Ercüment GENÇ, Derya GÜROY, Abdolsaleh QARANJİKİ, Faik Sertel SEÇER, Münevver Ayçe GENÇ, Doğukan KAYA

Effect of prebiotics on the growth performance, haematological, biochemical, and histological parameters of African catfish (Clarias gariepinus) in recirculating aquaculture system

In this study, African catfish (Clarias gariepinus) was investigated under controlled conditions in recirculating aquaculture system (RAS). The experiment tested the effects of three different dietary prebiotics (FOS: fructooligosaccharide, GOS: galactooligosaccharide, and MOS: mannanoligosaccharide) in two levels (1 g/kg and 2 g/kg) and a control diet on the growth performance, survival rate, haematological and biochemical parameters, and small intestinal and liver histology of the African catfish. Better growth results were obtained in MOS (2 g/kg) supplementation, and there was a statistical difference (P < 0.05) between the MOS (2 g/kg) and the control group. Haematological parameters (erythrocyte sedimentation rate, red blood cell, white blood cell, lymphocyte, neutrophil, and glucose) were similar among all groups (P > 0.05) while some (alanine aminotransferase, aspartate aminotransferase enzymes, and monocyte) were significantly different (P < 0.05). The MOS (2 g/kg) group had longer villi length values than the control group. There was no difference among the groups in terms of small intestine histomorphology and liver tissues in fish. According to the results of this experiment, it can be said that MOS addition has a positive effect on growth parameters and could improve health conditions in Clarias gariepinus culture.

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1. Béné C, Barange M, Subasinghe R, Pinstrup-Andersen P, Merino G et al. Feeding 9 billion by 2050 – Putting fish back on the menu. Food Security 2015; 7(2): 261-274. doi: 10.1007/ s12571-015-0427-z
2. Mylona K, Maragkoudakis P, Miko L, Bock AK, Wollgast J et al. Future of food safety and nutrition-Seeking win-wins, coping with trade-offs. Food Policy 2018; 74: 143-146. doi: 10.1016/j. foodpol.2017.12.002
3. World Bank. Fish to 2030: Prospects for Fisheries and Aquaculture. Washington, DC: World Bank; 2013.
4. FAO. The State of World Fisheries and Aquaculture 2018‐ Meeting the sustainable development goals. Food and Agriculture Organization of the United Nations, Rome; 2018.
5. Magnadottir B. Immunological control of fish diseases. Marine Biotechnolology 2010; 12(4): 361-379. doi: 10.1007/s10126- 010-9279-x
6. Miranda CD, Godoy FA, Lee MR, Keen PL, Miranda CD. Current status of the use of antibiotics and the antimicrobial resistance in the Chilean Salmon farms. Frontiers in Microbiology 2018; 9: 1-14.
7. Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: A growing problem for human and animal health and for the environment. Environmental Microbiology 2006; 8(7): 1137-1144. doi: 10.1111/j.1462-2920.2006.01054.x
8. Dimitroglou A, Merrifield DL, Spring P, Sweetman J, Moate R et al. Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture 2010; 300(1-4): 182-188. doi: 10.1016/j.aquaculture.2010.01.015
9. Ringø E, Olsen RE, Gifstad T, Dalmo RA, Amlund H et al. Prebiotics in aquaculture: A review. Aquaculture Nutrition 2010; 16(2): 117-136. doi: 10.1111/j.1365-2095.2009.00731.x
10. Guerreiro I, Oliva-Teles A, Enes P. Prebiotics as functional ingredients: focus on Mediterranean fish aquaculture. Reviews in Aquaculture 2018; 10(4): 800-832. doi: 10.1111/raq.12201
11. Pryor GS, Royes JB, Chapman FA, Miles RD. Mannanoligosaccharides in fish nutrition: effects of dietary supplementation on growth and gastrointestinal villi structure in Gulf of Mexico sturgeon. North American Journal of Aquaculture 2003; 65(2): 106-111. doi: 10.1577/1548-8454(2003)65<106:mifneo>2.0.co;2
12. Rodriguez-Estrada U, Satoh S, Haga Y, Fushimi H, Sweetman J. Effects of inactivated Enterococcus faecalis and mannan oligosaccharide and their combination on growth, immunity, and disease protection in rainbow trout. North American Journal of Aquaculture 2013; 75(3): 416-428. doi: 10.1080/15222055.2013.799620
13. Zhang CN, Li XF, Xu WN, Jiang GZ, Lu K et al. Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish Shellfish Immunology 2013; 35(5): 1380-1386. doi: 10.1016/j. fsi.2013.07.047
14. Ye JD, Wang K, Li FD, SunYZ. Single or combined effects of fructo‐and mannan oligosaccharide supplements and Bacillus clausii on the growth, feed utilization, body composition, digestive enzyme activity, innate immune response and lipid metabolism of the Japanese flounder Paralichthys olivaceus. Aquaculture Nutrition2011; 17(4): e902-e911. doi: 10.1111/j.1365- 2095.2011.00863.x
15. Akter MN, Sutriana A, Talpur AD, Hashim R. Dietary supplementation with mannan oligosaccharide influences growth, digestive enzymes, gut morphology, and microbiota in juvenile striped catfish, Pangasianodon hypophthalmus. Aquaculture international 2016; 24(1): 127-144. doi: 10.1007/ s10499-015-9913-8
16. Lu J, Qi C, Limbu SM, Han F, Yang L et al. Dietary mannan oligosaccharide (MOS) improves growth performance, antioxidant capacity, non-specific immunity and intestinal histology of juvenile Chinese mitten crabs (Eriocheir sinensis). Aquaculture 2019; 510: 337-346. doi: 10.1016/j.aquaculture.2019.05.048
17. Razeghi Mansour M, Akrami R, Ghobadi SH, Amani Denji K, Ezatrahimi N et al. Effect of dietary mannan oligosaccharide (MOS) on growth performance, survival, body composition, and some hematological parameters in giant sturgeon juvenile (Huso Linnaeus, 1754). Fish Physiology and Biochemistry 2012; 38(3): 829-835. doi: 10.1007/s10695-011-9570-4
18. Torrecillas S, Montero D, Caballero MJ, Robaina L, Zamorano MJ et al. Effects of dietary concentrated mannan oligosaccharides supplementation on growth, gut mucosal immune system and liver lipid metabolism of European sea bass (Dicentrarchus labrax) juveniles. Fish Shellfish Immunology 2015; 42(2): 508- 516. doi: 10.1016/j.fsi.2014.11.033
19. Chen WW, Romano N, Ebrahimi M, Natrah I. The effects of dietary fructooligosaccharide on growth, intestinal short chain fatty acids level and hepatopancreatic condition of the giant freshwater prawn (Macrobrachium rosenbergii) post-larvae. Aquaculture 2017; 469: 95-101.
20. Lima Paz A, da Silva JM, da Silva KMM, Val AL. Protective effects of the fructooligosaccharide on the growth performance, hematology, immunology indicators and survival of tambaqui (Colossoma macropomum, Characiformes: Serrasalmidae) infected by Aeromonas hydrophila. Aquaculture Reports 2019; 15: 100222. doi: 10.1016/j.aqrep.2019.100222
21. Hoseinifar SH, Soleimani N, Ringø E. Effects of dietary fructooligosaccharide supplementation on the growth performance, haemato-immunological parameters, gut microbiota and stress resistance of common carp (Cyprinus carpio) fry. British Journal of Nutrition 2014;112(8): 1296-1302. doi: 10.1017/ S0007114514002037
22. Nedaei S, Noori A, Valipour A, Khanipour AA, Hoseinifar SH. Effects of dietary galactooligosaccharide enriched commercial prebiotic on growth performance, innate immune response, stress resistance, intestinal microbiota and digestive enzyme activity in Narrow clawed crayfish (Astacus leptodactylus Eschscholtz, 1823). Aquaculture 2019; 499: 80-89.
23. Romano N, Kanmani N, Ebrahimi M, Chong CM, Teh JC et al. Combination of dietary pre-gelatinized starch and isomaltooligosaccharides improved pellet characteristics, subsequent feeding efficiencies and physiological status in African catfish, Clarias gariepinus, juveniles. Aquaculture 2018; 484: 293-302. doi: 10.1016/j.aquaculture.2017.09.022
24. Carbone D, Faggio C. Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunology 2016; 54: 172-178.
25. Jimoh WA, Kamarudin MS, Sulaiman MA, Dauda AB. Assessment of prebiotic potentials in selected leaf meals of high dietary fibre on growth performance, body composition, nutrient utilization and amylase activities of a tropical commercial carp fingerlings. Aquaculture Research 2019; 50(11): 3401-3411. doi: 10.1111/are.14298
26. İkizdoğan AT. (2006). Effects of different dietary supplements on growth performance and hepatopancreas and intestine histology of african catfish (Clarias gariepinus). MSc, Mustafa Kemal University, Hatay, Turkey, 2006.
27. Pouomogne V. Cultured aquatic species information programme. Clarias gariepinus. FAO, Rome; 2010. Accessed 4 May 2020
28. Akinwole AO, Faturoti EO. Biological performance of African Catfish (Clarias gariepinus) cultured in recirculating system in Ibadan. Aquacultural Engineering 2007; 36(1): 18-23. doi: 10.1016/j.aquaeng.2006.05.001
29. Blaxhall PC, Daisley KW. Routine haematological methods for use with fish blood. Journal of Fish Biology 1973; 5(6): 771-781. doi: 10.1111/j.1095-8649.1973.tb04510.x
30. Akinrotimi OA, Agokei EO, Aranyo AA. Changes in blood parameters of Tilapia guineensis exposed to different salinity levels. Journal of Environmental Engineering and Technology2012; 1(2): 4-12.
31. Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. American Journal of Clinical Pathology1957; 28(1): 56-63. doi: 10.1093/ajcp/28.1.56
32. Takashima F, Hibiya T. An Atlas of Fish Histology Normal and Pathological Features. 2nd ed. Kodansha Ltd., Tokyo;1995.
33. AOAC. Official Methods of Analysis of the Association of Official Analytical Chemistry. 16th. Washington, USA: AOAC International; 1995.
34. Bligh EG. Dyer WJ. Canadian Journal of Biochemistry and Physiology. Canadian Journal of Biochemistry and Physiology 1959;37: 912-917.
35. Manning TS. Gibson GR. Prebiotics. Best Practice & Research Clinical Gastroenterology 2004;18: 287-298. doi: 10.1016/j. bpg.2003.10.008
36. Grisdale-Helland B, Helland SJ, Gatlin DM. The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture 2008; 283(1-4): 163-167. doi: 10.1016/j. aquaculture.2008.07.012
37. Zhang CN, Li XF, Jiang GZ, Zhang DD, Tian HY et al. Effects of dietary fructooligosaccharide levels and feeding modes on growth, immune responses, antioxidant capability and disease resistance of blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunology2014; 41(2): 560-569. doi: 10.1016/j. fsi.2014.10.005
38. Abd El-Gawad EA, Abd El-latif AM, Shourbela RM. Enhancement of antioxidant activity, non-specific immunity and growth performance of Nile tilapia, Oreochromis niloticus by dietary fructooligosaccharide. Journal of Aquaculture Research and Development 2016; 7(427): 2. doi: 10.4172/2155- 9546.1000427
39. Hoseinifar SH, Ahmadi A, Raeisi M, Hoseini SM, Khalili M et al. Comparative study on immunomodulatory and growth enhancing effects of three prebiotics (galactooligosaccharide, fructooligosaccharide and inulin) in common carp (Cyprinus carpio). Aquaculture Reearch2017; 48(7): 3298-3307. doi: 10.1111/are.13156
40. Miandare HK, Farvardin S, Shabani A, Hoseinifar SH, Ramezanpour SS. The effects of galactooligosaccharide on systemic and mucosal immune response, growth performance and appetite related gene transcript in goldfish (Carassius auratus gibelio). Fish Shellfish Immunology2016; 55: 479-483. doi: 10.1016/j.fsi.2016.06.020
41. Yousefi S, Hoseinifar SH, Paknejad H, Hajimoradloo A. The effects of dietary supplement of galactooligosaccharide on innate immunity, immune related genes expression and growth performance in zebrafish (Danio rerio). Fish Shellfish Immunology2018; 73: 192-196. doi: 10.1016/j.fsi.2017.12.022
42. Khodadadi M, Abbasi N, Adorian TJ, Farsani HG, Hedayati A et al. Growth performance, survival, body composition, hematological parameters, intestinal histomorphology, and digestive enzymes’ activity in juvenile rainbow trout (Oncorhynchus mykiss) fed dietary Immunogen®. Journal of Applied Aquaculture2018; 30(2): 174-186. doi: 10.1080/10454438.2017.1420515
43. Yarahmadi P, Miandare HK, Hoseinifar SH, Gheysvandi N, Akbarzadeh A. The effects of stocking density on hematoimmunological and serum biochemical parameters of rainbow trout (Oncorhynchus mykiss). Aquaculture international2015; 23(1): 55-63. doi: 10.1007/s10499-014-9797-z
44. Al-Dohail MA, Hashim R, Aliyu-Paiko M. Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquaculture Research 2009; 40(14): 1642- 1652. doi: 10.1111/j.1365-2109.2009.02265.x
45. Denji KA, Mansour MR, Akrami R, Ghobadi S, Jafarpour SA et al. Effect of dietary prebiotic mannan oligosaccharide (mos) on growth performance, intestinal microflora, body composition, haematological and blood serum biochemical parameters of rainbow trout (Oncorhynchus mykiss) juveniles. Journal of Fisheries and Aquatic Science2015; 10(4): 255-265. doi: 10.3923/jfas.2015.255.265
46. Welker TL, Lim C, Yildirim-Aksoy M, Shelby R, Klesius PH. Immune response and resistance to stress and Edwardsiella ictaluri challenge in channel catfish, Ictalurus punctatus, fed diets containing commercial whole-cell yeast or yeast subcomponents. Journal of World Aquaculture Society2007; 38(1): 24-35. doi: 10.1111/j.1749-7345.2006.00070.x
47. Falaye A, Emikpe B, Ogundipe E. Influence of Lactobacillus plantarum supplemented diet on growth response, gut morphometry and microbial profile in gut of Clarias gariepinus fingerlings. Journal of Coastal Life Medicine 2016; 4(8): 597- 602.doi: 10.12980/jclm.4.2016J6-104
48. Abdel-Tawwab M, Adeshina I, Jenyo-Oni A, Ajani EK, Emikpe BO. Growth, physiological, antioxidants, and immune response of African catfish, Clarias gariepinus (B.), to dietary clove basil, Ocimum gratissimum, leaf extract and its susceptibility to Listeria monocytogenes infection. Fish Shellfish Immunology 2018; 78: 346-354. doi: 10.1016/j.fsi.2018.04.057
49. Adel M, Safari R, Yeganeh S, Binaii M, Ghiasi M et al. Effect of dietary GroBiotic®‐A supplementation as a prebiotic on the intestinal microflora, growth performance, haemato‐ serological parameters, survival rate and body composition in juvenile beluga (Huso Linnaeus, 1754). Aquaculture nutrition 2017; 23(3): 492-499. doi: 10.1111/anu.12417
50. Guerreiro I, Oliva-Teles A, Enes P. Improved glucose and lipid metabolism in European sea bass (Dicentrarchus labrax) fed short-chain fructooligosaccharides and xylooligosaccharides. Aquaculture 2015; 441: 57-63. doi: 10.1016/j.aquaculture.2015.02.015
51. Hoseinifar SH, Mirvaghefi A, Merrifield DL, Amiri BM, Yelghi S et al. The study of some haematological and serum biochemical parameters of juvenile beluga (Huso huso) fed oligofructose. Fish Physiology and Biochemistry 2011; 37(1): 91-96. doi: 10.1007/s10695-010-9420-9