Skip to main content
Log in

Can the European abalone Haliotis tuberculata survive on an invasive algae? A comparison of the nutritional value of the introduced Grateloupia turuturu and the native Palmaria palmata, for the commercial European abalone industry

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The suitability of two red algae species, the introduced Grateloupia turuturu and the native Palmaria palmata, as feed for the culture of the European abalone Haliotis tuberculata, was compared over a 5-month period. Three experimental diets were tested: (1) P. palmata, (2) G. turuturu, and (3) a mixed diet of P. palmata and G. turuturu (1:1). Biochemical composition (proteins, carbohydrates, lipids, ashes) of algae was measured. No mortality was observed during the time of the experiment in any of the treatments. Growth in length and weight was higher for abalone fed with P. palmata and the mixed diet. Abalone exhibited a preference for P. palmata and showed the highest weight gain with this macroalgae (107.8 ± 7.2 %). Grateloupia turuturu disintegrated faster in abalone rearing conditions and was not suitable for significant growth of H. tuberculata in a monospecific diet. However, when it is provided in a mixed diet, abalone seem to show a higher lipid content than when fed a P. palmata monospecific diet. The invasive G. turuturu could be an interesting food supplement for European abalone.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alcantara L, Noro T (2006) Growth of the abalone Haliotis diversicolor (reeve) fed with macroalgae in floating net cage and plastic tank. Aquac Res 37:708–717

    Article  Google Scholar 

  • Bansemer MS, Qin JG, Harris JO, Howarth GS, Stone DA (2014) Nutritional requirements and use of macroalgae as ingredients in abalone feed. Rev Aquac. doi:10.1111/raq.12085

    Google Scholar 

  • Basuyaux (1997) Study and modelisation of the physico-chemical parameters influencing the growth of the ormer (Haliotis tuberculata) reared in a semi-closed system. Thesis, Université de Caen.

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cook PA (2014) The worldwide abalone industry. Mod Econ 5:1181

    Article  Google Scholar 

  • D’Archino R, Nelson WA, Zuccarello GC (2007) Invasive marine red alga introduced to New Zealand waters: first record of Grateloupia turuturu (Halymeniaceae, Rhodophyta). N Z J Mar Freshw Res 41:35–42

    Article  Google Scholar 

  • Demetropoulos C, Langdon CJ (2004a) Pacific dulse (Palmaria mollis) as a food and biofilter in recirculated, land-based abalone culture systems. Aquac Eng 32:57–75

    Article  Google Scholar 

  • Demetropoulos CL, Langdon CJ (2004b) Effects of nutrient enrichment and biochemical composition of diets of Palmaria mollis on growth and condition of Japanese abalone, Haliotis discus hannai and red abalone, Haliotis rufescens. J Exp Mar Biol Ecol 308:185–206

    Article  CAS  Google Scholar 

  • Denis C, Morançais M, Li M, Deniaud E, Gaudin P, Wielgosz-Colin G, Barnathan G, Fleurence J (2010) Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chem 119:913–917

    Article  CAS  Google Scholar 

  • Dunstan GA, Baillie HJ, Barrett SM, Volkman JK (1996) Effect of diet on the lipid composition of wild and cultured abalone. Aquaculture 140:115–127

    Article  CAS  Google Scholar 

  • FAO (2014) Global aquaculture production 1950−2012. http://www.fao.org/fishery/statistics/global-aquaculture-production/query/en, accessed on 26 July 2014.

  • Fleming AE, Hone PW (1996) Abalone aquaculture. Aquaculture 140:1–4

    Article  Google Scholar 

  • Fleming AE, Van Barneveld RJ, Hone PW (1996) The development of artificial diets for abalone: a review and future directions. Aquaculture 140:5–53

    Article  CAS  Google Scholar 

  • Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28

    Article  CAS  Google Scholar 

  • Galland-Irmouli AV, Fleurence J, Lamghari R, Luçon M, Rouxel C, Barbaroux O, Bronowicki JP, Villaume C, Guéant JL (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J Nutr Biochem 10:353–359

    Article  CAS  PubMed  Google Scholar 

  • García-Bueno N, Decottignies P, Turpin V, Dumay J, Paillard C, Stiger-Pouvreau V, Kervarec N, Pouchus YF, Marin-Atucha A, Fleurence J (2014) Seasonal antibacterial activity of two red seaweeds, Palmaria palmata and Grateloupia turuturu, on European abalone pathogen Vibrio harveyi. Aquat Living Resour 27:83–89

    Article  Google Scholar 

  • Huchette SH, Koh CS, Day R (2003) The effects of density on the behaviour and growth of juvenile blacklip abalone (Haliotis rubra). Aquac Int 11:411–428

    Article  Google Scholar 

  • Hudson JB, Kim JH, Lee MK, DeWreede RE, Hong YK (1998) Antiviral compounds in extracts of Korean seaweeds: evidence for multiple activities. J Appl Phycol 10:427–434

    Article  Google Scholar 

  • Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144

    Article  CAS  Google Scholar 

  • Janiak DS, Whitlatch RB (2012) Epifaunal and algal assemblages associated with the native Chondrus crispus (Stackhouse) and the non-native Grateloupia turuturu (Yamada) in eastern Long Island sound. J Exp Mar Biol Ecol 413:38–44

    Article  Google Scholar 

  • Kirkendale L, Robertson-Andersson DV, Winberg PC (2010) Review on the use and production of algae and manufactured diets as feed for sea-based abalone aquaculture in Victoria. University of Wollongong, Australia, p 188

    Google Scholar 

  • Lafontaine N, Mussio I, Rusig AM (2011) Production and regeneration of protoplasts from Grateloupia turuturu Yamada (Rhodophyta). J Appl Phycol 23:17–24

    Article  Google Scholar 

  • Mabeau S, Fleurence J (1993) Seaweed in food products: biochemical and nutritional aspects. Trends Food Sci Technol 4:103–107

    Article  CAS  Google Scholar 

  • Mai K, Mercer JP, Donlon J (1995a) Comparative studies on the nutrition of two species of abalone. Haliotis tuberculata L and Haliotis discus hannai Ino III response of abalone to various levels of dietary lipid. Aquaculture 134:65–80

    Article  CAS  Google Scholar 

  • 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 136:165–180

    Article  Google Scholar 

  • Mai K, Mercer JP, Donlon J (1996) Comparative studies on the nutrition of two species of abalone. Haliotis tuberculata L and Haliotis discus hannai Ino V the role of polyunsaturated fatty acids of macroalgae in abalone nutrition. Aquaculture 139:77–89

    Article  CAS  Google Scholar 

  • Mercer JP, Mai KS, Donlon J (1993) Comparative-studies on the nutrition of two species of abalone, Haliotis tuberculata Linnaeus and Haliotis discus hannai Ino. I. Effects of algal diets on growth and biochemical composition. Int J Invertebr Reprod Dev 23:75–88

    Article  CAS  Google Scholar 

  • Mgaya YD, Mercer JP (1995) The effects of size grading and stocking density on growth performance of juvenile abalone, Haliotis tuberculata Linnaeus. Aquaculture 136:297–312

    Article  Google Scholar 

  • Miller GL, Miller EE (1948) Determination of nitrogen in biological materials. Anal Chem 20:481–488

    Article  CAS  Google Scholar 

  • Morgan KC, Simpson FJ (1981) Cultivation of Palmaria (Rhodymenia) palmata: effect of high concentrations of nitrate and ammonium on growth and nitrogen uptake. Aquat Bot 11:167–171

    Article  CAS  Google Scholar 

  • Morgan K, Wright J, Simpson F (1980) Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ Bot 34:27–50

    Article  CAS  Google Scholar 

  • Mulvaney W, Winberg P, Adams L (2013) Comparison of macroalgal (Ulva and Grateloupia spp.) and formulated terrestrial feed on the growth and condition of juvenile abalone. J Appl Phycol 25:815–824

    Article  Google Scholar 

  • 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 18:437–443

    Article  CAS  Google Scholar 

  • Pang SJ, Xiao T, Shan TF, Wang ZF, Gao SQ (2006) Evidences of the intertidal red alga Grateloupia turuturu in turning Vibrio parahaemolyticus into non-culturable state in the presence of light. Aquaculture 260:369–374

    Article  Google Scholar 

  • Petton B, Pernet F, Robert R, Boudry P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile pacific oysters Crassostrea gigas. Aquac Environ Interact 3:257–273

    Article  Google Scholar 

  • 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 300:189–193

    Article  Google Scholar 

  • Rosen G, Langdon CJ, Evans F (2000) The nutritional value of Palmaria mollis cultured under different light intensities and water exchange rates for juvenile red abalone Haliotis rufescens. Aquaculture 185:121–136

    Article  Google Scholar 

  • Saunders TM, Mayfield S, Hogg A (2008) A simple, cost-effective, morphometric marker for characterising abalone populations at multiple spatial scales. Mar Freshw Res 59:32–40

    Article  Google Scholar 

  • Segarra A, Pépin JF, Arzul I, Morga B, Faury N, Renault T (2010) Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 153:92–99

    Article  CAS  PubMed  Google Scholar 

  • Shepherd SA, Steinberg PD (1992) Food preference of three Australian abalone species with the review of the algal food of abalone. In: Shepherd SA, Tegner MJ, Del Proo SAG (eds) Abalone of the world. Biology, fisheries and culture. Fishing News Books, Oxford, pp 169–181

    Google Scholar 

  • Shpigel M, Marshall A, Lupatsch I, Mercer JP, Neori A (1996) Acclimation and propagation of the abalone Haliotis tuberculata in a land-based culture system in Israel. J World Aquacult Soc 27:435–442

    Article  Google Scholar 

  • 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 18:227–234

    Google Scholar 

  • Steneck RS, Watling L (1982) Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Mar Biol 68:299–319

    Article  Google Scholar 

  • Taylor MH, Tsvetnenko E (2004) A growth assessment of juvenile abalone Haliotis laevigata fed enriched macroalgae Ulva rigida. Aquac Int 12:467–480

    Article  CAS  Google Scholar 

  • Thongrod S, Tamtin M, Chairat C, Boonyaratpalin M (2003) Lipid to carbohydrate ratio in donkey’s ear abalone (Haliotis asinina, linne) diets. Aquaculture 225:165–174

    Article  CAS  Google Scholar 

  • Troell M, Robertson-Andersson D, Anderson RJ, Bolton JJ, Maneveldt G, Halling C, Probyn T (2006) Abalone farming in South Africa: an overview with perspectives on kelp resources, abalone feed, potential for on-farm seaweed production and socio-economic importance. Aquaculture 257:266–281

    Article  Google Scholar 

  • Viera MP, Gómez Pinchetti JL, Courtois de Vicose G, Bilbao A, Suárez S, Haroun RJ, Izquierdo MS (2005) Suitability of three red macroalgae as a feed for the abalone Haliotis tuberculata coccinea Reeve. Aquaculture 248:75–82

    Article  Google Scholar 

  • Viera MP, Courtois de Vicose G, Fernández‐Palacios H, Izquierdo M (2014) Grow‐out culture of abalone Haliotis tuberculata coccinea Reeve, fed land‐based IMTA produced macroalgae, in a combined fish/abalone offshore mariculture system: effect of stocking density. Aquac Res. doi:10.1111/are.12467

    Google Scholar 

  • White C, Kennedy J, Chaplin M (1986) Carbohydrate analysis: a practical approach, second ed. The practical approach series.

  • Yates J, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus versiculosus. Ecology 74:1757–1766

    Article  Google Scholar 

Download references

Acknowledgments

All authors participated in the collection and interpretation of results. Mireille Amat, who is also a translator, corrected the English of the manuscript. The authors thank Katarzyna Lawreniuk for her technical assistance during feeding experiments. This project was funded by the Fundació “Obra Social la Caixa” through a doctoral scholarship to Nuria García Bueno and by the Syndicat Mixte pour le Développement de l’Aquaculture et de la Pêche (SMIDAP) de la Région des Pays de la Loire.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Priscilla Decottignies.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Bueno, N., Turpin, V., Cognie, B. et al. Can the European abalone Haliotis tuberculata survive on an invasive algae? A comparison of the nutritional value of the introduced Grateloupia turuturu and the native Palmaria palmata, for the commercial European abalone industry. J Appl Phycol 28, 2427–2433 (2016). https://doi.org/10.1007/s10811-015-0741-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0741-z

Keywords

Navigation