Haemato-biochemical Responses in Cyprinus carpio (Linnaeus, 1758) Fry Exposed to Sub-lethal Concentration of a Phenylpyrazole Insecticide, Fipronil

Abstract

The present study evaluates the haemato-biochemical responses associated with fipronil exposure [(±)-5-amino-1-(2,6-dichloro-α,α,α-trifluoro-p-tolyl)-4-trifluoromethylsulfinyl-pyrazole-3-carbonitrile] in Cyprinus carpio fry. Fish were exposed to sublethal concentration (1/3rd of LC50) (0.142 mg L−1) for 15 days and corresponding changes in different haemato-biochemical parameters were recorded at the end of experimental period. Significant (P < 0.05) increase in white blood cell counts, blood glucose, serum complement reactive protein and serum cortisol level were noticed, whereas haemoglobin and serum total protein contents were significantly (P < 0.05) decreased. Aspartate amino transferase, catalase and super oxide dismutase activities were significantly (P < 0.05) increased while alkaline phosphatase and malate dehydrogenase activities were significantly (P < 0.05) decreased. Similarly, 47 % inhibition in acetylcholine esterase activity was noticed due to fipronil stress. Results indicated that sublethal exposure of fipronil can induce haemato-biochemical alterations causing stress to C. carpio fry. Thus, haemato-biochemical parameters can be used as biomarkers for the sublethal toxicity of fipronil in the water bodies.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Kilgore WW, Li M (1975) Environmental toxicology. In: Wilkinson CF Insecticide biochemistry and physiology, Olenum Press, New York, p 669

  2. 2.

    Bhatnagar MC, Bana AK, Tyagi M (1992) Respiratory distress to Clarias batarachus (Linn.) exposed to endosulfan: a histological approach. J Environ Biol 13:227–231

    CAS  Google Scholar 

  3. 3.

    Prusty AK, Kohli MPS, Sahu NP, Pal AK, Saharan N, Mohapatra S, Gupta SK (2011) Effect of short term exposure of fenvalerate on biochemical and haematological responses in Labeo rohita (Hamilton) fingerlings. Pest Biochem Physiol 100:124–129

    CAS  Article  Google Scholar 

  4. 4.

    Kumar A, Prasad MR, Srivastava K, Srivastav SK, Suzuki N, Srivastav AK (2013) Cyto-histopathological alterations in the liver of azadirachtin treated catfish heteropneustes fossilis. Proc Nat Acad Sci India Sect B Biol Sci. doi:10.1007/s40011-013-0169-7

    Google Scholar 

  5. 5.

    US Environmental protection Agency (USEPA) (1997) Environmental fate and effects Section 3 registration decision for fipronil: use on rice seed, D235912, Environmental Fate and Effects Division, Office of Pesticide Programs, Washington, DC

  6. 6.

    US Environmental protection Agency (USEPA) (2001) Fipronil environmental fate and ecological effects assessment and characterization for a Section 3 for broadcast treatment with granular product to control turf insects and fire ants (addendum), Environmental Fate and Effects Division, Office of Pesticide Programs, Washington, DC

  7. 7.

    Fenet H, Beltran E, Gadji B, Cooper JF, Coste CM (2001) Fate of phenylpyrazole in vegetation and soil under tropical field conditions. J Agric Food Chem 49(3):1293–1297

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Schlenk D, Huggett DB, Allgood J, Bennett EJ, Rimoldi AB, Beeler D, Block D, Wolder AW, Hovinga R, Bedient P (2001) Toxicity of fipronil and its degradation products to Procambarus sp.: field and laboratory studies. Arch Environ Contam Toxicol 41:325–332

    CAS  PubMed  Article  Google Scholar 

  9. 9.

    Walse SS, Pennington PL, Scott GI, Ferry JL (2004) The fate of fipronil in modular estuarine mesocosms. J Environ Monitor 6:58–64

    CAS  Article  Google Scholar 

  10. 10.

    Gupta SK, Pal AK, Sahu NP, Saharan N, Mandal SC, Chandraprakash, Akhtar MS, Prusty AK (2012) Dietary microbial levan ameliorates stress and augments immunity in Cyprinus carpio fry (Linnaeus, 1758) exposed to sublethal toxicity of fipronil. Aquacult Res. doi:10.1111/are.12030

    Google Scholar 

  11. 11.

    Mulrooney JE, Wolfenbarger DA, Howard KD, Goli D, Goli D (1998) Efficacy of ultra low volume and high volume applications of fipronil against the boll weevil. J Cotton Sci 2:110–116

    CAS  Google Scholar 

  12. 12.

    Colliot F, Kukorowski KA, Hawkins DW, Roberts DA (1992) Fipronil: a new soil and foliar broad spectrum insecticide. Brighton Crop Prot Conf-Pests Dis 2(1):29–34

    Google Scholar 

  13. 13.

    US Environmental protection Agency (USEPA) (1996) New pesticide fact sheet, EPA 737-F-96-005, Office of Pesticide Programs, Washington, DC

  14. 14.

    APHA–AWWA–WPCF (1975) Bioassay for aquatic organisms. Standard methods for the estimation of water and waste water, 19th edn. American Public Health Association, Washington, p 800–869

  15. 15.

    Finney DY (1971) Probit analysis, 3rd edn. Cambridge University Press, London

    Google Scholar 

  16. 16.

    Das BK, Mukherjee SC (2003) Toxicity of cypermethrin in Labeo rohita fingerlings: biochemical, enzymatic and haematological consequences. Comp Biochem Physiol 134(C):109–121

    Google Scholar 

  17. 17.

    Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5(6):771–781

    Article  Google Scholar 

  18. 18.

    Dacie JV, Lewis SM (2001) Practical haematology, 9th edn. Churchill Livingstone, London, p 633

    Google Scholar 

  19. 19.

    Nelson-Somogii (1944, 1945) Cited by Oser BL (1965). In: Hawk’s physiological chemistry, 14th edn. McGraw Hill Publication, New York, pp 113

  20. 20.

    Afonso LOB, Basu N, Nakano K, Devlin RH, Iwama GK (2003) Sex related differences in organismal and cellular stress response in juvenile salmon exposed to treated bleached kraft mill effluent. Fish Physiol Biochem 29(2):173–179

    CAS  Article  Google Scholar 

  21. 21.

    Stefansson SO, Nilsen TO, Ebbesson LOE, Wargelius A, Madsen SS, Bjornsson BT, McCormick SD (2007) Molecular mechanisms of continuous light inhibition of Atlantic salmon parr smolt transformation. Aquaculture 273(2–3):235–245

    CAS  Article  Google Scholar 

  22. 22.

    Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune related effects of Atlantic salmon (Salmo salar L.) subjected to short and long term stress. Fish Shellfish Immunol 24(2):194–204

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Reinhold JG (1953) Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Reiner M (ed) Standard method of clinical chemistry. Academic Press, New York, p 88

    Google Scholar 

  24. 24.

    Doumas BT, Watson WA, Biggs HG (1971) Albumin standards and measurement of serum albumin with bromocresol green. Clinica Chimica Act 31(1):87–96

    CAS  Article  Google Scholar 

  25. 25.

    Wroblewski F, Ladue JS (1955) LDH activity in blood. Proc Soc Exp Biol Med 90:210–213

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Ochoa S (1995) Malic dehydrogenase and ‘malic’ enzyme. In: Coloric Kaplan SP (ed) Methods of enzymology I. Academic Press, New York, pp 735–745

    Google Scholar 

  27. 27.

    Hestrin L (1949) modified by Augustinsson (1957) The reaction of acetyl choline esters and other carboxylic acid derivatives with hydroxylamine and its analytical application. J Biol Chem 180:249–261

    Google Scholar 

  28. 28.

    Garen A, Levinthal CA (1960) A Fine-structure genetic and chemical study of the enzyme alkaline phosphatase of E. coli. I. Purification and characterization of alkaline phosphatase. Biochim Biophys Acta 38:470–483

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400

    CAS  Google Scholar 

  30. 30.

    Wotton IDP (1964) Microanalysis. In: Coloric, Kaplan (eds) Medical biochemistry, vol 4. Churchill J & A, London, pp 101–107

    Google Scholar 

  31. 31.

    Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of method in oxygen radical research. CRC Press, Boca Raton, pp 283–284

    Google Scholar 

  32. 32.

    Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for super oxide dismutase. J Biol Chem 217(10):3170–3175

    Google Scholar 

  33. 33.

    Lowry OH, Ronebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–276

    CAS  PubMed  Google Scholar 

  34. 34.

    Baily NTJ (1959) Statistical methods in biology. The English University press, London

    Google Scholar 

  35. 35.

    Joshi P, Deep H, Smith J (2002) Effect of lindane and malathion exposure to certain blood parameters in a freshwater teleost fish Clarias batarachus. Poll Res 21:55–57

    CAS  Google Scholar 

  36. 36.

    Matkovics B, Witas H, Gabrielak T, Szabo L (1987) Paraquat an agent affecting antioxidant enzymes of common carp erythrocytes. Comp Biochem Physiol Part C 87(1):217–219

    CAS  Article  Google Scholar 

  37. 37.

    Nemcsok J, Boross L (1982) Comparative studies on sensitivity of different fish species to metal pollution. Acta Biol Acad Sci Hung 33(1):23–27

    CAS  PubMed  Google Scholar 

  38. 38.

    van Raaji MT, VandenThillart GE, Hallemeesch M, Balm PH, Steffens AB (1995) Effect of arterially infused catecholamines and insulin on plasma glucose and free acids in carp. Am J Physiol Regul Integr Comp Physiol 268:1163–1170

    Google Scholar 

  39. 39.

    Jenkins F, Smith J, Rajanna B, Shameem U, Umadevi K, Sanhya V, Madhavi R (2003) Effect of sublethal concentration of endosulfan on hematological and serum biochemical parameters in the carp, Cyprinus carpio. Bull Environ Contam Toxicol 70(5):993–997

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Ravinder V, Suryanarayan N, Narayana G (1988) Decis induced biochemical alterations in a fresh water catfish, Clarias batrachus. Ind J Comp Anim Physiol 6:5–12

    CAS  Google Scholar 

  41. 41.

    Neff JM (1985) Use of biochemical measurement to detect pollutant-mediated damage to fish. In: Cardwel RD, Purdy R, Bahner RC (eds) Aquatic toxicology and hazard assessment. American Society for Testing Materials, Philadelphia, pp 155–181

    Google Scholar 

  42. 42.

    Tejpal CS, Pal AK, Sahu NP, Kumar JA, Muthappa NA, Vidya S, Rajan MG (2008) Dietary supplementation of l-tryptophan mitigates crowding stress and augments the growth in Cirrhinus mrigala fingerlings. Aquaculture 293(3–4):272–277

    Google Scholar 

  43. 43.

    Gagnon A, Jumarie C, Hontela A (2006) Effects of Cu on plasma cortisol and cortisol secretion by adrenocortical cells of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 78(1):59–65

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Blahova J, Dobsikova R, Svobodova Z, Kalab P (2007) Simultaneous determination of plasma cortisol by high performance liquid chromatography and radioimmunoassay methods in fish. Acta Vet Brno 76(1):59–64

    CAS  Article  Google Scholar 

  45. 45.

    Grant BF, Mehrle PM (1973) Endrin toxicosis in rainbow trout (Salmon gairdneri). J Fish Res Board Can 30(1):31–40

    CAS  Article  Google Scholar 

  46. 46.

    Brown SB, Eales JG, Evans RE, Hara TJ (1984) Interrenal thryroidal and carbohydrate responses of rainbow trout (Salmo gairdneri) to environmental acidification. Can J Fish Aquat Sci 41(1):36–45

    CAS  Article  Google Scholar 

  47. 47.

    Bleau H, Daniel C, Chevalier G, Van-Rra H, Hontela A (1996) Effect of acute exposure to mercury chloride and methylmercury on plasma cortisol, T3, T4, glucose and liver glycogen in rainbow trout (Onchorynchus mykiss). Aquat Toxicol 34(3):221–235

    CAS  Article  Google Scholar 

  48. 48.

    Dincel AS, Benli ACK, Selvi M, Sarıkaya R, Sahin D, Ozkule IA, Erkoc F (2009) Sublethal cyfluthrin toxicity to carp (Cyprinus carpio L.) fingerlings: biochemical, hematological, histopathological alterations. Ecotoxicol Environ Safe 72(5):1433–1439

    Article  Google Scholar 

  49. 49.

    Sinha S, Mandal C, Allen AK, Mandal C (2001) Acute phase response of C-reactive protein of Labeo rohita to aquatic pollutants is accompanied by the appearance of distinct molecular forms. Arch Biochem Biophys 396:139–150

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Szalai AJ, Bly JE, Clem LW (1994) Changes in serum concentrations of channel catfish (Ictalurus punctatus Rafinesque) phosphorylcholine-reactive protein (PRP) in response to inflammatory agents, low temperature-shock and infection by the fungus Saprolegnia sp. Fish Shellfish Immunol 4(5):323–336

    Article  Google Scholar 

  51. 51.

    Paul I, Mandal C, Mandal C (1998) Effect of environmental pollutants on the C-reactive protein of a freshwater major carp Catla catla. Dev Comp Immunol 22(5–6):519–532

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Sarma K (2003) Biochemical responses of Channa punctatus to endosulfan and its implication in environmental monitoring, PhD Dissertation, Central Institute of Fisheries Education, Mumbai

  53. 53.

    Devraj P, Selvarajan VR, Durairaj S (1991) Relationship between acetyl cholinesterase and monoamine oxidase in brain regions of O. mossambicus exposed to phosalone. Ind J Exp Biol 29:790–792

    Google Scholar 

  54. 54.

    Sarma K, Pal AK, Sahu NP, Ayyappan S, Baruah K (2009) Dietary high protein and vitamin C mitigates endosulfan toxicity in the spotted murrel, Channa punctatus (Bloch, 1793). Sci Total Environ 407(12):3668–3673

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Akhtar MS, Pal AK, Sahu NP, Alexander CJ, Gupta SK, Choudhary AK, Jha AK, Rajan MG (2010) Stress mitigating and immuno-modulatory effect of dietary pyridoxine in Labeo rohita (Hamilton) fingerlings. Aquacult Res 41:991–1002

    CAS  Google Scholar 

  56. 56.

    Awasthi M, Shah P, Dubale MS, Gadhia P (1984) Metabolic changes induced by organophosphates in the piscine organs. Environ Res 35(1):320–325

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Ghosh TK (1989) Influence of cypermethrin on the oxidative metabolism of fish Labeo rohita. Proc Ind Natl Sci Acad B 55:115–120

    CAS  Google Scholar 

  58. 58.

    Belinski E (1974) Biochemical aspects of fish swimming. In: Malins BC, Sargent JR (eds) Biochemical perspectives in marine biology. Academic press, New York, pp 239–288

    Google Scholar 

  59. 59.

    Verma AK, Pal AK, Manush SM, Das T, Dalvi RS, Chandrachoodan PP, Ravi PM, Apte SK (2007) Persistent sub-lethal chlorine exposure elicits the temperature induced stress responses in Cyprinus carpio early fingerlings. Pest Biochem Physiol 87(3):229–237

    CAS  Article  Google Scholar 

  60. 60.

    Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci Total Environ 309(1–3):105–115

    CAS  PubMed  Article  Google Scholar 

  61. 61.

    Farombi EO, Ajimoko YR, Adelowo OA (2008) Effect of butachlor on antioxidant enzyme status and lipid peroxidation in fresh water African catfish, (Clarias gariepinus). Int J Environ Res Public Health 5(5):423–427

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

The financial support and necessary facilities provided by Indian Council of Agricultural Research (ICAR), New Delhi to first author is duly acknowledged. Experimental animals were conducted in accordance with national and institutional guidelines for the protection of animal welfare.

Author information

Affiliations

Authors

Corresponding author

Correspondence to S. K. Gupta.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gupta, S.K., Pal, A.K., Sahu, N.P. et al. Haemato-biochemical Responses in Cyprinus carpio (Linnaeus, 1758) Fry Exposed to Sub-lethal Concentration of a Phenylpyrazole Insecticide, Fipronil. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 84, 113–122 (2014). https://doi.org/10.1007/s40011-013-0201-y

Download citation

Keywords

  • Fipronil
  • Sublethal
  • Biochemical
  • Cortisol
  • CRP
  • Stress