Triiodothyronine (T3) levels fluctuate in response to ambient temperature rather than nutritional status in a wild tropical ungulate

Abstract

Animals can employ a range of physiological mechanisms in response to unpredictable changes within their environment, such as changes in food availability and human disturbances. For example, impala exhibit higher faecal glucocorticoid metabolite (FGM) levels—indicative of physiological stress—in response to low food quality and higher human disturbance. In this study, we measured faecal triiodothyronine (T3) metabolite (FTM) levels in 446 wild impala from 2016 to 2018 to test the hypothesis that environmental and human disturbances would affect their physiological status. We also validated a faecal thyroid hormone assay. T3 levels mainly regulate metabolic rate and drive thermoregulation—increasing with colder temperatures. We predicted that individuals would have lower FTM levels, indicative of poor physiological status, (i) when food quality was poor, (ii) when ambient temperature (Ta) was high, (iii) in areas of high human disturbance (due to food competition with livestock) and (iv) when FGM levels were high. Interestingly, we found that Ta was the most important predictor of FTM—FTM levels decreased by 70% from lowest to highest Ta—and food quality and human disturbance only influenced FTM levels when Ta was accounted for. FTM levels also tended to increase with increasing FGM levels, opposite our predictions. Our results suggest that food quality and availability may only partially influence FTM levels and that fluctuations in Ta are a significant driver of FTM levels in a wild tropical ungulate. Given that thyroid hormones are primarily responsible for regulating metabolic rate, they may be better indicators of how wild animals metabolically and energetically respond to environmental factors and only indicate poor nutritional status in extreme cases.

Non-invasive Assay for Measurement of Fecal Triiodothyronine (T3) Metabolite Levels in European Mouflon (Ovis aries musimon)

“…The biological validation did not show differences in FTM levels between mouflon ewes and rams, thus confirming previous findings in wild ungulates ( 26 , 27 ). As expected, FTM levels varied according to the ambient temperature, being higher in both sexes in March compared to July ( Table 3 ; p < 0.0001).…”

“…As expected, FTM levels varied according to the ambient temperature, being higher in both sexes in March compared to July ( Table 3 ; p < 0.0001). This preliminary result confirms that ambient temperatures is a main driver in T3 fluctuations in wild ungulates ( 27 ). Moreover, the obtained FTM levels were comparable with those reported in literature for another wild ungulate species ( 12 , 22 ).…”

Fecal thyroid hormone metabolites in wild ungulates: a mini-review

“…Considering the growing need of monitoring wild animal populations, the determination of the seasonal fluctuations of THs can provide valuable insights into their response to environmental changes and ability to adapt to harsh conditions. Wild animals are more exposed to unpredictable changes in their living environment, and they can implement various physiological mechanisms in response to such changes ( 3 , 4 ), such as increasing energy demands or reducing energy turnover ( 5 ).…”

“…For this reason, in the last few years, analytical methods to assess the concentration of hormones and metabolites in alternative biological matrices, such as feces ( 3 , 6 – 9 ) and hairs ( 10 , 11 ) have been intensively developed. A non-invasive approach is an animal-friendly technique that allows easy access to a great number of samples in a larger spatial–temporal window and provides a measure of hormone concentrations over a longer period ( 12 ).…”

Editorial: Biochemical and endocrinological parameters in animals matrices

“…Therefore, their monitoring is fundamental to assess animal's wellbeing. Nevertheless, these procedures can be very challenging, especially when these parameters have to be monitored on wild or protected species ( 3 ). In fact, the matrix to analyse, usually blood, is not always easily available without affecting animal welfare or stressing the animal.…”