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Journal of Applied Phycology

, Volume 31, Issue 5, pp 3245–3254 | Cite as

Substitution effect of the combined fouling macroalgae Ulva australis and Sargassum horneri for Undaria pinnatifida in formulated diets on growth and body composition of juvenile abalone (Haliotis discus, Reeve 1846) subjected to air exposure stressor

  • Most. Waheda Rahman Ansary
  • Seong Il Baek
  • Hae Seung Jeong
  • Ki Wook Lee
  • Sung Hwoan ChoEmail author
  • Hee Sung Kim
  • Min-Seok Jwa
Article

Abstract

The effect of substituting the combined macroalgae Ulva australis and Sargassum horneri for Undaria pinnatifida in formulated diets on growth and body composition of abalone subjected to air exposure stressor was investigated. A total of 1260 juvenile abalone were distributed into 21 cages. Six formulated diets were prepared. The control (CUS0) diet contained 20% U. pinnatifida. Twenty, 40, 60, 80, and 100% of U. pinnatifida were substituted with an equal amount of the combined U. australis and S. horneri, referred to as the CUS20, CUS40, CUS60, CUS80, and CUS100 diets, respectively. Finally, dry U. pinnatifida was prepared to compare the growth performance of abalone. Abalone were fed with one of the experimental diets once a day for 16 weeks and then subjected to air stressor for 24 h. The cumulative mortality of abalone was monitored for the following 4 days after 24 h of air exposure. Abalone fed all formulated diets attained higher survival, weight gain, and specific growth rate (SGR) than U. pinnatifida. Abalone fed the CUS100 diet achieved greatest weight gain and SGR, followed by the CUS80 and CUS60 diets. The greatest shell growth and heaviest soft-body weight were obtained in abalone fed the CUS100 diet. Proximate composition of the soft body of abalone, except for moisture content, was not affected by the experimental diets. The cumulative mortality of abalone fed the U. pinnatifida was higher than that of abalone fed all formulated diets at 84 h until the end of the 4-day post observation. The lowest cumulative mortality was obtained in abalone fed the CUS80 diet at the end of the 4-day post observation. Therefore, U. pinnatifida could be completely replaced with the combined U. australis and S. horneri in abalone (H. discus) feed.

Keywords

Abalone (Haliotis discusUndaria pinnatifida Substitution effect Sargassum horneri Ulva australis Formulated diet Air exposure stressor 

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 and Future Planning (2017R1A2B4009773). This work was also supported by a grant from the National Institute of Fisheries Science, Republic of Korea (R2019010).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu Rev Mar Sci 4:143–176CrossRefGoogle Scholar
  2. Ansary MWR, Jeong HS, Lee KW, Kim PY, Kim J, Yun A, Cho SH (2019a) Dietary substitution effect of Ulva australis for Undaria pinnatifida on growth, body composition and air exposure of juvenile abalone, Haliotis discus (Reeve 1846). J Appl Phycol 31:1467–1474CrossRefGoogle Scholar
  3. Ansary MWR, Jeong HS, Lee KW, Kim HS, Kim J, Yun A, Cho SH, Kim PY, Kim T (2019b) The effect of substituting Undaria pinnatifida in formulated feeds with Sargassum horneri on growth and body composition of juvenile abalone (Haliotis discus, Reeve 1846). J Appl Phycol.  https://doi.org/10.1007/s10811-018-1672-2
  4. AOAC (1990) Official methods of analysis (15th edn). Association of Official Analytical Chemists, Arlington, VA, USAGoogle Scholar
  5. Baldwin J, Wells RMG, Low M, Ryder JM (1992) Tauropine and D-lactate as metabolic stress indicators during transport and storage of live Paua (New Zealand abalone) (Haliotis iris). J Food Sci 57:280–282CrossRefGoogle Scholar
  6. Bansemer MS, Qin J, Harris JO, Howarth GS, Stone DAJ (2016) Nutritional requirements and use of macroalgae as ingredients in abalone feed. Rev Aquac 8:121–135CrossRefGoogle Scholar
  7. Britz PJ (1996) Effect of dietary protein level on growth performance of South African abalone, Haliotis midae, fed fishmeal-based semi-purified diets. Aquaculture 140:55–61Google Scholar
  8. Chao WR, Huang CY, Sheen SS (2010) Development of formulated diet for post-larval abalone, Haliotis diversicolor supertexta. Aquaculture 307:89–94CrossRefGoogle Scholar
  9. 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
  10. Cho SH, Kim C, Cho YJ, Lee B, Park J, Yoo J, Lee S (2008) Effects of the various dietary additives on growth and tolerance of abalone Haliotis discus hannai against stress. J Aquac 21:309–316Google Scholar
  11. 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 49:1095–1104Google Scholar
  12. Cody RP, Smith JK (1991) Applied statistics and the SAS programming language, 3rd edn. Prentice-Hall, Inc, Englewood Cliffs, pp 163–206Google Scholar
  13. 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
  14. Daume S, Davidson M, Ryan S, Parker F (2007) Comparisons of rearing systems based on algae or formulated feed for juvenile greenlip abalone (Haliotis laevigata). J Shellfish Res 26:729–735CrossRefGoogle Scholar
  15. Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42CrossRefGoogle Scholar
  16. Fleming AE (1995) Digestive efficiency of the Australian abalone Haliotis rubra in relation to growth and feed preference. Aquaculture 134:279–293CrossRefGoogle 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. Hwang EK, Lee SJ, Ha DS, Park CS (2016) Sargassum golden tides in the Shinnan-gun and Jeju Island, Korea. Kor J Fish Aquat Sci 49:689–693Google Scholar
  19. 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
  20. Jang B, Kim PY, Kim HS, Lee KW, Kim HJ, Choi DG, Cho SH, Min B, Kim K, Han H (2018) 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
  21. Jiang X, Tang Y, Lonsdale DJ, Gobler CJ (2009) Deleterious consequences of a red tide dinoflagellate Cochlodinium polykrikoides for the calanoid copepod Acartia tonsa. Mar Ecol Prog Ser 390:105–116CrossRefGoogle Scholar
  22. 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
  23. Kemp JOG, Britz PJ, Toledo Agüero PH (2015) The effect of macroalgal, formulated and combination diets on growth, survival and feed utilization in the red abalone Haliotis rufescens. Aquaculture 448:306–314CrossRefGoogle Scholar
  24. Kim HG (2006) Mitigation and controls of HABs. In: Graneli E, Turner J (eds) Ecology of harmful algae. Springer, Berlin, pp 327–338CrossRefGoogle Scholar
  25. Kim Y, Myung SH, Kim HS, Jung W, Cho SH, Jwa MS, Kim PY, 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
  26. 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
  27. Knauer J, Britz PJ, Hecht T (1993) The effect of seven binding agents on 24 hour water stability of an artificial weaning diet for the South African abalone, Haliotis midae (Haliotidae, Gastropoda). Aquaculture 115:327–334Google Scholar
  28. KOSIS (2018) Korean statistical information service. DaejeonGoogle Scholar
  29. 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
  30. 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
  31. Lee KW, Kim HS, Choi DG, Jang BI, Yun A, Cho SH, Min B, Kim K, Han H (2017) Effects of substitution of fish meal (FM) and macroalgae (MA) with soybean meal and rice bran in a commercial juvenile abalone (Haliotis duscus hannai) diet on growth performance. Turk J Fish Aquat Sci 17:519–526Google Scholar
  32. Lee KW, Kim HS, Kim PY, Jeong HS, Kim J, Yun A, Cho SH (2018) Substitution effect of white radish (Raphanus sativus L.)’ by-product and tunic of sea squirt (Halocynthia rorentzi, von Drasche) for Undaria pinnatifida in feed of abalone (Haliotis discus, Reeve 1846). Fish Aquat Sci 21:1–8CrossRefGoogle Scholar
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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 430:9–16Google Scholar
  39. O’Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Mar Drugs 8:2038–2064CrossRefPubMedPubMedCentralGoogle Scholar
  40. Park C, Kim SY (2013) Abalone aquaculture in Korea. J Shellfish Res 32:17–19CrossRefGoogle Scholar
  41. Qi Z, Liu H, Li B, Mao Y, Jiang Z, Zhang J, Fang J (2010) Suitability of two seaweeds, Gracilaria lemaneiformis and Sargassum pallidum, as feed for the abalone Haliotis discus hannai Ino. Aquaculture 300:189–193CrossRefGoogle Scholar
  42. Robertson-Andersson DV, Maneveldt GW, Naidoo K (2011) Effects of wild and farm-grown macroalgae on the growth of juvenile South African abalone Haliotis midae Linnaeus. Afr J Aquat Sci 36:331–337CrossRefGoogle Scholar
  43. Sales J, Britz PJ (2001) Research on abalone (Haliotis midae L.) cultivation in South Africa. Aquac Res 32:863–874CrossRefGoogle Scholar
  44. Sales J, Britz PJ (2002) Influence of ingredients particle size and inclusion level of pre-gelatinised maize starch on apparent digestibility coefficients of diets in South African abalone (Haliotis midae L.). Aquaculture 212:299–309CrossRefGoogle Scholar
  45. Sales J, Janssens GP (2004) Use of feed ingredients in artificial diets for abalone: a brief update. Nutr Abstr Rev B:13N–21NGoogle Scholar
  46. 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
  47. Stone DAJ, Harris JO, Wang H, Mercer GJ, Schaefer EN, Bansemer MS (2013) Dietary protein level and water temperature interactions for greenlip abalone Haliotis laevigata. J Shellfish Res 32:119–130CrossRefGoogle Scholar
  48. Su L, Shan T, Pang S, Li J (2018) Analyses of the genetic structure of Sargassum horneri in the Yellow Sea: implications of the temporal and spatial relations among floating and benthic populations. J Appl Phycol 30:1417–1424CrossRefGoogle Scholar
  49. Uki N, Kemuyama A, Watanabe T (1986) Optimum protein level in diets for abalone. Bull Jpn Soc Sci Fish 52:1005–1012CrossRefGoogle Scholar
  50. 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
  51. Wells RMG, Baldwin J (1995) A comparison of metabolic stress during air exposure in two species of New Zealand abalone, Haliotis iris and Haliotis australis: implications for the handling and shipping of live animals. Aquaculture 134:361–370CrossRefGoogle Scholar
  52. 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

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Convergence Study on the Ocean Science and TechnologyKorea Maritime and Ocean UniversityBusanSouth Korea
  2. 2.Division of Marine BioscienceKorea Maritime and Ocean UniversityBusanSouth Korea
  3. 3.East Sea Fisheries Research InstituteNational Institute of Fisheries ScienceBusanSouth Korea
  4. 4.Jeju Research InstituteJejuSouth Korea

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