Variation of Tolerance to Isothiazolinones Among Daphnia pulex Clones.
Aquatic invertebrates
Emerging pollutants
Evolutionary ecotoxicology
Freshwater toxicology
Risk extrapolation
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:
04 2023
04 2023
Historique:
revised:
12
12
2022
received:
13
09
2022
accepted:
14
01
2023
medline:
30
3
2023
pubmed:
21
1
2023
entrez:
20
1
2023
Statut:
ppublish
Résumé
Isothiazolinones are a family of broad-spectrum biocides widely used in industry and consumer products. Chloro- and methyl-isothiazolinones (CMIT and MIT) are documented as strong irritants, yet they are still used in a wide variety of applications, including cosmetics, cleansers, hygienic products, and various industrial applications. The subsequent substantial release of these molecules from urban sources into freshwater environments, and their potential impacts on aquatic species, have nevertheless received little attention so far, with few studies reporting on the toxicity of either CMIT or MIT to nontarget organisms. The present study addresses this current knowledge gap by evaluating the acute toxicity to Daphnia pulex (Cladocera) of CMIT/MIT (3:1) and MIT, the two formulations most commonly used by manufacturers. In addition, genetic diversity is known to be a major component of variability in phenotypic responses, although it is largely overlooked in typical toxicity tests. Thus the potential range of responses inherent to genetic diversity is rarely considered. Therefore, to account for intraspecific variations in sensitivity, our design involved eight clonal lines of D. pulex stemming from distinct natural populations or commercial strains. Clones exhibited strong variation in their responses, with median lethal concentration (LC50) values ranging from 0.10 to 1.84 mg/L for the mixture CMIT/MIT, and from 0.68 to 2.84 mg/L for MIT alone. These intraspecific ranges of LC50 values challenge the use of single clones of daphnids in standard ecotoxicological tests and the predictions based on their results. The present study brings new evidence that assessing ecological risk of chemicals while ignoring genotype diversity is neither ecologically relevant, nor a representative evaluation of the diversity of potential adverse outcomes. Environ Toxicol Chem 2023;42:805-814. © 2023 SETAC.
Substances chimiques
Disinfectants
0
Water Pollutants, Chemical
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
805-814Subventions
Organisme : Agence Nationale de Sécurité Sanitaire de l'Alimentation, de l'Environnement et du Travail
ID : EST/2017/1/093
Informations de copyright
© 2023 SETAC.
Références
Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail. (2016). Méthylisothiazolinone dans les produits à usage courant et risques associés de sensibilisation cutanée et respiratoire. (p. 88) [Avis de l ' Anses. Rapport d'expertise collective.]. https://www.anses.fr/fr/system/files/CONSO2014SA0186Ra.pdf
Almeida, R. A., Lemmens, P., De Meester, L., & Brans, K. I. (2021). Differential local genetic adaptation to pesticide use in organic and conventional agriculture in an aquatic non-target species. Proceedings of the Royal Society B: Biological Sciences, 288(1963), 20211903. https://doi.org/10.1098/rspb.2021.1903
Amat, A. M., Arques, A., López-Pérez, M. F., Nacher, M., & Palacios, S. (2015). Effect of methylisothiazolinone on biological treatment: Efficiency of SBRs and bioindicative studies. Environmental Engineering Science, 32(6), 479-485. https://doi.org/10.1089/ees.2014.0283
Baranowska, I., & Wojciechowska, I. (2013). The determination of preservatives in cosmetics and environmental waters by HPLC. Polish Journal of Environmental Studies, 22(6), 1609-1625.
Barata, C., Markich, S. J., Baird, D. J., Taylor, G., & Soares, A. M. V. M. (2002). Genetic variability in sublethal tolerance to mixtures of cadmium and zinc in clones of Daphnia magna straus. Aquatic Toxicology, 60(1), 85-99. https://doi.org/10.1016/S0166-445X(01)00275-2
Baudrot, V., & Charles, S. (2021). morse: An R-package to analyse toxicity test data. Journal of Open Source Software, 6(68), 3200. https://doi.org/10.21105/joss.03200
Bester, K., Vollertsen, J., & Bollmann, U. E. (2014). Water driven leaching of biocides from paints and renders: Methods for the improvement of emission scenarios concerning biocides in buildings. Danish Environmental Protection Agency.
Bickham, J. W., Sandhu, S., Hebert, P. D. N., Chikhi, L., & Athwal, R. (2000). Effects of chemical contaminants on genetic diversity in natural populations: Implications for biomonitoring and ecotoxicology. Mutation Research/Reviews in Mutation Research, 463(1), 33-51. https://doi.org/10.1016/S1383-5742(00)00004-1
Bollmann, U. E., Fernández-Calviño, D., Brandt, K. K., Storgaard, M. S., Sanderson, H., & Bester, K. (2017). Biocide runoff from building facades: Degradation kinetics in soil. Environmental Science & Technology, 51(7), 3694-3702. https://doi.org/10.1021/acs.est.6b05512
Bollmann, U. E., Vollertsen, J., Carmeliet, J., & Bester, K. (2014). Dynamics of biocide emissions from buildings in a suburban stormwater catchment-Concentrations, mass loads and emission processes. Water Research, 56, 66-76. https://doi.org/10.1016/j.watres.2014.02.033
Brady, S. P., Monosson, E., Matson, C. W., & Bickham, J. W. (2017). Evolutionary toxicology: Toward a unified understanding of life's response to toxic chemicals. Evolutionary Applications, 10(8), 745-751. https://doi.org/10.1111/eva.12519
Brans, K. I., Almeida, R. A., & Fajgenblat, M. (2021). Genetic differentiation in pesticide resistance between urban and rural populations of a nontarget freshwater keystone interactor, Daphnia magna. Evolutionary Applications, 14(10), 2541-2552. https://doi.org/10.1111/eva.13293
Capkin, E., Ozcelep, T., Kayis, S., & Altinok, I. (2017). Antimicrobial agents, triclosan, chloroxylenol, methylisothiazolinone and borax, used in cleaning had genotoxic and histopathologic effects on rainbow trout. Chemosphere, 182, 720-729. https://doi.org/10.1016/j.chemosphere.2017.05.093
Chatterjee, N., Lee, H., Kim, J., Kim, D., Lee, S., & Choi, J. (2021). Critical window of exposure of CMIT/MIT with respect to developmental effects on zebrafish embryos: Multi-level endpoint and proteomics analysis. Environmental Pollution, 268, 115704. https://doi.org/10.1016/j.envpol.2020.115784
Cho, K.-H., & Kim, J.-R. (2020). Comparison study of dermal cell toxicity and zebrafish brain toxicity by humidifier sterilizer chemicals (PHMG, PGH, CMIT/MIT. Environmental Biology Research, 38(2), 271-277. https://doi.org/10.11626/KJEB.2020.38.2.271
Collier, P. J., Ramsey, A., Waigh, R. D., Douglas, K. T., Austin, P., & Gilbert, P. (1990). Chemical reactivity of some isothiazolone biocides. Journal of Applied Bacteriology, 69(4), 578-584. https://doi.org/10.1111/j.1365-2672.1990.tb01551.x
Côte, J., Bouétard, A., Pronost, Y., Besnard, A.-L., Coke, M., Piquet, F., Caquet, T., & Coutellec, M.-A. (2015). Genetic variation of Lymnaea stagnalis tolerance to copper: A test of selection hypotheses and its relevance for ecological risk assessment. Environmental Pollution, 205, 209-217. https://doi.org/10.1016/j.envpol.2015.05.040
Coustau, C., Chevillon, C., & ffrench-Constant, R. (2000). Resistance to xenobiotics and parasites: Can we count the cost. Trends in Ecology & Evolution, 15(9), 378-383. https://doi.org/10.1016/S0169-5347(00)01929-7
Coutellec, M.-A., & Barata, C. (2011). An introduction to evolutionary processes in ecotoxicology. Ecotoxicology, 20(3), 493-496. https://doi.org/10.1007/s10646-011-0637-x
Coutellec, M.-A., & Barata, C. (2013). Special issue on long-term ecotoxicological effects: An introduction. Ecotoxicology, 22(5), 763-766. https://doi.org/10.1007/s10646-013-1092-7
Crane, M., Burton, G. A., Culp, J. M., Greenberg, M. S., Munkittrick, K. R., Ribeiro, R., Salazar, M. H., & St-Jean, S. D. (2007). Review of aquatic in situ approaches for stressor and effect diagnosis. Integrated Environmental Assessment and Management, 3(2), 234-245. https://doi.org/10.1897/IEAM_2006-027.1
Da-Silva-Correa, L. H., Smith, H., Thibodeau, M. C., Welsh, B., & Buckley, H. L. (2022). The application of non-oxidizing biocides to prevent biofouling in reverse osmosis polyamide membrane systems: A review. Journal of Water Supply: Research and Technology-Aqua, 71(2), 261-292. https://doi.org/10.2166/aqua.2022.118
Delos Santos, N., Azmat, S., Cuenca, Y., Drenth, J., Lauper, J., & Tseng, A.-S. (2016). Effects of the biocide methylisothiazolinone on Xenopus laevis wound healing and tail regeneration. Aquatic Toxicology, 181, 37-45. https://doi.org/10.1016/j.aquatox.2016.10.016
Ducup de Saint Paul, L., Ravier, S., Wortham, H., Maupetit, F., Nicolas, M., & Quivet, E. (2021). Development and validation of a UPLC-MS/MS method for the quantification of isothiazolinones in the composition and emissions from consumer products. Analytical and Bioanalytical Chemistry, 413, 6617-6626. https://doi.org/10.1007/s00216-021-03627-7
European Chemicals Agency. (2014). 2-Methylisothiazol-3(2H)-one (MIT). Assessment report (Evaluation of active substances No. 528/2012). http://dissemination.echa.europa.eu/Biocides/ActiveSubstances/1229-13/1229-13_Assessment_Report.pdf
European Chemicals Agency. (2015). C(M)IT/MIT. Assessment report (Evaluation of active substances No. 528/2012; p. 266). http://dissemination.echa.europa.eu/Biocides/ActiveSubstances/1373-06/1373-06_Assessment_Report.pdf
European Food Safety Authority Scientific Committee. (2016). Guidance to develop specific protection goals options for environmental risk assessment at EFSA, in relation to biodiversity and ecosystem services. EFSA Journal, 14(6), 4499. https://doi.org/10.2903/j.efsa.2016.4499
Forbes, V. E., Calow, P., & Sibly, R. M. (2008). The extrapolation problem and how population modeling can help. Environmental Toxicology and Chemistry, 27(10), 1987-1994. https://doi.org/10.1897/08-029.1
Geissen, V., Mol, H., Klumpp, E., Umlauf, G., Nadal, M., van der Ploeg, M., van de Zee, S. E. A. T. M., & Ritsema, C. J. (2015). Emerging pollutants in the environment: A challenge for water resource management. International Soil and Water Conservation Research, 3(1), 57-65. https://doi.org/10.1016/j.iswcr.2015.03.002
Gouin, N., Bertin, A., Espinosa, M. I., Snow, D. D., Ali, J. M., & Kolok, A. S. (2019). Pesticide contamination drives adaptive genetic variation in the endemic mayfly Andesiops torrens within a semi-arid agricultural watershed of Chile. Environmental Pollution, 255, 113099. https://doi.org/10.1016/j.envpol.2019.113099
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1-22. https://doi.org/10.18637/jss.v033.i02
Hu, K., Li, H.-R., Ou, R.-J., Li, C.-Z., & Yang, X.-L. (2014). Tissue accumulation and toxicity of isothiazolinone in Ctenopharyngodon idellus (grass carp): Association with P-glycoprotein expression and location within tissues. Environmental Toxicology and Pharmacology, 37(2), 529-535. https://doi.org/10.1016/j.etap.2013.12.017
Jager, T., Albert, C., Preuss, T. G., & Ashauer, R. (2011). General unified threshold model of survival-A toxicokinetic-toxicodynamic framework for ecotoxicology. Environmental Science & Technology, 45(7), 2529-2540. https://doi.org/10.1021/es103092a
Jansen, M., Coors, A., Stoks, R., & De Meester, L. (2011). Evolutionary ecotoxicology of pesticide resistance: A case study in Daphnia. Ecotoxicology, 20(3), 543-551. https://doi.org/10.1007/s10646-011-0627-z
Kim, M. K., Kim, K.-B., Lee, J. Y., Kwack, S. J., Kwon, Y. C., Kang, J. S., Kim, H. S., & Lee, B.-M. (2019). Risk assessment of 5-chloro-2-methylisothiazol-3(2H)-one/2-methylisothiazol-3(2H)-one (CMIT/MIT) used as a preservative in cosmetics. Toxicological Research, 35(2), 103-117. https://doi.org/10.5487/TR.2019.35.2.103
Klerks, P. L., Xie, L., & Levinton, J. S. (2011). Quantitative genetics approaches to study evolutionary processes in ecotoxicology; A perspective from research on the evolution of resistance. Ecotoxicology, 20(3), 513-523. https://doi.org/10.1007/s10646-011-0640-2
Kresmann, S., Arokia, A. H. R., Koch, C., & Sures, B. (2018). Ecotoxicological potential of the biocides terbutryn, octhilinone and methylisothiazolinone: Underestimated risk from biocidal pathways? Science of the Total Environment, 625, 900-908. https://doi.org/10.1016/j.scitotenv.2017.12.280
Lee, J. H., Paek, J. H., Park, H. N., Park, S., & Kang, H. (2020). Screening and detection of methylisothiazolinone and chloromethylisothiazolinone in cosmetics by UPLC-MS/MS. Analytical Science and Technology, 33(3), 125-133. https://doi.org/10.5806/AST.2020.33.3.125
Lee, S., Lee, J.-S., Kho, Y., & Ji, K. (2022). Effects of methylisothiazolinone and octylisothiazolinone on development and thyroid endocrine system in zebrafish larvae. Journal of Hazardous Materials, 425, 127994. https://doi.org/10.1016/j.jhazmat.2021.127994
Li, A., Wu, Q.-Y., Tian, G.-P., & Hu, H.-Y. (2016). Effective degradation of methylisothiazolone biocide using ozone: Kinetics, mechanisms, and decreases in toxicity. Journal of Environmental Management, 183, 1064-1071. https://doi.org/10.1016/j.jenvman.2016.08.057
Li, M.-H. (2019). Comparative toxicities of 10 widely used biocides in three freshwater invertebrate species. Chemistry and Ecology, 35(5), 472-482. https://doi.org/10.1080/02757540.2019.1579311
Loria, A., Cristescu, M. E., & Gonzalez, A. (2022). Genotype diversity promotes the persistence of Daphnia populations exposed to severe copper stress. Journal of Evolutionary Biology, 35(2), 265-277. https://doi.org/10.1111/jeb.13979
Major, K. M., Weston, D. P., Lydy, M. J., Wellborn, G. A., & Poynton, H. C. (2018). Unintentional exposure to terrestrial pesticides drives widespread and predictable evolution of resistance in freshwater crustaceans. Evolutionary Applications, 11(5), 748-761. https://doi.org/10.1111/eva.12584
Medina, M. H., Correa, J. A., & Barata, C. (2007). Micro-evolution due to pollution: Possible consequences for ecosystem responses to toxic stress. Chemosphere, 67(11), 2105-2114. https://doi.org/10.1016/j.chemosphere.2006.12.024
Nowak, M., Zawadzka, K., & Lisowska, K. (2020). Occurrence of methylisothiazolinone in water and soil samples in Poland and its biodegradation by Phanerochaete chrysosporium. Chemosphere, 254, 126723. https://doi.org/10.1016/j.chemosphere.2020.126723
Organisation for Economic Co-operation and Development. (2004). Test No. 202: Daphnia sp. acute immobilisation test. OECD guidelines for the testing of chemicals, Section 2. https://doi.org/10.1787/9789264069947
Organisation for Economic Co-operation and Development. (2012). Test No. 211: Daphnia magna reproduction test. OECD guidelines for the testing of chemicals.
Orsini, L., Marshall, H., Cuenca Cambronero, M., Chaturvedi, A., Thomas, K. W., Pfrender, M. E., Spanier, K. I., & De Meester, L. (2016). Temporal genetic stability in natural populations of the waterflea Daphnia magna in response to strong selection pressure. Molecular Ecology, 25(24), 6024-6038. https://doi.org/10.1111/mec.13907
Oziolor, E. M., De Schamphelaere, K., & Matson, C. W. (2016). Evolutionary toxicology: Meta-analysis of evolutionary events in response to chemical stressors. Ecotoxicology, 25(10), 1858-1866. https://doi.org/10.1007/s10646-016-1735-6
Oziolor, E. M., DeSchamphelaere, K., Lyon, D., Nacci, D., & Poynton, H. (2020). Evolutionary toxicology-An informational tool for chemical regulation. Environmental Toxicology and Chemistry, 39(2), 257-268. https://doi.org/10.1002/etc.4611
Paijens, C., Bressy, A., Frère, B., & Moilleron, R. (2020). Biocide emissions from building materials during wet weather: Identification of substances, mechanism of release and transfer to the aquatic environment. Environmental Science and Pollution Research, 27(4), 3768-3791. https://doi.org/10.1007/s11356-019-06608-7
Paijens, C., Bressy, A., Frère, B., Tedoldi, D., Mailler, R., Rocher, V., Neveu, P., & Moilleron, R. (2021). Urban pathways of biocides towards surface waters during dry and wet weathers: Assessment at the Paris conurbation scale. Journal of Hazardous Materials, 402, 123765. https://doi.org/10.1016/j.jhazmat.2020.123765
Paijens, C., Frère, B., Caupos, E., Moilleron, R., & Bressy, A. (2020). Determination of 18 biocides in both the dissolved and particulate fractions of urban and surface waters by HPLC-MS/MS. Water, Air, & Soil Pollution, 231(5), 210. https://doi.org/10.1007/s11270-020-04546-6
Posthuma, L., Suter, G. W., II, & Traas, T. P. (2001). Species sensitivity distributions in ecotoxicology. CRC Press.
Romero-Blanco, A., & Alonso, Á. (2022). Laboratory versus wild populations: The importance of population origin in aquatic ecotoxicology. Environmental Science and Pollution Research, 29, 22798-22808. https://doi.org/10.1007/s11356-021-17370-0
Roubeau Dumont, E., Larue, C., Lorber, S., Gryta, H., Billoir, E., Gross, E. M., & Elger, A. (2019). Does intraspecific variability matter in ecological risk assessment? Investigation of genotypic variations in three macrophyte species exposed to copper. Aquatic Toxicology, 211, 29-37. https://doi.org/10.1016/j.aquatox.2019.03.012
Shahid, N., Becker, J. M., Krauss, M., Brack, W., & Liess, M. (2018). Adaptation of Gammarus pulex to agricultural insecticide contamination in streams. Science of the Total Environment, 621, 479-485. https://doi.org/10.1016/j.scitotenv.2017.11.220
Siddique, A., Liess, M., Shahid, N., & Becker, J. M. (2020). Insecticides in agricultural streams exert pressure for adaptation but impair performance in Gammarus pulex at regulatory acceptable concentrations. Science of the Total Environment, 722, 137750. https://doi.org/10.1016/j.scitotenv.2020.137750
Silva, V., Silva, C., Soares, P., Garrido, E. M., Borges, F., & Garrido, J. (2020). Isothiazolinone biocides: Chemistry, biological, and toxicity profiles. Molecules, 25(4), 991. https://doi.org/10.3390/molecules25040991
Speksnijder, P., van Ravestijn, J., & de Voogt, P. (2010). Trace analysis of isothiazolinones in water samples by large-volume direct injection liquid chromatography tandem mass spectrometry. Journal of Chromatography A, 1217(32), 5184-5189. https://doi.org/10.1016/j.chroma.2010.06.010
Van Huizen, A. V., Tseng, A.-S., & Beane, W. S. (2017). Methylisothiazolinone toxicity and inhibition of wound healing and regeneration in planaria. Aquatic Toxicology, 191, 226-235. https://doi.org/10.1016/j.aquatox.2017.08.013
Vanvelk, H., Govaert, L., Berg, E. M. van den, Brans, K. I., & Meester, L. D. (2021). Interspecific differences, plastic, and evolutionary responses to a heat wave in three co-occurring Daphnia species. Limnology and Oceanography, 66(4), 1201-1220. https://doi.org/10.1002/lno.11675
Wang, X.-X., Zhang, T.-Y., Dao, G.-H., & Hu, H.-Y. (2018). Tolerance and resistance characteristics of microalgae Scenedesmus sp. LX1 to methylisothiazolinone. Environmental Pollution, 241, 200-211. https://doi.org/10.1016/j.envpol.2018.05.066
Weston, D. P., Poynton, H. C., Wellborn, G. A., Lydy, M. J., Blalock, B. J., Sepulveda, M. S., & Colbourne, J. K. (2013). Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca. Proceedings of the National Academy of Sciences, 110(41), 16532-16537. https://doi.org/10.1073/pnas.1302023110
Wieck, S., Olsson, O., & Kuemmerer, K. (2016). Possible underestimations of risks for the environment due to unregulated emissions of biocides from households to wastewater. Environment International, 94, 695-705. https://doi.org/10.1016/j.envint.2016.07.007
Willi, Y., Van Buskirk, J., & Hoffmann, A. A. (2006). Limits to the adaptive potential of small populations. Annual Review of Ecology, Evolution, and Systematics, 37(1), 433-458. https://doi.org/10.1146/annurev.ecolsys.37.091305.110145
Williams, T. M. (2007). The mechanism of action of isothiazolone biocides. PowerPlant Chemistry, 9(1), 9.
Wittenberg, J. B., Canas, B. J., Zhou, W., Wang, P. G., Rua, D., & Krynitsky, A. J. (2015). Determination of methylisothiazolinone and methylchloroisothiazolinone in cosmetic products by ultra high performance liquid chromatography with tandem mass spectrometry. Journal of Separation Science, 38(17), 2983-2988. https://doi.org/10.1002/jssc.201500365
Wittmer, I. K., Scheidegger, R., Bader, H.-P., Singer, H., & Stamm, C. (2011). Loss rates of urban biocides can exceed those of agricultural pesticides. Science of the Total Environment, 409(5), 920-932. https://doi.org/10.1016/j.scitotenv.2010.11.031
Zeng, D., Liang, K., Guo, F., Wu, Y., & Wu, G. (2020). Denitrification performance and microbial community under salinity and MIT stresses for reverse osmosis concentrate treatment. Separation and Purification Technology, 242, 116799. https://doi.org/10.1016/j.seppur.2020.116799