Ir para o conteúdo principal Ir para o menu de navegação principal Ir para o rodapé
Publicado: 2023-04-30

In situ works on ecotoxicology in amphibians: current state of the art

Universidade Federal da Fronteira Sul
Universidade Federa da Fronteira Sul
Universidade Federal da Fronteira Sul
Universidade Federal da Fronteira Sul
Anura, tadpoles, pesticides, field condition


Amphibians play a fundamental role in the functioning of ecosystems, mainly in the nutrient cycle, energy flow, and pest control. This group has a massive population decline, with approximately 41% of all species at risk, highlighting pesticide pollution as one of the main threats to the loss of anuran biodiversity. This occurs since amphibians have an epidermis with high permeability and a biphasic life cycle, where they use both the aquatic and terrestrial environments, allowing exposure and making them susceptible to chemical agents released into the environment. This makes amphibians a model group in ecotoxicological studies. However, due to the greater control of experimental conditions, the vast majority of studies are carried out in the laboratory, thus maintaining a gap in knowledge about the effects of pesticides on amphibians in natural environments. Under natural conditions, where environmental variables are not controlled, experiments must relate all the dynamics of the interaction of substances existing in the environment, and their influences on organisms. To evaluate the studies already performed under natural conditions, a bibliographic survey was carried out through a search with the Web of Science and SCOPUS databases, considering articles published in the last twenty years, using the terms 'field experimentation' or 'in situ study', associated with 'tadpole' and 'agrochemical' or 'pesticide', using a descriptive methodology. Twenty-one abstracts were pre-selected, they were further evaluated and the methodologies were checked to ensure only the analysis of experiments conducted in the field conditions. Thus, ten works were selected for the construction of the review. The works selected used native amphibian species, considered generalists, present in the study region, and were carried out in environments intended for agricultural cultivation with control groups in preserved locations. In these works, different methodologies were used, such as intentional spraying of water bodies, quantification of pesticides in the study sites, and verification of changes caused by the environment on tadpoles. The main evaluations were based on the survival and morphological changes of the tadpoles and, in some cases, on cytological and biochemical assays.


  1. AGOSTINI, M.G., ROESLER, I., BONETTO, C., RONCO, A.E., BILENCA, D. Pesticides in the real world: The consequences of GMO-based intensive agriculture on native amphibians. Biological Conservation 241, 108355, 2020.
  2. ALTWEGG, R., REYER, H.-U. Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57, 872-882, 2003.
  3. ARAÚJO, M.C., ASSIS, C.R.D., SILVA, L.C., MACHADO, D.C., SILVA, K.C.C., LIMA, A.V.A., CARVALHO JR., L.B., BEZERRA, R.S., OLIVEIRA, M.B.M. Brain acetylcholinesterase of jaguar cichlid (Parachromis managuensis): From physicochemical and kinetic properties to its potential as biomarker of pesticides and metal ions. Aquatic Toxicology 177, 188-189, 2016.
  4. ATTADEMO, A.M., PELTZER, P.M., LAJMANOVICH, R.C., CABAGNA-ZENKLUSEN, M.C., JUNGES, C.M., BASSO, A. Biological endpoints, enzyme activities, and blood cell parameters in two anuran tadpole species in rice agroecosystems of mid-eastern Argentina. Environmental Monitoring and Assessment 186, 635-649, 2014.
  5. BANK, M.S., CROCKER, J.B., DAVIS, S., BROTHERTON, D.K., COOK, R., BEHLER, J., CONNERY, B. Population decline of northern dusky salamanders at Acadia National Park, Maine, USA. Biological Conservation 130, 230-238, 2006.
  6. BANK, M.S., LOFTIN, C.S., JUNG, R.E. Mercury bioaccumulation in northern two-lined salamanders from streams in the northeastern United States. Ecotoxicology 14, 181-191, 2006.
  7. BARNI, S., BONCOMPAGNI, E., GROSSO, A., BERTONE, V., FREITAS, I., FASOLA, M., FENOGLIO, C. Evaluation of Rana snk esculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquatic Toxicology 81,45-54, 2007.
  8. BEATTIE, R.C., TYLER-JONES, R. The effects of low pH and aluminum on breeding success in the frog Rana temporaria. Journal of Herpetology 26, 353-360, 1992.
  9. BONFANTI, P., SAIBENE, M., BACCHETTA, R., MANTECCA, P., COLOMBO, A. A glyphosate micro-emulsion formulation displays teratogenicity in Xenopus laevis. Aquatic Toxicology 195, 103-113, 2018.
  10. CAMP, A.A., BUCHWALTER, D.B. Can’t take the heat: temperature-enhanced toxicity in the mayfly Isonychia bicolor exposed to the neonicotinoid insecticide imidacloprid. Aquatic Toxicology 178, 49-57, 2016.
  11. CHEN, C.Y., HATHAWAY, K.M., FOLT, C.L. Multiple stress effects of vision herbicide, pH, and food on zooplankton and larval amphibian species from forest wetlands. Environmental Toxicology and Chemistry 23, 823-831, 2004.
  12. CONAMA - Conselho Nacional do Meio Ambiente. Resolução CONAMA Nº 001, de 23 de janeiro de 1986. "Dispõe sobre critérios básicos e diretrizes gerais para a avaliação de impacto ambiental”. Ministério do Meio Ambiente (MMA). Brasil. Available at: Accessed 08 November 2022
  13. DARCOVICH, K., O’MEARA, J. An olympic legacy: green and golden bell frog conservation at Sydney Olympic Park 1993–2006, 2008. Australian Zoologist 34, 236-248.
  14. DYCK, A., ROBINSON, S.A., YOUNG, S.D., RENAUD, J.B., SABOURIN, L., LAPEN, D.R., PICK, F.R. The effects of ditch management in agroecosystems on embryonic and tadpole survival, growth, and development of northern leopard frogs (Lithobates pipiens). Archives of Environmental Contamination and Toxicology 81, 107-122, 2021.
  15. EDGE, C.B., THOMPSON, D.G., HAO, C., HOULAHAN, J.E. A silviculture application of the glyphosate-based herbicide VisionMAX to wetlands has limited direct effects on amphibian larvae. Environmental Toxicology and Chemistry 31, 2375-2383, 2012.
  16. EDGE, C., THOMPSON, D., HAO C., HOULAHAN J. The response of amphibian larvae to exposure to a glyphosate-based herbicide (Roundup WeatherMax) and nutrient enrichment in an ecosystem experiment. Ecotoxicology and Environmental Safety 109, 124-132, 2014.
  17. FREDA, J., DUNSON, W.A. The influence of external cation concentration on the hatching of amphibian embryos in water of low pH. Canadian Journal of Zoology 63, 2649-2656, 1985.
  18. GILL, J.P.K., SETHI, N., MOHAN, A., DATTA, S., GIRDHAR, M. Glyphosate toxicity for animals. Environmental Chemistry Letters 16, 401-426, 2018.
  19. GLINSKI, D.A., HENDERSON, W.M., VAN METER, R.J., PURUCKER, T. Effect of hydration status on pesticide uptake in anurans following exposure to contaminated soils. Environmental Science and Pollution Research 25, 16192-16201, 2018.
  20. GONÇALVES, M.W., VIEIRA, T.B., MACIEL, N.M., CARVALHO, W.F., LIMA, L.S.F., GAMBALE, P.G., CRUZ, A.D., NOMURA, F., BASTOS, R.P., SILVA, D.M. Detecting genomic damages in the frog Dendropsophus minutus: preserved versus perturbed areas. Environmental Science and Pollution Research 22, 3947-3954, 2015.
  21. GONÇALVES, M.W., CAMPOS, C.B.M., GODOY, F.R., GAMBALE, P.G., NUNES, H.F., NOMURA, F., BASTOS, R.P., CRUZ, A.D., SILVA, D.M. Assessing genotoxicity and mutagenicity of three common amphibian species inhabiting agroecosystem environment. Archives of Environmental Contamination and Toxicology 77, 409-420, 2019.
  22. GUIDA, Y.S., MEIRE, R.O., TORRES, J.P.M., MALM, O. Air contamination by legacy and current-use pesticides in Brazilian mountains: An overview of national regulations by monitoring pollutant presence in pristine areas. Environmental Pollution, 242, 19-30, 2018.
  23. HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., LOEBMANN, D., GASPARINI, J.L., SAZIMA, I. Guia dos anfíbios da mata atlântica: Diversidade e biologia (Guide to the amphibians of the Atlantic forest: Diversity and biology). Anolis Books:São Paulo. ISBN: 9788565622035. 544p., 2013.
  24. HAYES, T.B., STUART, A.A., MENDOZA, M., COLLINS, A., NORIEGA, N., VONK, A., JOHNSTON, G., LIU, R., KPODZO, D. Characterization of atrazine-induced gonadal malformations in african clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen (17β-estradiol): Support for the demasculinization/feminization hypothesis. Environmental Health Perspectives 114, 134-141, 2006.
  25. HEREK, J.S., VARGAS, L., TRINDADE, S.A.R., RUTKOSKI, C.F., MACAGNAN, N., HARTMANN, P.A., HARTMANN, M.T. Can environmental concentrations of glyphosate affect survival and cause malformation in amphibians? Effects from a glyphosate-based herbicide on Physalaemus cuvieri and P. gracilis (Anura, Leptodactylidae). Environmental Science and Pollution Research 27, 22619-22630, 2020.
  26. HEREK, J.S., VARGAS, L., TRINDADE, S.A.R., RUTKOSKI, C.F., MACAGNAN, N., HARTMANN, P.A., HARTMANN, M.T. Genotoxic effects of glyphosate on Physalaemus tadpoles. Environmental Toxicology and Pharmacology 81, 103516, 2021.
  27. ILHA P., SCHIESARI L. Lethal and sublethal effects of inorganic nitrogen on gladiator frog tadpoles (Hypsiboas faber, Hylidae). Copeia 2014, 221-230, 2014.
  28. IUCN. The IUCN Red List of Threatened Species. Version 2022-1. Available at: Accessed 08 November 2022.
  29. KHAN, M.Z., TABASSUM, R., NAQVI, S.N.-U.-H., SHAH, E.Z., TABASSUM, F., AHMED, I., FATIMA, F., KHAN, M.F. Effect of cypermethrin and permethrin on cholinesterase activity and protein contents in Rana tigrina (Amphibia). Turkish Journal of Zoology 27, 243-246, 2003.
  30. LANCTÔT, C., NAVARRO-MARTÍN, L., ROBERTSON, C., PARK, B., JACKMAN, P., PAULI, B.D., TRUDEAU, V.L. Effects of glyphosate-based herbicides on survival, development, growth and sex ratios of wood frog (Lithobates sylvaticus) tadpoles. II: Agriculturally relevant exposures to Roundup WeatherMax® and Vision® under laboratory conditions. Aquatic Toxicology 154, 291-303, 2014.
  31. LASKOWSKI, D.A. Physical and chemical properties of pyrethroids. Reviews of Environmental Contamination and Toxicology 174, 149-170, 2002.
  32. LLEWELYN, V. K., BERGER, L., GLASS, B.D. Permeability of frog skin to chemicals: effect of penetration enhancers. Heliyon 5, e02127, 2019.
  33. LÓPEZ, S.L., AIASSA, D., BENÍTEZ-LEITE, S., LAJMANOVICH, R., MAÑAS, F., POLETTA, G., SÁNCHEZ, N., SIMONIELLO, M.F., CARRASCO, A.E. Pesticides used in South American GMO-based agriculture: a review of their effects on humans and animal models. Advances in Molecular Toxicology 6, 41-75, 2012.
  34. MACAGNAN, N., RUTKOSKI, C.F., KOLCENTI, C., VANZETTO, G.V., MACAGNAN, L.P., STURZA, P.F., HARTMANN, P.A., HARTMANN, M.T. Toxicity of cypermethrin and deltamethrin insecticides on embryos and larvae of Physalaemus gracilis (Anura: Leptodactylidae). Environmental Science and Pollution Research 24, 20699-20704, 2017.
  35. MAHMOOD, I., IMADI, S.R., SHAZADI, K., GUL, A., HAKEEM, K.R. Effects of pesticides on environment. In: Hakeem, K., Akhtar, M., Abdullah, S. (Eds) Plant, Soil and Microbes. Springer:Cham, 253-269, 2016.
  36. MATSON, C.W., GILLESPIE, A.M., MCCARTHY, C., MCDONALD, T.J., BICKHAM, J.W., SULLIVAN, R., DONNELLY, K.C. Wildlife toxicology: biomarkers of genotoxic exposures at a hazardous waste site. Ecotoxicology 18, 886-898, 2009.
  37. NWANI, C.D., LAKRA, W.S., NAGPURE, N.S., KUMAR, R., KUSHWAHA, B., SRIVASTAVA, S.K. Toxicity of the herbicide atrazine: Effects on lipid peroxidation and activities of antioxidant enzymes in the freshwater fish Channa punctatus (Bloch). International Journal of Environmental Research and Public Health 7, 3298-3312, 2010.
  38. NYSTRÖM, P., HANSSON, J., MÅNSSON, J., SUNDSTEDT, M., RESLOW, C., BROSTRÖM, A. A documented amphibian decline over 40 years: possible causes and implications for species recovery. Biological Conservation 138, 399-411, 2007. https://doi:10.1016/j.biocon.2007.05.007
  39. ORTIZ-SANTALIESTRA, M.E., MAIA, J.P., EGEA-SERRANO, A., LOPES, I. Validity of fish, birds and mammals as surrogates for amphibians and reptiles in pesticide toxicity assessment. Ecotoxicology 27, 819-833, 2018.
  40. ORTON, F., ROUTLEDGE, E. Agricultural intensity in ovo affects growth, metamorphic development and sexual differentiation in the Common toad (Bufo bufo). Ecotoxicology 10, 901-911, 2011.
  41. PAVAN, F.A., SAMOJEDEN, C.G., RUTKOSKI, C.F., FOLADOR, A., DA FRÉ, S.P., MÜLLER, C., HARTMANN, P.A., HARTMANN, M.T. Morphological, behavioral and genotoxic effects of glyphosate and 2,4-D mixture in tadpoles of two native species of South American amphibians. Environmental Toxicology and Pharmacology 85, 103637, 2021. https://doi:10.1016/j.etap.2021.103637
  42. PICKETT, E.J., STOCKWELL, M.P., BOWER, D.S., GARNHAM, J.I., POLLARD, C.J., CLULOW, J., MAHONY, M.J. Achieving no net loss in habitat offset of a threatened frog required high offset ratio and intensive monitoring. Biological Conservation 157, 156-162, 2013.
  43. POLLARD, C.J., STOCKWELL, M.P., BOWER, D.S., CLULOW, J., MAHONY, M.J. Combining ex situ and in situ methods to improve water quality testing for the conservation of aquatic species. Aquatic Conservation: Marine and Freshwater Ecosystems 27, 559-568, 2016.
  44. ROJAS-HUCKS, S., ROJAS-HUCKS, S., GUTLEB, A.C., GONZÁLEZ, C.M., CONTAL, S., MEHENNAOUI, K., JACOBS, A., WITTERS, H.E., PULGAR, J. Xenopus laevis as a bioindicator of endocrine disruptors in the region of central Chile. Archives of Environmental Contamination and Toxicology 77, 390-408, 2019.
  45. ROSENBAUM, E.A., DUBOSCQ, L., SOLEÑO, J., MONTAGNA, C.M., FERRARI, A., VENTURINO, A. Response of biomarkers in amphibian larvae to in situ exposures in a fruit-producing region in North Patagonia, Argentina. Environmental Toxicology and Chemistry 31, 2311-2317, 2012.
  46. RUDOLF, V.H.W., RÖDEL, M.O. Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evolutionary Ecology 21, 121-142, 2007.
  47. RUTHSATZ, K., PECK, M.A., DAUSMANN, K.H., SABATINO, N.M., GLOS, J. Patterns of temperature induced developmental plasticity in anuran larvae. Journal of Thermal Biology 74, 123-132, 2018.
  48. RUTKOSKI, C.F., MACAGNAN, N., KOLCENTI, C., VANZETTO, G.V., STURZA, P.F., HARTMANN, P.A., HARTMANN, M.T. Lethal and sublethal effects of the herbicide atrazine in the early stages of development of Physalaemus gracilis (Anura: Leptodactylidae). Archives of Environmental Contamination and Toxicology 74, 587-593, 2018.
  49. RUTKOSKI, C.F., MACAGNAN, N., FOLADOR, A., SKOVRONSKI, V.J., AMARAL, A.M.B., LEITEMPERGER, J., DORNELLES, M., HARTMANN, P.A., MÜLLER, C., LORO, V. L., HARTMANN, M.T. Cypermethrin- and fipronil-based insecticides cause biochemical changes in Physalaemus gracilis tadpoles. Environmental Science and Pollution Research 28, 4377-4387, 2021.
  50. RUTKOSKI, C. F., MACAGNAN, N., FOLADOR, A., SKOVRONSKI, V. J., AMARAL, A. M. B., LEITEMPERGER, J., DORNELLES, M., HARTMANN, P. A., MÜLLER, C., LORO, V. L., HARTMANN, M. Morphological and biochemical traits and mortality in Physalaemus gracilis (Anura: Leptodactylidae) tadpoles exposed to the insecticide chlorpyrifos. Chemosphere 250, 126162, 2020.
  51. SÁNCHEZ-BAYO, F., WYCKHUYS, K.A.G. Worldwide decline of the entomofauna: a review of its drivers. Biological Conservation 232, 8-27, 2019.
  52. SILVA, H.S.V.P., LOIOLA, C., PEREIRA, S.R.F., SANTOS, R.L., ANDRADE, G.V., NUNES, G.S. Toxicidade aguda e genotoxicidade do agrotóxico comercial Folisuper 600br a girinos de Physalaemus cuvieri (Anura: Leiuperidae). Pesticidas: Revista de Ecotoxicologia e Meio Ambiente 23, 1-10, 2013.
  53. SPADOTTO, C.A., GOMES, M.A.F., LUCHINI, L.C., ANDRÉA, M.M. Monitoramento do risco ambiental de agrotóxicos: princípios e recomendações. Embrapa Meio Ambiente: Jaguariúna. ISSN 1516-4691, 29 p, 2004.
  54. SPARLING, D.W., BICKMAN, J., COWMAN, D., FELLERS, G.M., LACHER, T., MATSON, C.W., MCCONNELL, L. In situ effects of pesticides on amphibians in the Sierra Nevada. Ecotoxicology 24, 262-278, 2014.
  55. SZÉKELY, D., DENOËL, M., SZÉKELY, P., COGĂLNICEANU, D. Pond drying cues and their effects on growth and metamorphosis in a fast developing amphibian. Journal of Zoology 303, 129-135, 2017.
  56. THOMPSON, D.G., WOJTASZEK, B.F., STAZNIK, B., CHARTRAND, D.T., STEPHENSON, G.R. Chemical and biomonitoring to assess potential acute effects of vision® herbicide on native amphibian larvae in forest wetlands. Environmental Toxicology and Chemistry 23, 843-849, 2004.
  57. VANZETTO, G.V., SLAVIERO, J., STURZA, P.F., RUTKOSKI, C.F., MACAGNAN, N., KOLCENTI, C., HARTMANN, P.A., FERREIRA, C.M., HARTMANN, M.T. Toxic effects of pyrethroids in tadpoles of Physalaemus gracilis (Anura: Leptodactylidae). Ecotoxicology 28, 1105-1114, 2019.
  58. VENTURINO, A., ROSENBAUM, E., CASTRO, A.C., ANGUIANO, O.L., GAUNA, L., SCHROEDER, T.F., D'ANGELO, A.M.P. 2003 Biomarkers of effect in toads and frogs. Biomarkers 8, 167-186, 2003.
  59. WOJTASZEK B.F., STAZNIK, B., CHARTRAND, D.T., STEPHENSON, G.R., THOMPSON, D.G. Effects of Vision herbicide on mortality, avoidance response, and growth of amphibian larvae in two forest wetlands. Environmental Toxicology and Chemistry 23, 832-842, 2004.
  60. WRUBLESWSKI J., REICHERT JR, F.W., GALON, L., HARTMANN, P.A., HARTMANN, M.T. Acute and chronic toxicity of pesticides on tadpoles of Physalaemus cuvieri (Anura, Leptodactylidae). Ecotoxicology 27, 360-368, 2018.

Como Citar

Marion, G. A. N. ., Müller, C., Hartmann, P. A., & Hartmann, M. T. . (2023). In situ works on ecotoxicology in amphibians: current state of the art. Scientific Electronic Archives, 16(5).