Fathead Minnows Exposed to Organic Compounds from Oil Sands Tailings as Embryos Have Reduced Survival, Impaired Development, and Altered Behaviors That Persist into Larval Stages

Abstract

Our study evaluated whether exposure to naphthenic acid fraction compounds (NAFCs) extracted from oil sands process-affected waters (OSPW) has adverse effects on fish embryos that persist into later life. We exposed fathead minnow (Pimephales promelas) embryos to concentrations of NAFCs found in OSPW (2.5-54 mg/L) for 7 days (1 day postfertilization to hatch), then raised surviving larvae in outdoor mesocosms of uncontaminated lake water for 1 month. Embryos exposed to NAFCs were more likely to exhibit malformations (by up to 8-fold) and had slower heart rates (by up to 24%) compared to controls. Fish raised in uncontaminated lake water following exposure to NAFCs as embryos, were 2.5-fold less likely to survive during the larval stage than control fish. These fish also showed up to a 45% decrease in swim activity and a 36% increase in swim burst events during behavioral tests relative to controls. We conclude that exposure to NAFCs during the embryonic stage can have lasting effects on fish survival, physiology, and behavior that persist at least through the larval stage. These findings of delayed mortalities and persistent sublethal effects of embryonic NAFC exposure are relevant to informing the development of regulations on treated OSPW releases from mining operations.

Naphthenic acid fraction compounds, produced by the extraction of bitumen from oil sands, alter survival and behaviour of juvenile yellow perch (Perca flavescens)

“…These treatment concentrations are below those reported for fresh oil sands tailings (19.7-85 mg/L; Mahaffey and Dubé 2017) and are at the low end of the range of concentrations reported for reclamation ponds (5-40 mg/L; Anderson et al 2012;Kavanagh et al 2013) and bitumen-affected wetlands in Canada's oil sands region (3.3-72 mg/L; Vander Meulen et al 2021a). Background concentrations of NAFCs in natural water in control mesocosms were 1.2 ± 0.3 mg/L (mean ± SD; n = 11), which is comparable to values we reported previously for natural lake water (∼0.5 mg/L) (Reynolds et al 2022;Robinson et al 2023) and reference wetlands in Canada's oil sands region unaffected by bitumen-derived inputs (Vander Meulen et al 2021b). The background acid-extractable compounds that were detected in natural water included substantial amounts of z = 0 compounds (i.e., C 9, C 10 , C 16 , and C 18 ) that were likely fatty acids, as well as oxygen-rich formulae (e.g., O 3 -, O 4 -, O 5 -, and O 6 -containing formulae) reflective of ubiquitous humic and/or fulvic materials, similar to previous observations from Athabasca region surface waters observed with this method (Sun et al 2017).…”

“…Equilibrium losses have also been observed in juvenile pink salmon exposed to crude oil, which is notable as NAFCs are found in oil residues (Yang et al 2021). Reynolds et al (2022) observed similar equilibrium losses in recently hatched fathead minnows exposed to 21 and 29.5 mg/L of NAFCs, concentrations that were also associated with higher rates of mortality. One study suggests that loss of equilibrium in fish can serve as an alternate endpoint that can identify a larger portion of the population that is under stress and potential forthcoming mortality (Gosselin and Anderson 2020).…”

“…Our findings of substantially reduced yellow perch survival following exposure to 15 mg/L NAFCs provide important new context for the impacts of NAFCs on fish survival. A recent study on embryonic fathead minnows using the same NAFC extract reported an LC 50 value of 28.5 mg/L and a 10% benchmark dose value of 22.3 mg/L (Reynolds et al 2022). Laboratory-based studies using NAFCs derived from the same settling basin (Industry A, but sampled in different years) and using the same extraction method as this study reported an EC 50 value for hatch success of 11 mg/L for walleye embryos and 23.2 mg/L for fathead minnow embryos (Marentette et al 2015b).…”

“…This experiment used an NAFC extract prepared from a large volume sample from an active tailings pond in Canada's oil sands region. The preparation and analysis of this NAFC extract have been described in detail elsewhere (Marentette et al 2015a, b;Bartlett et al 2017;Reynolds et al 2022). In summary, a large volume (<1000 L) of OSPW was acidified to pH < 2 and allowed to settle for 24 h prior to centrifugation.…”

“…Moreover, embryonic exposure to OSPW causes decreased activity, alters swim speed, and impairs alarm responses in zebrafish (Danio rerio), and these changes in behaviour are transgenerational (Philibert et al 2019). Only one study to date has reported changes in fish behaviour in response to NAFCs specifically, showing embryonic exposure alters swimming activity in larval fathead minnows (Reynolds et al 2022).…”