Kang-Woong KIM, Sung-Sam KIM, Sanaz KHOSRAVI, Samad RAHIMNEJAD, Kyeong-Jun LEE

Evaluation of sargassum fusiforme and ecklonia cava as dietary additives for olive flounder (paralichthys olivaceus)

A 6 -week feeding trial was conducted to evaluate the efficiency of hijiki (Sargassum fusiforme ) and ecklonia (Ecklonia cava ) as dietary supplements for juvenile olive flounder. Fish growth performance, hematology, innate immunity and disease resistance were examined. A basal experimental diet was used as a control and supplemented with 6% of either S. fusiforme or E. cava and another diet was prepared to contain 0.5% oxytetracycline (designated as Con, Hij-6, Eck-6 and OTC-0.5, respectively). The experiment was conducted in triplicate (25 fish per replicate) and the fish (initial body weight, 18.3±0.04 g) were fed one of the test diets at a rate of 3% body weight twice daily. Significantly higher (P<0.05) antioxidant capacity and polyphenolic compounds concentration were detected in hijiki and ecklonia supplemented diets. At the end of the feeding trial, fish growth performance and feed utilization were not significantly affected by dietary treatments. Significantly high er (P<0.05) hemoglobin level and respiratory burst activity were found in fish fed Hij-6 diet. The fish fed Hij-6 and Eck-6 diets exhibited higher resistance against Edwardsiella tarda challenge compared to those fed Con and OTC-0.5 diets. The findings in this study may show that hijiki and ecklonia can be used as environment friendly substitutes for antibiotics in diets for olive flounder.

PDF

___

Ahn, G., Hwang, I., Park, E., Kim, J., Jeon, Y.J., Lee, J., Park, J.W. and Jee, Y. 2008. Immunomodulatory effects of an enzymatic extract from Ecklonia cava on murine splenocytes . Marine Biotechnology, 10: 278 289. doi: 10.1007/s10126 -007 -9062 -9

Amandi, A., Hiu, S.F., Rohovec, J.S. and Fryer, J.L. 1982. Isolation and characterization of Edwardsiella tarda from fall Chinook salmon (Oncorhynchus tshawytscha ). Applied and Environmental Microbiology, 43: 1380 -1384.

Anderson, D.P. and Siwicki, A.K. 1995. Basic hematology and serology for ﬁsh health programs. In: M. Shariff, J.R. Arthur and R.P. Subasinghe (Eds.), Diseases in Asian Aquaculture II. Philippines ﬁsh Health Section , Asian Fisheries Society, Manila, 185 p p .

AOAC (Association of Ofﬁcial Analytical Chemists), 1995. Ofﬁcial Methods of Analysis of Ofﬁcial Analytical Chemists International 16th ed. Association of Ofﬁcial Analytical Chemists, Arlington, VA, USA.

Aoki, T., Kitao, T. and Fukudome, M. 1989. Chemotherapy against infection with multiple drug resistance strains of Edwardsie lla tarda in cultured eels. Fish Pathology, 24: 161 168.

Aquilano, K., Baldelli, S., Rotilio, G. and Ciriolo, M.R. 2008. Role of nitric oxide syntheses in Parkinsons disease: A review on the antioxidant and antiinflammatory activity of polyphenols. Neuroc hemical Research, 33: 2416 2426. doi: 10.1007/s11064 -008 -9697 -6

Austin, B. and Austin, D.A. 2007. Control. In Bacterial Fish Pathogens, Springer Netherlands: 337 -404.

Brand Williams, W. 1995. Use of a free radical method to evaluate antioxidant activity. Food Science and Technology International, 28: 25 -30.

Bravo, L. 1998. Polyphenols: Chemistry, Dietary Sources, Metabolism, and Nutritional Significance. Nutrition Reviews, 56: 317 -333. doi:10.1111/j.1753 -4887.1998. tb01670.x .

Brown, B.A. 1980. Routine hematology procedures. In: B.A. Brown (Ed.), Hematology, Principles and Procedures. Lea and Febiger , Philadelphia, USA: 71 - 112.

Castro, R., Zarra, I. and Lamas, J. 2004. Water soluble extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture, 229: 67 -78. doi:10.1016/S0044 -8486(03)00401 -0 .

Citarasu, T. 2010. Herbal biomedicines: a new opportunity for aquaculture industry. Aquaculture International, 18: 403 -414. doi: 10.1007/s10499 -009 -9253 -7 .

Chen, X., Nie, W., Yu, G., Li, Y., Hu, Y., Lu, J. and Jin, L. 2012. Antitumor and immunomodulatory activity of polysaccharides from Sargassum fusiforme . Food and Chemical Toxicology, 50: 695 -700. doi:10.1016/j.fct.2011.11.015

Cheng, A.C., Tu, C.W., Chen, Y.Y., Nan, F.H. and Chen, J.C. 2007. The immunostimulatory effects of sodium alginate and iota-carrageenan on orange-spotted grouper Epinephelus coioides and its resistance against Vibrio alginolyticus . Fish and Shellﬁsh Immunology, 22: 197 205. doi:10.1016/j.fsi.2006.04.009

Chiu, S.T., Tsai, R.T., Hsu, J.P., Liu, C.H. and Cheng, W. 2008. Dietary sodium alginate administration to enhance the non -speciﬁc immune responses, and disease resistance of the juvenile grouper Epinephelus fuscoguttatus . Aquaculture, 277: 66 72. doi:10.1016/j.aquaculture.2008 .01.032

Dalmo, R.A. and Seljelid, R. 1995. The immunomodulatory effect of LPS, laminaran and sulphated laminaran [β (l,3)-D -glucan] on Atlantic salmon, Salmo salar L., macrophages in -vitro. Journal of Fish Diseases, 18: 175 -185.

Dantagnan, P., Hernandez, A., Borquez, A. and Mansilla, A. 2009. Inclusion of macroalgae meal (Macrocystis pyrifera ) as feed ingredient for rainbow trout (Oncorhynchus mykiss ): effect on flesh fatty acid composition. Aquaculture Research, 41: 87 94. doi: 1 0.1111/ j.1365 -2109.2009.02308.x

Diler, I., Tekinay, A.A., Güroy, D., Güroy, B.K. and Soyutürk, M. 2007. Effects of Ulva rigida on the growth, feed intake and body composition of common carp , Cyprinus carpio L. Journal of Biological Sciences, 7: 305 -308. doi:10.3923/jbs.2007.305.3 08 .

Ergün, S., Soyutürk, M., Güroy, B., Güroy, D. and Merrifield, D. 2008. Influence of Ulva meal on growth, feed utilization, and body composition juvenile Nile tilapia, Oreochromis niloticus at two levels of dietary lipid. Aquaculture International, 17: 355 -361. doi: 10.1007/s10499 -008 -9207 -5

Franova, S., Joskova, M., Sutovska, M., Novakova, E., Adamicova, K., Pechanova, O. and Nosalova, G. 2010. The efﬁciency of polyphenolic compounds on allergen induced hyperreactivity of the airways. Biomedicine and Preventive Nutrition, 1: 232 235. doi:10.1016/j.bionut.2010.09.002

Fujiki, K., Matsuyama, H. and Yano, T. 1994. Protective effect of sodium alginates against bacterial infection in common carp, Cyprinus carpio L. Journal of Fish Diseases, 17: 349 -355. doi: 10.1111/j.1365 -2761. 1994.tb00230.x

Fujiki, K. and Yano, T. 1997. Effects of sodium algina te o n the non -speciﬁc defence system of the common carp (Cyprinus carpio L.). Fish and Shellﬁsh Immunology, 7: 417 427.

Fujiki, K., Shin, D., Nakao, M. and Yano, T. 1997. Effects of k-carrageenan on the non -speciﬁc defense system of carp Cyprinus carpio . Fishe ries Science, 63: 934 938.

Güroy, B.K., Cirik, Ş., Güroy, D., Sanver, F. and Tekinay, A.A. 2007: Effects of Ulva rigida or Cystoseira barbata meals as a feed additive on growth performance, feed utilization, and body composition in Nile tilapia, Oreochromis niloticus . Turkish Journal of Veterinary and Animal Sciences, 31: 91 97.

Heo, S.J., Lee, K.W., Song, C.B. and Jeon, Y.J. 2003. Antioxidant activity of enzymatic extracts from brown seaweeds. Algae, 18: 71 -81. doi: 10.4490/ALGAE. 2003.18.1.071 .

Heo, S.J., Park, E.J., Lee, K.W. and Jeon, Y.J. 2005. Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresource Technology, 96: 1613 1623. doi:10.1016/j.biortech.2004.07.013 .

Hernández Serrano, P. 2005. Responsible Use of Antibiotics in Aquaculture. FAO Fisheries Technical Paper. No. 469. FAO, Rome, 109 pp .

Jang, M.S., Kim, J., Lim, C., Kim, Y.K. and Park, H.Y. 2005. Boiled -Water Extract from Hizikia fusiformis Showing Antioxidant Effects. Agricultural Chemistry and Biotechnology, 48: 202 -206.

Jung , S.J., Kitamura, S.I., Song, J.Y., Joung, I.Y. and Oh, M.J. 2005. Complete small subunit rRNA gene sequence of the scuticociliate Miamiensis avidus parhogenic to olive flounder Paralichthys olivaceus . Diseases of Aquatic Organisms, 64: 159 162. doi: 10.3 354/dao064159

Karawita, R., Siriwardhana, N., Lee, K.W., Heo, M.S., Yeo, I.K., Lee, Y.D. and Jeon, Y.J. 2005. Reactive oxygen species scavenging, metal chelation, reducing power and lipid peroxidation inhibition properties of different solvent fractions from Hizikia fusiformis. Food Research Technology, 220: 363 371. doi: 10.1007/s00217 -004 -1044 -9

Kang, K.A., Lee, K.H., Chae, S., Koh, Y.S., Yoo, B.S., Kim, J.H., Ham, Y.M., Baik, J.S., Lee, N.H. and Huun, J.W. 2005. Triphlorethol-A from Ecklonia cava protec ts V79 -4 lung ﬁbroblast against hydrogen peroxide induced cell damage. Free Radical Research, 39: 883 892. doi: 10.1080/10715760500161165

Kang, R.S., Won, K.S., Hong, K.P. and Kim, J.M. 2001. Population studies on the Kelp Ecklonia cava and Eisenia bicyclis in Dokdo, Korea. Algae, 16: 209 -215.

Kim, J.A., Lee, J.M., Shin, D.B. and Lee, N.H. 2004. The antioxidant activity and tyrosinase inhibitory activity of phlorotannins in Ecklonia cava . Food Science and Biotechnology, 13: 476 480.

Kim, S.S., Rahimnejad, S ., Kim, K.W. and Lee, K.J. 2013. Partial Replacement of Fish Meal with Spirulina pacifica in Diets for Parrot Fish (Oplegnathus fasciatus ). Turkish Journal of Fisheries and Aquatic Sciences, 13: 197 204. doi: 10.4194/1303 -2712 - v13_2_01

Kim, S.S. and Lee, K .J. 2008. Effects of dietary kelp (Ecklonia cava ) on growth and innate immunity in juvenile olive flounder Paralichthys olivaceus (Temminck et Schlegel). Aquaculture Research, 39: 1687 -1690. doi: 10.1111/j.1365 -2109.2008.02046.x

Kubota, S.S., Kaige, N., Miyazaki, T. and Miyashita, T. 1981. Histopathological studies on Edwardsiellosis of tilapia -1. Natural infection. Bulletin of the Faculty of Fisheries. Mie University, 9: 155 -165.

Lee, D.J. and Putn a m, G.B. 1973. The response of rainbow trout to varying protein/energy ratios in a test diet. Journal of Nutrition, 103: 916 -922.

Leiro, J.M., Castro, R., Arranz, J.A. and Lamas, J. 2007. Immunomodulating activities of acidic sulphatated polysaccharides obtained from the seaweed Ulva rigida C.Agardh. International Immunopharmacology, 7: 879 -888.

Liang, M., Wang, J., Chang, Q. and Mai, K. 2006. Effects of different levels of fish protein hydrolysate in the diet on the nonspecific immunity of Japanese sea bass, Lateolabrax japonicus (Cuvieret Valenciennes , 1828). Aquaculture Research, 37: 102 106. doi: 10.1111/j.1365 -2109.2005.01392.x

Lindequist, U. and Schweder, T. 2001. Marine Biotechnology. In: H.J. Rehm and G. Reed (Eds.), Biotechnology, Wiley-VCH, Weinheim, 10 : 441 -484.

Liu, J.N., Yoshida, Y., Wang, M.Q., Okai, Y. and Yamashita, U. 1997. B cell stimulating activity of seaweeds extracts. International Journal of Immunopharmacology, 19: 135 -142. doi: 10.1016/S0192 -0561(97)00016 -7

McPhearson, R.M., DePaola, A., Zwyno, Z.R., Motes, M.L. and Guarino, A.M. 1991. Antibiotic resistance in Gram-negative bacteria from cultured catfish and aquaculture ponds. Aquaculture, 99: 203 -211. doi: 10.1016/0044 -8486(91)90241 -X

Minagawa, T., Nakai, T. and Muroga, K. 1983. Edwardsiella tarda in eel culture environment. Fish Patholog y, 17: 243 -250.

Nakagawa, H. 2011. Quality control of cultured fish by feed supplements . In: H -J. Ceccaldi, I. Dekeyser, M. Girault, G. Stora (Eds.), Global Change: Mankind - Marine Environment Interactions , Springer Science+Business Media B.V., Netherlands: 31 -34.

Nakatsugawa, T. 1983. Edwardsiella tarda isolated from cultured young flounder, Fish Pathology, 18: 99 101. Newman, D.J., Cragg, G.M. and Snader, K.M. 2003.

Natural products as source of new drugs over the period 1981 -2002, Journal of Natural Products, 66 : 1022 -1037. doi: 10.1021/np030096l

Okai, Y., Okai, K.H., Ishizaka, S. and Yamashita, U. 1997. Enhancing effect of polysaccharides from an edible brown alga, Hijikia fusiformes (Hijikia), on release of tumor necrosis factor alpha from macrophages of endotoxin -nonresponder C3H/HeJ mice. Nutrition and Cancer, 27: 74 -79. doi:10.1 080/01635589709514505 .

Okai, Y., Okai, K.H., Ishizaka, S., Ohtani, K., Yuasa, I.M. and Yamashita, U. 1998. Possible immunomodulating activities in an extract of edible brown algae, Hijikia fusiformes (Hijikia). Journal of the Science of Food and Aqriculture, 76: 56 -62. doi: 10.1002/(SICI)1097 - 0010(199801)76:1_____56::AID-JSFA927>3.0.CO;2 -L. Park, S.L. 2009. Disease control in Korean aquaculture. Fish Pathology, 44: 19 -23. doi: 10.3147/jsfp.44.19 .

Peddie, S., Zou, J. and Secombes, C.J. 2002. Immunostimulation in the rainbow trout (Oncorhynchus mykiss) following intraperitoneal administration of Ergosan. Veterinary Immunology and Immunopathology, 86: 101 113. doi: 10.1016/S0165 -2427(02)00019 -3 .

Pham, M.A., Lee, K.J., Lee, B.J., Lim, S.J., Kim, S.S., Lee, Y.D., He o, M.S. and Lee, K.W. 2006. Effects of dietary Hizikia fusiformis on growth and immune responses in juvenile olive flounder ( Paralichthys olivaceus ). Asian - Australasian Journal of Animal Sciences, 19: 1769 -1775.

Plumb, J.A. 1999. Edwardsiella septicaemia s . In: P.T.K. Woo (Ed.), Fish Disease and Disorders. Viral, Bacterial and Fungal Infections. CAB International Wallingford, UK: 479 -521 .

Sae-Oui, D., Muroga, K. and Nakai, T. 1984. A case of Edwardsiella tarda in cultured colored carp, Cyprinus carpio . Fish Pathology, 19: 197 199.

Shan, B.E., Yoshida, Y., Koroda, E. and Yamashita, U. 1999. Immunomodulating activity of seaweed extract on human lymphocytes in vitro. International Journal of Immunopharmacology, 21: 59 -70. doi: 10.1016/S0192 -0561(98)00063 -0 .

Siriwardhana, N., Lee, K.W., Kim, S.H., Ha, J.H. and Jeon, Y.J. 2003a. Antioxidant activity of Hizikia fusiformis on reactive oxygen species scavenging and lipid peroxidation inhibition. Food Science and Technology International, 9: 339 -348. doi: 10.1177 /108201303039014 .

Siriwardhana, N., Lee, K.W., Kim, S.H., Ha, J.H., Park, G.T. and Jeon, Y.J. 2003b. Lipid peroxidation inhibitory effects of Hizikia fusiformis methanolic extract on fish oils and linoleic acid. Food Science and Technology International, 1 0: 65 -72. doi: 10.1177/1082013204043883 .

Siriwardhana, N., Jeon, Y.J., Kim, S.H., Ha, J.H., Heo, S.J. and Lee, K.W. 2004. Enzymatic hydrolysis for effective extraction of antioxidative compounds from Hizikia fusiformis. Algae, 19: 59 -68. doi: 10.4490/ algae.2004.19.1.059 .

Siriwardhana, N., Lee, K.W. and Jeon, Y.J. 2005. Radical scavenging potential of hydrophilic phlorotannins of Hizikia fusiformis. Algae, 20: 69 75. doi: 10.4490/algae.2005.20.1.069

Skerget, M., Kotnik, P., Hadolin, M., Hras, A.R., Simonic, M. and Knez, Z. 2005. Phenols, proanthocyanidins, flavones and flavonols in some plant materials and the antioxidant activities. Food Chemistry, 89: 191 -198. doi: 10.1016/j.foodchem.2004.02.025 .

Skjermo, J., Defoort, T., Dehasque, M., Espevik, T., Olsen, Y., Skjåk-Braek, G., Sorgeloos, P. and Vadstein, O. 1995. Immunostimulation of juvenile turbot (Scophthalmus maximus L.) using an alignate with high mannuronic acid content administered via the live food organism Artemia. Fish and Shellfish Immunology, 5: 5 31 -534. doi:10.1016/S1050 -4648 (95)80053 -0 .

Song, J.W., Jang, J.W., Kim, S.S., Oh, D.H., Cha, J.H. and Lee, K.J. 2011. Effect of Dietary Supplementation with Alga (Hizikia fusiformis and Ecklonia cava ) on the Non -specific Immune Responses of Parrot Fish Oplegnathus fasciatus . Korean Journal of Fisheries and Aquatic Sciences, 44: 332 -338. doi: 10.5657/KFAS.2011.0332 .

Takashi, N., Akihiro, F., Terukazu, N., Michio, F. and Eisuke, K. 1999. Inhibition of the generation of thrombin and factor Xa by a fucoidan f rom the brown seaweed Ecklonia kurome . Thrombosis Research, 96: 37 -49. doi: 10.1016/S0049 -3848(99)00060 -2 .

Takashi, N., Tomoko, Y., Mariko, H., Terukazu, N. and Haruo, S. 2000. Effects of a fucoidan on the activation of plasminogen by u -PA and t-PA. Thromb osis Research, 99: 623 -634. doi:10.1016/S0049 -3848(00) 00289 -9 .

Whyte, S.K. 2007. The innate immune response of finfish: A review of current knowledge. Fish and Shellfish Immunology, 23: 1127 -1151. doi:10.1016/j.fsi.2007.06.005

Yeh, S.P., Chang, C.A., Ch ang, C.Y., Liu, C.H. and Cheng, W. 2008. Dietary sodium alginate administration affects ﬁngerling growth and resistance to Streptococcus sp. and iridovirus , and juvenile non - speciﬁc immune responses of the orange -spotted grouper, Epinephelus coioides . Fish and Shellﬁsh Immunology, 25: 19 -27. doi: 10.1016/j.fsi.2007.11.011 .