Impact of organophosphate pesticides on anurans: a mini review
DOI:
https://doi.org/10.11160/bah.309Keywords:
anurans, ecotoxicology, insecticides, pollutants, sub-lethal effectsAbstract
Organophosphate pesticides (OPs) are a group of widely used insecticides in agriculture and vector control. The primary mechanism of action of OPs is the inhibition of acetylcholinesterase (AChE), leading to the accumulation of acetylcholine and disruption of neural transmission. As acetylcholine acts as neurotransmitter in most animal groups, exposure to OPs has raised increasing ecological concerns due to their toxicity to non-target organisms. Among vertebrates, amphibians are particularly vulnerable to OP exposure given their dual life cycle, which makes them susceptible to contamination in both water and lands. The impairment of neural transmission by OPs can result in behavioral impairments such as abnormal swimming and decreased predator avoidance, ultimately reducing individual fitness and survival. Exposure to OPs also poses developmental risks, causing morphological abnormalities, delayed metamorphosis and reduced growth. Liver and muscle tissues exhibit histopathological changes, indicating systemic stress, while exposure to even low concentrations impairs immune function, increasing susceptibility to infection and reducing resistance against environmental stressors. This mini review synthesizes findings from peer-reviewed studies and reviews published in the last 10 years about the impact of OPs on amphibians, with special focus on anurans as the most studied group in this context. Despite the thematic evolution of ecotoxicology towards more ecology-focused studies, the fact that OPs are not emerging pesticides has somehow excluded them from this pattern. However, OP toxicity to anurans is still of concern, hence future research should prioritize field-based assessments, long-term studies, and species-specific sensitivity to better understand the ecological implications of OP exposure.
References
Acquaroni, M.; Svartz, G. & Pérez Coll, C. (2022). Acute, chronic and neurotoxic effects of dimethoate pesticide on Rhinella arenarum throughout the development. Journal of Environmental Science and Health B 57: 142-152.
Ali, N.; Kalsoom, Khan, S.; Ihsanullah, Rahman, I.U. & Muhammad, S. (2018). Human health risk assessment through consumption of organophosphate pesticide-contaminated water of Peshawar Basin, Pakistan. Exposure and Health 10: 259-272.
Aroniadou-Anderjaska, V.; Figueiredo, T.H.; De Araujo Furtado, M.; Pidoplichko, V.I. & Braga, M.F.M. (2023). Mechanisms of organophosphate toxicity and the role of acetylcholinesterase inhibition. Toxics 11: 866.
Ascoli-Morrete, T.; Bandeira, N.M.G.; Signor, E., Gazola, H.A.; Homrich, I. S.; Biondo, R., Rossato-Grando, L.G. & Zanella, N. (2022). Bioaccumulation of pesticides and genotoxicity in anurans from southern Brazil. Environmental Science and Pollution Research 29: 45549-45559.
Atkinson, C.L.; Knapp, D.D. & Smith, L.L. (2021). Long-term patterns of amphibian diversity, abundance and nutrient export from small, isolated wetlands. Diversity 13: 598.
Attademo, A.M.; Peltzer, P.M.; Lajmanovich, R.C.; Cabagna-Zenklusen, M.; Junges, C.M.; Lorenzatti, E.; Aró, C. & Grenón, P. (2015). Biochemical changes in certain enzymes of Lysapsus limellium (Anura: Hylidae) exposed to chlorpyrifos. Ecotoxicology and Environmental Safety 113: 287-294.
Attademo, A.M.; Sanchez-Hernandez, J.C.; Lajmanovich, R.C.; Peltzer, P.M. & Junges, C. (2017). Effect of diet on carboxylesterase activity of tadpoles (Rhinella arenarum) exposed to chlorpyrifos. Ecotoxicology and Environmental Safety 135: 10-16.
Awkerman, J.A.; Glinski, D.A.; Henderson, W.M.; Meter, R.V. & Purucker, S.T. (2024). Framework for multi-stressor physiological response evaluation in amphibian risk assessment and conservation. Frontiers in Ecology and Evolution 12: 1336747.
Baker, E.S.; Moon, K.J. & Branco, R.C. (2024). Chlorpyrifos: who paid and who profited? Environmental Justice 17: 79-84.
Balali-Mood, M.; Balali-Mood, K.; Moodi, M. & Balali-Mood, B. (2012). Health aspects of organophosphorous pesticides in Asian countries. Iranian Journal of Public Health 41: 1-14.
Bandara, M.G.D.K.; Wijesinghe, M.R.; Ratnasooriya, W.D. & Priyani, A.A.H. (2012). Chlorpyrifos-induced histopathological alterations in Duttaphrynus melanostictus (Schneider 1799) tadpoles: evidence from empirical trials. Journal of Tropical Forestry and Environment 2: 27-36.
Barreto, E.; Salgado Costa, C.; Demetrio, P.; Lascano, C.; Venturino, A. & Natale, G.S. (2020). Sensitivity of Boana pulchella (Anura: Hylidae) tadpoles to environmentally relevant concentrations of chlorpyrifos: Effects at the individual and biochemical levels. Environmental Toxicology and Chemistry 39: 834-841.
Beasley, V.R. (2020). Direct and indirect effects of environmental contaminants on amphibians. In Reference Module in Earth Systems and Environmental Sciences Elsevier, 112746.
Bernabò, I.; Gallo, L.; Sperone, E.; Tripepi, S. & Brunelli, E. (2011a). Survival, development, and gonadal differentiation in Rana dalmatina chronically exposed to chlorpyrifos. Journal of Experimental Zoology A 315: 314-327.
Bernabò, I., Sperone, E., Tripepi, S. & Brunelli, E. (2011b). Toxicity of chlorpyrifos to larval Rana dalmatina: acute and chronic effects on survival, development, growth and gill apparatus. Archives of Environmental Contamination and Toxicology 61: 704-718.
Bernal-González, K.G.; Covantes-Rosales, C.E.; Camacho-Pérez, M.R.; Mercado-Salgado, U.; Barajas-Carrillo, V.W.; Girón-Pérez, D.A.; Montoya-Hidalgo, A.C.; Díaz-Resendiz, K.J.G.; Barcelos-García, R.G.; Toledo-Ibarra, G.A. & Girón-Pérez, M.I. (2023). Organophosphate pesticide-mediated immune response modulation in invertebrates and vertebrates. International Journal of Molecular Sciences 24: 5360.
Bondareva, L. & Fedorova, N. (2021). Pesticides: Behavior in agricultural soil and plants. Molecules 26: 5370.
Borković-Mitić, S.S.; Prokić, M.D.; Krizmanić, I.I.; Mutić, J.; Trifković, J.; Gavrić, J.; Despotović, S.G.; Gavrilović, B.R.; Radovanović, T.B.; Pavlović, S.Z. & Saičić, Z.S. (2016). Biomarkers of oxidative stress and metal accumulation in marsh frog (Pelophylax ridibundus). Environmental Science and Pollution Research 23: 9649-9659.
Brühl, C.A.; Schmidt, T.; Pieper, S. & Alscher, A. (2013). Terrestrial pesticide exposure of amphibians: An underestimated cause of global decline? Scientific Reports 3: 1135.
Camacho-Pérez, M.R.; Covantes-Rosales, C.E.; Toledo-Ibarra, G.A.; Mercado-Salgado, U.; Ponce-Regalado, M.D.; Díaz-Resendiz, K.J.G. & Girón-Pérez, M.I. (2022). Organophosphorus pesticides as modulating substances of inflammation through the cholinergic pathway. International Journal of Molecular Sciences 23: 4523.
CCOHS (2018). What is a LD₅₀ and LC₅₀? Canadian Centre for Occupational Health and Safety, Hamilton, Canada. Available at https://www.ccohs.ca/oshanswers/chemicals/ld50.html. Retrieved on 03 January 2025.
Cohn, J. & MacPhail, R.C. (1996). Ethological and experimental approaches to behavior analysis: implications for ecotoxicology. Environmental Health Perspectives 104: 299-305.
Costa, C.S.; Rimoldi, F.; Pantucci Saralegui, M.J.; Rubio Puzzo, M.L.; Trudeau, V.L. & Natale, G.S. (2021). Disruptive effects of chlorpyrifos on predator-prey interactions of Ceratophrys ornata tadpoles: Consequences at the population level using computational modeling. Environmental Pollution 285: 117344.
Curi, L.M.; Cuzziol Boccioni, A.P.; Peltzer, P.M.; Attademo, A.M.; Bassó, A.; León, E.J. & Lajmanovich, R.C. (2022). Signals from predators, injured conspecifics, and pesticide modify the swimming behavior of the gregarious tadpole of the Dorbigny’s Toad, Rhinella dorbignyi (Anura: Bufonidae). Canadian Journal of Zoology 100: 19-27.
David, M. & Kartheek, R.M. (2015). Malathion acute toxicity in tadpoles of Duttaphrynus melanostictus, morphological and behavioural study. The Journal of Basic and Applied Zoology 72: 1-7.
David, M.; Marigoudar, S.R.; Patil, V.K. & Halappa, R. (2012). Behavioral, morphological deformities and biomarkers of oxidative damage as indicators of sublethal cypermethrin intoxication on the tadpoles of D. melanostictus (Schneider, 1799). Pesticide Biochemistry and Physiology 103: 127-134.
David, M.; Kartheek, R.M. & Manjunath, G.P. (2018). Acute and sublethal toxicity of chlorpyrifos on developmental stages of Dattaphrynus melanostictus. Journal of Applied Pharmaceutical Science 8: 87-93.
Davidson, C. (2004). Declining downwind: Amphibian population declines in California and historical pesticide use. Ecological Applications 14: 1892-1902.
Denoël, M.; D’Hooghe, B.; Ficetola, G.F.; Brasseur, C.; De Pauw, E.; Thomé, J.P. & Kestemont, P. (2012). Using sets of behavioral biomarkers to assess short-term effects of pesticide: A study case with endosulfan on frog tadpoles. Ecotoxicology 21: 1240-1250.
Dhas, S. & Srivastava, M. (2010). An assessment of carbaryl residues on brinjal crop in an agricultural field in Bikaner, Rajasthan (India). Asian Journal of Agricultural Sciences 2: 15-17.
FAO (2024). Pesticides Use and Trade. 1990–2022. Food and Agricultural Organization of the United Nations, Rome, Italy. Available at https://www.fao.org/statistics/highlights-archive/highlights-detail/pesticides-use-and-trade-1990-2022/en. Retrieved on 03 January 2025.
Garcês, A.; Pires, I. & Rodrigues, P. (2020). Teratological effects of pesticides in vertebrates: A review. Journal of Environmental Science and Health B 55: 75-89.
Ghodageri, M.G. & Pancharatna, K. (2011). Morphological and behavioral alterations induced by endocrine disrupters in amphibian tadpoles. Toxicological and Environmental Chemistry 93: 2012-2021.
Giri, A.; Yadav, S.S.; Giri, S. & Sharma, G.D. (2012). Effect of predator stress and malathion on tadpoles of Indian skittering frog. Aquatic Toxicology 106-107: 157-163.
Goessens, T.; De Baere, S.; Deknock, A.; De Troyer, N.; Van Leeuwenberg, R.; Martel, A.; Pasmans, F.; Goethals, P.; Lens, L.; Spanoghe, P.; Vanhaecke, L. & Croubels, S. (2022). Agricultural contaminants in amphibian breeding ponds: Occurrence, risk and correlation with agricultural land use. Science of The Total Environment 806: 150661.
Gordillo, L.; Quiroga, L.; Ray, M. & Sanabria, E. (2024). Changes in thermal sensitivity of Rhinella arenarum tadpoles (Anura: Bufonidae) exposed to sublethal concentrations of different pesticide fractions (Lorsban® 75WG). Journal of Thermal Biology 120: 103816.
Hasan, G.M.M.A.; Das, A.K.; Satter, M.A. & Asif, M. (2022). Bioaccumulation of organophosphorus (OPs) and carbamate (CBs) residues in cultured Pangas Catfish (Pangasius pangasius) and health risk assessment. Journal of Toxicology 1: 4644227.
Hayes, T.B.; Case, P.; Chui, S.; Chung, D.; Haeffele, C.; Haston, K.; Lee, M.; Mai, V.P.; Marjuoa, Y.; Parker, J. & Tsui, M. (2006). Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environmental Health Perspectives 114: 40-50.
Hayes, T.B.; Khoury, V.; Narayan, A.; Nazir, M.; Park, A.; Brown, T.; Adame, L.; Chan, E.; Buchholz, D.; Stueve, T. & Gallipeau, S. (2010). Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proceedings of the National Academy of Sciences 107: 4612-4617.
Henao, L.M.; Mendez, J.J. & Bernal, M.H. (2022). UVB radiation enhances the toxic effects of three organophosphorus insecticides on tadpoles from tropical anurans. Hydrobiologia 849: 141-153.
Henao Muñoz, L.M.; Triana Velásquez, T.M.; Galindo Martínez, C.A. & Bernal Bautista, M.H. (2020). Toxicity of three organophosphate insecticides in anuran embryos at different temperatures. Acta Biológica Colombiana 26: 5-11.
Herek, J.S.; Vargas, L.; Rinas Trindade, S.A.; Rutkoski, C.F.; Macagnan, N.; Hartmann, P.A. & Hartmann, M.T. (2021). Genotoxic effects of glyphosate on Physalaemus tadpoles. Environmental Toxicology and Pharmacology 81: 103516.
Hocking, D.J. & Babbitt, K.J. (2014). Amphibian contributions to ecosystem services. Herpetological Conservation and Biology 9: 1-17.
Jayawardena, U.A.; Navaratne, A.N.; Amerasinghe, P.H. & Rajakaruna, R.S. (2011). Acute and chronic toxicity of four commonly used agricultural pesticides on the Asian common toad, Bufo melanostictus Schneider. Journal of the National Science Foundation of Sri Lanka 39: 267.
Junges, C.M.; Maglianese, M.I.; Lajmanovich, R.C.; Peltzer, P.M. & Attademo, A.M. (2017). Acute toxicity and etho-toxicity of three insecticides used for mosquito control on amphibian tadpoles. Water, Air, & Soil Pollution 228: 143.
Kaur, R.; Mavi, G.K.; Raghav, S. & Khan, I. (2019). Pesticides classification and its impact on environment. International Journal of Current Microbiology and Applied Sciences 8: 1889-1897.
Kharkongor, M.; Hooroo, R.N.K. & Dey, S. (2018). Effects of the insecticide chlorpyrifos, on hatching, mortality and morphology of Duttaphrynus melanostictus embryos. Chemosphere 210: 917-921.
Koo, M.S.; Vredenburg, V.T.; Gross, J.; Spencer, C.L.; Tunstall, T. & Wake, D.B. (2013). Visualizing AmphibiaWeb Data with Continuous Cartograms. AmphibiaWeb: Information on Amphibian Biology and Conservation, Berkeley, California, USA. Available at https://amphibiaweb.org/amphibian/cartograms/. Retrieved on 05 July 2025.
Kundu, C.R.; Roychoudhury, S. & Capcarova, M. (2011). Malathion-induced sublethal toxicity on the intestine of cricket frog (Fejervarya limnocharis). Journal of Environmental Science and Health B 46: 691-696.
Lajmanovich, R.C.; Attademo, A.M.; Simoniello, M.F.; Poletta, G.L.; Junges, C.M.; Peltzer, P.M.; Grenón, P. & Cabagna-Zenklusen, M.C. (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 Pollution 226: 427.
Lawrence, E., & Isioma, T. (2010). Acute toxic effects of endosulfan and diazinon pesticides on adult amphibians (Bufo regularis). Journal of Environmental Chemistry and Ecotoxicology 2: 73-78.
Lee, T.H.Y.; Chuah, J. & Snyder, S.A. (2022). Occurrence of emerging contaminants in southeast asian environments: present status, challenges, and future prospects. ACS ES&T Water 2: 907-931.
Leemans, M.; Couderq, S.; Demeneix, B. & Fini, J.B. (2019). Pesticides with potential thyroid hormone-disrupting effects: a review of recent data. Frontiers in Endocrinology 10: 743.
Li, B.; Ma, Y. & Zhang, Y.H. (2017). Oxidative stress and hepatotoxicity in the frog, Rana chensinensis, when exposed to low doses of trichlorfon. Journal of Environmental Science and Health B 52: 476-482.
Liendro, N.; Ferrari, A.; Mardirosian, M.; Lascano, C.I. & Venturino, A. (2015). Toxicity of the insecticide chlorpyrifos to the South American toad Rhinella arenarum at larval developmental stage. Environmental Toxicology and Pharmacology 39: 525-535.
Luedtke, J.A.; Chanson, J.; Neam, K.; Hobin, L.; Maciel, A.O.; Catenazzi, A.; Borzée, A.; Hamidy, A.; Aowphol, A.; Jean, A.; Sosa-Bartuano, Á.; Fong, A.G.; de Silva, A.; Fouquet, A.; Angulo, A.; Kidov, A.A.; Muñoz Saravia, A.; Diesmos, A.C.; Tominaga, A.; Shrestha, B.; Gratwicke, B.; Tjaturadi, B.; Martínez Rivera, C.C.; Vásquez Almazán, C.R.; Señaris, C.; Chandramouli, S.R.; Strüssmann, C.; Cortez Fernández, C.F.; Azat, C.; Hoskin, C.J.; Hilton-Taylor, C.; Whyte, D.L.; Gower, D.J.; Olson, D.H.; Cisneros-Heredia, D.F.; Santana, D.J.; Nagombi, E.; Najafi-Majd, E.; Quah, E.S.H.; Bolaños, F.; Xie, F.; Brusquetti, F.; Álvarez, F.S.; Andreone, F.; Glaw, F.; Castañeda, F.E.; Kraus, F.; Parra-Olea, G.; Chaves, G.; Medina-Rangel, G.F.; González-Durán, G.; Ortega-Andrade, H.M.; Machado, I.F.; Das, I.; Dias, I.R.; Urbina-Cardona, J.N.; Crnobrnja-Isailović, J.; Yang, J.-H.; Jianping, J.; Wangyal, J.T.; Rowley, J.J.L.; Measey, J.; Vasudevan, K.; Chan, K.O.; Gururaja, K.V.; Ovaska, K.; Warr, L.C.; Canseco-Márquez, L.; Toledo, L.F.; Díaz, L.M.; Khan, M.M.H.; Meegaskumbura, M.; Acevedo, M.E.; Napoli, M.F.; Ponce, M.A.; Vaira, M.; Lampo, M.; Yánez-Muñoz, M.H.; Scherz, M.D.; Rödel, M.-O.; Matsui, M.; Fildor, M.; Kusrini, M.D.; Ahmed, M.F.; Rais, M.; Kouamé, N.G.; García, N.; Gonwouo, N.L.; Burrowes, P.A.; Imbun, P.Y.; Wagner, P.; Kok, P.J.R.; Joglar, R.L.; Auguste, R.J.; Brandão, R.A.; Ibáñez, R.; von May, R.; Hedges, S.B.; Biju, S.D.; Ganesh, S.R.; Wren, S.; Das, S.; Flechas, S.V.; Robleto-Hernández, S.J.; Loader, S.P.; Incháustegui, S.J.; Garg, S.; Phimmachak, S.; Richards, S.J.; Slimani, T.; Osborne-Naikatini, T.; Abreu-Jardim, T.P.F.; Condez, T.H.; De Carvalho, T.R.; Cutajar, T.P.; Pierson, T.W.; Nguyen, T.Q.; Kaya, U.; Yuan, Z.; Long, B.; Langhammer, P. & Stuart, S.N. (2023). Ongoing declines for the world’s amphibians in the face of emerging threats. Nature 622: 308-314.
Lutz, I. & Kloas, W. (1999). Amphibians as a model to study endocrine disruptors: I. Environmental pollution and estrogen receptor binding. Science of the Total Environment 225: 49-57.
Ma, Y.; Li, B.; Ke, Y. & Zhang, Y. (2019). Effects of low doses trichlorfon exposure on Rana chensinensis tadpoles. Environmental Toxicology 34: 30-36.
Mackay, D.; Giesy, J.P. & Solomon, K.R. (2014). Fate in the environment and long-range atmospheric transport of the organophosphorus insecticide, chlorpyrifos and its oxon. Reviews of Environmental Contamination and Toxicology 231: 35-76
Mahananda M.R. & Mohanty B.P. (2012). Toxicity on biochemical and hematological parameters in Bufo melanostictus (Schneider) (Common Indian Toad) exposed to malathion, In R.P. Soundararajan (ed.) Pesticides - Advances in Chemical and Botanical Pesticides. InTech, London, UK, pp. 24-30.
Majumder, R. (2024). Acute toxicity of chlorpyrifos to some non-target freshwater organisms: which one is more toxic—technical grade or commercial formulation? Ecotoxicology 33: 1171-1179.
Marrone, P.G. (2019). Pesticidal natural products – status and future potential. Pest Management Science 75: 2325-2340.
McClelland, S.J. & Woodley, S.K. (2022). Developmental exposure to trace concentrations of chlorpyrifos results in nonmonotonic changes in brain shape and behavior in amphibians. Environmental Science & Technology 56: 9379-9386.
McClelland, S.J.; Bendis, R.J.; Relyea, R.A. & Woodley, S.K. (2018). Insecticide-induced changes in amphibian brains: How sublethal concentrations of chlorpyrifos directly affect neurodevelopment. Environmental Toxicology and Chemistry 37: 2692-2698.
Mikó, Z.; Bókony, V.; Ujhegyi, N.; Nemesházi, E.; Erös, R.; Orf, S. & Hettyey, A. (2021). Effects of chlorpyrifos on early development and anti-predator behavior of agile frogs. bioRxiv 2021: 11.03.467073.
Miyata, K. & Ose, K. (2012). Thyroid hormone-disrupting effects and the amphibian metamorphosis assay. Journal of Toxicologic Pathology 25: 1-9.
Monroe, M.J.; South, S.H.; & Alonzo, S.H. (2015). The evolution of fecundity is associated with female body size but not female‐biased sexual size dimorphism among frogs. Journal of Evolutionary Biology 28: 1793-1803.
Ortega-Andrade, H.M.; Rodes Blanco, M.; Cisneros-Heredia, D.F.; Guerra Arévalo, N.; López de Vargas-Machuca, K.G.; Sánchez-Nivicela, J.C.; Armijos-Ojeda, D.; Cáceres Andrade, J.F.; Reyes-Puig, C.; Quezada Riera, A.B.; Székely, P.; Rojas Soto, O.R.; Székely, D.; Guayasamin, J.M.; Siavichay Pesántez, F.R.; Amador, L.; Betancourt, R.; Ramírez-Jaramillo, S.M.; Timbe-Borja, B.; Gómez Laporta, M.; Webster Bernal, J.F.; Oyagata Cachimuel, L.A.; Chávez Jácome, D.; Posse, V.; Valle-Piñuela, C.; Padilla Jiménez, D.; Reyes-Puig, J.P.; Terán-Valdez, A.; Coloma, L.A.; Pérez Lara, M.B.; Carvajal-Endara, S.; Urgilés, M. & Yánez Muñoz, M.H. (2021). Red List assessment of amphibian species of Ecuador: A multidimensional approach for their conservation. PLoS ONE 16: e0251027.
Ortiz‐Santaliestra, M.E.; Maia, J.P.; Egea‐Serrano, A.; Brühl, C.A. & Lopes, I. (2017). Biological relevance of the magnitude of effects (considering mortality, sub‐lethal and reproductive effects) observed in studies with amphibians and reptiles in view of population level impacts on amphibians and reptiles. EFSA Supporting Publications 14: 1251.
Peltzer, P.M.; Junges, C.M.; Attademo, A.M.; Bassó, A.; Grenón, P. & Lajmanovich, R.C. (2013). Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) tadpoles exposed to glufosinate ammonium herbicide. Ecotoxicology 22: 1165-1173.
Pérez-Iglesias, J.M.: Natale, G.S.; Soloneski, S. & Larramendy, M.L. (2018). Are the damaging effects induced by the imazethapyr formulation Pivot® H in Boana pulchella (Anura) reversible upon ceasing exposure? Ecotoxicology and Environmental Safety 148: 1-10.
Poulsen, R.; Luong, X.; Hansen, M.; Styrishave, B. & Hayes, T. (2015). Tebuconazole disrupts steroidogenesis in Xenopus laevis. Aquatic Toxicology 168: 28-37.
Quiroga, L.B.; Sanabria, E.A.; Fornés, M.W.; Bustos, D.A. & Tejedo, M. (2019). Sublethal concentrations of chlorpyrifos induce changes in the thermal sensitivity and tolerance of anuran tadpoles in the toad Rhinella arenarum? Chemosphere 219: 671-677.
Rahman, S. & Chima, C. (2018). Determinants of pesticide use in food crop production in southeastern Nigeria. Agriculture 8: 35.
Ramadani, S.; Marhendra, A.P.W.; Wiadnya, D.G.R. & Kurniawan, N. (2022). Effect of acute toxicity of commercial organophosphate insecticide based on chlorpyrifos on Fejervarya limnocharis tadpoles (Anura: Dicroglossidae). Journal of Tropical Life Science 12: 231-240.
Rimoldi, F.; Salgado Costa, C.; Pantucci Saralegui, M.J.; Bahl, M.F. & Natale, G.S. (2023). Recovery of Ceratophrys ornata tadpoles exposed to environmental concentrations of chlorpyrifos: Evaluation of biomarkers of exposure. Ecotoxicology 32: 638-645.
Roach, N.S.; Urbina-Cardona, N. & Lacher, T.E. (2020). Land cover drives amphibian diversity across steep elevational gradients in an isolated neotropical mountain range: Implications for community conservation. Global Ecology and Conservation 22: e00968.
Rutkoski, C.F.; Macagnan, N.; Folador, A.; Skovronski, V.J.; Do Amaral, A.M.B.; Leitemperger, J.; Costa, M.D.; Hartmann, P.A.; Müller, C.; Loro, V.L. & Hartmann, M.T. (2020). Morphological and biochemical traits and mortality in Physalaemus gracilis (Anura: Leptodactylidae) tadpoles exposed to the insecticide chlorpyrifos. Chemosphere 250: 126162.
Salgado Costa, C.; Ronco, A.E.; Trudeau, V.L.; Marino, D. & Natale, G.S. (2018). Tadpoles of the horned frog Ceratophrys ornata exhibit high sensitivity to chlorpyrifos for conventional ecotoxicological and novel bioacoustic variables. Environmental Pollution 235: 938-947.
Samojeden, C.G.; Pavan, F.A.; Rutkoski, C.F.; Folador, A.; Da Fré, S.P.; Müller, C.; Hartmann, P.A. & Hartmann, M. (2022). Toxicity and genotoxicity of imidacloprid in the tadpoles of Leptodactylus luctator and Physalaemus cuvieri (Anura: Leptodactylidae). Scientific Reports 12: 11926.
Santos, T.; Melo, R.; Costa-Silva, D.; Nunes, M.; Rodrigues, N. & Franco, J. (2015). Assessment of water pollution in the Brazilian Pampa biome by means of stress biomarkers in tadpoles of the leaf frog Phyllomedusa iheringii (Anura: Hylidae). PeerJ 3: e1016.
Schavinski, C.R.; Santos, M.B.D.; Londero, J.E.L.; Rocha, M.C.D.; Amaral, A.M.B.D.; Ruiz, N.Q.; Leandro, G.D.S.; Loro, V.L. & Schuch, A.P. (2022). Effects of isolated and combined exposures of Boana curupi (Anura: Hylidae) tadpoles to environmental doses of trichlorfon and ultraviolet radiation. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 883-884: 503549.
Segalla, M.V.; Berneck, B.; Canedo, C.; Caramaschi, U.; Cruz, C.A.G.; Garcia, P.C.A.; Grant, T.; Haddad, C.F.B.; Lourenço, A.C.C.; Mângia, S.; Mott, T.; Nascimento, L.B.; Toledo, L.F.; Werneck, F.P. & Langone, J.A. (2021). List of Brazilian amphibians. Herpetologia Brasileira 10: 121-216.
Sharma, A.; Shukla, A.; Attri, K.; Kumar, M.; Kumar, P.; Suttee, A.; Singh, G.; Barnwal, R.P. & Singla, N. (2020). Global trends in pesticides: A looming threat and viable alternatives. Ecotoxicology and Environmental Safety 201: 110812.
Sidhu, G.K.; Singh, S.; Kumar, V.; Dhanjal, D.S.; Datta, S. & Singh, J. (2019). Toxicity, monitoring and biodegradation of organophosphate pesticides: A review. Critical Reviews in Environmental Science and Technology 49: 1135-1187.
Silva, M.B.D., Fraga, R.E., Silva, F.L., Oliveira, L.A.A.D., Queiroz, T.S.D., Rocha, M.A., & Juncá, F.A. (2020a). Effects of acute exposure of chlorpyrifos on the survival, morphology and swimming ability of Odontophrynus carvalhoi tadpoles. Ecotoxicology and Environmental Contamination 15: 37-42.
Silva, M.B.D., Fraga, R.E., Nishiyama, P.B., Silva, I.S.S.D., Costa, N.L.B., De Oliveira, L.A.A., Rocha, M.A., & Juncá, F.A. (2020b). Leukocyte profiles in Odontophrynus carvalhoi (Amphibia: Odontophrynidae) tadpoles exposed to organophosphate chlorpyrifos pesticides. Water, Air, & Soil Pollution 231: 372.
Simon-Delso, N.; Amaral-Rogers, V.; Belzunces, L.P.; Bonmatin, J.M.; Chagnon, M.; Downs, C.; Furlan, L.; Gibbons, D.W.; Giorio, C.; Girolami, V.; Goulson, D.; Kreutzweiser, D.P.; Krupke, C.H.; Liess, M.; Long, E.; McField, M.; Mineau, P.; Mitchell, E.A.D.; Morrissey, C.A.; Noome, D.A.; Pisa, L.; Settele, J.; Stark, J.D.; Tapparo, A.; Van Vyck, H.; Van Praagh, J.; Van der Sluijs, J.P.; Whitehorn, P.R. & Wiemers, M. (2015). Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22: 5-34.
Sotomayor, V.; Lascano, C.; De D’Angelo, A.M.P. & Venturino, A. (2012). Developmental and polyamine metabolism alterations in Rhinella arenarum embryos exposed to the organophosphate chlorpyrifos. Environmental Toxicology and Chemistry 31: 2052-2058.
Sparling, D.W.; Fellers, G. & McConnell, L. (2001). Pesticides are involved with population declines of amphibians in the California Sierra Nevadas. The Scientific World Journal 1: 200-201.
Srivastav, A.K.; Srivastava, S.; Srivastav, S.K. & Suzuki, N. (2017). Acute toxicity of an organophosphate insecticide chlorpyrifos to an anuran, Rana cyanophlyctis. Iranian Journal of Toxicology 11: 45-49.
Srivastav, A.K.; Srivastav, S.; Srivastav, S.K. & Suzuki, N. (2018). Alterations in the serum electrolytes of the Indian Skipper Frog Euphlyctis cyanophlyctis caused by an organophosphate pesticide: Chlorpyrifos. Jordan Journal of Biological Sciences 11: 395-399.
Statista (2024a). Agricultural Consumption of Pesticides Worldwide from 1990 to 2022. Statista Research Department, New York, USA. Available at https://www.statista.com/statistics/1263077/global-pesticide-agricultural-use/. Retrieved on 05 January 2025.
Statista (2024b). Forecast agricultural consumption of pesticides worldwide from 2023 to 2027. Statista Research Department, New York, USA. Available at https://www.statista.com/statistics/1401556/global-agricultural-use-of-pesticides-forecast/. Retrieved on 05 January 2025.
Suratman, S.; Edwards, J.W. & Babina, K. (2015). Organophosphate pesticides exposure among farmworkers: Pathways and risk of adverse health effects. Reviews on Environmental Health 30: 65-79.
Svartz, G.; Meijide, F. & Pérez Coll, C. (2016). Effects of a fungicide formulation on embryo-larval development, metamorphosis, and gonadogenesis of the South American toad Rhinella arenarum. Environmental Toxicology and Pharmacology 45: 1-7.
Szuroczki, D.; Koprivnikar, J. & Baker, R.L. (2019). Effects of dietary antioxidants and environmental stressors on immune function and condition in Lithobates (Rana) sylvaticus. Comparative Biochemistry and Physiology A 229: 25-32.
Tabb, M.M. & Blumberg, B. (2006). New modes of action for endocrine-disrupting chemicals. Molecular Endocrinology 20: 475-482.
Tesi, G.O.; Okpara, K.E.; Tesi, J.N.; Agbozu, I.E. & Techato, K. (2025). Assessment of organophosphate pesticides in soils and vegetables from agricultural areas of Delta Central District, Nigeria. Scientific Reports 15: 8267.
Venturino, A.; Rosenbaum, E.; Caballero de Castro, A.; Anguiano, O.L.; Gauna, L.; Fonovich de Schroeder, T. & Pechen de D’Angelo, A.M. (2003). Biomarkers of effect in toads and frogs. Biomarkers 8: 167-186.
Wang, A.; Cockburn, M.; Ly, T.T.; Bronstein, J.M. & Ritz, B. (2014). The association between ambient exposure to organophosphates and Parkinson’s disease risk. Occupational and Environmental Medicine 71: 275-281.
Wang, A.; Liu, Y.; Yan, Y.; Jiang, Y.; Shi, S.; Wang, J.; Qiao, K.; Yang, L.; Wang, S.; Li, S. & Gui, W. (2025). Chlorpyrifos influences tadpole development by disrupting thyroid hormone signaling pathways. Environmental Science & Technology 59: 142-151.
West, J. (2018). Importance of Amphibians: a Synthesis of their Environmental Functions, Benefits to Humans, and Need for Conservation. Honors Program Thesis, Bridgewater State University, Bridgewater, Massachusetts, USA.
Wisnujati, N.S. (2023). Unveiling the epoch: exploring pesticide utilization and trade trends globally and regionally from 1990 to 2020. SCIENTIA: Journal of Multi Disciplinary Science 2: 108-121.
Womack, M.C.; Steigerwald, E.; Blackburn, D.C.; Cannatella, D.C.; Catenazzi, A.; Che, J.; Koo, M.S.; McGuire, J.A.; Ron, S.R.; Spencer, C.L.; Vredenburg, V.T. & Tarvin, R. D. (2022). State of the amphibia 2020: A review of five years of amphibian research and existing resources. Ichthyology & Herpetology 110: 638-661.
Zhang, Y.; Xiao, Z.; Chen, F.; Ge, Y.; Wu, J. & Hu, X. (2010). Degradation behavior and products of malathion and chlorpyrifos spiked in apple juice by ultrasonic treatment. Ultrasonics Sonochemistry 17: 72-77.
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