Determining potential natural and anthropogenic drivers of adrenocortical activity in African clawless otters (Aonyx capensis) by evaluating faecal glucocorticoid metabolite concentrations

Abstract

The rate of human-induced disturbance over the last century constitutes a major threat to wildlife species’ distribution, behaviour, physiological function, and overall fitness as populations struggle to respond to rapid transformation in the environment. Otters are piscivorous predators and, despite their low abundance, are considered keystone species in aquatic environments given their key role in the functioning of this ecosystem. Their trophic II position as apex predators and sensitivity to environmental change make otters suitable indicator species for environmental monitoring. Elsewhere, river otters (Lontra canadensis) have been used to assess environmental conditions, and the likely effect of contaminants on habitat health. To date however, African clawless otters (Aonyx capensis) have not been used to monitor environmental change in aquatic systems. Thus, the overall aim of this study was to examine the effect of water quality, diet, and anthropogenic disturbance on faecal glucocorticoid metabolite (fGCM) concentrations (a reliable indicator of stress) in African clawless otters to evaluate how these relationships vary by sex and season. As a prerequisite, enzyme immunoassays (EIAs) for quantifying faecal androgen metabolites (fAM) and faecal progestagen metabolites (fPM) were validated. Subsequently, the suitability of using a fPM:fAM ratio to distinguish between male and female otter faecal deposits was assessed. As environmental conditions and bacterial enzymes can affect immunoreactive faecal hormone metabolite (fGCM, fAM, and fPM) concentrations post-defecation, the stability of steroid hormone metabolite composition post-defaecation was also determined for each sex and steroid class before the stress responses or reproductive physiology were examined. This allowed me to determine the time window in which faecal samples should be collected for steroid hormone quantification so that respective results can reliably compared. Utilizing a previously established Cortisol EIA to measure fGCM concentrations, the hormone stability study showed that immunoreactive fGCM concentrations of samples collected from a male exposed to full sun and full shade remained stable for 3 hours and 12 hours post-defaecation, respectively. In comparison, fGCM concentrations for samples collected from a female, as well as fAM and fPM concentrations of samples from both sexes, remained stable for at least 12 hours post-defaecation, regardless of the environmental conditions to which they were exposed. After successfully evaluating the sample collection procedure, I collected faecal samples from free ranging African clawless otters from three study sites: Kalkfontein Nature Reserve (KNR), Rietvlei Nature Reserve (RNR), and Millstream Farm (MF). The investigation of spatial and temporal differences in otter diet using faeces highlights a variation in diet composition across all three sites during the dry winter season, suggesting that African clawless otters have a broad dietary niche. Additionally, the occurrence of specific prey items differed significantly across sites, with insects identified as a key resource in African clawless otters for the first time. Finally, I compared changes in fGCM concentrations of otters across the three study sites in relation to different environmental and anthropogenic disturbances. The fGCM concentrations of otters were measured and compared between a pristine (KNR), polluted (RNR), and artificially transformed (MF) site. Overall, considerably higher fGCM concentrations were measured in male otters compared to females. Apart from potential sexspecific metabolic processes, this may indicate sex-specific drivers of adrenocortical activity. The fGCM concentrations differed significantly across the three study sites. The fGCM concentrations of individuals from the transformed site were significantly higher compared to fGCM concentrations measured in individuals at the pristine site. However, fGCM concentrations in individuals at the polluted site showed no significant difference from individuals at either KNR or MF. Otters at KNR exhibited higher fGCM concentrations III associated with colder minimum and maximum ambient temperatures. This suggest that fGCM concentrations may reflect thermoregulatory demands in African clawless otters and could be used as a tool to further investigate thermoregulatory load in the species. Anthropogenic presence and a diet consisting of predominantly rainbow trout (Oncorhynchus mykiss) associated with higher internal parasite loads observed in otter faecal deposits were factors that exerted a significant effect on glucocorticoid secretion in individuals at MF. The composition of rainbow trout consists of high saturated fatty acid content and low monounsaturated fatty acids. High-fat diets are known to induce obesity and cause other related health problems in mammals. An investigation of the body mass index and body condition of otters at MF could provide a better understanding of whether this dietary item poses health concerns for otters, and possibly other piscivorous animals inhabiting the area. Finally, of the variables investigated in this study, none adequately explain the fGCM concentrations observed in individuals at RNR. Although the fGCM concentrations from otters at RNR was not significantly different from either KNR or MF, mean fGCM concentrations were only 2.9% lower than those at MF, and 58.5% higher than those at KNR. Considering that water quality was categorised as class 2 (acceptable) or class 3 (regular) according to criteria outlined in the water quality index (WQI) score classification system used for all three study sites, it was difficult to determine the effect of water quality on the adrenocortical activity of African clawless otters. However, RNR had the highest seasonal difference in its WQI score, with a difference of 12 points, which could explain the increased fGCM concentrations observed at this study site. It is also possible that other biotic factors including age, reproductive status, predation, competition, food abundance and availability, disease, and parasite load, known to elicit a physiological stress response, could explain the results observed at this site. Evidence from this study supports the theory that African clawless otters have a broad dietary niche and are able to adapt to prey availability and abundance within their habitat. Although otters can exploit rainbow trout when availability and abundance is high, the findings of this study suggest that the consumption of anthropogenically provided resources is a major driver of glucocorticoid secretion and could result in obesity and other related health concerns including increased intestinal parasite loads. Future research focussing on otter reproductive physiology, behavioural responses to anthropogenic disturbances, and how anthropogenically provided food sources could affect body mass and disease burdens in otters could provide opportunities for otter conservation and improved management strategies.