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Nutritive and Xenobiotic Compounds in the Alien Algae Undaria pinnatifida From Argentine Patagonia

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Abstract

Seaweeds have been used as food since ancient times. The edible brown algae Undaria pinnatifida is native to northeast Asia; however, in 1992, the first specimens in Patagonian environments were found and, since then, have rapidly expanded. The main object of this study was to determine, for the first time in Argentina, the nutritive composition and concentrations of trace elements and hydrocarbons in these alien algae and evaluate their usefulness as food. Sexually mature U. pinnatifida samples were collected at 10-m depth in the Nuevo and San José gulfs. The first site is influenced by activities from Puerto Madryn city, and the latter place was considered as the control. Protein, dietary fiber, and mineral concentrations were similar in both gulfs and in the same order as in eastern countries. Crude protein, indigestible fiber, and calcium and magnesium concentrations were greatest in blade; lipid concentration was greatest in sporophyll; and sodium and potassium concentrations were greatest in midrib. Amino acids showed the greatest concentrations in blades, and these were greater than those reported in kelp from Japan. Cadmium (Cd), arsenic, mercury, and hydrocarbons were detected, but only Cd showed concentrations that could be a risk for consumption. In Argentina, maximum acceptable levels of these contaminants in seaweeds are not established.

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References

  • Almela C, Clemente MJ, Vélez D, Montoro R (2006) Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain. Food Chem Toxicol 44:1901–1908

    Article  CAS  Google Scholar 

  • Andrade LR, Salgado LT, Farina M, Pereira MS, Mourao PAS, Amado Filho GM (2004) Ultrastructure of acidic polysaccharides from the cell walls of brown algae. J Struct Biol 145(3):216–225

    Article  CAS  Google Scholar 

  • Association of Official Analytical Chemists (2005) Official methods of analysis of the association of official analytical chemists, 18th edn. AOAC, Arlington

    Google Scholar 

  • Besada V, Andrade JM, Schultze F, González JJ (2009) Heavy metals in edible seaweeds commercialised for human consumption. J Mar Syst 75:305–313

    Article  Google Scholar 

  • Billakanti JM, Catchpole O, Fenton T, Mitchell K, MacKenzie AD (2013) Enzyme-assisted extraction of fucoxanthin and lipids containing polyunsaturated fatty acids from Undaria pinnatifida using dimethyl ether and ethanol. Process Biochem 48:1999–2008

    Article  CAS  Google Scholar 

  • Bremmer JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, vol part 2, agronomy no. 9. American Society of Agronomy, Madison, pp 595–624

    Google Scholar 

  • Brownlee IA, Allen A, Pearson JP, Dettmar PW, Havler ME, Atherton MR et al (2005) Alginate as a source of dietary fiber. Crit Rev Food Sci Nutr 45:497–510

    Article  CAS  Google Scholar 

  • Burtin P (2003) Nutritional value of seaweeds. J Environ Agric Food Chem 2(4):498–503

    Google Scholar 

  • Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326/327(1):213–215

    Article  Google Scholar 

  • Casas GN, Scrosati R, Piriz ML (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invasions 6(4):411–416

    Article  Google Scholar 

  • Casas GN, Piriz ML, Parodi EL (2008) Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae:Laminariales) in Nuevo Gulf (Patagonia, Argentina). J Mar Biol Assoc UK 88(1):21–28

    Article  Google Scholar 

  • Cofrades S, López-López I, Bravo L, Ruiz-Capillas C, Bastida S, Larrea MT et al (2010) Nutritional and antioxidant properties of different brown and red Spanish edible seaweeds. Food Sci Technol Int 16(5):361–370

    Article  CAS  Google Scholar 

  • Commendatore MG, Esteves JL (2004) Natural and anthropogenic hydrocarbons in sediments from the Chubut River (Patagonia, Argentina). Mar Pollut Bull 48:910–918

    Article  CAS  Google Scholar 

  • Commendatore MG, Esteves JL, Colombo JC (2000) Hydrocarbons in coastal sediments of Patagonia, Argentina: levels and probable sources. Mar Pollut Bull 40(11):989–998

    Article  CAS  Google Scholar 

  • Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330

    Article  CAS  Google Scholar 

  • Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    Article  CAS  Google Scholar 

  • Erickson MC (1993) Lipid extraction from channel catfish muscle: comparison of solvent systems. J Food Sci 58(1):84–89

    Article  CAS  Google Scholar 

  • European Commission (2003) Opinion of the scientific committee for animal nutrition on the use of copper in feedingstuffs. Health and Consumer Protection Directorate General, Directorate C: Scientific Opinions, C2 Management of Scientific Committees. Scientific Co-operation and Networks, Brussels, pp 1–47

    Google Scholar 

  • European Commission (2008) Commission regulation (EC) Nº 629/2008 of 2 July 2008 Amending Regulation (EC) Nº 1881/2006. Setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union 173:6–9

    Google Scholar 

  • European Food Safety Authority (2009) Scientific opinion on arsenic in food. EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA J 7(10):1351

    Google Scholar 

  • European Food Safety Authority (2012) Scientific opinion on mineral oil hydrocarbons in food. EFSA Panel on Contaminants in the Food Chain (CONTAM). EFSA J 10(6):2704

    Google Scholar 

  • Eyras MC (2002) Tratamiento agroecológico de las algas marinas de arribazón en Puerto Madryn, Chubut. PhD thesis, La Plata National University, Argentina

  • Fahy E, Subramaniam S, Murphy R, Nishijima M, Raetz C, Shimizu T, Spener F et al (2009) Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res 50:S9–S14

    Article  Google Scholar 

  • Fernández-Saá C (2002) Las verduras del océano Atlántico. Algas de Galicia. Alimento y Salud: Propiedades, recetas, descripción. Pontevedra, Spain, Editorial

  • Fleurence J, La Coeur C (1994) Influence of digestion procedures on the determination of lead and cadmium levels in the Laminariale Undaria pinnatifida (Wakame) by flame atomic absorption spectrophotometry. Bot Mar 37:555–559

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization/World Health Organization WHO/UNU (1985) Energy and protein requirements: Report of a joint FAO/WHO/UNU expert consultation. WHO Technical Report Series No. 724. WHO, Geneva, Switzerland, pp 120–126

  • Giarratano E, Amin OA (2010) Heavy metals monitoring in the southernmost mussel farm of the world (Beagle Channel, Argentina). Ecotox Environ Saf 73:1378–1384

    Article  CAS  Google Scholar 

  • Gil MN, Esteves JL (2000) Nutrient budgets in Bahía Nueva, Golfo Nuevo (Patagonia, Argentina). Estuarine systems of the South American region: carbon, nitrogen and phosphorus fluxes. Loicz Reports & Studies No. 15, pp 44–50

  • Gil MN, Torres AI, Harvey M, Esteves JL (2006) Metales pesados en organismos marinos de la zona costera de la Patagonia argentina continental. Rev Biol Mar Oceanogr 41(2):167–176

    Article  Google Scholar 

  • Handbook on Human Nutritional Requirements (1974) Published by FAO and WHO. FAO Nutritional Studies No. 28; WHO Monograph Series No. 61, Geneva

  • Instituto Nacional de Estadísticas y Censos) (2010) Available at: hppt:www.indec.gov.ar/. Accessed

  • Irigoyen AJ, Trobbiani G, Sgarlatta MP, Raffo MP (2011) Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biol Invasions 13:1521–1532

    Article  Google Scholar 

  • Joint Food and Agriculture Organization/World Health Organization Expert Committee on Food Additives (1996) Toxicological evaluation of certain food additives and contaminants. WHO Food Additive Series 35. WHO, Geneva, Switzerland

  • Kolb N, Vallorani L, Milanovi N, Stocchi V (2004) Evaluation of marine algae wakame (Undaria pinnatifida) and kombu (Laminaria digitata japonica) as food supplements. Food Technol Biotechnol 42(1):57–61

    CAS  Google Scholar 

  • Lagarda MJ, García-Llatas G, Farr R (2006) Analysis of phytosterols in foods. J Pharm Biomed Anal 41:1486–1496

    Article  CAS  Google Scholar 

  • Lahaye M, Kaeffer B (1997) Seaweed dietary fibres: structure, physico–chemical and biological properties relevant to intestinal physiology. Sci Aliments 17:563–584

    CAS  Google Scholar 

  • Li J (2013) Lipid, fatty acid and sterol analysis content of New Zealand Undaria pinnatifida. Master’s thesis. Auckland University of Technology, Aukland, New Zealand

  • Massara Paletto V, Commendatore MG, Esteves JL (2008) Hydrocarbon levels in sediments and bivalve mollusks from Bahía Nueva (Patagonia, Argentina): an assessment of probable origin and bioaccumulation factors. Mar Pollut Bull 56:2100–2105

    Article  CAS  Google Scholar 

  • Millie G, Rivet L, Jalad AI, Bertrand JC (1992) Hydrocarbon distribution in low polluted surface sediments from Kuwait, Bahrain and Oman coast zones (before the Gulf War). Mar Pollut Bull 24(12):622–626

    Article  Google Scholar 

  • Moreiras O, Carvajal A, Cabrera L, Cuadrado C (2003) Tablas de composición de alimentos, 7th edn. Ediciones Pirámide, Madrid

    Google Scholar 

  • Murata M, Nakazoe J (2001) Production and use of marine algae in Japan. Jpn Agr Res Q 35(4):281–290

    Google Scholar 

  • Nisizawa K, Noda H, Kikuchi R, Watanabe T (1987) The main seaweed foods in Japan. Hydrobiologia 151(152):5–29

    Article  Google Scholar 

  • Olvera Novoa MA, Martinez Palacios CA, Real de León E (1993) Manual de técnicas para laboratorio de nutrición de peces y crustáceos. Apoyo a las Actividades Regionales de Acuicultura para América Latina y el Caribe. FAO-Italia. Available at: http://www.fao.org/docrep/field/003/AB489S/AB489S00.htm. Accessed: June 18 2012

  • Pavoni V, Caliceti M, Sperni L, Sfriso A (2003) Organica micropollutants (PAHs, PCBs, pesticidas) in seaweeds of the lagoon of Venice. Oceanol Acta 26:585–596

    Article  CAS  Google Scholar 

  • Perez AA, Perez LB, Strobl AM, Camarda S, Farias SS, López CM et al (2010) Variación estacional de arsénico total en algas comestibles recolectadas en el Golfo San Jorge (Chubut, Argentina). Rev Lat Am Biotecnol Amb Algal 1(1):16–30

    Google Scholar 

  • Pérez-Cirera JL, Salinas JM, Cremades J, Bárbara I, Granja A, Viega AJ et al (1997) Cultivo de Undaria pinnatifida (Laminariales, Phaeophyta) en Galicia. Nova Acta Científica Compostelana 7:3–28

    Google Scholar 

  • Piriz ML, Casas GN (1994) Occurrence of Undaria pinnatifida in Golfo Nuevo, Argentina. Appl Phycol Forum 10:4

    Google Scholar 

  • Prabhasankar P, Ganesan P, Bhaskar N, Hirose A, Stephen N, Gowda LR et al (2009) Edible Japanese seaweed, wakame (Undaria pinnatifida), as an ingredient in pasta: chemical, functional and structural evaluation. Food Chem 115:501–508

    Article  CAS  Google Scholar 

  • Punín Crespo MO, Yusty MA (2006) Comparison of supercritical fluid extraction and Soxhlet extraction for the determination of aliphatic hydrocarbons in seaweed samples. Ecotoxicol Environ Saf 64:400–405

    Article  Google Scholar 

  • Raffo P, Eyras MC, Iribarne OO (2009) The invasion of Undaria pinnatifida to a Macrocystis pyrifera kelp in Patagonia (Argentina, south-west Atlantic). J Mar Biol Assoc UK 89(8):1571–1580

    Article  Google Scholar 

  • Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26

    Article  Google Scholar 

  • Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212(3):349–354

    Article  Google Scholar 

  • Rupérez P, Ahrazem O, Leal JA (2002) Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. J Agric Food Chem 50:840–845

    Article  Google Scholar 

  • Sakurai A, Fujioka S (1997) Studies on biosynthesis of brassinosteroids. Biosci Biotech Biochem 61:757–762

    Article  CAS  Google Scholar 

  • Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004a) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Article  Google Scholar 

  • Sánchez-Machado DI, López-Hernández P, Paseiro-Losada P, López-Cervantes J (2004b) An HPLC method for the quantification of sterols in edible seaweeds. Biomed Chromatogr 18:183–190

    Article  Google Scholar 

  • Siegel S (1980) Estadística no paramétrica aplicada a las ciencias de la conducta. Trillas, México City

    Google Scholar 

  • Skalar (2005a) Skalar methods. Analysis: Nitrate + nitrate. Catalogue number 461 + 031 + Diamond. Issue 081505/MH/99235956. Breda, Netherlands

  • Skalar (2005b) Skalar method. Analysis: Phosphate. Catalogue number 503 + 010w/r + Diamond. Issue 081505/MH/99235956. Breda, Netherlands

  • Skalar (2005c) Skalar method. Analysis: Silicate. Catalogue number 563|051 + Diamond. Issue 081505/MH/99235956. Breda, Netherlands

  • Sokal RR, Rohlf FJ (1981) Biometry. Freeman, New York

    Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fisheries Research Board of Canada, Canada

    Google Scholar 

  • Tabarsa M, Rezaei M, Ramezanpour Z, Robert Walland J, Rabiei R (2012) Fatty acids, amino acids, mineral contents, and proximate composition of some brown seaweeds. J Phycol 48:285–292

    Article  CAS  Google Scholar 

  • Torres AI, Gil MN, Esteves JL (2004) Nutrient uptake rates by the alien alga Undaria pinnatifida (Phaeophyta) (Nuevo Gulf, Patagonia, Argentina) when exposed to diluted sewage effluent. Hydrobiologia 520:1–6

    Article  CAS  Google Scholar 

  • United Nations Environment Programme/Intergovernmental Oceanographic Commission/International Atomic Energy Agency (1992) Determination of petroleum hydrocarbons in sediments. Reference Method for Marine Pollution Studies no. 20

  • United Nations Organization for Education, Science and Culture (1982) Determinación de los hidrocarburos del petróleo en los sedimentos. Comisión Oceanográfica Intergubernamental. Manuales y Guías no. 11

  • Urbano MG, Goñi I (2002) Bioavailability of nutrients in rats fed on edible seaweeds, Nori (Porphyra tenera) and Wakame (Undaria pinnatifida), as a source of dietary fibre. Food Chem 76:281–286

    Article  CAS  Google Scholar 

  • Van Söest P, Robertson J (1985) Analysis of forages and fibrous foods. Laboratory Manual for Animal Science Cornell University, New York

    Google Scholar 

  • Vinot C, Durand P (1986) Algues alimentaires: Undaria, des résultats prometteurs. Equinoxe 8:29–34

  • Wong KH, Cheung PCK (2000) Nutritional evaluation of some subtropical red and green seaweeds. Part I: approximate composition, amino acid profiles and some physico–chemical properties. Food Chem 71:475–482

    Article  CAS  Google Scholar 

  • Yamada M, Yamamoto K, Ushihara Y, Kawai H (2007) Variation in metal concentrations in the brown alga Undaria pinnatifida in Osaka Bay, Japan. Phycol Res 55:222–230

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by Dirección General de Promoción Científica y Técnica of the Chubut Province, Funding B No. 319. We thank student Julieta Sturla for help in laboratory analyses.

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Gil, M.N., Torres, A.I., Commendatore, M.G. et al. Nutritive and Xenobiotic Compounds in the Alien Algae Undaria pinnatifida From Argentine Patagonia. Arch Environ Contam Toxicol 68, 553–565 (2015). https://doi.org/10.1007/s00244-014-0090-y

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