Advertisement

Enriched Ulva pertusa as partial replacement of the combined fish and soybean meals in juvenile abalone Haliotis asinina (Linnaeus) diet

  • Rena Santizo-TaanEmail author
  • Myrna Bautista-Teruel
  • Jean Rose H. Maquirang
Article

Abstract

The potential of enriched Ulva pertusa meal as feed ingredient in abalone juveniles, Haliotis asinina was evaluated. Four isonitrogenous and isolipidic diets were formulated which contain 27% protein and 5% lipid. Enriched U. pertusa meal replaced 0% (control), 10%, 20%, and 30% of protein from fish and soybean meals in the formulated diets. Thirty randomly selected abalone juveniles with average weight and shell length of 0.45 g ± 0.01 and 12.71 mm ± 0.01, respectively, were placed in each of the twelve 60-L oval fiberglass tanks equipped with a flow-through seawater system. Abalone were given diets at 3–5% body weight daily for 120 days in three replicate samples. Results showed no significant differences (p > 0.05) in percent weight gain, shell length, specific growth rate, feed conversion ratio, and protein efficiency ratio even up to 30% replacement level. Apparent dry matter digestibility of U. pertusa meal in abalone diet was 92%. Crude protein content of the abalone fed diets 1 (10% enriched U. pertusa meal) and 3 (30% enriched U. pertusa meal) was significantly (p < 0.05) higher than those fed on basal diet. Enriched U. pertusa meal can partially replace fish and soybean meals as protein source in formulated diets for abalone, Haliotis asinina juveniles.

Keywords

Abalone Green algae Haliotis asinina Nitrogen enrichment Ulva pertusa 

Notes

Acknowledgments

The author would like to acknowledge the chemists of the Laboratory Facilities for Advanced Aquaculture Technology (LFAAT) for doing the proximate analysis, Mr. Richard Tantiado for his assistance, and Juan Miguel Taan for data analysis.

Funding information

The author would like to acknowledge the Aquaculture Department, Southeast Asian Fisheries Development Center (study code: FD-01-M2015T) for providing funds for this study.

References

  1. Ansary MWR, Jeong HS, Lee KW, Kim PY, Kim J, Yun A-Y, Cho SH, Kim T-I (2019) 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
  2. AOAC (2000) Official methods of analysis, 17th edn. Association of Official Analytical Chemists, ArlingtonGoogle Scholar
  3. Arndt RE, Hardy RW, Sugiura SH, Dong FM (1999) Effects of heat treatment and substitution level on palatability and nutritional value of soy defatted flour in feeds for Coho Salmon, Oncorhynchus kisutch. Aquaculture 180:129–145CrossRefGoogle Scholar
  4. Azaza MS, Mensi F, Ksouri J, Dhraief MN, Brini B, Abdelmouleh A, Kraiem MM (2008) Growth of Nile tilapia (Oreochromis niloticus L.) fed with diets containing graded levels of green algae Ulva meal (Ulva rigida) reared in geothermal waters of southern Tunisia. J Appl Ichthyol 24:202–207CrossRefGoogle Scholar
  5. Bansemer MS, Qin JQ, Harris JO, Howarth GS, Stone DAJ (2014) Nutritional requirements and use of macroalgae as ingredients in abalone feed. Rev Aquacult 5:1–15Google Scholar
  6. Bansemer MS, Qin JG, Harris JO, Duong DN, Hoang TH, Howarth GS, Stone DAJ (2016) Growth and feed utilisation of greenlip abalone (Haliotis laevigata) fed nutrient enriched macroalgae. Aquaculture 452:62–68CrossRefGoogle Scholar
  7. Bautista-Teruel MN, Millamena OM (1999) Diet development and evaluation for juvenile abalone, Haliotis asinina: protein/energy levels. Aquaculture 178:117–126CrossRefGoogle Scholar
  8. Bautista-Teruel MN, Maquirang JRH, Dela Pena MR, Balinas VT (2016) Test of refined formulated feed for the grow-out culture of tropical abalone Haliotis asinina (Linnaeus 1758) in concrete land-based tanks. J Shellfish Res 35:633–639CrossRefGoogle Scholar
  9. 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
  10. Brett JR, Grooves TD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish Physiology, vol 8. Academic Press, London, pp 280–344Google Scholar
  11. Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol 73B:25–41Google Scholar
  12. Cook PA (2014) The Worldwide Abalone Industry. Modern Economy 5:1181–1186CrossRefGoogle Scholar
  13. Cook PA, Gordon GH (2010) World abalone supply, markets, and pricing. J Shellfish Res 29:569–571CrossRefGoogle 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 448:306–314Google Scholar
  15. Davies SJ, Brown MT, Camilleri M (1997) Preliminary assessment of the seaweed Porphyra purpurea in artificial diets for thick-lipped grey mullet ( Chelon labrows). Aquaculture 152:249–258CrossRefGoogle Scholar
  16. El-Saidy DMSD, Gaber MMA (2002) Complete replacement of fish meal by soybean meal with dietary L-lysine supplementation for Nile tilapia Oreochromis niloticus (L.) fingerlings. J World Aquacult Soc 33:297–306CrossRefGoogle Scholar
  17. Erasmus JH, Cook PA, Coyne VE (1997) The role of bacteria in the digestion of seaweed by the abalone Haliotis midae. Aquaculture 155:377–386CrossRefGoogle Scholar
  18. FitzGerald A (2008) Abalone feed requirements. Southwest Abalone Grower Association. pp 1-34. https://www.seafish.org/media/Publications/B40_AbaloneFeedRequirements.pdf
  19. Fleming AE (1995) Growth, intake, feed conversion efficiency and chemosensory preference of the Australian abalone, Haliotis rubra. Aquaculture 132:297–311CrossRefGoogle Scholar
  20. Fleming AE, Barneveld RJV, Hone PW (1996) The development of artificial diets for abalone: a review and future directions. Aquaculture 140:5–53CrossRefGoogle Scholar
  21. Fleurence J (1999) Seaweed proteins: biochemical nutritional aspects and potential uses. Trends Food Sci Techol 10:25–28CrossRefGoogle Scholar
  22. Francis G, Harinder M, Klaus B (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  23. Gatlin III DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, J Souza E, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38:551–579CrossRefGoogle Scholar
  24. Guzman JM, Viana MT (1998) Growth of abalone Haliotis fulgens fed diets with and without fish meal, compared to a commercial diet. Aquaculture 165:321–331CrossRefGoogle Scholar
  25. Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res 41:770–776CrossRefGoogle Scholar
  26. Harris JO, Burke CM, Maguire GB (1998) Characterization of the digestive tract of greenlip abalone, Haliotis laevigata Donovan. I. Morphology and histology. J Shellfish Res 17:979–988Google Scholar
  27. Hashim R, Saat MAM (1992) The utilization of seaweed meals as binding agents in pelleted feeds for snakehead (Channa striatus) fry and their effects on growth. Aquaculture 108:299–308CrossRefGoogle Scholar
  28. Hernández I, Martínez-Aragón JF, Tovar A, Pérez-Lloréns JL, Vergara JJ (2002) Biofiltering efficiency in removal of dissolved nutrients by three species of estuarine macroalgae cultivated with sea bass (Dicentrarchus labrax) waste waters 2. Ammonium. J Appl Phycol 14:375–384CrossRefGoogle Scholar
  29. Jung W-G, Kim HS, Lee KW, Kim YE, Choi DK, Jang B-I, Cho SH, Choi CY, Kim B-H, Joo Y-I (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
  30. Kemp JOG, Britz PJ, Aguero PHT (2015) The effect of macroalgal, formulated and combination diets on growth, survival and feed utilisation in the red abalone Haliotis rufescens. Aquaculture 306–314CrossRefGoogle Scholar
  31. Kikuchi K (1999) Use of defatted soybean meal as a substitute for fish meal in diets of Japanese flounder (Paralichthys olivaceus). Aquaculture 179:3–11CrossRefGoogle Scholar
  32. Krogdahl A, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9:361–371CrossRefGoogle Scholar
  33. Largo DB, Sembrano J, Hiraoka M, Ohno M (2004) Taxonomic and ecological profile of “green tide” species of Ulva (Ulvales, Chlorophyta) in central Philippines. Hydrobiologia 512:247–253CrossRefGoogle Scholar
  34. Mai K, Mercer JP, Donlon J (1995) 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. Marinho-Soriano E, Camara MR, de Cabral TM, do Carneiro MAA (2007) Preliminary evaluation of the seaweed Gracilaria cervicornis (Rhodophyta) as a partial substitute for the industrial feeds used in shrimp (Litopenaeus vannamei) farming. Aquacult Res 38:182–187Google Scholar
  36. Maynard LA, Loosli JK (1969) Animal Nutrition, 6th edn. McGraw-Hill, New York, USAGoogle Scholar
  37. Miles R, Chapman F (2006) The benefits of fish meal in aquaculture diets. Series of the Department of Fisheries and Aquatic Sciences, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida (FA122). pp 1-6Google Scholar
  38. Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96CrossRefGoogle Scholar
  39. Montaño-Vargas J, Shimada A, Vasquez C, Viana MT (2002) Methods of measuring feed digestibility in the green abalone (Haliotis fulgens). Aquaculture 213:339–346CrossRefGoogle Scholar
  40. Mustafa MG, Nakagawa H (1995) A review: dietary benefits of algae as an additive in fish feed. Bamidgeh 47:155–162Google Scholar
  41. Myung SH, Jung W-G, Kim HS, Kim YE, Cho SH, Jwa MS, Kim PY, Kim MK, Park M-W, Kim B-H (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). Aquacult Res 47:341–348CrossRefGoogle Scholar
  42. 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 land-based aquaculture system. J Appl Phycol 18:437–443CrossRefGoogle Scholar
  43. Nakagawa H, Kasahara S, Sugiyama T (1987) Effect of Ulva meal supplementation on lipid metabolism of black sea bream, Acanthopagrus schlegeli (Bleeker). Aquaculture 62:109–121CrossRefGoogle Scholar
  44. 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
  45. O’Sullivan L, Murphy L, McLoughlin B, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Mar Drugs 8:2038–2064PubMedPubMedCentralCrossRefGoogle Scholar
  46. Pereira R, Valente LMP, Sousa-Pinto I, Rema P (2012) Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Res 1:77–82CrossRefGoogle Scholar
  47. Riche M, Williams TN (2011) Fish meal replacement with solvent-extracted soybean meal or soy protein isolate in a practical diet formulation for Florida pompano (Trachinotus carolinus, L.) reared in low salinity. Aquacult Nutr 17:368–379CrossRefGoogle Scholar
  48. Shamshak GL, Anderson JL (2010) Protein production advantages in the face of increasing feed cost: identifying opportunities within the aquaculture industry. Bull Fish Res Agen 31:55–62Google Scholar
  49. 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
  50. Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F, Rema P (2015) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. J Appl Phycol 27:1671–1681CrossRefGoogle Scholar
  51. Soler-Vila A, Coughlan S, Guiry MD, Kraan S (2009) The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency, and carcass composition. J Appl Phycol 21:617–624CrossRefGoogle Scholar
  52. Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158CrossRefGoogle Scholar
  53. Thongrod S, Tamtin M, Chairat C, Boonyarapatlin M (2003) Lipid to carbohydrate ratio in donkey’s ear abalone (Haliotis asinina, Linne) diets. Aquaculture 225:165–174CrossRefGoogle Scholar
  54. Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Pinto IS (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252:85–91CrossRefGoogle Scholar
  55. Viana MT, Lopez LM, Salas A (1993) Diet development for juvenile abalone Haliotis fulgens evaluation of two artificial diets and macroalgae. Aquaculture 117:149–156CrossRefGoogle Scholar
  56. Viera MP, de Vicose GC, Gómez-Pinchetti JL, Bilbao A, Fernandez-Palacios H, Izquierdo MS (2011) Comparative performances of juvenile abalone (Haliotis tuberculata coccinea Reeve) fed enriched vs non-enriched macroalgae: effect on growth and body composition. Aquaculture 319:423–429CrossRefGoogle Scholar
  57. Waseff EA, El-Masry MH, Mikhail FR (2001) Growth enhancement and muscle structure of striped mullet, (Mugil cephalus L.) fingerlings by feeding algal meal-based diet. Aquacult Res 32:315–322CrossRefGoogle Scholar
  58. Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68:242–252CrossRefGoogle Scholar
  59. Xia S, Yang H, Li Y, Liu S, Zhang L (2012) Effects of different seaweed diets on growth, digestibility, and ammonia-nitrogen production of the sea cucumber Apostichopus japonicus (Selenka). Aquaculture 338-341:304–308CrossRefGoogle Scholar
  60. Zhang Y, Ji W, Wu Y, Han H, Qin J, Wang Y (2016) Replacement of dietary fish meal by soybean meal supplemented with crystalline methionine for Japanese seabass (Lateolabrax japonicus). Aquacult Res 47:243–252CrossRefGoogle Scholar
  61. Zhu D, Wen X, Xuan X, Li S, Li Y (2016) The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. J Appl Phycol 28:703–711CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Aquaculture DepartmentSoutheast Asian Fisheries Development CenterIloiloPhilippines

Personalised recommendations