Hemolymph Biochemical and Immune Indices of Green Tiger Shrimp (Penaeus semisulcatus) in a Biofloc Aquaculture System: Influenced By Different Feeding Levels
Subject Areas : Journal of Animal Biology
1 - Department of Fisheries Sciences and Engineering, Faculty of Natural Resources, University of Jiroft, Jiroft, Kerman, Iran
Keywords: Green tiger shrimp, Biofloc, Immunity, Hemolymph,
Abstract :
The effect of different feeding levels on the biochemical indicators and immunity of green tiger shrimp in a biofloc aquaculture system was investigated. The experiment was conducted for 45 days with shrimps with an average weight of 2.85 g. Rearing tanks was filled with 150 liters of filtered water with a sand filter, and then 53 individual shrimps were stored in each tank. 7 experimental groups were considered for this research, which included three control groups with different feeding levels in terms of body weight, 6% (CW6), 4% (CW4) and 2% of body weight (CW2), and four biofloc treatments of 6% (BFT6), 4% (BFT4), 2% (BFT2) and 0% (BFT0). The results showed that the highest levels of triglyceride (175.0 mg/dl) and cholesterol (142 mg/dl) were observed in the CW2 treatment. The highest amount of glucose (47 mg/dl) was obtained in BFT0 treatment and the lowest amount was 35.66 and 36.35 in BFT6 and BFT4 treatments, which showed a significant difference with other treatments (p < 0.05). The highest value of lysozyme activity was obtained in BFT6 and BFT4 treatments (24.6 and 24.3 u/ml/min), respectively, and the lowest value was obtained in BFT0 treatment (15 u/ml/min), which showed a significant difference with other treatments (p > 0.05). The highest amount of phenol oxidase activity was the highest in BFT6 (0.74 u/ml) and BFT4 (0.75 u/ml) treatments, and the lowest value was obtained in BFT0 treatment (0.37 u/ml). In general, the results showed that different feed levels affect the biochemical activities and immunity of green tiger shrimp hemolymph. Feeding with food levels of 6 and 4% in biofloc system leads to improvement of lysozyme, total immunoglobulin and phenol oxidase activities in green tiger shrimp.
1. Yuan X, Lv Z, Zhang Z, Han Y, Liu Z, Zhang H. A review of antibiotics, antibiotic resistant bacteria, and resistance genes in aquaculture: qccurrence, contamination, and transmission. Toxics. 2023;11(5):420.
2. Lee D, Yu YB, Choi JH, Jo AH, Hong SM, Kang JC, Kim JH. Viral shrimp diseases listed by the OIE: A review. Viruses, 2022;14(3):585.
3. Yu YB, Choi JH, Kang JC, Kim HJ, Kim JH. Shrimp bacterial and parasitic disease listed in the OIE: A review. Microb Pathog. 2022;166:105545.
4. Khanjani MH, Sharifinia M, Emerenciano MGC. A detailed look at the impacts of biofloc on immunological and hematological parameters and improving resistance to diseases. Fish Shellfish Immunol. 2023;137:108796.
5. Khanjani MH, Eslami J, Emerenciano MGC. Wheat flour as carbon source on water quality, growth performance, hemolymph biochemical and immune parameters of Pacific white shrimp (Penaeus vannamei) juveniles in biofloc technology (BFT). Aquac Rep. 2025;40:102623.
6. Kumar S, Anand PS, De D, Deo AD, Ghoshal TK, Sundaray JK, et al. Effects of biofloc under different carbon sources and protein levels on water quality, growth performance and immune responses in black tiger shrimp Penaeus monodon (Fabricius, 1978). Aquac Res. 2017;48:1168-1182.
7. Khanjani MH, Sharifinia M. Biofloc as a food source for Banana shrimp (Fenneropenaeus merguiensis) postlarvae. North Am J Aquac. 2022;45(4):469-479.
8. Kaya D, Genc E, Genc MA, Aktas M, Eroldogan OT, Guroy D. Biofloc technology in recirculating aquaculture system as a culture model for green tiger shrimp, Penaeus semisulcatus: Effects of different feeding rates and stocking densities. Aquaculture. 2020;528:735526.
9. Mohammad Moradi S, Safaei M, Saraji F. Feeding habits of green tiger prawn, Penaeus semisulcatus (De Hann, 1848) in the coastal waters of the Persian Gulf (Hormozgan Province). Iran Fish Sci J. 2023;32(1):73-83. (In Persion)
10. Sarsangi Aliabad H, Naji A, Mortezaei SRS, Sourinejad I, Akbarzadeh A. Effects of restricted feeding levels and stocking densities on water quality, growth performance, body composition and mucosal innate immunity of Nile tilapia (Oreochromis niloticus) fry in a biofloc system. Aquaculture. 2022;546:737320.
11. Ullman C, Rhodes MA, Allen Davis D. Feed management and the use of automatic feeders in the pond production of Pacific white shrimp Litopenaeus vannamei. Aquaculture. 2019;498:44-49.
12. Xu WJ, Pan LQ. Enhancement of immune response and antioxidant status of Litopenaeus vannamei juvenile in biofloc-based culture tanks manipulating high C/N ratio of feed input. Aquaculture. 2013;412:117-124.
13. Liu G, Zhu S, Liu D, Guo X, Ye Z. Effects of stocking density of the white shrimp Litopenaeus vannamei (Boone) on immunities, antioxidant status, and resistance against Vibrio harveyi in a biofloc system. Fish Shellfish Immunol. 2017;67:19-26.
14. Chen J, Ren Y, Wang G, Xia B, Li Y. Dietary supplementation of biofloc influences growth performance, physiological stress, antioxidant status and immune response of juvenile sea cucumber Apostichopus japonicus (Selenka). Fish Shellfish Immunol. 2018;72:143-152.
15. Khanjani MH, Sharifinia M, Emerenciano MGC. Biofloc technology (BFT) in aquaculture: what goes right, what goes wrong? a scientific-based snapshot. Aquac Nutr. 2024; 2024:7496572.
16. Avnimelech Y. Biofloc Technology-A Practical Guide Book, 2nd ed.; The World Aquaculture Society: Baton Rouge, LA, USA, 2015; 268p.
17. Jones CM, Ng WK, King M. Alsever’s solution: a review of its history, chemistry, and production. Transfus Med Rev. 2010;24:259-267.
18. Liu T, Zhang G, Feng Y, Kong C, Ayisi CL, Huang X, Hua X. Dietary soybean antigen impairs growth and health through stress-induced non-specific immune responses in Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol. 2019;84:124-129
19. Xu Z, Guan W, Xie D, Lu W, Ren X, Yuan J, Mao L. Evaluation of immunological response in shrimp Penaeus vannamei submitted to low temperature and air exposure. Dev Comp Immunol. 2019;100:103413.
20. Ellis AE. Lysozyme Assays. In: Stolen, J.S., Fletcher, T.C., Anderson, D.P., Roberson, B.S. and Van Muiswinkel, W.B., Eds., Techniques in Fish Immunology, SOS Publications, Fair Haven, 1990;101-103.
21. Nayak B, Kumar S, Collins PL, Samal SK. Molecular characterization and complete genome sequence of avian paramyxovirus type 4 prototype strain duck/Hong Kong/D3/75. Virol J. 2008;5:24.
22. Söderhäll K, Hall L. Lipopolysaccharide-induced activation of prophenoloxidase activating system in crayfish haemocyte lysate. BBA-Bioenergetics, 1984;797:99-104.
23. Cuesta A, Meseguer J, Esteban MA. Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.), Veterinary Immunol Immunopathol. 2004;101(3-4):203-210.
24. Guemez-Sorhouet E, Villarreal H, Racotta IS, Naranjo J, Mercier L. Zootechnical and physiological responses of whiteleg shrimp (Litopenaeus vannamei) postlarvae reared in bioflocs and subjected to stress conditions during nursery phase. Aquac Res. 2019;50:1198-1211.
25. Mercier L, Palacios E, Campa-Córdova A, Tovar-Ramírez D, Hernández-Herrera R, Racotta I. Metabolic and immune responses in Pacific whiteleg shrimp Litopenaeus vannamei exposed to a repeated handling stress. Aquaculture. 2006;258:633-640.
26. Shan H, Geng Z, Ma S, Wang T. Comparative study of the key enzymes and biochemical substances involved in the energy metabolism of Pacific white shrimp, Litopenaeus vannamei, with different ammonia-N tolerances. Comp Biochem Physiol C. 2019; 221:73-81.
27. Martinez-Porchas M, Ezquerra-Brauer M, Mendoza-Cano F, Higuera JEC, Vargas-Albores F, Martinez-Cordova LR. Effect of supplementing heterotrophic and photoautotrophic biofloc, on the production response, physiological condition and post-harvest quality of the whiteleg shrimp, Litopenaeus vannamei. Aquac Rep. 2020;16:100257.
28. Hussain AS, Mohammad DA, Sallam WS, Shoukry NM, Davis DA. Effects of culturing the Pacific white shrimp Penaeus vannamei in biofloc vs synbiotic systems on the growth and immune system. Aquaculture, 2021;542:736905.
29. Kannenberg EL, Poralla K. Hopanoid biosynthesis and function in bacteria. Naturwissenschaften. 1999;86(4):168-176
30. Annies J, Rosamma P. Acute salinity stress alters the haemolymph metabolic profile of Penaeus monodon and reduces immune competence to white spot syndrome virus infection. Aquaculture. 2007;272: 87-97.
31. Yong ASK, Mok WY, Tamrin MLM, Shapawi R, Kim YS. Effects of dietary nucleotides on growth, survival and metabolic response in whiteleg shrimp, Litopenaeus vannamei against ammonia stress condition. Aquac Res. 2020;51:2252-2260.
32. Xu WJ, Pan LQ. Evaluation of dietary protein level on selected parameters of immune and antioxidant systems, and growth performance of juvenile Litopenaeus vannamei reared in zero-water exchange biofloc-based culture tanks. Aquaculture. 2014;426:181-188.
33. Long L, Liu H, Lu S. Effects of Low Salinity on Growth, Digestive Enzyme Activity, Antioxidant and Immune Status, and the Microbial Community of Litopenaeus vannamei in biofloc technology aquaculture systems. J Mai Sci Eng. 2023;11:2076.
34. Outama P, Xuan CL, Wannavijit S, Lumsangkul C, Linh NV, Montha N, et al. Modulation of growth, immune response, and immune antioxidant related gene expression of Nile tilapia (Oreochromis niloticus) reared under biofloc system using mango peel powder, Fish Shellfish Immunol. 2022;131:1136-1143.
35. Haridas H, Verma AK, Rathore G, Prakash C, Sawant PB, Babitha Rani AM. Enhanced growth and immuno-physiological response of genetically improved farmed tilapia in indoor biofloc units at different stocking densities, Aquac Res. 2017;48:4346-4355,
36. Liu G, Ye Z, Liu D, Zhao J, Sivaramasamy E, Deng Y, Zhu S. Influence of stocking density on growth, digestive enzyme activities, immune responses, antioxidant of Oreochromis niloticus fingerlings in biofloc systems, Fish Shellfish Immunol. 2018;81:416-422.
37. Lee C, Kim S, Lim SJ, Lee KJ. Supplemental effects of biofloc powder on growth performance, innate immunity, and disease resistance of Pacific white shrimp Litopenaeus vannamei. Fish Aquat Sci. 2017;20:15.
38. Ju ZY, Forster IP, Conquest L, Dominy W. Enhanced growth effects on shrimp (Litopenaeus vannamei) from inclusion of whole shrimp floc or floc fractions to a formulated diet. Aquac Nutr. 2008;14:533-43
39. Zhang J, Duan Y, Zhang Z, Dong H, Li Z. Research progress of intestinal microbial flora in shrimp. South China Fish Sci. 2015;11(6):114-119.
40. Kim SK, Pang Z, Seo HC, Cho YR, Samocha T, Jang I.K. Effect of bioflocs on growth and immune activity of Pacific white shrimp, Litopenaeus vannamei postlarvae. Aquac Res. 2014;45(2):362-371.
41. Promthale P, Pongtippatee P, Withyachumnarnkul B, Wongprasert K. Bioflocs substituted fishmeal feed stimulates immune response and protects shrimp from Vibrio parahaemolyticus infection. Fish Shellfish Immunol. 2019;93: 1067–1075.
42. Fan T, Jing Z, Fan X, Yu M, Jiang G. Purification and characterization of phenoloxidase from brine shrimp Artemia sinica. Acta Biochim Biophys Sin. 2011; 43:722-728.
43. Fagutao FF, Koyama T, Kaizu A, Saito-Taki T, Kondo H, Aoki T, Hirono I. Increased bacterial load in shrimp hemolymph in the absence of prophenoloxidase. FEBS J. 2009; 276:5298-5306.
44. Amparyup P, Charoensapsri W, Tassanakajon A. Two prophenol oxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon. Dev Comp Immunol. 2009; 33:247-256.
45. Panigrahi A, Sundaram M, Saranya C., Satish Kumar R, Syama Dayal J, Saraswathy R, et al. Influence of differential protein levels of feed on production performance and immune response of pacific white leg shrimp in a biofloc–based system. Aquaculture. 2019; 503:118-127.
46. Panigrahia A, Sundarama M, Saranya C, Swain S, Dash RR, Syama Dayal J. Carbohydrate sources deferentially influence growth performances, microbial dynamics and immunomodulation in Pacific white shrimp (Litopenaeus vannamei) under biofloc system. Fish Shellfish Immunol. 2019;86:1207-1216.
47. Ekasari J, Azhar MH, Surawidjaja EH, Nuryati S, De Schryver P, Bossier P. Immune response and disease resistance of shrimp fed biofloc grown on different carbon sources, Fish Shellfish Immunol. 2014;41(2):332-339.
48. Rao XJ, Ling E, Yu XQ. The role of lysozyme in the prophenoloxidase activation system of Manduca sexta: an in vitro approach, Dev Comp Immunol. 2010; 34(3):264-271.
49. Amparyup P, Charoensapsri W, Tassanakajon A. Prophenoloxidase system and its role in shrimp immune responses against major pathogens, Fish Shellfish Immunol. 2013;34(4):990-1001.
50. Qiao G, Chen P, Sun Q, Zhang M, Zhang J, Li Z, Li Q. Poly-βhydroxybutyrate (PHB) in bioflocs alters intestinal microbial community structure, immunerelated gene expression and early Cyprinid herpesvirus 2 replication in gibel carp (Carassius auratus gibelio), Fish Shellfish Immunol. 2020; 97:72-82.
51. Crab, R., Chielens, B., Wille, M., Bossier, P., Verstraete, W. The effect of different carbon sources on the nutritional value of bioflocs, a feed for (Macrobrachium rosenbergii) postlarvae. Aquac Res. 2010; 41:559-567.