Sublethal, sex-specific, osmotic, and metabolic impairments in embryonic and adult round stingrays from a location exposed to environmental contamination in southern California, USA

Abstract

Organic contaminants are known to affect a suite of physiological processes across vertebrate clades. However, despite their ancient lineage and important roles in maintaining healthy ecosystems, elasmobranchs (sharks, skates, and rays) are understudied with regard to sublethal effects of contaminant exposure on metabolic processes. Perturbations resulting from contaminant exposure can divert energy away from maintaining physiological homeostasis, particularly during energetically challenging life stages, such as pregnancy and embryonic development. Using the round stingray (Urobatis halleri) as a model elasmobranch species, we captured adult males and pregnant females (matrotrophic histotrophy) and their embryos from two populations differing in their environmental exposure to organic contaminants (primarily polychlorinated biphenyls (PCBs)). Pregnant females from the PCB-exposed population experienced significant decreases from early- to late-pregnancy in tissue mass and quality not seen in reference females. PCB-exposed pregnant females also failed to maintain plasma urea concentrations as pregnancy progressed, which was accompanied by a loss in muscle protein content. Despite the energetic demands of late-term pregnancy, females had significantly greater liver lipid content than reproductively inactive adult males. PCB-exposed adult males also had high metabolic capacity (i.e., enzyme activity) for most substrate groupings of all sex-site groups, suggesting that males may be even more negatively impacted by contaminant exposure than pregnant females. Evidence that in utero exposure to PCBs via maternal offloading impairs embryo outcomes is accumulating. Embryos from the PCB-contaminated site had lower tissue quality measures and indications that sex-based differences were manifesting in utero as males had higher metabolic capacities than females. This study indicates that accumulated PCB contaminants are not physiologically inert in the stingray.