2035 CORE 1 − a ary 2018 Brage IMR Brage by provided brought to you by by you to brought a* Nina S Liland, c In recent decades, there has been increasing 2 and Erik-Jan Lock † d Moreover, certain species common in Norwegian 5 These properties, coupled with high variations in shape, 6,7 Current address: Station Biologique de Roscoff, Roscoff, National Institute of Nutrition and Seafood Research (NIFES), Bergen, Department of Biology, University of Bergen, Bergen, Norway Norwegian Institute of Bioeconomy Research, Bodø, Norway Irish Seaweed Research Group, RyanGalway, Galway, Institute, National University of Ireland Correspondence to: EJResearch (NIFES), Lock, Bergen, Norway. E-mail: National [email protected] Institute of Nutrition and Seafood published by John Wiley & Sons Ltd on behalf of Society of c a ∗ † d b and polyunsaturated fattyacid acids (PUFAs) (EPA)). (e.g. eicosapentaenoic colour, texture and taste,food make and feed marine items. macroalgae attractive as dry weight (DW)) andacids. a considerable amount of essential amino waters can contain relatively high protein levels (200–300 g kg Christian G Bruckner, 3 a Algae published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Svenja Heesch 4 a Ikram Belghit, a,b Heidi Amlund, a,b such as industrial production of biofuels Journal of the Science of Food and Agriculture 2 Journal of the Science of Food and Agriculture In the last decade, in Norway, an increasing number Several algal species can be found growing naturally seaweeds; Norway; nutrients; arsenic; heavy metals 2 1

Keywords: Supporting information may be found in the online version of this article. Chemical Industry. This is an open access articlemedium, under provided the the terms original of work the is Creative properly Commons cited. Attribution License, which permits use, distribution and reproduction in any of research projects have focusedrange on of the applications, use of algae for a wide in enormous volumes alongamong the the coastline world’s ofthe longest Norway, interest which and to is cultivated. most utilize productive, this enhancing resource both wild-harvested and © 2017 The Authors. and compounds of medical and pharmaceutical value. INTRODUCTION Marine macroalgae or seaweedsgroup are of a large photosynthetic and organismsenvironments, heterogeneous found commonly worldwide classified into in three marine taxonomicbrown groups: algae (Phaeophyceae), red algaealgae (Rhodophyta) (Chlorophyta). and Macroalgae green areculture part of of many Asian the countries, traditional whereon they food have a been cultivated large scaletion for of this centuries. resource In infocused contrast on has to the been industrial Asia, very productionalginates). the limited of and exploita- thickeners mainly (e.g. agar and Abstract BACKGROUND: In the past few years,cultivating much effort and has processing been invested marine intoe.g. macroalgae developing as a in source new Norway. blue of economy Macroalgae pharmaceuticals,macroalgae based have production on from harvesting, high of Norwegian biofuels potential waters or for arespecies. as Both a scant. macro- food This wide and and study micronutrients range feed. were waswere of analysed. However, also designed data Concentrations quantified. applications, of to on heavy characterize the metals and the chemical the composition chemical metalloid of composition arsenic of inRESULTS: The the 21 results algae confirm algal that marine macroalgae containthe nutrients which concentrations are relevant whereof for are both human highly andstudied, animal dependent concentrations nutrition, were on mostly species. below maximum Although allowed heavy levels set metals by and food arsenic andCONCLUSION: This feed were study legislation detected provides in chemical in the data EU. thered on algae and a green wide algae) range and of discusses algal© both species 2017 benefits covering the of The three and Authors. taxonomic potential groups limitations (brown, to their use for food and feed purposes. potential use in food and feed Rune Waagbø, waters: benefits of and limitations to their Irene Biancarosa, marine macroalgae common in Norwegian (wileyonlinelibrary.com) DOI 10.1002/jsfa.8798 Chemical characterization of 21 species of Research Article Received: 26 September 2017 Revised: 21 November 2017 Accepted article published: 28 November 2017 Published online in Wiley Online Library: 18 Janu are naturally rich in valuable nutrients such as minerals, vitamins View metadata, citation and similar papers at core.ac.uk at papers similar and citation metadata, View et al. : 2035–2042 98 C until constant ∘ N and 14.47 and 2018; ∘ 67.305987, 14.727638 GPS coordinates b C in vacuum (0.2–0.01 mbar) ∘ J Sci Food Agric 20 − 17 et al. branched weed Sugar tang 67.240804, 14.712079 E) in the intertidal or upper subtidal zone. Each sample Briefly, the algae were rinsed in cold freshwater to remove C prior to analyses. ∘ 7 ∘ A complete list of the species identified in the current study as Fatty acid (FA) composition was quantified by gas chromatog- 30 cadmium (Cd), leadAs. (Pb) We discuss and differences mercury amongbenefits the of (Hg) and species and limitations studied, to assessing the theiringredients. potential metalloid use as food and feed adhering foreign material, then ground,− powdered and stored at well as the sample locations is given in Table 1. Chemical analyses Dry matterfreeze-drying (DM) the samples content at was estimated gravimetrically by for 24 h and then leavingweight was them reached. in vacuum at 25 raphy coupled with flamedescribed by ionisation Torstensen detection using a method MATERIALS AND METHODS Sample collection and species identification Macroalgae were harvested in Octobercoast 2014 of along the Norway Northern (between 67.24 and 67.32 14.72 consisted of pooled material of at least fiveThe individuals processing per of species. the samples iset described al. in detail in Biancarosa 8 10 6,7,16 (sugar Marine © 2017 The Authors. www.soci.org I Biancarosa Porphyra (O.F. Müller) C. Agardh Slimy whip weed 67.239783, 14.510323 (L.) Le Jolis Egg wrack 67.305987, 14.727638 11,12 (L.) S.F. Gray Thong weed 67.276063, 14.572370 (Hudson) J.V. Lamouroux Clawed fork weed 67.305987, 14.727638 (Stackhouse) Guiry Grape pip weed 67.325565, 14.478626 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. and coordinates of sampling locations (L.) Kützing Common green (L.) Decaisne & Thuret Channel wrack 67.326911, 14.478223 (L.) C.E. Lane, C. Mayes, Druehl & G.W. Kützing Tough laver 67.239783, 14.510323 a (Roth) Agardh Purple laver 67.323491, 14.478753 (Hudson) J.V. Lamouroux Sea girdle 67.240804, 14.712079 (rockweed) and (L.) Weber & Mohr Dulse 67.322567, 14.457314 (L.) Lyngbye Sea oak 67.239783, 14.510323 L. Bladder wrack 67.240804, 14.712079 Stackhouse Irish moss 67.412274, 14.621368 (red sea lettuce). (L.) Greville Wing kelp 67.276063, 14.572370 L. Gut weed 67.323491, 14.478753 J. Brodie & L.M. Irvine Black laver 67.323491, 14.478753 L. Serrated wrack 67.323491, 14.478753 L. Spiral wrack 67.305987, 14.727638 L. Sea lettuce 67.323491, 14.478753 Saccharina latissima Saunders which can be toxic to living Porphyra dioica Porphyra purpurea Porphyra umbilicalis Chondrus crispus Mastocarpus stellatus Furcellaria lumbricalis Palmaria palmata Ulva intestinalis Ulva lactuca Cladophora rupestris Laminaria digitata Alaria esculenta Chordaria flagelliformis serratus Fucus vesiculosus Pelvetia canaliculata Halidrys siliquosa Himanthalia elongata Ascophyllum nodosum Saccharina latissima Palmaria palmata 13,14 Ascophyllum nodosum (winged kelp) and the red algae for European Nucleotide Archive (ENA)/GenBank accession numbers. 7 9 et al. Documentationofbothnutrientsandundesirable Journal of the Science of Food and Agriculture Marine macroalgal species included in study (red algae) (green algae) () 15 sp. (kelp). Alaria esculenta According to www.algaebase.org. See Biancarosa Marine macroalgae can contain high concentrations of iodine. In the present study, we characterized the chemical composition No. Taxon Species Common name a b 1 Rhodophyta Table 1. 3 2 4 5 6 7 8 Chlorophyta 9 10 11 Phaeophyceae 20 19 21 12 17 13 14 15 16 18 elements potentially present in algae is fundamentalpotentials to determine and limitationsposes. of However, such data their on species use from Norwegian for waters food and feed pur- wileyonlinelibrary.com/jsfa are very scarce. of 21 species ofgian marine coast, representing macroalgae the collected three groups along ofalgae. red, the green We and Norwe- brown also determined concentrations of the heavy metals Iodine is a traceroid element hormones thyroxine essential (T3) for andin the triiodothyronine the synthesis (T4) of regulation involved the ofAn thy- metabolism insufficient in dietarydevelopment both supply of humans several of disorders and such this asmalities, animals. thyroid element function goitre abnor- can and lead cretinism,shown to whereas to the excess cause intake toxic has effects been in humans and fish. Moreover, marine macroalgae haveas also feed seen ingredients for renewedtry), livestock interest especially (e.g. the ruminants, species pigs and poul- interest in eating macroalgae infood Norway, species with being the the most brown relevant algae kelp) and organisms. macroalgae can accumulate undesirablerounding elements from environment, the sur- especially(As) certain in high metals concentrations, and arsenic Laminaria sp. (red and purple laver) and

2036 2037 1 1 1 1 1 − − − − − -3 DW n LOQ 1 < -6/ − n -6 n Sum 3000 mg kg (4600 mg kg tty acids; MUFAs, > -3 DW respectively). n Sum 1 − DW). 1 ). In this study, Pb was − DW in green, brown and Sum S. latissima PUFAs 1 − wileyonlinelibrary.com/jsfa DW)comparedwithredand -3 n 1 DW) algae. Levels of inorganic − (EPA) 1 20:5 − (10 000 mg kg -6 n the concentration of iAs was 2.4 mg kg Pelvetia canaliculata ). -3 DW) compared with red (6.4–24 mg kg DW in most red algal species to n 1 LOQ 0.01 0.01 0.03 0.01 0.01 0.9 ) compared with green algae (up to 3 mg kg 1 − DW ( < (ALA) 20:4 − 18:3 1 − DW) (Supplementary Table 1). However, in the brown -6 1 n LOQ − Laminaria digitata < (LA) 18:2 200 mg kg Ulva intestinalis < Halidrys siliquosa -3 Porphyra dioica n LOQLOQ 4.99 0.33 1.51 0.24 6.32 0.48 2.06 0.39 18.8 2.03 4.57 14.1 1.15 0.88 0.3 1.3 LOQ 0.06 0.01 0.13 0.86LOQ 1.17LOQ 0.38 0.88LOQ 1.78 0.28LOQ 0.25 2.86 3.1 LOQ 0.49 2.52 0.74LOQ 0.99 4.28 2.50LOQ 0.71 0.48 2.83 1.23LOQ 1.45 1.09 0.38 2.52 2.31LOQ 1.09 1.76 0.44 3.91 7.23 1.09 0.45 0.95 0.56 3.02 1.21 8.75 2.08 0.43 1.57 1.10 5.12 7.67 0.9 4.34 0.42 1.30 0.91 4.41 13.5 0.4 1.99 0.42 0.59 5.63 9.81 1.0 3.89 0.46 9.57 2.96 0.4 3.07 0.82 6.71 2.58 0.4 1.37 1.57 3.10 0.5 1.14 1.43 0.9 1.89 1.21 0.8 1.6 LOQ 0.02LOQ 0.01 0.23 0.36 0.10 0.92 1.06 1.34 0.92 2.79 0.40 4.76 2.3 3.11 1.64 1.9 Arsenic content (as total As) in the samples is shown in Fig. 1. The heavy metals Cd, Hg and Pb were found in all samples anal- < < < < < < < < < < < < < < ee2123 2–19 g and 0.03–5mg 2.1–2.3, were As (iAs) were generally low0.5 mg in kg the species studied (mostly below DW in DW) and green (6.4–10 mg kg DW, amounting to 10% of total As. DW in some brown algal species suchDW) as and Higher levels of(21–120 mg this kg metalloid were found in brown algae alga ysed, with their concentrations(Fig. varying 1; Supplementary widely Table 1). between The species in level green of algae Cd was (0.12–0.18 relatively mg low kg in brown algae (0.07–3.1 and 0.03–2.6 mg kg red algae respectively. Elemental composition A detailed overview of the mineral compositionstudy of the is algae presented in in this Table 3.from Iodine contents of the algae ranged foundtobelowinredandbrownalgae(upto0.58mgkg The concentrations of Hg in the species studied ranged from to 0.04 mg kg -3) Sum n MUFAs 16:3 using -7 18 n LOQ 3.58 < et al. published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. -9 18:1 n -linolenic acid; EPA, eicosapentaenoic acid; PUFAs, polyunsaturated fatty acids; LOQ, limit of quantification 𝛼 algal DW) of 21 macroalgal species 18 1 − DW), comprising mainly -linolenic acid (18:3 -7 18:1 -7), hexadecatrienoic acid n 𝛼 1 et al. n − DW). Concentrations of PUFAs 21 1 − -7) and Sum SFAs 16:1 et al. n DW respectively (Table 2). Total saturated 1 : 2035–2042 © 2017 The Authors. − DW of total FAs respectively; while in red 98 1 − -9) (0.48–20 mg g 2.50 2.700.45 0.76 0.67 6.51 0.04 1.23 0.45 0.13 17.37 0.48 0.04 0.01 18.2 0.64 0.02 0.470.06 0.02 0.39 0.51 0.030.41 0.50 0.02 1.120.03 0.04 0.06 0.860.03 0.08 1.66 0.02 1.05 0.11 0.95 0.04 0.98 0.080.28 1.19 0.05 0.98 0.051.83 0.28 0.32 0.08 0.03 2.051.58 0.03 1.43 0.27 0.12 2.88 0.202.65 0.10 4.16 0.77 0.13 3.23 0.464.65 0.2 5.59 1.50 0.14 0.29 3.63 0.432.82 0.99 6.23 0.56 0.33 0.04 2.40 0.060.39 0.01 8.62 9.05 0.58 0.14 0.30 1.24 0.030.26 0.18 3.54 5.60 0.07 0.08 0.46 1.12 1.17 0.040.29 0.13 10.31 1.88 1.15 0.03 0.24 0.29 1.09 19.69 0.13 0.11 1.57 9.22 0.05 0.03 0.05 0.27 8.09 0.97 1.56 0.04 0.10 0.70 0.16 10.9 1.12 0.78 0.13 0.02 0.02 20.9 0.62 1.25 0.32 0.01 0.08 1.23 0.96 8.61 0.05 0.01 2.33 0.27 1.21 0.10 0.01 2.17 0.80 3.5 0.76 1.34 2.13 1.80 1.41 0.36 0.6 1.68 0.43 4.9 3.9 0.06 0.650.08 0.02 0.620.23 0.74 0.03 0.740.06 0.75 0.03 0.14 2.03 1.04 0.11 0.08 0.25 2.31 0.03 0.42 0.11 0.02 0.16 0.05 0.28 0.41 0.08 0.58 0.16 0.32 0.01 0.74 0.02 0.04 0.14 0.03 0.20 0.72 0.13 0.57 1.50 1.45 2.31 0.63 0.80 2.00 0.31 0.8 6.4 0.01 0.04 0.01 0.04 0.01 0.02 0.01 0.02 0.3 n 2018; 19 LOQ (below limit of quantification)–0.3, 0.01–0.16 Fatty acid composition (mg g Journal of the Science of Food and Agriculture < et al. as described by Hamre -3), vaccenic acid (18:1 LOQ–1.51 mg g n 20 DW in green, brown and red algae respectively (Table 2). < 1 Iodine was quantified according to Julshamn Inorganic As (iAs) was analysed by anion exchange high-pressure Multi-element analysis was carried out by inductively cou- VitaminEformswereanalysedbyHPLCaccordingtoKonings P. canaliculata S. latissima P. purpurea P. umbilicalis A. nodosum C. flagelliformis F. serratus F. spiralis F. vesiculosus H. siliquosa H. elongata L. digitata Green algae C. rupestris U. intestinalis U. lactuca Brown algae A. esculenta F. lumbricalis M. stellatus P. palmata P. dioica monounsaturated fatty acids;(0.1 LA, area %). linoleic acid; ALA, Data represent mean values of two analytical measurements conducted on pooled algal material of several individuals per species. SFAs, saturated fa Red algae C. crispus Species 14:0 16:0 18:0 Table 2. − in green algal species were0.11–0.97 0.03–0.98, mg 0.01–0.18, g 0.20–0.46 and fatty acid (SFAs) amounted tog 0.96–1.7, 1.23–9 and 0.04–2.3 mg liquid chromatography coupled with ICPMS (HPLC/ICPMS),on based Sloth pled plasma mass spectrometrymicrowave (ICPMS) oven, after similarly to wet Julshamn digestion in a and brown algal0.01–046, samples these FAs reached concentrations of J Sci Food Agric RESULTS Fatty acid profile Concentrations of palmitoleic acid (16:1 (16:3 Chemical composition of Norwegian marine macroalgae www.soci.org Palmitic acid (16:0) was theples. Concentrations of most monounsaturated fatty abundant acids (MUFAs) SFA were inhighest all in brown algal algae sam- (0.64–21 mg g oleic acid (18:1 ICPMS (Agilent 7500, Agilent, Santaautosampling Clara, (ASX-500, CA, Cetac, Omaha, USA) NE, coupled USA). with et al. and 15 31 , 1 − et al. Thus Today, 29 -3 PUFAs 29 n : 2035–2042 68 13 17 67 05 29 03 16 29 24 08 28 142 09 42 09 37 06 25 12 43 172 05 28 06 84 18 55 123 07 81 14 19 05 23 76 21 14 55 ...... 98 they may still be EPA is well known 2018; 27,28 70 70 10 70 10 00 70 50 10 10 6,25 ...... species, where this marine -3 FAs in biological tissues n 5:1, they have the potential to J Sci Food Agric -3 is around 15–20:1 in Western < DHA is about 200–250 mg day -3 FAs is considered an index for n Porphyra n + -6 and n algal DW for Cu, Fe, I, Mn, Se and Zn) of 21 1 − -6 and -6 and n n Despite their high concentrations of EPA, red On the other hand, another health-promoting -3 ratio of the algae in this study was within n 6,25 26 -6/ n 0 930 480 56 0 8 160 110 21 0 120596 089226 77 16 710 2 7 290 260 37 0 1 73 220 4 5 120 150 33 0 1 240 440 69 0 2 160 4600 5 0 63 1100 140 0 7 200 340 7 6 100 670 13 0 9 300 200 8 0 72 380 3 2 130 84 7 3 150 10000 3 1 1800 43 26 0 7 5800 130 180 0 6 330 200 22 0 ...... ; this contrasts with the ideal ratio, which should not exceed 30 In red algae, high relative concentrations of EPA (36% of total FAs) An imbalance between 5:1, as recommended by the World Health Organization (WHO). is known to cause inflammatory processes in the body. < algae cannot be considered good dietary sources of LC owing to their low total lipid contents. Currently, themendation global for recom- intake of EPA marine omega-3 PUFA,present docosahexaenoic in acid the (DHA), samplesvious was findings. analysed in not this study, confirming pre- were observed, especially in Since the and while the useproducts of is red thus unlikely algae compared asomega-3 with stand-alone PUFAs other such oil-based sources as of dietary microalgae marine or fish, the recommended rangeenhance the of nutritional quality of food products, e.g.low-density by regulating lipoprotein and cholesterol levels, and thus may help for its beneficial effectscular on diseases. health, especially against cardiovas- the ratio between evaluating the nutritionalrespect value to of human and a animal development dietary and lipid health. source with used as supplements in diets for both human and animal nutrition. omega-3 fatty acid comprised more thanrelative a third concentrations of of total FAs. this High ously long-chain been (LC) reported PUFA in have previ- red algal species. the ratio between diets 87 48 24 07 55 . . . . . DM DW 1 -and 1 − − 𝛽 © 2017 The Authors. www.soci.org I Biancarosa -, algalDWforCa,Mg,P,KandNa;mgkg 𝛼 ( 1 DM respec- 23,24 -tocopherol − 𝛿 1 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. − -3). 1mg kg n < -and 6211 5174 547391 3 31 100 8 136130 3 26 4 10 570 84 25 0 025183 128272 1283 76 30 32 2 5 100 24 1 334211 420273 83 17 33 3 70 17 23 3 754162 242106 631271 2287 7128 430187 ...... 𝛾 -, H. siliquosa 𝛽 -, 𝛼 DW respectively) (Table 4). 1 − 01 82 41 21 83 71 21 22 40 72 22 91 60 90 93 91 31 LOQ–194 mg kg The FA profiles of green algae ...... < 22 -linolenic acid (18:3 𝛼 64 4173 51 77 78 . . . . . 8 73 5 2 6 3 6) and 18 9 16 6 19 3 30 6 17 8 16 7 17 7 16 8 17 8 14 7 22 7 15 6 16 27 2 29 11 1 13 9 2 -tocopherol (10–26 and 8.8–12 mg kg n- 𝛼 Journal of the Science of Food and Agriculture Macro- and micromineral concentrations (g kg U. intestinalis Green algae C. rupestris P. umbilicalis H. elongata P. purpurea H. siliquosa P. dioica F. vesiculosus F. spiralis F. serratus P. palmata S. latissima C. flagelliformis A. nodosum M. stellatus P. canaliculata Brown algae A. esculenta L. digitata U. lactuca F. lumbricalis macroalgal species Species Ca Mg P K Na Cu Fe I Mn Se Zn Data represent mean values of twomagnesium; P, analytical phosphorus; measurements K, conducted potassium; on Na, pooled sodium; Cu, algal copper; material Fe, of iron; several I, individuals iodine; per Mn, species. manganese; Ca, Se, calcium; selenium; Mg, Zn, zinc. Red algae C. crispus Table 3. -tocotrienol: 3.8, 8.7 and 3.2 mg kg (6.2–93, 0.06–23, 0.07–179 and 𝛾 wileyonlinelibrary.com/jsfa Fatty acid profile The FA compositions of the algae studied variedthe not three only between phyla but alsothe between same different phylum. species belonging Thisallows the to is FA profiles consistent to with bedifferentiate used taxonomic previous for groups. reports chemotaxonomic analysis and to The macroalgal samples collected insuch this as study omega-3 contain fatty nutrients relevant acids, for iodine food and and vitamin feedundesirable E purposes; which elements however, can they such be alsobenefits as and contain potential Cd limitations to and the usefor As. of food the Here and species feed studied we purposes. will discuss DISCUSSION Vitamin E Brown algae had higher contents of in all samples except for the brown alga tively) compared withonly red low levels and of green algae, which contained differed from those ofresemblance brown to and the redaccordance algae FA with and previous profiles studies, showed of thestudy more green contained related higher algae concentrations of in terrestrial C16 the and plants. C18as current PUFAs linoleic such In acid (18:2 respectively). Tocotrienol was not detected or

2038 2039 S. DW) DW). In the (up to 1 1 6 − − U. intestinalis reported low levels Lead was found to (10 000 mg kg 16 1 DW) and the kelps − 6,14,16 (0.18–0.23 mg kg et al. wileyonlinelibrary.com/jsfa L. digitata (1100 mg kg Ulva lactuca The level of Cd was relatively low in green DW) and 1 13 − 6,16 and confirm that Norwegian marine macroalgae DW). Interestingly, Duinker 6,16 1 (4600 mg kg − Chordaria flagelliformis The concentrations of Hg were relatively low in all species salinity and temperature of the surrounding water,of depth, and the age thalli. Thedance iodine with previous values data found on macroalgae inworldwide collected in this Norway study and are in accor- 3mgkg studied, in line with previous findings. of Pb in the green alga current study, very high iodine contentsalga were found in the brown latissima be low in red andalgae brown were higher, algae, especially while in the its green concentrations alga in green are good sources of iodine.brown algae Among can the accumulate iodine three in high taxonomic concentrations. groups, algae compared withmacroalgae red collected in and Norway support brownlevels these of algae. findings, this as Previous lower metal datataxonomic were groups. found on in green algae than in the other Since excess iodine can causefunctions adverse of health the effects thyroid such gland, as dietaryhave dys- to uptake be of limited. these algae may Heavy metals and arsenic The heavy metals Cd, Hg andAccumulation Pb were of found in all these speciesin studied. undesirable marine elements, environments, naturally canincluding present macroalgae. easily occur in marine organisms, collected in the south of Norway during spring/summer. Variability 35 Fucus and -3 ratio and n published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. DW, the level -6/ 1 − n algal DW respectively. DW, although variabil- U. intestinalis is higher than in many 1 1 , − − ) having among the high- Thus exploring this marine 34 Major sources of iodine in Nor- wet weight (WW) on average). P. dioica 31 1 − U. intestinalis gkg Gadus morhua 𝜇 Moreover, at 5800 mg kg : 2035–2042 © 2017 The Authors. 33 32 98 2018; reached 19, 29 and 30 g kg Journal of the Science of Food and Agriculture Concentrations of heavy metals cadmium, lead and mercury and metalloid arsenic (total) in red, green and brown algae. Horizontal lines indicate -3 LC PUFA contents could improve the FA composition of n vesiculosus J Sci Food Agric In this study,high, the ranging iodine from 22 contents to of 10 the 000 mg algae kg were generally farmed fish species. Elements The species inmicrominerals this which study areposes. were relevant For for found example, both calcium to feed in contain and macro- food and pur- to prevent inflammatory,system cardiovascular disorders. Likewise, macroalgae diseases with low and nervous Figure 1. average values. high Chemical composition of Norwegian marine macroalgae www.soci.org ity among different species andand phylogenetic brown algae) groups was (red, considerable. green Thehas uptake of been iodine in shown algae to be dependent on several factors such as This indicates that eating aprovides 10 g approximately portion 24, of 36 theseommended and dry daily macroalgae 37% intake respectively of ofin calcium the Nordic for rec- countries. adult males and females est iodine contents (86 wegian foods arefish seafood, species milk such as and cod ( dairy products, with lean of iron in thewell-known terrestrial green sources alga of thisvegetables, mineral such legumes, as nuts leafy green between and 2 cereal and 4 grains, mg iron which per all 100 g. contain macroalga as a natural foodvent resource iron could be deficiency, a whichtional solution deficiencies is to in pre- one the of word. the most prevalent nutri- 46 et al. (120 g 1 LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ − < < < < < < < < < < < < < < < : 2035–2042 -Tocotrienol 𝛿 98 -tocopherol. The The presence of 𝛼 and amendments, -tocopherol, while 𝛿 2018; : 24, 0.18, 0.75 and 45 LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ LOQ 14,40,41 < < < < < < < < < < < < < -and ThepresenceofAsinfeed 𝛾 -Tocotrienol -, 44 𝛾 𝛽 -, -tocopherol range from a low 𝛼 A. esculenta 𝛿 J Sci Food Agric LOQ 0.58 0.46 LOQ LOQ LOQ . However, four species of brown algae < < < < 1 -and − 𝛾 -Tocotrienol 𝛽 -, 𝛽 -, moisture content) for ‘seaweed meal and feed 𝛼 1 − LOQ 0.21 LOQ 0.90 LOQ 0.18 LOQ 0.13 LOQ 1.06 LOQ 0.30 LOQ LOQ 0.76 LOQ 0.18 LOQ 0.19 LOQ LOQ LOQ 0.11 LOQ 0.15 LOQ < < < < < < < < < < < < < < -Tocotrienol 𝛼 (120 g kg moisture content). In the current study, all species of red and 1 1 − − level in the order Laminariales ( green algae contained Asallowed level concentrations of below 40 mg the kg EU current materials derived from seaweed’.total This As, but maximum authorities can level requestconcentrations is documentation of showing iAs set that in for feed materials are below 2 mg kg Among brown algae, the contents ofvary the four between forms close of tocopherol relatives withinthe a contents single genus. of For example, As in macroalgae has safetyfeed. However, regulations implications on As for in food their are currently use limitedEU, in and as the no food maximum allowed or levels ofvegetables As or food (either supplements total exist. As or iAs) in previous studies revealed thatreached between iAs 20 levels and in 80% of some total brown As. algae had levels of totalalgal As feed exceeding materials, thus the limiting maximum thefeed level use ingredients of allowed in these the for algal EU. species as Vitamin E Brownalgaehadhighcontentsof red and green algae contained only low levelsabundance of of tocopherols detectedaccordance in with the earlier present reports workto where contain was brown higher levels in algae of tocopherols were than green shown and red algae. in the EU is regulated by Directive 2002/32/EC which set the maximum allowedkg level of this metalloid at 40 mg kg LOQ LOQ LOQ LOQ LOQ LOQ < < < < < < 1 38 In − -Tocopherol 𝛿 15 7% of green) © 2017 The Authors. < www.soci.org I Biancarosa > ; however, 16 red published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. > -Tocopherol WW for Pb and Hg 𝛾 1 While organoarsenic − sp., with lowest metal 39 algal DW) of 21 macroalgal species 1 DW). Ulva − 1 LOQ 0.07 LOQ 0.10 0.07 LOQ 0.11 − < < < Moreover, a seasonal pattern in -Tocopherol 𝛽 as well as on macroalgae collected 6,36,37 However, in the current study, some 6,16,40 WW respectively. These levels were not 40,43 80 8.1 51 194 0.29 0.52 0.62 51 0.18 1.0 LOQ 44 10.3 15.3 82 0.20 68606765 23 14 1.8 0.29 12.9 9.3 179 5.0 144 94 30 0.26 0.13 0.16 3.8 0.88 0.33 8.7 0.14 0.10 3.2 LOQ LOQ 0.82 9313 18 0.16 20 0.10 0.83 123 0.36 1.2 0.10 0.15 26 0.24 0.25 24 0.18 0.75 0.11 9.6 0.10 0.06 6.2 0.06 0.07 8.8 NA NA NA NA NA NA NA NA 1 14.4 0.05 0.05 16.0 13.3 0.04 0.32 0.06 10.1 0.05 0.16 0.09 13.1 0.16 0.23 0.21 12.0 − -Tocopherol in which the concentration of iAs (2.4 mg kg 𝛼 Journal of the Science of Food and Agriculture Vitamin E composition (mg kg 14,41,42 H. siliquosa Levels of iAs in the species studied comprised overall Arsenic in biological matrices exists either in organic forms (e.g. Species A. nodosum Data represent mean values of twoLOQ, analytical limit measurements of conducted quantification on (0.08 pooled mg algal kg material of several individuals per species. NA, not analysed; Red algae C. crispus Table 4. C. flagelliformis F. lumbricalis F. serratus F. spiralis F. vesiculosus H. siliquosa H. elongata M. stellatus L. digitata P. canaliculata S. latissima P. palmata P. dioica P. purpurea P. umbilicalis Green algae C. rupestris U. intestinalis U. lactuca Brown algae A. esculenta total As; that is,be As mainly present in inhave organic these shown forms. macroalgae that Previous was themacroalgae studies is found most on organic. to abundant As form speciation of this metalloid in wileyonlinelibrary.com/jsfa DW) reached 10% ofmacroalgal species total from Norwegian As. waters Data are scarce on concentrations of iAs in For Pb andelements Hg, in food EU supplements (which legislationat also apply sets 3 for maximum macroalgae) and levels 0.1 mg for kg these of metal levelsseasons in and collection algae sites. can be high among different species, has been previously shown infrom studies Norwegian conducted waters on macroalgae forms are consideredregarded to as be the non-toxic most or toxic form of of low As toxicity, for iAs living organisms. is species of brownalga algae had high levels of iAs, e.g. the brown exceeded by any ofalgae the in Pb this study and (up Hg to concentrations 0.3 and found 0.01 in mg kg the respectively). arsenobetaine and arsenosugars) or as iAs. metal accumulation has been found in concentrations in spring/summer and highest in autumn/winter. worldwide. the current study, Astotal content As in and the iAs.brown Overall, samples algae higher was than levels quantified in of the as of total other total As As taxonomic in groups. were relation This to found gradation the in group of algae (brown

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