Advertisement

Nutritional value and production performance of the rotifer Brachionus plicatilis Müller, 1786 cultured with different feeds at commercial scale

  • Kamil Mert EryalçınEmail author
Article
  • 39 Downloads

Abstract

The rotifer Brachionus plicatilis is the first live feed in larviculture of marine fish species. Rotifer diets differ in their biochemical composition, physical properties, and production technology while feeding protocols largely vary among facilities. The objective of the present study was to determine the effects of two different forms of Nannochloropsis oculata and commonly used commercial diets on growth performance and biochemical composition of rotifers produced under commercial conditions. Rotifers were fed one of five different types of feed: Algome® (dried Schizochytrium sp.), Protein Plus® (PP), Inactive Baker’s Yeast® (INBY), spray-dried Nannochloropsis oculata (SDN), or freshly cultured Nannochloropsis oculata (FN). Rotifers fed SDN diet resulted in significantly higher rotifer biomass during 16 days of semi-continuous culture, with an increasing biomass trend that lasted 11 days, high egg production, and egg-carrying female numbers, whereas rotifers fed PP showed highest ∑n-3, arachidonic acid, eicosapentaenoic acid, and docosahexaenoic acid contents. Amino acid profiles of rotifers were enhanced by utilization of both INBY and SDN diets. Overall, the results indicated that SDN is optimal for long-term biomass production of rotifers. However, their nutritional profile needs to be enriched by feeding PP (EFA source) and INBY (EAA source) once desired biomass production is obtained.

Keywords

Amino acids Essential fatty acids Growth Nannochloropsis oculata Rotifer Spray-dried 

Abbreviations

HUFA

Highly unsaturated fatty acids

PP

Protein Plus®

INBY

Inactive Baker’s Yeast®

SDN

Spray-dried Nannochloropsis oculata

FN

Fresh Nannochloropsis oculata

ARA

Arachidonic acid

EPA

Eicosapentaenoic acid

DHA

Docosahexaenoic acid

LA

Linoleic acid

LNA

Linolenic acid

Notes

Acknowledgements

Nihan Arığ and Kadir Vardı are acknowledged for helping during experiments. The author also thank Prof. Marisol Izquierdo for very helpful comments

Funding

This work was supported by Tubitak-Teydeb 1507 Kobi-Arge Project No. 7170299 (The Scientific and Technological Research Council of Turkey) and Istanbul University, Research Foundation Project No. 29086.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

References

  1. Association of Official Analytical Chemists (AOAC) (2010) Official methods of analysis, 18th edn., revision 3 edition. AOAC, Washington, District of Colombia, USAGoogle Scholar
  2. Borowitzka MA (2013) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  3. Bransden MP, Butterfield GM, Walden J, McEvoy LA, Bell JG (2005) Tank colour and dietary arachidonic acid affects pigmentation, eicosanoid production and tissue fatty acid profile of larval Atlantic cod (Gadus morhua). Aquaculture 250:328–340CrossRefGoogle Scholar
  4. Cavonius LR, Albers E, Undeland I (2015) pH-shift processing of Nannochloropsis oculata microalgal biomass to obtain a protein-enriched food or feed ingredient. Algal Res 11:95–102CrossRefGoogle Scholar
  5. Chen HM, Muramoto K, Yamauchi F, Nokihara K (1996) Antioxidant activity of designed peptides based on the antioxidative peptide isolated from digests of a soybean protein. J Agric Food Chem 44:2619–2623CrossRefGoogle Scholar
  6. Cheng SH, Kâ S, Kumar R, Kuo CS, Hwang JS (2011) Effects of salinity, food level, and the presence of microcrustacean zooplankters on the population dynamics of rotifer Brachionus rotundiformis. Hydrobiologia 666:289–299CrossRefGoogle Scholar
  7. Cho SH, JI SC, Hur SB, Bae J, Park IS, Song YC (2007) Optimum temperature and salinity conditions for growth of green algae Chlorella ellipsoidea and Nannochloris oculata. Fish Sci 73:1050–1056CrossRefGoogle Scholar
  8. Christie WW (1982) Lipid analysis, 2nd edn. Permagon Press, OxfordGoogle Scholar
  9. Conceição LEC, Grasdalen H, Rønnestad I (2003) Amino acid requirements of fish larvae and post-larvae: new tools and recent findings. Aquaculture 227:221–232CrossRefGoogle Scholar
  10. Conceição LE, Yúfera M, Makridis P, Morais S, Dinis MT (2010) Live feeds for early stages of fish rearing. Aquac Res 41:613–640CrossRefGoogle Scholar
  11. Dhert P, Rombaut G, Suantika G, Sorgeloos P (2001) Advancement of rotifer culture and manipulation techniques in Europe. Aquaculture 200:129–146CrossRefGoogle Scholar
  12. Dhert P, King N, O'brien E (2014) Stand-alone live food diets, an alternative to culture and enrichment diets for rotifers. Aquaculture 431:59–64CrossRefGoogle Scholar
  13. Dhont J, Dierckens K, Støttrup J, Van Stappen G, Wille M, Sorgeloos P (2013) Rotifers, Artemia and copepods as live feeds for fish larvae in aquaculture. Advances in Aquaculture Hatchery Technology 157–202Google Scholar
  14. Eryalçın KM, Roo J, Saleh R, Atalah E, Benítez T, Betancor M, Hernandez Cruz M, Izquierdo M (2013) Fish oil replacement by different microalgal products in microdiets for early weaning of gilthead sea bream (Sparus aurata, L.). Aquac Res 44:819–828CrossRefGoogle Scholar
  15. Eryalçın KM, Ganuza E, Atalah E, Cruz MCH (2015) Nannochloropsis gaditana and Crypthecodinium cohnii, two microalgae as alternative sources of essential fatty acids in early weaning for gilthead seabream. Hidrobiológica 25:193–203Google Scholar
  16. Ferreira M, Coutinho P, Seixas P, Fábregas J, Otero A (2009) Enriching rotifers with “premium” microalgae. Nannochloropsis gaditana. Mar Biotechnol 11:585–595CrossRefGoogle Scholar
  17. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  18. Ganuza E, Anderson AJ, Ratledge C (2008) High-cell-density cultivation of Schizochytrium sp. in an ammonium/pH-auxostat fed-batch system. Biotechnol Lett 30:1559–1564CrossRefGoogle Scholar
  19. Garcia AS, Parrish CC, Brown JA (2008) A comparison among differently enriched rotifers (Brachionus plicatilis) and their effect on Atlantic cod (Gadus morhua) larvae early growth, survival and lipid composition. Aquac Nutr 14:14–30CrossRefGoogle Scholar
  20. Grima EM, Belarbi EH, Fernández FA, Medina AR, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20(7-8):491–515Google Scholar
  21. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefGoogle Scholar
  22. Haas S, Bauer JL, Adakli A, Meyer S, Lippemeier S, Schwarz K, Schulz C (2016) Marine microalgae Pavlova viridis and Nannochloropsis sp. as n-3 PUFA source in diets for juvenile European sea bass (Dicentrarchus labrax L.). J Appl Phycol 28:1011–1021CrossRefGoogle Scholar
  23. Haché R, Plante S (2011) The relationship between enrichment, fatty acid profiles and bacterial load in cultured rotifers (Brachionus plicatilis L-strain) and Artemia (Artemia salina strain Franciscana). Aquaculture 311(1–4):201–208CrossRefGoogle Scholar
  24. Hamre K (2016) Nutrient profiles of rotifers (Brachionus sp.) and rotifer diets from four different marine fish hatcheries. Aquaculture 450:136–142CrossRefGoogle Scholar
  25. Hamre K, Srivastava A, Rønnestad I, Mangor Jensen A, Stoss J (2008) Several micronutrients in the rotifer Brachionus sp. may not fulfil the nutritional requirements of marine fish larvae. Aquac Nutr 14:51–60CrossRefGoogle Scholar
  26. Hamre K, Yúfera M, Rønnestad I, Boglione C, Conceição LE, Izquierdo M (2013) Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Rev Aquac 5:26–58CrossRefGoogle Scholar
  27. Harel M, Koven W, Lein I, Bar Y, Behrens P, Stubblefield J, Zohar Y, Place AR (2002) Advanced DHA, EPA and ArA enrichment materials for marine aquaculture using single cell heterotrophs. Aquaculture 213:347–362CrossRefGoogle Scholar
  28. Hawkyard M, Stuart K, Langdon C, Drawbridge M (2016) The enrichment of rotifers (Brachionus plicatilis) and Artemia franciscana with taurine liposomes and their subsequent effects on the larval development of California yellowtail (Seriola lalandi). Aquac Nutr 22:911–922CrossRefGoogle Scholar
  29. Hemaiswarya S, Raja R, Kumar RR, Ganesan V, Anbazhagan C (2011) Microalgae: a sustainable feed source for aquaculture. World J Microbiol Biotechnol 27:1737–1746CrossRefGoogle Scholar
  30. Izquierdo MS, Koven W (2011) Lipids. Larval fish nutrition. Wiley-Blackwell, John Wiley and Sons Publisher, OxfordGoogle Scholar
  31. Izquierdo MS, Watanabe T, Takeuchi T, Arakawa T, Kitajima C (1990) Optimal EFA levels in Artemia to meet the EFA requirements of red seabream (Pagrus major). In: Takeda M, Watanabe T (eds) The current status of fish nutrition in aquaculture. Tokyo University Fisheries, Tokyo, pp 221–232Google Scholar
  32. Ju ZY, Deng DF, Dominy W (2012) A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fishmeal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquaculture 354:50–55CrossRefGoogle Scholar
  33. Knuckey RM, Semmens GL, Mayer RJ, Rimmer MA (2005) Development of an optimal microalgal diet for the culture of the calanoid copepod Acartia sinjiensis: effect of algal species and feed concentration on copepod development. Aquaculture 249:339–351CrossRefGoogle Scholar
  34. Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37(1):43–53Google Scholar
  35. Lubzens E, Gibson O, Zmora O, Sukenik A (1995) Potentialadvantages of frozen algae (Nannochloropsis sp.) for rotifer (Brachionus plicatilis) culture. Aquacul 133:295–309Google Scholar
  36. Ma Z, Qin JG (2014) Replacement of fresh algae with commercial formulas to enrich rotifers in larval rearing of yellowtail kingfish Seriola lalandi (Valenciennes, 1833). Aquac Res 45:949–960CrossRefGoogle Scholar
  37. Maisashvili A, Bryant H, Richardson J, Anderson D, Wickersham T, Drewery M (2015) The values of whole algae and lipid extracted algae meal for aquaculture. Algal Res 9:133–142CrossRefGoogle Scholar
  38. Matsunari H, Hashimoto H, Oda K, Masuda Y, Imaizumi H, Teruya K, Furuita H, Yamamato T, Yamamato T, Hamada K, Mushiake K (2012) Effect of different algae used for enrichment of rotifers on growth, survival, and swim bladder inflation of larval amberjack Seriola dumerili. Aquac Int 20:981–992CrossRefGoogle Scholar
  39. Nanton DA, Castell JD (1999) The effects of temperature and dietary fatty acids on the fatty acid composition of harpacticoid copepods, for use as a live food for marine fish larvae. Aquaculture 175:167–181CrossRefGoogle Scholar
  40. Norsker NH, Barbosa MJ, Vermuë MH, Wijffels RH (2011) Microalgal production—a close look at the economics. Biotechnol Adv 29:24–27CrossRefGoogle Scholar
  41. Park HG, Puvanendran V, Kellett A, Parrish CC, Brown JA (2006) Effect of enriched rotifers on growth, survival, and composition of larval Atlantic cod (Gadus morhua). ICES J Mar Sci 63(2):285–295CrossRefGoogle Scholar
  42. Patil V, Källqvist T, Olsen E, Vogt G, Gislerød HR (2007) Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquac Int 15:1–9CrossRefGoogle Scholar
  43. Patterson D, Gatlin DM (2013) Evaluation of whole and lipid-extracted algae meals in the diets of juvenile red drum (Sciaenops ocellatus). Aquaculture 416:92–98CrossRefGoogle Scholar
  44. Pedro C, Fernandez-Diaz JC (2001) Pilot evaluation of freeze-dried microalgae in the mass rearing of gilthead seabream (Sparus aurata) larvae. Aquaculture 193:257–269CrossRefGoogle Scholar
  45. Qie G, Reitan KI, Evjemo JO, Støttrup J, Olsen Y (2011) Live feeds. Larval Fish Nutrition 307–334Google Scholar
  46. Rainuzzo JR, Reitan KI, Olsen Y (1997) The significance of lipids at early stages of marine fish: a review. Aquaculture 155:103–115CrossRefGoogle Scholar
  47. Rasdi NW, Qin JG (2016) Improvement of copepod nutritional quality as live food for aquaculture: a review. Aquac Res 47:1–20CrossRefGoogle Scholar
  48. Reitan KI, Rainuzzo JR, Øie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–221CrossRefGoogle Scholar
  49. Ringø E, Olsen RE, Jensen I, Romero J, Lauzon HL (2014) Application of vaccines and dietary supplements in aquaculture: possibilities and challenges. Rev Fish Biol Fish 24:1005–1032CrossRefGoogle Scholar
  50. Rocha RJ, Ribeiro L, Costa R, Dinis MT (2008) Does the presence of microalgae influence fish larvae prey capture? Aquac Res 39:362–369CrossRefGoogle Scholar
  51. Rocha GS, Katan T, Parrish CC, Gamperl AK (2017) Effects of wild zooplankton versus enriched rotifers and Artemia on the biochemical composition of Atlantic cod (Gadus morhua) larvae. Aquaculture 479:100–113CrossRefGoogle Scholar
  52. Rothhaupt KO (1995) Algal nutrient limitation affects rotifer growth rate but not ingestion rate. Limnol Oceanogr 40:1201–1208CrossRefGoogle Scholar
  53. Ryckebosch E, Muylaert K, Eeckhout M, Ruyssen T, Foubert I (2011) Influence of drying and storage on lipid and carotenoid stability of the microalga Phaeodactylum tricornutum. J Agric Food Chem 59:11063–11069CrossRefGoogle Scholar
  54. Sales R, Mélo RCS, de Moraes RM, da Silva RCS, Cavalli RO, Navarro DMDAF, Souza Santos LP (2016) Production and use of a flocculated paste of Nannochloropsis oculata for rearing newborn seahorse Hippocampus reidi. Algal Res 17:142–149CrossRefGoogle Scholar
  55. Salvesen I, Reitan KI, Skjermo J, Qie G (2000) Microbial environments in marine larviculture: impacts of algal growth rates on the bacterial load in six microalgae. Aquac Int 8:275–287CrossRefGoogle Scholar
  56. Schwarz MH, Craig SR, Delbos BC, McLean E (2008) Efficacy of concentrated algal paste during greenwater phase of cobia larviculture. J Appl Aquac 20:285–294CrossRefGoogle Scholar
  57. Seychelles LH, Audet C, Tremblay R, Fournier R, Pernet F (2009) Essential fatty acid enrichment of cultured rotifers (Brachionus plicatilis, Müller) using frozen-concentrated microalgae. Aquac Nutr 15(4):431–439CrossRefGoogle Scholar
  58. Sharifah EN, Eguchi M (2011) The phytoplankton Nannochloropsis oculata enhances the ability of Roseobacter clade bacteria to inhibit the growth of fish pathogen Vibrio anguillarum. PLoS One 6(10):e26756CrossRefGoogle Scholar
  59. Shields RJ, Lupatsch I (2012) Algae for aquaculture and animal feeds. J Anim Sci 21:23–37Google Scholar
  60. Skiftesvik AB, Browman HI, St-Pierre JF (2003) Life in green water: the effect of microalgae on the behaviour of Atlantic cod (Gadus morhua) larvae. In The Big Fish Bang. Proceedings of the 26th Annual Larval Fish Conference. Institute of Marine Research, Bergen, Norway (pp 97–103)Google Scholar
  61. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96CrossRefGoogle Scholar
  62. Srivastava A, Hamre K, Stoss J, Chakrabarti R, Tonheim SK (2006) Protein content and amino acid composition of the live feed rotifer Brachionus plicatilis: with emphasis on the water soluble fraction. Aquaculture 254:534–543CrossRefGoogle Scholar
  63. Taniguchi A, Sharifah NE, Eguchi M (2011) Possible role of microalga Nannochloropsis in controlling Vibrio species in fish larva rearing water. Aquacult Sci 59:451–458Google Scholar
  64. Tendencia EA, Bosma RH, Verdegem MC, Verreth JA (2015) The potential effect of greenwater technology on water quality in the pond culture of Penaeus monodon Fabricius. Aquac Res 46:1–13CrossRefGoogle Scholar
  65. Tibaldi E, Zittelli GC, Parisi G, Bruno M, Giorgi G, Tulli F, Venturini S, Tredici MR, Poli BM (2015) Growth performance and quality traits of European sea bass (D. labrax) fed diets including increasing levels of freeze-dried Isochrysis sp.(T-ISO) biomass as a source of protein and n-3 long chain PUFA in partial substitution of fish derivatives. Aquaculture 440:60–68CrossRefGoogle Scholar
  66. Van der Meeren T, Mangor-Jensen A, Pickova J (2007) The effect of green water and light intensity on survival, growth and lipid composition in Atlantic cod (Gadus morhua) during intensive larval rearing. Aquaculture 265:206–217CrossRefGoogle Scholar
  67. Vigani M, Parisi C, Rodríguez-Cerezo E, Barbosa MJ, Sijtsma L, Ploeg M, Enzing C (2015) Food and feed products from micro-algae: market opportunities and challenges for the EU. Trends Food Sci Technol 42:81–92CrossRefGoogle Scholar
  68. Walker AB, Berlinsky DL (2011) Effects of partial replacement of fish meal protein by microalgae on growth, feed intake, and body composition of Atlantic cod. N Am J Aquac 73:76–83Google Scholar
  69. Yin XW, Min WW, Lin HJ, Chen W (2013) Population dynamics, protein content, and lipid composition of Brachionus plicatilis fed artificial macroalgal detritus and Nannochloropsis sp. diets. Aquaculture 380:62–69CrossRefGoogle Scholar
  70. Yoshimatsu T, Hossain MA (2014) Recent advances in the high-density rotifer culture in Japan. Aquac Int 22:1587–1603CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Faculty of Aquatic Sciences, Aquaculture Department, Fish Nutrition & Phytoplankton-Zooplankton Culture LaboratoryIstanbul UniversityIstanbulTurkey

Personalised recommendations