A Critical Review of Amphibian Per- and Polyfluoroalkyl Substance Ecotoxicity Research Studies: Identification of Screening Levels in Water and Other Useful Resources for Site-Specific Ecological Risk Assessments.
Amphibians
Per- and polyfluoroalkyl substance (PFAS)
Risk assessment
Journal
Environmental toxicology and chemistry
ISSN: 1552-8618
Titre abrégé: Environ Toxicol Chem
Pays: United States
ID NLM: 8308958
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
10
04
2023
received:
28
02
2023
accepted:
10
06
2023
medline:
28
9
2023
pubmed:
14
6
2023
entrez:
14
6
2023
Statut:
ppublish
Résumé
With the goal of aiding risk assessors conducting site-specific risk assessments at per- and polyfluoroalkyl substance (PFAS)-contaminated sites, this critical review synthesizes information on the ecotoxicity of PFAS to amphibians in 10 amphibian species and 16 peer-reviewed publications. The studies in this review consisted of spiked-PFAS chronic toxicity experiments with perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorohexane sulfonate (PFHxS), and 6:2 fluorotelomer sulfonate (6:2 FTS) that evaluated apical endpoints typical of ecological risk-based decision making (survival, growth, and development). Body mass was the most sensitive endpoint, showing clear and biologically meaningful population level adverse effect sizes (≥20% adverse effects). From these results, we recommend chronic no observed effect concentration (NOEC) screening levels of 590 µg/L for PFOS and 130 µg/L for PFOA. At or above recommended chronic lowest observed effect concentration screening levels of 1100 µg/L PFOS and 1400 µg/L PFOA, there is an increased chance of adverse biologically relevant chronic effects. Biologically relevant adverse effects were not observed for PFHxS and 6:2 FTS, so unbounded NOECs of 1300 µg/L PFHxS and 1800 µg/L 6:2 FTS are recommended. Screening levels are also provided for the concentration of PFAS in an amphibian diet, amphibian tissue, and moss substrate. In addition, we recommend bioconcentration factors that can be useful to predict concentrations of PFAS in amphibians using concentrations in water; these values are useful for food web modeling to understand risks to vertebrate wildlife that prey on amphibians. Overall, the present study provides a guide to the wealth of ecotoxicological research on PFAS conducted by our research group and highlights the need for additional work that would improve the understanding of chemical risks to amphibians. Environ Toxicol Chem 2023;42:2078-2090. © 2023 SETAC.
Substances chimiques
fluorotelomer sulfonic acids
0
Water
059QF0KO0R
perfluorooctane sulfonic acid
9H2MAI21CL
Alkanesulfonic Acids
0
Fluorocarbons
0
perfluorooctanoic acid
947VD76D3L
Alkanesulfonates
0
perflexane
FX3WJ41CMX
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2078-2090Informations de copyright
© 2023 SETAC.
Références
Abercrombie, S. A., de Perre, C., Choi, Y. J., Tornabene, B. J., Sepúlveda, M. S., Lee, L. S., & Hoverman, J. T. (2019). Larval amphibians rapidly bioaccumulate poly- and perfluoroalkyl substances. Ecotoxicology and Environmental Safety, 178, 137-145. https://doi.org/10.1016/j.ecoenv.2019.04.022
Abercrombie, S. A., de Perre, C., Iacchetta, M., Flynn, R. W., Sepúlveda, M. S., Lee, L. S., & Hoverman, J. T. (2021). Sublethal effects of dermal exposure to poly- and perfluoroalkyl substances on postmetamorphic amphibians. Environmental Toxicology and Chemistry, 40, 717-726. https://doi.org/10.1002/etc.4711
Ankley, G. T., Kuehl, D. W., Kahl, M. D., Jensen, K. M., Butterworth, B. C., & Nichols, J. W. (2004). Partial life-cycle toxicity and bioconcentration modeling of perfluorooctane sulfonate in the northern leopard frog (Rana pipiens). Environmental Toxicology and Chemistry, 23, 2745. https://doi.org/10.1897/03-667
Australian Government Department of Agriculture and Water Resources. (2018). Technical rationale for changes to the method for deriving Australian and New Zealand water quality guideline values for toxicants.
Biek, R., Funk, W.C., Maxell, B. A, & Mills, L. S. (2002). What is missing in amphibian decline research: Insights from ecological sensitivity analysis. Conservation Biology,16, 728-734. https://doi.org/10.1046/j.1523-1739.2002.00433.x
Brown, S. R., Flynn, R. W., & Hoverman, J. T. (2021). Perfluoroalkyl substances increase susceptibility of northern leopard frog tadpoles to trematode infection. Environmental Toxicology and Chemistry, 40, 689-694. https://doi.org/10.1002/etc.4678
Canadian Council of Ministers of the Environment. (2007). A protocol for the derivation of water quality guidelines for the protection of aquatic life.
Conder, J., Arblaster, J., Larson, E., Brown, J., & Higgins, C. (2020). Guidance for assessing the ecological risks of PFASs to threatened and endangered species at aqueous film forming foam-impacted sites (SERDP Contract Report ER18-1614). https://www.serdp-estcp.org/Program-Areas/Environmental-Restoration/ER18-1614
Conder, J., Zodrow, J., Arblaster, J., Kelly, B., Gobas, F., Suski, J., Osborn, E., Frenchmeyer, M., Divine, C., & Leeson, A. (2021). Strategic resources for assessing PFAS ecological risks at AFFF sites. Integrated Environmental Assessment and Management, 17, 746-752. https://doi.org/10.1002/ieam.4405
Environmental and Climate Change Canada. (2018). Canadian Environmental Protection Act, 1999 Federal Environmental Quality Guidelines Bisphenol A Environment and Climate Change Canada.
European Chemicals Agency. (2008). Guidance on information requirements and chemical safety assessment, Chapter R.10: Characterisation of dose [concentration]-response for environment.
Environment Protection Authority of Victoria, Australia. (2016). Incoming water standards for aquatic ecosystem protection: PFOS and PFOA.
Flynn, R. W., Chislock, M. F., Gannon, M. E., Bauer, S. J., Tornabene, B. J., Hoverman, J. T., & Sepúlveda, M. S. (2019). Acute and chronic effects of perfluoroalkyl substance mixtures on larval American bullfrogs (Rana catesbeiana). Chemosphere, 236, 124350. https://doi.org/10.1016/j.chemosphere.2019.124350
Flynn, R. W., Hoover, G., Iacchetta, M., Guffey, S., de Perre, C., Huerta, B., Li, W., Hoverman, J. T., Lee, L., & Sepúlveda, M. S. (2022). Comparative toxicity of aquatic per- and polyfluoroalkyl substance exposure in three species of amphibians. Environmental Toxicology and Chemistry, 41, 1407-1415. https://doi.org/10.1002/etc.5319
Flynn, R. W., Iacchetta, M., Perre, C., Lee, L., Sepúlveda, M. S., & Hoverman, J. T. (2021). Chronic per-/polyfluoroalkyl substance exposure under environmentally relevant conditions delays development in northern leopard frog (Rana pipiens) larvae. Environmental Toxicology and Chemistry, 40, 711-716. https://doi.org/10.1002/etc.4690
Flynn, R. W., Hoskins, T. D., Iacchetta, M., de Perre, C., Lee, L. S., Hoverman, J. T., & Sepulveda, M. S. (2021). Dietary exposure and accumulation of per- and polyfluoroalkyl substances alters growth and reduces body condition of post-metamorphic salamanders. Science of the Total Environment, 765, 142730. https://doi.org/10.1016/j.scitotenv.2020.142730
Foguth, R. M., Hoskins, T. D., Clark, G. C., Nelson, M., Flynn, R. W., de Perre, C., Hoverman, J. T., Lee, L. S., Sepúlveda, M. S., & Cannon, J. R. (2020). Single and mixture per- and polyfluoroalkyl substances accumulate in developing northern leopard frog brains and produce complex neurotransmission alterations. Neurotoxicology and Teratology, 81, 106907. https://doi.org/10.1016/j.ntt.2020.106907
Fort, D. J., Mathis, M. B., Guiney, P. D., & Weeks, J. A. (2019). Evaluation of the developmental toxicity of perfluorooctane sulfonate in the Anuran, Silurana tropicalis. Journal of Applied Toxicology, 39, 365-374. https://doi.org/10.1002/jat.3727
Goldstein, J. A., Hoff, K. v. S., & Hillyard, S. D. (2017). The effect of temperature on development and behaviour of relict leopard frog tadpoles. Conservation Physiology, 5, 1-8. https://doi.org/10.1093/conphys/cow075
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 5, 183-190.
Hanson, M. L., Solomon, K. R., Van Der Kraak, G. J., & Brian, R. A. (2019). Effects of atrazine on fish, amphibians, and reptiles: Update of the analysis based on quantitative weight of evidence. Critical Reviews in Toxicology, 49, 670-709. https://doi.org/10.1080/10408444.2019.1701985
Hoover, G., Kar, S., Guffey, S., Leszczynski, J., & Sepúlveda, M. S. (2019). In vitro and in silico modeling of perfluoroalkyl substances mixture toxicity in an amphibian fibroblast cell line. Chemosphere, 233, 25-33. https://doi.org/10.1016/j.chemosphere.2019.05.065
Hoover, G. M., Chislock, M. F., Tornabene, B. J., Guffey, S. C., Choi, Y. J., De Perre, C., Hoverman, J. T., Lee, L. S., & Sepúlveda, M. S. (2017). Uptake and depuration of four per/polyfluoroalkyl substances (PFAS) in northern leopard frog Rana pipiens tadpoles. Environmental Science and Technology Letters, 4, 399-403. https://doi.org/10.1021/acs.estlett.7b00339
Hoskins, T. D., Allmon, E. B., Flynn, R. W., Lee, L. S., Choi, Y., Hoverman, J. T., & Sepúlveda, M. S. (2022). An environmentally relevant mixture of perfluorooctane sulfonic acid and perfluorohexane sulfonic acid does not conform to additivity in northern leopard frogs exposed through metamorphosis. Environmental Toxicology and Chemistry, 41, 3007-3016. https://doi.org/10.1002/etc.5486
Johnson, M. S., Aubee, C., Salice, C. J., Leigh, K. B., Liu, E., Pott, U., & Pillard, D. (2017). A review of ecological risk assessment methods for amphibians: Comparative assessment of testing methodologies and available data. Integrated Environmental Assessment and Management, 13, 601-613. https://doi.org/10.1002/ieam.1881
Larson, E. S., Conder, J. M., & Arblaster, J. A. (2018). Modeling avian exposures to perfluoroalkyl substances in aquatic habitats impacted by historical aqueous film forming foam releases. Chemosphere, 201, 335-341. https://doi.org/10.1016/j.chemosphere.2018.03.004
Lech, M. E., Choi, Y. J., Lee, L. S., Sepúlveda, M. S., & Hoverman, J. T. (2022). Effects of per- and polyfluoroalkyl substance mixtures on the susceptibility of larval American bullfrogs to parasites. Environmental Science & Technology, 56, 15953-15959. https://doi.org/10.1021/acs.est.2c04574
Organization for Economic Co-operation and Development. (2009). OECD Guideline for the testing of chemicals 231: Amphibian Metamorphosis Assay. OECD Guidelines for the Testing of Chemicals.
Peig, J., & Green, A. J. (2009). New perspectives for estimating body condition from mass/length data: The scaled mass index as an alternative method. Oikos, 118, 1883-1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x
National Institute for Public Health and the Environment. (2010). Environmental risk limits for PFOS. RIVM, The Netherlands.
Rohr, J. R., & McCoy, K. A. (2010). A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives, 118, 20-32. https://doi.org/10.1289/ehp.0901164
Sharpe, R. L., Benskin, J. P., Laarman, A. H., MacLeod, S. L., Martin, J. W., Wong, C. S., & Goss, G. G. (2010). Perfluorooctane sulfonate toxicity, isomer-specific accumulation, and maternal transfer in zebrafish (Danio rerio) and rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry, 29, 1957-1966. https://doi.org/10.1002/etc.257
Suter, G. (2018). Specifying the dimensions of aquatic life benchmark values in clear, complete, and justified problem formulations. Integrated Environmental Assessment and Management, 14, 631-638. https://doi.org/10.1002/ieam.4059
Suter, G. W. (2000). Ecological risk assessment and ecological epidemiology for contaminated sites. Human and Ecological Risk Assessment: An International Journal, 12, 31-38. https://doi.org/10.1080/10807030500428553
Tornabene, B. J., Chislock, M. F., Gannon, M. E., Sepúlveda, M. S., & Hoverman, J. T. (2021). Relative acute toxicity of three per- and polyfluoroalkyl substances on nine species of larval amphibians. Integrated Environmental Assessment and Management, 17, 684-690. https://doi.org/10.1002/ieam.4391
US Environmental Protection Agency. (2016). Aquatic life ambient water quality criteria cadmium. USEPA Publishing. 721.
US Environmental Protection Agency. (2000). Method guidance and recommendations for whole effluent toxicity (wet) testing (40 CFR Part 136) (EPA821-B-00-004).
US Environmental Protection Agency. (2022a). Draft aquatic life ambient water quality criteria for perfluorooctanoic acid (PFOA).
US Environmental Protection Agency. (2022b). Draft aquatic life ambient water quality criteria for perfluorooctane sulfonate (PFOS).
Vonesh, J. R., & De la Cruz, O. (2002). Complex life cycles and density dependence: Assessing the contribution of egg mortality to amphibian declines. Oecologia, 133, 325-333. https://doi.org/10.1007/s00442-002-1039-9
Wang, M., Chen, J., Lin, K., Chen, Y., Hu, W., Tanguay, R. L., Huang, C., & Dong, Q. (2011). Chronic zebrafish PFOS exposure alters sex ratio and maternal related effects in F1 offspring. Environmental Toxicology and Chemistry, 30, 2073-2080. https://doi.org/10.1002/etc.594
Zodrow, J. M., Frenchmeyer, M., Dally, K., Osborn, E., Anderson, P., & Divine, C. (2021). Development of per and polyfluoroalkyl substances ecological risk-based screening levels. Environmental Toxicology and Chemistry, 40, 921-936. https://doi.org/10.1002/etc.4975