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

Abstract

There is growing evidence from experimental and human epidemiological studies that many pollutants can disrupt lipid metabolism. In Arctic wildlife, the occurrence of such compounds could have serious consequences for seasonal feeders. We set out to study whether organohalogenated compounds (OHCs) could cause disruption of energy metabolism in female polar bears (Ursus maritimus) from Svalbard, Norway (n = 112). We analyzed biomarkers of energy metabolism including the abundance profiles of nine lipid-related genes, fatty acid (FA) synthesis and elongation indices in adipose tissue, and concentrations of lipid-related variables in plasma (cholesterol, high-density lipoprotein, triglycerides). Furthermore, the plasma metabolome and lipidome were characterized by low molecular weight metabolites and lipid fingerprinting, respectively. Polychlorinated biphenyls, chlordanes, brominated diphenyl ethers and perfluoroalkyl substances were significantly related to biomarkers involved in lipid accumulation, FA metabolism, insulin utilization, and cholesterol homeostasis. Moreover, the effects of pollutants were measurable at the metabolome and lipidome levels. Our results indicate that several OHCs affect lipid biosynthesis and catabolism in female polar bears. Furthermore, these effects were more pronounced when combined with reduced sea ice extent and thickness, suggesting that climate-driven sea ice decline and OHCs have synergistic negative effects on polar bears.

Persistent Organic Pollutant Burden, Experimental POP Exposure, and Tissue Properties Affect Metabolic Profiles of Blubber from Gray Seal Pups

“…Previous studies of metabolic effects of POPs on marine mammals have focussed on adults 55,63,64,66 . Concentrations of POPs in adult seals are an order of magnitude greater than those found in pups, with adult seal blubber containing several thousand ∑PCBs (ng/g) 115 compared to the levels detected in the pups here, which were in the hundreds of ng/g range (Table 1).…”

“…Phocid pups thus experience high POP exposure during both feeding and fasting, two fundamentally important periods for adipogenesis, fat mobilisation and maturation of energy balance pathways. Their reliance on adipose tissue to fuel metabolism during fasting or while searching for food in changing environments 55 properties with blubber depth 54,[56][57][58][59][60][61] . Effects of blubber depth and nutritional state on metabolic function and sensitivity to POP exposure have not been explored.…”

“…Experimental studies have demonstrated that POPs can alter adipocyte function in rodents and human cell lines25,104 . POPs are associated with altered adipose and liver expression of metabolic pathway genes in adult polar bears55,66 and ringed seals (Pusa hispida)63,64 , but the functional consequences of such changes for fat tissue have not been identified.Recent experimental studies that replicate environmental or physiological POP concentrations and congener mixtures provide causal evidence of their immunological105 and adipogenic effects91 . Our work builds on these findings by showing that existing POP concentrations in blubber tissue, generated in utero and through lactational transfer, can alter metabolic properties of adipose tissue in young, developing seals.Our data are consistent with experimental studies showing PCB 77, 153 and dioxin reduce glucose and insulin tolerance in mice, guinea pigs (Cavia porcellus),…”

Dioxin impacts on lipid metabolism of soil microbes: towards effective detection and bioassessment strategies

“…Such lipidic alterations can allow organisms to maintain essential biological functions while adapting to environmental changes including toxic contaminants. Much research has been conducted to determine the major metabolic responses in lipid metabolism of microorganisms exposed to environmental stressors, including persistent toxicants (Tartu et al 2017). The overall lipidic profile of an organism, or part thereof, at a given time is referred to as the lipidome.…”

Investigating decadal changes in persistent organic pollutants in Scottish grey seal pups

“…POPs such as CBs, BDEs, and organochlorine pesticides (OCPs), including dichlorodiphenyltrichoroethane (DDT), have been linked to endocrine disruption (Noël et al, 2017;Routti et al, 2010;Tanabe, 2002;Villanger et al, 2011Villanger et al, , 2013 and negative impacts on reproductive (Helle, Olsson, & Jensen, 1976b;Hoydal et al, 2017;Murphy et al, 2010;Reijnders, 1986) and immune (Fisk et al, 2005, Hall et al, 2006, Hammond, Hall, & Dyrynda, 2005, reviewed in Desforges et al, 2016Penin et al, 2018) function in marine mammals. POPs have also recently been connected with lipid disruption in a range of phyla (Lee et al, 2016;Speranza et al, 2016;Yadetie et al, 2017), including marine mammals (Castelli, Rusten, Goksøyr, & Routti, 2014;Robinson et al, 2018;Tartu et al, 2017), because they alter pathways that enable individuals to accumulate or mobilize fat reserves appropriately. Viable immune and endocrine function, successful reproductive efforts, and the ability to use energy stores are all crucial to the fitness and survival of individuals in the wild.…”