Utilization of Fermented Pistia Leaves in the Diet of Rohu, Labeo rohita (Hamilton): Effects on Growth, Digestibility and Whole Body Composition

Original Paper

Abstract

The present study aimed at re-cycling of an aquatic weed (water lettuce, Pistia sp.) as a component in formulation of low cost non-conventional carp diet. Dried Pistia leaves (PL) was bio-processed through solid state fermentation (SSF) for 15 days at  32 ± 1 °C by a tannase producing yeast, Pichia kudriavzevii (GU939629) isolated from the gut of a freshwater carp, Cirrhinus cirrhosus. SSF of PL was effective in reducing the contents of crude fibre and antinutritional factors (e.g., tannin, phytic acid and trypsin inhibitor) significantly (P < 0.05), whereas enhancing crude protein, lipid, ash, total free amino acids and fatty acids. Six isonitrogenous (35%) and isocaloric (17 kJ g−1) experimental diets were prepared incorporating raw (R1–R3) and fermented (F1–F3) PL at 10, 20 and 30% levels by weight replacing fishmeal (FM) and other feed ingredients into a FM-based reference diet and fed to rohu, Labeo rohita fingerlings (initial weight 3.39 ± 0.06 g) for 80 days. In general, fish fed diets with SSF-processed PL resulted in significantly better growth, nutrient digestibility, carcass composition and digestive enzyme activity compared to the diets with raw PL. Fish fed the diet F2 containing 20% fermented PL had the highest live weight gain (106.3%), specific growth rate (SGR, % day−1), protein efficiency ratio and apparent net protein utilization. The highest protein gain (40.84%) and lipid accumulation in the carcass were also recorded in the fish reared on the diet F2. The present study might suggest incorporation of bio-processed PL up to 20% level (12.5% of FM replacement) without interfering growth, feed utilization efficiency and body composition in L. rohita fingerlings.

Keywords

Pistia leaves Yeast Solid state fermentation Carp feed Growth Labeo rohita 

Notes

Acknowledgements

The authors are grateful to the Head, Department of Zoology (DST-FIST and UGC-SAP-DRS sponsored), The University of Burdwan, West Bengal, India; The Department of Science and Technology (PURSE programme) and Science and Engineering Research Board (SERB Research Project No. SR/FT/LS-193/2009), New Delhi, India for providing research facilities. The first author is grateful to The University of Burdwan for awarding the university fellowship.

References

  1. 1.
    Naylor, R.L., Goldburg, R.J., Primavera, J.H., Kautsky, N., Beveridge, M.C.M., Clay, J., Folke, C., Lubchenco, J., Mooney, H., Troell, M.: Effect of aquaculture on world fish supplies. Nature 405, 1017–1024 (2000)CrossRefGoogle Scholar
  2. 2.
    Ray, A.K., Das, I.: Utilization of diets containing composted aquatic weed (Salvinia cuculata) by the Indian major carp, rohu, (Labeo rohita Ham.) fingerlings. Bioresour. Technol. 40, 67–72 (1992)CrossRefGoogle Scholar
  3. 3.
    Ray, A.K., Das, I.: Apparent digestibility of some aquatic macrophytes in rohu, Labeo rohita (Ham.) fingerlings. J. Aquac. Trop. 9, 335–342 (1994)Google Scholar
  4. 4.
    Ray, A.K., Das, I.: Evaluation of dried aquatic weed, Pistia stratiotes, meal as a feedstuff in pelleted feed for rohu, Labeo rohita, fingerlings. J. Appl. Aquac. 5(4), 35–44 (1996)CrossRefGoogle Scholar
  5. 5.
    Bairagi, A., Ghosh, K.S., Sen, S.K., Ray, A.K.: Duckweed (Lemna polyrhiza) leaf meal as a source of feedstuff in formulated diets for rohu, Labeo rohita (Ham.) fingerlings after fermentation with a fish intestinal bacterium. Bioresour. Technol. 85, 17–24 (2002)CrossRefGoogle Scholar
  6. 6.
    Bairagi, A., Ghosh, K.S., Sen, S.K., Ray, A.K.: Evaluation of nutritive value of Leucaena leucocephala leaf meal inoculated with fish intestinal bacteria Bacillus subtilis and Bacillus circulans in formulated diets for rohu, Labeo rohita (Ham.) fingerlings. Aquac. Res. 35, 436–446 (2004)CrossRefGoogle Scholar
  7. 7.
    Gomes, E.F., Rema, P., Kaushik, S.J.: Replacement of fish meal by plant proteins in the diets of rainbow trout (Oncorhynchus mykiss). Aquaculture 130, 177–186 (1995)CrossRefGoogle Scholar
  8. 8.
    Kalita, P., Mukhopadhyay, P.K., Mukherjee, A.K.: Evaluation of the nutritional quality of four unexplored aquatic weeds from northeast India for the formulation of cost-effective fish feeds. Food Chem. 103, 204–209 (2007)CrossRefGoogle Scholar
  9. 9.
    Khan, A., Ghosh, K.: Evaluation of phytase production by fish gut bacterium, Bacillus subtilis for processing of ipomea aquatica leaves as probable aquafeed ingredient. J. Aquat. Food Prod. Technol. 22(5), 508–519 (2013)CrossRefGoogle Scholar
  10. 10.
    Mandal, S., Ghosh, K.: Optimization of tannase production and improvement of nutritional quality of two potential low-priced plant feedstuffs under solid state fermentation by Pichia kudriavzevii isolated from fish gut. Food Biotechnol. 27, 86–103 (2013)CrossRefGoogle Scholar
  11. 11.
    Saha, S., Ray, A.K.: Evaluation of nutritive value of water hyacinth (Eichhornia crassipes) leaf meal in compound diets for rohu, Labeo rohita (Hamilton, 1822) fingerlings after fermentation with two bacterial strains isolated from fish gut. Turk J. Fish. Aquat. Sci. 11, 199–207 (2011)CrossRefGoogle Scholar
  12. 12.
    Lech, G.P., Reigh, R.C.: Plant products affect growth and digestive efficiency of cultured Florida pompano (Trachinotus carolinus) fed compounded diets. PLoS ONE 7(4), e34981 (2012)CrossRefGoogle Scholar
  13. 13.
    Chowdhary, S., Srivastava, P.P., Jena, J.K., Raizada, S., Yadav, J.K., Dayal, R., Mishra, S.: Growth responses on major replacement of animal protein with plant protein and graded levels of dietary supplement amino sugar, glucosamine in threatened Magur (Clarias batrachus, Linnaeus, 1758) fry. J. Appl. Biol. Biotechnol. 4(4), 42–50 (2016)Google Scholar
  14. 14.
    So, O., Si, O.: The effect of replacing Fish meal with 10% of groundnut cake in the diets of H. longifilis on its growth, food conversion and survival. J. Appl. Sci. Environ. Manag. 11(3), 87–90 (2007)Google Scholar
  15. 15.
    Francis, G., Makkar, H.P.S., Becker, K.: Anti-nutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197–227 (2001)CrossRefGoogle Scholar
  16. 16.
    Khan, I.A., Maqbool, A.: Effects of dietary protein levels on the growth, feed utilization and haemato-biochemical parameters of freshwater fish, Cyprinus carpio Var. specularis. Fish Aquac J. 8(1), 187 (2017).  https://doi.org/10.4172/2150-3508.10001 Google Scholar
  17. 17.
    Mandal, S., Ghosh, K.: Development of plant derived low-cost fish feed through overcoming adverse effects of plant anti-nutrients. Fish. Chim. 29(1), 156–161 (2009)Google Scholar
  18. 18.
    Mandal, S., Ghosh, K.: Accumulation of tannin in different tissues of Indian major carps & exotic carps. Aquac. Res. 41, 945–948 (2010)CrossRefGoogle Scholar
  19. 19.
    Hernes, P.J., Hedges, J.I.: Determination of condensed tannin monomers in plant tissues, soils, and sediments by capillary gas chromatography of acid hydrolysis extracts. Anal. Chem. 72, 5115–5124 (2000)CrossRefGoogle Scholar
  20. 20.
    Olvera, N.M.A., Martinez, P., Galvan, C.R., Chavez, S.C.: The use of seed of the leguminous plant Sesbania grandijlora as a partial replacement for fish meal in the diets for tilapia (Oreochromis mossambicus). Aquaculture 71, 51–60 (1988)CrossRefGoogle Scholar
  21. 21.
    Al-Owafeir, M.: The effects of dietary saponin and tannin on growth performance and digestion in Oreochromis niloticus and Clarias gariepinus. In: Ph. D. Thesis, pp. 220. Institute of Aquaculture, University of Stirling (1999)Google Scholar
  22. 22.
    Becker, K., Makkar, H.P.S.: Effects of dietary tannic acid and quebracho tannin on growth performance and metabolic rates of common carp (Cyprinus carpio L.). Aquaculture 175, 327–335 (1999)CrossRefGoogle Scholar
  23. 23.
    Hossain, M.A., Jauncey, K.: Nutritional evaluation of some Bangladeshi oilseed meals as partial substitutes for fish meal in the diet of common carp, Cyprinus carpio L.. Aquac. Fish. Manag. 20, 255–268 (1989)Google Scholar
  24. 24.
    Krogdahl, A.: Alternative protein sources from plants contain anti-nutrients affecting digestion in salmonids. In: Takeda, M., Watanabe, T. (eds.) The Current Status of Fish Nutrition in Aqua-culture. Proceedings of the Third International Symposium on Feeding and Nutrition in Fish, pp. 253–261. Tokyo University of Fisheries, Tokyo (1989)Google Scholar
  25. 25.
    Maitra, S., Ray, A.K.: Inhibition of digestive enzymes in rohu, Labeo rohita (Hamilton) fingerlings by tannin, an in vitro study. Aquac. Res. 34, 93–95 (2003)CrossRefGoogle Scholar
  26. 26.
    Mandal, S., Ghosh, K.: Inhibitory effect of Pistia tannin on digestive enzymes of Indian major carps, an in vitro study. Fish Physiol. Biochem. 36, 1171–1180 (2010)CrossRefGoogle Scholar
  27. 27.
    Goel, G., Puniya, A.K., Aguilar, C.N., Sing, K.: Interaction of gut microflora with tannins in feeds. Naturwissenschaften 92, 497–503 (2005)CrossRefGoogle Scholar
  28. 28.
    Soetan, K.O., Oyewole, O.E.: The need for adequate processing to reduce the anti-nutritional factors in plants used as human foods and animal feeds: a review. Afr. J. Food Sci. 3(9), 223–232 (2009)Google Scholar
  29. 29.
    Bhat, T.K., Singh, B., Sharma, O.P.: Microbial degradation of tannins—a current perspective. Biodegradation 9, 343–357 (1998)CrossRefGoogle Scholar
  30. 30.
    Nelson, K.E., Pell, A.N., Schofield, P., Zinder, S.H.: Isolation and characterization of anaerobic ruminal bacterium capable of degrading hydrolyzable tannins. Appl. Environ. Microbiol. 61, 3293–3298 (1995)Google Scholar
  31. 31.
    Mandal, S., Ghosh, K.: Isolation of tannase-producing microbiota from the gastrointestinal tracts of some freshwater fish. J. Appl. Ichthyol. 29, 145–153 (2013).  https://doi.org/10.1111/j.1439-0426.2012.02054.x CrossRefGoogle Scholar
  32. 32.
    Talukdar, S., Ringo, E., Ghosh, K.: Extracellular tannase-producing bacteria detected in the digestive tracts of freshwater fishes (Actinopterygii: Cyprinidae and Cichlidae). Acta Ichtyol. Pisc. 46(3), 201–210 (2016)CrossRefGoogle Scholar
  33. 33.
    Ghosh, K., Ray, A.K.: Tannins in plant feed ingredients: facts and probable consequences in fish nutrition. In: Petridis, G.K. (ed.) Tannins: Types, Foods Containing, and Nutrition, pp. 265–280. Nova Publishers, Hauppauge (2011)Google Scholar
  34. 34.
    Ghosh, K., Mandal, S.: Nutritional evaluation of groundnut oil cake in formulated diets for rohu, Labeo rohita (Hamilton) fingerlings after solid state fermentation with a tannase producing yeast, Pichia kudriavzevii (GU939629) isolated from fish gut. Aquac. Rep. 2, 82–90 (2015).  https://doi.org/10.1016/j.aqrep.2015.08.006 CrossRefGoogle Scholar
  35. 35.
    Wee, K.L.: Use of non-conventional feedstuff of plant origin as fish feeds—is it practical and economically feasible? In: De Silva, S.S. (ed.) Fish Nutrition Research in Asia. Proceedings of the Fourth Asian Fish Nutrition Workshop. Asian Fisheries Society Special Publication 5, Asian Fisheries Society, Manila (1991)Google Scholar
  36. 36.
    Mondal, S., Roy, T., Ray, A.K.: Characterization and identification of enzyme producing bacteria isolated from the digestive tract of bata, Labeo bata. J. World Aquac. Soc. 41, 369–376 (2010)CrossRefGoogle Scholar
  37. 37.
    Jhingran, V.G.: Fish and Fisheries of India, 3rd edn., pp. 335–337. Hindustan Publishing Corporation, Delhi (1997)Google Scholar
  38. 38.
    Mondal, K., Banerjee, D., Banerjee, R., Pati, B.: Production and characterization of tannase from Bacillus cereus KBR9. J. Gen. Appl. Microbiol. 47, 263–267 (2001)CrossRefGoogle Scholar
  39. 39.
    Saha, S., Ghosh, K.: Evaluation of nutritive value of raw and fermented de-oiled physic nut, Jatropha curcas seed meal in the formulated diets for rohu, Labeo rohita (Hamilton) fingerlings. Proc. Zool. Soc. 66(1), 41–50 (2013)CrossRefGoogle Scholar
  40. 40.
    Roy, T., Banerjee, G., Dan, S.K., Ghosh, P., Ray, A.K.: Improvement of nutritive value of sesame oilseed meal in formulated diets for rohu, Labeo rohita (Hamilton), fingerlings after fermentation with two phytase-producing bacterial strains isolated from fish gut. Aquac. Int. 22, 633–652 (2014)CrossRefGoogle Scholar
  41. 41.
    Spyridakis, P., Metailler, R., Gabaudan, J., Riaza, A.: Studies on nutrient digestibility in European sea bass (Dicentrarchus labrax) 1. Methodological aspects concerning faeces collection. Aquaculture 77, 61–70 (1989)CrossRefGoogle Scholar
  42. 42.
    AOAC (Association of Official Analytical Chemists): Official Methods of Analysis of the Official Association of Analytical Chemists, 18th edn. Association of the Official Analytical Chemists, Arlington (2005)Google Scholar
  43. 43.
    Maynard, L., Loosil, J., Hintz, H., Warner, R.: Animal Nutrition, 7th edn., pp. 13–14. McGraw-Hill, New York (1979)Google Scholar
  44. 44.
    Moore, S., Stein, W.W.: Photometric ninhydrin method for use in the chromatography of amino acids. J. Biol. Chem. 176, 367–388 (1948)Google Scholar
  45. 45.
    Cox, H.E., Pearson, D.: The Chemical Analysis of Foods. Chemical Publishing Co. Inc, New York (1962)Google Scholar
  46. 46.
    Schanderi, S.H.: Methods in Food Analysis, p. 709. Academic Press, New York (1970)Google Scholar
  47. 47.
    Vaintraub, I.A., Lapteva, N.A.: Colorimetric determination of phytate in unpurified extracts of seeds and the products of their processing. Anal. Biochem. 175, 227–230 (1988)CrossRefGoogle Scholar
  48. 48.
    Smith, C., Van Megen, W., Twaalhoven, L., Hitchcock, C.: The determination of trypsin inhibitor levels in foodstuffs. J. Sci. Food. Agric. 3, 341–350 (1980)CrossRefGoogle Scholar
  49. 49.
    Bolin, D.W., King, R.P., Klosterman, E.W.: A simplified method for the determination of chromic oxide (Cr2O3) when used as a index substance. Science 116, 634–635 (1952)CrossRefGoogle Scholar
  50. 50.
    Steffens, W.: Principles of Fish Nutrition. pp.384. Ellis Horwood Ltd., Chichester (1989)Google Scholar
  51. 51.
    Cho, C.Y., Slinger, S.J., Bayley, H.S.: Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp. Biochem. Physiol. 73, 25–41 (1982)CrossRefGoogle Scholar
  52. 52.
    APHA (American Public Health Association, American Water Works Association, Water Environment Federation): Standard Methods for the Examination of Water and Wastewater, 19th edn. American Public Health Association, New York (1995)Google Scholar
  53. 53.
    Lowry, O.H., Ronebrough, N.J., Farr, A.L., Randell, R.J.: Protein measurement with Folin phenol reagent. J. Biol. Chem. 193, 265–276 (1951)Google Scholar
  54. 54.
    Bernfeld, P.: Amylase (alpha) and (beta). In: Colowick, S.P., Kaplan, N.O. (eds.) Methods in Enzymology, vol. 1, pp. 149–150. Academic Press, New York (1955)Google Scholar
  55. 55.
    Bier, M.: Lipases. In: Colowick, S.P., Kaplan, N.O. (eds.) Methods in Enzymology, vol. 1. Academic Press, New York (1955)Google Scholar
  56. 56.
    Beveridge, M.C.M., Sikdar, P.K., Frerichs, G.N., Millar, S.: The ingestion of bacteria in suspension by the common carp Cyprinus carpio L. J. Fish Biol. 39, 825–831 (1991)CrossRefGoogle Scholar
  57. 57.
    Rahmatullah, S.M., Beveridge, M.C.M.: Ingestion of bacteria in suspension Indian major carps (Catla catla, Labeo rohita) and Chinese carps (Hypophthalmichthys molitrix, Aristichthys nobilis). Hydrobiologica. 264, 79–84 (1993)CrossRefGoogle Scholar
  58. 58.
    Zar, J.H.: Biostatistical Analysis, 4th edn. Pearson Education Singapore Pte. Ltd (Indian Branch), New Delhi (1999)Google Scholar
  59. 59.
    Kinnear, P.R., Gray, C.D.: In: SPSS for Windows Made Simple. Release 10. Psychology Press, Sussex (2000)Google Scholar
  60. 60.
    Ayoade, G.O., Sharma, B.M., Spridhar, M.K.C.: Trials of Pistia stratiotes L. as animal feed. J. Aquat. Plant. Manag. 20, 56–57 (1982)Google Scholar
  61. 61.
    Makkar, H.P.S., Becker, K.: Isolation of tannins from leaves of some trees and shrubs and their properties. J. Agric. Food Chem. 42, 73–734 (1994)CrossRefGoogle Scholar
  62. 62.
    Mukhopadhyay, N., Ray, A.K.: Improvement of quality of sesame Sesamum indicum seed meal protein with supplemental amino acids in feeds for rohu Labeo rohita (Hamilton) fingerlings. Aquac. Res. 30, 549–557 (1999)CrossRefGoogle Scholar
  63. 63.
    Mukhopadhyay, N., Ray, A.K.: Utilization of copra meal in the formulation of compound diets for rohu, Labeo rohita fingerlings. J. Appl. Ichthyol. 15, 127–131 (1999)CrossRefGoogle Scholar
  64. 64.
    Pandey, A., Soccol, C.R., Rodriguez-Leon, J.A., Nigam, P.: History and Development of Solid State Fermentation. In: Pandey, A. (ed.) Biotechnology: Fundamentals and Applications, Asiatech Publishers, New Delhi (2001)Google Scholar
  65. 65.
    Tengerdy, R.P.: Solid substrate fermentation for enzyme production. In: Pandey, A. (ed.) Advances in Biotechnology, pp. 13–16. Educational Publishers and Distributors, New Delhi (1998)Google Scholar
  66. 66.
    El-Sayed, A.F.M., Mansour, C.R., Ezzat, A.A.: Effects of dietary protein levels on spawning performance of Nile tilapia (Oreochromis niloticus) brood stock reared at different water salinities. Aquaculture 220, 619–632 (2003)CrossRefGoogle Scholar
  67. 67.
    Allan, G.L., Parkinson, S., Booth, M.A., Stone, D.A.J., Rowland, S.J., Frances, J., Warner-Smith, R.: Replacement of fishmeal in diets for Australian silver perch, Bidyanus bidyanus: digestibility of alternative ingredients. Aquaculture 186, 293–310 (2000)CrossRefGoogle Scholar
  68. 68.
    Lee, S.M.: Apparent digestibility coefficients of various feed ingredients for juvenile and grower rockfish (Sebastes schlegeli). Aquaculture 207, 79–95 (2002)CrossRefGoogle Scholar
  69. 69.
    Mukhopadhyay, N., Ray, A.K.: Effect of fermentation on the nutritive value of sesame seed meal in the diets for rohu, Labeo rohita (Hamilton), fingerlings. Aquac. Nutr. 5, 229–236 (1999)CrossRefGoogle Scholar
  70. 70.
    Ramachandran, S., Bairagi, A., Ray, A.K.: Improvement of nutritive value of grass pea (Lathyrus sativus) seed meal in the formulated diets for rohu, Labeo rohita (Ham.) fingerlings after fermentation with a fish gut bacterium. Bioresour. Technol. 96, 1465–1472 (2005)CrossRefGoogle Scholar
  71. 71.
    Krogdahl, A., Lea, T.B., Olli, J.L.: Soybean proteinase inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 107, 215–219 (1994)CrossRefGoogle Scholar
  72. 72.
    Santigosa, E., Sa´nchez, J., Me´dale, F., Kaushik, S., Pe´rez-Sa´nchez, J., Gallardo, M.A.: Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282, 68–74 (2008)CrossRefGoogle Scholar
  73. 73.
    Kumar, V., Makkar, H.P.S., Becker, K.: Detoxified Jatropha curcas kernel meal as a dietary protein source: growth performance, nutrient utilization and digestive enzymes in common carp (Cyprinus carpio L.) fingerlings. Aquac. Nutr. 17(3), 313–326 (2011)CrossRefGoogle Scholar
  74. 74.
    Scalbert, A.: Antimicrobial properties of tannins. Phytochemistry. 30, 3875–3883 (1991)CrossRefGoogle Scholar
  75. 75.
    McSweeney, C.S., Palmer, B., Bunch, R., Krause, D.O.: Microbial interactions with tannins: nutritional consequences for ruminants. Anim. Feed Sci. Technol. 91, 83–93 (2001)CrossRefGoogle Scholar
  76. 76.
    Smith, A.H., Zoetendal, E., Mackie, R.I.: Bacterial mechanism to overcome inhibitory effects of dietary tannins. Microb. Ecol. 50, 197–205 (2005)CrossRefGoogle Scholar
  77. 77.
    Phuong, N.T., Thanonkeo, P., Phong, H.X.: Screening useful isolated yeasts for ethanol fermentation at high temperature. Int. J. Appl. Sci. Technol. 2(4), 65–71 (2012)Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Aquaculture Laboratory, Department of ZoologyThe University of BurdwanBurdwanIndia
  2. 2.Post Graduate Department of ZoologyBangabasi CollegeKolkataIndia

Personalised recommendations