Abstract
Glyphosate (N-(phosphonomethyl)glycine) is an active substance of many herbicides. According to literature studies, glyphosate residues and their metabolites have been commonly detected in surface waters and toxicological reports confirmed negative effects on living organisms. In this study, the acute embryo toxicity of glyphosate into two different fish species—common carp (Cyprinus carpio) and zebrafish (Danio rerio)—was investigated. Lethal endpoints, development disorder, and, in addition, other sublethal endpoints such as hatching rate, formation of somites, and development of eyes, spontaneous movement, heartbeat/blood circulation, pigmentation, and edema were recorded to indicate the mode of action of the toxic compound. Hatching retardation (p < 0.05) was observed in experimental groups of common carp exposed to glyphosate with significant statistical difference especially at the highest concentration after 72, 96, and 120 hpf. The significantly highest cumulative mortality at concentration of 50 mg/l was observed. In contrast, hatching stimulation was observed in embryos of zebrafish exposed to the highest concentration of glyphosate. The significantly highest cumulative mortality for zebrafish was observed only at concentration of 50 mg/l. Based on our results, early life stages of common carp are more sensitive in comparison to zebrafish to the toxic action of glyphosate.
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Aliko V, Hajdaraj G, Caci A, Faggio C (2015) Copper induced lysosomal membrane destabilisation in haemolymph cells of Mediterranean green crab (Carcinus aestuarii, Nardo, 1847) from the Narta Lagoon (Albania). Braz Arch Biol Technol 58(5):750–756. https://doi.org/10.1590/S1516-89132015050244
AmidC, OlstedtM, Gunnarsson JS, le Lan H, Tran Thi MinhH, van den Brink PJ, HellströmM, TedengrenM (2017) Additive effects of the herbicide glyphosate and elevated temperature on the branched coral Acropora formosa in Nha Trang, VietnamEnviron Sci Pollut Res doi:https://doi.org/10.1007/s11356-016-8320-7
Bai SH, Ogbourne SM (2016) Glyphosate: environmental contamination, toxicity and potential risks to human health via food contamination. Environ Sci Pollut Res 23(19):18988–19001. https://doi.org/10.1007/s11356-016-7425-3
Banaee M, Sureda A, Mirvaghefi AR, Ahmadi K (2011) Effects of diazinon on biochemical parameters of blood in rainbow trout (Oncorhynchus mykiss). Pestic Biochem Physiol 99(1):1–6. https://doi.org/10.1016/j.pestbp.2010.09.001
Bartoskova M et al (2013) Evaluation of ibuprofen toxicity for zebrafish (Danio rerio) targeting on selected biomarkers of oxidative stress. Neuroendocrinol Lett 34:102–108
Botta F, Lavison G, Couturier G, Alliot F, Moreau-Guigon E, Fauchon N, Guery B, Chevreuil M, Blanchoud H (2009) Transfer of glyphosate and its degradate AMPA to surface waters through urban sewerage systems. Chemosphere 77(1):133–139. https://doi.org/10.1016/j.chemosphere.2009.05.008
Bridi D, Altenhofen S, Gonzalez JB, Reolon GK, Bonan CD (2017) Glyphosate and Roundup® alter morphology and behavior in zebrafish. Toxicology 392:32–39. https://doi.org/10.1016/j.tox.2017.10.007
Burgos-Aceves MA, Faggio C (2017) An approach to the study of the immunity functions of bivalve haemocytes: physiology and molecular aspects. Fish Shellfish Immunol 67:513–517. https://doi.org/10.1016/j.fsi.2017.06.042
Chromcova L et al (2015) NeemAzal T/S–toxicity to early-life stages of common carp (Cyprinus carpio L.) Vet Med 60:23–30
Cuhra M, Bøhn T, Cuhra P (2016) Glyphosate: too much of a good thing? Front Environ Sci 4. https://doi.org/10.3389/fenvs.2016.00028
Faggio C, Pagano M, Alampi R, Vazzana I, Felice MR (2016) Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of quaternium-15 in Mytilus galloprovincialis. Aquat Toxicol 180:258–265. https://doi.org/10.1016/j.aquatox.2016.10.010
Fazio F, Cecchini S, Faggio C, Caputo AR, Piccione G (2014a) Stability of oxidative stress biomarkers in flathead mullet, Mugil cephalus, serum during short-term storage. Ecol Indic 46:188–192. https://doi.org/10.1016/j.ecolind.2014.06.021
Fazio F, Piccione G, Tribulato K, Ferrantelli V, Giangrosso G, Arfuso F, Faggio C (2014b) Bioaccumulation of heavy metals in blood and tissue of striped mullet in two Italian lakes. J Aquat Anim Health 26(4):278–284. https://doi.org/10.1080/08997659.2014.938872
Friends of the Earth Europe FOE (2013) The environmental impacts of glyphosate
Glaberman S, Padilla S, Barron MG (2017) Evaluating the zebrafish embryo toxicity test for pesticide hazard screening. Environ Toxicol Chem 36(5):1221–1226. https://doi.org/10.1002/etc.3641
Haarstad K, Bavor HJ, Mæhlum T (2011) Organic and metallic pollutants in water treatment and natural wetlands: a review. Water Sci Technol 65(1):76–99. https://doi.org/10.2166/wst.2011.831
Horie Y, Yamagishi T, Takahashi H, Shintaku Y, Iguchi T, Tatarazako N (2017) Assessment of the lethal and sublethal effects of 20 environmental chemicals in zebrafish embryos and larvae by using OECD TG 212. J Appl Toxicol 37(10):1245–1253. https://doi.org/10.1002/jat.3487
Hostovsky M, Blahova J, Plhalova L, Kopriva V, Svobodova Z (2014) Effects of the exposure of fish to triazine herbicides. Neuroendocrinol Lett 35:3–25
ISO 7346 (1996) Water quality — Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] — Part 1: Static method
Jofré DM, García MJG, Salcedo R, Morales M, Alvarez M, Enriz D, Giannini F (2014) Fish toxicity of commercial herbicides formulated with glyphosate. J Environ Anal Toxicol 4:1
Köprücü K, Aydın R (2004) The toxic effects of pyrethroid deltamethrin on the common carp (Cyprinus carpio L.) embryos and larvae. Pestic Biochem Physiol 80(1):47–53. https://doi.org/10.1016/j.pestbp.2004.05.004
Lauriano ER, Pergolizzi S, Capillo G, Kuciel M, Alesci A, Faggio C (2016) Immunohistochemical characterization of Toll-like receptor 2 in gut epithelial cells and macrophages of goldfish Carassius auratus fed with a high-cholesterol diet. Fish Shellfish Immunol 59:250–255. https://doi.org/10.1016/j.fsi.2016.11.003
Li M-H, Ruan L-Y, Zhou J-W, Y-H F, Jiang L, Zhao H, Wang J-S (2017) Metabolic profiling of goldfish (Carassius auratis) after long-term glyphosate-based herbicide exposure. Aquat Toxicol 188:159–169. https://doi.org/10.1016/j.aquatox.2017.05.004
Lopes FM, Caldas SS, Primel EG, da Rosa CE (2017) Glyphosate adversely affects Danio rerio males: acetylcholinesterase modulation and oxidative stress. Zebrafish 14(2):97–105. https://doi.org/10.1089/zeb.2016.1341
Mottier A, Kientz-Bouchart V, Serpentini A, Lebel JM, Jha AN, Costil K (2013) Effects of glyphosate-based herbicides on embryo-larval development and metamorphosis in the Pacific oyster, Crassostrea gigas. Aquat Toxicol 128-129:67–78. https://doi.org/10.1016/j.aquatox.2012.12.002
Nagel R (2002) DarT: the embryo test with the zebrafish Danio rerio—a general model in ecotoxicology and toxicology. ALTEX 19:38–48
Nešković N, Poleksić V, Elezović I, Karan V, Budimir M (1996) Biochemical and histopathological effects of glyphosate on carp, Cyprinus carpio L. Bull Environ Contam Toxicol 56(2):295–302
OECD (2013) OECD guidelines for the testing of chemicals, test no. 236: Fish Embryo Acute Toxicity (FET) Test. OECD Publishing. doi: https://doi.org/10.1787/9789264203709-en
Pagano M, Capillo G, Sanfilippo M, Palato S, Trischitta F, Manganaro A, Faggio C (2016) Evaluation of functionality and biological responses of Mytilus galloprovincialis after exposure to Quaternium-15 (methenamine 3-chloroallylochloride). Molecules 21(2):144. https://doi.org/10.3390/molecules21020144
Pagano M, Porcino C, Briglia M, Fiorino E, Vazzana M, Silvestro S, Faggio C (2017) The influence of exposure of cadmium chloride and zinc chloride on haemolymph and digestive gland cells from Mytilus galloprovincialis. Int J Environ Res 11(2):207–216. https://doi.org/10.1007/s41742-017-0020-8
ParisP, PaceE, Parisi PresicceD, MaschioG, UrsinoS (2016) Rapporto nazionale pesticidi nelle acque. Dati 2013–2014. ISPRA
PeňázM, ProkešM, KouřilJ, J H (1983) Early development of the carp, Cyprinus carpio Acta Sci Nat Brno17:1–39
Piešova E (2005) The effect of glyphosate on the frequency of micronuclei in bovine lymphocytes in vitro. Acta Vet 55:101–109
RzymskiP, KlimaszykP, KubackiT, PoniedziałekB (2013) The effect of glyphosate-based herbicide on aquatic organisms—a case study vol 13. doi:https://doi.org/10.2478/limre-2013-0024
Samanta P, Pal S, Mukherjee AK, Ghosh AR (2014) Biochemical effects of glyphosate based herbicide, Excel Mera 71 on enzyme activities of acetylcholinesterase (AChE), lipid peroxidation (LPO), catalase (CAT), glutathione-S-transferase (GST) and protein content on teleostean fishes. Ecotoxicol Environ Saf 107:120–125. https://doi.org/10.1016/j.ecoenv.2014.05.025
Sánchez JAA, Varela Junior AS, Corcini CD, da Silva JC, Primel EG, Caldas S, Klein RD, Martins CDMG (2017) Effects of roundup formulations on biochemical biomarkers and male sperm quality of the livebearing Jenynsia multidentata. Chemosphere 177:200–210. https://doi.org/10.1016/j.chemosphere.2017.02.147
SarıgülZ, BekcanS (2009) Acute toxicity of the herbicide glyphosate on Daphnia magna. J Agric Sci (Turkey)
Saunders LE, Pezeshki R (2015) Glyphosate in runoff waters and in the root-zone: a review. Toxics 3(4):462–480. https://doi.org/10.3390/toxics3040462
Savorelli F, Manfra L, Croppo M, Tornambè A, Palazzi D, Canepa S, Trentini PL, Cicero AM, Faggio C (2016) Fitness evaluation of Ruditapes philippinarum exposed to Ni. Biol Trace Elem Res 177(2):1–10. https://doi.org/10.1007/s12011-016-0885-y
Schaumburg LG, Siroski PA, Poletta GL, Mudry MD (2016) Genotoxicity induced by Roundup® (Glyphosate) in tegu lizard (Salvator merianae) embryos. Pestic Biochem Physiol 130:71–78. https://doi.org/10.1016/j.pestbp.2015.11.009
Sehonova P, Plhalova L, Blahova J, Berankova P, Doubkova V, Prokes M, Tichy F, Vecerek V, Svobodova Z (2016) The effect of tramadol hydrochloride on early life stages of fish. Environ Toxicol Pharmacol 44:151–157. https://doi.org/10.1016/j.etap.2016.05.006
Sehonova P, Plhalova L, Blahova J, Doubkova V, Marsalek P, Prokes M, Tichy F, Skladana M, Fiorino E, Mikula P, Vecerek V, Faggio C, Svobodova Z (2017a) Effects of selected tricyclic antidepressants on early-life stages of common carp (Cyprinus carpio). Chemosphere 185:1072–1080. https://doi.org/10.1016/j.chemosphere.2017.07.092
Sehonova P, Plhalova L, Blahova J, Doubkova V, Prokes M, Tichy F, Fiorino E, Faggio C, Svobodova Z (2017b) Toxicity of naproxen sodium and its mixture with tramadol hydrochloride on fish early life stages. Chemosphere 188:414–423. https://doi.org/10.1016/j.chemosphere.2017.08.151
Sobjak TM, Romão S, do Nascimento CZ, dos Santos AFP, Vogel L, Guimarães ATB (2017) Assessment of the oxidative and neurotoxic effects of glyphosate pesticide on the larvae of Rhamdia quelen fish. Chemosphere 182:267–275. https://doi.org/10.1016/j.chemosphere.2017.05.031
Solomon K, Thompson D (2003) Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. J Toxicol Environ Health B 6(3):289–324. https://doi.org/10.1080/10937400306468
Stehr CM, Linbo TL, Baldwin DH, Scholz NL, Incardona JP (2009) Evaluating the effects of forestry herbicides on fish development using rapid phenotypic screens. N Am J Fish Manag 29(4):975–984. https://doi.org/10.1577/M08-173.1
Sulukan E, Köktürk M, Ceylan H, Beydemir Ş, Işik M, Atamanalp M, Ceyhun SB (2017) An approach to clarify the effect mechanism of glyphosate on body malformations during embryonic development of zebrafish (Daino rerio). Chemosphere 180:77–85. https://doi.org/10.1016/j.chemosphere.2017.04.018
Tarazona JV, Court-Marques D, Tiramani M, Reich H, Pfeil R, Istace F, Crivellente F (2017) Glyphosate toxicity and carcinogenicity: a review of the scientific basis of the European Union assessment and its differences with IARC. Arch Toxicol 91(8):2723–2743. https://doi.org/10.1007/s00204-017-1962-5
Torre A, Trischitta F, Faggio C (2013) Effect of CdCl2 on regulatory volume decrease (RVD) in Mytilus galloprovincialis digestive cells. Toxicol in Vitro 27(4):1260–1266. https://doi.org/10.1016/j.tiv.2013.02.017
Velisek J, Stara A, Koutnik D, Machova J (2015) Effects of prometryne on early life stages of common carp (Cyprinus carpio L.) Pestic Biochem Physiol 118:58–63. https://doi.org/10.1016/j.pestbp.2014.11.011
Wagner N, Lötters S, Veith M, Viertel B (2015) Acute toxic effects of the herbicide formulation Focus® Ultra on embryos and larvae of the Moroccan painted frog, Discoglossus scovazzi. Arch Environ Contam Toxicol 69(4):535–544. https://doi.org/10.1007/s00244-015-0176-1
Wagner N, Reichenbecher W, Teichmann H, Tappeser B, Lötters S (2013) Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environ Toxicol Chem 32(8):1688–1700. https://doi.org/10.1002/etc.2268
Webster TMU, Laing LV, Florance H, Santos EM. (2014) Effects of Glyphosate and its Formulation, Roundup, on Reproduction in Zebrafish (Danio rerio). Environ. Sci. Technol. 48 (2), 1271–1279. https://doi.org/10.1021/es404258h
Yusof S, Ismail A, Alias MS. (2014). Effect of glyphosate-based herbicide on early life stages of Java medaka (Oryzias javanicus): a potential tropical test fish. Mar Pollut Bull.;85 (2):494-8. https://doi.org/10.1016/j.marpolbul.2014.03.022
Zanuncio JC et al (2018) Glyphosate-based herbicides toxicity on life history parameters of zoophytophagous Podisus nigrispinus (Heteroptera: Pentatomidae). Ecotoxicol Environ Saf 147:245–250. https://doi.org/10.1016/j.ecoenv.2017.08.055
Zhang S, Xu J, Kuang X, Li S, Li X, Chen D, Zhao X, Feng X (2017) Biological impacts of glyphosate on morphology, embryo biomechanics and larval behavior in zebrafish (Danio rerio). Chemosphere 181:270–280. https://doi.org/10.1016/j.chemosphere.2017.04.094
Zivna D, Plhalova L, Chromcova L, Blahova J, Prokes M, Skoric M, Marsalek P, Praskova E, Stepanova S, Svobodova Z. (2016).The effects of ciprofloxacin on early life stages of common carp (Cyprinus carpio). Environmental Toxicology and Chemistry 35, 17336–1740.
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Fiorino, E., Sehonova, P., Plhalova, L. et al. Effects of glyphosate on early life stages: comparison between Cyprinus carpio and Danio rerio. Environ Sci Pollut Res 25, 8542–8549 (2018). https://doi.org/10.1007/s11356-017-1141-5
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DOI: https://doi.org/10.1007/s11356-017-1141-5