Skip to main content

Advertisement

Log in

Lethal and Sublethal Effects of the Herbicide Atrazine in the Early Stages of Development of Physalaemus gracilis (Anura: Leptodactylidae)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Water sources used as reproductive sites by crying frog, Physalaemus gracilis, are extensively associated with agroecosystems in which the herbicide atrazine is employed. To evaluate the lethal and sublethal effects of atrazine commercial formulation, acute and chronic toxicity tests were performed in the embryonic phase and the beginning of the larval phase of P. gracilis. Tests were started on stage 19 of Gosner (Herpetologica 16:183–190, 1960) and performed in 24-well cell culture plates. Acute tests had a duration of 96 h with embryo mortality monitoring every 24 h. Chronic assays contemplated the transition from the embryonic to larval stages and lasted 168 h. Every 24 h the embryos/larvae were observed for mortality, mobility, and malformations. The LC50 of atrazine determined for P. gracilis embryos was 229.34 mg L−1. The sublethal concentrations did not affect the development of the larvae but were observed effects on mobility and malformations, such as spasmodic contractions, reduced mobility, malformations in mouth and intestine, and edema arising. From 1 mg L−1 atrazine, the exposed larvae began to have changes in mobility and malformations. The atrazine commercial formulation has caused early life effects of P. gracilis that may compromise the survival of this species but at higher concentrations than recorded in the environment, so P. gracilis can be considered tolerant to this herbicide at environmentally relevant concentrations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci Process Impacts 18:779–787. https://doi.org/10.1039/C6EM00268D

    Article  CAS  Google Scholar 

  • Belanger RM, Peters TJ, Sabhapathy GS, Khan S, Katta J, Abraham NK (2015) Atrazine exposure affects the ability of crayfish (Orconectes rusticus) to localize a food odor source. Arch Environ Contam Toxicol 68:636–645. https://doi.org/10.1007/s00244-015-0142-y

    Article  CAS  Google Scholar 

  • Belanger RM, Mooney LN, Nguyen HM, Abraham NK, Peters TJ, Kana MA, May LA (2016) Acute atrazine exposure has lasting effects on chemosensory responses to food odors in Crayfish (Orconectes virilis). Arch Environ Contam Toxicol 70:289–300. https://doi.org/10.1007/s00244-015-0234-8

    Article  CAS  Google Scholar 

  • Brazil (2008) Resolução Conama no. 396, de 3 de abril de 2008. http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=562. Accessed 19 Dec 2017

  • Brazil (2011) Portaria no. 2.914, de 12 de dezembro de 2011. http://bvsms.saude.gov.br/bvs/saudelegis/gm/2011/prt2914_12_12_2011.html. Accessed 19 Dec 2017

  • Bridges CM (2000) Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch Environ Contam Toxicol 39:91–96. https://doi.org/10.1007/s002440010084

    Article  CAS  Google Scholar 

  • Brodeur JC, Svartz G, Perez-Coll CS, Marino DJG, Herkovits J (2009) Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat Toxicol 91:161–170. https://doi.org/10.1016/j.aquatox.2008.07.003

    Article  CAS  Google Scholar 

  • Casara KP, Vecchiato AB, Lourencetti C, Pinto AA, Dores EFGC (2012) Environmental dynamics of pesticides in the drainage area of the São Lourenço River Headwaters, Mato Grosso State, Brazil. J Braz Chem Soc 23:1719–1731

    Article  CAS  Google Scholar 

  • Cerejeira MJ, Viana P, Batista S, Pereira T, Silva E, Valerio MJ, Silva A, Ferreira M, Fernandes AM (2003) Pesticides in Portuguese surface and ground waters. Water Res 37:1055–1063. https://doi.org/10.1016/S0043-1354(01)00462-6

    Article  CAS  Google Scholar 

  • Chicati ML, Nanni MR, Cézar E (2012) Chemical contamination of water in irrigated rice on Paraná State, Brazil. Semina Cienc Agrar 33:1455–1462

    Article  CAS  Google Scholar 

  • Christopher R, Kinney O, Fiori A, Congdon J (1996) Oral deformities in tadpoles (Rana catesbeiana) associated with coal ash deposition: effects on grazing ability and growth. Freshw Biol 36:723–730. https://doi.org/10.1046/j.1365-2427.1996.00123.x

    Article  Google Scholar 

  • Duellman WE, Trueb L (1994) Biology of amphibians. McGraw-Hill, New York

    Google Scholar 

  • Ezemonye L, Tongo I (2009) Lethal and sublethal effects of atrazine to amphibian larvae. Jordan J Biol Sci 2:29–36

    Google Scholar 

  • Freitas CM, Porto MFS, Pivetta F, Moreira JC, Machado JMH (2001) Poluição química ambiental: um problema de todos, que afeta uns mais que os outros. http://www6.ensp.fiocruz.br/repositorio/resource/353526. Accessed 3 July 2017

  • Frost DR (2017) Amphibian species of the world: an online reference. Version 6.0 5.5. http://research.amnh.org/herpetology/amphibia/index.html. Accessed 7 Aug 2017

  • GHS (2011) Globally harmonized system of classification and labelling of chemicals. United Nations, New York

    Google Scholar 

  • Gonçalves MW, Carvalho WF, Pereira RR, Silva DM, Bastos RP, Cruz AD (2014) Avaliação de danos genômicos em anfíbios anuros do cerrado goiano. Estudos 41:89–104

    Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine in aquatic ecosystems. Environ Int 26:483–495. https://doi.org/10.1016/S0160-4120(01)00031-9

    Article  CAS  Google Scholar 

  • Hayes TB, Collins A, Lee M, Mendonza M, Noriega N, Stuart AA, Vonk A (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. PNAS 99:5476–5480. https://doi.org/10.1073/pnas.082121499

    Article  CAS  Google Scholar 

  • Herkovits J, Ponce B, Olabe J (1980) Efecto de la prostaglandina F2 alfa sobre la proliferación celular y el transporte de Na, K, Ca y Mg en células epiteliales embrionarias. Medicina 40:858–859

    Google Scholar 

  • IBAMA (2014) Brazilian Institute of Environment and Renewable Natural Resources Pesticides and related products marketed in 2014 in Brazil. http://www.ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos. Accessed 1 Aug 2017

  • Knapp RA, Morgan AT (2006) Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2:188–197

    Article  Google Scholar 

  • Knutson MG, Richardson WB, Reineke DM, Gray BR, Parmelee JR, Weick SE (2004) Agricultural ponds support amphibian populations. Ecol Appl 14:669–684

    Article  Google Scholar 

  • Lajmanovich RC, Sandoval MT, Peltzer PM (2003) Induction of mortality and malformation in Scinax nasicus larvae exposed to glyphosate formulations. Bull Environ Contam Toxicol 70:612–618. https://doi.org/10.1007/s00128-003-0029-x

    Article  CAS  Google Scholar 

  • Larson DL, McDonald S, Fivizzani AJ, Newton WE, Hamilton SJ (1998) Effects of the herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response. Physiol Zool 71:671–679

    Article  CAS  Google Scholar 

  • Lavilla E, Kwet A, Segalla MV, Langone J, Baldo D (2010) Physalaemus gracilis. In the IUCN red list of threatened species. The IUCN red list of threatened species. Version 2017-1. www.Iucnredlist.org. Accessed 7 Aug 2017

  • Lenkowski JR, Reed MJ, Deininger L, Mclaughlin KA (2008) Perturbation of organogenesis by the herbicide atrazine in the amphibian Xenopus laevis. Environ Health Perspect 116:223–230. https://doi.org/10.1289/ehp.10742

    Article  CAS  Google Scholar 

  • Lingnau R (2009) Distribuição temporal, atividade reprodutiva e vocalizações em uma assembleia de anfíbios anuros de uma floresta ombrófila mista em Santa Catarina, sul do Brasil. Tesis, Pontifícia Universidade Católica do Rio Grande do Sul

  • McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. The University of Chicago Press, Chicago

    Google Scholar 

  • McMahon TA, Romansic JM, Rohr JR (2013) Non-monotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on larvae. Environ Sci Technol 47:7958–7964. https://doi.org/10.1021/es401725s

    Article  CAS  Google Scholar 

  • Miltner RJ, Baker DB, Speth TF (1989) Treatment of seasonal pesticides in surface water. J Am Water Works Assoc 81:43–52

    Article  CAS  Google Scholar 

  • Montagner CC, Vidal C, Acayaba RD, Jardim WF, Jardim ICSF, Umbuzeiro G (2014) Trace analysis of pesticides and an assessment of their occurrence in surface and drinking waters from the State of São Paulo (Brazil). Anal Methods 6:6668–6677

    Article  CAS  Google Scholar 

  • Moreira JC, Peres F, Simões AC, Pignati WA, Dores EC, Vieira SN, Strüssmann C, Mott T (2012) Contaminação de águas superficiais e de chuva por agrotóxicos em uma região do estado do Mato Grosso. Ciência e Saúde Coletiva 17:1557–1568. https://doi.org/10.1590/S1413-81232012000600019

    Article  Google Scholar 

  • Morgan MK, Scheuerman PR, Bishop CS, Pyles RA (1996) Teratogenic potential of atrazine and 2,4-D using FETAX. J Toxicol Environ Health 48:151–168

    Article  CAS  Google Scholar 

  • Newman MC, Unger MA (2003) Fundamentals of ecotoxicology. Lewis Publishers, Boca Raton

    Google Scholar 

  • Nieves-Puigdoller K, Björnsson BT, McCormick SD (2007) Effects of hexazinone and atrazine on the physiology and endocrinology of smolt development in Atlantic salmon. Aquat Toxicol 84:27–37. https://doi.org/10.1016/j.aquatox.2007.05.011

    Article  CAS  Google Scholar 

  • OECD (2013) Test No. 236: Fish Embryo Acute Toxicity (FET) test. OECD guidelines for the testing of chemicals, Section 2. OECD Publishing, Paris

    Google Scholar 

  • Ortiz-Santaliestra ME, Marco A, Fernández MJ, Lizana M (2006) Influence of developmental stage on sensitivity to ammonium nitrate of aquatic stages of amphibians. Environ Toxicol Chem 25:105–111. https://doi.org/10.1897/05-023R.1

    Article  CAS  Google Scholar 

  • Peltzer PM, Junges CM, Attademo AM, Bassó A, Grenón P, Lajmanovich RC (2013) Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) larvae exposed to glufosinate ammonium herbicide. Ecotoxicology 22:1165–1173. https://doi.org/10.1007/s10646-013-1103-8

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Soloneski S, Nikoloff N, Natale GS, Larramendy ML (2015) Toxic and genotoxic effects of the imazethapyr-based herbicide formulation Pivot H® on Montevideo tree frog Hypsiboas pulchellus larvae (Anura, Hylidae). Ecotoxicol Environ Saf 119:15–24. https://doi.org/10.1016/j.ecoenv.2015.04.045

    Article  Google Scholar 

  • Rao DG, Senthilkumar R, Byrne JA, Feroz S (2013) Waste water treatment: advanced processes and technologies. CRC, New York

    Google Scholar 

  • Rohr JR, McCoy KA (2010) A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environ Health Perspect 118:20–32. https://doi.org/10.1289/ehp.0901164

    Article  CAS  Google Scholar 

  • Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD (2003) Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander (Ambystoma barbouri). Environ Toxicol Chem 22:2385–2392. https://doi.org/10.1897/02-528

    Article  CAS  Google Scholar 

  • Sass JB, Colangelo A (2006) European Union bans Atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267. https://doi.org/10.1179/oeh.2006.12.3.260

    Article  CAS  Google Scholar 

  • Schiesari L, Grillittsch B, Grillittsch H (2007) Biogeographic biases in research and their consequences for linking amphibian declines to pollution. Conserv Biol 21:465–471

    Article  Google Scholar 

  • Semlitsch RD (ed) (2003) Introduction: general threats to amphibians. In: Amphibian conservation. Smithsonian books, Washington, London, pp 1–7

  • Simon E, Puky M, Braun M, Tóthmérész B (2012) Assessment of the effects of urbanization on trace elements of toe bones. Environ Monit Assess 184:5749. https://doi.org/10.1007/s10661-011-2378-y

    Article  CAS  Google Scholar 

  • Sousa AS, Duaví WC, Cavalcante RM, Milhome MA, Nascimento RF (2016) Estimated levels of environmental contamination and health risk assessment for herbicides and insecticides in surface water of Ceará, Brazil. Bull Environ Contam Toxicol 96:90

    Article  CAS  Google Scholar 

  • Svartz GV, Herkovits J, Pérez-Coll CS (2012) Sublethal effects of Atrazine on embyo-larval development of Rhinella arenarum (Anura: Bufonidae). Ecotoxicology 21:1251–1259. https://doi.org/10.1007/s10646-012-0880-9

    Article  CAS  Google Scholar 

  • USEPA (United States Environmental Protection Agency) (2014) Atrazine ecological exposure monitoring program data Document ID: EPA-HQ-OPP-2003-0367-0303

  • Venesky MD, Parris MJ, Storfer A (2010) Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6:565–575. https://doi.org/10.1007/s10393-009-0272-7

    Article  Google Scholar 

  • Zhang JJ, Lu YC, Zhang JJ, Tan LR, Yang H (2014) Accumulation and toxicological response of atrazine in rice crops. Ecotoxicol Environ Saf 102:105–112

    Article  Google Scholar 

Download references

Acknowledgements

Valuable help in laboratorial work was provided by Jessica Herek, Jéssica G. Slaviero, and Gregori B. Bieniek. The authors are grateful to the Federal University of Fronteira Sul—UFFS for providing logistical support. Camila Rutkoski, Natani Macagnan, and Cassiane Kolcenti were supported by fellowship from Fundação de Amparo a Pesquisa do Estado do Rio Grande do Sul—FAPERGS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marilia T. Hartmann.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was licensed by IBAMA (50398-1) and authorized by the Ethics Committee for Animal Use of the Federal University of Fronteira Sul.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rutkoski, C.F., Macagnan, N., Kolcenti, C. et al. Lethal and Sublethal Effects of the Herbicide Atrazine in the Early Stages of Development of Physalaemus gracilis (Anura: Leptodactylidae). Arch Environ Contam Toxicol 74, 587–593 (2018). https://doi.org/10.1007/s00244-017-0501-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-017-0501-y

Navigation