress in free‐ranging Asian elephants in a human‐production habitat

Measuring Faecal Epi-Androsterone as an Indicator of Gonadal Activity in Spotted Hyenas (Crocuta crocuta)

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