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Effects of glyphosate formulations on the population dynamics of two freshwater cladoceran species

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Abstract

The general objective of this work is to experimentally assess the effects of acute glyphosate pollution on two freshwater cladoceran species (Daphnia magna and Ceriodaphnia dubia) and to use this information to predict the population dynamics and the potential for recovery of exposed organisms. Five to six concentrations of four formulations of glyphosate (4-Gly) (Eskoba®, Panzer Gold®, Roundup Ultramax® and Sulfosato Touchdown®) were evaluated in both cladoceran species through acute tests and 15-day recovery tests in order to estimate the population dynamics of microcrustaceans. The endpoints of the recovery test were: survival, growth (number of molts), fecundity, and the intrinsic population growth rate (r). A matrix population model (MPM) was applied to r of the survivor individuals of the acute tests, followed by a Monte Carlo simulation study. Among the 4-Gly tested, Sulfosato Touchdown® was the one that showed higher toxicity, and C. dubia was the most sensitive species. The Monte Carlo simulation study showed an average value of λ always <1 for D. magna, indicating that its populations would not be able to survive under natural environmental conditions after an acute Gly exposure between 0.25 and 35 a.e. mg L−1. The average value of λ for C. dubia was also <1 after exposure to Roundup Ultramax®: 1.30 and 1.20 for 1.21 and 2.5 mg a.e. L−1,respectively. The combined methodology—recovery tests and the later analysis through MPM with a Monte Carlo simulation study—is proposed to integrate key demographic parameters and predict the possible fate of microcrustacean populations after being exposed to acute 4-Gly contamination events.

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References

  • Alberdi JL, Sáenz 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

    Article  CAS  Google Scholar 

  • American Public Health Association (APHA) (1998) Standard methods for the examination of water and wastewater. 20th edn. Ap. 8010G, Washington D.C., USA

  • Anton FA, Laborda E, Laborda P, Ramos E (1993) Carbofuran acute toxicity to Eisenia foetida (Savigny, 1826). Earthworms. Bull Environ Contam Toxicol 50:407–412

    CAS  Google Scholar 

  • Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P (2013) Environmental fate of glyphosate and aminomethyl phosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:1866–1873

    Article  CAS  Google Scholar 

  • ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians, American Society for Testing and Materials, Philadelphia, E 729–780

  • Botev Z, Grotowski J, Kroese D (2010) Kernel density estimation via diffusion The Ann of Statistics 38(5):2916–2957. https://doi.org/10.1214/10-AOS799c

    Article  Google Scholar 

  • Cámara de Sanidad Agropecuaria y Fertilizantes (CASAFE) (2011) Guía de Productos Fitosanitarios para la República Argentina. 15 Edn

  • Canadian water quality guidelines for the protection of aquatic life: Glyphosate. (2012) Canadian Council of Ministers of the Environment. In: Canadian environmental quality guidelines, Canadian Council of Ministers of the Environment, Winnipeg.

  • Caswell H (2001) Matrix population models: Construction, analysis and interpretation. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Cerejeira MJ, Viana P, Batista S, Pereira T, Silva E, Valerio MJ, Silva A, Ferreira M, Silva-Fernandes AM (2003) Pesticides in Portuguese surface and ground waters. Water Res 37:1055–1063

    Article  CAS  Google Scholar 

  • Chaparro M, Canziani G (2010) A discrete model for estimating the development time from egg to infecting larva of Ostertagia ostertagi parameterized using a fuzzy rule-based system. Ecol Modell 221:2582–2589

    Article  Google Scholar 

  • Choung CB, Hyneb RV, Stevensc MM, Hosea GC (2013) The ecological effects of a herbicide–insecticide mixture on an experimental freshwater ecosystem. Environ Pollut 172:264–274

    Article  CAS  Google Scholar 

  • Cox C (2004) Glyphosate. J Pestic Reform Winter 24(4):11–15

    Google Scholar 

  • Cuhra M, Traavik T, Bøhn 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 

  • Defarge N, Takács E, Lozano V, Mesnage R, Spiroux de Vendômois J, Séralini G-E, Székács A (2016) Co-Formulants in Glyphosate-Based Herbicides Disrupt Aromatase Activity in Human Cells below Toxic Levels. Int J Environ Res Public Health 13(3):264

    Article  CAS  Google Scholar 

  • de Souza JS, Kizys MM, da Conceição RR, Glebocki G, Romano RM, Ortiga-Carvalho TM, Giannocco G, da Silva ID, Dias da Silva MR, Romano MA, Chiamolera MI (2017) Perinatal exposure to glyphosate-based herbicide alters the thyrotrophic axis and causes thyroid hormone homeostasis imbalance in male rats. Toxicology 377:25–37

    Article  CAS  Google Scholar 

  • Dominguez-Cortinas G, Mejía-Saavedra J, 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 90:377–384

    Article  CAS  Google Scholar 

  • Emlen JM, Springman KR (2007) Developing methods to assess and predict the population level effects of environmental contaminants. Integr Environ Assess Manag 3:157–165

    Article  CAS  Google Scholar 

  • Finney DJ (1971) Probit Analysis, 3rd edn. Cambridge University Press, New York

    Google Scholar 

  • Forbes VE, Galic N, Schmolke S, Vavra J, Pastorok R, Thorbek P (2016) Assessing the risks of pesticides to threatened and endangered species using population modeling: A critical review and recommendations for future work. Environ Toxicol Chem 35(8):1904–1913

    Article  CAS  Google Scholar 

  • Gagneten AM, Maitre MA, Reno U, Regaldo L, Roldán S, Enrique S (2014) Efectos del herbicida Ron–do® sobre Ceriodaphnia reticulata (Crustacea, Cladocera) y degradabilidad del glifosato (N–fosfometilglicina) en condiciones experimentales. Nat Neotrop 45:71–85

    Article  Google Scholar 

  • Gilliom RJ, Hamilton PA (2006) Pesticides in nation’s streams and ground water 1992–2001. A summary. U.S. Department of the Interior. U.S. Geological Survey. U.S. Circular 1291. Geological Survey, Reston, Virginia.

  • Grube A, Donaldson D, Kiely T, Wu L (2011) Pesticide industry sales and usage: 2006 and 2007 market estimates. Biological and Economic Analysis Division, U.S. Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Hanson N, Stark JD (2012) Utility of population models to reduce uncertainty and increase value relevance in ecological risk assessments of pesticides: An example based on acute mortality data for daphnids. Integr Environ Assess Manag 8:262–270

    Article  CAS  Google Scholar 

  • Harper E, Rittenhouse T, Semlitsch R (2008) Demographic consequences of terrestrial habitat loss for pool-breeding amphibians: predicting extinction risks associated with inadequate size of buffer zones. Conserv Biol 22:1205–1215

    Article  Google Scholar 

  • Heinemann JA, Agapito-Tenfen SZ, Carman JA (2013) A comparative evaluation of the regulation of GM crops or products containing dsRNA and suggested improvements to risk assessments. Environ Int 55:43–55

    Article  CAS  Google Scholar 

  • Hua J, Relyea RA (2014) Chemical cocktails in aquatic ecosystems: Pesticide effects on resistance and resilience. Environ Pollut 189:18–26

    Article  CAS  Google Scholar 

  • Ibrahim L, Preuss TG, Schaeffer A, Hommen U (2014) A contribution to the identification of representative vulnerable fish species for pesticide risk assessment in Europe—A comparison of population resilience using matrix models. Ecol Model 280:65–75

    Article  CAS  Google Scholar 

  • James C (2014) Global status of commercialized biotech/GM crops: 2014. ISAAA Brief No. 49. ISAAA, Ithaca, NY

  • Kitulagodage M, Astheimer LB, Buttemer WA (2008) Diacetone alcohol, a dispersal solvent, contributes to acute toxicity of a fipronil-based insecticide in a passerine bird. Ecotoxicol Environ Saf 71:597–600

    Article  CAS  Google Scholar 

  • Lanctôt C, Navarro-Martin L, Robertson C, Park B, Jackman P, Pauli BD, Trudeau VL (2014) Effects of glyphosate-based herbicides on survival, development, growth and sex ratios of wood frog (Lithobates sylvaticus) tadpoles II: agriculturally relevant exposures to roundup weather maxs and visions under laboratory conditions. Aquat Toxicol 154:291–303

    Article  CAS  Google Scholar 

  • Lupi L, Miglioranza KSB, Aparicio VC, Marino D, Bedmar F, Wunderlin DA (2015) Occurrence of glyphosate and AMPA in an agricultural watershed from the southeastern region of Argentina. Sci Total Environ 536:687–694

    Article  CAS  Google Scholar 

  • Macneale KH, Spromberg JA, Baldwin DH, Scholz NL (2014) A modeled comparison of direct and food web-mediated impacts of common pesticides on Pacific salmon. PLoS ONE 9:1–13

    Article  CAS  Google Scholar 

  • Momo FR, Capurro AF (2006) Ecología Matemática: Principios y aplicaciones, 1 edn. Ediciones Cooperativas, Buenos Aires, Argentina

    Google Scholar 

  • Monsanto (2009) Monsanto Glyphosate—explaining the active ingredient. Growing Knowledge Bull. Monsanto Can. Inc., p 1–2

  • Nardi J, Moras PB, Koeppe C, Dallegrave E, Leal MB, Rossato-Grando LG (2017) Prepubertal subchronic exposure to soy milk and glyphosate leads to endocrine disruption. Food and Chemical Toxicology 100:247–252

    Article  CAS  Google Scholar 

  • National Council of Science and Technology (CONICET) (2009) Report: evaluation of information scientific linked to glyphosate in incidence on human health and the environment. National Council of Science and Technology (ed). Buenos Aires, Argentina, p 133

  • National Research Council of the United States (2013) Assessing Risks to Endangered and Threatened Species From Pesticides. National Academies Press, Washington, DC

  • Octave community (2014) GNU Octave 3.8.2. www.gnu.org/software/octave/

  • Olvera-Ramírez R, Centeno-Ramos C, Martínez-Jerónimo F (2010) Toxic effects of Pseudanabaena tenuis (cyanobacteria) on the cladocerans Daphnia magna and Ceriodaphnia dubia. Hidrobiológica 20(3):203–212

    Google Scholar 

  • Organisation for Economic Co-operation and Development (OECD) (2004) Guideline 202 on Daphnia sp., acute immobilisation test.OECD, Geneva

  • Pereira JL, Antunes SC, Castro BB, Marques CR, Gonclaves AMM, Gonclaves F, Pereira R (2009) Toxicity evaluation of three pesticides on non-target aquatic and soil organisms: Commercial formulation versus active ingredient. Ecotoxicology 18:455–463

    Article  CAS  Google Scholar 

  • Peruzzo P, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in North Pampasic region of Argentina. Environ Pollut 156:61–66

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Puglis HJ, Boone MD (2011) Effects of technical-grade active ingredient vs. commercial formulation of seven pesticides in the presence or absence of uv radiation on survival of green frog tadpoles. Arch Environ Contam Toxicol 60:145–155

    Article  CAS  Google Scholar 

  • Raipulis J, Toma MM, Balode M (2009) Toxicity and genotoxicity testing of roundup. Proc Latv Ac Sci 63:29–32

    CAS  Google Scholar 

  • Rand GM, Petrocelli SR (1985) Fundamentals of aquatic toxicology. Hemisphere Publishing Corporation, Washington, p 666

    Google Scholar 

  • Regaldo L (2013) Efecto de metales pesados y plaguicidas sobre organismos planctónicos de diferente nivel trófico y eficacia de acumulación por microalgas. Facultad de Bioquímica y Ciencias Biológicas. Universidad Nacional del Litoral

  • Reno U, Gutierrez MF, Longo M, Vidal E, Regaldo L, Negro A, Mariani M, Zalazar C, Gagneten AM (2015) Microcrustaceans: biological models to evaluate a remediation process of glyphosate-based formulations. Water Air Soil Pollut 226(10):226–349

    Article  CAS  Google Scholar 

  • Reno U, Gutierrez MF, Regaldo L, Gagneten AM (2014) The impact of eskobat, a glyphosate formulation on the freshwater plankton community. Water Environ Res 86(12):2294–2300

    Article  CAS  Google Scholar 

  • Reno U, Regaldo L, Vidal E, Mariani M, Zalazar C, Gagneten AM (2016) Water polluted with glyphosate formulations: effectiveness of a decontamination process using Chlorella vulgaris growing as bioindicator. J Appl Phycol 28(4):2279–2286

    Article  CAS  Google Scholar 

  • Rinderhagen M, Ritterhoff J, Zauke G (2000) Crustaceans as bioindicators.Environ Res Forum 9:161–197

    CAS  Google Scholar 

  • Ronco AE, Marino DJG, Abelando M, Almada P, Apartin CD (2016) Water quality of the main tributaries of the Paraná Basin: glyphosate and AMPA in surface water and bottom sediments. Environ Monit Assess 188:458.https://doi.org/10.1007/s10661-016-5467-0

    Article  CAS  Google Scholar 

  • Rubinstein RY, Kroese DP (2007) Simulation and the Monte Carlo method. Wiley, Hoboken

    Book  Google Scholar 

  • Salazar LG (2010) Análisis sobre el impacto ambiental del uso de glifosato y sus mezclas (coadyudantes) derivada de las actividades productivas (agrícolas) en Colombia, alternativa de producción mediante la optimización (BPA) y el desarrollo sostenible. Monografía para obtener el título de Especialista en Ingeniería Ambiental. Universidad Industrial de Santander. Escuela de Ingeniería Química. Especialización en Ingeniería Ambiental. Bucaramanga, España

  • 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 225:2207

    Article  CAS  Google Scholar 

  • Schimpf MG, Milesi MM, Ingaramo PI, Luque EH, Varayoud J (2017) Neonatal exposure to a glyphosate based herbicide alters the development of the rat uterus. Toxicology 376:2–14

    Article  CAS  Google Scholar 

  • Spurgeon D, Svendsen C, Kille P, Morgan A, Weeks J (2004) Responses of earthworms (Lumbricus rubellus) to copper and cadmium as determined by measurement of juvenile traits in a specially designed test system. Ecotoxicol Environ Saf 57:54–64

    Article  CAS  Google Scholar 

  • Thai-Hoang L, Eun-Suk L, Sung Kyu L, Young-Woo C, Yang-Hoon K, Jiho M (2010) Effects of glyphosate and methidathion on the expression of the Dhb, Vtg, Arnt, CYP4 and CYP314 in Daphnia magna. Chemosphere 79(1):67–71

    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 52:1189–1197

    Article  CAS  Google Scholar 

  • University National of the Littoral (UNL) (2010) Report about the degree of toxicity of glyphosate. University National of the Littoral (ed). Santa Fe, Argentina

  • Undersecretariat of Hydrological Resources, Argentina (2003) Developments of national guide levels of Ambient water quality corresponds to a glyphosate. Undersecretariat of Hydrological Resources, Argentina (ed). Buenos Aires, Argentina

  • Venkateswara RJ, Sutya Pavan Y, Madhavendra S (2003) Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm. Eisenia foetida Ecotoxicol Environ Saf 54:296–301

    Article  CAS  Google Scholar 

  • Willson JD, Hopkins WA, Bergeron CM, Todd BD (2012) Making leaps in amphibian ecotoxicology: Translating individual-level effects of contaminants to population viability. Ecol Appl 22:1791–1802

    Article  CAS  Google Scholar 

  • Wong P, Dixon D (1998) Standard methods for whole effluent toxicity testing: development and application. Report no. MFE80205. NIWA report for the Ministry for the Environment, Wellington, New Zealand

  • World Health Organization (2015) International Agency for Research of Cancer: Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate. www.thelancet.com/oncology. Accessed 20 March 2014

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Acknowledgements

This research was supported by grants from the Universidad Nacional del Litoral, Projects CAI + D Orientado No.: 1.6 and CAI + D N°: 501 201101 00215 LI.

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Reno, U., Doyle, S., Momo, F. et al. Effects of glyphosate formulations on the population dynamics of two freshwater cladoceran species. Ecotoxicology 27, 784–793 (2018). https://doi.org/10.1007/s10646-017-1891-3

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