Mercury Bioaccumulation and Cortisol Interact to Influence Endocrine and Immune Biomarkers in a Free-Ranging Marine Mammal

Abstract

Mercury bioaccumulation from deep-ocean prey and the extreme life history strategies of adult female northern elephant seals (Mirounga angustirostris) provide a unique system to assess the interactive effects of mercury and stress on animal health by quantifying blood biomarkers in relation to mercury (skeletal muscle and blood mercury) and cortisol concentrations. The thyroid hormone thyroxine (tT4) and the antibody immunoglobulin E (IgE) were associated with mercury and cortisol concentrations interactively, where the magnitude and direction of the association of each biomarker with mercury or cortisol changed depending on the concentration of the other factor. For example, when cortisol concentrations were lowest, tT4 was positively related to muscle mercury, whereas tT4 had a negative relationship with muscle mercury in seals that had the highest cortisol concentrations. Additionally, we observed that two thyroid hormones, triiodothyronine (tT3) and reverse triiodothyronine (rT3), were negatively (tT3) and positively (rT3) associated with mercury concentrations and cortisol in an additive manner. As an example, tT3 concentrations in late breeding seals at the median cortisol concentration decreased by 14% across the range of observed muscle mercury concentrations. We also observed that immunoglobulin M (IgM), the pro-inflammatory cytokine IL-6 (IL-6), and a reproductive hormone, estradiol, were negatively related to muscle mercury concentrations but were not related to cortisol. Specifically, estradiol concentrations in late molting seals decreased by 50% across the range of muscle mercury concentrations. These results indicate important physiological effects of mercury on free-ranging apex marine predators and interactions between mercury bioaccumulation and extrinsic stressors. Deleterious effects on animals’ abilities to maintain homeostasis (thyroid hormones), fight off pathogens and disease (innate and adaptive immune system), and successfully reproduce (endocrine system) can have significant individual- and population-level consequences.

Bioaccumulation and Potential Endocrine Disruption Risk of Legacy and Emerging Organophosphate Esters in Cetaceans from the Northern South China Sea

“…The mean concentrations of testosterone, T3, T4, and cortisol were 1.4 ± 2.7, 51.9 ± 48.4, 10.6 ± 5.4, and 23.0 ± 31.8 ng/g lw, respectively (Table S10). As a stress indicator in mammals, cortisol tends to positively correlate with the severity of the stressor . In this study, no significant correlations were found between the concentrations of all five OPE congeners (TDBPP, TBOEP, TCIPP, TCrP, and TDCIPP) and cortisol in humpback dolphins (Figure S4), suggesting that current OPE exposure did not cause physiological stress in the dolphin species.…”

“…The findings suggest that OPE exposure may have impacted the thyroid function in the dolphins. While studies on the relationship between OPEs and thyroid hormones in cetaceans are limited, in vitro and in vivo studies have demonstrated that OPE exposure could cause thyroid hormone disturbances in mammals, leading to an increased risk of cancer, impaired brain development of offspring during gestation, and other adverse health outcomes. , Considering the sensitive thyroid axis of marine mammals, which helps manage the different demands of their lifestyles, our findings suggest that disturbances in thyroid hormones might have adverse downstream health effects to humpback dolphins . For example, increased oxygen consumption has been documented in diving harbor seals (Phoca vitulina) with induced hyperthyroidism …”

“…87,88 Considering the sensitive thyroid axis of marine mammals, which helps manage the different demands of their lifestyles, our findings suggest that disturbances in thyroid hormones might have adverse downstream health effects to humpback dolphins. 86 For example, increased oxygen consumption has been documented in diving harbor seals (Phoca vitulina) with induced hyperthyroidism. 89 Testosterone is a steroid hormone primarily produced by the testes in males and the ovaries and adrenal glands in females.…”