Abstract
Uruguay River is the most important river in western Rio Grande do Sul, separating Brazil from Argentina and Uruguay. However, its pollution is of great concern due to agricultural activities in the region and the extensive use of pesticides. In a long term, this practice leads to environmental pollution, especially to the aquatic system. The objective of this study was to analyze the physicochemical characteristics, metals and pesticides levels in water samples obtained before and after the planting and pesticides’ application season from three sites: Uruguay River and two minor affluents, Mezomo Dam and Salso Stream. For biomonitoring, the free-living nematode Caenorhabditis elegans was used, which were exposed for 24 h. We did not find any significant alteration in physicochemical parameters. In the pre- and post-pesticides’ samples we observed a residual presence of three pesticides (tebuconazole, imazethapyr, and clomazone) and metals which levels were above the recommended (As, Hg, Fe, and Mn). Exposure to both pre- and post-pesticides’ samples impaired C. elegans reproduction and post-pesticides samples reduced worms’ survival rate and lifespan. PCA analysis indicated that the presence of metals and pesticides are important variables that impacted C. elegans biological endpoints. Our data demonstrates that Uruguay River and two affluents are contaminated independent whether before or after pesticides’ application season. In addition, it reinforces the usefulness of biological indicators, since simple physicochemical analyses are not sufficient to attest water quality and ecological safety.
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Data Availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ajima MN, Nnodi PC, Ogo OA, Adaka GS, Osuigwe DI, Njoku DC (2015) Bioaccumulation of heavy metals in Mbaa River and the impact on aquatic ecosystem. Environ Monit Assess 187:768
Arocena R, Chalar G, Pacheco JP (2018) Agriculture and elevation are the main factors for Pampasic stream habitat and water quality. Environ Monit Assess 190:254
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
Caballero-Gallardo K, Guerrero-Castilla A, Johnson-Restrepo B, de la Rosa J, Olivero-Verbel J (2015) Chemical and toxicological characterization of sediments along a Colombian shoreline impacted by coal export terminals. Chemosphere 138:837–846
Carneiro FF, Rigotto RM, Augusto LGS, Friedrich K, Burigo AC (2015) Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde. Oswaldo Cruz Foundation-1st edn. Expressão Popular Publishing, São Paulo, p 624 (in Portuguese)
Carvalho WF, Ruiz de Arcaute C, Perez-Iglesias JM, Laborde MRR, Soloneski S, Larramendy ML (2019) DNA damage exerted by mixtures of commercial formulations of glyphosate and imazethapyr herbicides in Rhinella arenarum (Anura, Bufonidae) tadpoles. Ecotoxicology 28:367–377
Chanpiwat P, Kim KW (2019) Arsenic health risk assessment related to rice consumption behaviors in adults living in Northern Thailand. Environ Monit Assess 191:674
Clavijo A, Kronberg MF, Rossen A, Moya A, Calvo D, Salatino SE, Pagano EA, Morabito JA, Munarriz ER (2016) The nematode Caenorhabditis elegans as an integrated toxicological tool to assess water quality and pollution. Sci Total Environ 569-570:252–261
Crestani M, Menezes C, Glusczak L, dos Santos MD, Spanevello R, Silveira A, Goncalves FF, Zanella R, Loro VL (2007) Effect of clomazone herbicide on biochemical and histological aspects of silver catfish (Rhamdia quelen) and recovery pattern. Chemosphere 67:2305–2311
Fao N, Nascimento S, de La Cruz AH, Calderon D, Rocha R, Saint’Pierre T, Gioda A, Thiesen FV, Brucker N, Emanuelli T, Garcia SC (2019) Estimation of total arsenic contamination and exposure in Brazilian rice and infant cereals. Drug Chem Toxicol 2:1–9
Ferreira AS, da Silva HC, Rodrigues HO, Silva M, Junior A (2016) Occurrence and spatial-temporal distribution of herbicide residues in the Ipojuca River sub-basin, Pernambuco, Brazil. Rev Bras Eng Agríc Ambient 20:1124–1128
Fukagawa NK, Ziska LH (2019) Rice: importance for global nutrition. J Nutr Sci Vitaminol 65:S2–s3
Glinski DA, Purucker ST, Van Meter RJ, Black MC, Henderson WM (2018) Analysis of pesticides in surface water, stemflow, and throughfall in an agricultural area in South Georgia, USA. Chemosphere 209:496–507
Goncalves C, Marins AT, do Amaral AMB, Nunes MEM, Muller TE, Severo E, Feijo A, Rodrigues CCR, Zanella R, Prestes OD, Clasen B, Loro VL (2020) Ecological impacts of pesticides on Astyanax jacuhiensis (Characiformes: Characidae) from the Uruguay river, Brazil. Ecotoxicol Environ Saf 205:111314
Gonzalez-Macias C, Schifter I, Lluch-Cota DB, Mendez-Rodriguez L, Hernandez-Vazquez S (2006) Distribution, enrichment and accumulation of heavy metals in coastal sediments of Salina Cruz Bay, Mexico. Environ Monit Assess 118:211–230
Guimaraes B, Bandow C, Amorim MJB, Kehrer A, Coors A (2018) Mixture toxicity assessment of a biocidal product based on reproduction and avoidance behaviour of the collembolan Folsomia candida. Ecotoxicol Environ Saf 165:284–290
He X, Deng H, Hwang HM (2019) The current application of nanotechnology in food and agriculture. J Food Drug Anal 27:1–21
Kaur B, Ranawana V, Henry J (2016) The glycemic index of rice and rice products: a review, and table of GI values. Crit Rev Food Sci Nutr 56:215–236
Khammanee N, Qiu Y, Kungskulniti N, Bignert A, Meng Y, Zhu Z, Lekew Teffera Z (2020) Presence and health risks of obsolete and emerging pesticides in paddy rice and soil from Thailand and China. Int J Environ Res Public Health 17(11):3786
Kim SW, Moon J, Jeong SW, An YJ (2018) Development of a nematode offspring counting assay for rapid and simple soil toxicity assessment. Environ Pollut 236:91–99
Kitazume H, Dayi M, Tanaka R, Kikuchi T (2018) Assessment of the behaviour and survival of nematodes under low oxygen concentrations. PLoS One 13:e0197122
Kumarathilaka P, Seneweera S, Meharg A, Bundschuh J (2018) Arsenic accumulation in rice (Oryza sativa L.) is influenced by environment and genetic factors. Sci Total Environ 642:485–496
Li S, Jiang Y, Sun Q, Coffin S, Chen L, Qiao K, Gui W, Zhu G (2020) Tebuconazole induced oxidative stress related hepatotoxicity in adult and larval zebrafish (Danio rerio). Chemosphere 241:125129
Lohren H, Bornhorst J, Galla HJ, Schwerdtle T (2015) The blood-cerebrospinal fluid barrier--first evidence for an active transport of organic mercury compounds out of the brain. Metallomics 7:1420–1430
Machado-Neves M, Neto MJO, Miranda DC, Souza ACF, Castro MM, Sertorio MN, Carvalho TF, Matta SLP, Freitas MB (2018) Dietary exposure to tebuconazole affects testicular and epididymal histomorphometry in frugivorous bats. Bull Environ Contam Toxicol 101:197–204
Majumder B, Das S, Pal B, Biswas AK (2020) Evaluation of arsenic induced toxicity based on arsenic accumulation, translocation and its implications on physio-chemical changes and genomic instability in indica rice (Oryza sativa L.) cultivars. Ecotoxicology 29:13–34
Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Cambell RCJ, Sun G, Zhu Y-G, Feldmann J, Raab A, Zhao F-J, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43:1612–1617
Meyer S, Markova M, Pohl G, Marschall TA, Pivovarova O, Pfeiffer AFH, Schwerdtle T (2018) Development, validation and application of an ICP-MS/MS method to quantify minerals and (ultra-)trace elements in human serum. J Trace Elem Med Biol 49:157–163
Miller DL, Roth MB (2009) C. elegans are protected from lethal hypoxia by an embryonic diapause. Curr Biol 19:1233–1237
Miron DS, Silva LVF, Golombieski JI, Machado SLO, Marchezan E, Baldisserotto B (2004) Lethal concentration of clomazone, metsulfuron-metil, and quinclorac for silver catfish, Rhamdia quelen, fingerlings. Cienc Rural 34:1465–1469
Moraes BS, Clasen B, Loro VL, Pretto A, Toni C, de Avila LA, Marchesan E, Machado SL, Zanella R, Reimche GB (2011) Toxicological responses of Cyprinus carpio after exposure to a commercial herbicide containing imazethapyr and imazapic. Ecotoxicol Environ Saf 74:328–335
Pereira L, Fernandes MN, Martinez CB (2013) Hematological and biochemical alterations in the fish Prochilodus lineatus caused by the herbicide clomazone. Environ Toxicol Pharmacol 36:1–8
Perez-Iglesias JM, Soloneski S, Nikoloff N, Natale GS, Larramendy ML (2015) Toxic and genotoxic effects of the imazethapyr-based herbicide formulation Pivot H(R) on montevideo tree frog Hypsiboas pulchellus tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 119:15–24
Perez-Iglesias JM, Ruiz de Arcaute C, Natale GS, Soloneski S, Larramendy ML (2017) Evaluation of imazethapyr-induced DNA oxidative damage by alkaline Endo III- and Fpg-modified single-cell gel electrophoresis assay in Hypsiboas pulchellus tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 142:503–508
Pignati WA, Lima FANS, Lara SS, Correa MLM, Barbosa JR, Leão LHC, Pignatti MG (2017) Distribuição espacial do uso de agrotóxicos no Brasil: uma ferramenta para a Vigilância em Saúde. Cien Saude Colet 22:3281–3293
Primel EG, Zanella R, Kurz MHS, Gonçalves FF, Machado SO, Marchezan E (2005) Poluição das águas por herbicidas utilizados no cultivo do arroz irrigado na região central do estado do Rio Grande do Sul, Brasil: predição teórica e monitoramento. Quim Nova 28:605–609
Rebelo RM, Vasconcelos R, Buys B, Rezende J, Moraes K, Oliveira R (2010) Produtos agrotóxicos e afins comercializados em 2009 no Brasil: uma abordagem ambiental. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), Brasília, Brazil
Rojo M, Alvarez-Munoz D, Domanico A, Foti R, Rodriguez-Mozaz S, Barcelo D, Carriquiriborde P (2019) Human pharmaceuticals in three major fish species from the Uruguay River (South America) with different feeding habits. Environ Pollut 252:146–154
Ruan Q-L, Ju J-J, Li Y-H, Liu R, Pu Y-P, Yin L-H, Wang D-Y (2009) Evaluation of pesticide toxicities with differing mechanisms using Caenorhabditis elegans. J Toxic Environ Health A 72:746–751
Salem FB, Said OB, Aissa P, Mahmoudi E, Monperrus M, Grunberger O, Duran R (2016) Pesticides in Ichkeul Lake-Bizerta Lagoon Watershed in Tunisia: use, occurrence, and effects on bacteria and free-living marine nematodes. Environ Sci Pollut Res Int 23:36–48
Soloneski S, Ruiz de Arcaute C, Nikoloff N, Larramendy ML (2017) Genotoxicity of the herbicide imazethapyr in mammalian cells by oxidative DNA damage evaluation using the Endo III and FPG alkaline comet assays. Environ Sci Pollut Res Int 24:10292–10300
Speranza ED, Colombo M, Heguilor S, Tatone LM, Colombo JC (2020) Alterations in the sterol signature of detritivorous fish along pollution gradients in the Rio de la Plata basin (Argentina): from plant to sewage-based diet. Environ Res 184:109351
Stevanovic M, Gasic S, Pipal M, Blahova L, Brkic D, Neskovic N, Hilscherova K (2017) Toxicity of clomazone and its formulations to zebrafish embryos (Danio rerio). Aquat Toxicol 188:54–63
Sun XD, Su P, Shan H (2017) Mycotoxin contamination of rice in China. J Food Sci 82:573–584
Tejeda-Benitez L, Flegal R, Odigie K, Olivero-Verbel J (2016) Pollution by metals and toxicity assessment using Caenorhabditis elegans in sediments from the Magdalena River, Colombia. Environ Pollut 212:238–250
Vallejo Toro PP, Vasquez Bedoya LF, Correa ID, Bernal Franco GR, Alcantara-Carrio J, Palacio Baena JA (2016) Impact of terrestrial mining and intensive agriculture in pollution of estuarine surface sediments: spatial distribution of trace metals in the Gulf of Uraba, Colombia. Mar Pollut Bull 111:311–320
Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol Toxicol Pharmacol 146:281–300
Vijver MG, Van Gestel CA, Lanno RP, Van Straalen NM, Peijnenburg WJ (2004) Internal metal sequestration and its ecotoxicological relevance: a review. Environ Sci Technol 38:4705–4712
Von Sperling M (2005) Principles of biological treatment of residual waters. In: Von Sperling M (ed) Introduction to water quality and sewage treatment, 3rd edn. Federal University of Minas Gerais Publishing, Belo Horizonte, p 452
Von Sperling M (2007) Biological wastewater treatment series: basic principles of wastewater treatment, 1st edn. IWA Publishing, London
Wah Chu K, Chow KL (2002) Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. Aquat Toxicol 61:53–64
Yang JD, Liu SH, Liao MH, Chen RM, Liu PY, Ueng TH (2018) Effects of tebuconazole on cytochrome P450 enzymes, oxidative stress, and endocrine disruption in male rats. Environ Toxicol 33:899–907
Zanella R, Primel E, Oliveira M, Gonçalves F, Marchezan E (2002) Monitoring of the herbicide clomazone in environmental water samples by solid-phase extraction and high-performance liquid chromatography with ultraviolet detection. Chromatographia 55:573–577
Zhao FJ, Zhu YG, Meharg AA (2013) Methylated arsenic species in rice: geographical variation, origin, and uptake mechanisms. Environ Sci Technol 47:3957–3966
Zhu YG, Williams PN, Meharg AA (2008) Exposure to inorganic arsenic from rice: a global health issue? Environ Pollut 154:169–171
Funding
This study was funded in part by CNPq (Universal Grants- 453963/2014-5), FAPERGS/PqG # 18/2551-0000434-0, CNPq/FAPERGS/DECIT/SCTIE-MS/PRONEM #16/2551-0000248-7, PROPPI/ UNIPAMPA, and the German Research Foundation Research Unit TraceAge (FOR 2558). Authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. D.S.A is recipient of researcher fellowship (PQ2/CNPq).
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E.C.K conceptualization, investigation, methodology, data curation, formal analysis, writing- original draft; M.T.J conceptualization, supervision, methodology, formal analysis, writing - original draft; D.T methodology, data curation, formal analysis, writing; S.M methodology, data curation, formal analysis; T.G methodology, data curation, formal analysis, writing; R.R data curation, formal analysis, supervision, funding acquisition, writing; S. C data curation, formal analysis, writing- original draft; T. S methodology, data curation, formal analysis, resources, writing; J. B methodology, data curation, formal analysis, writing; D.S.A conceptualization, funding acquisition, investigation, methodology, project administration, data curation, formal analysis, resources, supervision, writing.
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Kuhn, E.C., Jacques, M.T., Teixeira, D. et al. Ecotoxicological assessment of Uruguay River and affluents pre- and post-pesticides’ application using Caenorhabditis elegans for biomonitoring. Environ Sci Pollut Res 28, 21730–21741 (2021). https://doi.org/10.1007/s11356-020-11986-4
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DOI: https://doi.org/10.1007/s11356-020-11986-4