Abstract
The effect of fungicides, commonly used in vine cultures, on the health of terrestrial and aquatic ecosystems has been poorly studied. The objective of this study was to evaluate the toxicity of three viticulture fungicides (myclobutanil, cymoxanil, and azoxystrobin) on non-target organisms, the bacteria Rhodopirellula rubra, Escherichia coli, Pseudomonas putida, and Arthrobacter sp., the microalgae Raphidocelis subcapitata, and the macrophyte Lemna minor. Fungicide toxicity was performed in acute cell viability assay for bacteria; 72-h and 7-day growth inhibition tests for R. subcapitata and L. minor, respectively. Contents of photosynthetic pigments and lipid peroxidation in L. minor were evaluated. Arthrobacter sp. and P. putida showed resistance to these fungicides. Even though azoxystrobin affected R. rubra and E. coli cell viability, this effect was due to the solvent used, acetone. Cell viability decrease was obtained for R. rubra exposed to cymoxanil and E. coli exposed to myclobutanil (30 min of exposure at 10 mg/L and 240 min of exposure at 46 mg/L, respectively). R. subcapitata showed about 10-fold higher sensitivity to azoxystrobin (EC50-72h = 0.25 mg/L) and cymoxanil (EC50-72h = 0.36 mg/L) than L. minor to azoxystrobin and myclobutanil (EC50-72h = 1.53 mg/L and EC50-72h = 1.89 mg/L, respectively). No lipid peroxidation was observed in L. minor after fungicide exposure, while changes of total chlorophyll were induced by azoxystrobin and myclobutanil. Our results showed that non-target aquatic organisms of different trophic levels are affected by fungicides used in viticulture.
Similar content being viewed by others
References
Adetutu EM, Ball AS, Osborn AM (2008) Azoxystrobin and soil interactions: degradation and impact on soil bacterial and fungal communities. J Appl Microbiol 105(6):1777–1790. https://doi.org/10.1111/j.1365-2672.2008.03948.x
Aislabie J, Lloyd-Jones G (1995) A review of bacterial-degradation of pesticides. Aust J Soil Res 33:925–942. https://doi.org/10.1071/SR9950925
Akbar S, Sultan S (2016) Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement. Braz J Microbiol 47(3):563–570. https://doi.org/10.1016/j.bjm.2016.04.009
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. https://doi.org/10.1016/j.chemosphere.2009.04.025
Alkimin GD, Daniel D, Frankenbach S, Serôdio J, Soares AMVM, Barata C, Nunes B (2019) Evaluation of pharmaceutical toxic effects of non-standard endpoints on the macrophyte species Lemna minor and Lemna gibba. Sci Total Environ 657:926–937. https://doi.org/10.1016/j.scitotenv.2018.12.002
Anayo OF, Scholastica EC, Peter OC, Nneji UG, Obinna A, Mistura LO (2019) The beneficial roles of Pseudomonas in medicine, industries, and environment: a review. In: Pseudomonas aeruginosa—an armory within. IntechOpen. https://doi.org/10.5772/intechopen.85996
Anon (1993) Decision document: myclobutanil. E93-01. Agriculture Canada. http://publications.gc.ca/collections/Collection/H93-013-4-93-01E.pdf. Accessed 12 September 2019
Athiel P, Mercadier C, Vega D, Bastide J, Davet P, Brunel B, Cleyet-Marel JC (1995) Degradation of iprodione by a soil Arthrobacter-like strain. Appl Environ Microbiol 61(9):3216–3220
Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58(7):649–662. https://doi.org/10.1002/ps.520
Battaglin WA, Sandstrom MW, Kuivila KM, Kolpin DW, Meyer MT (2011) Occurrence of azoxystrobin, propiconazole, and selected other fungicides in US streams, 2005–2006. Water Air Soil Pollut 218:307–322. https://doi.org/10.1007/s11270-010-0643-2
Bedil B, Kendirlioglu G, Agirman N, Cetin AK (2015) Effects of azoxystrobin and flusilazole on growth and protein amount of Scenedesmus acutus. Fresenius Environ Bull 24(4):1258–1262
Berenzen N, Lentzen-Godding A, Probst M, Schulz H, Schulz R, Liess M (2005) A comparison of predicted and measured levels of runoff-related pesticide concentrations in small lowland streams on a landscape level. Chemosphere 58(5):683–691. https://doi.org/10.1016/j.chemosphere.2004.05.009
Bereswill R, Golla B, Streloke M, Schulz R (2012) Entry and toxicity of organic pesticides and copper in vineyard streams: erosion rills jeopardise the efficiency of riparian buffer strips. Agric Ecosyst Environ 146:81–92. https://doi.org/10.1016/j.agee.2011.10.010
Botelho RG, Froes CM, Santos JB (2012) Toxicity of herbicides on Escherichia coli growth. Braz J Biol 72(1):141–146. https://doi.org/10.1590/S1519-69842012000100016
Burrell RE, Corke CT (1980) Interactions of the solvent acetone with the fungicides benomyl and captan in fungal assays. Bull Environ Contam Toxicol 25(1):554–561. https://doi.org/10.1007/BF01985571
Cabral JP, Marques C (2006) Faecal coliform bacteria in Febros river (northwest Portugal): temporal variation, correlation with water parameters, and species identification. Environ Monit Assess 118:21–36. https://doi.org/10.1007/s10661-006-0771-8
Cedergreen N, Kamper A, Streibig JC (2006) Is prochloraz a potent synergist across aquatic species? A study on bacteria, daphnia, algae and higher plants. Aquat Toxicol 78(3):243–252. https://doi.org/10.1016/j.aquatox.2006.03.007
Cedergreen N, Abbaspoor M, Sorensen H, Streibig JC (2007) Is mixture toxicity measured on a biomarker indicative of what happens on a population level? A study with Lemna minor. Ecotoxicol Environ Saf 67(3):323–332. https://doi.org/10.1016/j.ecoenv.2006.12.006
Cui F, Chai T, Liu X, Wang C (2017) Toxicity of three strobilurins (kresoxim-methyl, pyraclostrobin, and trifloxystrobin) on Daphnia magna. Environ Toxicol Chem 36(1):182–189. https://doi.org/10.1002/etc.3520
Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8(5):1402–1419. https://doi.org/10.3390/ijerph8051402
Derbalah AS, Belal EB (2008) Biodegradation kinetics of cymoxanil in aquatic system. Chem Ecol 24(3):169–180. https://doi.org/10.1080/02757540802032173
Durjava MK, Kolar B, Arnus L, Papa E, Kovarich S, Sahlin U, Peijnenburg W (2013) Experimental assessment of the environmental fate and effects of triazoles and benzotriazole. ATLA 41(1):65–75. https://doi.org/10.1177/026119291304100108
Environment Canada (1992) Biological test method: growth inhibition test using the freshwater alga Selenastrum capricornutum. Report EPS1/RM/25, Environment Canada, Ottawa, Ont., Canada
European Commission (2015) Review report for the active substance azoxystrobin. https://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/public/?event=activesubstance.detail&language=EN&selectedID=984. Accessed 10 September 2019
EFSA European Food Safety Authority (2009) Conclusion on pesticide peer review regarding the risk assessment of the active substance myclobutanil. EFSA J 8(10):1682. https://doi.org/10.2903/jefsa.2010.1682
EFSA European Food Safety Authority (2010) Conclusion on the peer review of the pesticide risk assessment of the active substance azoxystrobin. EFSA J 8(4):1542. https://doi.org/10.2903/j.efsa.2010.1542
Elkahoui S, Hernández JA, Abdelly C, Ghrir R, Limam F (2005) Effects of salt on lipid peroxidation and antioxidant enzyme activities of Catharanthus roseus suspension cells. Plant Sci 168(3):607–613. https://doi.org/10.1016/j.plantsci.2004.09.006
Elskus AA (2012) Toxicity, sublethal effects, and potential modes of action of select fungicides on freshwater fish and invertebrates. Geological Survey Open-File Report. https://doi.org/10.3133/ofr20121213
Fairchild JF, Ruessler DS, Haverland PS, Carlson AR (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32(4):353–357. https://doi.org/10.1007/s002449900196
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. Period Polytech Chem Eng 59(4):262–271. https://doi.org/10.3311/PPch.8077
Filipov NM, Lawrence DA (2001) Developmental toxicity of a triazole fungicide: consideration of interorgan communication. Toxicol Sci 62(2):185–186. https://doi.org/10.1093/toxsci/62.2.185
Fishel FM (2005) Pesticide toxicity profile: triazole pesticides. PI68, University of Florida, IFAS extension. https://edis.ifas.ufl.edu/pdffiles/PI/PI10500.pdf. Accessed 11 September 2019
Fishel FM, Dewdney MM (2006) Fungicide resistance action committee’s (FRAC) classification scheme of fungicides according to mode of action. PI94, University of Florida, IFAS extension. https://edis.ifas.ufl.edu/pdffiles/PI/PI13100.pdf. Accessed 12 September 2019
Fletcher RA, Gilley A, Sankhla N, Davis TD (2000) Triazoles as plant growth regulators and stress protectants. Janick J (Ed) Horticultural reviews 24:55–138. https://doi.org/10.1002/9780470650776.ch3
Flores C, Catita JA, Lage OM (2014) Assessment of planctomycetes cell viability after pollutants exposure. Anto Leeuw 106:399–411. https://doi.org/10.1007/s10482-014-0206-4
Fraga H, Malheiro AC, Moutinho-Pereira J, Santos JA (2012) An overview of climate change impacts on European viticulture. Food Energy Secur 1(2):94–110. https://doi.org/10.1002/fes3.14
Garanzini DS, Menone ML (2015) Azoxystrobin causes oxidative stress and DNA damage in the aquatic macrophyte Myriophyllum quitense. Bull Environ Contam Toxicol 94(2):146–151. https://doi.org/10.1007/s00128-014-1428-x
Gary C, Metral R, Metay A, Garcia L, Mérot A, Smits N, Wéry J (2017) Towards an agroecological viticulture: advances and challenges. In: Proceedings of the 20th GiESCO International Meeting. Mendoza, Argentina, pp 1122–1127
Gianessi L, Williams A (2011) Fungicides have protected European wine grapes for 150 years. International pesticide benefits case study N°. 19
Gopi R, Jaleel CA, Sairam R, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R (2007) Differential effects of hexaconazole and paclobutrazol on biomass, electrolyte leakage, lipid peroxidation and antioxidant potential of Daucus carota L. Colloids Surf B: Biointerfaces 60(2):180–186. https://doi.org/10.1016/j.colsurfb.2007.06.003
Gustafsson K, Blidberg E, Elfgren IK, Hellström A, Kylin H, Gorokhova E (2010) Direct and indirect effects of the fungicide azoxystrobin in outdoor brackish water microcosms. Ecotoxicology 19(2):431–444. https://doi.org/10.1007/s10646-009-0428-9
Huang Y, Xiao L, Li F, Xiao M, Lin D, Long X, Wu Z (2018) Microbial degradation of pesticide residues and an emphasis on the degradation of cypermethrin and 3-phenoxy benzoic acid: a review. Molecules 23(9):2313. https://doi.org/10.3390/molecules23092313
Idalia VMN, Bernardo F (2017) Escherichia coli as a model organism and its application in biotechnology. In: Recent Advances on Physiology, Pathogenesis and Biotechnological Applications. In Tech Open, pp 253–274. https://doi.org/10.5772/67306
ISO International Organization of Standardization (2005) Water quality—determination of the toxic effect of water constituents and waste water on duckweed (Lemna minor)—duckweed growth inhibition test.
Ivic D (2010) Curative and eradicative effects of fungicides. In: Carisse O (ed) Fungicides. ISBN: 978-953-307-266-1. InTech, pp 3–22
Jianyi M, Senmiao T, Pinwei W, Jianmeng C (2011) Differential toxicity of agricultural fungicides toward three cyanobacterial and five green algal species. Asian J Chem 23(2):533–536
Kahle M, Buerge IJ, Hauser A, Muller MD, Poiger T (2008) Azole fungicides: occurrence and fate in wastewater and surface waters. Environ Sci Technol 42(19):7193–7200. https://doi.org/10.1021/es8009309
Karpouzas DG, Walker A (2000) Factors influencing the ability of Pseudomonas putida strains epI and II to degrade the organophosphate ethoprophos. J Appl Microbiol 89:40–48. https://doi.org/10.1046/j.1365-2672.2000.01080.x
Kemmitt GM, DeBoer G, Ouimette D, Iamauti M (2008) Systemic properties of myclobutanil in soybean plants, affecting control of Asian soybean rust (Phakopsora pachyrhizi). Pest Manag Sci 64(12):1285–1293. https://doi.org/10.1002/ps.1630
Komárek M, Čadková E, Chrastný V, Bordas F, Bollinger JC (2010) Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environ Int 36(1):138–151. https://doi.org/10.1016/j.envint.2009.10.005
Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78(2):366–375. https://doi.org/10.1111/j.1574-6941.2011.01168.x
Liang HJ, Lu XM, Zhu ZQ, Zhu FX (2016) Effect of organic solvent on fungicide toxicity to Sclerotinia sclerotiorum and Botrytis cinerea. Eur J Plant Pathol 146(1):37–45. https://doi.org/10.1007/s10658-016-0889-7
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu L, Zhu B, Wang GX (2015) Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris. Environ Sci Pollut Res 22(10):7766–7775. https://doi.org/10.1007/s1135
Lu T, Zhu Y, Xu J, Ke M, Zhang M, Tan C, Fu Z, Qian H (2018) Evaluation of the toxic response induced by azoxystrobin in the non-target green alga Chlorella pyrenoidosa. Environ Pollut 234:379–388. https://doi.org/10.1016/j.envpol.2017.11.081
Maltby L, Brock TC, van den Brink PJ (2009) Fungicide risk assessment for aquatic ecosystems: importance of interspecific variation, toxic mode of action, and exposure regime. Environ Sci Technol 43(19):7556–7563. https://doi.org/10.1021/es901461c
Mercadier C, Garcia D, Vega D, Bastide J, Coste C (1996) Metabolism of iprodione in adapted and non-adapted soils; effect of soil inoculation with an iprodione-degrading Arthrobacter strain. Soil Biol Biochem 28(12):1791–1796. https://doi.org/10.1016/S0038-0717(96)00285-4
Mohsin SM, Hasanuzzaman, Bhuyan MHM, Parvin K, Fujita M (2019) Exogenous tebuconazole and trifloxystrobin regulates reactive oxygen species metabolism toward mitigating salt-induced damages in cucumber seedling. Plants 8:428. https://doi.org/10.3390/plants8100428
Mónica P, Darwin RO, Manjunatha B, Zúñiga JJ, Diego R, Bryan RB, Mulla SI, Maddela NR (2016) Evaluation of various pesticides-degrading pure bacterial cultures isolated from pesticide-contaminated soils in Ecuador. Afr J Biotechnol 15(40):2224–2233. https://doi.org/10.5897/AJB2016.15418
Mouzaki-Paxinou AC, Foudoulakis M, Arapis G (2013) The use of the biomarkers chlorophylls and carotenoids, for the interpretation of the effects in Lemna minor after exposure of two herbicides with different mode of action. In: Proceedings of the 13th International Conference of Environmental Science and Technology, Athens, Greece
Muller R, Berghahn R, Hilt S (2010) Herbicide effects of metazachlor on duckweed (Lemna minor and Spirodela polyrhiza) in test systems with different trophic status and complexity. J Environ Sci Health B 45(2):95–101. https://doi.org/10.1080/03601230903471829
Murtaza I, Bushra SS, Ubaid-Ullah S, Laila O, Majid S, Dar NA, Ahmad M, Sharma G (2018) A comparative study on biodegradation of chlorpyrifos by wild E. coli and Pseudomonas fluorescens bacterial isolates inhabiting different ecosystems of Kashmir valley. Curr Sci 115(4):753. https://doi.org/10.18520/cs/v115/i4/753-758
National Research Council (2006) Toxicity testing for assessment of environmental agents: Interim report. The National Academies Press, Washington. https://doi.org/10.17226/11523
Nunes B, Antunes SC, Santos J, Martins L, Castro BB (2014) Toxic potential of paracetamol to freshwater organisms: a headache to environmental regulators? Ecotoxicol Environ Saf 107:178–185. https://doi.org/10.1016/j.ecoenv.2014.05.027
Ochoa-Acuña HG, Bialkowski W, Yale G, Hahn L (2009) Toxicity of soybean rust fungicides to freshwater algae and Daphnia magna. Ecotoxicology 18(4):440–446. https://doi.org/10.1007/s10646-009-0298-1
OECD Organisation for Economic Cooperation and Development (2006) Lemna sp. growth inhibition test. Guidelines for Testing of Chemicals, Test Guideline N° 221. Paris, France
OECD Organisation for Economic Cooperation and Development (2011) Freshwater alga and cyanobacteria, growth inhibition test. Guidelines for testing of chemicals, Test Guidelines N° 201. Paris, France.
OIV Organisation Internationale de la Vigne et du Vin (2019) State of the vitiviniculture world market. France, Paris
Ortiz JO, Peñalver PP, Navarro AB (2010) Influence of fungicide residues in wine quality. In: Carisse O (ed) Fungicides. ISBN: 978-953-307-266-1. InTech, pp 421–440
Osman AG (2006) Degradation of the fungicide azoxystrobin by soil microorganisms. U of K J Agric Sci 14(1):124–134. https://doi.org/10.1111/j.1365-2672.2008.03948.x
Paul V, Sharma L, Kumar R, Pandey R, Meena RC (2017) Estimation of chlorophylls/photosynthetic pigments—their stability is an indicator of crop plant tolerance to abiotic stresses. In: Manual of ICAR Sponsored Training Programme for Technical Staff of ICAR Institutes on “Physiological Techniques to Analyze the Impact of Climate Change on Crop Plants”, pp 8–14. https://doi.org/10.13140/RG.2.2.13845.83680
Pérez DJ, Menone ML, Tognetti JA, Lukaszewicz G (2019) Azoxystrobin induces chromosomal aberrations in roots of the hydrophyte Bidens laevis L. Rev Int Contam Ambie 35(3):553–563. https://doi.org/10.20937/RICA.2019.35.03.03
Pimenta FM (2010) Biofluorescência no meio marinho: estrutura e propriedades de uma Pioverdina. University of Lisbon, Dissertation
PPDB Pesticide Properties DataBase (2019) University Hertfordshire. https://sitem.herts.ac.uk/aeru/ppdb/en/. Accessed 9 October 2019
Qiao W, Zhou Z, Liang Q, Mosongo I, Li C, Zhang Y (2019) Improving lupeol production in yeast by recruiting pathway genes from different organisms. Sci Rep 9(1):2992. https://doi.org/10.1038/s41598-019-39497-4
Radic S, Stipanicev D, Cvjetko P, Mikelic IL, Rajcic MM, Sirac S, Pevalek-Kozlina B, Pavlica M (2010) Ecotoxicological assessment of industrial effluent using duckweed (Lemna minor L.) as a test organism. Ecotoxicology 19(1):216–222. https://doi.org/10.1007/s10646-009-0408-0
Repetto M, Semprine J, Boveris A (2012) Lipid peroxidation: chemical mechanism, biological implications and analytical determination. In: Lipid peroxidation, InTech, pp 3–30. https://doi.org/10.5772/45943
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12(5):1–22. https://doi.org/10.18637/jss.v012.i05
Ritz C (2010) Toward a unified approach to dose–response modeling in ecotoxicology. Environ Toxicol Chem 29(1):220–229. https://doi.org/10.1002/etc.7
Rodrigues ET, Lopes I, Pardal MA (2013) Occurrence, fate and effects of azoxystrobin in aquatic ecosystems: a review. Environ Int 53:18–28. https://doi.org/10.1016/j.envint.2012.12.005
Rouabhi R (2010) Introduction and toxicology of fungicides. In: Carisse O (ed) Fungicides. ISBN: 978-953-307-266-1. InTech, pp 363–382
Sauter H, Steglich W, Anke T (1999) Strobilurins: evolution of a new class of active substances. Angew Chem Int Ed 38(10):1328–1349. https://doi.org/10.1002/(SICI)1521-3773(19990517)38:10<1328::AID-ANIE1328>3.0.CO;2-1
Stein JR (1973) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, UK
Trumpower BL (1990) Cytochrome bc1 complexes of microorganisms. Microbiol Rev 54(2):101–129
USEPA United States Environmental Protection Agency (1997) Azoxystrobin pesticide fact sheet. https://www3.epa.gov/pesticides/chem_search/reg_actions/registration/fs_PC-128810_07-Feb-97.pdf. Accessed 5 September 2019
USEPA United States Environmental Protection Agency (1998) Cymoxanil pesticide fact sheet. https://www3.epa.gov/pesticides/chem_search/reg_actions/registration/fs_PC-129106_21-Apr-98.pdf. Accessed 12 September 2019
USEPA United States Environmental Protection Agency (2009) Risks of myclobutanil use to federally threatened California red-legged frog (Rana aurora draytonii). http://www.epa.gov/espp/litstatus/effects/redleg-frog/myclobutanil/appendix-k.pdf. Accessed 11 September 2019
USEPA United States Environmental Protection Agency (2019) ECOTOX database. https://cfpub.epa.gov/ecotox/. Accessed 19 April 2019
Verdisson S, Couderchet M, Vernet G (2001) Effects of procymidone, fludioxonil and pyrimethanil on two non-target aquatic plants. Chemosphere 44(3):467–474. https://doi.org/10.1016/S0045-6535(00)00468-9
Vischetti C, Cardinali A, Monaci E, Nicelli M, Ferrari F, Trevisan M, Capri E (2008) Measures to reduce pesticide spray drift in a small aquatic ecosystem in vineyard estate. Sci Total Environ 389(2-3):497–502. https://doi.org/10.1016/j.scitotenv.2007.09.019
Wang W (1990) Literature review on duckweed toxicity testing. Environ Res 52(1):7–22. https://doi.org/10.1016/S0013-9351(05)80147-1
Wang Y, Wang C, Li A, Gao J (2015) Biodegradation of pentachloronitrobenzene by Arthrobacter nicotianae DH 19. Lett Appl Microbiol 61(4):403–410. https://doi.org/10.1111/lam.12476
Wightwick A, Walters R, Allinson G, Reichman S, Menzies N (2010) Environmental risks of fungicides used in horticultural production systems. In: Carisse O (ed) Fungicides. ISBN: 978-953-307-266-1. InTech, pp 273–304
Wightwick A, Bui AD, Zhang P, Rose G, Allinson M, Myers JH, Reichman SM, Menzies N, Pettigrove V, Allinson G (2012) Environmental fate of fungicides in surface waters of a horticultural-production catchment in southeastern Australia. Arch Environ Contam Toxicol 62(3):380–390. https://doi.org/10.1007/s00244-011-9710-y
Wu YX, von Tiedemann A (2001) Physiological effects of azoxystrobin and epoxiconazole on senescence and the oxidative status of wheat. Pestic Biochem Physiol 71:1–10. https://doi.org/10.1006/pest.2001.2561
Yamagishi T, Yamaguchi H, Suzuki S, Horie Y, Tatarazako N (2017) Cell reproductive patterns in the green alga Pseudokirchneriella subcapitata (= Selenastrum capricornutum) and their variations under exposure to the typical toxicants potassium dichromate and 3, 5-DCP. PLoS One 12(2):e0171259. https://doi.org/10.1371/journal.pone.0171259
Zhang YJ, Zhang X, Chen CJ, Zhou MG, Wang HC (2010) Effects of fungicides JS399-19, azoxystrobin, tebuconazole, and carbendazim on the physiological and biochemical indices and grain yield of winter wheat. Pestic Biochem Physiol 98(2):151–157. https://doi.org/10.1016/j.pestbp.2010.04.007
Ziogas BN, Davidse LC (1987) Studies on the mechanism of action of cymoxanil in Phytophthora infestans. Pestic Biochem Physiol 29(2):89–96. https://doi.org/10.1016/0048-3575(87)90066-6
Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, Payraudeau S, Rasmussen JJ, Rohr J, Scharmüller A, Smalling K, Stehle S, Schulz R, Schäfer RB (2019) Fungicides: an overlooked pesticide class? Environ Sci Technol 53:3347–3365. https://doi.org/10.1021/acs.est.8b04392
Acknowledgments
S.C.A. is hired through the Regulamento do Emprego Científico e Tecnológico—RJEC from the Portuguese Foundation for Science and Technology (FCT) program (CEECIND/01756/2017). This work was supported by National Funds (through the Portuguese Science Foundation) and by the European Regional Development Fund (through COMPETE2020 and PT2020) by means of the research project FunG-Eye (POCI-01-0145-FEDER-029505), and by the Strategic Funding UID/Multi/04423/2019 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the program PT2020, and by the project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Marinho, M.d., Diogo, B.S., Lage, O.M. et al. Ecotoxicological evaluation of fungicides used in viticulture in non-target organisms. Environ Sci Pollut Res 27, 43958–43969 (2020). https://doi.org/10.1007/s11356-020-10245-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10245-w