Naphthenic Acid Mixtures and Acid-Extractable Organics from Oil Sands Process-Affected Water Impair Embryonic Development of Silurana (Xenopus) tropicalisClick to copy article linkArticle link copied!
- Juan M. Gutierrez-VillagomezJuan M. Gutierrez-VillagomezDepartment of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5More by Juan M. Gutierrez-Villagomez
- Kerry M. PeruKerry M. PeruWatershed Hydrology and Ecology Research Division, Water Science and Technology, Environment and Climate Change Canada, Saskatoon, Saskatchewan, Canada S7N 3H5More by Kerry M. Peru
- Connor EdingtonConnor EdingtonDepartment of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5More by Connor Edington
- John V. HeadleyJohn V. HeadleyWatershed Hydrology and Ecology Research Division, Water Science and Technology, Environment and Climate Change Canada, Saskatoon, Saskatchewan, Canada S7N 3H5More by John V. Headley
- Bruce D. PauliBruce D. PauliEcotoxicology and Wildlife Health Division, Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment and Climate Change Canada, Ottawa, Ontario, Canada K1S 5B6More by Bruce D. Pauli
- Vance L. Trudeau*Vance L. Trudeau* E-mail: [email protected]Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5More by Vance L. Trudeau
Abstract
Naphthenic acids (NAs) are carboxylic acids naturally occurring in crude oils and bitumen and are suspected to be the primary toxic substances in wastewaters associated with oil refineries and mining of oil sands. Oil sands process-affected water (OSPW) generated by the extraction of bitumen from oil sands are a major source of NAs and are currently stored in tailings ponds. We report on the acute lethality and teratogenic effects of aquatic exposure of Silurana (Xenopus) tropicalis embryos to commercial NA extracts and from the acid extractable organics (AEOs) fraction of a Canadian OSPW. Using electrospray ionization-high resolution mass spectrometry, we determined that the O2 species proportion were 98.8, 98.9 and 58.6% for commercial mixtures Sigma 1 (S1M) and Sigma 2 (S2M), and AEOs, respectively. The 96h LC50 estimates were 10.4, 11.7, and 52.3 mg/L for S1M, S2M, and the AEOs, respectively. The 96h EC50 estimates based on frequencies of developmental abnormalities were 2.1, 2.6, and 14.2 mg/L for S1M, S2M, and the AEOs, respectively. The main effects observed were reduced body size, edema, and cranial, heart, gut and ocular abnormalities. Increasing concentrations of the mixtures resulted in increased severity and frequency of abnormalities (p < 0.05). The rank-order potency was S1M > S2M > AEO based on LC50 and EC50 estimates. These data provide insight into the effects NAs in amphibian embryos and can contribute to the development of environmental guidelines for the management of OSPW.
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(19)
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(18)
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(12)
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(12)
https://doi.org/10.1093/femsec/fiad153
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(3)
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(3)
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(3)
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(1)
https://doi.org/10.1093/conphys/coac030
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- John V. Headley, Kerry M. Peru, Ian Vander Meulen. Advances in mass spectrometry for molecular characterization of oil sands naphthenic acids and process chemicals in wetlands. Canadian Journal of Chemistry 2021, 99
(10)
, 821-830. https://doi.org/10.1139/cjc-2020-0478
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(10)
, 1582. https://doi.org/10.3390/antiox10101582
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(4)
, 483-492. https://doi.org/10.1002/jat.3920
- Barry N. Madison, Jessie Reynolds, Lauren Halliwell, Tim Leshuk, Frank Gu, Kerry M. Peru, John V. Headley, Diane M. Orihel, . Can the toxicity of naphthenic acids in oil sands process-affected water be mitigated by a green photocatalytic method?. FACETS 2020, 5
(1)
, 474-487. https://doi.org/10.1139/facets-2019-0053
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