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Glyphosate toxicity for animals

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Abstract

Pesticides and herbicides gained popularity due to a strong need to curb the starvation of billions of humans. Glyphosate is the most commonly used herbicide and was considered to be non-toxic. But its use in excess in agricultural lands has polluted soils and waters. Nowadays, glyphosate residues are found in soil, water and food. As a result glyphosate causes severe acute and chronic toxicological effects. We review toxicological effects of glyphosate and metabolites on organisms of the kingdom animalia, both unicellular and multicellular organisms. Adverse effects on unicellular organisms have been established in many experiments. For instance, glyphosate has reduced the rate of photosynthesis in Euglena, has decreased the radial growth of mycorrhizal fungal species and is also reducing the profusion of certain bacteria present in rhizospheric microbial communities. Glyphosate poses serious threat to multicellular organisms as well. Its toxicological effects have been traced from lower invertebrates to higher vertebrates. Effects have been observed in annelids (earthworms), arthropods (crustaceans and insects), mollusks, echinoderms, fish, reptiles, amphibians and birds. Toxicological effects like genotoxicity, cytotoxicity, nuclear aberration, hormonal disruption, chromosomal aberrations and DNA damage have also been observed in higher vertebrates like humans.

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Fig. 1

Data from Benbrooke (2016)

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References

  • Achiorno CL, de Villalobos C, Ferrari L (2008) Toxicity of the herbicide glyphosate to Chordodes nobilii (Gordiida, Nematomorpha). Chemosphere 71(10):1816–1822. https://doi.org/10.1016/j.chemosphere.2008.02.001

    Article  CAS  Google Scholar 

  • Alberdi JL, Saenz ME, Di Marzio WD, Tortorelli MC (1996) Comparative acute toxicity of two herbicides, paraquat and glyphosate, to Daphnia magna and D. spinulata. Bull Environ Contam Toxicol 57(2):229–235. https://doi.org/10.1007/s00128990018

    Article  CAS  Google Scholar 

  • Alliance GT (1996) Glyphosphate Fact Sheet. (Pesticides News No.33, Sept 1996, pp 28–29). http://www.ernslaw.co.nz/assets/resources-contractors/HealthSafety/Chemical-Fact-Sheets/Glyphosate-fact-sheet-PAN-UK-1996.pdf

  • Al-Rajab AJ, Amellal S, Schiavon M (2008) Sorption and leaching of 14C-glyphosate in agricultural soils. Agron Sustain Dev 28(3):419–428. https://doi.org/10.1051/agro:2008014

    Article  CAS  Google Scholar 

  • Austin AP, Harris GE, Lucey WP (1991) Impact of an organophosphate herbicide (glyphosate) on periphyton communities developed in experimental streams. Bull Environ Contam Toxicol 47(1):29–35. https://doi.org/10.1007/BF01689449

    Article  CAS  Google Scholar 

  • Avigliano L, Fassiano AV, Medesani DA, De Molina MR, Rodríguez EM (2014) Effects of glyphosate on growth rate, metabolic rate and energy reserves of early juvenile crayfish, Cherax quadricarinatus M. Bull Environ Contam Toxicol 92(6):631–635. https://doi.org/10.1007/s00128-014-1240-7

    Article  CAS  Google Scholar 

  • Bach NC, Natale GS, Somoza GM, Ronco AE (2016) Effect on the growth and development and induction of abnormalities by a glyphosate commercial formulation and its active ingredient during two developmental stages of the South-American Creole frog, Leptodactylus latrans. Environ Sci Pollut Res 23(23):23959–23971

    Article  CAS  Google Scholar 

  • Balbuena MS, Tison L, Hahn ML, Greggers U, Menzel R, Farina WM (2015) Effects of sublethal doses of glyphosate on honeybee navigation. J Exp Biol 218(17):2799–2805. https://doi.org/10.1242/jeb.117291

    Article  Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28(1):3. https://doi.org/10.1186/s12302-016-0070-0

    Article  CAS  Google Scholar 

  • Boily M, Sarrasin B, DeBlois C, Aras P, Chagnon M (2013) Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environ Sci Pollut Res 20(8):5603–5614

    Article  CAS  Google Scholar 

  • Bradberry SM, Proudfoot AT, Vale JA (2004) Glyphosate poisoning. Toxicol Rev 23(3):159–167

    Article  CAS  Google Scholar 

  • Bueno ADF, Bueno RCODF, Parra JRP, Vieira SS (2008) Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Cienc Rural 38(6):1495–1503. https://doi.org/10.1590/S0103-84782008000600001

    Article  CAS  Google Scholar 

  • Burlew DA (2010) The effects of pesticide-contaminated pollen on larval development of the honey bee, Apis mellifera (Doctoral dissertation, Evergreen State College)

  • Carpenter JK, Monks JM, Nelson N (2016) The effect of two glyphosate formulations on a small, diurnal lizard (Oligosoma polychroma). Ecotoxicology 25(3):548–554. https://doi.org/10.1007/s10646-016-1613-2

    Article  CAS  Google Scholar 

  • Casabe N, Piola L, Fuchs J, Oneto ML, Pamparato L, Basack S, Kesten E (2007) Ecotoxicological assessment of the effects of glyphosate and chlorpyrifos in an Argentine soya field. J Soils Sediments 7(4):232–239. https://doi.org/10.1065/jss2007.04.224

    Article  CAS  Google Scholar 

  • Cattaneo R, Clasen B, Loro VL, de Menezes CC, Pretto A, Baldisserotto B, Santi A, de Avila LA (2011) Toxicological responses of Cyprinus carpio exposed to a commercial formulation containing glyphosate. Bull Environ Contam Toxicol 87(6):597–602. https://doi.org/10.1007/s00128-011-0396-7

    Article  CAS  Google Scholar 

  • CCM International (2011) Outlook for China Glyphosate Industry 2012–2016. http://www.researchandmarkets.com/reports/2101356/outlook for china glyphosate industry 201122016

  • Cerdeira AL, Gazziero DL, Duke SO, Matallo MB (2011) Agricultural impacts of glyphosate-resistant soybean cultivation in South America. J Agric Food Chem 59(11):5799–5807. https://doi.org/10.1021/jf102652y

    Article  CAS  Google Scholar 

  • Chakravarty P, Sidhu SS (1987) Effect of glyphosate, hexazinone and triclopyr on in vitro growth of five species of ectomycorrhizal fungi. Eur J For Pathol 17(4–5):204–210

    Article  CAS  Google Scholar 

  • Christian FA, Jackson RN, Tate TM (1993) Effect of sublethal concentrations of glyphosate and dalapon on protein and aminotransferase activity in Pseudosuccinea columella. Bull Environ Contam Toxicol 51:703–709

    Article  CAS  Google Scholar 

  • Correia FV, Moreira JC (2010) Effects of glyphosate and 2, 4-D on earthworms (Eisenia foetida) in laboratory tests. Bull Environ Contam Toxicol 85(3):264–268

    Article  CAS  Google Scholar 

  • Cuhra M, Traavik T, Bohn T (2013) Clone-and age-dependent toxicity of a glyphosate commercial formulation and its active ingredient in Daphnia magna. Ecotoxicology 22(2):251–262

    Article  CAS  Google Scholar 

  • Dallegrave E, Mantese FD, Oliveira RT, Andrade AJ, Dalsenter PR, Langeloh A (2007) Pre-and postnatal toxicity of the commercial glyphosate formulation in Wistar rats. Arch Toxicol 81(9):665–673

    Article  CAS  Google Scholar 

  • Datta S, Singh J, Singh S, Singh J (2016) Earthworms, pesticides and sustainable agriculture: a review. Environ Sci Pollut Res 23(9):8227–8243

    Article  Google Scholar 

  • De Souza Filho J, Sousa CCN, Da Silva CC, De Saboia-Morais SMT, Grisolia CK (2013) Mutagenicity and genotoxicity in gill erythrocyte cells of Poecilia reticulata exposed to a glyphosate formulation. Bull Environ Contam Toxicol 91(5):583–587

    Article  CAS  Google Scholar 

  • Dick RE, Quinn JP (1995) Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl Microbiol Biotechnol 43(3):545–550. https://doi.org/10.1007/BF00218464

    Article  CAS  Google Scholar 

  • Domínguez A, Brown GG, Sautter KD, de Oliveira CMR, de Vasconcelos EC, Niva CC, Bedano JC (2016) Toxicity of AMPA to the earthworm Eisenia andrei Bouché, 1972 in tropical artificial soil. Sci Rep. https://doi.org/10.1038/srep19731

    Article  Google Scholar 

  • Dominguez-Cortinas G, Saavedra JM, Santos-Medrano GE, Rico-Martínez R (2008) Analysis of the toxicity of glyphosate and Faena® using the freshwater invertebrates Daphnia magna and Lecane quadridentata. Toxicol Environ Chem 90(2):377–384

    Article  CAS  Google Scholar 

  • Dornelles MF, Oliveira GT (2016) Toxicity of atrazine, glyphosate, and quinclorac in bullfrog tadpoles exposed to concentrations below legal limits. Environ Sci Pollut Res 23(2):1610–1620

    Article  CAS  Google Scholar 

  • Druart C, Millet M, Scheifler R, Delhomme O, De Vaufleury A (2011) Glyphosate and glufosinate-based herbicides: fate in soil, transfer to, and effects on land snails. J Soils Sediments 11(8):1373–1384

    Article  CAS  Google Scholar 

  • Duke SO, Powles SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64(4):319–325. https://doi.org/10.1002/ps.1518

    Article  CAS  Google Scholar 

  • Duke SO, Lydon J, Koskinen WC, Moorman TB, Channey RL, Hammerschmidt R (2012) Glyphosate effects on plant mineral nutrition, crop rhizosphere microbiota and plant disease in glyphosate-resistant crops. J Agric Food Chem 60(42):10375–10397. https://doi.org/10.1021/jf302436u

    Article  CAS  Google Scholar 

  • Dutra BK, Fernandes FA, Failace DM, Oliveira GT (2011) Effect of Roundup (glyphosate formulation) in the energy metabolism and reproductive traits of Hyalella castroi (Crustacea, Amphipoda, Dogielinotidae). Ecotoxicology 20(1):255–263

    Article  CAS  Google Scholar 

  • Estok D, Freedman B, Boyle D (1989) Effects of the herbicides 2, 4-D, glyphosate, hexazinone, and triclopyr on the growth of three species of ectomycorrhizal fungi. Bull Environ Contam Toxicol 42(6):835–839

    Article  CAS  Google Scholar 

  • Fishel FM, Ferrell JA (2013) Managing pesticide drift. Agronomy Department, PI232 University of Florida, Gainesville, FL, USA

  • Folmar LC, Sanders HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environ Contam Toxicol 8(3):269–278

    Article  CAS  Google Scholar 

  • Forest info.ca. http://forestinfo.ca/faqs/what-are-the-effects-of-glyphosate-based-herbicides-on-wildlife-species-such-as-small-mammals-or-birds/

  • Franz JE, Mao MK, Sikorski JA (1997) Glyphosate: a unique global herbicide. American Chemical Society, Washington, DC, p 653

    Google Scholar 

  • Frontera JL, Vatnick I, Chaulet A, Rodríguez EM (2011) Effects of glyphosate and polyoxyethylenamine on growth and energetic reserves in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Arch Environ Contam Toxicol 61(4):590–598

    Article  CAS  Google Scholar 

  • García-Torre T, Giuffre L, Romaniuk R, Rios RP, Pagano EA (2014) Exposure assessment to glyphosate of two species of annelids. Bull Environ Contam Toxicol 93(2):209–214

    Article  CAS  Google Scholar 

  • Garthwaite D, Barker I, Parrish G, Smith L, Chippindale C, Pietravalle S (2010) Pesticide usage survey report 235: Arable crops in the United Kingdom. https://secure.fera.defra.gov.uk/pusstats/surveys/documents/arable2010V2.pdf

  • Gasnier C, Dumont C, Benachour N, Clair E, Chagnon M-C, Séralini G-E (2009) Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262:184–191

    Article  CAS  Google Scholar 

  • Gaupp-Berghausen M, Hofer M, Rewald B, Zaller JG (2015) Glyphosate-based herbicides reduce the activity and reproduction of earthworms and lead to increased soil nutrient concentrations. Sci Rep 5:12886

    Article  CAS  Google Scholar 

  • Geiger DR, Shieh WJ, Fuchs MA (1999) Causes of self-limited translocation of glyphosate in Beta vulgaris plants. Pest Biochem Physiol 64(2):124–133

    Article  CAS  Google Scholar 

  • Gill JPK, Sethi N, Mohan A (2017) Analysis of the glyphosate herbicide in water, soil and food using derivatising agents. Environ Chem Lett 15(1):85–100

    Article  CAS  Google Scholar 

  • Glyphosate report By Pesticide Action Network Asia and the Pacific November 2009. http://www.national-toxic-encephalopathy-foundation.org/roundup.pdf

  • Goldsborough LG, Brown DJ (1988) Effect of glyphosate (Roundup® formulation) on periphytic algal photosynthesis. Bull Environ Contam Toxicol 41(2):253–260

    Article  CAS  Google Scholar 

  • Gonzalez EL, Latorre MA, Larriera A, Siroski PA, Poletta GL (2013) Induction of micronuclei in broad snouted caiman (Caiman latirostris) hatchlings exposed in vivo to Roundup (glyphosate) concentrations used in agriculture. Pest Biochem Physiol 105(2):131–134

    Article  CAS  Google Scholar 

  • Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pest Biochem Physiol 99(2):200–207

    Article  CAS  Google Scholar 

  • Hartman WA, Martin DB (1984) Effect of suspended Bentonite clay on the acute toxicity of glyphosate to Daphnia pulex and Lemna minor. Bull Environ Contam Toxicol 33(1):355–361

    Article  CAS  Google Scholar 

  • Henderson AM, Gervais JA, Luukinen B, Buhl K, Stone D (2010) Glyphosate Technical Fact Sheet; National Pesticide Information Center, Oregon State University Extension Services. http://npic.orst.edu/factsheets/archive/glyphotech.html

  • Herbert LT, Vazquez DE, Arenas A, Farina WM (2014) Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J Exp Biol 217(19):3457–3464

    Article  Google Scholar 

  • Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N (2004) Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Chem 23(8):1928–1938

    Article  CAS  Google Scholar 

  • Hued AC, Oberhofer S, de los Ángeles Bistoni M (2012) Exposure to a commercial glyphosate formulation (Roundup®) alters normal gill and liver histology and affects male sexual activity of Jenynsia multidentata (Anablepidae, Cyprinodontiformes). Arch Environ Contam Toxicol 62(1):107–117

    Article  CAS  Google Scholar 

  • Jacob GS, Schaefer J, Stejskal EO, McKay RA (1985) Solid-state NMR determination of glyphosate metabolism in a Pseudomonas sp. J Biol Chem 260(10):5899–5905

    CAS  Google Scholar 

  • Johnson WG, Davis VM, Kruger GR, Weller SC (2009) Influence of glyphosate-resistant cropping systems on weed species shifts and glyphosate-resistant weed populations. Eur J Agron 31(3):162–172. https://doi.org/10.1016/j.eja.2009.03.008

    Article  CAS  Google Scholar 

  • joint FAO/WHO Meeting on Pesticide Residues, Geneva (2016) Summary Report: 1-6. http://www.who.int/foodsafety/jmprsummary2016.pdf

  • Kirkwood RC, Hetherington R, Reynolds TL, Marshall G (2000) Absorption, localisation, translocation and activity of glyphosate in barnyardgrass (Echinochloa crus-galli (L) Beauv): influence of herbicide and surfactant concentration. Pest Manag Sci 56(4):359–367

    Article  CAS  Google Scholar 

  • Kittle RP, McDermid KJ (2016) Glyphosate herbicide toxicity to native Hawaiian macroalgal and seagrass species. J Appl Phycol 28(4):2597–2604

    Article  CAS  Google Scholar 

  • Koller VJ, Fürhacker M, Nersesyan A, Misik M, Eisenbauer M, Knasmueller S (2012) Cytotoxic and DNA-damaging properties of glyphosate and Roundup in human-derived buccal epithelial cells. Arch Toxicol 86(5):805–813

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Attademo AM, Peltzer PM, Junges CM, Cabagna MC (2011) Toxicity of four herbicide formulations with glyphosate on Rhinella arenarum (Anura: Bufonidae) tadpoles: B-esterases and glutathione S-transferase inhibitors. Arch Environ Contam Toxicol 60(4):681–689

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Attademo AM, Simoniello MF, Poletta GL, Junges CM, Peltzer PM, Cabagna-Zenklusen MC (2015) Harmful effects of the dermal intake of commercial formulations containing chlorpyrifos, 2, 4-D and glyphosate on the common toad Rhinella arenarum (Anura: Bufonidae). Water Air Soil Pollut 226(12):427

    Article  CAS  Google Scholar 

  • Lane M, Lorenz N, Saxena J, Ramsier C, Dick RP (2012) The effect of glyphosate on soil microbial activity, microbial community structure, and soil potassium. Pedobiologia 55(6):335–342. https://doi.org/10.1016/j.pedobi.2012.08.001

    Article  CAS  Google Scholar 

  • Latorre MA, Lopez González EC, Larriera A, Poletta GL, Siroski PA (2013) Effects of in vivo exposure to Roundup® on immune system of Caiman latirostris. J Immuno Toxicol 10(4):349–354

    Article  CAS  Google Scholar 

  • Lee HL, Kan D, Tsai CL, Liou MJ, Guo HR (2009) Comparative effects of the formulation of glyphosate-surfactant herbicides on hemodynamics in swine. Clin Toxicol 47(7):651–658

    Article  Google Scholar 

  • Linz GM, Blixt DC, Bergman DL, Bleier WJ (1996) Responses of red-winged blackbirds, yellow-headed blackbirds and marsh wrens to glyphosate-induced alterations in cattail density (Respuesta de Agelaius phoeniceus, Xanthocephalus xanthocephalus y Cistothorus palustris a Alteración en la Densidad de Eneas Tratadas con Yerbicidas. J Field Ornithol 167–176

  • Liu CM, McLean PA, Sookdeo CC, Cannon FC (1991) Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl Environ Microbiol 57(6):1799–1804

    CAS  Google Scholar 

  • Mamy L, Barriuso E (2007) Desorption and time-dependent sorption of herbicides in soils. Eur J Soil Sci 58(1):174–187

    Article  CAS  Google Scholar 

  • Manas F, Peralta L, Raviolo J, Ovando HG, Weyers A, Ugnia L, Gorla N (2009) Genotoxicity of glyphosate assessed by the comet assay and cytogenetic tests. Environ Toxicol Pharmacol 28(1):37–41

    Article  CAS  Google Scholar 

  • Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Arch Environ Contam Toxicol 36(2):193–199

    Article  CAS  Google Scholar 

  • Marc J, Mulner‐Lorillon O, Belle R (2004) Glyphosate‐based pesticides affect cell cycle regulation. Biol Cell 96(3):245–249

    Article  CAS  Google Scholar 

  • Marc J, Le Breton M, Cormier P, Morales J, Belle R, Mulner-Lorillon O (2005) A glyphosate-based pesticide impinges on transcription. Toxicol Appl Pharmacol 203(1):1–8

    Article  CAS  Google Scholar 

  • Martini CN, Gabrielli M, Codesido MM, Del Vila MC (2016) Glyphosate-based herbicides with different adjuvants are more potent inhibitors of 3T3-L1 fibroblast proliferation and differentiation to adipocytes than glyphosate alone. Comp Clin Path 25(3):607–613

    Article  CAS  Google Scholar 

  • McAuliffe KS, Hallas LE, Kulpa CF (1990) Glyphosate degradation by Agrobacterium radiobacter isolated from activated sludge. J Ind Microbiol 6(3):219–221. https://doi.org/10.1007/BF01577700

    Article  CAS  Google Scholar 

  • Menéndez-Helman RJ, Ferreyroa GV, dos Santos Afonso M, Salibián A (2012) Glyphosate as an acetylcholinesterase inhibitor in Cnesterodon decemmaculatus. Bull Environ Contam Toxicol 88(1):6–9

    Article  CAS  Google Scholar 

  • Mesnage R, Bernay B, Seralini GE (2013) Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity. Toxicology 313(2):122–128

    Article  CAS  Google Scholar 

  • Monsanto International and Monsanto Europe (2010) The agronomic benefits of glyphosate in Europe—benefits of glyphosate per market use. Review 1–82. https://monsanto.com/app/uploads/.../agronomic-benefits-of-glyphosate-in-europe.pdf

  • Moore JK, Braymer HD, Larson AD (1983) Isolation of a Pseudomonas sp. which utilizes the phosphonate herbicide glyphosate. Appl Environ Microbiol 46(2):316–320

    CAS  Google Scholar 

  • Murussi CR, Costa MD, Leitemperger JW, Guerra L, Rodrigues CC, Menezes CC, Severo ES, Flores-Lopes F, Salbego J, Loro VL (2016) Exposure to different glyphosate formulations on the oxidative and histological status of Rhamdia quelen. Fish Physiol Biochem 42(2):445–455

    Article  CAS  Google Scholar 

  • Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG, Vandenberg LN (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Health 15(1):19. https://doi.org/10.1186/s12940-016-0117-0

    Article  CAS  Google Scholar 

  • Nedelkoska TV, Low GC (2004) High-performance liquid chromatographic determination of glyphosate in water and plant material after pre-column derivatisation with 9-fluorenylmethyl chloroformate. Anal Chim Acta 511(1):145–153. https://doi.org/10.1016/j.aca.2004.01.027

    Article  CAS  Google Scholar 

  • Neskovic NK, Poleksic V, Elezovic 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

    Article  CAS  Google Scholar 

  • Newman MM, Hoilett N, Lorenz N, Dick RP, Liles MR, Ramsier C, Kloepper JW (2016) Glyphosate effects on soil rhizosphere-associated bacterial communities. Sci Total Environ 543:155–160

    Article  CAS  Google Scholar 

  • Obojska A, Lejczak B, Kubrak M (1999) Degradation of phosphonates by streptomycete isolates. Appl Microbiol Biotechnol 51(6):872–876. https://doi.org/10.1007/s002530051476

    Article  CAS  Google Scholar 

  • Oliveira AG, Telles LF, Hess RA, Mahecha GA, Oliveira CA (2007) Effects of the herbicide Roundup on the epididymal region of drakes Anas platyrhynchos. Reprod Toxicol 23(2):182–191

    Article  CAS  Google Scholar 

  • Oliveira RD, Boas LK, Branco CC (2016) Assessment of the potential toxicity of glyphosate-based herbicides on the photosynthesis of Nitella microcarpa var. wrightii (Charophyceae). Phycologia 55(5):577–584

    Article  CAS  Google Scholar 

  • Osteen CD, Fernandez-Cornejo J (2013) Economic and policy issues of US agricultural pesticide use trends. Pest Manag Sci 69(9):1001–1025

    Article  CAS  Google Scholar 

  • Padgette SR, Re DB, Barry GF, Eichholtz DE, Delannay X, Fuchs RL, Fraley RT (1996) New weed control opportunities: development of soybeans with a Roundup Ready™ gene. Herbic Resist Crops 53–84

  • Pérez GL, Vera MS, Miranda L (2011) Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. In: Herbicides and environment. InTech

  • Pérez-Iglesias JM, Franco-Belussi L, Moreno L, Tripole S, de Oliveira C, Natale GS (2016) Effects of glyphosate on hepatic tissue evaluating melanomacrophages and erythrocytes responses in neotropical anuran Leptodactylus latinasus. Environ Sci Pollut Res 23(10):9852–9861

    Article  CAS  Google Scholar 

  • Piola L, Fuchs J, Oneto ML, Basack S, Kesten E, Casabe N (2013) Comparative toxicity of two glyphosate-based formulations to Eisenia andrei under laboratory conditions. Chemosphere 91(4):545–551

    Article  CAS  Google Scholar 

  • Pipke R, Amrhein N (1988) Degradation of the phosphonate herbicide glyphosate by Arthrobacter atrocyaneus ATCC 13752. Appl Environ Microbiol 54(5):1293–1296

    CAS  Google Scholar 

  • Pipke R, Amrhein N, Jacob GS, Schaefer J, Kishore GM (1987) Metabolism of glyphosate in an Arthrobacter sp. GLP-1. Eur J Biochem 165(2):267–273. https://doi.org/10.1111/j.1432-1033.1987.tb11437.x

    Article  CAS  Google Scholar 

  • Poletta GL, Larriera A, Kleinsorge E, Mudry MD (2009) Genotoxicity of the herbicide formulation Roundup®(glyphosate) in broad-snouted caiman (Caiman latirostris) evidenced by the Comet assay and the Micronucleus test. Mutat Res, Genet Toxicol Environ Mutagen 672(2):95–102

    Article  CAS  Google Scholar 

  • Pollegioni L, Schonbrunn E, Siehl D (2011) Molecular basis of glyphosate resistance—different approaches through protein engineering. FEBS J 278(16):2753–2766

    Article  CAS  Google Scholar 

  • Riah W, Laval K, Laroche-Ajzenberg E, Mougin C, Latour X, Trinsoutrot-Gattin I (2014) Effects of pesticides on soil enzymes: a review. Environ Chem Lett 12(2):257–273. https://doi.org/10.1007/s10311-014-0458-2001

    Article  CAS  Google Scholar 

  • Richard S, Moslemi S, Sipahutar H, Benachour N, Seralini GE (2005) Differential effects of glyphosate and roundup on human placental cells and aromatase. Environ Health Perspect 113(6):716

    Article  CAS  Google Scholar 

  • Richardson JT, Frans RE, Talbert RE (1979) Reactions of Euglena gracilis to fluometuron, MSMA, metribuzin, and glyphosate. Weed Sci 27(6):619–624

    CAS  Google Scholar 

  • Romano RM, Romano MA, Bernardi MM, Furtado PV, Oliveira CAD (2010) Prepubertal exposure to commercial formulation of the herbicide glyphosate alters testosterone levels and testicular morphology. Arch Toxicol 84(4):309–317

    Article  CAS  Google Scholar 

  • Saenz ME, Di Marzio WD, Alberdi JL, del Carmen Tortorelli M (1997) Effects of technical grade and a commercial formulation of glyphosate on algal population growth. Bull Environ Contam Toxicol 59(4):638–644

    Article  CAS  Google Scholar 

  • Salbego J, Pretto A, Gioda CR, de Menezes CC, Lazzari R, Neto JR, Baldisserotto B, Loro VL (2010) Herbicide formulation with glyphosate affects growth, acetylcholinesterase activity, and metabolic and hematological parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 58(3):740–745

    Article  CAS  Google Scholar 

  • Samsel A, Seneff S (2013) Glyphosate’s suppression of cytochrome P450 enzymes and amino acid biosynthesis by the gut microbiome: pathways to modern diseases. Entropy 15(4):1416–1463

    Article  CAS  Google Scholar 

  • Sansom M (2012) Glyphosate use in the amenity sector. Presentation by Monsanto to the AmenityForum. http://www.amenityforum.co.uk/downloads/Presentations/GLYPHOSATE%20USE%20IN%20THE%20AMENITY%20SECTOR%20Nov%202012%20MSansom.pdf

  • Santadino M, Coviella C, Momo F (2014) Glyphosate sublethal effects on the population dynamics of the earthworm Eisenia fetida (Savigny, 1826). Water Air Soil Pollut 225(12):2207

    Article  CAS  Google Scholar 

  • Santillo DJ, Brown PW, Leslie Jr DM (1989) Response of songbirds to glyphosate-induced habitat changes on clearcuts. J Wildl Manag 64–71

  • Santos MJG, Ferreira MFL, Cachada A, Duarte AC, Sousa JP (2012) Pesticide application to agricultural fields: effects on the reproduction and avoidance behaviour of Folsomia candida and Eisenia andrei. Ecotoxicology 21(8):2113–2122

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shehata AA, Schrödl W, Aldin AA, Hafez HM, Krüger M (2013) The effect of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro. Curr Microbiol 66(4):350–358

    Article  CAS  Google Scholar 

  • Siehl DL (1997) Inhibitors of EPSP synthase, glutamine synthetase and histidine synthesis. Rev Toxicol 1:37–68

    CAS  Google Scholar 

  • Sinhorin VD, Sinhorin AP, Teixeira JM, Miléski KM, Hansen PC, Moeller PR, Moreira PS, Baviera AM, Loro VL (2014) Metabolic and behavior changes in surubim acutely exposed to a glyphosate-based herbicide. Arch Environ Contam Toxicol 67(4):659–667

    Article  CAS  Google Scholar 

  • Siroski PA, Poletta GL, Latorre MA, Merchant ME, Ortega HH, Mudry MD (2016) Immunotoxicity of commercial-mixed glyphosate in broad snouted caiman (Caiman latirostris). Chem Biol Interact 244:64–70

    Article  CAS  Google Scholar 

  • Soloneski S, de Arcaute CR, Larramendy ML (2016) Genotoxic effect of a binary mixture of dicamba-and glyphosate-based commercial herbicide formulations on Rhinella arenarum (Hensel, 1867) (Anura, Bufonidae) late-stage larvae. Environ Sci Pollut Res 23(17):17811–17821

    Article  CAS  Google Scholar 

  • Steinmann HH, Dickeduisberg M, Theusen L (2012) Uses and benefits of glyphosate in German arable farming. Crop Prot 42:164–169. https://doi.org/10.1016/j.cropro.2012.06.015

    Article  CAS  Google Scholar 

  • Sullivan DS, Sullivan TP, Bisalputra T (1981) Effects of Roundup herbicide on diatom populations in the aquatic environment of a coastal forest. Bull Environ Contam Toxicol 26(1):91–96

    Article  CAS  Google Scholar 

  • Szekacs I, Fejes A, Klatyik S, Takacs E, Patko D, Pomóthy J, Szekacs A (2014) Environmental and toxicological impacts of glyphosate with its formulating adjuvant. Int J Biol Vet Agric Food Eng 8(3):212–218

    Google Scholar 

  • Tate TM, Spurlock JO, Christian FA (1997) Effect of glyphosate on the development of Pseudosuccinea columella snails. Arch Environ Contam Toxicol 33(3):286–289

    Article  CAS  Google Scholar 

  • Taylor EL, Holley AG, Kirk M (2007) Pesticide development: a brief look at the history. Southern Regional Extension Forestry, Athens, GA

    Google Scholar 

  • The environmental impacts of glyphosate—Friends of the Earth Europe (2013). https://www.foeeurope.org/sites/…/foee_5_environmental_impacts_glyphosate.pdf

  • Thongprakaisang S, Thiantanawat A, Rangkadilok N, Tawit Suriyo T, Satayavivad J (2013) Glyphosate induces human breast cancer cells growth via estrogen receptors. Food Chem Toxicol 59:129–136

    Article  CAS  Google Scholar 

  • Tizhe EV, Ibrahim NDG, Fatihu MY, Onyebuchi II, George BDJ, Ambali SF, Shallangwa JM (2014a) Influence of zinc supplementation on histopathological changes in the stomach, liver, kidney, brain, pancreas and spleen during subchronic exposure of Wistar rats to glyphosate. Comp Clin Pathol 23(5):1535–1543

    Article  CAS  Google Scholar 

  • Tizhe EV, Ibrahim NDG, Fatihu MY, Igbokwe IO, George BDJ, Ambali SF, Shallangwa JM (2014b) Serum biochemical assessment of hepatic and renal functions of rats during oral exposure to glyphosate with zinc. Comp Clin Pathol 23(4):1043–1050

    Article  CAS  Google Scholar 

  • Tsui MT, Chu LM (2003) Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52(7):1189–1197

    Article  CAS  Google Scholar 

  • Tu M, Hurd C, Randall JM (2001) Weed control methods handbook, The Nature Conservancy7E.1-7E.10. http://digitalcommons.usu.edu/cgi/viewcontent.cgi?article=1532&context=govdocs

  • Vande Berg BJ, Hammer PE, Chun BL, Schouten LC, Carr B, Guo R, Deter R (2008) Characterization and plant expression of a glyphosate-tolerant enolpyruvylshikimate phosphate synthase. Pest Manag Sci 64(4):340–345. https://doi.org/10.1002/ps.1507

    Article  CAS  Google Scholar 

  • Vereecken H (2005) Mobility and leaching of glyphosate: a review. Pest Manag Sci 61(12):1139–1151

    Article  CAS  Google Scholar 

  • Verrell P, Van Buskirk E (2004) As the worm turns: Eisenia fetida avoids soil contaminated by a glyphosate-based herbicide. Bull Environ Contam Toxicol 72(2):219–224

    Article  CAS  Google Scholar 

  • Webster TMU, 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 Genom 16(1):32

    Article  CAS  Google Scholar 

  • Whiles MR, Charlton RE (2006) The ecological significance of tallgrass prairie arthropods. Annu Rev Entomol 51:387–412

    Article  CAS  Google Scholar 

  • Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, Montgomery C (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front Ecol Environ 4(1):27–34

    Article  Google Scholar 

  • Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate for humans. Regul Toxicol Pharmacol 31(2):117–165

    Article  CAS  Google Scholar 

  • Yasmin S, D’Souza D (2007) Effect of pesticides on the reproductive output of Eisenia fetida. Bull Environ Contam Toxicol 79(5):529–532

    Article  CAS  Google Scholar 

  • Zaller JG, Heigl F, Ruess L, Grabmaier A (2014) Glyphosate herbicide affects belowground interactions between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Sci Rep. https://doi.org/10.1038/srep05634

  • Zhou CF, Wang YJ, Yu YC, Sun RJ, Zhu XD, Zhang HL, Zhou DM (2012) Does glyphosate impact on Cu uptake by, and toxicity to, the earthworm Eisenia fetida? Ecotoxicology 21(8):2297–2305

    Article  CAS  Google Scholar 

  • Zobiole L, Kremer R, Oliveira R, Constantin J (2011) Glyphosate affects microorganisms in rhizospheres of glyphosate-resistant soybeans. J Appl Microbiol 110:118–127

    Article  CAS  Google Scholar 

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Gill, J.P.K., Sethi, N., Mohan, A. et al. Glyphosate toxicity for animals. Environ Chem Lett 16, 401–426 (2018). https://doi.org/10.1007/s10311-017-0689-0

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