Dietary microbial levan ameliorates stress and augments immunity in Cyprinus carpio fry (Linnaeus, 1758) exposed to sublethal toxicity of fipronil

Aquaculture Research

Volumn 45, Issue 5, 2014, Pages 893-906

  Gupta, Sanjay Kumar ^a,b   Pal, Asim Kumar ^a   Sahu, Narottam Prasad ^a   Saharan, Neelam ^a   Mandal, Sagar Charan ^a,c   Prakash, Chandra ^a   Akhtar, Mohammed Shahbaz ^a,b   Prusty, Ashisa Kumar ^a,d  

^a CENTRAL INSTITUTE OF FISHERIES EDUCATION   (India)

^b Division of Fish Nutrition Biochemistry and Physiology Central Institute of Fisheries Education ^*  (India)

^c Central Agriculture University   (India)

^d ICAR Indian Institute of Farming Systems Research   (India)

Author keywords

Amelioration; Cyprinus carpio; Fipronil; Levan; Stress; Sublethal

Indexed keywords

CYPRINID; DIETARY SHIFT; DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; IMMUNITY; MICROBIAL ACTIVITY; PESTICIDE; PROTEIN; SERUM; SUBLETHAL EFFECT; TOXICITY;

CYPRINIDAE; CYPRINUS CARPIO; TRIFLUORO;

EID: 84897527256     PISSN: 1355557X     EISSN: 13652109     Source Type: Journal    
DOI: 10.1111/are.12030     Document Type: Article

References (77)

1. Afonso L.O.B., Basu N., Nakano K., Devlin R.H. & Iwama G.K. (2003) Sex related differences in organismal and cellular stress response in juvenile salmon exposed to treated bleached kraft mill effluent. Fish Physiology and Biochemistry 29, 173-179.
2. Akhtar M.S., Pal A.K., Sahu N.P., Ciji A., Gupta S.K., Choudhary A.K., Jha A.K. & Rajan M.G. (2010) Stress mitigating and immuno-modulatory effect of dietary pyridoxine in Labeo rohita (Hamilton) fingerlings. Aquaculture Research 41, 991-1002.
3. APHA-AWWA-WPCF (1975) Bioassay for aquatic organisms. In: Standard Methods for the Estimation of Water and Wastewater, (19th edn) (ed. by F. Arega & J.H.W. Lee ), pp. 800-869. American Public Health Association, Washington DC, USA.
4. Areechon N. & Plump J.A. (1990) Sub lethal effects of malathion on channel cat fish, Ictalaurus punctatus. Bulletin of Environmental Contamination and Toxicology 44, 435-442.
5. Barton B.A. & Schreck C.B. (1987) Influence of acclimation temperature on interrenal and carbohydrate stress responses in juvenile Chinook salmon (Oncorhynchus tshawytscha). Aquaculture 62, 299-310.
6. Baskaran P., Palanichamy S., Visalakshi S. & Balasubramanian M.P. (1989) Effects of mineral fertilizers on survival of the fish Oreochromis mossambicus. Environment and Ecology 7, 463-465.
7. Bello F.D., Walter J., Hertel C. & Hammes W.P. (2001) In vitro study of probiotic properties of levan-type exopolysaccharides from Lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Systematic and Applied Microbiology 24, 232-237.
8. Belo M.A.A., Schalch S.H.C., Moraes F.R., Soares V.E., Otoboni A.M.M.B. & Moraes J.E.R. (2005) Effect of dietary supplementation with Vitamin E and stocking density on macrophage recruitment and giant cell formation in the teleost fish, Piaractus mesopotamicus. Journal of Comparative Pathology 133, 146-154.
9. 4, glucose and liver glycogen in rainbow trout (Onchorynchus mykiss). Aquatic Toxicology 34, 221-235.
10. Brown S.B., Eales J.G., Evans R.E. & Hara T.J. (1984) Interrenal, thryroidal and carbohydrate responses of rainbow trout (Salmo gairdneri) to environmental acidification. Canadian Journal of Fisheries and Aquatic Sciences 41, 36-45.
11. Carey J.B. & Mc Cormick S.D. (1998) Atlantic salmon smolts are more responsive to an acute handling and confinement stress than parr. Aquaculture 168, 237-253.
12. Cary T.L., Chandler G.T., Volz D.C., Walse S.S. & Ferry J.L. (2004) Phenylpyrazole insecticide fipronil induces male infertility in the estuarine meiobenthic crustacean Amphiascus tenuiremis. Environmental Science and Technology 38, 522-528.
13. Chatterjee N., Pal A.K., Das T., Manush S.M., Sarma K., Venkateshwarlu G. & Mukherjee S.C. (2006) Secondary stress response in Indian major carps Labeo rohita (Ham), Catla catla (Ham) and Cirrhinus mrigala (Ham) fry to increasing packing densities. Aquaculture Research 37, 472-476.
14. Choudhury D., Pal A.K., Sahu N.P., Kumar S., Das S.S. & Mukherjee S.C. (2005) Dietary yeast RNA supplementation reduces mortality by Aeromonas hydrophila in rohu (Labeo rohita L.) juveniles. Fish and Shellfish Immunology 19, 281-91.
15. Clarke M.A., Roberts E.J. & Garegg P.J. (1997) New compounds from microbiological product of sucrose. Carbohydrate Polymer 34, 425.
16. Colliot F., Kukorowski K.A., Hawkins D.W. & Roberts D.A. (1992) Fipronil: a new soil and foliar broad spectrum insecticide. Brighton Crop Protection Conference-Pests and Diseases 2/1, 29-34.
17. Das B.K. & Mukherjee S.C. (2003) Toxicity of cypermethrin in Labeo rohita fingerlings: biochemical, enzymatic and haematological consequences. Comparative Biochemistry and Physiology 134, 109-121.
18. Demeal N.A. (1978) Some characteristics of carbohydrate metabolism in fish. Oceanis, DOC. Oceanography 4, 35-365.
19. Doumas B.T., Watson W. & Biggs H.G. (1971) Albumin standards and measurement of serum albumin with bromocresol green. Clinica Chimica Acta 31, 87-96.
20. Fast M.D., Hosoya S., Johnson S.C. & Afonso L.O.B. (2008) Cortisol response and immune related effects of Atlantic salmon (Salmo salar L.) subjected to short and long term stress. Fish and Shellfish Immunology 24, 194-204.
21. Finney D.J. (1971) Probit Analysis, (3rd edn). Cambridge University Press, London.
22. Fiske C.H. & Subbarow Y. (1925) The colorimetric determination of phosphorus. Journal of Biological Chemistry 66, 375-400.
23. Freeland R.A. & Harper A.L. (1959) The study of metabolic pathway by means of adaptation. Journal of Biological Chemistry 234, 1350-1354.
24. Garen A. & Levinthal C.A. (1960) A Fine-structure genetic and chemical study of the enzyme Alkaline phosphatase of E. coli. I. Purification and characterization of Alkaline phosphatase. Biochemica et Biophysica Acta 38, 470-483.
25. Gupta S.K., Pal A.K., Sahu N.P., Dalvi R., Kumar V. & Mukherjee S.C. (2008) Microbial levan in the diet of Labeo rohita juvenile: effect on non-specific immunity and histopathological changes after challenged with Aeromonas hydrophilla. Journal of Fish Diseases 31, 649-57.
26. Gupta S.K., Pal A.K., Sahu N.P., Dalvi R.S., Akhtar M.S., Jha A.K. & Baruah K. (2010) Dietary microbial levan enhances tolerance of Labeo rohita (Hamilton) juveniles to thermal stress. Aquaculture 306, 398-402.
27. Hestrin S. (1949) Modified by Augustinsson (1957) The reaction of acetyl choline esters and other carboxylic acid derivatives with hydroxylamine and its analytical application. Journal of Biological Chemistry 180, 249-261.
28. Jang K.H., Kang S.A., Cho Y.H., Kim Y.Y., Lee Y.J., Hong K.H., Seong K.H., Kim S.H., Kim C.H., Rhee S.K., Ha S.D. & Choue R.W. (2003) Prebiotic properties of levan in rats. Journal of Microbiology and Biotechnology 13, 348-353.
29. Jeney G. & Anderson D.P. (1993a) Glucan injection or bath exposures given alone or in combination with bacterin enhance the non-specific defense mechanisms in rainbow trout (Oncorhynchus mykiss). Aquaculture 116, 315-329.
30. Jeney G. & Anderson D.P. (1993b) Enhanced immune response and protection in rainbow trout to Aeromonas salmonicida bacterin following prior immersion in immunostimulants. Fish and Shellfish Immunology 3, 51-58.
31. Kalavathy K., Sivakumar A.A. & Chandran R. (2001) Toxic effect of the pesticide Dimethoate on the fish Sarotherodon mossambicus. Journal of Ecological Research and Bioconservation 2, 27-32.
32. Karunasagar I., Ali A., Otta S.K. & Karunasagar I. (1997) Immunization with bacterial antigen: infection with motile Aeromonas. In: Fish Vaccinology. Developments in Biological Standardization, Vol.90 (ed. by R. Gudding, A. Lillehaug & J. Midtlyng ), pp. 1-7. Karger, Basel, Switzerland.
33. Khangarot B.S., Ray P.K. & Singh K.P. (1988) Influence of copper treatment on the immune response in an airbreathing teleost Saccobranchus fossilis. Bulletin of Environmental Contamination and Toxicology 41, 222-226.
34. Kilgore W.W. & Mingyuli (1975) Environmental toxicology. In: Insecticide Biochemistry and physiology (ed. by C. F. Wilkinson ), 669pp. Plenum Press, New York, NY, USA.
35. Kumar D. & Dey R.K. (1988) Fish diseases in India. In: Proceedings of the symposium on aquaculture productivity (ed. by V.R. Sinha, & H.C. Shrivastava ), pp 315-343. Hindustan Liver Research Foundation, Calcutta, India.
36. Lionetto M.G., Giordano M.E., Vilella S. & Schettino T. (2000) Inhibition of eel enzymatic activities by cadmium. Aquatic Toxicology 48, 561-71.
37. Lowry O.H., Ronebrough N.J., Farr A.L. & Randall R.J. (1951) Protein measurement with folin phenol reagent. Journal of Biological Chemistry 193, 265-76.
38. Madhuban D. & Anilava K. (2003) Ascorbic acid supplementation of diet for reduction of deltamethrin induced stress in freshwater catfish Clarias gariepinus. Chemosphere 53, 883-888.
39. Manush S.M., Pal A.K., Das T. & Mukherjee S.C. (2005) Dietary high protein and vitamin C mitigate stress due to chelate claw ablation in Macrobrachium rosenbergii males. Comparative Biochemistry and Physiology, Part A 142, 10-18.
40. McKim J.M. (1977) Evaluation of tests with the early life stages of fish for predicting long-term toxicity. Journal of the Fisheries Research Board of Canada 34, 1148-1154.
41. Mishra R. & Shukla S.P. (1997) Impact of endosulfan on lactate dehydrogenase from the freshwater catfish, Clarius batrachus. Pesticide Biochemistry Physiology 57, 220-234.
42. Misra C.K., Das B.K., Mukherje S.C. & Pattnaik P. (2006) Effect of long term administration of dietary β-glucan on immunity, growth and survival of Labeo rohita fingerlings. Aquaculture 255, 82-94.
43. Mulrooney J.E., Wolfenbarger D.A., Howard K.D., Goli D. & Goli D. (1998) Efficacy of ultra low volume and high volume applications of fipronil against the boll weevil. Journal of Cotton Science 2, 110-116.
44. Murthy V.K., Reddy Y.D., Reddy R.M., Bhaskar K.M. & Govindappa S. (1984) Changes in brain acetylenoline esterase activity in behavior of freshwater fish in acid polluted environment. Environment and Ecology 2, 79-82.
45. Nelson N.A. & Somogii M. (1944, 1945) Cited by Oser B.L. (1965). In:Hawk's Physiological Chemistry (14th edn) pp. 113. McGraw Hill Publication, New York, USA.
46. Ochoa S. (1995) Malic dehydrogenase and 'malic' enzyme. In: Methods of enzymology, Vol. I (ed. by S.P. Coloric & N. Kaplan ), pp. 735-745. Academic Press, NewYork, NY, USA.
47. Ortuno J., Esteban M.A. & Meseguer J. (2003) The effect of dietary intake of vitamins C and E on the stress response of gilthead seabream, Sparus aurata. Fish and Shellfish Immunology 14, 145-156.
48. Prusty A.K., Kohli M.P.S., Sahu N.P., Pal A.K., Saharan N., Mohapatra S. & Gupta S.K. (2011) Effect of short term exposure of fenvalerate on biochemical and haematological responses in Labeo rohita (Hamilton) fingerlings. Pesticide Biochemistry and Physiology 100, 124-129.
49. Rairakhwada D., Pal A.K., Bhathena Z.P., Sahu N.P., Jha A.K. & Mukherjee S.C. (2007) Dietary microbial levan enhances cellular non-specific immunity and survival of common carp, Cyprinus carpio juveniles. Fish and Shellfish Immunology 22, 477-86.
50. Rath R.K. (1993) Fresh water Aquaculture. Scientific Publishers, Jodhpur, India.
51. Reinhold J.G. (1953) Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Standard Method of Clinical Chemistry (ed. by M. Reiner ), pp. 88. Academic Press, New York, USA.
52. Sahoo P.K. & Mukherjee S.C. (2001) Effect of dietary β-1-3- glucan on immune responses and disease resistance of healthy and aflatoxinB1 induced immunocompromised rohu (L. rohita). Fish and Shellfish Immunology 11, 683-695.
53. Sakai M., Taniguchi K., Mamoto K., Ogawa H. & Tabata M. (2001) Immunostimulant effect of nucleotide isolated from yeast RNA on carp, Cyprinus carpio L. Journal of Fish Diseases 24, 433-8.
54. Sarma K., Pal A.K., Sahu N.P., Ayyappan S. & Baruah K. (2009) Dietary high protein and vitamin C mitigates endosulfan toxicity in the spotted murrel, Channa punctatus (Bloch, 1793). Science of the Total Environment 407, 3668-73.
55. Secombes C.J. (1990) Isolation of salmonid macrophage and analysis of their killing ability. In: Techniques in Fish Immunology, (ed. by J.S.T. C Stolen, D.P. Fletcher, B.S. Anderson, M. Van & W.B. Winkel ), pp. 137-152. SOS Publications, New Jersey, USA.
56. Secombes C.J. (1996) The non-specific immune system: cellular defenses. In: The fish immune system: organism, pathogens and environment (ed. by G. Iwawa, & T. Nakanishi ), pp 63-103. Academic Press, San Diego, CA, USA.
57. Selvaraj V., Sampath K. & Sekar V. (2005) Administration of yeast glucan enhances survival and some non-specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish and Shellfish Immunology 19, 293-306.
58. Shaffi S.A. (1982) DDT Toxicity: gluconeogenic enzymes and non-specific phosphomono-esterases in three teleosts. Toxicology Letters 13, 11-15.
59. Sharma R.M. (1990) Effect of endosulfan on acid and alkaline phosphatase activity in liver, kidney and muscle of Channa gachua. Bulletin of Environmental Contamination and Toxicology 44, 443-8.
60. Sharp G.J.E. & Secombes C.J. (1993) The role of reactive oxygen species in the killing of the bacterial fish pathogen Aeromonas salmonicida by rainbow trout macrophages. Fish and Shellfish Immunology 3, 19-129.
61. Siwicki A.K., Anderson D.P. & Rumsey G.L. (1994) Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Veterinary Immunology and Immunopathology 4, 125-39.
62. +- ATPase activity in the gills of the flounder (Platichthys flesus) in a relation to mercury contamination in the firth of forth. Marine Environmental Research 33, 255-266.
63. Stark Y. & Leibovici J. (1986) Different effects of the polysaccharide levan on the oncogenicity of cells of two variants of Lewis lung carcinoma. British Journal of Experimental Pathology 67, 141-47.
64. Stasiack A.S. & Bauman C.P. (1996) Neutrophil activity as a potent indicator for concomitant analysis. Fish and Shellfish Immunology 6, 537-539.
65. Stefansson S.O., Nilsen T.O., Ebbesson L.O.E., Wargelius A., Madsen S.S., Bjornsson B.T. & McCormick S.D. (2007) Molecular mechanisms of continuous light inhibition of Atlantic salmon parr smolt transformation. Aquaculture 273, 235-245.
66. Stowe C.M. (1969) Cholinergic (Parasympathomiactic) Drugs: drugs acting on the autonomic nervour system. In: Veterinary Pharmacology and Therapeutics (ed. by M. Jones ), pp 265-350. Oxford and IBH Publishing Company.
67. Tejpal C.S., Pal A.K., Sahu N.P., Jha A.K., Muthappa N.A., Sagar V. & Rajan M.G. (2008) Dietary supplementation of l-tryptophan mitigates crowding stress and augments the growth in Cirrhinus mrigala fingerlings. Aquaculture 293, 272-277.
68. Tripathi G. & Verma P. (2004) Endosulfan mediated biochemical changes in the fresh water fish Clarias batrachus. Biomedical Environmental Sciences 17, 47-56.
69. USEPA (U.S. Environmental protection Agency) (1996) New pesticide fact sheet, EPA 737-F-96-005. Office of Pesticide Programs, Washington, DC.
70. Verma A., Pal A.K., Manush S.M., Das T., Dalvi R.S., Chandrachoodan P.P. & Apte S.K. (2007) Persistent sub-lethal chlorine exposure augments immunosuppression in Cyprinus carpio advanced fingerlings due to increasing acclimation temperatures. Fish and Shellfish Immunology 22, 547-555.
71. Vijayan M.M., Foster G.D. & Moon T.W. (1993) Cortisol implantation alters hepatic metabolism and hormonal responsiveness in the sea raven. Fish Physiology and Biochemistry. 12, 327-335.
72. Vijayaraghavan S. & Rao J.V.R. (1986) Starvational stress effects on tissue lactate and lactate dehydrogenase activity in Anabas scandens (Cuvier). Comparative Physiology and Ecology 4, 233-236.
73. Waring C.P. & Mooreb A. (2004) The effect of atrazine on Atlantic salmon (Salmo salar) smolts in fresh water and after sea water transfer. Aquatic Toxicology 66, 93-104.
74. Wedemeyer G.A. (1972) Some physiological consequences of handling stress in the juvenile coho salmon (O. kisutch) and rainbow trout (S. gairdneri). Journal of Fisheries Research Board of Canada 29, 1780-1783.
75. Wiegertjes G.F., Stet R.J.M., Parmentier H.K. & Muiswinkel W.B. (1996) Immunogenetics of disease resistance in fish; a comparable approach. Developmental and Comparative Immunology 20, 365-381.
76. Wroblewski F. & Ladue J.S. (1955) LDH activity in blood. Proceedings of the Society for Experimental Biology and Medicine 90, 210-213.
77. Xu G., Yajima T., Li W., Saito K., Ohshima Y. & Yoshikai Y. (2006) Levan (β 2-6 fructan), a major fraction of fermented soybean mucilage, displays immunostimulating properties via Toll-like receptor 4 signalling: induction of interleukin-12 production and suppression of T-helper type 2 response and immunoglobulin E production. Clinical and Experimental Allergy 36, 94-101.