Climate variations and a local PCB hotspot have altered metabolomic profiles in ringed seals.

Abstract

Environmental contaminants and climate change pose ongoing threats to Arctic marine mammals, yet their combined physiological impacts remain poorly understood. Here, we analyzed 234 metabolites in liver (n = 27, from 2010 to 2011) and serum/plasma (n = 38, from 2009 to 2011) to assess the health of ringed seals exposed to a local polychlorinated biphenyl (PCB) "hotspot" as well as other co-occurring contaminants from long-range sources. Demographic analyses revealed significant age and sex differences, with adult males carrying higher ∑PCB and ∑DDT (dichlorodiphenyltrichloroethane) concentrations than juveniles and females, reflecting bioaccumulation and maternal offload during lactation. Liver metabolite profiles showed stronger contaminant correlations than blood, indicating hepatic metabolism is more directly affected by contaminant exposure. Seals in the year 2010, marked by high sea surface temperatures and reduced ice cover, exhibited distinct serum/plasma signatures including polyunsaturated fatty acid depletion and increased saturated fatty acids, suggesting metabolic adaptation to environmental stress. Liver methionine sulfoxide levels correlated with PCBs (r_s = 0.44, p = 0.02), suggesting that PCBs may be inducing oxidative stress, while chlordanes correlated with amino acids (r_s = -0.49 to 0.45, p = 0.01-0.03), suggesting disrupted protein metabolism. Significant correlations between stable isotope values and contaminant-associated metabolites indicated that dietary factors may confound toxicological relationships. For example, mercury correlations with specific fatty acids paralleled δ¹³C patterns, highlighting challenges in distinguishing direct toxicological effects from shared ecological drivers. These metabolite profiles reveal how persistent pollutants and warming conditions jointly disrupt energy balance, oxidative status, and protein metabolism, demonstrating metabolomics' value for detecting sub-lethal health impacts in Arctic marine mammals.