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Ecotoxicology

, Volume 22, Issue 9, pp 1395–1402 | Cite as

Toxicity of endosulfan to tadpoles of Fejervarya spp. (Anura: Dicroglossidae): mortality and morphological deformities

  • Ngangom Nganbi Devi
  • Abhik Gupta
Article

Abstract

The acute toxicity of endosulfan to the tadpoles of three coexisting species of the anuran genus Fejervarya revealed 96 h LC50 values of 46.715, 6.596, and 3.015 μg l−1 for Fejervarya sp.1, F. teraiensis and Fejervarya sp.2, respectively. Toxicity of endosulfan was also tested at the sublethal concentrations of 5 and 0.5, and 0.3 and 0.03 μg l−1 (c 10 and 1 % of their respective 96 h LC50 values) in Fejervarya sp.1 and Fejervarya sp.2, and 0.35 and 0.18 μg l−1 (c 5 and 2.5 % of 96 h LC50) in F. teraiensis. Endosulfan was observed to cause mortality at concentrations as low as c 1, 2.5 and 10 % of their respective 96 h LC50 values in Fejervarya sp.2, F. teraiensis, and Fejervarya sp.1. Such vulnerabilities are likely to have implications for the survival of natural populations of these co-existing species as well as other anurans present in the study area where pesticide use is relatively high in the tea plantations. Morphological deformities caused by endosulfan comprised failure to develop one or both forelimb in Fejervarya sp.1 and F. teraiensis, stunted hindlimb growth in Fejervarya sp.1, and axial malformation in Fejervarya sp.1 and Fejervarya sp.2. Fore- and hind-limb deformities were likely to have occurred due to the impairment of thyroid metabolism by endosulfan. These effects illustrate the threat that continued endosulfan use poses to natural populations of anuran amphibians.

Keywords

Anura Endosulfan Mortality Sublethal toxicity Deformity 

Notes

Acknowledgments

The authors are grateful to the University Grants Commission, India, for providing funding assistance for a major research project (Grant Number: F. No. 37-51/2009-SR) during 2010–2013, and to two anonymous reviewers for suggesting revisions that helped to improve the original manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Agostini MG, Natale GS, Ronco AE (2010) Lethal and sublethal effects of cypermethrin to Hypsiboas pulchellus tadpoles. Ecotoxicology 19:1545–1550. doi: 10.1007/s10646-010-0539-3 CrossRefGoogle Scholar
  2. Bernabò I, Brunelli E, Berg C, Bonacci A, Tripepi S (2008) Endosulfan acute toxicity in Bufo bufo gills: ultrastructural changes and nitric oxide synthase localization. Aquat Toxicol 86:447–456CrossRefGoogle Scholar
  3. Bernabò I, Sperone E, Tripepi S, Brunelli E (2011) Toxicity of chlorpyrifos to larval Rana dalmatina: acute and chronic effects on survival, development, growth and gill apparatus. Arch Environ Contam Toxicol 61:704–718. doi: 10.1007/s00244-011-9655-1 CrossRefGoogle Scholar
  4. Berrill M, Coulson D, McGillivray L, Pauli B (1998) Toxicity of endosulfan to aquatic stage of anuran amphibians. Environ Toxicol Chem 9:1738–1744. doi: 10.1002/etc.5620170914 CrossRefGoogle Scholar
  5. Blaustein AR, Romansic JM, Kiesecker JM, Hatch AC (2003) Ultraviolet radiation, toxic chemicals and amphibian population declines. Divers Distrib 9:123–140. doi: 10.1046/j.1472-4642.2003.00015.x CrossRefGoogle Scholar
  6. Borthakur R, Kalita J, Hussain B, Sengupta S (2007) Study on the Fejervarya (Anura: Dicroglossidae) species of Assam. Zoos Print J 22:2639–2643CrossRefGoogle Scholar
  7. Brian JV, Harris CA, Scholze M, Backhaus T, Booy P, Lamoree M, Pojana G, Jonkers N, Runnalls T, Bonfà A, Marcomini A, Sumpter JP (2005) Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals. Environ Health Perspect 113:721–728CrossRefGoogle Scholar
  8. Broomhall S, Shine R (2003) Effects of the insecticide endosulfan and presence of congeneric tadpoles on Australian treefrog (Litoria freycineti) tadpoles. Arch Environ Contam Toxicol 45:221–226. doi: 10.1007/s00244-003-0172-8 CrossRefGoogle Scholar
  9. Brown DD, Cai L (2007) Amphibian metamorphosis. Dev Biol 306:20–33CrossRefGoogle Scholar
  10. Brown DD, Cai L, Das B, Marsh-Armstrong N, Schreiber AM, Juste R (2005) Thyroid hormone controls multiple independent programs required for limb development in Xenopus laevis metamorphosis. Proc Natl Acad Sci 102:12455–12458CrossRefGoogle Scholar
  11. Burggren WW, Just JJ (1992) Developmental changes in physiological systems. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 467–530Google Scholar
  12. Caride A, Lafuente A, Cabaleiro T (2010) Endosulfan effects on pituitary hormone and both nitrosative and oxidative stress in puberty male rats. Toxicol Lett 197:106–112CrossRefGoogle Scholar
  13. Carriger JF, Oang TC, Rand GM (2010) Survival time analysis of least killifish (Heterandria formosa) and mosquitofish (Gambusia affinis) in acute exposures to Endosulfan sulfate. Arch Environ Contam Toxicol 58:1015–1022. doi: 10.1007/s00244-009-9415-7 CrossRefGoogle Scholar
  14. Coimbra AM, Reis-Henriques MA, Darras VM (2005) Circulating thyroid hormone levels and iodothyronine deiodinase activities in Nile tilapia (Oreochromis niloticus) following dietary exposure to endosulfan and aroclor 1254. Comp Biochem Physiol C 141:8–14CrossRefGoogle Scholar
  15. Denoël M, D’Hooghe B, Ficetola GF, 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 21:1240–1250CrossRefGoogle Scholar
  16. Denoël M, Libon S, Kestemont P, Brasseur C, Focant J-F, De Pauw E (2013) Effects of a sublethal pesticide exposure on locomotor behavior: a video-tracking analysis in larval amphibians. Chemosphere 90:945–951CrossRefGoogle Scholar
  17. Dimitrie D (2010) The effects of two insecticides on California anurans (Rana sierrae and Pseudacris sierra) and the implications for declining amphibian populations. Dissertation, Southern Illinois University CarbondaleGoogle Scholar
  18. Dinesh KP, Radhakrishnan C, Gururaja KV, Deuti K, Bhatta G (2012) A checklist of amphibia of India with IUCN Red list status. Updated till April 2013 (Online Version) http://zsi.gov.in/checklist/Amphibia_final.pdf Accessed 19 August 2013
  19. Fellers GM, McConnell LL, Pratt D, Datta S (2004) Pesticides in mountain yellow-legged frogs (Rana muscosa) from the sierra nevada mountains of California, USA. Environ Toxicol Chem 23:2170–2177CrossRefGoogle Scholar
  20. Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge, p 333Google Scholar
  21. Gosner KL (1960) A simplified table for staging anuran embryo and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  22. Gurusubramanian G, Rahman A, Sarmah M, Ray S, Bora S (2008) Pesticide usage pattern in tea ecosystem, their retrospects and alternative measures. J Environ Biol 29:813–826Google Scholar
  23. Harris ML, Chora L, Bishop A, Bogart JP (2000) Species- and age-related differences in susceptibility to pesticide exposure for two amphibians, Rana pipiens and Bufo americanus. Bull Environ Contam Toxicol 64:263–270. doi: 10.1007/s001289910039 CrossRefGoogle Scholar
  24. Hayes T, Haston K, Tsui M, Hoang A, Haefelle C, Vonk A (2003) Atrazine induced hermorphropdism at 01 ppb in American Leopard frogs (Rana pipiens) Laboratory and field evidence. Environ Health Perspect 111:568–575CrossRefGoogle Scholar
  25. Hii YS, Lee MY, Chuah TS (2007) Acute toxicity of organochlorine insecticide endosulfan and its effect on behaviour and some haematological parameters of Asian swamp eel (Monopterus albus, Zuiew). Pesticide Biochem Physiol 89:46–53CrossRefGoogle Scholar
  26. Huang H, Cai L, Remo BF, Brown DD (2001) Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis. Proc Natl Acad Sci 98:7348–7353CrossRefGoogle Scholar
  27. IUCN (2009) India: The state of amphibians in India. http://www.iucn.org/about/union/secretariat/offices/asia/regional_activities/asian_amphibian_crisis/india/ Accessed 19 August 2013
  28. Jones DK, Hammond JI, Relyea RA (2009) Very highly toxic effects of endosulfan across nine species of tadpole: lag effects and family level selectivity. Environ Toxicol Chem 28:1939–1945CrossRefGoogle Scholar
  29. Kang HS, Gye MC, Kim MK (2008) Effects of endosulfan on survival and development of Bombina orientalis (Boulenger) embryos. Bull Environ Contam Toxicol 81:262–265CrossRefGoogle Scholar
  30. Lavorato M, Bernabò I, Crescente A, Denoël M, Tripepi S, Brunelli E (2013) Endosulfan effects on Rana dalmatina tadpoles: quantitative developmental and behavioural analysis. Arch Environ Contam Toxicol 64:253–262CrossRefGoogle Scholar
  31. Leight AK, Van Dolah RF (1999) Acute toxicity of the insecticides endosulfan, chlorpyrifos, and malathion to the epibenthic estuarine amphipod Gammarus palustris (Bousfield). Environ Toxicol Chem 18:958–964Google Scholar
  32. Mahapatra D (2012) Lift endosulfan ban, exhaust stocks: panel. http://articles.timesofindia.indiatimes.com/2012-11-21/india/35256892_1_endosulfan-ban-food-security-exhaust. Accessed 19 August 2013
  33. Mathew M, Andrews MI (2003) Impact of some pesticides on the growth of tadpoles of common Indian toad Bufo melanostictus Schneider. Zoos Print J 18:1007–1010CrossRefGoogle Scholar
  34. OECD (1992) OECD Guideline for testing of chemicals: fish acute toxicity test http://www.oecd.org/chemicalsafety/risk-assessment/1948241.pdf. Accessed 19 August 2013
  35. Rasel MMR, Hannan MA, Howlader MSA (2007) Four new country records of Fejervarya Bolkay, 1915 (Amphibia: Anura: Dicroglossidae) from Bangladesh. Bangladesh Wildl Bull 4:1–2Google Scholar
  36. Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363–376. doi: 10.1007/s00442-008-1213-9 CrossRefGoogle Scholar
  37. Relyea RA, Mills N (2001) Predator-induced stress makes the pesticides Carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci 98:2491–2496CrossRefGoogle Scholar
  38. Rolland RM (2000) A review of chemically-induced alterations in thyroid and vitamine A status from field studies of wildlife and fish. J Wildl Dis 36:615–635Google Scholar
  39. Schreiber AM, Das B, Huang H, Marsh-Armstrong N, Brown DD (2001) Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. Proc Natl Acad Sci 98:10739–10744CrossRefGoogle Scholar
  40. Sparling DW, Fellers GM, McConnell LL (2001) Pesticides and amphibian population declines in California, USA. Environ Toxicol Chem 20:1591–1595CrossRefGoogle Scholar
  41. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786CrossRefGoogle Scholar
  42. USEPA (1996) Ecological effects tests guidelines: OPPTS 850.1075—fish acute toxicity test, freshwater and marine. http://www.epa.gov/ocspp/pubs/frs/publications/OPPTS_Harmonized/850_Ecological_Effects_Test_Guidelines/Drafts/850-1075.pdf. Accessed 19 August 2013
  43. Verreault J, Skarre JU, Jenssen BM, Gabrielsen GW (2004) Effects of organochlorine contaminants on thyroid hormone levels in arctic breeding glaucous gulls, Larus hyperboreus. Environ Health Perspect 112:532–537CrossRefGoogle Scholar
  44. Viju B (2012) Greens hail Supreme Court decision on endosulfan. http://articles.timesofindia.indiatimes.com/2012-09-01/thiruvananthapuram/33534880_1 endosulfan-victims-c-jayakumar-supreme-court. Accessed 19 August 2013
  45. Wan MT, Kuo J, Buday C, Schroeder G, Van Aggelen G, Pasternak J (2005) Toxicity of a-, b-, (a + b)-endosulfan and their formulated and degradation products to Daphnia magna, Hyalella azteca, Oncorhynchus mykiss, Oncorhynchus kisutch, and biological implications in streams. Environ Toxicol Chem 24:1146–1154. doi: 10.1897/04-300R1.1 CrossRefGoogle Scholar
  46. Westman ADJ, Elliott J, Cheng K, Van Aggelen G, Bishop CA (2010) Effects of environmentally relevant concentrations of endosulfan, azinphosmethyl, and diazinon on Great Basin spadefoot (Spea intermontana) and Pacific treefrog (Pseudacris regilla). Environ Toxicol Chem 7:1604–1612CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Ecology and Environmental ScienceAssam UniversitySilcharIndia

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