Abstract
Glyphosate levels and the transfer of glyphosate across trophic levels have rarely been studied in zooplankton. The food preferences of zebrafish during the first-feeding stage (which is critical for the survival of organisms), were analyzed because of the requirement for live food. Larval survival begins to be affected when glyphosate intake exceeds 0.3666 µg/larvae/day, in the case that only the food is contaminated; if the medium is also contaminated, the effects on survival start from 0.2456 µg/larvae/day. It was shown that glyphosate was more likely to be incorporated through the medium than through the food (zooplankton), which supports the results of previous studies that have ruled out the potential for biomagnification. The bioconcentration factor (BCF) of glyphosate was determined using an ELISA tests specific to measure glyphosate in the fish D. rerio, the rotifers Brachionus calyciflorus and Lecane papuana, and the cladoceran Ceriodaphnia dubia. The experimental design consisted in exposing seven zebrafish adults per replica (four replicates) in three treatments 1, 5, and 10 mg/L of glyphosate for 96 h to obtain bioconcentration factors in the gills, liver, and muscle. These concentrations were selected as potential glyphosate concentrations right after application as double highest reported concentration. Glyphosate levels in zooplankton can represent up to 6.26% of the total weight of rotifers (BFC = 60.35) and in zebrafish adult organs were less than 8 µg/mg of tissue (BCF values < 6). Although glyphosate does not biomagnify, our results suggest that glyphosate affected the dynamics between zooplankton and zebrafish larvae, diminishing survival and feeding rates, given that zooplankton species bioconcentrate glyphosate in large quantities. The BCF values found in this contribution are higher than expected. Glyphosate exposure affected energy metabolism and feeding behavior of zebrafish larvae, which presented high mortality rates at environmentally relevant concentrations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability and materials
The database generated in the present study are available from corresponding authors on reasonable request.
Code availability
N/A.
References
Aidan Al-Hussieny A, Thijar LA, Faiq A, Sameer Mohammed E (2014) Study of sludge and comparison for various wastewater treatment. Int J Adv Res 2(7):292–304. https://doi.org/10.21474/IJAR01
Annett R, Habibi HR, Hontela A (2014) Impact of glyphosate and glyphosate-based herbicides on the freshwater environment. J Appl Toxicol 34(5):458–479. https://doi.org/10.1002/jat.2997
Arzate-Cárdenas MA, Martínez-Jerónimo F (2012) Energy resource reallocation in Daphnia schodleri (Anomopoda: Daphniidae) reproduction induced by exposure to hexavalent chromium. Chemosphere 87(4):326–332. https://doi.org/10.1016/j.chemosphere.2011.12.014
Bejarano GF (ed) (2018) Los Plaguicidas Altamente Peligrosos en México. Red de Acción sobre Plaguicidas y Alternativas en México, A.C. (RAPAM), Estado de México, México
Best J, James A, Lawrence C, Adatto I, Cockington J (2010) A novel method for rearing first-feeding larval zebrafish: polyculture with type L saltwater rotifers ( Brachionus plicatilis ). Zebrafish 7(3):289–295. https://doi.org/10.1089/zeb.2010.0667
Braz-Mota S, Sadauskas-Henrique H, Duarte RM, Val AL, Almeida-Val VMF (2015) Roundup® exposure promotes gills and liver impairments, DNA damage and inhibition of brain cholinergic activity in the Amazon teleost fish Colossoma macropomum. Chemosphere 135:53–60. https://doi.org/10.1016/j.chemosphere.2015.03.042
Bridi D, Altenhofen S, Gonzalez JB, Reolon GK, Bonan CD (2017) Glyphosate and Roundup® alter morphology and behavior in zebrafish. Toxicology 392(July):32–39. https://doi.org/10.1016/j.tox.2017.10.007
Burkhardt-Holm P, Oulmi Y, Schroeder A, Storch V, Braunbeck T (1999) Toxicity of 4-Chloroaniline in early life stages of zebrafish (Danio rerio): II. Cytopathology and regeneration of liver and gills after prolonged exposure to waterborne 4-chloroaniline. Arch Environ Contam Toxicol 37(1):85–102. https://doi.org/10.1007/s002449900493
Bus JS (2015) Analysis of Moms Across America report suggesting bioaccumulation of glyphosate in U.S. mother’s breast milk: implausibility based on inconsistency with available body of glyphosate animal toxicokinetic, human ´biomonitoring, and physico-chemical data. Regul Toxicol Pharm 73(3):758–764. https://doi.org/10.1016/j.yrtph.2015.10.022
Carbajal-Hernández AL, Valerio-García RC, Martínez-Ruíz EB, Jarquín-Díaz VH, Martínez-Jerónimo F (2017) Maternal-embryonic metabolic and antioxidant response of Chapalichthys pardalis (Teleostei: Goodeidae) induced by exposure to 3,4-dichloroaniline. Environ Sci Pollut Res 24(21):17534–17546. https://doi.org/10.1007/s11356-017-9340-7
Castro-Barrera T (2003) Alimento Vivo Para Organismos Acuáticos, First edit. AGT (ed), Distrito Federal, México
Contardo-Jara V, Klingelmann E, Wiegand C (2009) Bioaccumulation of glyphosate and its formulation Roundup Ultra in Lumbriculus variegatus and its effects on biotransformation and antioxidant enzymes. Environ Pollut 157(1):57–63. https://doi.org/10.1016/j.envpol.2008.07.027
Dey S, Samanta P, Pal S, Mukherjee AK, Kole D, Ghosh AR (2016) Integrative assessment of biomarker responses in teleostean fishes exposed to glyphosate-based herbicide (Excel Mera 71). Emerg Contam 2(4):191–203. https://doi.org/10.1016/j.emcon.2016.12.002
Edwards WM, Triplett GB, Kramer RM (1980) A watershed study of glyphosate transport in runoff. J Environ Qual 9(4):661–665. https://doi.org/10.2134/jeq1980.00472425000900040024x
Ferrario C, Parolini M, De Felice B, Villa S, Finizio A (2018) Linking sub-individual and supra-individual effects in Daphnia magna exposed to sub-lethal concentration of chlorpyrifos. Environ Pollut 235:411–418. https://doi.org/10.1016/j.envpol.2017.12.113
Fiałkowska E, Pajdak-Stós A, Fyda J, Kocerba-Soroka W, Sobczyk M (2016) Lecane tenuiseta (Rotifera, Monogononta) as the best biological tool candidate selected for preventing activated sludge bulking in a cold season. Desalin Water Treat 57(59):28592–28599. https://doi.org/10.1080/19443994.2016.1192565
Fiorino E, Sehonova P, Plhalova L, Blahova J, Svobodova Z, Faggio C (2018) Effects of glyphosate on early life stages: comparison between Cyprinus carpio and Danio rerio. Environ Sci Pollut Res 25(9):8542–8549. https://doi.org/10.1007/s11356-017-1141-5
Forner-Piquer I, Faucherre A, Byram J, Blaquiere M, de Bock F, Gamet-Payrastre L, Ellero-Simatos S, Audinat E, Jopling C, Marchi N (2021) Differential impact of dose-range glyphosate on locomotor behavior, neuronal activity, glio-cerebrovascular structures, and transcript regulations in zebrafish larvae. Chemosphere 267:128986. https://doi.org/10.1016/j.chemosphere.2020.128986
Garza-León CV, Arzate-Cárdenas MA, Rico-Martínez R (2017) Toxicity evaluation of cypermethrin, glyphosate, and malathion, on two indigenous zooplanktonic species. Environ Sci Pollut Res 24(22):18123–18134. https://doi.org/10.1007/s11356-017-9454-y
Hallare A, Nagel K, Köhler HR, Triebskorn R (2006) Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicol Environ Safety 63(3):378–388
Harangi S, Baranyai E, Fehér M, Tóth CN, Herman P, Stündl L, Fábián I, Tóthmérész B, Simon E (2017) Accumulation of metals in juvenile carp (Cyprinus carpio) exposed to sublethal levels of iron and manganese: survival, body weight and tissue. Biol Trace Elem Res 177(1):187–195. https://doi.org/10.1007/s12011-016-0854-5
Hernández-Ruiz E, Alvarado-Flores J, Rubio-Franchini I, Ventura-Juárez J, Rico-Martínez R (2016) Adverse effects and bioconcentration of chromium in two freshwater rotifer species. Chemosphere 58:107–115. https://doi.org/10.1016/j.chemosphere.2016.05.067
IARC (2017) Glyphosate. In: IARC (ed) Some organophosphate insecticides and herbicides, vol 112, 1st edn. World Health Organization, Lyon, pp 321–412
International Standard Organization (2012) ISO 6341:2012 Water quality—determination of the inhibition of the mobility of Daphnia magna Straus (Cladocera, Crustacea)—acute toxicity test. Publishing International Standard Organization https://www.iso.org/obp/ui/#iso:std:iso:6341:ed-4:v1:en. Accessed 9 October 2021
Jansons M, Pugajeva I, Bartkevičs V (2018) Occurrence of glyphosate in beer from the Latvian market. Food Addit Contam A 35(9):1767–1775. https://doi.org/10.1080/19440049.2018.1469051
Jofré DM, Alvarez M, Perez E, Mohamed F, Jerez MB, Juri AM, Enriz RD, Giannini F (2016) Studies of acute and chronic toxicity of commercial herbicides with glyphosate against Danio rerio. J Environ Anal Toxicol 06(01):1–5. https://doi.org/10.4172/2161-0525.1000340
Jofré DM, Garcia MJG, Salcedo R, Morales M, Alvarez M, Enriz D, Giannini F (2013) Fish toxicity of commercial herbicides formulated with glyphosate. J Environ Anal Toxicol 4(1):1–3. https://doi.org/10.4172/2161-0525.1000199
Lanzarin GAB, Félix LM, Santos D, Venâncio CAS, Monteiro SM (2019) Dose-dependent effects of a glyphosate commercial formulation – Roundup® UltraMax - on the early zebrafish embryogenesis. Chemosphere 223:514–522. https://doi.org/10.1016/j.chemosphere.2019.02.071
Kristofco LA, Cruz LC, Haddad SP, Behra ML, Chambliss CK, Brooks BW (2016) Age matters: developmental stage of Danio rerio larvae influences photomotor response thresholds to diazinion or diphenhydramine. Aquat Toxicol 170(1):344–354. https://doi.org/10.1016/j.aquatox.2015.09.011
Lawrence C (2019) Zebrafish larviculture. In: Cartner C, Eisen J, Farmer S, Guillemin K, Kent M, Sanders G (eds) The zebrafish in biomedical research: biology, husbandry, diseases, and research applications. Academic Press, London, pp 365–378
Li M, Ruan L, Zhou J, Fu Y, Jiang L, Zhao H, Wang J (2017) Metabolic profiling of goldfish (Carassius auratus) after long-term glyphosate- based herbicide exposure. Aquat Toxicol 188(May):159–169. https://doi.org/10.1016/j.aquatox.2017.05.004
Martínez-Jerónimo F, Arzate-Cárdenas M, Ortiz-Butrón R (2013) Linking sub-individual and population level toxicity effects in Daphnia schoedleri (Cladocera: Anomopoda) exposed to sublethal concentrations of the pesticide α-cypermethrin. Ecotoxicology 22(6):985–995. https://doi.org/10.1007/s10646-013-1077-6
Miyasaka N, Wanner AA, Li J, Mack-Bucher J, Genoud C, Yoshihara Y, Friedrich RW (2013) Functional development of the olfactory system in zebrafish. Mech Dev 130(6–8):336–346. https://doi.org/10.1016/j.mod.2012.09.001
Moreira LF, Sandrini JZ, Marques SM (2018) Toxicity induced by glyphosate and glyphosate-based herbicides in the zebrafish hepatocyte cell line (ZF-L). Ecotoxicol Environ Saf 162:201–207. https://doi.org/10.1016/j.ecoenv.2018.07.005
National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. National Academies Press, Washington, D.C
OECD (2013) Test No. 236: Fish Embryo Acute Toxicity (FET) Test. Publishing OECD Library. http://www.oecd-ilibrary.org/environment/test-no-236-fish-embryo-acute-toxicity-fet-test_9789264203709-en. Accessed 9 October 2021
OECD (2019) Test Guideline No. 203 Fish, acute toxicity testing. Publishing OECD Library. https://www.oecd-ilibrary.org/environment/test-no-203-fish-acute-toxicity-test_9789264069961-en. Accessed 9 October 2021
Osorio-Treviño OC, Arzate-Cárdenas MA, Rico-Martínez R (2019) Energy budget in Alona guttata (Chydoridae: Aloninae) and toxicant-induced alterations. J Environ Sci Health A 54(5):398–407. https://doi.org/10.1080/10934529.2018.1558901
Panetto OS, Gomes HF, Fraga Gomes DS, Campos E, Romeiro NC, Costa EP, do Carmo PRL, Feitosa NM, Moraes J (2019) The effects of Roundup® in embryo development and energy metabolism of the zebrafish (Danio rerio). Comp Biochem Phys C 222(November 2018):74–81. https://doi.org/10.1016/j.cbpc.2019.04.007
Pekkan K, Chang B, Uslu F, Mani K, Chen CY, Holzman R (2016) Characterization of zebrafish larvae suction feeding flow using μPIV and optical coherence tomography. Exp Fluids 57(7):1–7. https://doi.org/10.1007/s00348-016-2197-6
Pérez DJ, Okada E, Menone ML, Costa JL (2017) Can an aquatic macrophyte bioaccumulate glyphosate? Development of a new method of glyphosate extraction in Ludwigia peploides and watershed scale validation. Chemosphere 185:975–982. https://doi.org/10.1016/j.chemosphere.2017.07.093
Persch TSP, Weimer RN, Freitas BS, Oliveira GT (2017) Metabolic parameters and oxidative balance in juvenile Rhamdia quelen exposed to rice paddy herbicides: Roundup®, Primoleo®, and Facet®. Chemosphere 174:98–109. https://doi.org/10.1016/j.chemosphere.2017.01.092
Rodríguez-Estrada J, Sobrino-Figueroa AS, Martínez-Jerónimo F (2016) Effect of sublethal α-cypermethrin exposure on main macromolecules concentration, energy content, and malondialdehyde concentration in free-feeding Danio rerio larvae. Fish Physiol Biochem 42(3):859–868. https://doi.org/10.1007/s10695-015-0180-4
Sancho JV, Hernández F, López FJ, Hogendoorn EA, Dijkman E, Van Zoonen P (1996) Rapid determination of glufosinate, glyphosate and aminomethylphosphonic acid in environmental water samples using precolumn fluorogenic labeling and coupled-column liquid chromatography. J Chromatogr A 737(1):75–83. https://doi.org/10.1016/0021-9673(96)00071-4
Sanden M, Jørgensen S, Hemre GI, Ørnsrud R, Sissener NH (2012) Zebrafish (Danio rerio) as a model for investigating dietary toxic effects of deoxynivalenol contamination in aquaculture feeds. Food Chem Toxicol 50(12):4441–4448. https://doi.org/10.1016/j.fct.2012.08.042
Székács A, Darvas B (2018) Re-registration challenges of glyphosate in the European Union. Front Environ Sci 6:78. https://doi.org/10.3389/fenvs.2018.00078
Sulukan E, Köktürk M, Ceylan H, Beydemir S, Işik M, Atamanalp M, Ceyhun SB (2017) An approach to clarify the effect mechanism of glyphosate on body malformations during embryonic development of zebrafish (Danio 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
United States Environmental Protection Agency (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms Fifth Edition October 2002
Uren Webster TM, Santos EM (2015) Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup. BMC Genomics 16(32):1–14. https://doi.org/10.1186/s12864-015-1254-5
Uren Webster TM, 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
Vannini A, Guarnieri M, Paoli L, Sorbo S, Basile A, Loppi S (2016) Bioaccumulation, physiological and ultrastructural effects of glyphosate in the lichen Xanthoria parietina (L.) Th. Fr. Chemosphere 164:233–240. https://doi.org/10.1016/j.chemosphere.2016.08.058
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
Acknowledgements
This contribution is part of the PhD thesis of GBAS that was supported by Consejo Nacional de Ciencia y Tecno1logía, CONACyT (No. 666012) and project (CB2016 288306). Authors thank the Sistema Nacional de Investigadores and Cátedras CONACYT for their support. We thank Andrea Lievana MacTavish for English language editing.
Funding
This work was supported by the Consejo Nacional de Ciencia y Tecnología CONACYT [grant numbers CB2016 288306 and doctoral scholarship 666012], and Institutional projects (UAA, PIT17-4, and PIT19-4).
Author information
Authors and Affiliations
Contributions
GBAS: conceptualization, investigation, writing-original draft, formal analysis, data curation, methology, writing—review and editing; MSB: conceptualization, writing—review and editing; MAAC: investigation, formal analysis, writing—review and editing; ALCH: investigation, methodology, writing—review and editing; BYR: conceptualization, funding acquisition, writing—review and editing, supervision; RRM: conceptualization, funding acquisition, writing—review and editing, supervision. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethics approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. In the case of Dario rerio methodology, the Bioethical Committee of the Universidad Autónoma de Aguascalientes approved these procedures.
Consent to participate
N/A
Consent for publication
N/A
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Bruno Nunes
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Beatriz Yáñez-Rivera and Roberto Rico-Martínez are both PhD thesis co-directors of Gabriela Beatriz Alvarado-Suárez.
Electronic Supplementary Material
ESM 1
(DOCX 276 kb)
Rights and permissions
About this article
Cite this article
Alvarado-Suárez, G.B., Silva-Briano, M., Arzate-Cárdenas, M.A. et al. Feeding behavior of early life stages of the zebrafish Danio rerio is altered by exposure to glyphosate. Environ Sci Pollut Res 29, 85172–85184 (2022). https://doi.org/10.1007/s11356-022-21790-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-21790-x