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

  • Nataraj Makkimane Bhaskar Rao 
  • Krishnamurthy Sannanegunda Venkatarama Bhatta Email author
Original Paper
  • 69 Downloads

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.

Keywords

Malathion Carbaryl Survival Tadpole Pesticide combinations Froglet 

Notes

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.

References

  1. 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.CrossRefGoogle Scholar
  2. 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
  3. 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.CrossRefGoogle Scholar
  4. 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
  5. Boone, M. D. (2008). Examining the single and interactive effects of three insecticides on amphibian metamorphosis. Environmental Toxicology and Chemistry, 27, 1561–1568.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. Boone, M. D., & James, S. M. (2003). Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecological Applications, 13, 829–841.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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
  12. Ecobichon, D. J. (2001). Carbamate insecticides. In R. Krieger (Ed.), Handbook of pesticide toxicology (Vol. 2, pp. 1087–1106). San Diego: Academic Press.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetology, 16, 183–190.Google Scholar
  16. Groner, M. L., & Relyea, R. A. (2011). A tale of two pesticides: how common insecticides affect aquatic communities. Freshwater Biology, 56, 391–404.CrossRefGoogle Scholar
  17. 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
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.Google Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. Relyea, R. A. (2009). A cocktail of contaminants: How pesticide mixtures at low concentrations affect aquatic communities. Oecologia, 159, 363–376.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.Google Scholar
  38. 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
  39. 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
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. Snawder, J. E., & Chambers, J. E. (1993). Osteolathyrogenic effects of malathion in Xenopus embryos. Toxicology and Applied Pharmacology, 121, 210–216.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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
  46. 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
  47. 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.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Environmental ScienceKuvempu UniversityShimogaIndia

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