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Journal of Applied Phycology

, Volume 31, Issue 2, pp 1467–1474 | Cite as

Dietary substitution effect of Ulva australis for Undaria pinnatifida on growth, body composition and air exposure of juvenile abalone, Haliotis discus (Reeve 1846)

  • Most. Waheda Rahman Ansary
  • Hae Seung Jeong
  • Ki Wook Lee
  • Pil Youn Kim
  • June Kim
  • Ah-Yeong Yun
  • Sung Hwoan ChoEmail author
  • Tae-Ik Kim
Article

Abstract

Substitution effect of Undaria pinnatifida with Ulva australis in formulated diet on growth, body composition and air exposure of abalone (Haliotis discus) was investigated. A total of 1260 juvenile abalone were distributed into 21 cages. Six formulated diets and dry Undaria were prepared. The control (UA0) diet contained 20% U. pinnatifida. Twenty, 40, 60, 80, and 100% U. pinnatifida were substituted with the same amount of U. australis, referred to as the UA20, UA40, UA60, UA80, and UA100 diets, respectively. Undaria was prepared to compare effect of formulated diet on performance of abalone. Abalone were fed with one of the experimental diets for 16 weeks. After the 16-week feeding trial, abalone were subjected to air exposure for 24 h, and then, cumulative mortality was monitored for the next 4 days. Higher survival, weight gain, and specific growth rate (SGR) were observed in abalone fed all formulated diets than the Undaria. Abalone fed the UA60 diet produced the greatest weight gain and SGR. No difference in proximates of the soft body of abalone was observed. The cumulative mortality of abalone fed the Undaria was higher than all formulated diets at 84 h until the end of the 4-day post observation after 24-h air exposure. Abalone fed the UA0 diet showed higher mortality than other formulated diets at 84 h until the end of the 4-day post observation. In conclusion, U. pinnatifida could be completely replaced with U. australis in abalone feed. The best growth was obtained in abalone fed the UA60 diet.

Keywords

Algae Abalone (Haliotis discusUndaria pinnatifida Ulva australis Dietary substitution Air exposure 

Notes

Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (2017R1A2B4009773). This work was also supported by a grant from the National Institute of Fisheries Science, Republic of Korea (R2018009).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. AOAC (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists, ArlingtonGoogle Scholar
  2. Bansemer MS, Qin JG, Currie K, Stone DAJ (2015) Temperature dependent feed consumption patterns of greenlip (Haliotis laevigata) and hybrid (H. laevigata × Haliotis rubra) abalone fed fresh macroalgae or a formulated diet. J Shellfish Res 34:1–8CrossRefGoogle Scholar
  3. Bautista-Teruel MN, Fermin AC, Koshio SS (2003) Diet development and evaluation for juvenile abalone, Haliotis asinina: animal and plant protein sources. Aquaculture 219:645–653CrossRefGoogle Scholar
  4. Bolton JJ, Robertson-Andersson DV, Shuuluka D, Kandjengo L (2009) Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J Appl Phycol 21:575–583CrossRefGoogle Scholar
  5. Britz PJ (1996) Effect of dietary protein level on growth performance of south African abalone, Haliotis midae, fed fishmeal-based semi-purified diets. Aquaculture 140:55–61CrossRefGoogle Scholar
  6. Cho SH (2010) Effect of fishmeal substitution with various animal and/or plant protein sources in the diet of the abalone Haliotis discus hannai Ino. Aquac Res 41:e587–e593Google Scholar
  7. Cho SH, Park J, Kim C, Yoo J, Lee S (2006) Effect of the various sources of dietary additives on growth, body composition and shell color of abalone Haliotis discus hannai. J Aquac 19:275–280Google Scholar
  8. Cho SH, Park J, Kim C, Yoo J (2008a) Effect of casein substitution with fishmeal, soybean meal and crustacean meal in the diet of the abalone Haliotis discus hannai Ino. Aquac Nutr 14:61–66CrossRefGoogle Scholar
  9. Cho SH, Kim C, Cho YJ, Lee B, Park J, Yoo J, Lee S (2008b) Effects of the various dietary additives on growth and tolerance of abalone Haliotis discus hannai against stress. J Aquac 21:309–316Google Scholar
  10. Choi TS, Kang EJ, Kim J, Kim KY (2010) Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae 25:17–26CrossRefGoogle Scholar
  11. Choi J, Ma Y, Lee B, Moon HE, Cho KK, Cho IS (2014) Seasonal variation of antibacterial activities in the green alga Ulva pertusa Kjellman. J Environ Biol 35:341–344Google Scholar
  12. Choi DG, Kim J, Yun A, Cho SH, Jeong HS, Lee KW, Kim HS, Kim PY, Ha MS (2018) Dietary substitution effect of fish meal with tunic meal of sea squirt, Halocynthia roretzi, Drasche on growth and soft body composition of juvenile abalone, Haliotis discus, reeve 1846. J World Aquacult Soc (in press)Google Scholar
  13. Cook PA (2016) Recent trends in worldwide abalone production. J Shellfish Res 35:581–583CrossRefGoogle Scholar
  14. Dang VT, Li Y, Speck P, Benkendorff K (2011) Effects of micro and macroalgal diet supplementations on growth and immunity of greenlip abalone, Haliotis laevigata. Aquaculture 320:91–98CrossRefGoogle Scholar
  15. Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42CrossRefGoogle Scholar
  16. FishStatJ (2018) Food and Agriculture Organization of the United Nations. RomeGoogle Scholar
  17. Fleming AE, Barneveld RJ, Hone PW (1996) The development of artificial diet for abalone: a review and future directions. Aquaculture 140:5–53CrossRefGoogle Scholar
  18. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28CrossRefGoogle Scholar
  19. Gao G, Clare AS, Rose C, Caldwell GS (2017) Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase future challenge scenarios. Mar Pollut Bull 114:439–447CrossRefGoogle Scholar
  20. Garcia-Esquivel Z, Felbeck H (2009) Comparative performance of juvenile red abalone, Haliotis rufescens, reared in laboratory with fresh kelp and balanced diets. Aquac Nutr 15:209–217CrossRefGoogle Scholar
  21. Hernández J, Uriarte I, Viana MT, Westermeier R, Farías A (2009) Growth performance of weaning red abalone (Haliotis rufescens) fed with Macrocystis pyrifera plantlets and Porphyra columbina compared with a formulated diet. Aquac Res 40:1–9CrossRefGoogle Scholar
  22. Hooper C, Day R, Slocombe R, Benkendorff K, Handlinger J (2011) Effect of movement stress on immune function in farmed Australian abalone (hybrid Haliotis laevigata and Haliotis rubra). Aquaculture 315:348–354CrossRefGoogle Scholar
  23. Hooper C, Day R, Slocombe R, Benkendorff K, Handlinger J, Goulias J (2014) Effects of severe heat stress on immune function, biochemistry and hitopathology in farmed Australian abalone (hybrid Haliotis laevigata × Haliotis rubra). Aquaculture 432:26–37CrossRefGoogle Scholar
  24. Jang B, Kim PY, Kim HS, Lee KW, Kim HJ, Choi DG, Cho SH, Min B, Kim K, Han H (2017) Substitution effect of sea tangle (ST) (Laminaria japonica) with tunic of sea squirt (SS) (Halocynthia roretzi) in diet on growth and carcass composition of juvenile abalone (Haliotis discus, Reeve 1846). Aquac Nutr 24:586–593CrossRefGoogle Scholar
  25. Jung W, Kim HS, Lee KW, Kim YE, Choi DK, Jang B, Cho SH, Choi CY, Kim B, Joo Y (2016) Growth and body composition effects of tuna byproduct meal substituted for fish meal in the diet of juvenile abalone, Haliotis discus. J World Aquacult Soc 47:74–81CrossRefGoogle Scholar
  26. Kim KY, Choi TS, Kim JH, Han T, Shin HW, Garbary DJ (2004) Physiological ecology and seasonality of Ulva pertusa on a temperate rocky shore. Phycologia 43:483–492CrossRefGoogle Scholar
  27. Kim YE, Myung SH, Kim HS, Jung W, Cho SH, Jwa MS, Kim PY, Kim MK, Park M, Kim B (2016) Effect of dietary substitution of sea tangle (ST), Laminaria japonica with rice bran (RB) on growth and body composition of juvenile abalone (Haliotis discus). Aquac Res 47:1202–1208CrossRefGoogle Scholar
  28. Kim J, Kwak HS, Kim BG (2017) Effects of various physical and chemical factors on the death of trouble seaweed Ulva australis. Weed Turf Sci 6:222–234CrossRefGoogle Scholar
  29. Lange B, Currie K, Howarth GS, Stone DAJ (2014) Grape seed extract and dried macroalgae, Ulva lactuca Linnaeus, improve survival of greenlip abalone, Haliotis laevigata Donovan, at high water temperature. Aquaculture 43:348–360CrossRefGoogle Scholar
  30. Lee J, Kim B (2013) Feeding stimulants and feeding preference of Haliotis discus Reeve (Jeju island) to marine algae. Korean J Environ Biol 31:458–470CrossRefGoogle Scholar
  31. Lee KW, Kim HS, Yun A, Choi DG, Jang BI, Kim HJ, Cho SH, Joo Y, Kim B, Min B (2016) Effect of the formulated diets on performance and resistance of juvenile abalone [(Haliotis discus, (Reeve 1846)] subjected to various stress conditions. J Shellfish Res 35:1–11CrossRefGoogle Scholar
  32. Li Y, Song W, Xiao J, Wang Z, Fu M, Zhu M, Li R, Zhang X, Wang X (2014) Tempo-spatial distribution and species diversity of green algae micro-propagules in the Yellow Sea during the large-scale green tide development. Harmful Algae 39:40–47CrossRefGoogle Scholar
  33. Li H, Zhang Y, Han X, Shi X, Rivkin RB, Legendre L (2016) Growth responses of Ulva prolifera to inorganic and organic nutrients: implications for macroalgal blooms in the southern Yellow Sea, China. Sci Rep 6:26498CrossRefGoogle Scholar
  34. Mai K, Mercer JP, Donlon J (1995a) Comparative studies on the nutrition of species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino. III. Responses of abalone to various levels of dietary lipid. Aquaculture 134:65–80CrossRefGoogle Scholar
  35. Mai K, Mercer JP, Donlon J (1995b) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino. IV. Optimum dietary protein level for growth. Aquaculture 136:165–180CrossRefGoogle Scholar
  36. Malham S, Lacoste A, Gelebart A, Cueff A, Poulet S (2003) Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata. J Exp Zool 295A:136–144CrossRefGoogle Scholar
  37. Morash AJ, Alter K (2016) Effects of environmental and farm stress on abalone physiology: perspectives for abalone aquaculture in the face of global climate change. Rev Aquac 8:342–368CrossRefGoogle Scholar
  38. Mulvaney WJ, Winberg PC, Adams L (2013) Comparison of macroalgal (Ulva and Gateloupia spp.) and formulated terrestrial feed on the growth and condition of juvenile abalone. J Appl Phycol 25:815–824CrossRefGoogle Scholar
  39. Myung SH, Jung W, Kim HS, Kim YE, Cho SH, Jwa MS, Kim PY, Kim MK, Park M, Kim B (2016) Effects of dietary substitution of fishmeal with the combined dry microalgae, Nannochloropsis oceanica (NO) biomass residue and casein on growth and body composition of juvenile abalone (Haliotis discus). Aquac Res 47:341–348CrossRefGoogle Scholar
  40. Naidoo K, Maneveldt G, Ruck K, Bolton JJ (2006) A comparison of various seaweed-based diets and formulated feed on growth rate of abalone in a landbased aquaculture system. J Appl Phycol 18:437–443CrossRefGoogle Scholar
  41. Nisizawa K, Noda H, Kikuchi R, Watanabe T (1987) The main seaweed foods in Japan. Hydrobiologia 151/152:5–29CrossRefGoogle Scholar
  42. O’Mahoney M, Rice O, Mouzakitis G, Burnell G (2014) Towards sustainable feeds for abalone culture: evaluating the use of mixed species seaweed meal in formulated feeds for the Japanese abalone, Haliotis discus hannai. Aquaculture 430:9–16CrossRefGoogle Scholar
  43. Oakes FR, Ponte RD (1996) The abalone market: opportunities for cultured abalone. Aquaculture 140:187–195CrossRefGoogle Scholar
  44. Ohno M (1999) Ulva and excessive growth. In: Notoya M (ed) Utilization of Ulva spp and environmental restoration. Seizando, Tokyo, pp 1–11 (in Japanese)Google Scholar
  45. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernández J, Bozzo CE, Navarrete CE, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem 99:98–104CrossRefGoogle Scholar
  46. Osako K, Ohashi S, Hossain MA, Kuwahara K, Okamoto A, Nozaki Y, Furukawa M (2004) The aptitude of sea lettuce (Ulva pertusa) as a diet for abalone, from a nutritional viewpoint. Suisanzoshoku 52:401–406Google Scholar
  47. Shpigel M, Ragg NL, Lupatsch I, Neori A (1999) Protein content determines the nutritional value of the seaweed Ulva lactuca L. for the abalone Haliotis tuberculata L. and H. discus hannai Ino. J Shellfish Res 18:227–233Google Scholar
  48. Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88CrossRefGoogle Scholar
  49. Taylor M, Tsvetnenko E (2004) A growth assessment of juvenile abalone Haliotis laevigata fed enriched macroalgae Ulva rigida. Aquac Int 12:467–480CrossRefGoogle Scholar
  50. Uki N, Kemuyama A, Watanabe T (1986) Optimum protein level in diets for abalone. Bull Jpn Soc Sci Fish 52:1005–1012CrossRefGoogle Scholar
  51. Viera MP, Courtois de Vicose G, Gomez-Pinchetti JL, Bilbao A, Fernandez-Palacios H, Izquierdo MS (2011) Comparative performance of juvenile abalone (Haliotis tuberculata coccinea reeve) fed enriched vs non-enriched macroalgae: effect on growth and body composition. Aquaculture 319:423–429CrossRefGoogle Scholar
  52. Wang C, Rencheng YU, Zhou M (2011) Acute toxicity of live and decomposing green alga Ulva (Enteromorpha) prolifera to abalone Haliotis discus hannai. Chin J Oceanol Limnol 29:541–546CrossRefGoogle Scholar
  53. Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2011) Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem 128:895–901CrossRefGoogle Scholar
  54. Yim E, Park I, Han H, Kim S, Cho H, Kim S (2010) Acute toxicity assessment of new algicides of thiazolidinediones derivatives, TD53 and TD49, using Ulva pertusa Kjellman. Environ Health Toxicol 25:273–278Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Convergence Study on the Ocean Science and TechnologyKorea Maritime and Ocean UniversityBusanSouth Korea
  2. 2.Ocean and Fisheries Research InstituteJejuSouth Korea
  3. 3.Division of Marine BioscienceKorea Maritime and Ocean UniversityBusanSouth Korea
  4. 4.Southeast Sea Fisheries Research InstituteNational Institute of Fisheries ScienceTongyeong-siSouth Korea

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