Log in

Diets comprising hen egg yolk and milk proteins as potential alternatives to shark egg-based diets for larvae of the Japanese eel Anguilla japonica

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

The only diet that has been capable of rearing eel larvae to the glass eel stage in captivity is the shark egg (SE)-based diet (SE). This study investigated the potential of alternative dietary components, namely hen egg yolk (HEY), milk proteins, and fish protein hydrolysate (FPH), on the growth and survival of eel larvae. In the first experiment, a diet containing HEY and skimmed milk powder (HS) was compared to SE. There were no significant differences in growth and survival rate between the two diets except in the early part of the experiment period. In the second experiment, HS was modified by the addition of FPH and casein (FC), and larval performance was evaluated for three dietary regimens (SE, HS, and FC). The performance of larvae fed HS and FC was found to be comparable or superior to those fed SE. It was observed that larvae fed the alternative diets to SE were able to progress to glass eels. However, more skeletal abnormalities were observed in HS in experiment 1. The results of this study indicate that a combination of HEY and milk proteins is suitable as a larval eel diet, and that it has the potential to replace SE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data presented in this study are contained within the article.

References

  • Bandara KA, Benini E, Politis SN, Conceição LE, Santos A, Sørensen SR, Tomkiewicz J, Vadstein O (2023) Exploring bacterial community composition and immune gene expression of European eel larvae (Anguilla anguilla) in relation to first feeding diets. PLoS ONE 18:e0288734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benini E, Bandara KA, Politis SN, Engrola S, Nielsen A, Conceição LE, Santos A, Sørensen SR, Tomkiewicz J (2023) Exploring first-feeding diets for European eel larval culture: Insights at morphological, nutritional, and molecular levels. PLoS ONE 18:e0283680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cahu CL, Zambonino Infante JL (1995) Maturation of the pancreatic and intestinal digestive functions in sea bass (Dicentrarchus labrax): effect of weaning with different protein sources. Fish Physiol Biochem 14:431–437

    Article  CAS  PubMed  Google Scholar 

  • Cahu C, Zambonino Infante J (2001) Substitution of live food by formulated diets in marine fish larvae. Aquaculture 200:161–180

    Article  Google Scholar 

  • Cahu CL, Zambonino Infante JL, Quazuguel P, Le Gall MM (1999) Protein hydrolysate vs. fish meal in compound diets for 10-day old sea bass (Dicentrarchus labrax) larvae. Aquaculture 171:109–119

    Article  CAS  Google Scholar 

  • Cahu C, Zambonino Infante J, Takeuchi T (2003) Nutritional components affecting skeletal development in fish larvae. Aquaculuture 227:245–258

    Article  CAS  Google Scholar 

  • Carvalho AP, Sá R, Oilva-Teles A, Bergot P (2004) Solubility and peptide profile affect the utilization of dietary protein by common carp (Cyprinus carpio) during early larval stages. Aquaculture 234:319–333

    Article  CAS  Google Scholar 

  • Coutteau P, Geurden I, Camara MR, Bergot P, Sprgeloos P (1997) Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155:149–164

    Article  CAS  Google Scholar 

  • Doi T, Satoh K, Kanzaki M, Matsumoto K (1991) An investigation to determine lactose by using oxidation-reduction reaction and its application to some kinds of milk and milk products. Nippon Shokuhin Kogyo Gakkaishi 38:575–580 (In Japanese with English abstract)

    Article  CAS  Google Scholar 

  • Dou Y, Yamada Y, Okamura A, Tanaka S, Shinoda A, Tsukamoto K (2007) Observations on the spawning behavior of artificially matured Japanese eels Anguilla japonica in captivity. Aquaculture 266:117–129

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Fernández I, Gisbert E (2011) The effect of vitamin A on flatfish development and skeletogenesis: a review. Aquaculture 315:34–48

    Article  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    Article  CAS  PubMed  Google Scholar 

  • Fu**o Y (1971) Chemistry of lipids in egg yolk. J Jpn Soc Food Nutr 24:317–324 (In Japanese with English abstract)

    CAS  Google Scholar 

  • Furuita H, Takeuchi T, Watanabe T, Fujimoto H, Sekiya S, Imaizumi K (1996) Requirements of larval yellowtail for eicosapentaenoic acid, docosahexaenoic acid, and highly unsaturated fatty acid. Fish Sci 62:372–379

    Article  CAS  Google Scholar 

  • Furuita H, Murashita K, Matsunari H, Yamamoto T, Nagao J, Nomura K, Tanaka H (2014a) Decreasing dietary lipids improves larval survival and growth of Japanese eel Anguilla japonica. Fish Sci 80:581–587

    Article  CAS  Google Scholar 

  • Furuita H, Tanaka H, Nomura K, Nagao J, Masuda Y, **bo T, Yamamoto T, Tokuda M, Murashita K, Matsunari H, Kurokawa T, Awaji M, Oku H, Kim, S-K, Yoshimatsu T (2014b) Improvement of slurry type diet and development of new diet for larval eel. In: Development of Seed Production Technology in Japanese Eel. Agriculture, Forestry and Fisheries Research Council, Tokyo, pp136–140 (In Japanese)

  • Geurden I, Radünz-Neto J, Bergot P (1995) Essentiality of dietary phospholipids for carp (Cyprinus carpio L.) larvae. Aquaculture 131:303–314

    Article  CAS  Google Scholar 

  • Gisbert E, Villeneuve L, Zambonino-Infante JL, Quazuguel P, Cahu CL (2005) Dietary phospholipids are more efficient than neutral lipids for long-chain polyunsaturated fatty acid supply in European sea bass Dicentrarchus labrax larval development. Lipids 40:609–618

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Kishimura H (2000) Distribution and compositions of diacyl glyceryl ethers in different tissues of the mature and immature spiny dogfish, Squalus acanthias. J Jpn Oil Chem Soc 49:325–331

    Article  CAS  Google Scholar 

  • Hemre G-I, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

    Article  CAS  Google Scholar 

  • Izquierdo MS, Watanabe T, Takeuchi T, Arakawa T, Kitajima C (1989) Optimum EFA levels in Artemia to meet the EFA requirements of red sea bream (Pagrus major). Proc. 3rd Int. Symp Feeding and Nutri Fish, Toba, August 28 Sep 1, Japan pp 221–232

  • Izquierdo MS, Arakawa T, Takeuchi T, Haroun R, Watanabe T (1992) Effect of n-3 HUFA levels in Artemia on growth of larval Japanese flounder (Paralichthys olivaceus). Aquaculture 105:73–82

    Article  CAS  Google Scholar 

  • Jang BI, Olowe OS, Cho SH (2022) Evaluation of the optimal protein required in granulated microdiets for rockfish (Sebastes schlegeli) larvae. Aquac Nutr. https://doi.org/10.1155/2022/2270384

    Article  PubMed  PubMed Central  Google Scholar 

  • Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non- phosphorous lipids from rat heart using silica cartridges. Lipids 20:40–41

    Article  CAS  PubMed  Google Scholar 

  • Kagawa H, Tanaka H, Ohta H, Okuzawa K, Iinuma N (1997) Induced ovulation by injection of 17,20ß-dihydroxy-4-pregnen-3-one in the artificially matured Japanese eel, with special reference to ovulation time. Fish Sci 63:365–637

    Article  CAS  Google Scholar 

  • Kagawa H, Sakurai Y, Horiuchi R, Kazeto Y, Gen K, Imaizumi H, Masuda Y (2013) Mechanism of oocyte maturation and ovulation and its application to seed production in the Japanese eel. Fish Physiol Biochem 39:13–17

    Article  CAS  PubMed  Google Scholar 

  • Kim S-K, Lee B-I, Kim D-J, Lee N-S (2014) Development of the slurry type diet for the growing leptocephalus, eel larvae (Anguill japonica). J Fish Mar Sci Edu 26:1209–1216 (In Korean with English abstract)

    Google Scholar 

  • Kuroki M, Okamura A, Takeuchi A, Tsukamoto K (2016) Effect of water current on the body size and occurrence of deformities in reared Japanese eel leptocephali and glass eels. Fish Sci 82:941–951

    Article  CAS  Google Scholar 

  • Masuda Y, Oku H, Nomura K, Teruya K, Tanaka H (2010) A colloid-type diet can be ingested by the larvae of the Japanese eel Anguilla japonica. J Fish Tech 2:99–104 (In Japanese with English abstract)

    Google Scholar 

  • Masuda Y, Imaizumi H, Oda K, Hashimoto H, Usuki H, Teruya K (2012) Artificial completion of the Japanese eel, Anguilla japonica, life cycle: challenge to mass production. Bull Fish Res Agency 35:111–117

    Google Scholar 

  • Masuda Y, **bo T, Imaizumi H, Fujimoto H, Nagao J, Kawakami Y (2013a) Simplification of changing rearing tank in the rearing procedure for Japanese eel Anguilla japonica larvae. J Fish Tech 6:33–38 (In Japanese with English abstract)

    Google Scholar 

  • Masuda Y, **bo T, Imaizumi H, Furuita H, Matsunari H, Murashita K, Fujimoto H, Nagao J, Kawakami Y (2013b) A step forward in development of fish protein hydrolysate-based diet for larvae of Japanese eel Anguilla japonica. Fish Sci 79:681–688

    Article  CAS  Google Scholar 

  • Masuda Y, Yatabe T, Matsunari H, Furuita H, Kamoshida M, Shima Y, Kuwada H (2016) Rearing of larvae of Japanese eel Anguilla japonica to metamorphosis into glass eel by feeding with fish protein hydrolysate-based diets. Nippon Suisan Gakkaishi 82:131–133 (In Japanese)

    Article  CAS  Google Scholar 

  • Miyashita K, Inukai N, Ota T, Sasaki S, Ota T (1999) Antioxidant activity of water extracts from fish eggs on PC liposomes. Nippon Suisan Gakkaishi 65:488–494 (In Japanese with English abstract)

    Article  Google Scholar 

  • Nose T, Arai S (1973) Optimum level of protein in purified diet for eel, Anguilla japonica. Bull Freshwater Fish Res Lab 22:145–154

    Google Scholar 

  • Ohta H, Sato Y, Imaizumi H, Kazeto Y (2017) Changes in milt volume and sperm quality with time after an injection of recombinant Japanese eel luteinizing hormone in male Japanese eels. Aquaculture 479:150–154

    Article  CAS  Google Scholar 

  • Okamura A, Yamada Y, Horie N, Mikawa N, Tanaka S, Kobayashi H, Tsukamoto K (2013) Hen egg yolk and skinned krill as possible foods for rearing leptocephalus larvae of Anguilla japonica Temminck & Schlegel. Aquac Res 44:1531–1538

    Article  CAS  Google Scholar 

  • Okamura A, Horie N, Mikawa N, Yamada Y, Tsukamoto K (2014) Recent advances in artificial production of glass eels for conservation of anguillid eel populations. Ecol Freshw Fish 23:95–110

    Article  Google Scholar 

  • Okamura A, Yamada Y, Horie N, Mikawa N, Tsukamoto K (2019) Long-term rearing of Japanese eel larvae using liquid-type diet: food intake, survival and growth. Fish Sci 85:687–694

    Article  CAS  Google Scholar 

  • Okamura A, Yamada Y, Mikawa N, Hiroe N, Tsukamoto K (2020) Dietary supplementation with chitin hydrolysate for Anguilla japonica leptocephali. Fish Sci 86:685–692

    Article  CAS  Google Scholar 

  • Okorie OE, Kim Y-C, Lee S, Bae J-Y, Yoo JH, Han K, Bai SC, Park G-J, Choi S-M (2007) Reevaluation of the dietary protein requirements and optimum dietary protein to energy ratios in Japanese eel, Anguilla japonica. J World Aquac Soc 38:418–426

    Article  Google Scholar 

  • Péres A, Cahu CL, Zambonino Infante JL, Le Gall MM, Quazuguel P (1996) Amylase and trypsin responses to intake of dietary carbohydrate and protein depend on the developmental stage in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 15:237–242

    Article  PubMed  Google Scholar 

  • Rodriguez C, Perez JA, Lorenzo A, Izquierdo MS, Cejas JR (1994) n-3 HUFA requirement of larval gilthead seabream Sparus aurata when using high levels of eicosapentaenoic acid. Comp Biochem Physiol A 107:693–698

    Article  Google Scholar 

  • Satoh H, Yamamori K, Hibiya T (1992) Induced spawning of the Japanese eel. Nippon Suisan Gakkaishi 58:825–832

    Article  Google Scholar 

  • Shiau S-Y, Chuang J-C (1995) Utilization of disaccharides by juvenile tilapia, Oreochromis niloticus × O. aureus. Aquaculture 133:249–256

    Article  CAS  Google Scholar 

  • Tachiki H, Nakagawa T, Tamura K, Hirose K (1997) Effects of oral administration of estradiol-17ß to young on gonadal sex and growth of Japanese eel Anguilla japonica. Aquacult Sci 45:61–66 (In Japanese with English abstract)

    CAS  Google Scholar 

  • Takeuchi T (2009) Carbohydrate. In: Watanabe T (ed) Nutrition and feeding in fish and crustacean. Koseisha Koseikaku, Tokyo, pp 106–115 (In Japanese)

    Google Scholar 

  • Takeuchi T, Shiina Y, Watanabe T (1992a) Suitable levels of n-3 highly unsaturated fatty acids in diet for fingerlings of red sea bream. Nippon Suisan Gakkaishi 58:509–514

    Article  CAS  Google Scholar 

  • Takeuchi T, Shiina Y, Watanabe T, Sekiya S, Imaizumi K (1992b) Suitable levels of n-3 highly unsaturated fatty acids in diet for fingerlings of yellowtail. Nippon Suisan Gakkaishi 58:1341–1346

    Article  Google Scholar 

  • Takeuchi T, Zheng F, Yoseda K, Hirokawa J, Watanabe T (1994) Nutritive value of DHA-enriched rotifer for larval cod. Nippon Suisan Gakkaishi 60:641–652 ((in Japanese with English abstract))

    Article  CAS  Google Scholar 

  • Tanaka H (2015) Progression in artificial seedling production of Japanese eel Anguilla japonica. Fish Sci 81:11–19

    Article  CAS  Google Scholar 

  • Tanaka H, Kagawa H, Ohta H, Unuma T, Nomura K (2003) The first production of glass eel in captivity: fish reproductive physiology facilitates great progress in aquaculture. Fish Physiol Biochem 28:493–497

    Article  Google Scholar 

  • Tonheim SK, Nordgreen A, Høgøy I, Hamre K, Rønnestad I (2007) In vitro digestibility of water-soluble and water-insoluble protein fractions of some common fish larval feeds and feed ingredients. Aquaculture 262:426–435

    Article  CAS  Google Scholar 

  • Unuma T, Hasegawa N, Sawaguchi S, Tanaka T, Matsubara T, Nomura K, Tanaka H (2011) Fusion of lipid droplets in Japanese eel oocytes: stage classification and its use as a biomarker for induction of final oocyte maturation and ovulation. Aquaculture 322–323:142–148

    Article  Google Scholar 

  • Unuma T, Sawaguchi S, Hasegawa N, Tsuda N, Tanaka T, Nomura K, Tanaka H (2012) Optimum temperature of rearing water during artificial induction of ovulation in Japanese eel. Aquaculture 358–359:216–223

    Article  Google Scholar 

  • Yamada Y, Okamura A, Mikawa N, Horie N, Tsukamoto K (2019) A new liquid-type diet for leptocephali in mass production of artificial grass eels. Fish Sci 85:545–551

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by MAFF commissioned project study on the ‘‘Development of Sustainable Aquaculture Technology Independent of Wild Fishery Resources’’ (JPJ000329).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hirofumi Furuita.

Ethics declarations

Conflict of interest

This study was funded by the Ministry of Agriculture, Forestry and Fisheries (MAFF) of Japan.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Furuita, H., **bo, T., Higuchi, M. et al. Diets comprising hen egg yolk and milk proteins as potential alternatives to shark egg-based diets for larvae of the Japanese eel Anguilla japonica. Fish Sci 90, 295–305 (2024). https://doi.org/10.1007/s12562-024-01752-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-024-01752-7

Keywords

Navigation