Potentiation of ecological factors on the disruption of thyroid hormones by organo-halogenated contaminants in female polar bears (Ursus maritimus) from the Barents Sea

Abstract

As apex predators, polar bears (Ursus maritimus) are among the most heavily polluted organisms in the Arctic. In addition to this anthropogenic stressor, climate warming has been shown to negatively affect their body condition, reproductive output and survival. Among potential underlying physiological mechanisms, thyroid hormones (THs), which control thermoregulation, metabolism and reproduction, can be affected by a variety of both natural and anthropogenic factors. While THs have been extensively used as proxies for pollution exposure in mammals, including polar bears, there is a lack of knowledge of their natural variations. In this context, we examined seasonal variations in body condition and circulating TH concentrations in free-ranging female polar bears. Females with variable reproductive status (i.e., solitary, with cubs of the year or with yearlings) were sampled from locations with contrasted sea ice conditions. Furthermore, we studied THs in relation to levels of organohalogenated contaminants. As predicted, solitary females were in better condition than females caring for offspring, especially in spring. In addition, TH levels were lower in autumn compared to spring, although this seasonal effect was mainly observed in solitary females.Finally, the negative relationships between organochlorine and perfluoroalkyl substances and some THs suggest a possible alteration of homeostasis of THs. Since the latter relationships were only observed during spring, we emphasize the importance of considering the ecological factors when using THs as proxies for pollution exposure. Yet, the combined effects of natural and anthropogenic stressors on THs might impair the ability of polar bears to adapt to ongoing climate changes.

Multiple-stressor effects in an apex predator: combined influence of pollutants and sea ice decline on lipid metabolism in polar bears

“…This association could involve a disruption of the hypothalamic-pituitary-thyroid (HPT) axis. As previously mentioned, PFASs predicted decreased concentrations of free triiodothyronine (T3) in the present female polar bears 31 . In humans, and in murine and primate models, studies have reported negative associations between thyroid hormones and lipid related plasma parameters such as cholesterol, triglycerides and HDL 61 – 63 .…”

“…We tested the effects of age, body condition index (BCI), body mass and diet proxies (nitrogen and carbon stable isotope values in red blood cells) on energy metabolism biomarkers (Table S3 ). All energy biomarkers were either predicted by BCI, body mass or diet proxies (Table S3 ) and as previously mentioned BCI, body mass and diet proxies are all confounded with season 31 , 39 , 92 , 96 . To remove the possible confounding effect of season and test the effect of pollutants on metabolism biomarkers, we used GLMMs with pollutant concentrations as fixed factors, and, female identity and season as random factors.…”

“…The best predictors of the concentrations of lipophilic and proteinophilic pollutants in the polar bears used in this study were previously determined to be body condition and diet, respectively, which are both related to season 31 , 39 , 92 , 96 . We tested the effects of age, body condition index (BCI), body mass and diet proxies (nitrogen and carbon stable isotope values in red blood cells) on energy metabolism biomarkers (Table S3 ).…”

Per‐ and Polyfluoroalkyl Substances Are Positively Associated with Thyroid Hormones in an Arctic Seabird

“…Positive correlations between various PFAS and circulating concentrations of T4 and/or T3 have been reported for seabirds (Braune et al 2011; Nøst et al 2012; Melnes et al 2017; Hovden 2018). In contrast, negative correlations have been found between PFAS and thyroid hormones in polar bears ( U. maritimus ; Bourgeon et al 2017), suggesting that the impact of PFAS on this endocrine axis may depend on the degree of PFAS contamination, the species, or the environmental context.…”

Contaminants in Atlantic walruses in Svalbard Part 2: Relationships with endocrine and immune systems

“…A large number of contaminants are known to affect mammalian thyroid systems through multiple target-points in the thyroid hormone system (Gore et al, 2015). Thyroid hormones (THs) are involved in growth, neurologic development and metabolism (McNabb, 1992;Zhu and Cheng, 2010) and altered TH levels have been associated with exposure to lipophilic POPs, their metabolites and/or PFASs in ringed seals (Pusa hispida), harbor seals (Phoca vitulina), hooded seals (Cystophora cristata), white whales (Delphinapterus leucas) and polar bears (Bourgeon et al, 2017;Gabrielsen et al, 2011;Routti et al, 2010;Tabuchi et al, 2006;Villanger et al, 2011). Both circulating TH levels as well as multiple other molecules involved in thyroid homeostasis such as receptors and enzymes involved in thyroid hormone action and metabolism, respectively, can be used as biomarkers to study effects of contaminants.…”