Effects of Aryl Hydrocarbon Receptor-Mediated Early Life Stage Toxicity on Lake Trout Populations in Lake Ontario during the 20th Century

Abstract

Lake trout embryos and sac fry are very sensitive to toxicity associated with maternal exposures to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and structurally related chemicals that act through a common aryl hydrocarbon receptor (AHR)-mediated mechanism of action. The loading of large amounts of these chemicals into Lake Ontario during the middle of the 20th century coincided with a population decline that culminated in extirpation of this species around 1960. Prediction of past TCDD toxicity equivalence concentrations in lake trout eggs (TEC(egg)s) relative to recent conditions required fine resolution of radionuclide-dated contaminant profiles in two sediment cores; reference core specific biota--sediment accumulation factors (BSAFs) for TCDD-like chemicals in lake trout eggs; adjustment of the BSAFs for the effect of temporal changes in the chemical distributions between water and sediments; and toxicity equivalence factors based on trout early life stage mortality. When compared to the dose-response relationship for overt early life stage toxicity of TCDD to lake trout, the resulting TEC(egg)s predict an extended period during which lake trout sac fry survival was negligible. By 1940, following more than a decade of population decline attributable to reduced fry stocking and loss of adult lake trout to commercial fishing, the predicted sac fry mortality due to AHR-mediated toxicity alone explains the subsequent loss of the species. Reduced fry survival, associated with lethal and sublethal adverse effects and possibly complicated by other environmental factors, occurred after 1980 and contributed to a lack of reproductive success of stocked trout despite gradually declining TEC(egg)s. Present exposures are close to the most probable no observable adverse effect level (NOAEL TECegg = 5 pg TCDD toxicity equivalence/g egg). The toxicity predictions are very consistent with the available historical data for lake trout population levels in Lake Ontario, stocking programs, and evidence for recent improvement in natural reproduction concomitant with declining levels of persistent bioaccumulative chemicals in sediments and biota.

Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish

“…A similar mechanism could be the basis for the population impacts of other cardiotoxic pollutants such as the dioxins and planar polychlorinated biphenyls (31). With the high degree of evolutionary conservation among vertebrate hearts, these findings in zebrafish also have implications beyond both fish populations and contaminants, relating to environmental impacts on heart shape and cardiac output in humans.…”

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

“…In fish embryos, DLCs normally produce a suite of developmental defects that came to be known as blue‐sac disease after their appearance in lake trout exposed to dioxin in the US Great Lakes (Cook et al., 2003; Tillitt, Cook, Giesy, Heideman, & Peterson, 2008). This toxicity is characterized by reduced embryo size, defects in swim bladder formation, alteration of jaw cartilage, vascular hemorrhaging in the yolk sac, brain, and tail, pericardial and yolk‐sac edema, and malformation of the heart (King‐Heiden et al., 2012).…”

Adverse outcome pathways and ecological risk assessment: Bridging to population-level effects

“…A relatively well-characterized response to AhR agonists in developing salmonid fish is a lethal condition termed blue sac disease [54]. Although the cascade of biochemical and physiological events linking activation of the AhR to blue sac disease are not fully defined, the relationship between activation of the receptor and early-life-stage mortality nonetheless has proved sufficient to conduct a robust retrospective assessment of effects of planar halogenated hydrocarbons on a Great Lakes lake trout population [55].…”

“…To assess the possible role of PCB, polychlorinated dibenzofuran, and PCDD contamination in causing this, Cook et al [55] reconstructed a historical exposure record of Lake Ontario lake trout to the mixture of AhR agonists present in the lake, using a combination of empirical sediment:tissue residue relationships and radio-dating approaches through analysis of sediment core samples. Based on potency (receptor binding or activation) of the different PCBs, polychlorinated dibenzofurans, and PCDDs in the sediments, they converted the exposure information for the mixture into a single potency value (assuming additivity based on the common AOP) calibrated to 2,3,7,8-tetrachlorodebenzo-p-dioxin.…”

“…Historic survival of the lake trout embryos then could be indexed to measured toxicity of 2,3,7,8-tetrachlorodebenzo-p-dioxin to developing embryos in controlled laboratory studies. Cook et al [55] compared their temporal exposure and toxicity predictions with historic commercial lake trout harvest data for Lake Ontario. They observed a strong correlation between predicted occurrence of early-lifestage mortality of the fish and observed harvest data and also reported indications of some degree of recent recovery of the lake trout population, associated perhaps with natural burial of historically contaminated sediments.…”