Effects of per- and polyfluoroalkyl substances (PFASs) on hatching of Folsomia candida (Collembola) on soil

Abstract

● Egg hatching of the soil collembolan Folsomia candida and the effects of per- and polyfluoroalkyl substances were investigated.

● New and effective laboratory methods for egg hatching studies with soil collembolans were established.

Per- and polyfluoroalkyl compounds (PFASs) have been used industrially worldwide and are persistent organic pollutants in many soils. Twenty eggs laid by synchronized adults of the collembolan Folsomia candida were added to each Petri dish containing compressed soil substrate mixed with perfluorooctanoic acid (PFOA), heptafluorobutyric acid (PFBA), or 6:2 chlorinated polyfluoroalkyl ether sulfonic acid (F-53B), and after 25 d of exposure the number hatched declined on average by 6.9%−49.7%, 10.3%−24.1%, and 3.4%−18.6%, respectively. PFASs delayed the peak of hatching by one day, and at different concentrations reduced the number of eggs hatched during the peak by 16.7%−30% and 23.3%−43.2% in PFOA and PFBA treatments, respectively. In the presence of F-53B the number of eggs hatched declined by 73.3% but the number of individuals increased by 29.3% at higher concentrations. The characteristics of egg hatching were stable and sensitive to PFASs, and may be suitable for use as indicators in the screening of contaminated soils for environmental risk assessment.

Graphical abstract

Keywords

PFOA / PFBA / F-53B / soil animals / soil mesofauna / springtails / soil pollution assessment / life history indicator

References

[1] Bart, S., Laurent, C., Péry, A.R.R., Mougin, C., Pelosi, C., 2017. Differences in sensitivity between earthworms and enchytraeids exposed to two commercial fungicides. Ecotoxicology and Environmental Safety140, 177–184.

[2] Biegel, L.B., Hurtt, M.E., Frame, S.R., O'Connor, J. C., Cook, J.C., 2001. Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicological Sciences60, 44–55.

[3] Briels, N., Ciesielski, T.M., Herzke, D., Jaspers, V.L.B., 2018. Developmental toxicity of perfluorooctanesulfonate (PFOS) and its chlorinated polyfluoroalkyl ether sulfonate alternative F-53B in the domestic chicken. Environmental Science & Technology52, 12859–12867.

[4] Cardoso, D.N., Ferreira, N.G.C., Tourinho, P.S., Santos, C., Soares, A.M.V.M., Loureiro, S., 2019. Mercury accumulation from food decreases collembolans' growth. Science of the Total Environment668, 25–31.

[5] Chen, Y.M., Guo, L.H., 2009. Fluorescence study on site-specific binding of perfluoroalkyl acids to human serum albumin. Archives of Toxicology83, 255–261.

[6] Das, P., Megharaj, M., Naidu, R., 2015. Perfluorooctane sulfonate release pattern from soils of fire training areas in Australia and its bioaccumulation potential in the earthworm Eisenia fetida. Environmental Science and Pollution Research22, 8902–8910.

[7] DeWitt, J.C., Meyer, E.B., Henshel, D.S., 2005. Environmental toxicity studies using chickens as surrogates for wildlife: effects of injection day. Archives of Environmental Contamination and Toxicology48, 270–277.

[8] Domingo, J.L., Ericson-Jogsten, I., Perelló, G., Nadal, M., Van Bavel, B., Kärrman, A., 2012. Human exposure to perfluorinated compounds in Catalonia, Spain: contribution of drinking water and fish and shellfish. Journal of Agricultural and Food Chemistry60, 4408–4415.

[9] Eriksson, U., Kärrman, A., Rotander, A., Mikkelsen, B., Dam, M., 2013. Perfluoroalkyl substances (PFASs) in food and water from Faroe Islands. Environmental Science and Pollution Research20, 7940–7948.

[10] González-Naranjo, V., Boltes, K., 2014. Toxicity of ibuprofen and perfluorooctanoic acid for risk assessment of mixtures in aquatic and terrestrial environments. International Journal of Environmental Science and Technology11, 1743–1750.

[11] Guimaräes, B., Römbke, J., Amorim, M.J.B., 2019. Novel egg life-stage test with Folsomia candida − A case study with Cadmium (Cd). Science of the Total Environment647, 121–126.

[12] Heo, J.J., Lee, J.W., Kim, S.K., Oh, J.E., 2014. Foodstuff analyses show that seafood and water are major perfluoroalkyl acids (PFAAs) sources to humans in Korea. Journal of Hazardous Materials279, 402–409.

[13] Higgins, C.P., McLeod, P.B., MacManus-Spencer, L.A., Luthy, R.G., 2007. Bioaccumulation of perfluorochemicals in sediments by the aquatic oligochaete Lumbriculus variegatus. Environmental Science & Technology41, 4600–4606.

[14] ISO 11267: 2023. Soil Quality—Inhibition of Reproduction of Collembola (Folsomia candida) by Soil Contaminants. International Organization for Standardization, 2023

[15] Jian, J.M., Guo, Y., Zeng, L.X., Liu, L.Y., Lu, X.W., Wang, F., Zeng, E.Y., 2017. Global distribution of perfluorochemicals (PFCs) in potential human exposure source-A review. Environment International108, 51–62.

[16] Kunacheva, C., Tanaka, S., Fujii, S., Boontanon, S.K., Musirat, C., Wongwattana, T., Shivakoti, B.R., 2011. Mass flows of perfluorinated compounds (PFCs) in central wastewater treatment plants of industrial zones in Thailand. Chemosphere83, 737–744.

[17] Kwak, J.I., Lee, T.Y., Seo, H., Kim, D., Kim, D., Cui, R.X., An, Y.J., 2020. Ecological risk assessment for perfluorooctanoic acid in soil using a species sensitivity approach. Journal of Hazardous Materials382, 121150.

[18] Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., Seed, J., 2007. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicological Sciences99, 366–394.

[19] Lee, Y.S., Son, J., Wee, J., Kim, Y., Kim, D.Y., Kwon, J.H., Cho, K., 2019. Contributions of egg production and egg hatching to the total toxicity of teflubenzuron in Yuukianura szeptyckii (Collembola) in soil toxicity test. Environmental Science and Pollution Research26, 26184–26192.

[20] Li, C.H., Ren, X.M., Ruan, T., Cao, L.Y., Xin, Y., Guo, L.H., Jiang, G.B., 2018. Chlorinated polyfluorinated ether sulfonates exhibit higher activity toward peroxisome proliferator-activated receptors signaling pathways than perfluorooctanesulfonate. Environmental Science & Technology52, 3232–3239.

[21] Lim, X., 2023. Could the world go PFAS-free? Proposal to ban 'forever chemicals' fuels debate. Nature620, 24–27.

[22] Liu, S.Y., Yang, R.J., Yin, N.Y., Faiola, F., 2020. The short-chain perfluorinated compounds PFBS, PFHxS, PFBA and PFHxA, disrupt human mesenchymal stem cell self-renewal and adipogenic differentiation. Journal of Environmental Sciences88, 187–199.

[23] Llorca, M., Farré, M., Picó, Y., Müller, J., Knepper, T.P., Barceló, D., 2012. Analysis of perfluoroalkyl substances in waters from Germany and Spain. Science of the Total Environment431, 139–150.

[24] Marczylo, E.L., Jacobs, M.N., Gant, T.W., 2016. Environmentally induced epigenetic toxicity: Potential public health concerns. Critical Reviews in Toxicology46, 676–700.

[25] Mayilswami, S., Krishnan, K., Megharaj, M., Naidu, R., 2016. Gene expression profile changes in Eisenia fetida chronically exposed to PFOA. Ecotoxicology25, 759–769.

[26] Mendes, L.A., Maria, V.L., Scott-Fordsmand, J.J., Amorim, M.J.B., 2018. Multigenerational exposure of Folsomia candida to silver: Effect of different contamination scenarios (continuous versus pulsed and recovery). Science of the Total Environment, 631–632, 631–632

[27] Mudumbi, J.B.N., Ntwampe, S.K.O., Matsha, T., Mekuto, L., Itoba-Tombo, E.F., 2017. Recent developments in polyfluoroalkyl compounds research: a focus on human/environmental health impact, suggested substitutes and removal strategies. Environmental Monitoring and Assessment189, 402.

[28] OECD., 2004. Test No. 232: Collembolan reproduction test in soil. OECD Guidelines for the Testing of Chemicals, Volume 1: 1-19

[29] Olsen, G.W., Butenhoff, J.L., Zobel, L.R., 2009. Perfluoroalkyl chemicals and human fetal development: an epidemiologic review with clinical and toxicological perspectives. Reproductive Toxicology27, 212–230.

[30] Pan, Y.T., Zhang, H.X., Cui, Q.Q., Sheng, N., Yeung, L.W.Y., Sun, Y., Guo, Y., Dai, J.Y., 2018. Worldwide distribution of novel perfluoroether carboxylic and sulfonic acids in surface water. Environmental Science & Technology52, 7621–7629.

[31] Princz, J., Jatar, M., Lemieux, H., Scroggins, R., 2018. Perfluorooctane sulfonate in surface soils: effects on reproduction in the collembolan, Folsomia candida, and the oribatid mite, Oppia nitens. Chemosphere208, 757–763.

[32] Rich, C.D., Blaine, A.C., Hundal, L., Higgins, C.P., 2015. Bioaccumulation of perfluoroalkyl acids by earthworms (Eisenia fetida) exposed to contaminated soils. Environmental Science & Technology49, 881–888.

[33] Roos, A., Berger, U., Järnberg, U., Van Dijk, J., Bignert, A., 2013. Increasing concentrations of perfluoroalkyl acids in scandinavian otters (Lutra lutra) between 1972 and 2011: a new threat to the otter population?. Environmental Science & Technology47, 11757–11765.

[34] Route, W.T., Russell, R.E., Lindstrom, A.B., Strynar, M.J., Key, R.L., 2014. Spatial and temporal patterns in concentrations of perfluorinated compounds in bald eagle nestlings in the upper midwestern United States. Environmental Science & Technology48, 6653–6660.

[35] Shi, G.H., Cui, Q.Q., Pan, Y.T., Sheng, N., Sun, S.J., Guo, Y., Dai, J.Y., 2017. 6:2 Chlorinated polyfluorinated ether sulfonate, a PFOS alternative, induces embryotoxicity and disrupts cardiac development in zebrafish embryos. Aquatic Toxicology185, 67–75.

[36] Shi, G.H., Guo, H., Sheng, N., Cui, Q.Q., Pan, Y.T., Wang, J.X., Guo, Y., Dai, J.Y., 2018. Two-generational reproductive toxicity assessment of 6:2 chlorinated polyfluorinated ether sulfonate (F-53B, a novel alternative to perfluorooctane sulfonate) in zebrafish. Environmental Pollution243, 1517–1527.

[37] Shi, Y.L., Vestergren, R., Xu, L., Zhou, Z., Li, C.X., Liang, Y., Cai, Y.Q., 2016. Human exposure and elimination kinetics of chlorinated polyfluoroalkyl ether sulfonic acids (Cl-PFESAs). Environmental Science & Technology50, 2396–2404.

[38] Son, J., Ryoo, M.I., Jung, J., Cho, K., 2007. Effects of cadmium, mercury and lead on the survival and instantaneous rate of increase of Paronychiurus kimi (Lee) (Collembola). Applied Soil Ecology35, 404–411.

[39] Sonthithai, P., Suriyo, T., Thiantanawat, A., Watcharasit, P., Ruchirawat, M., Satayavivad, J., 2016. Perfluorinated chemicals, PFOS and PFOA, enhance the estrogenic effects of 17β-estradiol in T47D human breast cancer cells. Journal of Applied Toxicology36, 790–801.

[40] Sun, S.J., Wang, J.S., Lu, Y., Dai, J.Y., 2018. Corticosteroid-binding globulin, induced in testicular Leydig cells by perfluorooctanoic acid, promotes steroid hormone synthesis. Archives of Toxicology92, 2013–2025.

[41] Szabó, B., Seres, A., Bakonyi, G., 2020. Distinct changes in the life-history strategies of Folsomia candida Willem (Collembola: Isotomidae) due to multi- and transgenerational treatments with an insecticide. Applied Soil Ecology152, 103563.

[42] Wang, S.W., Huang, J., Yang, Y., Hui, Y.M., Ge, Y.X., Larssen, T., Yu, G., Deng, S.B., Wang, B., Harman, C., 2013. First report of a chinese PFOS alternative overlooked for 30 years: its toxicity, persistence, and presence in the environment. Environmental Science & Technology47, 10163–10170.

[43] Wang, Z.Y., DeWitt, J.C., Higgins, C.P., Cousins, I.T., 2017. A never-ending story of per- and polyfluoroalkyl substances (PFASs)? Environmental Science & Technology 51, 2508–2518

[44] Wen, B., Pan, Y., Shi, X.L., Zhang, H.N., Hu, X.Y., Huang, H.L., Lv, J.T., Zhang, S.Z., 2018. Behavior of N-ethyl perfluorooctane sulfonamido acetic acid (N-EtFOSAA) in biosolids amended soil-plant microcosms of seven plant species: Accumulation and degradation. Science of the Total Environment642, 366–373.

[45] Xiao, F., 2017. Emerging poly- and perfluoroalkyl substances in the aquatic environment: a review of current literature. Water Research124, 482–495.

[46] Yang, L., He, L.Y., Xue, J.M., Ma, Y.F., Xie, Z.Y., Wu, L., Huang, M., Zhang, Z.L., 2020. Persulfate-based degradation of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) in aqueous solution: review on influences, mechanisms and prospective. Journal of Hazardous Materials393, 122405.

[47] Zareitalabad, P., Siemens, J., Hamer, M., Amelung, W., 2013. Perfluorooctanoic acid (PFOA) and perfluorooctanesulfonic acid (PFOS) in surface waters, sediments, soils and wastewater - A review on concentrations and distribution coefficients. Chemosphere91, 725–732.

[48] Zhang, Q., Zhu, D., Ding, J., Zhou, S.Y.D., Sun, L.W., Qian, H.F., 2019. Species-specific response of the soil collembolan gut microbiome and resistome to soil oxytetracycline pollution. Science of the Total Environment668, 1183–1190.

[49] Zhao, S.Y., Wang, B.H., Zhu, L.Y., Liang, T.K., Chen, M., Yang, L.P., Lv, J.P., Liu, L.F., 2018. Uptake, elimination and biotransformation of N-ethyl perfluorooctane sulfonamide (N-EtFOSA) by the earthworms (Eisenia fetida) after in vivo and in vitro exposure. Environmental Pollution241, 19–25.

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