Abstract
Amphibians are declining around the world as they are particularly sensitive to multiple environmental stressors, among them the increase of UVB radiation and the environmental contaminations of body waters caused by agrochemicals. Because of the limited research on the interaction between agrochemicals and UVB radiation on tropical amphibians, we performed this study to test the hypothesis that the exposure to UVB radiation will enhance the toxic effects of the organophosphorus (OPs) insecticides chlorpyrifos, diazinon and monocrotophos, which are widely used in Colombia, on tadpoles from three tropical anuran species. Under laboratory conditions, we exposed independently tadpoles of Boana xerophylla, Engystomops pustulosus and Rhinella horribilis to each of the three insecticides with the presence of UVB radiation and without UVB, during 96 h toxicity tests. We then examined their effects on tadpole mortality, capacity to swim and total length. We found that UVB enhanced the mortality of insecticides (these treatments had a lower LC50 than those without UVB radiation), increased the tadpole immobility (they were unable to swim), and decreased the total length. Therefore, we validated the prediction that UVB radiation enhances the toxicity of the OPs insecticides studied on our anuran species and consequently may be one of the causal factors of amphibian population declines in the tropical countries. However, we suggest to perform more realistic field studies in areas with agrochemical presence to a better understanding of the effect of these stressors on anurans as there are environmental factors that attenuate underwater UVB radiation and toxicity in aquatic organisms, although it is also known that under field conditions some OPs insecticides become more toxic in the presence of UVB.
Similar content being viewed by others
Data availability
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Aggarwal, V., X. Deng, A. Tuli & K. S. Goh, 2013. Diazinon-chemistry and environmental fate: a California perspective. Reviews of Environmental Contamination and Toxicology 223: 107–140.
Agostini, M. G., I. Roesler, C. Bonetto, A. E. Ronco & D. Bilenca, 2020. Pesticides in the real world: the consequences of GMO-based intensive agriculture on native amphibians. Biological Conservation 241: 108355.
Ankley, G. T., S. J. Degitz, S. A. Diamond & J. E. Tietge, 2004. Assessment of environmental stressors potentially responsible for malformations in North American anuran amphibians. Ecotoxicology and Environmental Safety 58: 7–16.
Baker, N. J., B. A. Bancroft & T. S. Garcia, 2013. A meta-analysis of the effects of pesticides and fertilizers on survival and growth of amphibians. Science of the Total Environment 449: 150–156.
Bancroft, B. A., N. J. Baker, C. L. Searle, T. S. Garcia & A. R. Blaustein, 2008. Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behavioral Ecology 19: 879–886.
Barreto, E., C. Salgado Costa, P. Demetrio, C. Lascano, A. Venturino & G. S. Natale, 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.
Barron, M. G. & K. B. Woodburn, 1995. Ecotoxicology of chlorpyrifos. Reviews of Environmental Contamination and Toxicology 144: 1–93.
Beani, J. C., 2014. Ultraviolet A-induced DNA damage: role in skin cancer. Bulletin De L’academie Nationale De Medecine 198: 273–295.
Belden, L. K. & A. R. Blaustein, 2002. Exposure of red-legged frog embryos to ambient UV-B radiation in the field negatively affects larval growth and development. Oecologia 130: 551–554.
Belden, L. K., I. T. Moore, R. T. Mason, J. C., Wingfield & A. R. Blaustein, 2003. Survival, the hormonal stress response and UV-B avoidance in cascades frog tadpoles (Rana cascadae) exposed to UV-B radiation. Functional Ecology 17: 409–416.
Bernabó, I., E. Sperone, S. Tripepi & E. Brunelli, 2011. 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.
Blaustein, A. R. & B. A. Bancroft, 2007. Amphibian population declines: evolutionary considerations. BioScience 57: 437–444.
Blaustein, A. R. & L. K. Belden, 2003. Amphibian defenses against ultraviolet-B radiation. Evolution & Development 5: 89–97.
Blaustein, A. R. & J. M. Kiesecker, 2002. Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5: 597–608.
Blaustein, A. R., P. D. Hoffman, D. G. Hokit, J. M. Kiesecker, S. C. Walls & J. B. Hays, 1994. UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proceedings of the National Academy of Sciences 91: 1791–1795.
Blaustein, A. R., J. M. Romansic, J. M. Kiesecker & A. C. Hatch, 2003. Ultraviolet radiation, toxic chemicals and amphibian population declines. Diversity and Distributions 9: 123–140.
Bonfanti, P., A. Colombo, F. Orsi, I. Nizzetto, M. Andrioletti, R. Bacchetta & C. Vismara, 2004. Comparative teratogenicity of chlorpyrifos and malathion on Xenopus laevis development. Aquatic Toxicology 70: 189–200.
Bridges, C. M. & M. D. Boone, 2003. The interactive effects of UV-B and insecticide exposure on tadpole survival, growth and development. Biological Conservation 113: 49–54.
Brühl, C. A., S. Pieper & B. Weber, 2011. Amphibians at risk? Susceptibility of terrestrial amphibian life stages to pesticides. Environmental Toxicology and Chemistry 30: 2465–2472.
Choudhury, P. P. & S. Saha, 2020. Dynamics of pesticides under changing climatic scenario. Environmental Monitoring and Assessment 192: 1–3.
Cramp, R. L. & C. E. Franklin, 2018. Exploring the link between ultraviolet B radiation and immune function in amphibians: implications for emerging infectious diseases. Conservation Physiology 6: 035.
da Rocha, M. C., M. B. dos Santos, R. Zanella, O. D. Prestes, A. S. Gonçalves & A. P. Schuch, 2020. Preserved riparian forest protects endangered forest-specialists amphibian species against the genotoxic impact of sunlight and agrochemicals. Biological Conservation 249: 108746.
da Silva, M. B., R. E. Fraga, P. B. Nishiyama, I. S. S. da Silva, N. L. B. Costa, L. A. A. de Oliveira & F. A. Juncá, 2020. Leukocyte profiles in Odontophrynus carvalhoi (Amphibia: Odontophrynidae) tadpoles exposed to organophosphate chlorpyrifos pesticides. Water, Air, & Soil Pollution 231: 1–11.
dos Santos, C. P., J. E. L. Londero, M. B. Dos Santos, R. dos Santos Feltrin, L. Loebens, L. B. Moura & A. P. Schuch, 2018. Sunlight-induced genotoxicity and damage in keratin structures decrease tadpole performance. Journal of Photochemistry and Photobiology b: Biology 181: 134–142.
Egea-Serrano, A., R. A. Relyea, M. Tejedo & M. Torralva, 2012. Understanding of the impact of chemicals on amphibians: a meta-analytic review. Ecology and Evolution 2: 1382–1397.
ENA ENCUESTA NACIONAL AGROPECUARIA, 2019. Boletín Técnico. https://www.dane.gov.co/files/investigaciones/agropecuario/enda/ena/2019/boletin_ena_2019.pdf. Accessed 18 Mar 2021.
Fisher, M. C. & T. W. J. Garner, 2020. Chytrid fungi and global amphibian declines. Nature Reviews Microbiology 18: 332–343.
Giesy, J. P. & K. A. Solomon, 2014. Ecological risk assessment for chlorpyrifos in terrestrial and aquatic systems in North America. Reviews of Environmental Contamination and Toxicology 231: 1–269.
Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.
Greer, J. B., J. T. Magnuson, K. Hester, M. Giroux, C. Pope, T. Anderson & D. Schlenk, 2019. Effects of chlorpyrifos on cholinesterase and serine lipase activities and lipid metabolism in brains of rainbow trout (Oncorhynchus mykiss). Toxicological Sciences 172: 146–154.
Guayara-Barragán, M. G. & M. H. Bernal, 2012. Fecundidad y fertilidad en once especies de anuros colombianos con diferentes modos reproductivos. Caldasia 34: 483–496.
Guth, J. A., 1994. Monocrotophos-environmental fate and toxicity. Reviews of Environmental Contamination and Toxicology 139: 75–136.
Hamilton, M. A., R. C. Russo & R. V. Thurston, 1977. Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environmental Science & Technology 11: 714–719.
Harte, J., C. Holdren, R. Schneider & C. Shirley, 1991. Toxics A to Z: a guide to everyday pollution hazards, University of California Press, Berkeley:
Hatch, A. C. & A. R. Blaustein, 2000. Combined effects of UV-B, nitrate, and low pH reduce the survival and activity level of larval cascades frogs (Rana cascadae). Archives of Environmental Contamination and Toxicology 39: 494–499.
Hatch, A. C. & G. A. Burton Jr., 1998. Effects of photoinduced toxicity of fluoranthene on amphibian embryos and larvae. Environmental Toxicology and Chemistry: an International Journal 17: 1777–1785.
Hatch, A. C. & G. A. Burton Jr., 1999. Photo-induced toxicity of PAHs to Hyalella azteca and Chironomus tentans: effects of mixtures and behavior. Environmental Pollution 106: 157–167.
Hoffman, D. J., B. A. Rattner, G. A. Burton & J. Cairns (eds), 2003. Handbook of ecotoxicology., 2nd ed. Lewis Publishers, New York.
IUCN International Union for Conservation of Nature, 2020. The IUCN Red List of Threatened Species. Version 2020–2. https://www.iucnredlist.org. Accessed 9 July 2020.
Koponen, P. S. & J. V. Kukkonen, 2002. Effects of bisphenol A and artificial UVB radiation on the early development of Rana temporaria. Journal of Toxicology and Environmental Health Part A 65: 947–959.
Lajmanovich, R. C., A. M. Attademo, M. F. Simoniello, G. L. Poletta, C. M. Junges, P. M. Peltzer & M. C. Cabagna-Zenklusen, 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. & T. Isioma, 2010. Acute toxic effects of Endosulfan and Diazinon pesticides on adult amphibians (Bufo regularis). Journal of Environmental Chemistry and Ecotoxicology 2: 73–78.
Levis, N. A. & J. R. Johnson, 2015. Level of UV-B radiation influences the effects of glyphosate-based herbicide on the spotted salamander. Ecotoxicology 24: 1073–1086.
Little, E. E. & R. D. Calfee, 2010. Solar UV radiation and amphibians. Ecotoxicology of amphibians and reptiles, 2nd ed. CRC Press, New York:
Londero, J. E. L., M. B. Dos Santos & A. P. Schuch, 2019. Impact of solar UV radiation on amphibians: focus on genotoxic stress. Mutation Research/genetic Toxicology and Environmental Mutagenesis 842: 14–21.
Macias, G., A. Marco & A. R. Blaustein, 2007. Combined exposure to ambient UVB radiation and nitrite negatively affects survival of amphibian early life stages. Science of the Total Environment 385: 55–65.
Marco, A., M. Lizana, A. Alvarez & A. R. Blaustein, 2001. Egg-wrapping behaviour protects newt embryos from UV radiation. Animal Behaviour 61: 639–644.
Matsushita, T., Y. Fujita, K. Omori, Y. Huang, Y. Matsui & N. Shirasaki, 2020. Effect of chlorination on anti-acetylcholinesterase activity of organophosphorus insecticide solutions and contributions of the parent insecticides and their oxons to the activity. Chemosphere 261: 127743.
McClelland, S. J., R. J. Bendis, R. A. Relyea & S. K. Woodley, 2018. Insecticide-induced changes in amphibian brains: how sublethal concentrations of chlorpyrifos directly affect neurodevelopment. Environmental Toxicology and Chemistry 37: 2692–2698.
Middleton, E. M., J. R. Herman, E. A. Celarier, J. W. Wilkinson, C. Carey & R. J. Rusin, 2001. Evaluating ultraviolet radiation exposure with satellite data at sites of amphibian declines in Central and South America. Conservation Biology 15: 914–929.
Misra, R. B., R. S. Ray & R. K. Hans, 2005. Effect of UVB radiation on human erythrocytes in vitro. Toxicology in Vitro 19: 433–438.
Moe, S. J., K. De Schamphelaere, W. H. Clements, M. T. Sorensen, P. J. Van den Brink & M. Liess, 2013. Combined and interactive effects of global climate change and toxicants on populations and communities. Environmental Toxicology and Chemistry 32: 49–61.
Newman, M. C. & W. H. Clements, 2007. Ecotoxicology: a comprehensive treatment, CRC Press, New York:
Nobonita, D. & D. Suchismita, 2013. Chlorpyrifos toxicity in fish: a review. Current World Environment 8: 77–84.
Oris, J. T. & J. P. Giesy Jr., 1985. The photoenhanced toxicity of anthracene to juvenile sunfish (Lepomis spp.). Aquatic Toxicology 6: 133–146.
Pahkala, M., A. Laurila & J. Merilä, 2001. Carry–over effects of ultraviolet-B radiation on larval fitness in Rana temporaria. Proceedings of the Royal Society of London. Series b: Biological Sciences 268: 1699–1706.
Palen, W. J., C. E. Williamson, A. A. Clauser & D. E. Schindler, 2005. Impact of UV-B exposure on amphibian embryos: linking species physiology and oviposition behaviour. Proceedings of the Royal Society b: Biological Sciences 272: 1227–1234.
Patrick, M. H. & R. O. Rahn, 1976. Photochemistry of DNA and polynucleotides. Photochemistry and Photobiology of Nucleic Acids 2: 35–91.
Peng, S., H. Liao, T. Zhou & S. Peng, 2016. Effects of UVB radiation on freshwater biota: a meta-analysis. Global Ecology and Biogeography 26: 500–510.
Quaranta, A., V. Bellantuono, G. Cassano & C. Lippe, 2009. Why amphibians are more sensitive than mammals to xenobiotics. PLoS ONE 4: e7699.
Robles-Mendoza, C., S. R. Zúñiga-Lagunes, C. A. P. de León-Hill, J. Hernández-Soto & C. Vanegas-Pérez, 2011. Esterases activity in the axolotl Ambystoma mexicanum exposed to chlorpyrifos and its implication to motor activity. Aquatic Toxicology 105: 728–734.
Rowe, C. L., O. M. Kinney, R. D. Nagle & J. D. Congdon, 1998. Elevated maintenance costs in an anuran (Rana catesbeiana) exposed to a mixture of trace elements during the embryonic and early larval periods. Physiological Zoology 71: 27–35.
Rutkoski, C. F., N. Macagnan, A. Folador, V. J. Skovronski, A. M. de Amaral, J. Leitemperger, M. D. Costa, P. A. Hartmann, C. Müller, L. V. Loro & M. T. Hartmann, 2020. Morphological and biochemical traits and mortality in Physalaemus gracilis (Anura: Leptodactylidae) tadpoles exposed to the insecticide chlorpyrifos. Chemosphere 250: 126162.
Schiesari, L., B. Grillitsch & H. Grillitsch, 2007. Biogeographic biases in research and their consequences for linking amphibian declines to pollution. Conservation Biology 21: 465–471.
Sparks, T. C., A. J. Crossthwaite, R. Nauen, S. Banba, D. Cordova, F. Earley, U. Ebbinghaus-Kintscher, S. Fujioka, A. Hirao, D. Karmon, R. Kennedy, T. Nakao, H. J. R. Popham, V. Salgado, G. B. Watson, B. J. Wedel & F. J. Wessels, 2020. Insecticides, biologics and nematicides: updates to IRAC’s mode of action classification—a tool for resistance management. Pesticide Biochemistry and Physiology 167: 104587.
Sparling, D. W. & G. Fellers, 2007. Comparative toxicity of chlorpyrifos, diazinon, malathion and their oxon derivatives to larval Rana boylii. Environmental Pollution 147: 535–539.
StatSoft. Inc., 2017. STATISTICA (data analysis software system). Version 13.3. www.statsoft.com.
Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. Rodrigues, D. L. Fischman & R. W. Waller, 2008. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.
Sumon, K. A., H. Rashid, E. T. Peeters, R. H. Bosma & P. J. Van den Brink, 2018. Environmental monitoring and risk assessment of organophosphate pesticides in aquatic ecosystems of north-west Bangladesh. Chemosphere 206: 92–100.
Swain, S. K. & M. R. Mahananda, 2014. Effect of monocrotophos, an organophosphorus pesticide on the growth of tadpoles of Limnonectis limnocharis, a rice field frog. Natural Resources and Conservation 2: 1–5.
US Environmental Protection Agency (USEPA), 2014. Draft Guideline for the Testing of Chemicals. The Larval Amphibian Growth and Development Assay (LAGDA).
Van Meter, R. J., D. A. Glinski, T. Hong, M. Cyterski, W. M. Henderson & S. T. Purucker, 2014. Estimating terrestrial amphibian pesticide body burden through dermal exposure. Environmental Pollution 193: 262–268.
Velmurugan, G., D. V. Babu & S. Ramasamy, 2013. Prolonged monocrotophos intake induces cardiac oxidative stress and myocardial damage in rats. Toxicology 307: 103–108.
Wake, D. B. & V. T. Vredenburg, 2008. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences 105: 11466–11473.
Watson, F. L., H. Schmidt, Z. K. Turman, N. Hole, H. Garcia, J. Gregg & E. A. Fradinger, 2014. Organophosphate pesticides induce morphological abnormalities and decrease locomotor activity and heart rate in Danio rerio and Xenopus laevis. Environmental Toxicology and Chemistry 33: 1337–1345.
Widder, P. D. & J. R. Bidwell, 2008. Tadpole size, cholinesterase activity, and swim speed in four frog species after exposure to sub-lethal concentrations of chlorpyrifos. Aquatic Toxicology 88: 9–18.
Wijesinghe, M. R., M. G. D. K. Bandara, W. D. Ratnasooriya & G. P. Lakraj, 2011. Chlorpyrifos-induced toxicity in Duttaphrynus melanostictus (Schneider 1799) larvae. Archives of Environmental Contamination and Toxicology 60: 690–696.
Yang, F. W., Y. X. Li & F. Z. Ren, 2019. Toxicity, residue, degradation and detection methods of the insecticide triazophos. Environmental Chemistry Letters 17: 1769–1785.
Yu, S., M. Wages, M. Willming, G. P. Cobb & J. D. Maul, 2015a. Joint effects of pesticides and ultraviolet-B radiation on amphibian larvae. Environmental Pollution 207: 248–255.
Yu, S., S. Tang, G. D. Mayer, G. P. Cobb & J. D. Maul, 2015b. Interactive effects of ultraviolet-B radiation and pesticide exposure on DNA photo-adduct accumulation and expression of DNA damage and repair genes in Xenopus laevis embryos. Aquatic Toxicology 159: 256–266.
Zaga, A., E. E. Little, C. F. Rabeni & M. R. Ellersieck, 1998. Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environmental Toxicology and Chemistry: an International Journal 17: 2543–2553.
Zahran, E., E. Risha, W. Awadin & D. Palić, 2018. Acute exposure to chlorpyrifos induces reversible changes in health parameters of Nile tilapia (Oreochromis niloticus). Aquatic Toxicology 197: 47–59.
Acknowledgements
This research was supported by Ministerio de Ciencia Tecnología e Innovación, Minciencias (Project Number 110574558312) and Oficina de Investigaciones y Desarrollo Científico of the Tolima University (Project Number 40230516). Experiments were authorized by the Bioethics Committee of Tolima University. Collection permit was approved by Corporación Autónoma Regional del Tolima, CORTOLIMA (Resolution Number 3758 from 16 November 2016). We thank the anonymous reviewers for their constructive comments.
Funding
This research was funded by Ministerio de Ciencia Tecnología e Innovación, Minciencias, and Oficina de Investigaciones y Desarrollo Científico of the Tolima University. The institutions not intervened in the design of the study and collection, or analysis, and interpretation of data or in writing the manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by LH, JM and MB. The first draft of the manuscript was written by MB and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts or competing interests.
Ethical approval
Experiments were authorized by the Bioethics Committee of Tolima University.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Handling editor: Lee B. Kats
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Henao, L.M., Mendez, J.J. & Bernal, M.H. UVB radiation enhances the toxic effects of three organophosphorus insecticides on tadpoles from tropical anurans. Hydrobiologia 849, 141–153 (2022). https://doi.org/10.1007/s10750-021-04717-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-021-04717-4