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Individual and combined effects of organophosphate and carbamate pesticides on the cricket frog Fejervarya limnocharis

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Abstract

Many amphibians use water bodies associated with agro-ecosystem for breeding and thus are exposed to multiple chemicals. Fejervarya limnocharis is a common frog occurring in rice paddy fields. The timings of pesticide application generally coincide with the tenure of the occurrence of tadpoles in shallow waters of paddy fields. Malathion and carbaryl are frequently used in rice paddy fields to control leafhoppers and rice bugs, respectively. Therefore, effects of mixtures of malathion and carbaryl insecticides on the survival of tadpoles and emergence of froglets of Fejervarya limnocharis were studied in the laboratory using combinations of three concentrations of carbaryl (0, 25, 50 µg l−1) with four concentrations of malathion (0, 100, 250, 500 µg l−1). Both malathion and carbaryl were found to be toxic to tadpoles. A reduction in tadpole survival and froglet emergence was recorded with increasing concentrations of carbaryl and malathion. We found significant interaction between carbaryl and malathion on tadpole survival and froglet emergence. Tadpoles exposed to combination of pesticides showed early emergence as froglets compared to control. The extent of toxicity and pesticide interactions are varied when mixed in different concentrations. The reduction in survival, froglet emergence and delay in emergence of metamorphs can occur in rice paddy field as both pesticides are used simultaneously. Therefore, combinations of pesticides may have significant negative effects on the frog population of agro-ecosystems, which requires further confirmation through appropriate field experiments.

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References

  • Abdullah, A. R., Bajet, C. M., Matin, M. A., Nhan, D. D., & Sulaiman, A. H. (1997). Ecotoxicology of pesticides in the tropical paddy field ecosystem. Environmental Toxicology and Chemistry,16, 59–70.

    CAS  Google Scholar 

  • Alford, R. A. (2000). Ecology–Resource use, competition and predation. In R. W. McDiarmid & R. Altig (Eds.), Tadpoles—The biology of anuran larvae (Paper back Ed., pp. 240–278). Chicago: The University of Chicago Press.

    Google Scholar 

  • Bacchetta, R., Mantecca, P., Andrioletti, M., Vismara, C., & Vailati, G. (2008). Axial-skeletal defects caused by carbaryl in Xenopus laevis embryos. Science of the Total Environment,392, 110–118.

    CAS  Google Scholar 

  • Bionda, C. L., Babini, S., Martino, A. L., Salas, N. E., & Lajmanovich, R. C. (2018). Impact assessment of agriculture and livestock over age, longevity and growth of populations of common toad Rhinella arenarum (anura: Bufonidae), central area of Argentina. Global Ecology and Conservation,14, 1–12.

    Google Scholar 

  • Boone, M. D. (2008). Examining the single and interactive effects of three insecticides on amphibian metamorphosis. Environmental Toxicology and Chemistry,27, 1561–1568.

    CAS  Google Scholar 

  • Boone, M. D., & Bridges, C. M. (2003). Effects of carbaryl on green frog (Rana clamitans) tadpoles: Timing of exposure versus multiple exposures. Environmental Toxicology and Chemistry,22, 2695–2702.

    CAS  Google Scholar 

  • Boone, M. D., Bridges, C. M., Fairchild, J. F., & Little, E. E. (2005). Multiple sublethal chemicals negatively affect tadpoles of the green frog, Rana clamitans. Environmental Toxicology and Chemistry,24, 1267–1272.

    CAS  Google Scholar 

  • Boone, M. D., & James, S. M. (2003). Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecological Applications,13, 829–841.

    Google Scholar 

  • Bridges, C. M. (2000). Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Archives of Environmental Contamination and Toxicology,39, 91–96.

    CAS  Google Scholar 

  • Distel, C. A., & Boone, M. D. (2010). Effects of aquatic exposure to the insecticide carbaryl are species-specific across life stages and mediated by hetero-specific competitors in anurans. Functional Ecology,24, 1342–1352.

    Google Scholar 

  • Ecobichon, D. J. (1993). Toxic effects of pesticides. In M. O. Amdur, J. Doull, & C. D. Klaassen (Eds.), Casarett and Doull’s toxicology—The basic science of poisons (4th ed., pp. 565–622). New York: McGraw-Hill Inc.

    Google Scholar 

  • Ecobichon, D. J. (2001). Carbamate insecticides. In R. Krieger (Ed.), Handbook of pesticide toxicology (Vol. 2, pp. 1087–1106). San Diego: Academic Press.

    Google Scholar 

  • Fordham, C. L., Tessari, J. D., Ramsdell, H. S., & Keefe, T. J. (2001). Effects of malathion on survival, growth, development, and equilibrium posture of bullfrog tadpoles (Rana catesbeiana). Environmental Toxicology and Chemistry,20, 179–184.

    CAS  Google Scholar 

  • Gonçalves, M. W., Gambale, P. G., Godoy, F. R., Alves, A. A., Rezende, P. H., Cruz, A. D., et al. (2017). The agricultural impact of pesticides on Physalaemus cuvieri tadpoles (Amphibia: Anura) ascertained by comet assay. Zoologia,34, 1–8.

    Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetology,16, 183–190.

    Google Scholar 

  • Groner, M. L., & Relyea, R. A. (2011). A tale of two pesticides: how common insecticides affect aquatic communities. Freshwater Biology,56, 391–404.

    Google Scholar 

  • Gurushankara, H. P., Krishnamurthy, S. V., & Vasudev, V. (2003). Estimation of acute toxicity of malathion insecticide on tadpoles and adults of Rana (Limnonectus)limnocharis. Indian Journal of Comparative Animal Physiology,21, 48–51.

    Google Scholar 

  • Gurushankara, H. P., Krishnamurthy, S. V., & Vasudev, V. (2007). Effect of malathion on survival, growth and food consumption of Indian cricket frog (Limnonectus limnocharis) tadpoles. Archives of Environmental Contamination and Toxicology,52, 251–256.

    CAS  Google Scholar 

  • Gurushankara, H. P., Krishnamurthy, S. V., & Vasudev, V. (2012). Changes in sialic acid content of jelly coat in pesticide-exposed frog eggs and their influence on fertilization. Advances in Experimental Medicine and Biology,749, 329–336.

    CAS  Google Scholar 

  • Gurushankara, H. P., Krishnamurthy, S. V., & Vasudev, V. (2016). Effect of Methyl Parathion on survival and Development of Tadpoles of Indian Cricket frog Fejervarya limnocharis. Journal of Tropical Life Science,6, 41–46.

    Google Scholar 

  • Hayes, T. B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A. A., et al. (2002). Hermaphroditic, demasculinized frogs following exposure to the herbicide, atrazine, at ecologically relevant doses. Proceedings of the National Academy of Sciences,99, 5476–5480.

    CAS  Google Scholar 

  • Hegde, G. (2014). Use of agrochemicals and their influence on population structure of anuran amphibians in agro-ecosystem of Western Ghats. Ph.D Thesis, Kuvempu University.

  • Hegde, G., & Krishnamurthy, S. V. (2014). Analysis of health status of the frog Fejervarya limnocharis (Anura: Ranidae) living in rice paddy fields of Western Ghats, using body condition factor and AChE content. Ecotoxicology & Environmental Contamination,9, 69–76.

    Google Scholar 

  • Hua, J., Jones, D. K., Mattes, B. M., Cothran, R. D., Relyea, R. A., & Hoverman, J. T. (2015). Evolved pesticide tolerance in amphibians: Predicting mechanisms based on pesticide novelty and mode of action. Environmental Pollution,206, 56–63.

    CAS  Google Scholar 

  • Johansson, M., Piha, H., Kylin, H., & Merila, J. (2006). Toxicity of six pesticides to common frog (Rana temporaria) tadpoles. Environmental Toxicology and Chemistry,25, 3164–3170.

    CAS  Google Scholar 

  • Kanazawa, J. (1981). Measurement of bioconcentration factors of pesticides by freshwater fish and their correlation with physico-chemical properties or acute toxicities. Pest Management Science,12(4), 417–424.

    CAS  Google Scholar 

  • Krishnamurthy, S. V., & Smith, G. R. (2010). Growth, abnormalities, and mortality of free feeding tadpoles of American toad Bufo americanus exposed to combination of malathion and nitrate. Environmental Toxicology and Chemistry,29, 2777–2782.

    CAS  Google Scholar 

  • Krishnamurthy, S. V., & Smith, G. R. (2011). Combined effects of malathion and nitrate on early growth, abnormalities, and mortality of wood frog (Rana sylvatica) tadpoles. Ecotoxicology,20, 1361–1367.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Mann, R. M., Hyne, R. V., Choung, C. B., & Wilson, S. P. (2009). Amphibians and agricultural chemicals: Review of the risks in a complex environment. Environmental Pollution,157, 2903–2927.

    CAS  Google Scholar 

  • Marian, M. P., Arul, V., & Pandian, T. J. (1983). Acute and chronic effects of carbaryl on survival, growth, and metamorphosis in the bullfrog (Rana tigrina). Archives of Environmental Contamination and Toxicology,12, 271–275.

    CAS  Google Scholar 

  • Nataraj, M. B., & Krishnamurthy, S. V. (2012). Effects of combinations of malathion and cypermethrin on survivability and time of metamorphosis of tadpoles of Indian cricket frog (Fejervarya limnocharis). Journal of Environmental Science and Health, Part-B,47, 67–73.

    CAS  Google Scholar 

  • Nataraj, M. B., & Krishnamurthy, S. V. (2014). Exposure of tadpoles of Fejervarya limnocharis (Anura: Ranidae) to combinations of carbaryl and cypermethrin. Toxicological and Environmental Chemistry,95, 1408–1415.

    Google Scholar 

  • Orizaola, G., & Laurila, A. (2009). Intraspecific variation of temperature-induced effects on metamorphosis in the pool frog (Rana lessonae). Canadian Journal of Zoology,87, 581–588.

    Google Scholar 

  • Relyea, R. A. (2009). A cocktail of contaminants: How pesticide mixtures at low concentrations affect aquatic communities. Oecologia,159, 363–376.

    Google Scholar 

  • Rohr, J. R., Raffel, T. R., Halstead, N. T., McMahon, T. A., Johnson, S. A., Boughton, R. K., et al. (2013). Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proceedings of the Royal Society B,280, 20131502.

    Google Scholar 

  • Sánchez-Bayo, F. (2012). Insecticides mode of action in relation to their toxicity to non-target organisms. Journal of Environmental and Analytical Toxicology,S4, 002. https://doi.org/10.4172/2161-0525.S4-002.

    Article  Google Scholar 

  • Sanuy, D., Oromi, N., & Galofré, A. (2008). Effects of temperature on embryonic and larval development and growth in the natterjack toad (Bufo calamita) in a semi arid zone. Animal Diversity and Conservation,31, 41–46.

    Google Scholar 

  • Sayim, F. (2008). Acute toxic effects of malathion on the 21st stage larvae of the marsh frog. Turkish Journal of Zoology,32, 99–106.

    Google Scholar 

  • Shreyas, R., Chethankumar, M. S., Kulkarni, K., Santosh Kumar, H. S., & Krishnamurthy, S. V. (2017). Nuclear abnormalities in erythrocytes of frogs from Wetlands and croplands of Western Ghats indicate environmental contaminations. Journal of Tropical Life Science,7, 208–212.

    Google Scholar 

  • Shuman-Goodier, M. E., & Propper, C. R. (2016). A meta-analysis synthesizing the effects of pesticides on swim speed and activity of aquatic vertebrates. Science of the Total Environment,565, 758–766.

    CAS  Google Scholar 

  • Smith, G. R., Krishnamurthy, S. V., Burger, A. C., & Mills, L. B. (2011). Differential effects of malathion and nitrate exposure on American toad and wood frog tadpoles. Archives of Environmental Contamination and Toxicology,60, 327–335.

    CAS  Google Scholar 

  • Snawder, J. E., & Chambers, J. E. (1993). Osteolathyrogenic effects of malathion in Xenopus embryos. Toxicology and Applied Pharmacology,121, 210–216.

    CAS  Google Scholar 

  • Sparling, D. W., & Fellers, G. M. (2009). Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environmental Toxicology and Chemistry,28, 1696–1703.

    CAS  Google Scholar 

  • Vasudev, V., Krishnamurthy, S. V., & Gurushankara, H. P. (2007). Organophosphate pesticides—A major threat to anuran populations in an agroecosystem of Western Ghats, India. Froglog,83, 8–9.

    Google Scholar 

  • Zhelev, Z., Tsonev, C. V., & Arnaudova, D. N. (2017). Health status of Pelophylax ridibundus (Pallas, 1771) (Amphibia: Ranidae) in a rice paddy ecosystem in southern Bulgaria: Body condition factor and fluctuating asymmetry. Acta Zoologia Bulgaria,69, 169–177.

    Google Scholar 

  • Zhelev, Z., Tsonev, S., Georgieva, K., & Arnaudova, D. (2018). Health status of Pelophylax ridibundus (Amphibia: Ranidae) in a rice paddy ecosystem in Southern Bulgaria and its importance in assessing environmental state: Haematological parameters. Environmental Science and Pollution Research,25, 7884–7895.

    CAS  Google Scholar 

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Acknowledgements

Authors are thankful to UGC for awarding minor research project (F. MRP(s)-523/09-10/KAMA011/UGC-SWRO) and No. F. No. 34-65/2008(SR) and munificent help. MBN is thankful to Kuvempu University for permission to conduct the work (KU/Ph.D./AC 478, dated 09-10-2009). Authors are thankful to Dr. H.P. Gurushankara and Mr. Ganapati Hegde for their help in compiling the data, and Ms. Devi Tungam and Ms. Soumya B, Research Scholars, IIHR, Bangalore who helped in the analyses of pesticide concentrations. The authors are thankful to anonymous reviewers whose comments and suggestions have immensely improved the manuscript.

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Correspondence to Krishnamurthy Sannanegunda Venkatarama Bhatta.

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Nataraj, M.B.R., Krishnamurthy, S.V.B. Individual and combined effects of organophosphate and carbamate pesticides on the cricket frog Fejervarya limnocharis. Environ Geochem Health 42, 1767–1774 (2020). https://doi.org/10.1007/s10653-019-00418-z

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