James P. Meador

Crude oil and its water-soluble fractions (WSF) are highly toxic to early life stages of fishes, while exposed adults are often considered more resilient. However, research suggests that parental exposure can result in toxic effects in subsequent generations. This study investigated the impact of a crude oil WSF on Atlantic cod ( Gadus morhua ) broodstock and the subsequent maternal effects on their offspring. Mature Atlantic cod at late gametogenesis were exposed for 20 days to either a crude oil WSF or to control conditions. Over the following month, fish from both groups were repeatedly strip-spawned, and egg batches were fertilized in vitro using pooled sperm from control males. Maternally exposed offspring had accumulated levels of petroleum-derived aromatic hydrocarbons, including monoaromatic and polyaromatic hydrocarbons (PAHs). However, the profile of accumulated compounds was skewed towards lower-molecular weight compounds compared to the exposure water. Crude oil WSF exposure appeared to accelerate spawning readiness in females, resulting in smaller egg diameters in strip-spawned eggs. Additionally, sperm from oil-exposed males showed reduced curvilinear velocity and linearity. Despite these impacts, no significant differences in larval malformations or cardiac activity were observed. Our findings highlight the importance of advancing our understanding of intergenerational impacts of crude oil contamination on key fish species to accurately assess the long-term ecological consequences of petroleum pollution.

The early-life stage (ELS) toxicity syndrome for fish is well described and has been reported in hundreds of toxicity studies. It is generally characterized by a reduced heart rate, yolk sac and pericardial edemas, and various morphological abnormalities, the most common being spinal curvature. For many of those studies, it appears that the ELS toxicity syndrome is the result of nonspecific (baseline) toxicity that occurs at aqueous and whole-body concentrations that are just below lethal concentrations. Baseline toxicity is essentially a nonspecific response that results from chemicals accumulating in and disturbing the function of biological membranes that leads to lethality and sublethal effects at relatively high doses. The commonality of this acute ELS toxicity syndrome among highly diverse organic and inorganic chemicals is remarkable. It is important to identify baseline toxicity because it is considered minimal toxicity that acts in all tissues and cells, and it has the potential to impair all cellular functions. This means if an effect is observed around baseline-toxic concentrations, it is likely that other cellular functions are also affected (i.e., the effect is not specific). The fish ELS toxicity syndrome can also be the result of specific effects involving receptor interactions; therefore, we emphasize the importance of distinguishing between specific and nonspecific toxicity responses to provide the most relevant data for environmental risk assessment.

Numerous studies of the water-soluble fraction (WSF) from crude oil have concluded that polycyclic aromatic hydrocarbons (PAHs) are the primary causative agents for early life stage (ELS) fish toxicity. Noteworthy is the lack of studies demonstrating that the sum of PAHs are capable of causing toxic effects in ELS fish at the low levels claimed (0.1–5 μg/L) without being part of a complex crude oil mixture. Crude oil and the WSF are composed of thousands of other compounds that co-occur and likely contribute to crude oil toxicity. Based on the available data, it appears that the syndrome of effects (lower heart rate, edemas, and morphological abnormalities) for ELS fish exposed to the aqueous fraction of a crude oil mixture is commonly observed in studies exposing fish embryos to high concentrations of a variety of compounds and may be a nonspecific response. We conclude that the available data support the hypothesis that this syndrome of effects is likely the result of baseline toxicity (not receptor based) due to membrane disruption and resulting alteration in ion (e.g., calcium and potassium) homeostasis. We acknowledge the possibility of some compounds in the WSF capable of causing a specific receptor based toxicity response to ELS fish; however, such compounds have not been identified nor their receptor characterized. Concluding that PAHs are the main toxic compounds for crude oil exposure is misleading and does not result in guideline values that can be useful for environmental protection. Water quality guidelines for any single chemical or suite of chemicals must be based on a complete understanding of exposure concentrations, mechanism of action, potency, and resulting response. This review focuses on the toxic effects reported for fish embryos and the purported toxic concentrations observed in the aqueous phase of an oil/water mixture, the known levels of toxicity for individual PAHs, a toxic unit approach for characterizing mixtures, and the potential molecular initiating event for ELS toxicity in fish. This review also has implications for a large number of studies exposing ELS fish to a variety of compounds at high concentrations that result in a common baseline toxic response.