Abstract
Pesticides are commonly found in the environment and pose a risk to target and non-target species; therefore, employing a set of bioassays to rapidly assess the toxicity of these chemicals to diverse species is crucial. The toxicity of nine individual pesticides from organophosphate, organochlorine, phenylurea, dinitroaniline, carbamate, and viologen chemical classes and a mixture of all the compounds were tested in three bioassays (Hydra vulgaris, Lemna minor, and Caenorhabditis elegans) that represent plant, aquatic, and soil-dwelling species, respectively. Multiple endpoints related to growth and survival were measured for each model, and EC10 and EC50 values were derived for each endpoint to identify sensitivity patterns according to chemical classes and target organisms. L. minor had the lowest EC10 and EC50 values for seven and five of the individual pesticides, respectively. L. minor was also one to two orders of magnitude more sensitive to the mixture compared to H. vulgaris and C. elegans, where EC50 values were calculated to be 0.00042, 0.0014, and 0.038 mM, respectively. H. vulgaris was the most sensitive species to the remaining individual pesticides, and C. elegans consistently ranked the least sensitive to all tested compounds. When comparing the EC50 values across all pesticides, the endpoints of L. minor were correlated with each other while the endpoints measured in H. vulgaris and C. elegans were clustered together. While there was no apparent relationship between the chemical class of pesticide and toxicity, the compounds were more closely clustered based on target organisms (herbicide vs insecticide). The results of this study demonstrate that the combination of these plant, soil, and aquatic specie can serve as representative indicators of pesticide pollution in environmental samples.
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The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Aghayev Z, Szafran AT, Tran A, Ganesh HS, Stossi F, Zhou L, Mancini MA, Pistikopoulos EN, Beykal B (2023) Machine learning methods for endocrine disrupting potential identification based on single-cell data. Chem Eng Sci 281:119086
Aliferis KA, Materzok S, Paziotou GN, Chrysayi-Tokousbalides M (2009) Lemna minor L. as a model organism for ecotoxicological studies performing 1H NMR fingerprinting. Chemosphere 76(7):967–973
Anderson GL, Boyd WA, Williams PL (2001) Assessment of sublethal endpoints for toxicity testing with the nematode Caenorhabditis elegans. Environ Toxicol Chem: Int J 20(4):833–838
ATSDR (2022) Substance priority list
Bailey HC, Deanovic L, Reyes E, Kimball T, Larson K, Cortright K, Connor V, Hinton DE (2000) Diazinon and chlorpyrifos in urban waterways in northern California, USA. Environ Toxicol Chem: Int J 19(1):82–87
Bart S, Short S, Jager T, Eagles EJ, Robinson A, Badder C, Lahive E, Spurgeon DJ, Ashauer R (2022) How to analyse and account for interactions in mixture toxicity with toxicokinetic-toxicodynamic models. Sci Total Environ 843:157048
Beach MJ, Pascoe D (1998) The role of Hydra vulgaris (Pallas) in assessing the toxicity of freshwater pollutants. Water Res 32(1):101–106
Bhatti MA, Felsot AS, Al-Khatib K, Kadir S, Parker R (1995) Effects of simulated chlorsulfuron drift on fruit yield and quality of sweet cherries (Prunus avium L.). Environ Toxicol Chem: Int J 14(3):537–544
Blacker AM, Kelly ID, Lantz JL, Mihlan GJ, Jones RL, Young BM (2010) Aldicarb: toxicity, exposure and risks to humans. Hayes' Handb Pestic Toxic 1619–1632
Blanco-Ayala T, Andérica-Romero A, Pedraza-Chaverri J (2014) New insights into antioxidant strategies against paraquat toxicity. Free Radical Res 48(6):623–640
Boutin C, Lee HB, Peart ET, Batchelor PS, Maguire RJ (2000) Effects of the sulfonylurea herbicide metsulfuron methyl on growth and reproduction of five wetland and terrestrial plant species. Environ Toxicol Chem: Int J 19(10):2532–2541
Boyd WA, Smith MV, Freedman JH (2012) Caenorhabditis elegans as a model in developmental toxicology. Methods Mol Biol 15–24
Cedergreen N, Streibig JC (2005) The toxicity of herbicides to non-target aquatic plants and algae: assessment of predictive factors and hazard. Pest Manag Sci: Formerly Pestic Sci 61(12):1152–1160
Chatzigeorgiou M, Schafer WR (2011) Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 70(2):299–309
Cole RD, Anderson GL, Williams PL (2004) The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol Appl Pharmacol 194(3):248–256
Coleman NV, Rich DJ, Tang FH, Vervoort RW, Maggi F (2020) Biodegradation and abiotic degradation of trifluralin: a commonly used herbicide with a poorly understood environmental fate. Environ Sci Technol 54(17):10399–10410
Cunha JP, Chueca P, Garcerá C, Moltó E (2012) Risk assessment of pesticide spray drift from citrus applications with air-blast sprayers in Spain. Crop Prot 42:116–123
de Alkimin GD, Santos J, Soares AM, Nunes B (2020) Ecotoxicological effects of the azole antifungal agent clotrimazole on the macrophyte species Lemna minor and Lemna gibba. Comp Biochem Physiol c: Toxicol Pharmacol 237:108835
Deneer JW (2000) Toxicity of mixtures of pesticides in aquatic systems. Pest Manag Sci: Formerly Pestic Sci 56(6):516–520
Devi RK, Ganesan M, Chen T-W, Chen S-M, Rasheed RA, Al-Onazi WA, Elshikh MS, Liu X, Yu J (2023) Hexagonal nanosheets of pyrrochlore-type lanthanum stannate for sensitive detection of chlorinated pesticide in food and environmental samples. Food Chem 404:134516
Drost W, Matzke M, Backhaus T (2007) Heavy metal toxicity to Lemna minor: studies on the time dependence of growth inhibition and the recovery after exposure. Chemosphere 67(1):36–43
Durand G, Barcelo D (1992) Environmental degradation of atrazine, linuron and fenitrothion in soil samples. Toxicol Environ Chem 36(3–4):225–234
Ellison CA, Tian Y, Knaak JB, Kostyniak PJ, Olson JR (2012) Human hepatic cytochrome P450-specific metabolism of the organophosphorus pesticides methyl parathion and diazinon. Drug Metab Dispos 40(1):1–5
EPA (2009) OECD Guidelines for the testing of chemicals 221: Lemna specific growth inhibition test
Fairchild J, Ruessler D, Haverland P, Carlson A (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32:353–357
Fekete-Kertész I, Kunglné-Nagy Z, Gruiz K, Magyar Á, Farkas É, Molnár M (2015) Assessing toxicity of organic aquatic micropollutants based on the total chlorophyll content of Lemna minor as a sensitive endpoint. Periodica Polytech, Chem Eng 59(4):262–271
Fernandes TC, Pizano MA, Marin-Morales MA (2013) Characterization, modes of action and effects of trifluralin: a review, IntechOpen
Fochtman P, Raszka A, Nierzedska E (2000) The use of conventional bioassays, microbiotests, and some “rapid” methods in the selection of an optimal test battery for the assessment of pesticides toxicity. Environ Toxicol: Int J 15(5):376–384
Freitag D, Ballhorn L, Behechti A, Fischer K, Thumm W (1994) Structural configuration and toxicity of chlorinated alkanes. Chemosphere 28(2):253–259
Fujita T, Nishimura K, Takayama C, Yoshida M, Uchida M (2010) Hydrophobicity as a key physicochemical parameter of environmental toxicology of pesticides. Hayes' Handb Pestic Toxicol 1229–1252
Galliot B (2012) Hydra, a fruitful model system for 270 years. Int J Dev Biol 56(6-7–8):411–423
Gatidou G, Stasinakis AS, Iatrou EI (2015) Assessing single and joint toxicity of three phenylurea herbicides using Lemna minor and Vibrio fischeri bioassays. Chemosphere 119:S69–S74
Gill JPK, Sethi N, Mohan A, Datta S, Girdhar M (2018) Glyphosate toxicity for animals. Environ Chem Lett 16:401–426
Graves AL, Boyd WA, Williams PL (2005) Using transgenic Caenorhabditis elegans in soil toxicity testing. Arch Environ Contam Toxicol 48(4):490–494
Grégoire G, Fortin J, Ebtehaj I, Bonakdari H (2022) Novel hybrid statistical learning framework coupled with random forest and grasshopper optimization algorithm to forecast pesticide use on golf courses. Agriculture 12(7):933
Hernández AF, Parrón T, Tsatsakis AM, Requena M, Alarcón R, López-Guarnido O (2013) Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology 307:136–145
Hernando M, Ejerhoon M, Fernandez-Alba A, Chisti Y (2003) Combined toxicity effects of MTBE and pesticides measured with Vibrio fischeri and Daphnia magna bioassays. Water Res 37(17):4091–4098
Höss S, Jänsch S, Moser T, Junker T, Römbke J (2009) Assessing the toxicity of contaminated soils using the nematode Caenorhabditis elegans as test organism. Ecotoxicol Environ Saf 72(7):1811–1818
Huber W, Schubert V, Sautter C (1982) Effects of pentachlorophenol on the metabolism of the aquatic macrophyte Lem na minor L. Environ Pollut Series a, Ecol Biol 29(3):215–223
Hunt PR (2017) The C. elegans model in toxicity testing. J Appl Toxicol 37(1):50–59
Johansen BE (2003) The dirty dozen: toxic chemicals and the earth’s future, Bloomsbury Publishing USA
Kammenga J, Van Gestel C, Bakker J (1994) Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Arch Environ Contam Toxicol 27:88–94
Karntanut W, Pascoe D (2000) A comparison of methods for measuring acute toxicity to Hydra vulgaris. Chemosphere 41(10):1543–1548
Kim SW, Kim D, Jeong S-W, An Y-J (2020) Size-dependent effects of polystyrene plastic particles on the nematode Caenorhabditis elegans as related to soil physicochemical properties. Environ Pollut 258:113740
Klementová Š, Hornychová L, Šorf M, Zemanová J, Kahoun D (2019) Toxicity of atrazine and the products of its homogeneous photocatalytic degradation on the aquatic organisms Lemna minor and Daphnia magna. Environ Sci Pollut Res 26:27259–27267
Leu C, Singer H, Stamm C, Müller SR, Schwarzenbach RP (2004) Variability of herbicide losses from 13 fields to surface water within a small catchment after a controlled herbicide application. Environ Sci Technol 38(14):3835–3841
Li Y, Li C, Li B, Ma Z (2021) Trifluralin residues in soils from main cotton fields of China and associated ecological risk. Chemosphere 284:131300
Lisiewska Z, Kmiecik W, Korus A (2006) Content of vitamin C, carotenoids, chlorophylls and polyphenols in green parts of dill (Anethum graveolens L.) depending on plant height. J Food Compos Anal 19(23):134–140
Lui A, Wrischer M (2002) Effect of insecticides (Dimiline WP 25, Torak EC 24 and Gamacide 20) on hydra (Hydra vulgaris Pallas). Int J Dev Biol 35(3):335–340
Maharaj S, El Ahmadie N, Rheingold S, El Chehouri J, Yang L, Souders CL II, Martyniuk CJ (2020) Sub-lethal toxicity assessment of the phenylurea herbicide linuron in developing zebrafish (Danio rerio) embryo/larvae. Neurotoxicol Teratol 81:106917
Maheshwari N, Khan AA, Mahmood R, Salam S (2023) Pentachlorophenol-induced hemotoxicity diminishes antioxidant potential and oxidizes proteins, thiols, and lipids in rat blood: an in vivo study. Heliyon 9(5)
Mariani L, De Pascale D, Faraponova O, Tornambè A, Sarni A, Giuliani S, Ruggiero G, Onorati F, Magaletti E (2006) The use of a test battery in marine ecotoxicology: the acute toxicity of sodium dodecyl sulfate. Environ Toxicol: Int J 21(4):373–379
Matsumura H, Matsuoka M, Igisu H, Ikeda M (1997) Cooperative inhibition of acetylcholinesterase activities by hexachlorophene in human erythrocytes. Arch Toxicol 71:151–156
Mayer P, Reichenberg F (2006) Can highly hydrophobic organic substances cause aquatic baseline toxicity and can they contribute to mixture toxicity? Environ Toxicol Chem: Int J 25(10):2639–2644
Metcalfe TL, Dillon PJ, Metcalfe CD (2008) Detecting the transport of toxic pesticides from golf courses into watersheds in the Precambrian Shield region of Ontario, Canada. Environ Toxicol Chem: Int J 27(4):811–818
Natal-da-Luz T, Moreira-Santos M, Ruepert C, Castillo LE, Ribeiro R, Sousa JP (2012) Ecotoxicological characterization of a tropical soil after diazinon spraying. Ecotoxicology 21:2163–2176
Nolan K, Kamrath J, Levitt J (2012) Lindane toxicity: a comprehensive review of the medical literature. Pediatr Dermatol 29(2):141–146
Nowell LH, Norman JE, Moran PW, Martin JD, Stone WW (2014) Pesticide toxicity index—a tool for assessing potential toxicity of pesticide mixtures to freshwater aquatic organisms. Sci Total Environ 476:144–157
OECD (2006) Test No. 221: Lemna sp. Growth Inhibition Test
Onel M, Beykal B, Ferguson K, Chiu WA, McDonald TJ, Zhou L, House JS, Wright FA, Sheen DA, Rusyn I (2019) Grouping of complex substances using analytical chemistry data: a framework for quantitative evaluation and visualization. PLoS One 14(10):e0223517
Park J, Yoo E-J, Shin K, Depuydt S, Li W, Appenroth K-J, Lillicrap AD, Xie L, Lee H, Kim G (2021) Interlaboratory validation of toxicity testing using the duckweed Lemna minor root-regrowth test. Biology 11(1):37
Pereira RC, Monterroso C, Macías F (2010) Phytotoxicity of hexachlorocyclohexane: effect on germination and early growth of different plant species. Chemosphere 79(3):326–333
Pollino CA, Holdway DA (1999) Potential of two hydra species as standard toxicity test animals. Ecotoxicol Environ Saf 43(3):309–316
Queirós L, Pereira J, Gonçalves F, Pacheco M, Aschner M, Pereira P (2019) Caenorhabditis elegans as a tool for environmental risk assessment: emerging and promising applications for a “nobelized worm.” Crit Rev Toxicol 49(5):411–429
Reinecke S, Reinecke A (2007) The impact of organophosphate pesticides in orchards on earthworms in the Western Cape, South Africa. Ecotoxicol Environ Saf 66(2):244–251
Repetto G, Jos A, Hazen M, Molero M, Del Peso A, Salguero M, Del Castillo P, Rodrıguez-Vicente M, Repetto M (2001) A test battery for the ecotoxicological evaluation of pentachlorophenol. Toxicol in Vitro 15(4–5):503–509
Repetto G (2013) Encyclopedia of aquatic ecotoxicology. Férard J, Blaise C (ed), Springer, Dordrecht
Rider CV, Simmons JE (2018) Chemical mixtures and combined chemical and nonchemical stressors: exposure, toxicity, analysis, and risk. Springer
Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. Plos One 10(12):e0146021
Rivenbark KJ, Wang M, Lilly K, Tamamis P, Phillips TD (2022) Development and characterization of chlorophyll-amended montmorillonite clays for the adsorption and detoxification of benzene. Water Res 221:118788
Sant’anna V, de Souza W, Vommaro RC (2016) Anthelmintic effect of herbicidal dinitroanilines on the nematode model Caenorhabditis elegans. Exp Parasitol 167:43–49
Santos SM, Videira RA, Fernandes MA, Santos MS, Moreno AJ, Vicente JA, Jurado AS (2014) Toxicity of the herbicide linuron as assessed by bacterial and mitochondrial model systems. Toxicol in Vitro 28(5):932–939
Sarkar B, Mukhopadhyay R, Ramanayaka S, Bolan N, Ok YS (2021) The role of soils in the disposition, sequestration and decontamination of environmental contaminants. Philos Trans R Soc B 376(1834):20200177
Schwingl PJ, Lunn RM, Mehta SS (2021) A tiered approach to prioritizing registered pesticides for potential cancer hazard evaluations: implications for decision making. Environ Health 20:1–14
Sharma A, Kumar V, Shahzad B, Tanveer M, Sidhu GPS, Handa N, Kohli SK, Yadav P, Bali AS, Parihar RD (2019) Worldwide pesticide usage and its impacts on ecosystem. SN Appl Sci 1:1–16
Silva J, Iannacone J, Cifuentes A, Troncoso L, Bay-Schmith E, Larrain A (2001) Assessment of sensitivity to pentachlorophenol (PCP) in 18 aquatic species, using acute and chronic ecotoxicity bioassays. Ecotoxicol Environ Restor 4(1):10–17
Silva AM, Martins-Gomes C, Silva TL, Coutinho TE, Souto EB, Andreani T (2022) In vitro assessment of pesticides toxicity and data correlation with pesticides physicochemical properties for prediction of toxicity in gastrointestinal and skin contact exposure. Toxics 10(7):378
Simonsen L, Fomsgaard IS, Svensmark B, Spliid NH (2008) Fate and availability of glyphosate and AMPA in agricultural soil. J Environ Sci Health B 43(5):365–375
Singh S, Kumar V, Gill JPK, Datta S, Singh S, Dhaka V, Kapoor D, Wani AB, Dhanjal DS, Kumar M (2020) Herbicide glyphosate: toxicity and microbial degradation. Int J Environ Res Public Health 17(20):7519
Sochová I, Hofman J, Holoubek I (2006) Using nematodes in soil ecotoxicology. Environ Int 32(3):374–383
Tagun R, Boxall AB (2018) The response of Lemna minor to mixtures of pesticides that are commonly used in Thailand. Bull Environ Contam Toxicol 100(4):516–523
Taraldsen JE, Norberg-King TJ (1990) New method for determining effluent toxicity using duckweed (Lemna minor). Environ Toxicol Chem: Int J 9(6):761–767
Teodorović I, Knežević V, Tunić T, Čučak M, Lečić JN, Leovac A, Tumbas II (2012) Myriophyllum aquaticum versus Lemna minor: sensitivity and recovery potential after exposure to atrazine. Environ Toxicol Chem 31(2):417–426
Thi Hue N, Nguyen TPM, Nam H, Hoang Tung N (2018) Paraquat in surface water of some streams in Mai Chau Province, the Northern Vietnam: concentrations, profiles, and human risk assessments. J Chem 2018:1–8
Trovato M, Funck D, Forlani G, Okumoto S, Amir R (2021) Amino acids in plants: regulation and functions in development and stress defense, p. 772810. Front Media SA
Tudi M, Daniel Ruan H, Wang L, Lyu J, Sadler R, Connell D, Chu C, Phung DT (2021) Agriculture development, pesticide application and its impact on the environment. Int J Environ Res Public Health 18(3):1112
Ueda K, Nagai T (2021) Relative sensitivity of duckweed Lemna minor and six algae to seven herbicides. J Pestic Sci 46(3):267–273
Ullah S, Zorriehzahra MJ (2015) Ecotoxicology: a review of pesticides induced toxicity in fish. Adv Anim Vet Sci 3(1):40–57
Uren Webster TM, Perry MH, Santos EM (2015) The herbicide linuron inhibits cholesterol biosynthesis and induces cellular stress responses in brown trout. Environ Sci Technol 49(5):3110–3118
Velki M, Di Paolo C, Nelles J, Seiler T-B, Hollert H (2017) Diuron and diazinon alter the behavior of zebrafish embryos and larvae in the absence of acute toxicity. Chemosphere 180:65–76
Wang W (1990) Literature review on duckweed toxicity testing. Environ Res 52(1):7–22
Wang M, Chen Z, Rusyn I, Phillips TD (2021) Testing the efficacy of broad-acting sorbents for environmental mixtures using isothermal analysis, mammalian cells, and H vulgaris. J Hazard Mater 408:124425
Warne MSJ, Reichelt-Brushett A (2023) Marine pollution–monitoring, management and mitigation, pp. 155–184, Springer
Weir SM, Yu S, Salice CJ (2012) Acute toxicity of herbicide formulations and chronic toxicity of technical-grade trifluralin to larval green frogs (Lithobates clamitans). Environ Toxicol Chem 31(9):2029–2034
Wessler I, Kilbinger H, Bittinger F, Kirkpatrick CJ (2001) The non-neuronal cholinergic system the biological role of non-neuronal acetylcholine in plants and humans. Japan J Pharmacol 85(1):2–10
WHO (2022) Peticie residues in food
Xing L, Liu H, Giesy JP, Yu H (2012) pH-dependent aquatic criteria for 2, 4-dichlorophenol, 2, 4, 6-trichlorophenol and pentachlorophenol. Sci Total Environ 441:125–131
Yu Y, Hua X, Chen H, Wang Z, Han Y, Chen X, Yang Y, Xiang M (2022) Glutamatergic transmission associated with locomotion-related neurotoxicity to lindane over generations in Caenorhabditis elegans. Chemosphere 290:133360
Zečić A, Dhondt I, Braeckman BP (2019) The nutritional requirements of Caenorhabditis elegans. Genes Nutr 14(1):1–13
Zhang C, Cui F, Zeng G-M, Jiang M, Yang Z-Z, Yu Z-G, Zhu M-Y, Shen L-Q (2015) Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Sci Total Environ 518:352–362
Zöngür A, Sari M (2023) Herbicides widely used in the world: an investigation of toxic effects on Caenorhabditis elegans. Biologia Futura 1–12
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This work was supported by the Superfund Hazardous Substance Research and Training Program (National Institute of Environmental Health Sciences) (P42 ES027704) and the United States Department of Agriculture (Hatch 6215). The manuscript contents are solely the responsibility of the grantee and do not necessarily represent the official views of the NIH.
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Kelly Rivenbark: study design, execution of in vitro experiments, preparation of original draft. Hasan Nikkhah: software, visualization, writing—review and editing. Meichen Wang: study design, execution of in vitro experiments, writing—review and editing. Burcu Beykal: software, visualization, funding acquisition, writing—review and editing. Timothy Phillips: funding acquisition, writing—review and editing.
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Rivenbark, K.J., Nikkhah, H., Wang, M. et al. Toxicity of representative organophosphate, organochlorine, phenylurea, dinitroaniline, carbamate, and viologen pesticides to the growth and survival of H. vulgaris, L. minor, and C. elegans. Environ Sci Pollut Res 31, 21781–21796 (2024). https://doi.org/10.1007/s11356-024-32444-5
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DOI: https://doi.org/10.1007/s11356-024-32444-5