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.
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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
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
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
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
Cook PA (2014) The worldwide abalone industry. Mod Econ 5:1181
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
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
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
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
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
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
Fleming AE, Van Barneveld RJ, Hone PW (1996) The development of artificial diets for abalone: a review and future directions. Aquaculture 140:5–53
Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28
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
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
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
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
Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144
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
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
Lafontaine N, Mussio I, Rusig AM (2011) Production and regeneration of protoplasts from Grateloupia turuturu Yamada (Rhodophyta). J Appl Phycol 23:17–24
Mabeau S, Fleurence J (1993) Seaweed in food products: biochemical and nutritional aspects. Trends Food Sci Technol 4:103–107
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
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
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
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
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
Miller GL, Miller EE (1948) Determination of nitrogen in biological materials. Anal Chem 20:481–488
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
Morgan K, Wright J, Simpson F (1980) Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ Bot 34:27–50
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
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
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
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
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
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
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
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
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
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
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
Steneck RS, Watling L (1982) Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Mar Biol 68:299–319
Taylor MH, Tsvetnenko E (2004) A growth assessment of juvenile abalone Haliotis laevigata fed enriched macroalgae Ulva rigida. Aquac Int 12:467–480
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s10811-015-0741-z