Abstract
Purpose
Risks to native soil-dwelling organisms in terrestrial ecosystems contaminated by petroleum hydrocarbons (PHCs) are difficult to assess due to the range of compounds and their varying toxicity. Weathering of PHCs in soil has been shown to alter their chemical composition and decrease their associated toxicity. Hence, generic regulatory guidelines may inadequately predict risks and exposure scenarios at some sites.
Methods
In this study, the toxicity of both coarse- and fine-grained subarctic soils contaminated with weathered PHCs was assessed using two soil invertebrates, Folsomia candida and Proisotoma minuta. In addition to survival and reproduction tests, avoidance behavior was investigated using F. candida, P. minuta, Oppia nitens, and Folsomia bisetosa. Reference toxicant tests using boric acid were conducted to provide confidence in the interpretation of the results and verified the sensitivity of F. candida and P. minuta to contaminants.
Results
Despite exceeding the Canada-wide generic guidelines for PHC fraction 3 (F3), weathered contaminated soils at concentrations between 1140 and 5880 mg/kg had no significant negative impacts on the reproduction or mortality rates of F. candida or P. minuta. Furthermore, all four soil invertebrates preferred to inhabit the contaminated soils during the 48 h avoidances tests.
Conclusion
Natural weathering processes to PHC-impacted soils at a Canadian Subarctic site have led to a decrease in toxicity on four native soil invertebrates.
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Data availability
Data recorded during this study are available from the corresponding author upon reasonable request.
References
Al-Mebayedh H, Niu A, Lin C (2022) Petroleum hydrocarbon composition of oily sludge and contaminated soils in a decommissioned oilfield waste pit under desert conditions. Appl Sci 12. https://doi.org/10.3390/app12031355
Angell RA, Kullman S, Shrive E et al (2012) Direct soil contact values for ecological receptors exposed to weathered petroleum hydrocarbon (PHC) fraction 2. Environ Toxicol Chem 31:2536–2544. https://doi.org/10.1002/etc.1974
ASTM (2017) Standard practice for classification of soils for engineering purposes, Unified Soil Classification System (D2487–17). West Conshohocken, PA
Bourdel G, Roy-Bolduc A, St-Arnaud M, Hijri M (2016) Concentration of petroleum-hydrocarbon contamination shapes fungal endophytic community structure in plant roots. Front Microbiol 7:1–11. https://doi.org/10.3389/fmicb.2016.00685
Brown KE, Wasley J, King CK (2023) Assessing risks from fuel contamination in Antarctica: Dynamics of diesel ageing in soil and toxicity to an endemic nematode. Ecotoxicol Environ Saf 249:114345. https://doi.org/10.1016/j.ecoenv.2022.114345
Canada Energy Regulator (2021) Canadian Crude Oil Exports: A 30 Year Review. Canada
CCME (2001) Reference method for the Canada- wide standard for petroleum hydrocarbons in soil - Tier 1 method. Canadian Council of Ministers of the Environment, Winnipeg, Manitoba. Canada Soils
CCME (2008a) Canada-Wide Standard for Petroleum Hydrocarbons (PHC) in Soil: Scientific Rationale. Canadian Council of Ministers of the Environment, Winnipeg, Manitoba. Canada
CCME (2008b) Canada-Wide Standards for Petroleum Hydrocarbons (PHC) in Soil. Canadian Council of Ministers of the Environment, Winnipeg, Manitoba. Canada
Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: An overview. Biotechnol Res Int 2011:1–13. https://doi.org/10.4061/2011/941810
Diogo JB, Natal-Da-Luz T, Sousa JP et al (2007) Tolerance of genetically characterized Folsomia candida Strains to phenmedipham exposure A comparison between reproduction and avoidance tests *. J Soils Sediments 7:388–392
DiToro DM, McGrath JA, Stubblefield WA (2007) Predicting the toxicity of neat and weathered crude oil: Toxic potential and the toxicity of saturated mixtures. Environ Toxicol Chem 26:24–36. https://doi.org/10.1897/06174R.1
Environment and Climate Change Canada (2020) Biological test method: test for measuring reproduction of oribatid mites exposed to contaminants in soil. Environment and Climate Change Canada, Ottawa, Ontario
Environment Canada (2014) Biological Test Method : Test for Measuring Survival and Reproduction of Springtails Exposed to Contaminants in Soil. Canadian Council of Ministers of the Environment, Winnipeg, Manitoba. Canada
Fajana HO, Gainer A, Jegede OO et al (2019) Oppia nitens C.L. Koch, 1836 (Acari: Oribatida): Current Status of Its Bionomics and Relevance as a Model Invertebrate in Soil Ecotoxicology. Environ Toxicol Chem 38:2593–2613. https://doi.org/10.1002/etc.4574
Gainer A, Cousins M, Hogan N, Siciliano SD (2018) Petroleum hydrocarbon mixture toxicity and a trait-based approach to soil invertebrate species for site-specific risk assessments. Environ Toxicol Chem 37:2222–2234. https://doi.org/10.1002/etc.4164
Gainer A, Hogan N, Siciliano SD (2019) Soil invertebrate avoidance behavior identifies petroleum hydrocarbon contaminated soils toxic to sensitive plant species. J Hazard Mater 361:338–347. https://doi.org/10.1016/j.jhazmat.2018.08.086
Gainer A, Owojori OJ, Maboeta M (2022) Use of soil invertebrate avoidance tests as an emerging tool in soil ecotoxicology. Rev Environ Contam Toxicol 260:1–18. https://doi.org/10.1007/s44169-021-00004-4
Gao H, Wu M, Liu H et al (2022) Effect of petroleum hydrocarbon pollution levels on the soil microecosystem and ecological function. Environ Pollut 293:118511. https://doi.org/10.1016/j.envpol.2021.118511
Ge J, Xiao Y, Chai Y et al (2018) Sub-lethal effects of six neonicotinoids on avoidance behavior and reproduction of earthworms (Eisenia fetida). Ecotoxicol Environ Saf 162:423–429. https://doi.org/10.1016/j.ecoenv.2018.06.064
Harmsen J, Rietra RPJJ (2018) 25 years monitoring of PAHs and petroleum hydrocarbons biodegradation in soil. Chemosphere 207:229–238. https://doi.org/10.1016/j.chemosphere.2018.05.043
Hewelke E, Szatyłowicz J, Hewelke P et al (2018) The impact of diesel oil pollution on the hydrophobicity and co2 efflux of forest soils. Water Air Soil Pollut 229:. https://doi.org/10.1007/s11270-018-3720-6
Jiang Y, Brassington KJ, Prpich G et al (2016) Insights into the biodegradation of weathered hydrocarbons in contaminated soils by bioaugmentation and nutrient stimulation. Chemosphere 161:300–307. https://doi.org/10.1016/j.chemosphere.2016.07.032
Kenneth N (2010) Handbook of hydrocarbon and lipid microbiology. Handb Hydrocarb Lipid Microbiol. https://doi.org/10.1007/978-3-540-77587-4
Larsen T, Ventura M, Damgaard C et al (2009) Nutrient allocations and metabolism in two collembolans with contrasting reproduction and growth strategies. Funct Ecol 23:745–755. https://doi.org/10.1111/j.1365-2435.2009.01564.x
Li Y, Wang H, Cai Z et al (2021) Molecular Analyses of Petroleum Hydrocarbon Change and Transformation during Petroleum Weathering by Multiple Techniques. ACS Omega. https://doi.org/10.1021/acsomega.1c02846
McGrath JA, Di Toro DM (2009) Validation of the target lipid model for toxicity assessment of residual petroleum constituents: Monocyclic and polycyclic aromatic hydrocarbons. Environ Toxicol Chem 28:1130–1148. https://doi.org/10.1897/08-271.1
Niemeyer JC, Carniel LSC, de Santo FB et al (2018) Boric acid as reference substance for ecotoxicity tests in tropical artificial soil. Ecotoxicology 27:395–401. https://doi.org/10.1007/s10646-018-1915-7
Pang A, Rutter A, Bordenave S et al (2022) Assessment of the toxicity of weathered petroleum hydrocarbon impacted soils to native plants from a site in the Canadian Subarctic. Ecotoxicology. https://doi.org/10.1007/s10646-022-02585-9
Princz J, Becker L, Scheffczyk A et al (2017) Ecotoxicity of boric acid in standard laboratory tests with plants and soil organisms. Ecotoxicology 26:471–481. https://doi.org/10.1007/s10646-017-1789-0
Princz JI, Behan-Pelletier VM, Scroggins RP, Siciliano SD (2010) Oribatid mites in soil toxicity testing - The use of Oppia nitens (C.L. KOCH) as a new test species. Environ Toxicol Chem 29:971–979. https://doi.org/10.1002/etc.98
Princz JI, Moody M, Fraser C et al (2012) Evaluation of a new battery of toxicity tests for boreal forest soils: Assessment of the impact of hydrocarbons and salts. Environ Toxicol Chem 31:766–777. https://doi.org/10.1002/etc.1744
Ramadass K, Megharaj M, Venkateswarlu K, Naidu R (2018) Bioavailability of weathered hydrocarbons in engine oil-contaminated soil: Impact of bioaugmentation mediated by Pseudomonas spp. on bioremediation. Sci Total Environ 636:968–974. https://doi.org/10.1016/j.scitotenv.2018.04.379
Redman AD, Parkerton TF, McGrath JA, Di Toro DM (2012) PETROTOX: An aquatic toxicity model for petroleum substances. Environ Toxicol Chem 31:2498–2506. https://doi.org/10.1002/etc.1982
Saeedi M, Li LY, Grace JR (2020) Effect of co-existing heavy metals and natural organic matter on sorption/desorption of polycyclic aromatic hydrocarbons in soil: A review. Pollution 6:1–24. https://doi.org/10.22059/POLL.2019.284335.638
Skrypnik L, Maslennikov P, Novikova A, Kozhikin M (2021) Effect of crude oil on growth, oxidative stress and response of antioxidative system of two rye (Secale cereale l.) varieties. Plants 10:1–22. https://doi.org/10.3390/plants10010157
Watzinger A, Hager M, Reichenauer T et al (2021) Unravelling the process of petroleum hydrocarbon biodegradation in different filter materials of constructed wetlands by stable isotope fractionation and labelling studies. Biodegradation 32:343–359. https://doi.org/10.1007/s10532-021-09942-1
Acknowledgements
This work was funded by the Natural Sciences and Engineering Research Council of Canada Collaborative Research and Development Grant (grant # 514935-17) and Imperial Oil Limited. We thank Rick Scroggins, Juliska Princz and their teams at the Biological Assessment and Standardization Section of Environment and Climate Change Canada for the careful culturing of invertebrates from the study site soils which led to the development of the original culture of Folsomia bisetosa. We thank Jeff Battigelli (then, Stantec Consulting Ltd.,) for invertebrate enumeration in the study site soils early in the project. We thank the Advisian staff that supported this project over the years, specifically Ann Glatiotis who initiated the original program.
Funding
This study was funded by Imperial Oil Limited and the Natural Sciences and Engineering Research Council of Canada Collaborative Research and Development Grant (grant # 514935–17).
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Conceptualization: Adrian Pang, Amy Gainer, Elizabeth Haack, Allison Rutter and Barbara Zeeb; Methodology: Adrian Pang; Data curation: Adrian Pang; Formal analysis: Adrian Pang; Investigation: Adrian Pang; Validation; Adrian Pang; Visualization: Adrian Pang; Writing-original draft: Adrian Pang; Writing- review and editing; Amy Gainer, Elizabeth Haack, Allison Rutter and Barbara Zeeb; Funding acquisition: Allison Rutter and Barbara Zeeb; Project administration: Allison Rutter and Barbara Zeeb; Supervision: Allison Rutter and Barbara Zeeb.
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Pang, A., Rutter, A., Gainer, A. et al. Assessment of heavily weathered petroleum hydrocarbon-impacted soils to native soil invertebrates from a Canadian subarctic site. J Soils Sediments 23, 2096–2105 (2023). https://doi.org/10.1007/s11368-023-03466-2
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DOI: https://doi.org/10.1007/s11368-023-03466-2