Abstract
The improvement in feed efficiency is one of the most important subjects in fish culture. The development of feed, in terms of good intake, high growth performance, and high feed efficiency is needed. Squid viscera are one of the candidates for alternative material in improving feed efficiency in fish culture. In the present study, we described the dietary effect of the squid viscera hydrolysate (SVH) on the growth performance of the red sea bream. The addition of SVH to feed caused significant increases in feed intake, fork length, and body weight and produced a marked improvement in feed conversion after 4 weeks of feeding. Furthermore, the results of this feeding revealed that low dietary levels of SVH promote growth performance in the red sea bream. We physiologically analyzed digestion and appetite in fish fed diet containing SVH. SVH promoted the activity of hepatic trypsin and lipase, gene expression of stomach pepsin, hepatic lipase, and pyloric caeca trypsin, thereby improving the nutrient availability in red sea bream. Moreover, the mRNA expression of appetite regulating factor, such as brain NPY and stomach ghrelin was significantly improved by dietary SVH. Our current results indicate that dietary SVH as alternative material produced excellent effects on growth performance, which is dependent on the promoting effect on digestion and appetite in red sea bream.
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References
Albo PW, Hall RD, Corbett JT, Schroder J (1985) Activation of nonspecific lipase by bile salts. Biochim Biophys Acta Lipids Lipid Metab 835(3):477–490
Chaudhri O, Small C, Bloom S (2006) Gastrointestinal hormones regulating appetite. Philos Trans R Soc Part B 361:1187–1209
Chen HY, Trumbauer ME, Chen AS, Weingarth DT, Adams JR, Frazier EG (2004) Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology 145(6):2607–2612
Chen R, Li W, Lin H (2005) cDNA cloning and mRNA expression of neuropeptide Y in orange spotted grouper, Epinephelus coioides. Comp Biochem Physiol Part B 142:79–89
Cheng ZY, Mai KS, Ai QH, Li Y, He AG (2013) Effects of dietary pregelatinized corn starch on growth, apparent digestibility, and digestive enzyme activity of large yellow croaker fingerlings (Pseudosciaena crocea). Israeli Journal of Aquaculture-Bamidgeh 65:843–850
Erlanger BF, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278
FAO (2009) The state of world fisheries and aquaculture- 2008 (SOFIA). FAO Fisheries and Aquaculture Department, Food And Agriculture Organization Of The United Nations, Rome
Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227
Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac res 38:551–579
Goh Y, Tamaru T (1980) Effect of amino acids on the feeding behavior in red sea bream. Comp Biochem Physiol Part C 66:225–229
Hakim Y, Uni Z, Hulata G (2006) Relationship between intestinal brush border enzymatic activity and growth rate in tilapias fed diets containing 30% or 48% protein. Aquaculture 257:420–428
Hidaka I, Kohbara J, Araki T, Morishita T, Miyajima T, Shimizu S, Kuriyama I (2000) Identification of feeding stimulants from a jack mackerel muscle extract for young yellowtail Seriola quinqueradiata. Aquaculture 181:115–126
Kasumyan AO, Døving KB (2003) Taste preferences in fishes. Fish Fish 4:289–347
Koshio S (2002) Red Sea bream, Pagrus major. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 51–63
Matsuda Y, Hayashi K, Yoshitomi U, Kanazawa A, Takeuchi T (2001) Effect of the combination of raw squid liver to extruded pellet on growth performance and digestibility of dietary nutrients for yellowtail and red sea bream. Aquacult Sci 49(4):483–488
Murashita K, Fukada H, Hosokawa H, Masumoto T (2006) Cholecystokinin and peptide Y in yellowtail (Seriola quinqueradiata): molecular cloning, real-time quantitative RT-PCR, and response to feeding and fasting. Gen Comp Endocrinol 145:287–297
Murray HM, Douglas SE, Gallant JW, Pérez-Casanova JC, Johnson SC (2003) Ontogeny of lipase expression in winter flounder, Pseuodopleuronectes americanus. J Fish Biol 62:816–833
Oku H, Koizumi N, Okumura T, Kobayashi T, Umino T (2006) Molecular characterization of lipoprotein lipase, hepatic lipase and pancreatic lipase genes: effects of fasting and refeeding on their gene expression in red sea bream Pagrus major. Comp Biochem Physiol Part B 145:168–178
Olsen RE, Henderson RJ, Sountama J, Hemre GI, Ringø E, Melle W, Tocher DR (2004) Atlantic salmon, Salmo salar, utilizes was esters-rich oil from Calanus finmarchicus effectively. Aquaculture 240:433–449
Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M (2005) Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245:273–286
Sakurai C, Ohta M, Kanai S, Uematsu H, Funakoshi A, Miyasaka K (2006) Lack of ghrelin secretion in response to fasting in cholecystokinin-A (−1), −B (−2) receptor–deficient mice. J Physiol Sci 56(6):441–444
Satoh N, Nobuta S, Wakasugi M, Satoh S, Takeuchi T (2013) Availability of squid viscera meal with cadmium removal treatment as a feed ingredient for fingerling black rockfish Sebastes schlegeli. Fish Sci 79:259–267
Seki S, Maruyama H, Kawabe M (2015) Modeling of competitive adsorption process for removing cadmium from squid viscera. Nippon Suisan Gakkaishi 81:90–96 (in Japanes)
Shrestha YB, Wickwire K, Giraudo SQ (2009) Direct effects of nutrients, acetylcholine, CCK, and insulin on ghrelin release from the isolated stomachs of rats. Peptides 30:1187–1191 nutritional, environmental and reproductive changes. Comp Biochem Physiol Part A 153:8-12
Stanley S, Wynne K, Mcgowan B, Bloom S (2005) Hormonal regulation of food intake. Physiol rev 85:1131–1158
Storebakken T, Refstie S, Ruyter B (2000) Soy products as fat and protein sources in fish feeds for intensive aquaculture. In: Drackly JK (ed) Soy in animal nutrition. Federation of Animal Science Societies, Champaign, pp 127–170
Takeda M, Takii K, Matsui K (1984) Identification of feeding stimulants for juvenile eel. Nippon Suisan Gakkaishi 59:645–651 (in Japanese)
Ukawa M, Takii K, Nakamura M, Kumai H (1994) Utilization of soybean meal for red sea bream diet. Aquacult Sci 42:335–338
Volkoff H, Eykelbosh AJ, Peter RE (2003) Role of leptin in the control of feeding of goldfish Carassius auratus: interactions with cholecystokinin, neuropeptide Y and orexin A, and modulation by fasting. Brain res 972:90–109
Volkoff H, Xu M, MacDonald E, Hoskins L (2009) Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp Biochem Physiol Part A 153:8–12
Wakasugi M, Tomita K, Nagano N, Sakata Y (2002) Development of processing and utilizing technology of squid viscera. Reports of the Hokkaido Industrial Research Institute Part1 301:39–47 (in Japanese)
Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68:242–252
Yeung CM, Chan CB, Woo NYS, Cheng CHK (2006) Seabream ghrelin: cDNA cloning, genomic organization and promoter studies. J Endocrinol 189:365–379
Acknowledgments
We thank Dr. Fritzie T. Celino-Brady, Department of Human Nutrition, Food and Animal Sciences, University of Hawaii, USA, for critical reading of the manuscript. This work was supported by an A-step Promoting R&D program from the Japan Science and Technology Agency, a grant-in-aid for Scientific Research from the Japan Society for the Promotion of Science, and by Shintoa Corporation.
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Kondo, F., Ohta, T., Iwai, T. et al. Effect of the squid viscera hydrolysate on growth performance and digestion in the red sea bream Pagrus major . Fish Physiol Biochem 43, 1543–1555 (2017). https://doi.org/10.1007/s10695-017-0391-y
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DOI: https://doi.org/10.1007/s10695-017-0391-y