Bioactive compounds in seaweed; review, with
emphasis on available species in Danish waters
This review was funded by DTU Aqua and written by:
Susan Løvstad Holdt
Post Doc.
Division of Industrial Food Research, DTU National Food Institute
Søltofts Plads, building 221
DK-2800 Kgs. Lyngby
Denmark
suho@aqua.dtu.dk
List of content
Sammenfatning ..................................................................................................................................IV
Summary ............................................................................................................................................. V
Abbreviations and common names ....................................................................................................VI
Gallery of genera or species mentioned in this review ........................................................................ 1
Bioactive compounds in seaweed; review, with emphasis on species in Danish waters ..................... 2
Introduction ...................................................................................................................................... 2
Seaweed and background ................................................................................................................. 3
General description of the main classification of seaweed .............................................................. 4
Danish conditions and seaweed species of interest .......................................................................... 4
Salinity, halocline, tidal variations and brackish water submergence ........................................ 5
Nutrients ....................................................................................................................................... 6
Seaweed species of interest in Denmark .......................................................................................... 7
Seaweed cultivation methods ........................................................................................................... 9
Cell, callus and protoplast cultivation methods........................................................................... 9
Seeding method .......................................................................................................................... 10
Fragments of thalli ..................................................................................................................... 13
Seaweed species appropriate for large production in Denmark ..................................................... 14
Nutritional elements ....................................................................................................................... 15
Polysaccharides .............................................................................................................................. 18
Dietary fibres ............................................................................................................................. 23
Hydro- or phycocolloids ............................................................................................................ 27
Fucans/fucanoids ....................................................................................................................... 28
Digestibility of polysaccharides ................................................................................................. 28
Proteins, peptides and amino acids ................................................................................................ 31
Proteins ...................................................................................................................................... 31
Peptides ...................................................................................................................................... 34
Free amino acids ........................................................................................................................ 34
Nutritional value and digestibility of seaweed proteins............................................................. 35
Lipids ............................................................................................................................................. 36
Fatty acids .................................................................................................................................. 41
The importance of algal PUFAs ................................................................................................ 42
Phospholipids ............................................................................................................................. 43
Glycolipids ................................................................................................................................. 43
Sterols......................................................................................................................................... 44
Pigments ......................................................................................................................................... 44
Chlorophylls ............................................................................................................................... 44
Carotenoids ................................................................................................................................ 45
Phycobiliproteins ....................................................................................................................... 48
Minerals ......................................................................................................................................... 49
Vitamins ......................................................................................................................................... 53
Phenols and other phorotannins ..................................................................................................... 56
Other metabolites ........................................................................................................................... 61
Antifouling.................................................................................................................................. 61
Extracts or powder of seaweed ...................................................................................................... 64
Antioxidant effect ....................................................................................................................... 64
Peroxidation of fatty acids ......................................................................................................... 64
Other effects ............................................................................................................................... 65
Feed supplement ........................................................................................................................ 67
Plant stimuli ............................................................................................................................... 69
Heavy metals and other undesirable compounds ........................................................................... 71
Legislations ................................................................................................................................ 73
Summary and conclusion ............................................................................................................... 74
Compounds................................................................................................................................. 74
Feedstock ................................................................................................................................... 76
III
Sammenfatning
Tang kendes af de fleste som det ubehagelige snask man får mellem tæerne på stranden
og det der holder risene sammen i sushi. Men det er meget mere end det. Asiaterne har
anvendt tang som helseprodukt og lægevidenskabeligt i flere tusinde år. Det har nu fanget
vores interesse i den vestlige verden, men vi vil have videnskabelige beviser på, at det
virker. Derudover er der øget interesse for at finde alternative energikilder end fossilt
brændstof. Disse to interesser kan forenes i et såkaldt ”bioraffinaderi”, hvor man først
udnytter højværdiproduktet i et råstof og derefter ”affaldsproduktet” til f.eks. foder, energi
og/eller gødning. I et bioraffinaderi er det vigtigt at kende sammensætningen og
mængderne af råstoffet.
Tang, der er en makroalge, kan kategoriseres i grøn-, brun- og rødalger. Disse grupper og
arter indenfor en gruppe er meget forskellige også hvad angår indeholdsstoffer.
Derudover reagerer tang på det omgivende miljø, hvilket giver årstids-, habitat- og
populationsvariationer.
Denne rapport er et sammendrag af international videnskabelig forskning. Der lægges
vægt på hovedsagelig 9 arter eller grupper af tang, der findes i de danske farvande, og
som kunne have potentiale i et fremtidigt dansk ”tang-bioraffinaderi”. Indholdstofferne er
beskrevet, kvantificeret og deres bioaktivet (helsefremmende eller anden påvirkning af
celler og organismer) er sammenfattet i tabeller. Disse tabeller overskueliggør valget af
evt. interessant stof, der kunne udnyttes og i hvilke danske arter man ville kunne finde
disse stoffer. Eller hvis man har en tangart i store mængder (fra høst eller dyrkning),
hvilket stof vil man da kunne finde i denne art, og hvad er der lavet eksperimentielt på det
bioaktive stof. Derudover giver rapporten indblik i tangs fysiske og kemiske rammer,
biologi, og hvilke metoder man kan anvende til dyrkning, samt konklusioner på hvilke arter
man vil kunne dyrke i stor skala i Danmark.
Med denne rapport, hvor over 400 referencer er samlet, er der grundlag for at vi vestlinge
kan give asiaterne ret. Tang har utallige positive virkninger på vores helbred. Det er både
blevet undersøgt i ekstrakter, pulver eller på et specifikt udtræk af et stof fra tang såsom
kulhydrater, proteiner, pigmenter, fedtsyrer, phenoler. Derudover er der også de gavnlige
effekter fra kostfibre, mineraler og vitaminer, som tang har et højt indhold af. De
helsefremmende effekter er bl.a. at tang hæmmer udviklingen af kræftceller, HIV-virus,
bakterievækst, er fedmereducerende, samt sænker blodet sammenklumpningsevne og
indhold af fedt og cholesterol, der mindsker hjerte- og karsygdomme. Derudover virker
tang som antioxidant, der bl.a. beskytter de flerumættede fedtsyrer mod at blive harske
eller giftige. Rapporten giver også eksempler på anvendelsen og de gavnlige effekter af
tang i dyrefoder, som anti-begroningsmiddel, jordforbedringsmiddel og gødning.
Med den viden om, at tang på rigtig mange måder er godt for helbredet, har vi dog stadig
meget at lære om indholdstofferne, årstid- og de lokale variationer, og deres egenskaber i
den tang vi kan høste og/eller dyrke herhjemme.
IV
Summary
People usullay recognize seaweed as the “sea weed” washed ashore on the beach, or as
the wrap around the rice in sushi. However, seaweed is much more than that. The
beneficial effects of seaweed have been exploited as nutraceuticals in Asia for more than
thousand years. This has attracted attention in the Western part of the world, but we want
scientific proofs before we believe in it. Furthermore, the search for alternatives to fossil
fuels is increasing. These interests can be combined in a so called “biorefinery” in wich
the high added value products are exploited and the “waste” product used as feed, energy
and/or fertilizer. The composition of the feedstock is important together with the quantities
of which it can be provided.
Seaweed (macroalgae) is categorized as green, brown and reed algae. The composition
of the algae is different within groups and species, and furthermore varies with season,
habitat and population.
This report reviews publications of international scientific research, each made one few
species and compounds. Emphasis is made on 9 seaweed species or genera native to
the inner Danish waters and possible candidates for a biorefinery of the future in
Denmark. Compounds are described, quantified and their bioactive effect (beneficial to
health or other affect on cells and organismes) are summed up in tables. These tables
illustrate the choice of exploitable bioactive compound and in which species this
compound could be found. Otherwise, the tables are useful if seaweed feedstock is
available (harvest or cultivation) and you want to know what bioactive compound to
search for, together with the effect the compound has shown experimentally. Furthermore,
this report introduces the physical and chemical variables, biology and which methods
that can be used to cultivate seaweed. Conclusions are made on candidate species for
future large scale cultivation in Denmark.
We can now, based on this report that reviewes more than 400 international publications,
agree with the Asians. Seaweed has countless health benefits and these have been
investigated in seaweed extracts, powder and even in extractions of specific compounds
e.g. polysaccharides, proteins, pigments, fatty acids or phenols. In addition, the high
content of the dietary fibers, minerals and vitamins has beneficial effects. The inhibition of
cancer cell lines, HIV, growth of bacteria, the obesity reducing, together with the anticoagulation and lowering of serum lipids and cholesterol, which reduces the
cardiovascular diseases are just some of the mentioned effects in this review.
Furthermore, seaweed has an effect as antioxidant that among other things protects the
poly unsaturated fatty acids from becoming rancid or toxic. The applicability and beneficial
effect of seaweed used as supplement in animal feed, anti-foulant, soil enrichment and
fertilizer are also exemplified in this report.
The beneficiel effects on health from this review needs to be supported by research and
knowledge on native harvested and/or cultivated specimen of seaweed in regard to
compounds seasonal and local variations and qualities.
V
Abbreviations and common names
List of abbreviations used in this report:
13-HODE: 13-hydroxy-9,11-octadecadienoic acid
13-HODTA: 13-hydroxy-6,9,11,15-octadecatetraenoic acid
15-HETE:15-hydroxy-5,8,11,13-eicosatetraenoic acid
Aa: Amino acids
ALA: α-linolenic acid (18:3 n-3)
Bb: The Baltic surrounding Bornholm (Østersøen omkring Bornholm)
Bm: The middle of the Baltic (Østersøen midt)
Bw: The western Baltic (Østersøen vest)
Comm: Commercial scale
DHA: Docosahexaenoic acid (22:6 n-3)
DGDG: Diglycosyldiacylglycerol
Dw: Dry weight
EPA: Eicosapentaenoic acid
Exp: Experimentally
HDL: High-density lipoprotein
Hijiki/hiziki: Sargassum fusiforme, formerly known as Hizikia fusiforme
Ke: The eastern Kattegat (Kattegat øst)
Kelp: Large brown seaweed
Km: The middle of Kattegat (Kattegat midt)
Kn: The northern Kattegat (Kattegat nord)
Ks: The southern Kattegat (Kattegat syd)
Lb: The Little Belt (Lillebælt)
LC-PUFA : Long chained polyunsaturated fatty acids
LDL: low-density lipoprotein
Lf: The Liim Fiord (Limfjorden)
MGDG: Monoglycosyldiacylglycerol
n-3: Omega 3: α-linolenic acid family (n-3 fatty acid)
n-6: Omega 6: linoleic acid family (n-6 fatty acid)
No ab: No abundance
Nori: Porphyra sp.
Ns: The North Sea (Nordsøen)
PA: Phosphatidic acid (glycerol-containing phospholipid)
PC: Phosphatidylcholine (glycerol-containing phospholipid)
PE: Phophatidylethanolamine (glycerol-containing phospholipid)
PI: Phophatidylinositol (glycerol-containing phospholipid)
PLs: Phospholipids
PS: Phosphatidylserine (glycerol-containing phospholipid)
Pilot: Pilot scale
PUFA : Polyunsaturated fatty acids
Sa: The waters surrounding Samsø (Farvandet omkring Samsø)
Sb: The Great Belt (Storebælt)
Sf: The archipelago of Southern Funen (Det sydfynske øhav)
Sk: Skagerak
Sm: The sea surrounded by (the islands of) Zealand, Møn, Falster, and Lolland (Smålandshavet)
Sp.: One species within the genera
SPH: Sphingomyelin (phospholipid, consisting of sphingosine and phosphatidylcholine)
Spp.: More than one species within the genera
Su: The Sund/ Oresund (Sundet/ Øresund)
Wakami: Undaria pinnatifida
Ww: wet weight
VI
Gallery of genera or species mentioned in this review
(examples; drawings by Holdt, 2010)
Laminaria/Saccharina
Laminaria digitata
Undaria
Undaria pinnatifida
Chondrus crispus (top)
Porphyra sp. (bottom)
Fucus
Fucus serratus
Sargassum
Sargassum muticum
Gracilaria
Gracilaria sp.
Ascophyllum
Ascophyllum nodosum
Ulva
Ulva sp.
Palmaria
Palmaria sp.
Bioactive compounds in seaweed; review, with
emphasis on species in Danish waters
Introduction
Seaweed is more than the wrap that keeps rice together in sushi. Seaweed biomass is
already used for a wide range of other products in food including stabilising agents.
Biorefineries with seaweed as feedstock are attracting worldwide interest and include the
low volume high added value products and high volume low value products.
Scientific research on bioactivity of seaweed usually takes place on few species
and compounds. This report reviews worldwide research on bioactive compounds mainly
performed at nine genera or species of seaweed, which are also available in the Danish
waters: Laminaria sp., Fucus sp., Ascophyllum nodosum, Chondrus crispus, Porphyra sp.,
Ulva sp., Sargassum sp., Gracilaria sp. and Palmaria palmata. In addition, Undaria
pinnatifida are included in this review as this is globally one of the most produced,
investigated and available species. However, not present in the waters of Denmark.
This review will supply fundamental information for biorefineries of the future
based on seaweed feedstock from Denmark. The preliminary selection of one or several
candidate seaweed species will be possible based on the summarizing tables and
previous research desribed in this report. This applies to the choice of either high added
value bioactive products to be exploited in an available species, or selection of seaweed
species when a bioactive compound is desired. Data are presented in tables with species,
effect and test organism (if present) with examples of uses to enhance comparisons. In
addition, scientific experiments performed on seaweed used as animal feed are presented.
The biology and technology of seaweed cultivation techniques are also described,
together with the physiology and chemistry of the marine environment in the inner Danish
waters.
The conclusion summarizes the potential exploitation of seaweed species in
regard to biochemical composition, characteristics and also possible large scale
production in the future.
Sargassum sp. (photo: Holdt, 2010)
2
Seaweed and background
Seaweed (macroalgae) is an “organisation of microalgae” with cell differentiation. This
multicellular algae has structures such as stem, fond, reproductive structures etc
depending on species. Exchange of gases, nutrient uptake and photosynthesis is possible
on the entire surface and thalli of the seaweed. The holdfast only works as a structure to
stay in the same location, and not as a root that we know from higher plants.
Natural populations of seaweed have worldwide been harvested for food
supplements, soil enrichment or sold for many years. Furthermore, seaweed has been
collected at shore and used as soil enrichment by locals in Denmark in hundreds of years.
Natural drifting populations of Furcellaria lumbricalis organised by currents in the sea was
harvested by nets by fishermen and sold for extraction of “Danish agar” as late as the
1970’s. Hand raked seaweed sold for production of grinded soil enrichment or fluid
fertilizer is still a business in e.g. Canada (Acadian Seaplants Limited, Nova Scotia) and
Ireland (Arramarra Teo). However, natural populations are subject to over-exploitations,
and cultivation of seaweed is therefore needed to meet the increasing demand of the
market.
Seaweed is used as food (about 150 species) and for phycocolloids, thickening
and gelling agents for various industrial applications including food (more than
100 species) worldwide (Kumar et al., 2008b).
Seaweed production is not a new invention, and techniques for growing and
harvesting seaweed were developed centuries ago in China and Japan (Guist, 1990). The
worldwide commercial seaweed production accounts for 20 % of the total aquaculture
biomass production; marine and fresh water land- and offshore production (including fish,
mussels etc.). The main seaweed species produced worldwide are the brown algae
Undaria pinnatifida (wakame), Laminaria japonica (kombu) and the red algae Eucheuma
cottonii1 (Zanzibar weed), Gracilaria verrucosa and Porphyra tenera (nori). Most kelps
(large brown seaweed) are more or less edible, but the two genera that are most important
economically are Undaria and L. japonica. Undaria has been a foodstuff of great
importance and high value in Japan since about A.D. 700 (Lobban and Harrison 1994).
Asia is the sovereign producer of 99.7 % of the total world seaweed production. In
Asia, China is the supreme producer with 67 % of the total Asian and also world wide
production, Korea (Dem. People Rep. and Republic of Korea) with 10 %, Indonesia with
7 % and Japan with 4 % (FAO, 2008)2. In addition to the biotechnology industry producing
large amounts of seaweed, the Chinese industry also includes phycocolloids (algin, agar
and carrageenan), chemicals and drugs (such as iodine, mannitol, phycocyanin, βcarotene, propylene glycol alginate sulfate and fucose-containing sulfated
polysaccharides) and food, feed and fertilizer (Tseng, 2001).
1
Eucheuma cottonii is the expression used by the industry for the species Kappaphycus alvarezii
In this review Laminaria spp. may be used as description of both genera Laminaria and Saccharina
acknowledging the recent proposal of dividing the genus Laminaria into these two genera. This is however
confusing when previously studies describes the species or groups by other names. Sorry for the confusion
when both genera are mixed when mentioned in this review.
2
3
General description of the main classification of seaweed
Seaweed species are divided into 3 main classes; brown algae (Phaeophytes), green
algae (Chlorophytes) and red algae (Rhodophytes).
Brown seaweed: The brown colour of these seaweed result from the dominance of the
xanthophyll pigments as for example fucoxanthin, that masks other pigments as
chlorophyll-a and –b, β-carotene and other xanthophyll (zeaxanthin). Storage of brown
seaweed is typically made of complex polysaccharides, sugars and higher alcohols. The
walls of these algae contain alginic acid, a long chained heteropolysaccharide, and fucan,
a sulphated fucose. True starch is absent (Table 1). There are 2,200 species and the
majority of brown seaweed is found in cold water and some species belongs to the families
Sargassum, Porphyra, Undaria, Sargassum and Fucus (Kumar et al., 2008b).
Red seaweed: The red colour of these algae results from dominance of the pigments
phycoerythrin and phycocyanin. Their walls are made of cellulose, agar and carrageenan
(Table 1). Both these long chain polysaccharides have wide spread commercial use.
There are about 6,500 species of red algae and some of the typical species are of the
families Gracilaria, Gelidium, Eucheuma, Porphyra, Acanthophora and Palmaria (Kumar et
al., 2008b).
Green seaweed: The green colour of the algae is due to the chlorophyll a and
chlorophyll b. The green algae are the only which have cell walls consisting of starch. The
storage compounds are mannane, ulvane, xylan, cellulose (Table 1). Typical examples of
species are from the families Ulva, Monostroma and Caulerpa (Kumar et al., 2008b).
Table 1: Storage and cell wall carbohydrates of green, red and green seaweed.
Brown seaweed
Red seaweed
Green seaweed
Storage
Cell walls
Laminarin (β-1, 3 glucan)
Floridian starch (amylopectin like glucan)
Starch
Alginate, fucans, cellulose
Agar, carrageenan, xylan, cellulose
Mannane, ulvane, xylan, cellulose
Biochemical composition of seaweed not only varies
between the 3 classes, but also varies with species,
habitat, maturity, salinity, temperature, irradiance,
environmental condition and even within specimen in
the same populations (Pavia and Åberg, 1996;
Floreto and Teshima, 1998).
Danish conditions and seaweed species of
interest
The inner Danish waters are a somewhat different
habitat compared to other coastal areas. The inner
Danish waters have “unique” physical factors such as
a salinity gradient, no tidal water level variations and
a halocline separating the high and low saline water
in the water column.
Boulders with seaweed (photo: Holdt, 2010)
4
Salinity, halocline, tidal variations and brackish water submergence
Salinity is the saltiness or dissolved salt content of a body of water and can be measured
by a refracometer (measures the light reduction inside a medium). The salinity gradient in
the inner Danish waters ranges from the high saline waters in the North Sea towards the
low saline Baltic in the South East direction. The Baltic is low saline because of river
outlets in this large estuary, the Baltics. The highly saline water from North is transported
towards South and the low saline water from South are transported from the Baltic towards
North. The density of high saline water is higher than the low saline. These waters are not
easily mixed and a distinct halocline is created in the in the Southern inner Danish waters
and the narrow strait between Denmark and Sweden (Øresund) especially during summer.
Tidal variations of water level are only found on the West coast of Jutland, but not in the
inner Danish waters. Water level variations can however be caused by currents and wind,
but usually not more than 0.5 m variations. The depth of the haloclines depends on
currents, winds and precipitation and needs strong autumn storms to create enough
turbulence to mix the “two” waters.
The number of seaweed species decreases with the decrease in salinity. This is
exemplified in Figure 1. Seaweed species are distinguished on the basis of their
responses to salinity variations. The first group shows no significant changes in respiration
rate with changing salinity, whereas the second group reveals considerably increased
intensities of respiration with decreasing salinity. The first group is represented, for
example, by Enteromorpha species, Fucus vesiculosus and Porphyra laciniata, the second
by F. serratus and Laminaria digitata. Increased respiratory rates, because of reduced
salinities, cause a reduction in final body size and in the number of species per habitat.
Higher respiratory rates lead to enlarged losses of organic matter produced by
photosynthesis. Consequently, the existence of marine algae in brackish water appears to
be limited by some kind of starvation (reference in (Gessner and Schramm, 1971; Nygård
and Dring, 2008)). As all marine plants require certain minimum salinities they tend to
follow the deep salt-water layers when entering coastal waters. This is called “brackish
water submergence” (Gessner and Schramm, 1971).
Various fucoids and other marine seaweed that occur in the Baltic also occur in
the North Sea. Although the populations in the Baltic have consistently lower salinity
optima, their thalli organisation differs from that of their open-coast counterparts in diverse
ways. Some have small thalli but similar-sized cells; some have smaller cells but not
smaller thalli; some have only certain cells reduced in size (Russell, 1988). The reduction
in body size is a rather general phenomenon in marine plants inhabiting with progressively
decreasing salinities. The tendency towards dwarf forms may be due to individual nongenetic adjustments, or to selection, or both (Gessner and Schramm, 1971).
Lowered salinity also promotes changes in the chemical compositions of
seaweed. Mannitol, ash, and chloride contents declines, as does dry weight as percentage
of fresh weight, whereas protein concentration increases (Munda and Kremer, 1977).
5
Figure 1. Horisontal distribution of selected algal species in the Hardanger and Sör
Fjords in Norway (the broken line shows the Sör Fjord turned to the right). In the lower
part of the figure, solid lines indicate common, broken lines scattered occurence
(Gessner and Schramm, 1971).
Nutrients
The ambient nutrient concentrations in the inner Danish waters are higher in autumn,
winter and spring (up to 30 μM dissolved inorganic nitrogen (DIN)) compared to summer
concentrations (less than 1 μM DIN) (Pedersen and Borum, 1996; Holdt, 2009). The high
productivity of especially microalgae and cyanobacteria/blue-green algae increases,
because of increased sunlight for photosynthesis, in late spring and summer. Nutrients
and especially nitrogen become limited in late summer, because most is bound in
microalgae biomass. The nutrients are available again in autumn, when the microalgae die
and the mineralisation of this biomass releases the nutrients. Storms in the autumn will mix
the water column that can have been stratified during late summer, and thereby make
nutrient accessible in the surface water layer. The stratification is caused by warmer
surface water during summer and colder bottom layers and also because of the halocline.
The bottom layer can be non-oxid, because of the mineralisation of algae by bacteria at
the sea floor.
6
Seaweed species of interest in Denmark
The seaweed of interest in Denmark has been selected by the criterias such as interest,
availability, producability or quantity of species. The main groups (genera or species) of
seaweed are listed in Table 2. Undaria a non-indigenous species have been added to the
species of interest as a reference species with a lot of impact and widely examined, as this
species account for one of the largest productions worldwide. Table 2 shows the
abundance, edibility, Danish species within genera, cultivation methods of the selected ten
species.
As mentioned, the number of species decreases towards the Baltic Sea, due to
the gradient in salinity with high in North (Sk and Kn in Figure 2) to low towards the Baltic
Sea (Bp).
Figure 2. Categorized regions in Denmark. Abbreviations shown in the
abbreviation list (Larsen and Hansen, 1986).
Gracilaria vermiculophylla (photo: Holdt, 2010)
7
Table 2. Worldwide cultivation and natural harvest, growth pattern, specific growth rate and abundance of seaweed species of interest in Denmark.
Species of interest
Brown seaweed
(Phaeophyta)
Fucus
Ascophyllum
Undaria
Sargassum
Ulva
Chondrus
Porphyra
Gracilaria
Palmaria
Danish species
within this group
Size
Growth zone
Specific Growth
Rate (/d based
on biomass)
Cultivation
method
Ephemeral or
perennial$
Red seaweed
(Rhodophyta)
√
√
√
-
√
-
√
-
√
√
Exp
Comm
-
-
Comm
-
Pilot
Comm
Comm
Exp
Comm
Comm
Pilot
Comm
Comm
Comm
Bb
Bp
Ks
No ab
Lf
Bm
Bm
Su
Sa
Bm
8-33 ‰
4‰
8-33 ‰
8-33 ‰
10-33 ‰r
8-33 ‰
Yes
Kombu
(L. japonica)
Yes
(no common
name)
Livestock
supplement
(A. nodosum)
Yes
Wakami
(U. pinnatifida)
Yes
Nori
(Porphyra
sp.)
F. vesiculosus
F. serratus
F. spiralis
0.5-1 m
Ascophyllum
nodosum
-
Yes
(mostlly agar
extraction)
(no common
name)
G. vermiculophylla
(invasive sp.)
Yes
Dulse
(P. palmata)
L. digitata
Saccharina
latissima
<4 m
Yes
Hana-nori™
(C. crispus,
mostly for
extraction)
C. crispus
0.3-1 m
0.3-1m
0.1-0.2 (0.5)m
Intercalary
(between stipe
and thalli)
Tanks in lab:
0.02p
Field: 0.07 in
area c 0.15 in lengthg
(4-10 kg/m
rope)
Seeding
Terminal
Laminaria/
Saccharina
Harvest (natural
population)
Cultivated
Tanks
Sea
Abundance goes
as South as*
Salinity range in
Denmark q
Edible/
Common name
Green
(Chlorophyta)
perennial
Yes
Hijiki
(S. fusiforme,
former Hiziki
fusiforme)
S. muticum
(invasive sp.)
Yes
Green laver
(Ulva sp.)
-
2-4 m
0.05-0.2 m
Terminal
Intercalary
Terminal
<0.2 m (larger if
free floating)
All cells in thalli
Terminal
All cells in
thalli
Terminal
Intercalary
Tanks in
laboratory:
0.01-0.015p
Field: 0.02 in
lengthj, 0.010.26 cms
Lab: 0.13 t
Field: 0.06
0.07 in lengthh
Field: 0.07??,
Lab; 0.21t
Tanks: 0.04k
0.12o
Bioreactor:
0.10a
Tank: 0.06d
Field: 0.02 a 0.04 e
Laboratory:
0.26l
Laboratory:
max 0.11m
Tanks: 0.04n
Field: 0.04 a -0.07 b
Field: 0.07 in
area c-0.08f
(0.6 kg/m
rope)f
-
-
Seeding
-
Vegetative and
seeding
Seeding
Vegetative
(seedling tested) a
Seedling
perennial
perennial
perennial
ephemeral/
perennial
ephemeral
Vegetative
(seeding
tested) a
perennial
ephemeral
perennial
perennial
U. lactuca
P. purpurea
P.umbicalis
P. linearis
0.05-0.3 m
P. palmata
Exp=experimentally, Pilot= pilot scale, Comm=commercial scale, No ab=no abundance in Denmark. Ephemeral means “existing only seasonally”. Perennial means “existing more than two years”. *Abbreviations refer to Figure 2 (Larsen
and Hansen, 1986). The region noted is the most South-East region the seaweed species is abundant. $ Ephemeral means that the thalli decayes after one season, but some holdfast survives during winter and the next season the thalli grow
from that. a= (Holdt, 2009), b= (Troell et al., 1997), c= (Makarov et al., 1999), d= (Simpson et al., 1977), e= (Chopin et al., 1999b), f= (Edwards, 2007b), g= (Buck and Buchholz, 2004b), h= (Choi et al., 2007), I= (Wernberg-Møller et al.,
1997), j= (Stengel and Dring, 1997), k= (Msuya et al., 2006), l= (Pereira et al., 2006), m= (Zhou et al., 2006b), n= Haglund et al 1993, o= (Neori et al., 1991), p= (Gordillo et al., 2002), q= (Athanasiadis, 1996), r= (pers. comm.. Nejrup,
2010), s= (Haddad and Ormond, 1994), t= (Steen and Rueness, 2004)
8
Seaweed cultivation methods
Cell, callus and protoplast cultivation methods
The cell and callus cultivation methods are often used in order to retrieve morphological
and genetically similar cultures of macroalgae and/or to reduce contaminants. Either by
isolation techniques where single cells are excised from field collected thalli and
recultured, or by callus induction and shoot tissue regeneration. The latter method,
undifferentiated cell filaments grow away from the cut face of a thallus explant and these
shoot tissues are regenerated into micro plantlets. This tissue does not fully regenerate
into an intact plant with asymmetric thallus stem and holdfast structures, however
emanates from a common centre and shoots symmetrically in liquid cultures (Rorrer and
Cheney, 2004d). These method has been tried on Saccharina latissima (Qi and Rorrer,
1995: Rorrer et al., 1995), Agardhiella subulata (Huang and Rorrer, 2002a+b),
Acrosiphonia coalita (Rorrer et al., 1996), Laminaria japonica (Gao et al., 2005; Gao et al.,
2006), Undaria pinnatifida (Xu et al., 2002) and Kappaphycus alvarezii (Munoz et al.,
2006).
Protoplasts are living plant cells without cell walls which offers an unique uniform
single cell system that facilitates several aspects of modern biotechnology, including
genetic transformation and metabolic engineering (Reddy et al., 2008). The proceedure is
performed on seaweed tissue without reproductive structures. Enzymes are added for
digestion of cell walls (e.g. agarase for red and alginase for brown seaweed). The
protoplast isolation is commenly done by filtration of the digestion mixture and gentle
centrifugation. Cell wall regeneration is done when the protoplasts are cultivated in media
used for seaweed tissue cultivation with addition of osmoticum (mannitol, sorbitol)
((Baweja et al., 2009). Pretreatment of thallus with proteases can leed to higher yields (ref
in (Reddy et al., 2008)). The protoplast method has mostly been investigated on red algae
species (41), followed by green (24) and brown species (24) (Reddy et al., 2008).
Mass cultivation of Chondrus crispus has been attempted several times in outdoor
tanks, but has only been profitable for Acadian Seaplants Limited (Canada). This massive
production is based on small cut offs from a mother plant kept in a laboratory, and this
vegetative reproduction gives almost morphologically identical thalli sold as Hana-nori™
for food applications to the Japanese (pers. comm. Hafting, Acadian Seaplants, 2008).
However, these techniques are usually performed for cultivation in bioreactor.
Bioreactors can be used as an engineered platform for either basic research,
production of high value natural products as secondary metabolites, or for bioremediation
of nutrients or contaminants in effluents or fresh and marine waters (free after (Rorrer and
Cheney, 2004c). Bioreactors are mainly used for microalgal production and different
designs such as open and closed system bubble column photobioreactor, externally
illuminated stirred tank and flat and tubular etc. (Eriksen et al., 1998; Eriksen, 2008). Some
of these designs have also been tested for macroalgal cultivation (Zhi and Rorrer, 1996;
Rorrer and Cheney, 2004b; Gao et al., 2006b; Holdt, 2009). Bioreactors can give the
cultivated organism optimal conditions and each variable can be changed one at a time to
study the effect. However, optimal physio- and chemical conditions for e.g. the
investigated macroalgae will also be a suitable environment for growth of undesirable
contaminants such as bacteria, microalgae etc. The effect of these undesirable
9
contaminants may also be expressed in the results of basic research or disturb the
production of high valuable products.
Reductions of such contaminants are not easy in macroalgal cultivation but can
be addressed in different ways; A) Cell and tissue culture including microscopic
gametophytes, undifferentiated callus filaments and “microplantlets” regenerated from
callus (Rorrer and Cheney, 2004a), B) Treat the macroalgae with chemicals and antibiotics
to eliminate growth of diatoms, other microalgae, bacteria and epiphytes (Garcia-Jimenez
et al., 1999; Choi et al., 2002), C) favour the growth of the cultivated species by increasing
density and thereby reducing light penetration eliminating growth of epiphytes (Bidwell et
al., 1985; Lüning and Pang, 2003), D) reducing the amount of nutrient e.g. by pulse
feeding, minimizing survival of fast growing microalgae or ephemeral macroalgae (Bidwell
et al., 1985; Pedersen and Borum, 1996), and last E) introducing grazers that do not harm
the cultivated macroalgal species (Shacklock and Doyle, 1983).
Applications of the bioreactor is reported for cultivation of the high value products
such as the secondary metabolites (antiviral), fatty acids or for transgenic productions of
e.g. genes encoding for antigens (Rorrer et al., 1997b; Cáceres et al., 2000; Gao et al.,
2006a; Queiroz et al., 2008).
The final application in which the photobioreactors are used is for microalgal
bioremediation of effluent from aquaculture (Christensen, 2007).
Seeding method
The seeding method consists of spores released from the reproductive structures of the
macroalgae and the spores settle and germinate on a substrate. In species such as
Gracilaria, Chondrus crispus and Palmaria reproductive thalli are placed above the
substrate in a tank. The spores either swim or passively settle, depending on the species,
to the substrate below when they are released. Alternatively, spores are collected in
suspension, matured and sprayed on the substrate (Arbona and Molla, 2006; Edwards,
2007a; Holdt, 2009).
The seeding method has several advantages, however also some disadvantages
(Oliveira and Alveal, 1990; Glenn et al., 1996):
The advantages are:
 Less seed stock from natural collected plants
 Less labour intensive to inoculate
 There can be selection for life phases with best properties
 Reduction in epiphytes introduced
Disadvantages:
 Fertile specimens are required
 Larger genetic variability with sexual reproduction
 Laboratory and tanks are needed
 Possible several life phases
 Slow initial production due to low biomass inoculated
 Unpredictability in spore survival, competition for space with other organisms and
sporelings being grazed upon
Less natural collected plants are needed as inoculum in the seeding method, and the
labour intensity of the collection of stock culture is therefore reduced. Furthermore,
10
undesired species such as epiphytes are also reduced, as the “old” thalli with possible
epiphytes are not transferred and cultivated. The life phase of the macroalgae may be
important. Especially for the species Chondrus crispus, because the gametophyte has the
best gelling properties and are therefore of most value (McCandless et al., 1973; Garbary
and DeWreede, 1988; Roberts and Quemener, 1999). In addition, the labour intensity are
reduced with the sporulation technique compared to the conventionally method where
thalli are inserted into ropes (see paragraph on fragments of thalli). This is especially
important in countries like Denmark with expensive labour.
Spore settlement can be done on a variety of substrates; hard, soft or strings as tested for
tetraspores of C. crispus in (Holdt, 2009). The method with spores seeded on string or net
for out planting to the field has been tried for a range of species e.g. Palmaria palmata,
Gracilaria chilensis, G. parvispora, Alaria esculenta, Saccharina latissima and Porphyra
sp. The latter species Porphyra (nori) has been cultivated with this method for e.g. sushi
wrap in Japan, China and Korea for centuries (Figure 3; (Glenn et al., 1996; Alveal et al.,
1997; Sahoo et al., 2002; Buck and Buchholz, 2004a; Arbona and Molla, 2006; Edwards,
2007a; Blouin et al., 2007b).
Figure 3. (a) Spores from Palmaria palmata settled on vinylon/kuralon string (2 mm in diameter),
(b) spores germinated in 3 weeks in nursery tanks with added nutrient and aeration and transferred to
the field at this stage, (c) harvestable thalli after 4 months of field cultivation (a-c seeded and
cultivated by Maeve Edwards). (d-e) Seeded string with Alaria esculenta coiled around culture rope
and (f) Alaria afer approximately 120 days culture at sea (Arbona and Molla, 2006).
Nurseries with tanks and even a laboratory are needed for the seeding method. The
settled spores have a lag-phase before upright shoots and need some shelter before being
exposed to the field environment for better success. Spores can be seeded on a thin string
to minimize space in the nurseries, during transport and ease handling. The string can
then be coiled around a culture rope that can carry the increasing biomass during
cultivation when transferred to field. The holdfasts of the seaweed will attach to the culture
rope as the seaweed grows (Figure 3; (Arbona and Molla, 2006).
11
Some species such as Porphyra spp. even have several life phases to be nursed as the
conchocelis phase on shells, which take up even more space and nursery time (Sahoo et
al., 2002; Blouin et al., 2007a).
Fertile specimens are required for spore release; however this is usually not a
problem as the reproductive structures are easily recognised as either dark spots or buds
on the thalli. Some species such as P. palmata and S. latissima can even be induced to be
reproductive. Sporogenesis and cultivation can therefore take place year round and not
only during the repdoductive season of the seaweed species (Pang and Lüning, 2004a;
Pang and Lüning, 2006). Spore release is usually for sexual reproduction which means
that there will be genetic variability; healthy for the genetic pool, for the survival in different
environments and also to avoid herbivores, pests or diseases such as “ice ice” in
Kappaphycus alverezii (Ask and Azanza, 2002).
Auxenic (clean) cultures can be obtained from isolation of the unicellular reproductive
cells (e.g. zoospores, gametes, tetraspores and carpospores), although numerous
bacteria, fungi and epiphytes are attached to the surfaces of the reproductive as well as
the vegetative thalli. While these contaminants might be killed and removed by various
antibiotics, it may be impossible to completely eliminate them, because they can penetrate
into the algal cell wall (see details in (Kawai et al., 2005).
Strings and nets are mostly used for cultivation in field. Several cultivation systems
for seaweed production in the field have been designed and tested, ranging from the
simple long line to ladder or grid with floats or even the more robust offshore ring structure
(some structures are presented in Figure 4). Systems can be site specific and work
optimally in some areas, whereas they are not suited in others depending on tides,
currents etc. In the massive Porphyra cultivation culture nets are seeded with concospores
and attached horizontally to semi floating rafts, and harvested by boats that can lift the
nets above them (Sahoo and Yarish, 2005).
Figure 4. (2) System designs for Laminaria culture tested within the area of Helgoland farm.
(A) Longline construction with perpendicular culture unit. (B) Ladder construction, with culture lines
knotted between the “steps”. (C) Grid design with rectangular culture units. (3) The successful patented
ring design for the culture of Laminaria at offshore locations. The major elements of the system design
are magnified (A,B,C)(Buck and Buchholz, 2004a; Buck and Buchholz, 2005).
However, all systems are more or less labor demanding, and there is a need for the
development of a mechanized technology to operate the systems with less labour for
inoculation and harvesting if seaweed production should be of profit in countries with
expensive man power.
12
Fragments of thalli
Mass cultivation of seaweed is still very much based on vegetative (asexual) reproduction
and especially for commercially interesting species such as Kappaphycus alverezii
(Eucheuma cottonii) Gracilaria spp. and Undaria spp. (Oliveira and Alveal, 1990; Ask and
Azanza, 2002; Sahoo and Yarish, 2005; Pereira and Yarish, 2008). In this method,
fragments of thalli collected from natural stock sources or from previous
cultivations/harvests are used as inoculatum in tank, pond or field systems. Different
species of seaweed have more or less differentiated cells e.g. with or without stipe
structure, branching of fronds and with apical or meristematic (intercalary) growth
(Table 1). This leads to different ways for preparation of thalli fragments to still include
growth zones in the fragments.
Chondrus crispus (photo: Holdt, 2010)
Tank or pond systems for thalli cultivation are usually provided with air-lift for mixing of
media to decrease the laminar layer for increased gas exchange and nutrient uptake and
to reduce epiphyte growth mechanically by the friction effect. Air-lift also reduces
decomposition of particulate material on surface of the thalli, which will lead to rotting of
thalli. In addition, biomass can be increased when bubbles keep thalli in suspension,
creating dark and light regimes (intermittent light, Figure 5, (Pang and Lüning, 2004b)).
Figure 5. Cross section of different kinds of tanks used to cultivate seaweed. The circulation of the algae
is given by air bubbling, or by paddlewheels as depicted in the sketch at the right (Oliveira and Alveal,
1990).
13
The design of the field cultivation system for production with thalli as inoculate is usually
long lines, and deployed on designs presented above (Figure 4). Several other designs
are also proposed or in use such as; inside nets or net bags (Browne, 2001), inside net
tubes (Zertuche-González et al., 2001) or plastic tubes filled with sand, anchored on the
sea floor (attached/tied to hard substrates or inserted in the soft sea floor with a stick).
Many of the methods are described in (Oliveira and Alveal, 1990; Sahoo and Yarish,
2005).
Thalli are usually inserted in the twist of the rope or tied onto the rope with a cable
tie or a small string (“tie tie”; Figure 6).
Figure 6. (a) Fragments of Gracilaria vermiculophylla thalli inserted in the twist of the rope with help by
the tool shown, (b) Eucheuma cottonii tied on cultivation ropes with a small string (“tie tie”), and (c)
cultivated in a simple setup with sticks inserted in the sandy sea floor near the beach and the ropes
stretched in between (Bali, Indonesia). The seaweed is deployed and harvested at low tide (pictures by
Holdt).
Seaweed species appropriate for large production in Denmark
The Danish seaweed production conditions would include high labor costs and as
mentioned a salinity gradient towards south in the inner Danish waters. This means that
highly appreciated properties of seaweed for productions are:
 Low salinity endurance
 Low labor intensity
 High specific growth rate for a fast and large production
 Autumn, winter and spring production
Open sea cultivation would have the lowest production costs for large scale production
compared to laboratory, bioreactor and also outdoor tanks, because these have higher
demands of equipment, maintenance, attention, and requirements of land-space.
Seaweed production in the open sea would be preferred beginning in autumn. In
this season the nutrients are naturally occurring in the sea water in higher concentrations
compared to summer. However, during summer a fish farm could act as a nutrient source.
Seaweed exploits the sunlight for photosynthesis during summer. Some species like
Laminaria/Saccharina exploit this sunlight eventhough minimal nutrient storage for survival
and growth is present. In this period the seaweed produces a lot of storage
polysaccharides from photosynthesis and when the nutrient concentration increases in
autumn the seaweed produces proteins, amino acids and increases in size/area. These
seasonal variations in biochemical composition should be considered when planning the
production and/or harvest of biomass. Another difficulty in cultivation is biofouling of other
14
organisms. Many other organisms (other macroalgae and invertebrates) release larvae or
spores during summer, and these will settle on any available substrate; ropes, strings,
bags and even the seaweed etc.
Some of the species mentioned in Table 1 are ephemeral and for only one
seasonal production. This seasonal growth is often during summer, such as Sargassum
and Ulva species.
The seedling method is the most appropriate regarding keeping labor time at the
lowest, and not having to harvest large amounts of naturally occurring seaweed. This
would favour species with a well known and “easy” lifecycle. This may exclude species as
Porphyra spp. that as mentioned have several life phases such as the conchocelis phase on
shells.
Fucus and Gracilaria would be best suited in regard to low salinity. However,
Gracilaria is an invasive species and this species should probably be harvested from
“natural populations” if exploited in Denmark. Laminaria/Saccharina, Palmaria, and Ulva
are fast growing species with well known lifecycles. Laminaria/Saccharina species even
have controllable lifecycle, and with inducible spore production. Ulva is fast growing, but
ephemeral and decays late autumn.
Taking these arguments into account the Laminaria digitata, Saccharina latissima
and Palmaria palmata may have the best potential for large open water production in
Denmark. However, natural populations of these species submerge in the Southern inner
Danish waters if the salinity is below their requirements. The production lines should
probably be submerged if seaweed cultivation is located in the south of Denmark,
compromising on the available sunlight for photosynthesis.
Nutritional elements
Seaweed is known for their richness in polysaccharides, minerals and certain vitamins
(Arasaki and Arasaki, 1983), but also contain bioactive substances like polysaccharides,
proteins, lipids, minerals and polyphenols with properties within antibacterial, antiviral and
antifungal among many others (Kumar et al., 2008b).
The nutrient composition of some seaweed and vegetables are shown in Table 3
(Murata and Nakazoe, 2001).
Saccharina latissima (photo: Holdt, 2010)
15
Table 3. Chemical composition of seaweed and vegetables (g/100 g) (Murata and Nakazoe, 2001). The
values refer to the analysed data of products available in the market. The seaweed products are therefore low
in moisture content.
Moisture
Protein
Lipid
Carbohydrate
Fiber
Ash
11.1
38.8
1.9
39.5
1.8
6.9
7.3
18.1
0.3
53.9
6.3
14.1
13.0
15.0
3.2
35.3
2.7
30.8
13.6
10.6
1.3
47.0
9.2
18.3
92.4
12.5
13.5
1.4
40.3
10.5
0.1
21.7
3.0
4.9
27.1
69.3
0.6
5.7
2.1
0.6
5.0
1.6
Porphyra comples
(Amanori)
Enteromorpha intestinalis
(Aonori)
Undaria pinnatifida
(Wakame)
Hizikia fusiformis
(Hiziki)
Cabbage
Soybean
Wheat
Seaweed biomass contains all the human body needs including vitamins, minerals and
trace elements, however not enough energy to live solely on seaweed as food. The lipid
content is low and even if the carbohydrate content is high most of these are dietary fibres
(see chapter below). Dietary fibres are good for the human health as it makes an excellent
intestinal environment, however low from a nutritional perspective because not many of
the carbohydrates are taken up by in the body (Mouritsen, 2009).
The moisture content of fresh marine algae is very high, and accounts for up to
90 % of the biomass (Table 4). Marine algae are usually sold dried or salted (from 7 to
20 % moisture) in order to preserve the food (see also Table 3). Though marine algae
contain nutritional elements such as proteins, lipids, carbohydrates, vitamins and minerals
as in the case of other plants, the content of these elements varies depending on the
season and the area of production (Murata and Nakazoe, 2001; Connan et al., 2004;
Marinho-Soriano et al., 2006; Khan et al., 2007; Zubia et al., 2008).
Table 4. Moisture (% of wet weight) and ash content (% of dry weight) of the seaweed species of interest
19 % g
25 % j
30 % h,i
18-27 %k
27 % I
31 %m
39 % h
40 % i
14 % x
44 % v
78 % s
80 % g, å
72 % ø
7278 % ω
77 % g
86 % s
91 % $
85 % $
Palmaria
61 % r
Gracilaria
88 % r
Porphyra
67-82 %d
71 % b
87 % e
Red seaweed
Chondrus
68-75 %b
70-87 %c
81 % g
84 % r
Ulva
Ascophyllum
Sargassum
84-87 % a
(fronds)
86 % g
73-90 % s
94 % $
15-37 % f
16-45 % f (fronds)
21-35 % å
38 % i
39 % $
Undaria
Moisture
Green
Fucus
Laminaria/
Saccharina
Species of interest
Brown seaweed
84 % (wild
and
cultured) z
11 % p
21 %h,i
7%m
8%x
12-37 % q
13-22 % s
8-16 s
29 % v
15 % r
17 % $
18 % g,o
9% g,u
15 % (wild) z
26 % æ
18 % $
27 %
(cultured)z
52 % t
21 %h,i
55 % n,y
a= (Horn, 2000), b= (Baardseth and Haug, 1953), c= (Larsen and Haug, 1958), d= (Jensen, 1960), e= (Jensen, 1966), f= ref in (Jensen and Haug,
1956), g=(Marsham et al., 2007), h= (Rupérez, 2002), i=(Rupérez and Saura-Calixto, 2001), j= (Rioux et al., 2007), k= (Jensen, 1960), l= (Je et al.,
2009), m= (Murata and Nakazoe, 2001), n=(Wong and Cheung, 2001b), o= (Ventura and Castañón, 1998), p=(Ortiz et al., 2006), q= (Morgan et al.,
1980), r=(Herbreteau et al., 1997), s=(Foti, 2007), t=(Foster and Hodgson, 1998), u=(Arasaki and Arasaki, 1983), v=(Robledo and Freile-Pelegrín,
1997), x= (Marinho-Soriano et al., 2006), y=(Wong and Cheung, 2000), z= (Mishra et al., 1993), æ= (Bobin-Dubigeon et al., 1997), ø= (Simpson and
Shacklock, 1979), å=(Lamare and Wing, 2001), $= (Wen et al., 2006), ω= (Holdt, 2009)
Ash
16
Researchers from Norwegian Institute of Seaweed Research have since the 1950s done
extensive studies of seasonal variations of biochemical composition of especially the large
brown seaweed species. Some results on Ascophyllum nodosum and Fucus vesiculosus
are summarised in Figure 7 (Ragan and Jensen, 1978).
Figure 7: Seasonal maxima (solid bars) and minima (shaded bars) of constituents (dry weight basis) of
Norwegian A. nodosum and F. resiculosus: (references in (Ragan and Jensen, 1978)).
The ash content is high in seaweed (Table 4) also compared to vegetables (Table 3). The
ash content includes macro minerals and trace elements (see chapter on minerals).
Ash content was in fronds of Saccharina, Laminaria species and Alaria esculenta
lowest during September, October and November and highest during spring (February to
June), however varied only slightly in the stipes during the years. Dry weight was lowest
from January to March and highest in July to September for the mentioned species (Haug
and Jensen, 1954; Jensen and Haug, 1956).
Physiologically active substances of marine algae are classified into 2 types
based on the difference in the mechanisms as follows: 1) the non-absorbed high-molecular
materials like dietary fibres; 2) low-molecular materials, which are absorbed and affect the
maintenance of human homeostasis directly. Among the physiologically active substances,
antibiotics, anti-tumour elements and anti-ulcer elements are present in marine algae.
(Murata and Nakazoe, 2001).
These seasonal and environmental variations in composition make
generalisations for this report difficult. However, this report summarises worldwide
scientific research on composition of and bioactivity of compounds in the species of
interest in Denmark
17
Polysaccharides
Marine algae contain large amounts of polysaccharides, notably cell wall structural, but
also mycopolysaccharides and storage polysaccharides (Murata and Nakazoe, 2001;
Kumar et al., 2008b). Polysaccharides are polymers of simple sugars (monosaccharides)
linked together by glycosidic bonds, and they have numerous commercial applications in
products such as stabilisers, thickener, emulsifiers, food, feed, beverages etc. (McHugh,
1987; Tseng, 2001). Food applications of the stabilisers utilised by seaweed are shown in
Table 5.
Table 5. Seaweed polysaccharides: Important properties and selected applications (Renn, 1997).
18
The total polysaccharide concentrations in the
seaweed species of interest ranges from 4-76 % of
the dry weight (Table 6). The highest contents are
found in species such as Ascophyllum, Porphyra and
Palmaria, but also the green seaweed species Ulva
has high content (up to 65 % of dry weight).
The frame polysaccharides mainly consist of
cellulose
and
hemicelluloses,
neutral
polysaccharides, and they are thought to physically
support the thallus in water. The building blocks
needed to support the thalli of seaweed in water are
less than to keep terrestial plants and trees erect. The
cellulose and hemicellulose content is 2-10 % and
9 % on dry weight basis, respectively in the seaweed
species of interest in this report. Lignin is to my
knowledge only found in Ulva sp.
and in
concentrations of 3 % of dw (Table 6).
The cell wall and storage polysaccharides are
species specific as mentioned in the introduction and
examples of concentrations are given in Table 7.
Green algae contain sulphuric acid
polysaccharides, sulphated galactans and xylans,
brown algae alginic acid, fucoidan (sulphated
fucose), laminarin (β-1, 3 glucan) and sargassan and
red algae agar-agar, xylans, floridean starch
(amylopectin like glucan), water soluble sulphated
galactan and porphyran as mucopolysaccharides
located in the intercellular spaces. Starch and
laminaran are present in marine algae as storage
polysaccharides (Table 3 and 7)(Murata and
Nakazoe, 2001; Kumar et al., 2008b).
Ascophyllum nodosum (photo: Holdt, 2010)
19
Table 6. Content of total polysaccharides and structural and dietary fibres in the seaweed species of interest in Denmark. See also Table 12 for content
of other polysaccharides including bioactivity.
Polysaccharides
Total
Structural and
dietary fibres
Total
Soluble
Lignin
Cellulose
38 % b
48 %%
58 % a
61 %%
36 % l
62 %%
66 % a
42-64 %%
44 % c
70 % a
38 % c
10 % in
stipe n
4.5-9 % o
2-4.5 % o
2%o
3.5-4.6 %n
35-45 % d, e
4%f
68 % f
15 % -65 % g-i, q
18 % p
42-46 %%
35-46 % l, m
49-62 % l, m
38 % lm
30 % lm
33 % lm
21 % lm
3%g
9%g
5566
%%
40 % e
41 % r
50-76 %%
54 % b
35-49 % l, m
36 % f
62 % b
63 % f
Palmaria
Gracilaria
Porphyra
Chondrus
Red seaweed
Ulva
Sargassum
Undaria
Green
Ascophyllum
Fucus
Laminaria/
Saccharina
Species of interest
Brown seaweed
38-74 % j
50 %%
66 % k
18 % lm
Hemicelluloses
9%g
a=(Rioux et al., 2007), b= (Wen et al., 2006), c= (Tseng, 2001), d= (Je et al., 2009), e= (Murata and Nakazoe, 2001), f= (Marinho-Soriano et al., 2006), g= (Ventura and Castañón, 1998), h= (Ortiz et al., 2006),
i=(Sathivel et al., 2008), j= (Heo and Jeon, 2008), k=(Mishra et al., 1993), l= (Dawczynski et al., 2007), m=(Lahaye, 1991), n=(Horn, 2000), o=(Black, 1950), p= (Foster and Hodgson, 1998), q= (Wong and
Cheung, 2000), r= (Arasaki and Arasaki, 1983), %=(Morrissey et al., 2001)
Palmaria palmata (photo: Holdt, 2010)
20
Contents of both total and also species-specific polysaccharides show seasonal variations
(Table 3 and 7; Figure 7 and 8).
The mannitol content varied markedly in the fronds of Saccharina and Laminaria
species with maximum amounts found during summer and autumn, from June to
November. The laminarin/an showed extreme variations during the year with very small
amounts or absent in February to June and maximum in September to November (Haug
and Jensen, 1954; Jensen and Haug, 1956; Honya et al., 1994). The maximum content of
alginic acid in the fronds of Saccharina and Laminaria species was generally found during
the period from March to June and the minimum in September to October (Haug and
Jensen, 1954). However, highest contents of alginic acid were found during winter in other
seasonal studies made at Laminaria species from the same areas in Norway (Jensen and
Haug, 1956).
Table 7. Species-specific polysaccharides and bioactive components (g/100 g on dry weight basis; NA: no
data available)(MacArtain et al., 2007).
Seaweed
Bioactive components
Alginic acid Fucoidan
Laminarin
Mannitol
Phorphyran
Floridoside
Ascophyllum nodosum
28
11.6
4.5
7.5
-
-
Laminaria digitata
32.2
5.5
14.4
13.3
-
-
Porphyra umbilicalis
-
-
-
-
47.8
41.8
NA
Palmaria palmata
-
-
-
-
NA
25
46
Pentoses
Porphyra sp. (photo: Holdt, 2010)
21
Figure 8. Seasonal variations of alginic acid, mannitol, laminarin and ash content (g/100 g dw)of Laminaria digitata in four locations (Reine, Vardø,
Espevær and Ingøy) in Norway during 1951-1953 (Jensen and Haug, 1956).
22
Further investigations on the hydrolysates of some brown algae showed complex mixtures
of monosaccharides. The components of galactose, glucose, mannose, fructose, xylose,
fucose and arabinose were found in the total sugars in the hydrolysates. The glucose
content was 65 %, 30 % and 20 % of the total sugars in an autumn sample of 50 individual
plants of Saccharina, Fucus (serratus and spiralis) and Ascophyllum, respectively (Jensen,
1956).
The polysaccharides are not solely species-specific, but get their names from
which species or genera they are most abundant e.g. laminaran from Laminaria spp. and
porphyran from Porphyra spp. (Table 7). These polysaccharides are composed of different
neutral sugars (Table 8).
Table 8. Composition (%) of ascophyllan, fucoidan, alginate fractions, and commercially available fucoidan
(Sigma) and molar ratios of the compositions (Nakayasu et al., 2009).
Polysaccharide
Composition of neutral sugars a
Fucose Xylose
Glucose Mannose
Galactose
Uronic Acid b
Ascophyllan
15.5 (1)
13.4 (0.95)
0.3 (0.02)
3.4 (0.2)
0.6 (0.04)
21.4 (1.17)
9.6 (1.06)
Fucoidan
28.4 (1)
4.3 (0.16)
2.0 (0.06)
0.8 (0.03)
5.3 (0.17)
5.8 (0.17)
19.4 (1.17)
Alginate
0.5 (1)
0.4 (0.79)
0.1 (0.16)
0.6 (1.07)
1.6 (2.99)
27.8 (47.4)
0 (0)
24.8 (1)
1.9 (0.09)
0.8 (0.03)
1.0 (0.04)
3.1 (0.11)
9.6 (0.33)
22.6 (1.56)
Sigma fucoidan d
SO42- c
a
Determined by HPLC assay after acid hydrolysis
Determined by carbazole method and calculated as glucuronic acid equivalent
c
Determined by turbidimetric assay after acid hydrolysis
d
Purified from Fucus vesiculosus
The numbers in brackets indicate the molar ratios of the composition, calculated from fucose content of 1
b
Several other polysaccharides are present in and utilised from seaweed, however not
described in this report e.g. furcellaran, funoran, xylans, sargassan.
Seaweed polysaccharides are separated into dietary fibres, hydrocolloids etc. in
the following paragraphs eventhough the polysaccharides belongs to more than just one of
the functional groups.
Dietary fibres
Edible seaweed contain 33-50 % total fibres on dry weight basis, which is higher than the
levels found in higher plants and these fibres are rich in soluble fractions (Lahaye, 1991).
The dietary fibres included in marine algae are classified into 2 types, namely into
insoluble such as cellulose, mannans and xylan, and water soluble dietary fibres such as
agar-agar, alginic acid, furonan, laminaran and porphyran, depending on the solubility in
water (Table 9, 10 and 11 (Fleury and Lahaye, 1991).
Table 9. Soluble (SDF), insoluble (IDF) and total (TDF) dietary fibre (% of dry
weight) in edible Spanish seaweedsa (Rupérez and Saura-Calixto, 2001).
Seaweed
Fucus
Laminaria
Wakame
Chondrus
Nori
SDF
IDF
TDF
9.80±0.78
40.29±0.98
50.09±1.77
9.15±0.48
26.98±1.97
36.12±2.46
17.31±0.51
16.26±0.79
33.58±1.31
22.25±0.99
12.04±2.89
34.29±3.89
14.56±1.33
19.22±2.05
33.78±3.38
a
AOAC method without starch treatment for brown seaweeds.
Mean values of triplicate determinations ± standard deviation
23
The undigested polysaccharides of seaweed can form important source of dietary fibres,
however, they might modify digestibility of dietary protein and minerals. Apparent
digestibility and retention coefficients of Ca, Mg, Fe, Na and K were lower in seaweed-fed
rats (Urbano and Goñi, 2002). The seaweed dietary fibres contain some valuable nutrients
and substances and interest has been created in seaweed meal, functional foods, and
nutraceuticals for human consumption (McHugh, 2003), as polysaccharides among other
things is showing bioactivity within anti-tumour action, anti-herpetitic, potent as a anticoagulant and decreases LDL-cholesterols in rats (Table 12; (Murata and Nakazoe, 2001;
Amano et al., 2005; Athukorala et al., 2007; Ye et al., 2008; Ghosh et al., 2009)).
Porphyran showed appreciable anti-tumor activity against Meth-A fibrosarcoma. In
addition, it can significantly lower the artificially enhanced level of hypertension and bloodcholesterol in rats (Noda, 1993).
Table 10. Neutral sugars in soluble dietary fibres from edible Spanish seaweed (Rupérez and Saura-Calixto,
2001)
Table 11. Neutral sugars in insoluble dietary fibres from edible Spanish seaweed (Rupérez and SauraCalixto, 2001)
.
24
Table 12. Bioactivity, source and characteristics of polysaccharides in seaweed species within the seaweed families of interests in Denmark. See also
Table 6 for total content of polysaccharides and other structural polysaccharides. Concentrations are given in % on a dry weight basis.
Characteristics
Source and content
Bioactivity
Total polysaccharides
Saccharina latissima a
Sargassum pallidum b, c
Algins/alginic acid
Polymer of two different units of
uronic acids (D-mannoronic acid
and L-glucoronic acid) Ю
Saccharina latissima: 17-33 % Ө, 18 %%
Laminaria digitata ф: 32 % g, 33-46 % Ө, 30-44 % ψ
Laminaria hyperborea: 17-34 %∞, 20-37 % Ө
Laminaria sp. h, a
Fucus vesiculosus: 18-22 %%
Ascophyllum nodosum: 28 % g; 24-29 %Ж, 26 %%
Undaria pinnatifida a: 24 % f, a
Sargassum vulgare i
Brown seaweed species: 10-47 % Ю
Ulva sp. i
Chondrus crispus j-l 47 % э, 50 %‫ ב‬, 58-71 %√,
Eucheuma cottonii/Kappaphycus alvereziim:22%‫ ש‬,88%‡
Kappaphycus striatum: 72 %‡
Gracilaria sp., Gigartina sp. etc. m
Gracilaria cornea: 21-31 % ¿
Gracilaria dominguensis [11]
Anti-tumour action a, in vitro (HepG2, A549 and MGC-803 cells; MMT and DPPH free radical assay) b
Anti-herpetic e
Potent anti-coagulant c
Decrease in LDL-cholesterol in rats d
Anticancer a
Increased (3.5-fold) the ileal viscosity of digesta and their hydration capacity in the ileum and colon in
pigs ф
Decrease in cholesterol concentration a
Anti-hypertension effect a
Dietary fibre for maintenance of human health a
Carrageenan
Sulfated polysaccharide. Several
types: iota, kappa- and lambda
Agar
Consist
of
agarose
and
agaropectin (ratio 7:3)
Fucoidan
ranging from typical fucoidans
(major components) to low
sulphate-containing heteropolysaccharide-like fucans (minor
components) o
Laminaria digitata: 5.5 % g, 2-4 % (in stipes) ∞
Laminaria hyperborea: 2-4 % in stipe∞
Laminaria sp. h, #, [16]
Sargassum horneri c
Sargassum vulgare: uronic acid, xylose and fucose
accounted for >90 % of total sugars i
Sargassum fulvellum [16]
Fucus vesiculosus o, y : 16-20 %%
Fucus sp. [16]
Undaria pinnatifida p, s, t, #, [16]: 1.5 % f
Ascophyllum nodosum r: 12 % g; 4-10 % Ж, [16]
Eisenia bicyclis u
Anti-tumour and immunomodulation j in mice k
Anti-HIV (UV and radioactive counting) n, but no efficacy on humans l
Decrease in blood glucose concentration a
Anti-aggregation effect of red blood cells a
Absorption effect of ultraviolet rays a
Anti-tumor: Inhibited the transplantation of Ehrlich ascites carcinoma in mice [11]
Activity against α-glucosidase [14]
Suppress the production of pro-inflammatory cytokine TNF-α [15]
Suppress the expression of inducible nitric oxide synthase (iNOS) [15]
Antioxidant activity (DPPH method) [14]
Anti-inflammatory [16]
Anti-arteriosclerosis a
Antioxidant activity (Cys/FeSO4 in vitro, DPPH, scavenging superoxidde radical) [16]
Reducing blood lipids (total cholesterol, triglyceride and LDL-C and increase HDL-C in serum of mice
and rats) [16]
Slightly anti-coagulant activity (gel filtration and anion-exchange chromatography) o
Potential antiviral c : against human cytomegalovirus and avian flue (human cytomegalovirus)s,
(Cryptosporidium parvum (parasite) adhesion to the human intestinal cells and on C.parvum
infection in neontenal mice) t Inhibits growth of C. parvum in micez
Anti-virus activity # (HSV e (methylation analyses and in vitro herpes virus type1 (HSV-1), HSV-2) s, HIV
v
, poliovirus III, adenovirus III, ECHO6 virus, coxsackie B3 virus and coxsackie A16) [16]
Anti-herpetic (in vitro, Herpes Simplex viruses, HSV-1, HSV-2 and HCMV) p
Anti-coagulant x, [16] (gel filtration and anion-exchange chromatography)o, #
Anti-thrombotic activity [16]
Anti-cancer a, # (in vitro,DPPH and human cancer cell lines)y
Anti-tumor and immunomodulatory activity (breast carcinoma cells, micewith transplanted Lewis lung
adenocarcinoma,inhibition of infected T-cell lines, anti-cancer on human HS-Sultan cells) [16], [17], (L1210 leukemia) u
Anti-complementary activity [16]
Therapeutic potential in surgery [16]
Gastric protection [16]
Against hepatopathy [16]
Against uropathy and renalpathy [16]
25
Table 12. (continued)
Characteristics
Source and content
Bioactivity
Ascophyllan
Fucan similar to fucoidan. Distinct
due to uronic acid backbone with
fucose containing branches [17]
Mannitol
Ascophyllum nodosum [17]
Cytotoxic effect: Inhibited the proliferation of U937 cells. Reduction of apoptosis [17]
Anti-tumor effect: Induced the secretion of tumor necrosis factor-α (TNF-α) and granulocyte colonystimulating factor (G-CSF) from mouse macrophage cell line (RAW264.7) [17]
Saccharina latissima: 2-19 % Ө, 14 %%
Laminaria digitata: 13 % g, 2.5-17 % Ө, 4-20 % ψ,
7.5 %%, 2-11 % (in stipes) ∞
Laminaria hyperborea: 4-25 %∞, 2-18 % Ө, 4-20 % ψ
Laminaria sp. h
Sargassum mangarevense: 1-12 % æ
Ascophyllum nodosum: 7.5 % g; 6.8-10.4 % Ж,
5.2-10.2 % д,, 7-11 %€
Saccharina latissima: 0-33 % Ө, 16 %%
Laminaria digitata: 14 % g, 0-18 % Ө, ψ, %
Laminaria hyperborea: 0-30 %∞, 0.5-24 % Ө, 0-32 %ψ
Laminaria sp. h : 99 % of total sugars α, 20-30 % Ю
Fucus vesiculosus: 84 % of total sugars α
Ascophyllum nodosum: 4.5 % g; 1.2-6.6 % Ж, 2-7 % €;
10 %, 90 % of total sugarsα
Undaria pinnatifida 3 % f
Effectively protects the photosynthetic apparatus from low-salinity damage ø, å
Laminaran / Laminarin
Branched (soluble) and
unbranched (insoluble)
polysaccharide: beta 1-3,beta 1-6glucan å, β. 84-94 % sugar and 6-9
% uronic acid α
Contains mannitol Ю
Only found in brown seaweed å
Phycarine
Porphyran
Polysaccharide: polymer of acidic
saccharide containing sulphate
groups, β-1,3-xylan $
Ulvan
Highly branched polymers of
soluble dietary fibre and contain
rhamnose, glucuronic acid and
xyloseμ, π. Structurally similar to
mammalian glycosaminoglycansω
Floridoside
Floridean starch (in red algae),
similar to starch amylopectin, but
more red iodine reaction Ю
Laminaria digitata δ
Porphyra umbilicalis: 48 % g
Porphyra sp. $, [18]
Ulva lactuca ω, [20], [19]
Ulva rigida
Monostroma sp. [19]
Anti-viral in agricultural applications [1]
Anti-bacterial [3]
Substratum for prebiotic bacteria [2]
Dietary fibre [2]
Hypocholesterolemic and hypolipidemic responses due to reduced cholesterol absorption in gut [5],[6],[7]
Reduce serum cholesterol levels and total serum lipid [4]
Reduction of total cholesterol, free cholesterol, tri-glyceride and phospholipid in the liver [10]
Decrease of systolic blood pressure (anti-hypertensive responses) [8],[9]
Surgical dusting powder [4]
Maybe value as tumor-inhibiting agent [4]
Anti-coagulant (sulphate ester form) [4],[13]
Protection against irradiation [4], [12], also severe [3]
Stimulates immune systems; B- and helper T-cells [3]
Immunostimulating activities in animals and plants; 1→3:1→6-β-D-glucans produced from laminarin [12]
Help in wound repair [4]
Immune system,stimulation of macrophage phagocytosisδ
Anti-blood coagulant [18]
Anti-hypercholesterolemia [18]
Anti-tumor [18]
Potential apopototic/programmed cell death activity $
Modify adhesion and proliferation of normal and tumoral human colonic cells [19]
Treatment of gastric ulcers [19]
Anti-influenza [19]
Cytotoxicity and cytostaticity, HU colon cell line ω
Porphyra umbilicalis : 42 % g
Palmaria palmata: 25 % g
a= (Murata and Nakazoe, 2001), b= (Ye et al., 2008), c= (Athukorala et al., 2007), d= (Amano et al., 2005), e= (Ghosh et al., 2009), f= (Je et al., 2009), g= (MacArtain et al., 2007), h= (Bartsch et al., 2008a), i= (Dietrich et
al., 1995), j= (Yan et al., 2004), k= (Zhou et al., 2006a), l= (Skoler-Karpoff et al., 2008), m= (FAO, 2008), n= (Vlieghe et al., 2002), o= (Nishino et al., 1994), p= (Hemmingson et al., 2006), q= (Matsubara et al., 2005),
r= (Marais and Joseleau, 2001), s= (Lee et al., 2004), t= (Maruyama et al., 2007), u= (Yamamoto et al., 1984), v= (Schaeffer and Krylov, 2000), x= (Mayer and Hamann, 2004), y= (Han et al., 2008), z= (Smit, 2004),
æ= (Zubia et al., 2008), ø= (Gessner, 1971), å= (Lobban and Harrison, 1994), α= (Rioux et al., 2007), β= (Deville et al., 2007), δ= (Mayer et al., 2007), $= (Plaza et al., 2008), ω=(Kaeffer et al., 1999), μ= (Bobin-Dubigeon
et al., 1997), π= (Michel and Macfarlane, 1996), Ж= (Jensen, 1960), ∞= (Jensen and Haug, 1956), Ө= (Haug and Jensen, 1954) only data of fronds, д=(Larsen and Haug, 1958), ψ= (Jensen and Haug, 1956)), ф= (Kim
and Lee, 2008), €= (Jensen, 1960), #= (Zhuang et al., 1995), ¿= (Freile-Pelegrín and Robledo, 1997), Ю= (Arasaki and Arasaki, 1983), %= (Morrissey et al., 2001), э= (Bruhn et al., 2008), ‫( =ב‬Chopin et al., 1995),
√= (Chopin et al., 1999a), ‫( =ש‬Hayashi et al., 2008), ‡= (Rodrigueza and Montaño, 2007b), [1]= (Goemar, 2010), [2]= (Deville et al., 2004), [3]= (Hoffman et al., 1995), [4]= (Miao et al., 1999), [5]= (Kiriyama et al., 1969),
[6]
= (Lamela et al., 1989), [7]= (Panlasigui et al., 2003), [8]= (Renn et al., 1994a), [9]= (Renn et al., 1994b), [10]= (Nishide and Uchida, 2003), [11]= (Fernandez et al., 1989), [12]= (Kuznetsova et al., 1994). [13]= (Shanmugam and
Mody, 2000), [14]= (Chen et al., 2004), [15]= (Enoki et al., 2003), [16]= (Li et al., 2008a), [17]= (Nakayasu et al., 2009), [18]= (Noda, 1993) , [19]= (Lahaye and Robic, 2007), [20]= (Nagaoka et al., 2003)
26
Hydro- or phycocolloids
Production of carbohydrates that dissolve in water is a growing industry. The three major
groups of phycocolloids are algins, carrageenan, and agar and are used as for
applications such as thickening aqueous solutions, forming gels and water-soluble films,
and are used for stabilising products such as ice cream, tooth paste, mayonnaise etc.
(Tseng, 2001; FAO, 2008).
Algins are extracted from brown seaweed and are available in both acid and salt
form. The acid form is a linear polyuronic acid and referred to as alginic acid, whereas the
salt form is an important cell wall component in all brown seaweed, constituting up to 4047 % of the dry weight of algal biomass (Arasaki and Arasaki, 1983; Rasmussen and
Morrissey, 2007). The algins has anticancer properties (Murata and Nakazoe, 2001) and
good dietary fibre properties in pig intestines (Table 12) (Kim and Lee, 2008). Various
industries related to food processing, pharmaceuticals, fodder and cosmetics use alginic
acid extracted from Saccharina and Undaria. Moreover, it is reported that alginic acid
leads to a decrease in the concentration of cholesterol and exerts an anti hypertension
effect, prevention effect of absorption of toxic chemical substances, and plays a major role
as dietary fibre for the maintenance of human health (Murata and Nakazoe, 2001). The
binding property of algenic acid to divalent metallic ions is correlated to the degree of the
gelation or precipitation in the range of Ba<Pb<Cu<Sr<Cd<Ca<Zn<Ni<Co<Mn<Fe<Mg.
No intestinal enzymes can digest alginic acid. This means that heavy metals taken into the
human body are gelated or rendered insoluble by algenic acid in the intestines and cannot
be absorbed in into the body tissue. (Arasaki and Arasaki, 1983)
Carrageenans are a group of biomolecules composed of linear polysaccharide
chains with sulphate half-esters attached to the sugar unit. These properties allow
carrageenans to dissolve in water, form highly viscous solutions, and remain stable over a
wide pH range. There are three general forms (kappa, lambda and iota), each with their
own gelling properties (Rasmussen and Morrissey, 2007). Chondrus crispus and
Kappaphycus sp. are species containing up to 71 % and 88 % of carrageenan,
respectively (Chopin et al., 1999a; Rodrigueza and Montaño, 2007a). In food industry it is
mainly used for dairy and processed meat products, however from a human health
perspective it has been reported that carrageenans has antitumor and antiviral properties
(Vlieghe et al., 2002; Yan et al., 2004; Zhou et al., 2006b; Skoler-Karpoff et al., 2008).
Agar is a mixture of polysaccharides, which can be composed of agarose and agropectin,
with similar structural and functional properties as carrageenan and extracted from red
seaweed such as Gracilaria sp. (Rasmussen and Morrissey, 2007; FAO, 2008). The agar
content in Gracilaria species can reach 31 % (Table 12). Agar –agar is a typical and
traditional food material in Japan and it is used as a material for cooking and Japanesestyle confectionary. In addition, agar-agar is used for the manufacture of capsules for
medical applications and as a medium for cell culture, etc. It is reported that agar-agar
leads to decrease in the concentration of blood glucose and exerts an anti-aggregation
effect of red blood cells and ultraviolet rays absorption effect (Murata and Nakazoe, 2001).
Furthermore, anti-tumor activity was found in an agar-type polysaccharide from cold water
extraction of another Gracilaria species and hydrolysates of agar resulted in agarooligosaccharides with activity against α-glucosidase and antioxidant ability (Chen et al.
2005; Fernandez et al. 1989). Agaro-oligosaccharides have also been shown to suppress
the production of a pro-inflammatory and an enzyme associated with the production of
nitric oxide (Enoki et al. 2003).
27
Fucans/fucanoids
Fucans are a group of polysaccharides primarily composed of sulphated L-fucose with less
than 10 % of other monosaccharides. They are widely found in the cell walls of brown
seaweed, but not in other algae or higher plants (Berteau and Mulloy, 2003). According to
Table 12 the species Fucus vesiculosus contain the highest concentration of fucoidans (up
to 20 % on a dry weight basis). Fucanoids can make up more than 40 % of dry weight of
isolated algal cell walls and can easily be extracted using either hot water or an acid
solution. Although the major physiological purposes of fucans in the algae are not
thoroughly understood, they are known to posses numerous biological properties with
potential human health applications (Berteau and Mulloy, 2003). The list of bioactivity of
fucoidan for human health is long. Fucoidan found in seaweed such as Undaria and
Laminaria shows anticoagulant, anti-viral and anti-cancer properties (Table 12) (Zhuang et
al., 1995). No toxicological changes were observed when 300 mg/kg body weight per day
fucoidan was administered to rats, however, significantly prolonged blood-clothing times
were observed when concentrations were increased three fold (Li et al., 2005).
The antioxidant activity of sulphated polysaccharides is related not only to
molecular weight and sulphated ester content, as previously determined, but also to
glucuronic acid and fucose content (Zhao et al., 2008).
Digestibility of polysaccharides
The dietary fibres are very diverse in composition and chemical structure as well as in their
physicochemical properties, their ability to be fermented by the colonic flora and their
biological effects on animal and human cells. The majority of edible seaweed fibres are
soluble anionic polysaccharides which are little-degraded or not fermented by the human
colonic micro flora (Lahaye and Kaeffer, 1997). The amount of dietary fibres not digested
by the human digestive tract in marine algae, is higher than that of other food materials,
and the content of dietary fibres is 58 % for Undaria, 30 % for Porphyra and 29 % for
Saccharina (g/100 g of dw)(ref in (Murata and Nakazoe, 2001).
Phycocolloids are more or less degraded following adaptation of the human micro
flora, but none of the seaweed polysaccharides have been shown to be metabolized,
although some may be partly absorbed. Nothing is known about the fate of other algal
polysaccharides in the human digestive tract, except that they cannot be digested by
human endogenous enzymes. Results of fermentation in vitro with human faecal bacteria
indicate that brown seaweed fibres exhibit an original fermentation pathway (Mabeau and
Fleurence, 1993).
Examples of digestibility of polysaccharides are given in the following paragraphs.
All soluble fibre fractions of Palmaria palmata consisted of linear beta-1,4/beta1,3
mixed linked xylans containing similar amounts of 1,4 linkages (70.5-80.2%). The
insoluble fibres contained essentially 1,4 linked xylans with some 1,3 linked xylose and a
small amount of 1,4-linked glucose (cellulose). Soluble fibres was fermented within 6 hours
by human faecal bacteria into short chain fatty acids (Lahaye et al., 1993).
Laminarin, alginic acid/cellulose (beta 1-3,beta 1-6-glucan) was almost totally
(more than 90% used) fermented after 24 hours of incubation with human intestinal
bacteria. Variations of mucus composition were observed both in lumen content and in
intestinal wall of rats after ingestion of this polysaccharide. In conclusion, laminarin
28
seemed to be a modulator of the intestinal metabolism by its effects on mucus
composition, intestinal pH and short chain fatty acid (SCFA) production, especially
butyrate (Deville et al., 2007).
The particular chemical structure of ulvan is responsible for the resistance of this
polysaccharide and of Ulva to colonic bacterial fermentation. Consumption of dietary fibres
from Ulva sp. could be expected to act mainly as bullring agents with little effect on nutrient
metabolism due to colonic bacterial fermentation products (short-chain fatty acids; Figure
9)(Bobin-Dubigeon et al., 1997).
Figure 9. Fermentation of carbohydrates by intestinal
bacteria. Short-chain fatty acid (SCFA) production
from native and chemically treated ulvan and related
carbohydrates by mixed populations of intestinal
bacteria. Results are from 24 h in vitro incubations and
are given after deduction of control values. Results are
modified from other reference. Error bors show SD.,
n=2 (Michel and Macfarlane, 1996).
Most of each of the total algal fibres
disappeared after 24 h (range 60-76 %) in in
vitro fermentation of e.g. Laminaria digitata
and Undaria pinnatifida using human faecal
flora. However, unlike the reference substrate
(sugar beet fibres), the algal fibres were not
completely metabolized to short chain fatty
acids (SCFA)(range 47-62 %). Among the
purified algal fibres, disappearance of
laminarans was approximately 90% and
metabolism to SCFA was approximately 85 %
in close agreement with the fermentation pattern of reference fibres. Sulphated fucans
were not degraded. Sodium alginates (Na-alginates) exhibited a fermentation pattern
quite similar to those of the whole algal fibres with a more pronounced discrepancy
between disappearance and production of SCFA: disappearance was approximately 83 %
but metabolism was only approximately 57 %. The characteristic fermentation pattern of
the total fibres from the brown algae investigated was attributed to the peculiar
fermentation of alginates (Michel et al., 1996).
Dietary fibres are found to be effective in the prevention of obesity,
hypercholesterolemia, large intestine cancer and diabetes and also have antiviral activities
(see also Table 13) (Murata and Nakazoe, 2001; Lee et al., 2004), and water insoluble
polysaccharides (celluloses) are mainly associated with a decrease in digestive tract
transit time (Mabeau and Fleurence, 1993).
29
Table 13. Anti-virus activity of fucoidan from mekabu; the sporophyll of Wakame (Undaria pinnatifida;
(Lee et al., 2004)).
Virus
Host cell
Cytotoxicity
(CC50, μg/ml)
Antivirus activity
(CC50, μg/ml)
Aa)
Bb)
Selectivity index
(CC50/IC50)
A
B
HSV-1
Vero
>2000
2.5
14
>800
>140
HSV-2
Vero
>2000
2.6
5.1
>770
>390
HCMV
HEL
>2000
1.5
16
>1300
>125
Influenz A virus
MDCK
>2000
15
55
>130
>36
Poliovirus
Vero
>2000
>100
>100
~20
~20
Coxsackie virus
Vero
>2000
>100
>100
~20
~20
a) Sample was added to the medium at the time of viral infection for 1 h and throughout the incubation thereafter. b) Sample was added to the
medium immediately after viral infection.
HSV: Herpes Simplex Virus
HCMV: Cytomegalovirus also known as Human Herpesvirus 5 (HHV-5)
Coxsackie virus: includes poliovirus, echovirus and hepatitis A virus
Vero: African green monkey kidney epithelium
MDCK: Dog kidney epithelium
Palmaria palmata (photo: Holdt, 2010)
30
Proteins, peptides and amino acids
Amino acids are molecules that contain an amine group, a carboxylic acid group and a
side chain that varies between different amino acids. They are critical to life, and their most
important function is their variety of roles in metabolism. The building blocks of proteins
are one very important function. The combination in the linear chains of the different amino
acids makes the differences in the structure (also three dimensional structures) and
function of the protein. Peptides are short polymers of linked amino acids. Proteins consist
of multiple polypeptide subunits. The distinction is that peptides are short and
polypeptides/proteins are long (chapter of nutritional elements)(Wikipedia, 2010).
Although the structure and biological properties of seaweed proteins are still
poorly documented, the amino acid compositions of several species have been known for
a long time (Murata and Nakazoe, 2001).
The non-protein nitrogen is thought to be an intermediate or final product of
nitrogen metabolism in plant tissue. This fraction consists of amino acids, peptides,
amines, and nucleotides and accounts for from 10 to 20 % of the nitrogen in seaweed
(Arasaki and Arasaki, 1983). In addition, other investigations found that the biochemical
composition of total nitrogen (57 %) in Fucus vesiculosus of which 7-8 % were the total
nitrogen peptides and 10 % free amino acids (Smith and Young, 1953).
Habitat, and especially seasonal variation, has an effect on proteins, peptides and
amino acids in seaweed (Haug and Jensen, 1954; Arasaki and Arasaki, 1983).
Proteins
The protein content of marine algae also varies with the species like the other biochemical
compositions. The protein fraction of brown seaweed is generally small. Undaria has the
maximal content of 24 % followed by several species (Sargassum, Fucus and
Laminaria/Saccharina) with maxima around 17 % to 21 % and with Ascophyllum with the
lowest content (maximum 10 % of the dry weight; Table 14). Higher protein contents are
recorded for green and red seaweed. Proteins can represent up to 35 %, 44 % and 44 %
of the dry matter in Palmaria palmata (dulse), Porphyra tenera (nori) and Ulva spp.,
respectively. These levels are comparable to those found in high-protein vegetables such
as soybeans in which proteins make up 40 % of the dry mass (Murata and Nakazoe,
2001).
The protein content in the fronds of Saccharina, Laminaria species and Alaria
esculenta showed a pronounced maximum during the period from February to May, the
young parts of the Saccharina and Laminaria species fronds being considerably richer
than the old parts (Haug and Jensen, 1954; Jensen and Haug, 1956).
The bioactive protein lectin is found in the two macroalgae species Ulva sp. and
Gracilaria sp. Lectin has been found to increase the agglutination of blood cells
(erythrocytes) and is furthermore useful in the detection of disease-related alterations of
glycan synthesis including infectious agent such as, viruses, bacteria, fungi and parasites
(Bird et al., 1993; Murata and Nakazoe, 2001; Cardozo et al., 2007). Furthermore, protein
extracts from 22 species of seaweed stimulates mitogenesis in human lymphocytes and
agglutinates erythrocytes in rabbits, sheep and bacteria (Bird et al., 1993).
31
Table 14. Total protein content as percent of dw, and amino acids as percent of total N or % of total protein N. Asterisk refer to essential amino acid.
Total protein
3-14 % æ
5-20 %
(fronds)y
1.4 % c
5-10 %%
7-13 %
(stipes)y
7.5 % a
6.2 % g
10 % #
57 %(total
N)m
17 % b
11 % g
1.2 % c
3.2 %
(total
N)h
4.89.8 % z
4.09.7 %ø
5-10 %
Palmaria
Gracilaria
4-9 % j
6%$
6-7 % e
13-18 % d
7%j
9-16 % e
5%e
21 % k
8-35 % l
17 % p
13 % i
20 % g
21 % n
28 % k
23 % e
12-22 % f
15 % q
6.3 % total amino acids ω
74 % AA of PC €
7 % j, ω
27 % r
30-50 % #
14 % π
16 % g
24 % d
29 % b
34 % t
20 % a
28 % g
39 % q
31 % a
34 % e
39 % q
44 % b
44 % b
% of total AA i
or proteint
% of total Nm or
proteinӨ
% of total AAs, t
or protein u
% of
total Nv
% of
total AAs
% of total
proteinx
% of
total Nk
% of dwπ
% of total
AAs or
proteinf
8.5
1.8
6.1 t
5.1
3.0
15 t
9.2
6.5 t
3.8
6.4
7.4 t
9.9 α
0.66
7.5
6.7
34
6.8
16
5.9 α
0.60
6.2
5.7
3.8
8.5
5.8
2.6
7.0
8.5 α
1.1
9.3
0.3
0.3 t
0.76
1.3
0
4.1
9.9
7.2
9.3 α
1.5
13
9.9
3.5
7.3
7.2
6.9 α
0.41
7.2
0.9
2.1
1.4
1.2 α
1.1
2.1
13
Alanin
8.0-9.0
5.4
1.3
4.8 t
6.2
6.9 Ө
Arginine
5.0-5.9
9.4
0.52
7.5 t
10
2.6 Ө
Aspartic acid
9.6-9.8
9.0
1.3
5.6 t
7.6
13 Ө
Citrulline
Cystine*
0.6-1.3
+
0.11
0.5 t
3.7
0.0 Ө
Glutamic acid
11-13
11
2.1
5.1 t
3.7
17 Ө
Glycine
6.5-7.0
5.4
0.6
4.4 t
0.6
6.3 Ө
Histidine
2.3-2.4
1.6
1.3
2.7 t
4.1
1.4 Ө
-
Porphyra
9%β
16 % e
12 % c
16 % b
21 % k
Hydroxyproline
Chondrus
24 % d
11-24 % t
å
512 %%
Amino acids (AA)
% of
% of
total AAs total Nm
Ulva
Sargassum
Undaria
Ascophyllum
Fucus
Laminaria/
Saccharina
Total protein
3.4
2.2
1.2 t
10
3.2
6.9 t
7.0
2.2
5.2 t
1.8
4.6
4.0 t
2.3
32
Table 14. (continued)
Amino acids (AA)
% of
% of
total AAs total Nm
% of total AA i
or proteint
% of total Nm or
proteinӨ
% of total AAs, t
or protein u
% of
total Nv
% of
total AAs
% of total
proteinx
% of
total Nk
% of total
AAs or
proteinf
Isoleucine*
5.5-5.8
3.0
0.5
2.9 t
4.7 Ө
6.1
2.8
3.5 t
1.8
5.7
4.0
4.0 α
3.0
5.3
Leucine*
8.7-9.2
5.0
0.9
5.1 t
0.4
7.8 Ө
2.9
7.8
8.7
7.7 α
4.5
0.46
7.8
7.1
Lysine*
6.5-7.3
6.0
0.6
4.3 t
6.9
5.8 Ө
4.9
8.1
4.5
2.6 α
3.2
0.66
8.2
3.3
Methionine*
1.9-2.2
0.4
0.32
2.2 t
0.0
0.9 Ө
0.5
1.5
1.7
3.4 α
+cysteine
>1.3
1.9
1.9
2.7
Ornithine
n.d.
9.2
5.0
6.9 t
6.3
17
4.5 t
1.8
19
1.6 t
n.d.
Phenylalanine*
5.7-6.2
2.6
0.6
3.7 t
0.4
4.3 Ө
Proline
4.8-4.9
3.3
0.6
2.8 t
9.5
4.4 Ө
Serine
3.8-3.9
3.5
0.5
2.8 t
5.5 Ө
Threonine
4.6-5.0
3.3
2.4 t
6.0 Ө
-
0.8 t
1.9
nd Ө
1.8
3.9 Ө
Tryptophan
t
Tyrosine*
4.0-4.3
1.2
1.6
Valine*
6.9
3.0
4.1 t
8.3
3.4 Ө
6.3
13
3.9 t
5.2
4.0 t
4.0
5.4
3.0 t
4.6
5.6
3.1 t
0.3 t
5.0
2.6
1.4 t
7.7
5.6
4.9 t
7.1
2.1
1.5
5.2
3.9
5.3 α
1.9
4.7
6.4
4.6 α
2.2
3.9
n.d.
+tyrosine
5.6
1.1
0.0005
5.2
5.1
2.9
4.8 α
0.75
4.6
6.3
2.2
4.2
4.0
3.2 α
3.0
0.64
4.5
3.6
1.0
6.3
1.3
1.1 α
2.4
2.4 α
0.39
4.5
3.4
2.7
7.0
6.4
9.3 α
3.0
0.77
7.3
6.9
4.4
Amide N
10 % v
Ammonia
15.3
10.5
Total amino acids
13.1
35.8
Lys-Met-Cys-Trp-Thr0.7 a
0.9 a
0.7 a
1.0 a
score
Amino acid score
31 a
100 q
82 q
91 q
(AAS)
61 a
40 a
62-64 a
Essential amino acid
66 a
96 a
40 Ө
37 ω
90-91 a
index (EAAI)
81 a
39 €
a= (Dawczynski et al., 2007), b=(Marsham et al., 2007), c=(Rioux et al., 2007), d=(Plaza et al., 2008), e= (Marinho-Soriano et al., 2006), f=(Galland-Irmouli et al., 1999), g=(Rupérez and Saura-Calixto, 2001), h= (Pavia
et al., 1997), i=(Je et al., 2009), j=(Barbarino and Lourenço, 2005), k=(Wen et al., 2006), l=(Morgan et al., 1980), m=(Smith and Young, 1953), n=(Ventura and Castañón, 1998), p=(Mishra et al., 1993), q= (Murata and
Nakazoe, 2001), r=(Ortiz et al., 2006), s=(Mai et al., 1994), t=(Arasaki and Arasaki, 1983), u=(Wahbeh, 1997), v=(Young and Smith, 1958), x=(Mabeau and Fleurence, 1993), y= (Haug and Jensen, 1954), z=(Jensen,
1960), æ=(Jensen and Haug, 1956), ø=(Larsen and Haug, 1958), å= (Jensen, 1960), $= (Foster and Hodgson, 1998), β=(Robledo and Freile-Pelegrín, 1997), ω= (Wong and Cheung, 2000), €= (Wong and Cheung,
2001c), Ө= (Wong and Cheung, 2001a), #= (McHugh, 2003), %=(Morrissey et al., 2001), α= (Noda, 1993), π= (Ortiz et al., 2009)
33
Peptides
Only few investigations have been made on peptides of macroalgae, and these include
findings of the depsipeptide3 kahalalide F from Bryopsis sp. which is active in the
treatment of lung cancer, tumours and AIDS (Smit, 2004). Ten dipeptides from Undaria
pinnatifida (wakame) reduced blood pressure in spontaneously hypertensive rats (Sato et
al., 2002; Suetsuna et al., 2004). Eisenine, isolated from Eisenia bicyclis4; octaglutamic
acid and L-pyrrolidonoyl-L-glutamyl-L-glutamine isolated from Pelvetia canaliculata;
carnosine in Acanthophora delilei and many peptides including glutamic and aspartic acid
are found in L. japonica (Arasaki and Arasaki, 1983).
The light-harvesting complex (LHC), fucoxanthin, from brown algae has been
found to contain four 20-kDa polypeptides. The gene coding sequences for these
polypeptides (lhcf-genes) show homology to those found in Macrocystis pyrifera and
Laminaria digitata (two other Laminariales) and indicate that these proteins are probably
similar in all brown algae (Douady et al., 1994; Martino et al., 2004).
Ornithine and citrulline (6 % of total N) have been established as occurring both in
the free state and in simple and complex peptides in Chondrus crispus, but not in the
insoluble protein (Young and Smith, 1958).
Free amino acids
The free amino acid fraction of seaweed is mainly composed of alanine, amino butyric
acid, taurine, omithine, citruiline and hydroxyproline. Levels differ according to the species.
In Porphyra tenera, alanine amounting to about 25 % of the total free amino acids,
probably accounts for the faintly sweet taste. Ulva contains large amounts of cysteinolic
acid, cysteic acid, praline, glutamic acid, and chondrine, and Undaria contain abundant
alanine, glycine, and praline, whereas the arginine content is high in Gracilaria. In addition,
such amino acids as citrulline, praline, taurine, arginine, and ornithine accumulate in cells
(Arasaki and Arasaki, 1983). Certain species have a high level of arginine (Ulva pertusa,
Undaria pinnatifida and Porphyra tenera) or glycine (P. tenera). The proteins from
P. tenera also exhibit an amino acid composition close to that of ovalbumin (Mabeau and
Fleurence, 1993). The major amino acids in Chondrus crispus is arginine (33 %) and
amide N (10%) of total (Young and Smith, 1958).
The eight essential amino acids (cystine, isoleucine, leucine, lysine, methionine,
phenylalanine, tyrosine and valine) cannot be synthesised by animals and neither can they
be replaced by other “less valuable” building blocks. Generally, the first limiting amino acid
in most of the proteins of marine algae is lysine, one of the essential amino acids (Murata
and Nakazoe, 2001), and the various edible seaweed exhibit similar essential amino acid
patterns (Mabeau and Fleurence, 1993). All essential amino acids were detected in some
investigated brown and red seaweed species and red species featured uniquely high
concentrations of taurine when compared to brown seaweed varieties (Dawczynski et al.,
2007). Taurine is mostly found in fish, shellfish and seaweed. The taurine content is at a
level of 0.4 % of dw in Saccharina latissima and P. tenera which is also the case in lobster,
crab, shellfish and squid (Murata and Nakazoe, 2001). However, taurine levels of >1.2 %
3
A depsipeptide is a peptide in which one or more of the amide (-CONHR-) bonds are replaced by ester
(COOR) bonds
4 Available in Asian supermarkets, health or internet shops as dried food. Common name is “Arame”
34
was found in dried nori by abother researcher (Noda, 1993). Taurine is not a true amino
acid due to the lack of a carboxyl group, but contains a sulfonated acid group instead. This
amino acid is not used as building blocks in proteins but is found in e.g. the gall bladder
where it works as emulsifier which binds and eases the uptake of lipids. Taurine is
important for the formation of bile by which cholesterols are bound. Taurine thereby
facilitates reduction of cholesterol content in the blood of humans (Mouritsen, 2009). In
addition, taurine significantly reduced the elevated level of cholesterol in serum and liver in
streptozotocin induced diabetec rats. The cholesterol degradation was possibly enhanced
by taurine (Mochizuki et al., 1999). Taurine leads to decrease of the concentration of
cholesterol in the serum and liver in rats also exerts an anti-hypertension effect, and
prevention effect of vascular diseases, chronic hepatitis and diabetes (Mochizuki et al.,
1999).
The characteristic taste of nori is caused by the large amounts of the three amino
acids: alanine, glutamic acid and glycine (McHugh 2003b).
Nutritional value and digestibility of seaweed proteins
The nutritional value of proteins referred to as “amino acid score” is evaluated based on
the composition of essential amino acids. The amino acid score of the proteins of the
marine algae ranges from 60 to 100, a value higher than that of the proteins in cereal and
vegetables. The amino acid score of proteins in Porphyra and Undaria was 91 and 100,
respectively, and the same as that of animal foods (Murata and Nakazoe, 2001).
The in vivo digestibility of seaweed proteins is not well documented, and
available studies about their assimilation by humans have not provided conclusive results.
However, several researchers have described a high rate of seaweed protein degradation
in vitro by proteolytic enzymes such as pepsin, pancreatin and pronase5. For instance, the
digestibility in vitro of proteins from the red seaweed Porphyra tenera is higher than 70%
(Table 15; (Fleurence, 1999)). Digestibility of Ulva lactuca protein concentrates was 86 %
determined by a multi-enzyme method using different trypsins and peptidases (Wong and
Cheung, 2001c). However, for brown seaweed species, the high phenolic content might
limit protein availability in vivo, and thus moderate in vitro figures. This situation is probably
not found for the green and red seaweed, which possess low levels of phenols and higher
protein content (Mabeau and Fleurence, 1993).
Table 15. Relative digestibility in vitro of alkali or water soluble proteins from seaweeds (Fleurence, 1999).
Seaweed species
Pepsin
% digestibility*
Pancreatin
% digestibility*
Ulva pertusa [2] (green seaweed)
17.0
66.6
Undaria pinnatifida [2] (brown
23.9
48.1
seaweed)
Porphyra tenera [2] (red seaweed)
56.7
56.1
Palmaria palmata [7] (red seaweed)
56.0
* Relative digestibility is expressed as a percentage compares with casein digestibility basis (100 %).
Pronase
% digestibility*
94.8
87.2
78.4
-
Seaweed proteins in fish feed can decrease the demand for fish meal and furthermore
have positive effects on the fish and/or the consumer (see chapter on seaweed in feed).
5
Pronase is a commercially available mixture of proteinases isolated from the extracellular fluid of
Streptomyces griseus. Activity extends to both denatured and native proteins leading to complete or nearly
complete digestion into individual amino acids (Wikipedia, 2010)
35
The profile of essential amino acids in fish feed show that lysine, leucine, valine and
arginin should be present in largest concentrations (36-56 g/kg). However, the biological
value of the amino acids depends on the proteins composition in which the amino acids
usually combine with. According to Table 15 Ulva, Laminaria/Saccharina, Sargassum and
Chondrus have highest concentrations of lysine, leucine, valine and arginin, respectively.
Lysine, the essential amino acid being the first limiting amino acid in Laminaria and
Sargassum as mentioned, however this should have the major concentration in fish feed
(Murata and Nakazoe, 2001). The four mentioned genera/species with the best essential
amino acid contents also have rather high protein content. Protein content of up to 44 and
50 % on dry weight basis is found in Ulva and Porphyra, respectively (Table 14).
Total substitution of fish meal proteins by seaweed proteins is probably too
expensive. The essential amino acids cannot be replaced by other compounds, and all
need to be present in the right quanteties in order to make proteins. Extracts of scarce and
thereby valuable amino acids can therefore be of interest in fish or animal feed.
Lipids
Lipids are a broad group of naturally-occurring molecules which includes fats, waxes,
sterols, fat-soluble vitamins (such as vitamins A, D, E and K), monoglycerides,
diglycerides, phospholipids, and others. The main biological functions of lipids include
energy storage, structural components of cell membranes, and important signaling
molecules (Wikipedia, 2010). The lipids of marine algae consist of sterols, tri-, di-,
monoacylglycerols and phospholipids. Some researchers mention phospholipids as the
main lipids of marine algae (Murata and Nakazoe, 2001), however others claim that it is
the glycolipids that forms the major lipid class in all seaweed, followed by neutral and
phospholipids (Bhaskar et al., 2004).
Besides fatty acids, unsaponifiable fraction of seaweed contain carotenoids, such
as β-carotene, lutein and violaxanthin red and green seaweed and fucoxanthin in brown
algae and furthermore tocopherols6 and sterols (Table 16; see also later chapters)(Jensen,
1969a).
Table 16. Composition of lipids in seaweed related to total lipids extract and in brackets amount of pigments
in the fraction (% of total lipids)(Le Tutour, 1990; Khotimchenko, 2005)
Fucus vesiculosus
Fucus serratus
Ascophyllum nodosum
Gracilaria verrucosa
Neutral lipids
Glycolipids
Phospholipids
Triacylglyceride
Monogalactosyldiacylglycerides
Diagalactosyldiacylglycerides
Sulfoquinovosyldiacylglycerides
18.0 (26.7)
18.3 (45.4)
38.7 (23.1)
5.5
33.5 (3.9)
30.1 (~0)
32.6
63.3
Phosphatidylcholines
Phosphatidylglycerines
Phosphatidylinosites
Phosphatidylethanolamines
Inositephosphoceramides
4.7 (1.9)
2.7 (3.5)
4.7 (1.5)
31.2
6
Tocopherols are a class of chemical compounds consisting of various methylated phenols of which many
have vitamin E activity. They are fat-soluble antioxidants but also seem to have many other functions in the
body
36
Lipids represent up to 4.5 % of the
seaweed on a dry weight basis and lower
than that of other marine organisms.
Their contribution as a food energy
source thus appears to be low
(Table 17)(Mabeau and Fleurence, 1993;
Murata and Nakazoe, 2001). Like the rest
of the seaweed biochemical composition
the fatty acid content varies with
environment, season etc., but it is known
that algae accumulate PUFA when there
is decrease in the environmental
temperature (Khotimchenko, 1991). The
maximum content of lipids in the fronds of
Saccharina, Laminaria species and Alaria
esculenta was generally found in winter
(Haug and Jensen, 1954). However, the
total lipids of Fucus exhibit seasonal
changes and were most abundant in
summer (especially in August). In
Gracilaria
attached
specimen
accumulated twice as much lipid as the
unattached form, but with no difference in
fatty acid composition (Kim et al., 1996;
Khotimchenko and Levchenko, 1997).
Induction of n-3 fatty acids
production has been reported in
seaweed. Cell suspension cultures in
photobioreactors of Saccharina latissima
produces three sulphate fatty acids
deriving from an n-6 lipoxygenase
oxidation
(15-hydroxy-5,8,11,13eicosatetraenoic acid (15-HETE), 13hydroxy-6,9,11,15-octadecatetraenoic
acid (13-HODTA), and 13-hydroxy-9,11octadecadienoic acid (13-HODE). The
yields of 15-HETE, 13-HODTA, and 13HODE
ranged
from
100
to
1000 μg product/g dry biomass, but
Laminaria digitata (photo: Holdt, 2010)
addition of linoleic and γ-linolenic acid in
the medium, increased the yield of all
three sulphate fatty acids up to 400 % times (Rorrer et al., 1997a).
The lack of studies of the bioavailability of algal lipids presently limits their nutritional
evaluation (Mabeau and Fleurence, 1993). It is however suggested that algael 18:4n-3
affects the immune system in humans (Ishihara et al., 1998). Generally, n-3
polyunsaturated fatty acids exert an anti-arteriosclerosis, anti-hypertension, antiinflammation and immunoregulation effect etc. (Table 10)(Maeda et al., 2005; Khan et al.,
2007; Plaza et al., 2008).
37
Table 17. Fatty acid profiles of the interesting seaweed species. Fatty acid content and composition given in mean (% of dw and % of total fatty acid,
respectively).
0.3-1.8 % æ
0.5 % b, %
0.6% (stipe)z,æ
0.7-2.9 % z
1 % c, %
1.8 % e
2%#
2.1 % d
total
0.5-1.5 % g
0.5-2 %%
1.4 d
1.8 % b
3.1 % f,g
1.2 % d
1.9-4.8 %x
2-4 %%
1%h
2.4 % f, l
3.2 % j
4.5 % c
Sterols
C10:0
C12:0
Capric acid
Lauric acid
0.06 % c
0.1 % f
n.d. c
C14:0
Myristic acid
2.9 % c
14 % f
2.3 % c
3.2 % h
4.5 % f
0.21 % c
0.5 % k
1.4 % c
2.6-3.8 %%
3.9 % f
0.3 % l,ø
0.5 % b
0.6-0.7 %ω
0.6-1 %%
1.6 % å
0.7 % v
1-3 %%
Palmaria
Gracilaria
Red seaweed
Porphyra
Ulva
Sargassum
Undaria
Ascophyllum
Fucus
Green
Chondrus
Species of interest
Brown seaweed
Laminaria/
Saccharina
Common name
0.4 % k
0.9 % e
1.5 % n
2.6 % m
1.3 %β
0.2-3.8 % o
0.7-3 %%
2.0 % p, π
1.8 %
cultured π
0.06 % c
5.2 % α
3.4 % c
0.53 % h
1.8 % α
0.41 % c
5.1 % m
4.6 % n
6.4 % p
23-34 %c,j
63 % h
21 % α
30 % m
33 % n
33 % e
23 % p
3.3 % m
2.0 % n
6.8 % e
1.1 % p
0.122.5 %%
0.6 % e
0.7%b,$,ω
1.0 % h
1-2.8 % c
1.9 % j
0.02 %
0.40 % c
C15:0
c, j
C16:0
Palmitic acid
23-36 %
C17:0
C18:0
Stearic acid
0.16 % c
1.5-2.3 % c, j
10 % f
24 % g
24 % g
11-14 % c, j
17 % h
25 % f
27 % c
24 % f
0.04 % c
0.76 % c
1.0 % f
8.4 % l
1.4 % q
0.01 % c
n.d. c
n.d. c
C20:0
0.28 % c
C22:0
C24:0
C14:1(n5)
C14:1 (n9)
n.d. c
n.d. c
n.d. c
n.d. c
n.d. c
n.d. c
0.17 % c
0.14 % l
1.3 % q
1.1 % l
1.5 % q
0.20 % l
1.1 % q
14 % l
3.2 % q
0.20 % c
0.86-1.1 % c, j
0.69 % h
3.0 % f
0.39 % c
1.0 % f
16 % f
n.d. c
0.03 % f
0.30 % c
5.2 % f
0.04 % c
0.19 % l
6.5 % q
0.27 % l
9.5 % l
1.0 % v
12 % v
3.5 % v
0.19 % c
0.71.3 %c,j,α
1.2 % h
0.33 % c
0.5 % α
0.21 % c
0.09 % c
0.03 % c
0.8 % m
4.8 % q
38
Table 17. (continued)
1.7 % c
0.44 % c
3.7 % h
0.15 % c
8.0 % f
1.9 % l
3.6 % q
6.1 % v
2.0 % c
6.2 % h
2.7 % m
2.2 % n
1.6 % e
0.3 % m
0.4 % n
20.3 % q
C16:2 (n6)
C16:3 (n4)
C16:3 (n6)
C16:4 (n3)
C17:1(n7)
∑C18:1
C20:1(n9)
2.3 % h
C18:2 (n9)
C20:2 (n6)
C18:3(8t,10t,12c)
C18:3 (n3)
0.13 % c
13-28 % c, j
1.6 % c
0.12 % c
5.0-6.0 % c, j
n.d. c
0.02 % c
0.96 % c
n.d. c
n.d. c
6.8 % h
19 % f
22 % g
25 % f
22 % g
Oleic acid
7.7 % c
4.09 % c
n.d. c
0.64 % c
8.5 % f
-
Lineoleic acid
5.5-7.9 % c, j
12 % f
Linolenic acid (n-3)
0.87 % c
n.d.
0.8-3.9 % c, j
3.4 % f
1.6 % c
1.1 % f
27 % l
6.9 % q
9.4 % v
1.3 % q
8.3 % l
9.7 % q
0.97 % c
0.56 % c
0.41 % c
2.2 % f
3.2 % c
1.1 % c
0.09 % c
0.10 % c
1.8 % α
1.2 % c
C20:3 (n3)
0.01 % c
0.14 % c
0.42 % c
1.6 % v
9.4 % q
3.0 % q
4.4 % l
7.1 % q
5.6 % q
7.3 % m
8.4 % n
31 % e
1.29 % h
-
3.6 % c
8.1 % f
C20:3 (n6)
Gamma linolenic acid
(n-6)
2.1 % q
0.2 % c
3.1-11%c,j
1.5 % c
4.7 % h
1.5 % c
0.58 % c
6.7 % h
2.9 % α
6.1-7.4 % c, j
6.1 % f
6.2 % h
0.12 % c
0.34 % c
2.8 % f
11-12 % c, j
12 % h
1.7 % c
2.2 % f
0.57 % c
C18:3 (n6)
1.56 % h
0.5 % q
6.1 % q
C18:1 (n7)
C18:1 (n5)
C18:2 (n6)
5.2 % p
1.2 % p
C16:1(n5)
C16:1trans
C22:1(n11)
C22:1(n13)
C18:1(n9cis)
Palmaria
Ulva
Sargassum
Undaria
Ascophyllum
Fucus
1.2 % f
Gracilaria
Palmitoleic acid
Red seaweed
Porphyra
C16:1(n7)
Green
Chondrus
Species of interest
Brown seaweed
Laminaria/
Saccharina
Common name
4.3 % v
2.8 % p
5.2 % p
1.85.5 %c, j, α
1.17 % h
2.1 % m
1.3 % n
22 % e
0.71 % c
0.53 % c
0.23.3 %c, j, α
0.23 % h
1.18 % c
0.5 % m
1.0 % e
0.3 % m
1.4 % p
1.1 % p
2.6 % m
2.8 % n
39
Table 17. (continued)
C18:4 (n3)
Octadecatetraenoic
acid
1.2-3.9 % h,
4.3 % f
C20:4 (n6)
Arachidonic acid
11-12 % c, j
C20:5 (n3)
Eicosapentanoic acid
(EPA- ω3)
5.4-16 % c, h, j
Docosahexaenoic acid
(DHA)
n.d. c
n.d. c
14 % g
24 % f
14 % g
3.6 % f
15 % f
26-up
40%c, r, j
23 % h
0.8 % j
0.70 % h
12-13 % c, j
16 % h
19 % f
13-15 % c, j
9.4 % h
2.9 % f
√s
n.d.-15 % c, j
n.d c, j
to
n.d. c
3.2 % f
0.41 % l
Up to 40 %
6.6 % v
r
25 % t
PUFA (ω6)
15-HETE, 13HODTA, and 13HODE u
Saturated FA
Monosaturated
FA
Ratio n6/n3
21 % t
100 to
1000μg/g dwu
Palmaria
2.2 % p
2.43.9%c,j
0.24 % h
4.6 % q
5.3 % c
19 % f
0.34 % l
20 % v
42 % c
2.5 % f
1.0 % l
35 %v
0.09 % c
n.d. c
1.8 % f
0.8 % l
0.8 % j
0.07 % h
3.0 % α
4.68.9%c,j
6.8 % h
6.054 %c,h, j
50 % α
6.0 %h
0.05 % c
Non c, j
Other
PUFA (ω3)
Gracilaria
Red seaweed
Porphyra
Ulva
Sargassum
Undaria
Ascophyllum
Fucus
j
0.5 % j
C20:4 (n3)
C22:5n3 (n3)
C22:6n3 (n3)
Green
Chondrus
Species of interest
Brown seaweed
Laminaria/
Saccharina
Common name
√s
45 % h, t
22 % t
6.6 % l
20 % h
11 % h
34 % l
68 % v
37 % m
41 % n
2.72 % e
1.0 % m
0.5 % n
2.8 % e
2.6 % p
7.0 % m
3.8 % n
1.1 % p
7.2 % h,t
47 % p
26 % t
8.0 % t
45 % n
65 % h
19 % h
39 % n
11 % n
2.1 % t
0.3 c
0.1 t
1.3 c
0.5 c, h, t
1.3 l
0.6-1.8c
3.4 β
0.81 t
1.2 h, t
a= (Maeda et al., 2005), b= (Marsham et al., 2007), c= (Dawczynski et al., 2007), d= (Rioux et al., 2007), e= (Wen et al., 2006), f= (Herbreteau et al., 1997), g= (Kim et al., 1996), h= (Plaza et al., 2008), i= (Le
Tutour, 1990), j= (Murata and Nakazoe, 2001), k= (Marinho-Soriano et al., 2006), l= (Ortiz et al., 2006), m= (Khotimchenko and Levchenko, 1997), n= (Khotimchenko, 2005), o= (Morgan et al., 1980),
p= (Mishra et al., 1993), q= (Wahbeh, 1997), r= (Ishihara et al., 2000), s= (Khan et al., 2007), t= (MacArtain et al., 2007), u= (Rasmussen and Morrissey, 2007), v= (Tasende, 2000), x= (Jensen,
1960), z= (Haug and Jensen, 1954), æ= (Jensen and Haug, 1956), ø= (Foster and Hodgson, 1998), å= (Wong and Cheung, 2000), $= (Arasaki and Arasaki, 1983), ω= (Indergaard and Minsaas, 1991),
#= (McHugh, 2003), %= (Morrissey et al., 2001), π= (Mishra et al., 1993), α= (Noda, 1993), β= (Ortiz et al., 2009)
40
Fatty acids
Poly unsaturated fatty acids (PUFAs) are essential structural components of cell and
organelle membranes. Marine based long-chain PUFAs (LC-PUFA) have 20 or more
carbons with 2 or more double bond from the methyl (omega) terminus. The omega-3 LCPUFAs (n-3 LC-PUFA) are of particular interest. In this the first double bond is located in
the third carbon from the methyl terminus, and can contain up to six double bonds.
(Rasmussen and Morrissey, 2007). PUFAs are occasionally classified to two families
because of their metabolic connections. One is the linoleic acid family (n-6 fatty acid), and
the other another is the α-linolenic acid family (n-3 fatty acid) (Table 17). Marine lipids
contain substantial amounts of LC PUFAs, with n-3 fatty acids as the significant
component, and mono-unsaturated fatty acids. Eicosapentaenoic acid (EPA; 20:5 n-3) and
docosahexaenoic acid (DHA; 22:6 n-3) are the two important fatty acids of marine lipids,
along with the precursor α-linolenic acid (ALA; 18:3 n-3) and docosapentaenoic acid (DPA;
22:5 n-3). Both EPA and DHA are basically derived from ALA through elongation and
desaturation (Narayan et al., 2006).
The predominant fatty acid in various seaweed products is EPA (C20:5, n-3)
which is at concentrations as high as 50% of total fatty acid content (Dawczynski et al.,
2007). Marine algae also contain the n-3 PUFA 18:4n-3, which is not included in other
organisms. Notably red seaweed contains significant quantities of polyunsaturated fatty
acids such as eicosapentaenoic acid (20:5) and arachidonic acid (20:4). The green algal
species were unusual in containing 16:4 varying from 4.9 to 23.1 % of the total fatty acids;
16:0, 18:1 and 18:3 acids were also found in high amounts. Unsaturated fatty acids
predominate in all the brown seaweed studied, and saturated fatty acids in the red
seaweed, but both groups are balanced sources of
n-3 and n-6 acids. Processed seaweed (canned
and dried) are left with substantial nutritional value
of protein, ash, and n-3 and n-6 fatty acid contents
(Mabeau and Fleurence, 1993; Sanchez-Machado
et al., 2004a).
Algae are therefore a magnificent source
of eicosapentaenoic acid (EPA) n-3 (Plaza et al.,
2008) and an important source of supply of n-3
polyunsaturated fatty acids (PUFA) for the
maintenance of health (Murata and Nakazoe,
2001).
According to Table 17 Palmaria and
Sargassum has the best n-6/n-3 ratio (0.1 and 0.3,
respectively), which also have the highest total
lipid content of 3.9 % and 3.8 % respectively.
Gracilaria, Ulva and Fucus the highest contents of
oleic acid (31 %, 27 % and 25 %, respectively).
One study on Laminaria japonica has
shown seasonal variations in fatty acid content,
with n-3 PUFA to be most abundant during cold
months when algal thalli were very young,
however n-6 PUFA’s was maximal during warm
months (Figure 10).
Fucus serratus (photo: Holdt, 2010)
41
Figure 10. Monthly variation in polysaturated
fatty acid content n-3 (a) and n-6 (b) in
cultivated Laminaria japonica (Honya et al.,
1994).
a
The importance of algal PUFAs
Lipids play a major role in human
nutrition and health. They account for
about 40% of the total calories in most
industrialized countries and they reduce
b
the bulk of the diet, because of the
concentrated source of energy. In
addition, lipids are indispensable from
the human diet as they form the major
sources of essential fatty acids and
contain fat-soluble substances like
vitamins and carotenoids. Plants and
animals, including those from the
aquatic environment, account for most
of the dietary lipids. Vegetable oils
contribute with 70 % while marine oils contribute with about 2 % of the global oil
production, with the remainder being contributed by fats from land animals. The per capita
consumption of marine oils is approximately 1 g per day. Fatty acid composition of lipids
varies depending on the source and marine lipids generally contain a wider range of fatty
acids than their terrestrial counterparts including both plants and animals. Vegetable oils
usually consist of saturated and unsaturated fatty acids with 16 and 18 carbon chain
lengths, while marine oils mainly consist of C14-C22 fatty acids. The two long chained
PUFAs EPA and DHA have been shown to cause significant biochemical and
physiological changes in the body. The main effects of n-3 fatty acids on human health can
be divided into three main categories: 1. Their essentiality in specific organs; 2. Their
significant role in lowering blood lipids; 3. Their role as precursors for mediating
biochemical and physiological responses. However, physiological effects of n-3 fatty acid
depend on the variety. Humans have to directly intake ALA, EPA and/or DHA, to obtain
physiological effects of EPA and DHA. The major sources of EPA and DHA in the human
diets are marine products. Terrestrial plants can produce small to moderate amounts of
ALA, however, the mammalian system can not synthesize ALA. Major sources of EPA and
DHA are unicellular phytoplankton and seaweed. EPA and DHA are accumulated in fish
and other marine animals that consume algae and get passed on to other species through
the food chain. It was found that individuals consuming a normal diet had low tissue levels
of EPA and DHA while those who consume fish had higher levels in their tissue. Aquatic
species that live in colder waters generally contain larger quantities of PUFAs (Narayan et
al., 2006).
42
Phospholipids
Phospholipids (PLs) consist of fatty acids and a phosphate-containing compound attached
to glycerol or the amino alcohol sphingosine, resulting in compounds with fat-soluble and
water-soluble regions. Cell membranes utilise the dual hydrophilic and hydrophobic
characteristic of PLs to maintain structure and transport materials. Glycerol-containing PLs
include phosphatidic acid (PA), phosphatidylcholine (PC), phophatidylethanolamine (PE),
phophatidylinositol (PI), and phosphatidylserine (PS). Sphingomyelin (SPH), the other
major PL, consists of sphingosine and PC. Phospholipids contribute to lipoprotein
formation in the liver, nervous-system conduction and protection, memory storage and
muscle control. Choline, a major component of PC and SPH, functions as a methyl donor
and a precursor to the neurotransmitter acetylcholine (Miraglio, 2009). The amount of
phospholipids in various red seaweed species varied from 10 to 21 % of the total lipid (0.5
to 2.6 mg/g dw). The major phospholipids appeared to be PC (62–78 %) and PG (10–
23 %). The presence of an unidentified polar phospholipids varied from 2.7 to 10 % and
PE and DPG were found as minor phospholipids (Dembitsky and Rozentsvet, 1990). The
major phospholipids in Fucus vesiculosus and Ascophyllum nodosum is
phosphatidylethanolamine, but this represented less than 10% of the total acyl lipids
(Jones and Harwood, 1992). Phospholipids in diet act as natural emulsifiers and as such
facilitate and ease the digestion and absorption of fatty acids, cholesterol and other
lipophilic nutrients. A producer of marine phopholipids explains that these phospholipids
have many benefits over fish oils, because they are much more resistant to oxidation
(rancidity), have much higher contents of the physiologically important EPA and DHA,
provide these fatty acids with much better bio-availability and have much better spectrum
of health benefits for humans and animals. Compared with triglycerides, marine
phospholipids provide a highly synergistic approach to combining the positive effects of LC
omega-3 fatty acids with excellent stability, perfect bioavailability and a much wider range
of health benefits (Sørensen, 2009).
Glycolipids
Glycolipids are carbohydrate-attached lipids. Their role is to provide energy and also
serve as markers for cellular recognition. They occur where a carbohydrate chain is
associated with phospholipids on the surface of cell membranes (Wikipedia, 2010). The
red algae contained almost equal quantities of monoglycosyldiacylglycerol (MGDG),
diglycosyldiacylglycerol (DGDG) and sulphaquinovosyldiacyl-glycerol with some
exceptions. MGDG and DGDG were the major glycolipids in green seaweed. Glycolipid
contents of total lipid extracts of red seaweed ranged from 16 to 32 μmol/g dw, while
those in green algae varied from 11 to 32 μmol/g dry wt. Examination of the composition
of glycolipids in some brown algae showed that MGDG content varied from 26-47 %,
DGDG content from 20 to 44 % and sulphaquinovosylglycerol content from 18 to 52 % of
total glycolipids (Dembitsky et al., 1990; Dembitsky et al., 1991). Glycolipid content in two
Fucus species made up 14 % of the ester-soluble lipids (Dembitsky et al., 1990). The
major acyl lipids in F. vesiculosus and A. nodosum are monogalactosyldiacylglycerol,
digalactosyldiacylglycerol,
sulphoquinovosyldiacylglycerol
and
trimethyl-betaalaninediacylglycerol (Jones and Harwood, 1992). The highest concentration of saturated
and monounsaturated fatty acids was found in sulfoquinovosyldiacylglycerides for species
of Palmaria, Undaria and Ulva (Khotimchenko, 2003).
43
Sterols
Sterols occur naturally in plants, animals and fungi, with the most familiar type of animal
sterol being cholesterol. Sterols and related compounds play essential roles in the
physiology of eukaryotic organisms. Cholesterol is vital to cellular function, and a precursor
to fat-soluble vitamins and steroid hormones. In addition, cholesterol forms part of the
cellular membrane in animals, where it affects the cell membrane's fluidity and serves as
secondary messenger in developmental signalling (Wikipedia, 2010).
Content and type of sterols vary with the seaweed species. Green seaweed
species contain 28-isofucocholesterol, cholesterol, 24-methylene-cholesterol and βsitosterol, while brown seaweed contains fucosterol, cholesterol and brassicasterol. Red
seaweed contains desmosterol, cholesterol, sitosterol, fucosterol and chalinasterol
(Whittaker et al., 2000; Sanchez-Machado et al., 2004b).
The predominant sterol, fucosterol in the brown seaweed (Laminaria and Undaria)
makes up 83-97% of total sterol content (662-2320 μg/g dw) and desmosterol in red
seaweed (Palmaria and Porphyra), 87-93% of total sterol content (87-337 μg/g dw).
However, the red seaweed Chondrus crispus has cholesterol as its major sterol (SanchezMachado et al., 2004b; Kumar et al., 2008b).
A study on seasonal changes in sterol content of cultivated Laminaria japonica showed
that total sterols were higher from February to May with a maximum of 2400 μg/g dw in
May. Decrease was noted from late summer to autumn. The fucosterol constituted 7288 % of total sterol content and 24-methylene cholesterol with 9-28 %. The content of
fucosterol remained high from late spring to early autumn and 24-methylene cholesterol
was high during cold months (Honya et al., 1994).
It is reported that plant sterols such as β-sitosterol and fucosterol lead to the
decrease of the concentration of cholesterol in the serum in experimental animals and
humans (Whittaker et al., 2000).
Pigments
Chlorophylls
Chlorophylls are green lipid soluble pigments found in all algae, higher plants or
cyanobacteria that carries out photosynthesis. Chlorophyll a is essential in the reaction
centre of the thylakoid, light harvesting structures in which the photosynthesis is carried
out (Lobban and Harrison, 1994; Rasmussen and Morrissey, 2007). Chlorophyll is known
to be converted into pheophytin, pyropheophytin, and pheophorbide in processed
vegetable food and following ingestion by humans. These derivates show anti-mutagenic
effect and may play a significant role in cancer prevention. The cellular uptake and
inhibition of myeloma cell multiplicity were found to be greater for pheophorbide than for
pheophytin. Calculated on the amount of cell associated chlorophyll derivative, however,
pheophytin was more cytostatic/cytotoxic than pheophorbide. (Table 18)(Chernomorsky et
al., 1999).
The pigment content (violaxanthin, fucoxanthin, carotene and chlorophyll a) in
Ascophyllum was high in March to June (peak in May) and with minimum in July to
November. This seasonal variation was not so distinct in Fucus serratus, however
44
somewhat lower during autumn (Jensen, 1966).
Prelimenary studies on chlorophyll showed that
the content was three times higher in seaweed
growing in harbour districts compared to those
from an open sea locality (Larsen and Haug,
1958).
According
to
Table 18
the
chlorophyll a content was 565-2000 mg/kg on a
dry weight basis in the brown species reported.
Carotenoids
Carotenoids are nature’s most widespread
pigments, which are present in all algae, higher
plants and many photosynthetic bacteria. They
represent photosynthetic pigments in the red,
orange or yellow wavelengths. Carotenoids are
linear polyenes that function both as light energy
harvesters and as antioxidants that inactivate
reactive oxygen species formed by exposure to
light and air (von Elbe and Schwartz, 1996).
Carotenoids are tetraterpenes; carotenes are
hydrocarbons, and xanthophylls contain one or
more oxygen molecules (Table 18)(Lobban and
Harrison, 1994).
Saccharina latissima (photo: Holdt, 2010)
The major carotenoids that occur in seaweed include β-carotene, lutein,violaxanthin,
neoxanthin and zeaxanthin in green seaweed, α—and β-carotene, lutein and zeaxanthin
in red seaweed and β-carotene, violaxanthin and fucoxanthin in brown seaweed (Haugan
and Liaaen-Jensen, 1994).
According to Table 18 the β-carotene content was in the range of 36 to
4500 mg/kg (or ppm) on a dry weight basis with Porphyra with the absolute highest
content, and Palmaria palmata with the second highest of 456 ppm.
The content of β-carotene was found to be highest during warm months, when
the cultivated kelp Laminaria japonica was no longer growing (Figure 11)(Honya et al.,
1994).
Figure 11. Monthly variation in β-carotene content of
cultivated Laminaria japonica (Honya et al., 1994)
Experimental studies strongly suggests that βcarotene, with provitamin A activity, could
prevent the onset of cancers, especially lung
cancer (Astorg, 1997). However, other studies
suggest that β-carotene could induce lung
cancer in smokers.
45
Table 18. Pigments (mg/kg on a dry weight basis equals parts per million (ppm)) in seaweed, their possible usage in industry, source and bioactivity.
Pigments
Carotenoids
Linear polymer
Tetraterpenes
Light energy
harvester
Lipid-soluble
Use
β-carotene
Natural colouring of e.g.
margarine and fish
Astaxanthin
Orange-red pigm. in aquatic animals, pink colour in salmoid fish
Fucoxanthin
Has an unique
structure including an
unusual allenic bond
and 5,6-monoepoxide
in its molecule h, i
Fucoxanthin is
converted to
fucoxanthinol before
uptake in the digestive
tract f. Fucoxanthinol
is the deacetylated
product of fucoxanthinf
Violaxanthin
A major xanthophyll in brown
seaweed
Source
Laminaria digitata: 63 u, 336 $
Laminariajaponica: 0-20 β
Fucus serratus: 80 a, 105 y, 102173 u
F. vesiculosus: 95 y, 80 u
Ascophyllum nodosum:
35-80 $, 47-84 x, 50 y,
42-98 u
Sargassum sp.: 36-60 $
Ulva sp.: 310 $
Chondrus crispus: 84 y
Porphyra sp: 85 y, 4500 $
Palmaria palmata : 456 $
Gracilaria chilensis : 114 α
Usually found species of
microalgae
Laminaria digitata: 468 mg/kg dw
u
Laminari japonica::
178-213 mg/kg ww z
Ascophyllum nodosum j:
660 mg/kg dw k,
172-272 mg/kg dw u
Undaria pinnatifida (not destroyed
by cooking) l, æ, ø
Fucus serratus j:
495-720 mg/kg dw u
F. vesiculosus j: 340 mg/kg dwu
Sargassum siliquastrum m
Laminaria digitata: 110 mg/kg dwu
Ascophyllum nodosum t :
64-129 mg/kg dw u
Fucus serratus:
129-198 mg/kg dw u
Fucus vesiculosus: 162 mg/kg dw
Effect
Provitamin A activity å
Cancer prevention å
Antioxidant b
Antioxidant effect and retinoid-dependent signalling, stimulation of gap junctional
communications, impact on the regulation of cell growth and induction of detoxifying
enzymes, such as cytochrome P450-dependent monooxygenases c, d
Antioxidant activity up to 10 times stronger than other carotenoids
e
Weight reduction in white adipose tissue in rats and mice with 0.5 % and 2 % added to feed h, n, o
Anti-obesity effect f, h and increase the metabolism r
Reduced blood glucose and plasma insulin in rats and mice f
Increased the level of hepatic docosahexaenoic acid (DHA) in rats and mice f
Antioxidant activity p
Protective effect on UV-B induced cell injury in human fibroblast q
Beneficial effect on cerebrovascular diseases r in stroke-prone rats (SHRSP), independent of
hypertension ø
Inhibits chemical carcinogenesis s and decreased growth of leukaemia and prostate cancer cellsh
Preventive function against cancer and metabolic syndrome without side effects z
Inhibitory effect on human leukemia (HL-60) cells and colon cancer (Caco-2) cells æ
Significanlty attenuated neuronal cell injury in hypoxia and re-oxygenation ø
Possible preventive effect against neuronal cell death seen in SHRSP with stroke ø
u
Zeaxanthin and
Lutein
Is together with lutein the
predominant carotenoid of the
retina in the human eye
Ascophyllum nodosum:
Up to 100mg/kg at storage t
Gracilaria chilensis : 2.0 α
Canthaxanthin
Phycobiliproteins
Tetrapyrroles
Water-soluble
Chlorophylls
Tetrapyrroles
Lipid-soluble
Form stable conjugates with e.g. biotin and antibodies b
Natural colouring: chewing
gums, dairy products etc.
Chlorophyll a
Food and beverages
Laminaria digitata:
1250 mg/kg dw u
Ascophyllum nodosum:
830 mg/kg dw u,
565-1030 mg/kg dw u
Fucus serratus:
1572-2000 mg/kg dw u
Anticancer activity v
Chlorophyll b, c and d
a= (Haugan and Liaaen-Jensen, 1989), b= (Rasmussen and Morrissey, 2007), c= (Stahl et al., 2002), d=(Stahl and Sies, 2005), e= (Miki, 1991), f=(Sugawara et al., 2002), h= (Maeda et al., 2008b), i= (Maeda et
al., 2008a), j= (Le Tutour et al., 1998), k= (Jensen, 1969a), l= (Plaza et al., 2008), m= (Heo and Jeon, 2008), n= (Maeda et al., 2005), o=(Weinberger, 2007), p= (Le Tutour et al., 1998), q= (Heo and Jeon,
2008), r=(Plaza et al., 2008), s= (Okuzumi et al., 1993), t= (Jensen, 1969a), u=(Jensen, 1966)), v= (Chernomorsky et al., 1999), x= (Larsen and Haug, 1958), y=(Haug and Larsen, 1957), z=(Kanazawa et al.,
2008), æ=(Nakazawa et al., 2009), ø= (Ikeda et al., 2003)) , å= (Astorg, 1997), $= (Morrissey et al., 2001) , α= (Ortiz et al., 2009), β= (Honya et al., 1994)
46
Fucoxanthin is a xanthophyll and has an unique structure including an unusual allenic
bond and 5,6-monoepoxide in its molecule (Maeda et al., 2008b). Fucoxanthin is one of
the most abundant carotenoids in nature. The content in seaweed varies during season
and life cycle. It is quit stable in the presence of organic ingredient apart from surviving the
drying process and storage at ambient temperature. In pure form, fucoxanthin is
vulnerable to oxidation (Figure 12)(Haugan and Liaaen-Jensen, 1994). The total
carotenoid content of Fucus serratus was found to be ca. 0.08 % of the dried extracted
cells. Fucoxanthin comprises of about 70 % of the total carotenoid (Chapman, 1970;
Haugan and Liaaen-Jensen, 1989). According to Table 18 the fucoxanthin content ranges
from 172 to 720 mg/kg on a dry weight basis in the brown seaweed species, with maximal
concentration in F. serratus.
Waste parts of cultivated Laminaria japonica (kombu) are a good biosource for
fucoxanthin extraction. These Japanese kombu discards are made from production during
thinning and forming processes. Only some part of the frond is utilised and the discarded
parts are the top, middle and stipe including holdfast. These discards have similar content
of fucoxanthin (178-196 mg/kg fresh weight). The recovery ratio of fucoxanthin was 82 %
and 1490 g of fucoxanthin was obtained from 10 tonnes of kombu waste. The fucoxanthin
obtained was stable and reduced by only 2 % at 4 ºC in 6 months storage, although
fucoxanthin are known to be sensitive to oxidation (Kanazawa et al., 2008).
Fucoxanthin from fresh Undaria is mostly found as the geometrical isomer alltrans (~88 %). Trans forms are more stable, however cis forms of fucoxanthin were found
to exert higher inhibitory effect compared to their trans counterparts on human leukemia
(HL-60) cells and colon cancer (Caco-2) cells. Uptake and incorporation of trans form of
fucoxanthin into cellular lipids were faster compared to cis-counterparts (Nakazawa et al.,
2009).
Fucoxanthin is easily converted to
fucoxanthinol in human intestinal cells and in
mice (suggesting that the active form of
fucoxanthin in biological system would be
fucoxanthinol)(Sugawara et al., 2002).
Fucoxanthin from brown seaweed
Undaria, significantly reduces the viability of
human prostate cancer cells and significantly
reduces the percentage of tumour-bearing
mice and the average number of tumours per
mouse when given in the drinking water
(Table 18)(Okuzumi et al., 1993; KotakeNara et al., 2001).
Laminaria digitata (photo: Holdt, 2010)
47
Figure 12. Impact of storage at ambient temperature after drying of seaweed
material on different algal components (Haugan and Liaaen-Jensen, 1994).
Phycobiliproteins
Phycobiliproteins are unlike chlorophylls and carotenoids water soluble, and not lipidsoluble, and form particles (phycobilisomes) on the surface of the thylakoids, rather than
being embedded in the membranes. Phycobiliproteins consist of pigmented phycobilins,
which are linear tetrapyrroles. Different combinations of the two principal phycobilins,
phycoerythrobilin (red) and phycocyanobilin (blue), that absorb different regions of
wavelengths, gives different absorption spectre (Lobban and Harrison, 1994). This
additional photosynthetic pigments makes light harvest possible at deep waters, because
more than 10 m below the water surface light wavelengths for some colours are almost
completely absorbed (Voet et al., 1999). No concentrations and bioactivity has been
reported for this pigment.
48
Minerals
Together with vitamins, the role of trace elements such as manganese (Mn), copper (Cu),
zinc (Zn), selenium (Se), nickel (Ni) and molybdenum (Mo) in algae appear to be as
enzyme cofactors. In addition is potassium (K) an enzyme activator, iron (Fe) important for
electron transfer in the respiratory chain and in photosynthesis. Sulphur (S) is incorporated
into the amino acids cysteine and methionine, which are important in maintaining the three
dimensional configurations of proteins through sulphur bridges. Calcium (Ca) is important
to all organisms for maintenance of cellular membranes, magnesium (Mg) is an essential
component of chlorophyll, and phosphorus (P) plays key roles in many biomolecules, such
as nucleic acids, proteins, and phospholipids. Nitrogen (N) has major metabolic
importance in compounds, such as amino acids and sugars, amines, purines and
pyrimidines (references in (Lobban and Harrison, 1994)).
Marine algae are known to be high in mineral content and are used as foods for
supply of minerals. As mentioned previously 10 to 100 times higher content than in
traditionary vegetables.
Ash and thereby mineral content of the species of interest in Denmark reaches
levels of up to 55 % on a dry weight basis (Table 4). Ash content in most land vegetables
is usually much lower than in marine seaweeds. Sweet corn has a lower content (2.6%),
while spinach has an exceptionally high mineral content (20 %) (Rupérez, 2002).
The mineral composition varies according to phylum as well as various other
factors such as seasonal, environmental, geographical and physiological variations. Most
of the seaweed species have high calcium, magnesium, phosphorus, potassium, sodium
and iron contents (Mabeau and Fleurence, 1993). All seaweed offer extraordinary level of
K that is very similar to our natural plasma level, and high intake of Ca, K and Na are
associated with lower risk of hypertension (reference in (Kumar et al., 2008b). During
processing to produce the sheets of nori, most salts are washed away, so the sodium
content is low (McHugh 2003b). Grinded seaweed can be a substitute of the table salt,
because the kalium (K) from seaweed is healthier than the sodium (Na) in table salt
(Mouritsen, 2009).
As a summary of Table 19, the species of Laminaria/Saccharina and Ulva were
the species of interest in Denmark with the highest content in most minerals. The
Laminaria/Saccharina had highest contents of Na, K, I, Mn, and Se and Ulva of Na*, P,
Ca, Fe, and Mn*. These speceis were followed by Ascophyllum (Na*, Zn, and Cu),
Sargassum (Mg and As) and Palmaria (Fe) species.
Some of the minerals are necessary for our health while some are toxic in varying
degrees. Laminaria japonica (kombu) is an excellent source of iodine, and it has been
used in China as dietary iodine supplement to prevent goitre, and has also been used for
medical and food purposes for over 1,500 years in China, Japan and Korea. Most of the
kombu is dried and eaten directly in soups, salads and tea, or used to make secondary
products with various seasonings (sugar, salt, soy sauce; (Lobban and Harrison, 1994).
The results of a study on the feasibility of naturally iodized salt, using seaweed as a source
of I, indicated that the level of iodine in seaweed ingredient is constant, consumer
acceptable, and of equal bioavailability of I (Mabeau and Fleurence, 1993). Species of the
genus Laminaria are the strongest iodine accumulators among all living systems and the
accumulation can be up to 30,000-fold that of the surrounding evironment (Table 15;

Several species shared the same high concentration
49
(Bartsch et al., 2008b). However, too much iodine can trigger a hyperactive thyroid gland
and cause goitre, just as if you don’t get enough iodine (Cloughley et al., 2008). Red,
green and other species of brown species of seaweed also accumulate iodine as for the
other minerals but not in such high concentrations (Table 19).
Palmaria (dulse) is a good source of minerals, being very high in iron and
containing all the trace elements needed in human nutrition (Figure 5; (McHugh, 2003)).
Raw Undaria (wakame) contains appreciable amounts of essential trace elements such as
Mg, Cu, cobalt (Co), Fe, Ni, and Zn similar to kombu (Lobban and Harrison 1994).
Selenium salts are toxic in large amounts, but trace amounts of the element are
necessary for cellular function in most, if not all, animals (Wikipedia, 2010). This mineral is
scarce in nature and therefore of high added value. A study showed that selenium was
most abundant in red seaweed (0.15-0.43 ppm) relative to that in green (0.05-0.26 ppm
which equals 0.005-0.026 mg/100 g) and brown seaweed (0.014-0.14 ppm) and
predominantly associated with amino acids and proteins (69-94 %). It was not present as
characterizable inorganic selenium species (Maher, 1985).
The maximum iodine content was found in L. digitata in February (1.2 % on a dry
weight basis which equals 1,200 mg/100 g) and higher than what was found in Saccharina
(0.5 %) and L. hyperborea (0.7 %)(Haug and Jensen, 1954). Iodine content of L. digitata
and L. hyperborea was highest during winter (Jensen and Haug, 1956).
A seasonal study on L. japonica from March to October showed that the iron
content (0.02-0.07 % on a dw basis) remained almost constant in this period, calcium
content increased toward autumn (0.7-1.2 % on a dw basis), and magnesium and
phosphate decreased toward autumn (1.3-0.6 % and 0.5-0.2 % on a dw basis,
respectively)(Honya et al., 1994).
The absorption of minerals might be limited by the linkage between certain
minerals and polysaccharides such as alginate, agar and carrageenan. In such cases,
mineral bioavailability is a function of the type of linkage between the polysaccharide and
the mineral, and also of the digestibility of the polysaccharide. For instance, the weakness
of the linkages between polysaccharides and iodine allows rapid release of this element. In
contrast, the strong affinity of divalent cat ions (particularly calcium) for carboxylic
polysaccharides (alginates) probably limits the availability of associated minerals. From a
nutritional standpoint, this high affinity might be compensated for by the high mineral
contents of seaweed (Mabeau and Fleurence, 1993).
50
2800
11579
a
4000 p
4322
3825 j
5000-11000
p
4300
p
2300
100-150
4400 b
350
938
a
150
730-1030
p
700
p
3000
p
1000-3000
e
931
960
b
2875 j
p
1000
420 a
1400
390 a
b
a
250 p
994
e
1181
1000-3000 e
540 g
1125 j
430 g
4.2
7.6
3.9 b
<1.0-8.0 c
52 c
4.0-80 e
15-100 k
g
730
75
j
397 g
i
900-1300 p 200-800 p
732
a
565
11 g
280 p
670-835 p
a
4.0
a
5.0-10
200-500 p
10.3
55 b
12 b
2.0-4.0 c
3.0 c
11-19 c
8.0-40 e
15
10-18
p
14
15-140 e
6-100 e
g
13 i
p
200-500 p
a
10
g
42 h
p
300
170-500 e
55 h
15 i
200-800p
a
7.0 b
9.0
139 h
i
470
730 p
560-1200 e
2000-5200 e
1000-16000 p
0.1 p
a
e
a
500-900 k
a
1400
130-150 p
500-2000 e
567-786 p
20 d
860-5600
i
800
390 b
270 h
i
100-300 p
a
190 h
p
600 g
1300
1240-1320 p
RDI
360 e
330 g
1100-3000
i
659
7800 p
580 b
90-270
140
e
2898 h
13
7000-9000 e
54 d
500-3000
3.3
e
100 b
e
p
a
Palmaria
2100 b
e
73 d
800
3500
2020 g
200-600
k
800-3000p
a, p
31 h
p
b
710
Fe (iron)
a
190 g
a
1005
Gracilaria
Ulva
3184
5500 b
7900-9500
k
g
2000-2600 p 500-3200 p
h
159
Mg (magnesium)
1700-2500e
200 g
190 g
Ca (calcium)
1100 p
a
400 b
150-800
900-5900 e
270
p
200 b
e
120 b
1500-1700 p
5500-6300
394 g
3627 a
g
8699
e
4270 a
b
1600-7000 e
3490
2000-3000k
1300-10600
1400
3000-4000 p
a
6100 b
Sargassum
Undaria
j
5865
2000-5200 p
P (phosphorus)
Ascophyllum
3000-4000k
g
1030
b
6100
900-6000 e
K (potassium)
7064 a
5469 a
b
Porphyra
3818 a
Chondrus
Na (sodium)
Fucus
Laminaria/
Saccharina
Table 19. Mineral content (mg/100 g on a dry weight basis) in the seaweed species of interest in Denmark.
RDI: Recommended Daily Intake
29 i
9.2-14
87 i
p
87-137
26 h
23 i
p
17-21
p
5.6-35 p
5.6-35 p
51
200-1000 e
25 e
17-18 c
RDI
Palmaria
Gracilaria
Porphyra
43 c
Chondrus
6-10 c
Ulva
Sargassum
73 c
Undaria
23-211 c
I (iodine)
Ascophyllum
Fucus
Laminaria/
Saccharina
Table 19. (continued)
0.150
2.0-25 e
10-100 e
250-1150 f
304 h
70-125 k
193-471 i
91 j
80-500 p
1.8
18-35 i
50 p
a
3.7
0.85-2.2 c
70-120 p
a
5-20
k
2.4 c
13 h
2.9-3.0 p
Mn (manganese)
<0.5
300 i
1,1 i
0.5 i
20-30 p
15-55 p
1.4-8.0 p
a
5.5
0.30-0.68 c
a
3p
1.7
7.1
1.3-1.4 c
0.4 c
0.83-2.7 r
0.47-1.9 r
7.0-24 p
1-5
k
0.7-1.6 p
0.56-0.61 r
a, p
5.2-5.3 r
2.0 p
a
13 p
a
<0.5
<0.05 c
1.0-1.5 p
a
0.14 c
4j
0.43 h
As (arsenic)
0.3-0.5 p
0.4 p
c
c
2.9-7.6
2.0
4.7-5.3 m
Se (selenium)
0.1-1
k
0.58 c
0.01-0.57
0.023 h
5.0 m
c
0.1
c
0.6-1.5 p
2.7
<0.5
0.11-0.17 r
0.18-0.78 r
1.8-3.5 p
0.9-1.1 p
2.0-5.5
c
3.2-4.2 m
0.3
35 p
c
0.2-2.8 p
<0.5
0.09 c
8.8
0.4
0.30-0.32 r
c
a
0.73
<0.5
1.0-16 p
a
0.16-0.22 r 0.63-0.89 c
0.56 p
0.28 h
0.79 p
2.9
5.2 m
0.67 h
0.7-8.3 p
0.77 h
c
12-14 m
2.9 p
3.2-4.9 c
a
<0.05-0.11 c
6.4 h
a
6.4 h
0.1-1.6 p
<0.5
3.1-3.7 c
4.1 p
1.3
0.33-0.65 c
2.2
15-55 p
a
2.3 h
a
0.84
2.8 c
24 p
a
32 h
Cu (copper)
426 h
l
150-1200
Zn (zinc)
3.6 h
1.1 p
c
2.4-3.0 m
0.2
0.003 h
0.08
7.6 m
c
nd h
q
a= (Rupérez, 2002), b= (Murata and Nakazoe, 2001), c= (van Netten et al., 2000), d= (Marsham et al., 2007), e= (Mabeau and
Fleurence, 1993), f= (Haug and Jensen, 1954) (Rupérez, 2002), g= (Tititudorancea, 2009), h= (Wen et al., 2006), i= (Arasaki and
Arasaki, 1983), j= (MacArtain et al., 2007), caculated from dw/ww ratio of 1:5 given in (Vadas et al., 2004), k= (Jensen, 1960),
l= (Jensen and Haug, 1956), m= (Almela et al., 2002), p= (Morrissey et al., 2001), q= (Noda, 1993), r= (Besada et al., 2009a)
52
Vitamins
Vitamins are organic compounds required as a nutrient in tiny amounts by an organism.
Compounds are called a vitamin when it cannot be synthesised in sufficient quantities by
an organism, and must be obtained from the diet. They are classified by their biological
and chemical activity, not their structure. Thus, each "vitamin" may refer to several vitamer
compounds that all show the biological activity associated with a particular vitamin. Such a
set of chemicals are grouped under an alphabetised vitamin "generic descriptor" title, such
as "vitamin A", which includes the compounds retinal, retinol, and four known carotenoids.
Vitamers are often inter-converted in the body. Vitamins have diverse biochemical
functions, including function as hormones (e.g. vitamin D), antioxidants (e.g. vitamin E),
and mediators of cell signaling and regulators of cell and tissue growth and differentiation
(e.g. vitamin A). The largest number of vitamins (e.g. B complex vitamins) functions as
precursors for enzyme cofactor bio-molecules (coenzymes) that help act as catalysts and
substrates in metabolism. For example, biotin is part of enzymes involved in making fatty
acids. Vitamins also act as coenzymes to carry chemical groups between enzymes
(Wikipedia, 2010).
The vitamin profile of seaweed can vary according to algal species, season, algal
growth stage and environmental parameters just like the rest of the compounds. Most red
seaweed (e.g. Palmaria palmata and Porphyra tenera) contain large amounts of
provitamin A as mentioned and significant quantities of vitamins B1 and B2. Vitamin B12 is
also found in these species and in certain green seaweed (Arasaki and Arasaki, 1983).
Vitamin B12 is not found in terrestrial plants. Porphyra can be called the great repository of
vitamins: especially choline, lipoic acid, B6, B7 and B12 and has the highest content of
vitamin A (Arasaki and Arasaki, 1983; Nisizawa et al., 1987). The content of all types of
vitamins in Porphyra complex is higher than that of spinach (contains a large amount of
vitamins), especially, that of vitamin A is about 3 times the content in carrot (Table 12;
(Murata and Nakazoe, 2001)).The amount of the vitamin B group is generally higher in
Ulva than that of common vegetables. In contrast, the vitamin A content is approximately
only half as much as that of spinach (Nisizawa et al., 1987).
The content of vitamins in the seaweed species of interest in Denmark varies
between species and also within species. Porphyra species has the highest content of
most the vitamins; vitamin A, C, E, B2, and B6. The highest content of vitamin K and B12 is
found in Palmaria followed by the species with only maximal content within one vitamin; B 1
in Ascophyllum, B3 in Ulva and B7 in Fucus species (Table 20).
The vitamin content of brown seaweed appears less remarkable. However, it
should be noted that most of the vitamin analyses carried out on brown seaweed have
used commercial algal products (meals or powders) that had been submitted to
transformation processes (e.g. high-temperature drying and cooking) known to alter the
vitamin content greatly, especially for vitamin C. The content of vitamin C in algae varies
depending on the state of the product; highest in raw material, since vitamin C is
decomposed under drying conditions and/or during processing (see ascorbic acid in
Figure 12)(Arasaki and Arasaki, 1983; Nisizawa et al., 1987; McHugh, 2003).
Air-dried Undaria (wakame) has similar vitamin content to the wet seaweed and is
relatively rich in the vitamin B group, especially niacin (B3); however processed wakame
products lose most of their vitamins (Lobban and Harrison 1994). In contrast, studies on
Ascophyllum showed that the drying process did not lower the B3 content (Jensen, 1956).
53
Vitamin A
140-810 a
590-1500 b
560 IU c
36 d
0.1-0.5 k
0.24 g
e
0.11
0.48 c
2.7
0.5 p
Riboflavin (B2)
0.5-1.0
0.20 e
0.5-1.0
0.6-22 l
l
8.6
38
p
1.0-2.9
2.0 l
1.3 l
100 i
90 i
p
9.8
0.013 i
5.0-9.8
3.2 i
0.01-0.05
n
0.031-0.078 m
0.2-1.2
n
0.07
11
0.9
k
50-200
12
0.0006 e
0.006 e
0.0006 p
0.6 p
g
12
15 c
0c
11 e
15 e
0e
Vitamin K
p
50-165
20-60 f
25-50 f
0.36
p
RDI
Palmaria
0.003 m
g
0.001
0.01-0.03 e
4.0 g
221
g
60
100 c
10 e
20 e
p
107 h
1-3
p
13-111
33 d
p
15-28p
5.7 g
i
1.7
0.91 p
16 i
8.9 p
0.06-0.4 p 1.0-2.0 p
b
10-20
26-45 p
1k
0.9 p
160 i
p
10-70
0.025 i
p
0.005 m
25 c
3.4
0.2-1.9 p
k
0.00008
g
0.01
i
0.01-0.06 p
0.89 p
10 i
p
1.5 i
p
0.005-0.044 j,k
0.03-0.9 n
i
1.4 l
2.0
p
0.0003 e
2.0 d
0.25 p
9.5 i
p
8.2 i
Vitamin E
1.0 i
p
1.0 e
p
1.2-1.8
0.73 d
q
0.01 g
0.035-0.042 m
13
1.6
11 q
~0.0004
Vitamin C
i
e
0.2-6.0
0.7p
g
0.9-1.2 e
l
1.0-3.0
6.4 i
Vitamin B12
1.2
0.01 g
0.27
0.3-0.6 g, p
2.5
0.03 e
0.38
p
0i
p
i
0.95-2.5 j,k
0.5-3
0.3 i
1.27 d
11.7
p
0.96 i
3.4 c,i
0.73 i
i
2.3 l
3.4
b
0.57
0.14 e
61 i
Biotin (B7)
0.92
g
0.32 e
10-45
0.75
i
0.12-0.25
0.25 p
k
0.14 c
2.2
Vitamin B6
5.0
1.15 c
0.14
0.06
1.4
e
1.2 c
i
0.37 c
1.78 d
Niacin (B3)
i
0.1-0.5 p
g
0.66
0.01
e
-d
13 q
0.08 b
e, c, p
0.30 c
i
0.14
e
0.8
14000 IU c
1800 IU c 310 IU c
0.22 g
0.08
Gracilaria
16000 IU q
3160 d
Thiamin (B1)
Porphyra
Chondrus
Ulva
Sargassum
Undaria
Ascophyllum
Fucus
Laminaria/
Saccharina
Table 20. Vitamin content (mg/100 g dw) in the seaweed species of interest in Denmark.
d
10
1.0
d
330 p
1.4 i
16 i
a= (Darcy-Vrillon, 1993), b= reference in (Nisizawa et al., 1987), c= (Murata and Nakazoe, 2001), d= (Wen et al., 2006), e= (Arasaki and Arasaki,
1983), f= (Jensen, 1969b), g= (Tititudorancea, 2009), h= (Ortiz et al., 2006), i= (MacArtain et al., 2007), B12 caculated from dw/ww ratio of 1:5
given in (Vadas et al., 2004), j= (Larsen and Haug, 1958)), k= (Jensen, 1960), l= (Larsen, 1958), m= (Larsen, 1961)), n= (Karlström, 1963),
p= (Morrissey et al., 2001), q= (Noda, 1993)
IU= The International Unit is a unit of measurement for the amount of a substance, based on measured biological activity or effect. 1 IU is the
biological equivalent of 0.3 μg retinol, or of 0.6 μg beta-carotene in the USA, and of 0.3 μg beta-carotene in Canada (Wikipedia, 2010).
RDI= Recommended Daily Intake
54
Though it is reported that the content of vitamin D is very low in marine algae, it is
confirmed that the green seaweed Enteromorpha intestinalis and the brown F. vesiculosus
contain ergosterol, i.e. provitamin D, and vitamin D3, respectively (Murata and Nakazoe,
2001).
As mentioned, the red seaweed Palmaria contain high contents of vitamin E
(tocols), followed by Ulva abd Ascophyllum and Fucus species (Table 20). Vitamin E
includes α-, β- and δ-tocopherol and acts as antioxidants (Kumar et al., 2008b). The
species of tocols are given in Table 21.
Table 21. Vitamin E (tocols) content (mg/kg on a dry weight basis, or based on the lipid content) and effect
and variations in some of the seaweed genera of interest in Denmark.
Compound
Effect and
variations
tocols (total)
Seasonal Variations;
highest content in
autumn and winter a
α-tocopherol (stable
to heat and acids,
unstable to alkali)
Antioxidant b
Highest content in
oldest part
Laminaria
(mg/kg dw)
0.1 c
2-30 g
Fucus
(mg/kg dw)
38-73 c
Ascophyllum
(mg/kg dw)
Ulva
(mg/kg lipid)
Gracilaria
(mg/kg dw)
250-500 a
1071 d
392 f
125 e
92 (average of 10)a
195 a
34 c
9d
87 f
α-tocotrienol
33 d
β-tocopherol
14 d
32 f
26 d
9.5 f
964 d
264 f
25 d
-
gamma-tocopherol
0.1 c
14-29 c
70 e
12 c
gamma-tocotrienol
δ-tocopherol
19-37 c
110 e
17 c
a= (Jensen, 1969b), b= reference in (Plaza et al., 2008), c= (Le Tutour, 1990), d= (Ortiz et al., 2006), e= (Jensen, 1969a), f= (Ortiz et
al., 2009), g= (Honya et al., 1994)
Seasonal changes of α-tocopherol were
found in cultivated Laminaria japonica with
highest content during the warm months,
when the kelp was no longer growing
(Figure 13)(Honya et al., 1994).
Figure 13 Monthly variation in α-tocopherol content
in cultivated Laminaria japonica (Honya et al., 1994)
Studies of seasonal variations show that the ascorbic acid (vitamin C) content in
Ascophyllum is higher (160 mg/100 g) during summer and niacin (B3) content is highest in
May and can reach levels of 3 mg/100 g on a dry weight basis (Jensen, 1960). The niacin
content of L. hyperborea and L. digitata was highest during March to June with
concentrations of up to 3.5 mg/100 g dw and 4.5 mg/100 g dw, respectively (Jensen,
1956).
Maximal content of biotin (B7) was found in L. hyperborea in February to April and
with a minimum during summer (second maximum during the fall and early winter).
Irregular and lower content of biotin was found in L. digitata with a maximum reached in
May and a minimum in during fall. Fucus serratus showed similar variations as in the
Laminaria species whereas almost no variations were seen in Ascophyllum. The young
parts of tissue contained more biotin than the older parts of Ascophyllum. More biotin was
55
found in samples of Ascophyllum, F. serratus and F. vesiculosus harvested near an
estuary than those from open-sea localities (Larsen, 1961).
Less content of vitamin B12 is found in species of Fucales compared to
Laminariales. A clear seasonal tendency was found L. digitata with a maximal
concentration from January to April and a minimum from July to August. This tendency
was irregular in L. hyperborea (Karlström, 1963).
Phenols and other phorotannins
Phenols, sometimes called phenolics, are a class of
chemical compounds consisting of a hydroxyl group (-OH)
bonded directly to an aromatic hydrocarbon group. The
simplest of the class is phenol, the parent compound
used as a disinfectant and for chemical synthesis.
Examples of other phenols are: Estradiol (estrogen
hormones), eugenol (the main constituent of the essential
oil of clove), gallic acid (found in galls), polyphenol (e.g.
flavonids7 and tannins8) and tyrosine (an amino acid)
(Wikipedia, 2010). Polyphenols from terrestrial plants are
derived from gallic and ellagic acid, whereas the algal
polyphenols are derived from polymerised phloroglucinol
units (1,3,5-trihydroxybenzene). Phlorotannins are a
group of phenolic compounds. Phlorotannin constitute an
extremely heterogeneous group of molecules (structure
and polymerisation degree heterogeneity) providing a
wide range of potential biological activity (Table 14;
(Burtin, 2003)). Phlorotannins are localised in physodes,
which are membrane-bound cytoplasmic vesicles. Fusion
of physodes with cell membranes results in a secretion of
phlorotannins (Lüder and Clayton, 2004; Bartsch et al.,
2008a) (Li et al., 2009). The size of the physodes is about
2500 μm in Fucus serratus and Laminaria hyperborea
and appearance does not differ much. The reducing
power (up to 3.0 m. eq./g dw) increased with increasing
physodes volume (3-11 %) of the volume of the entire
seaweed tissue of F. serratus, F. vesiculosus and
A. nodosum (Baardseth, 1958). Reducing power also
correlated positively with the dry matter content
(correlation coefficient of 0.73; (Larsen and Haug, 1958)).
Sargassum muticum (photo: Holdt, 2010)
7
A class of plant secondary metabolites collectively known as Vitamin P and citrin (Wikipedia, 2010).
Tannins are astringent, bitter plant polyphenols that either bind and precipitate or shrink proteins and
various other organic compounds including amino acids and alkaloids. The astringency from the tannins is
what causes the dry and puckery feeling in the mouth following the consumption of unripened fruit or red
wine. Likewise, the destruction or modification of tannins with time plays an important role in the ripening of
fruit and the aging of wine (Wikipedia, 2010)
8
56
Figure 14. Phenolic concentration (% of dry weight) in eight species of brown seaweed (mean±CI).
Pc= Pelvetia canaliculata; Fspi= Fucus spiralis; Fv= F. vesiculosus; An= Ascophyllum nodosum;
Fser= F. serratus; Bb= Bifurcaria bifurcate; He= Himanthalia elongata; Ld= Laminaria digitata.
The arrow demonstrates the habitat of the species from high shore (left) towards low shore (right).
Letters correspond to the results of Fisher’s LSD test. Results with the same letter above the error bar
are not significantly different at p<0.05 (Connan et al., 2004).
Green and red seaweed have low concentrations of phenols (Mabeau and Fleurence,
1993) compared to brown seaweed, which have high concentraions of the phenol group
phlorotannin. Phenol content varies from less than 1 % to 14 % of dry seaweed biomass
with Ascophyllum and Fucus as the species with the highest content (14 % and 12 %,
respectively) (Figure 14; Table 22).
Table 22. Phenolic (or when mentioned phlorotannin) content of seaweed genera of interest in Denmark.
Figures are given in percentage of dry weight. GAE= Gallic acid equivalents
Seaweed genera
Concentration
0.2-2.6%a
~0.2%b
less than 0.4%c
1.3-3.1% d
Up to 5.3 % j
Fucus
less than 0.4%c
0.7-8.5 % k
1.0-12.2 % k
>2% (2-6%) b
2.17 % q
Ascophyllum
0.5-14 %j
4-13% k (phlorotannin)
4-13% f
5 % a, e (phlorotannin)
Undaria
less than 0.4 % c
Sargassum
Yes with rapid rates of turnover g
1.1-2.3 % o
2-3% h
5.1 % of GAE m
6% a
12.7 % i
1.68-2.97 % q
Ulva
0.9 % of GAE n
Chondrus
less than 0.4% c
Porphyra
less than 0.4% c
Gracilaria
1.6 % of GAE p
a= (Connan et al., 2006), b= (Connan et al., 2004), c= (Rupérez and Saura-Calixto, 2001), d= (Hammerstrom et al., 1998), e= (Pavia et al., 1997), f=
(Pavia and Åberg, 1996), g= (Arnold and Targett, 2000), h= (Zubia et al., 2008), i= (Cho et al., 2007), j= (ref in (Horn, 2000)), k= (Haug and Larsen,
1958), m= (Lim et al., 2002), n= (Wong and Cheung, 2001c), o= (Wong and Cheung, 2001a), p= (Ganesan et al., 2008), q= (Chkhikvishvili and
Ramazanov, 2000)
Laminaria/Saccharina
57
Concentrations of polyphenols exhibits seasonal variations, but also varies within the
different parts of thalli such as; old versus new thalli, basal part or frond (Figure 15;
(Johnson and Mann, 1986)). Polyphenol content shows significantly temporal correlation
with the reproductive state of the algae. The polyphenol content in Ascophyllum is at a
minimum (~9-10 % of dw) during the period of maximal fruit body shedding (May), and
reaches a maximum (~12-14 %) during the “winter season”. In F. vesiculosus the minimum
(~8-10 %) is one to two months later, just before the period of maximum fertility.
Thereafter, the content rises to a maximum (~11-13 %) during the period of sterility
(August to March) (Ragan and Jensen, 1978). This does however not correspond to the
seasonal phenolic content shown in Figure 15. In this study the highest phenolic content in
F. vesiculosus is during summer. Seasonal variations in phenolic content are more
pronounced in some seaweed species like F. vesiculosus and Himanthalia elongata (sea
spaghetti) compared to that of L. digitata (Figure 15).
The content can also vary due to other environmental factors such as and salinity.
The reducing power of polyphenols was
10 times
higher
in
species
of
Ascophyllum from open coast localities
than from specimen from fjords near
river outlets (Baardseth, 1958; Larsen
and Haug, 1958). Preliminary studies of
polyphenols in
seaweed
species
collected in Denmark show that species
of
Fucus
showed
the
highest
antioxidative activity compared to
species such as e.g. Sargassum and
Laminaria (of the brown seaweed
species). The antioxidative activity was
tested with four methods; in vitro
established systems such as antioxidant
activity in liposome model systems, 1,1diphenyyl-2-picrylhydrazyl
(DPPH)
radical scavenging activity, reducing
power and metal chelating activity.
Ethanol extracts had the highest
antioxidant activity compared to water
extracts. Extracts were made from
freeze
dried
seaweed
samples
(unpublished data Farvin and Jacobsen,
2009).
Drying has no influence on the reducing
power of the Fucaceae, but this is not
the case for Laminaria and Ascophyllum
species. In these species the reducing
Fucus vesiculosus (photo: Holdt, 2010
power is usually markedly low in dry
samples (Haug and Larsen, 1958).
58
Figure 15. Seasonal variations of phenolic content in Laminaria digitata, Fucus
vesiculosus and Himanthalia elongata (% dw; average±standard deviations) on the
eulittoral fringe at Portsall, France (Connan et al., 2004).
A group of polyphenols (fucol, fucophlorethol, fucodiphloroethol G and ergosterol) have
shown effects as antioxidant, anti-allergic, anti-herbivore etc. (Table 14). Polyphenols and
the phenolic compound phlorotannin abundant in largest quantities in brown macroalgae
such as Sargassum sp., Fucus sp. and A. nodosum have effects as anti-oxidant and antiStaphylococcus activity, together with other broad therapeutic perspectives (Table 23)
(Zubia et al., 2008; Li et al., 2009).
59
Investigations on crude extracts and phenol content shows that the reducing power and
hydroxyl radical scavenging activity of some seaweed (Eucheuma kappaphycus and
Turbinaria conoides) is found to be higher compared to standard antioxidant (atocopherol). In several experiments, the total phenol content of several seaweed species
was significantly different in three out of six seaweed tested. The in vitro antioxidant
activities of methanol extracts of all six seaweed tested, exhibited dose dependency; and
increased with increasing concentration of the extract (Ganesan et al., 2008; Kumar et al.,
2008a).
Polyphenols are of pharmacological value because of their antioxidative activity,
and have also shown effects within e.g. radiation protection, anti-biotic and anti-diabetes.
These effects were tested in bacteria, cell cultures, rodents etc. and even in humans in
regard to sexual performance and desire (Table 23 and 24).
Table 23. Effects, source species and test system of phlorotannins found in genera of seaweed of interest in
Denmark.
Phlorotannins
Effects
Source
Test system
Antioxidant a, b, c, d, e, f, g
Laminaria setchelli b
Palmaria palmata b, h
Fucus spiralis c
Ascophyllum nodosum i
Sargassum mangarevense g
S. siliquastrum f
Radiation protection k
Palmaria palmata h
Ascophyllum nodosum e
Anti-proliferative activities b
Laminaria setchellii b
Palmaria palmata b
Ulva lactuca t
Sargassum natans and S. fluitans n
S. mangarevense g
Sargassum sp. m
Eisenia bicyclis m
Fucus vesiculosus o
In vitro k
ESR cellular systems in vitro l
HeLa cells b, h
Solvent partition and NMR experiments c
Improved blood antioxidant activity i
Inhibition of red blood cells hemolysis f
Supression of lipid peroxidation using rat brain
homogenates f
Scavenging activity of superoxide radicals f
In vitro, ascorbic acid calibration curve h
Absorption in UV-B range which leads to protection
against UV-B radiation e
In vitro, HeLa cells b, h
Antibiotics t
Antifouling
Sargassum natans and S. fluitans j
Anti-herbivore
Bacteria and epifauna j
Anti-Staphylococcus activity g, m
Strong antibacterial activity against the fish pathogens
Vibrio parahemolyticus and Edward tarda m
Bacteria and epifauna j
Different species p
Ecklonia radiate q
Laminaria longicruris r
Fucus vesiculosus o
Anti-diabetes
i, k
Ascophyllum nodosum i
In vivo, rats and mice: Inhibits intestinal a-glycosidase,
stimulates basal glucose uptake, decreases blood
total cholesterol and glycated serum protein levels,
normalizes the reduction in liver glycogen level i
Anti-cancer k
Anti-HIV k
Anti-allergic k
Anti-plasmin inhibition s
Photo chemoprevention s
a= (Plaza et al., 2008), b= (Yuan and Walsh, 2006), c= (Cérantola et al., 2006), d= (Kumar et al., 2008a), e= (Kang et al., 2003), f= (Lim et al., 2002),
g= (Zubia et al., 2008), h= (Yuan et al., 2005), i= (Zhang et al., 2007), j= (Sieburth and Conover, 1965), k= (Li et al., 2009), l= (Zou et al., 2008),
m= (Kim and Lee, 2008), n= (Sieburth and Conover, 1965), o= (Jormalainen et al., 2008), p= (Targett and Arnold, 1998), q= (Lüder and Clayton,
2004), r= (Johnson and Mann, 1986), s= (Li et al., 2008b), t= (Murata and Nakazoe, 2001).
60
Oral test on rats and humans by a commercially available sample containing 30 % of
polyphenols and 70 % of dietary fibres indicated good oral absorption of the compounds
and fast binding to the luminal surface of the blood vessels. Human clinical trial showed
significant improvement in erectile function (see Table 24).
Table 24. Human respons on sexual desire, erectile function and sexual satisfaction to
oral absorption of phenols. p values were <0.01 for all score types (Kang et al., 2003).
Score type
Total score
Erectile function
Question 3*
Question 4**
Orgasmic function
Sexual desire
Intercourse satisfaction
Overall satisfaction
0 week
(mean±SD)
8 week
(mean±SD)
Change
(%)
29.1 ± 13.1
11.6 ± 6.5
1.9 ± 1.4
1.8 ± 1.4
3.8 ± 2.7
5.0 ± 1.9
4.7 ± 3.0
4.0 ± 1.8
47.0 ± 14.5
19.3 ± 6.7
3.3 ± 1.5
3.2 ± 1.5
7.1 ± 2.6
6.0 ± 1.6
8.2 ± 2.9
6.5 ± 1.9
62
66
74
77
87
20
74
62
*When you attempted sexual intercourse, how often were you able to penetrate (enter) your partner? Rated
on a scale of 1 (almost never or never) to 5 (almost always or always); score of 0= no attempt made.
**During sexual intercourse, how often were you able to maintain your erection after you had penetrated
(entered) your partner? Rated on a scale of 1 to 5 (see above); score of 0= no attempt made.
Results furthermore demonstrate the usefulness of these polyphenolic compounds as
fundamental chemo preventive agents against vascular risk factors originating from
oxidative stress (Kang et al., 2003). Therefore, it could be suggested that phlorotannins
would be potential candidates for the development of unique natural antioxidants for
further industrial applications as functional foods, cosmetics and pharmaceuticals (Li et al.,
2009).
Other metabolites
Antifouling
Biofilm is the beginning of a community on a surface beginning with molecules, the
invasion of bacteria and macromolecules and then comes the invertebrate pioneers if
suitable substrate and environment. Biofilm of bacteria can also be unwanted on the
human skin or in a wound after surgery.
Biofouling of surfaces e.g. submerged in the marine environment, such as ship
hulls or water turbines, is a huge economic and environmental problem. In the search for
an effective, but non-toxic antifouling paint, many compounds as been tested, however
there is still no alternative to the copper-paint used ad present. The ban of this paint is
near as the tri-butyl-tin (TBT) was banned recently. This was because e.g. invertebrates
were affected, and turned into hermaphrodites. For the large boats there is the alternative
paint based on silicone, but this is not useful for small boats, as it is labor intensive, needs
special equipment, and the boats need to reach a certain speed in order for the surface to
be repellent.
Promising commercially interesting antifouling agents in some of the seaweed
species of interest in Denmark were scarce. However, the Delisea pulchra (species native
near the shores of Australia) has got most of the attention. The promising antibacterial
agent of this species is a halogenated furonone, or fimbrolide, that belongs to a class of
61
lactones. It has been examined for its effectiveness as an active ingredient in bacterial
antifouling agents (Dworjanyn et al., 1999; Dworjanyn et al., 2006; Nylund et al., 2007). A
positive bacterial inhibition was also seen when this furonone was tested in surgery lotion.
The bacteria could not communicate and thereby not invade new surfaces.
The concentrations of halogens, as the mentioned furanones and kalahide F, rare
earth elements and many of such transition metal elements in marine algae are
remarkably higher than those in terrestrial plants (Hou and Yan, 1998). Halogenated
compounds includes indoles, terpenes, acetogenins, phenols, fatty acids and volatile
halogenated hydrocarbons, tannins, bromated fatty acids (Cardozo et al., 2007).
Several algal species appear to be able to regulate colonisation of their surfaces
thorugh the production of secondary metabolites. Epiphytic marine bacteria have the
potential to control population on the seaweed, either through inhibition of growth, or by
influencing the tactic behaviour of potentially competing bacteria (Boyd et al., 1999).
Apart from the furanone from the Australien seaweed species, the search for
antifouling agents in seaweed mainly resulted in examples of bacterias associated on the
seaweed surface and chemical deterrents, such as phlorotannins, against herbivores in
the marine systems.
The potential antifouling and antibacterial roles of phlorotannins was investigated
in numerous studies (Ragan and Jensen, 1978; Amsler and Fairhead, 2005).
Phlorotannins apparently play a role in physiological defences against abiotic stress and
act as antibacterial agents, fouling inhibitors, herbivore deterrents and digestion inhibitors
together with wound healing of the seaweed. Wounding or ‘artificial grazing’ induced
phlorotannins in Ascophyllum (Pavia and Toth, 2000) and this phenomenon is also seen in
Laminaria species (Hammerstrom et al., 1998). A cytological study revealed that, one day
after wounding of Ecklonia radiata, phlorotannins accumulated around the wound sites and
that dense accumulations were found throughout the medulla of the entire algal section
after 9 days (Lüder and Clayton, 2004). In addition, direct feeding by an isopod triggered
the induction of chemical defence in several macroalgal species including Fucus serratus
(Rohde and Wahl, 2008).
Ulva sp. (photo:Holdt, 2010)
62
Associated bacterial communities in Laminaria and especially Ulva sp. have several
antifouling and anti-pathogenic properties (Table 25). Sixty of 280 isolated (21 %) of
epiphytic bacteria from a range of marine algae exhibited antibiotic activity against a test
battery of fouling bacteria. Anti-biotic activity was shown by 57 %, 17 % and 11 % of the
strain isolates tested from the surface of Laminaria digitata, Fucus serrratus and Palmaria
palmata, respectively (Boyd et al., 1999).
The presence of physodes (vesicles with phlorotannin), in especially young thalli,
appears to be coupled with antifouling in brown seaweed. The phlorotannin from
Sargassum species was tested at different concentrations in the laboratory, and showed
activity against bacteria and epifauna. Due to the economic problems of fouling, tannic
acid9 was tried out as an antifoulant in varnish on panels submerged in bays near Florida
and Rhode Island in 1955. Although the tannic acid preparations were inferior to
commercial antifouling paints, they did inhibit fouling by both barnacles and algae under
both temperate and tropical conditions (Sieburth and Conover, 1965). The use of tannins
from seaweed, bark and trees in antifouling paints were already patented in 1881,
however, although tannins may be effective, their economic application is undoubtly
limited, claimes Sieburth and Conover (1965).
Table 25. Effects of bacteria and specific metabolites found in seaweed
Origin
Species
Effect
Associated bacterial
communities
Ulva sp.
antifouling invertebrate larvae a-e
antifouling, bacteria c, f
antifouling, fungus c
anti-pathogenic b
antifouling, micro- and macroalgae d
antifouling bacteria k
anti-ulcer g
anti-ulcer g
anti-biotic g
induction of neurite outgrowth h
anti-biotic g
Antifouling I, j
Laminaria digitata
Porphyra tenera
Gracilaria verrucosa
Dictyota dichotoma
Sargaquinoic acid
Sargassum yezoense
Rhodomela subfusa
furanones
Laminaria sp.
Delisea pulchra
kahalalide F
Bryopsis sp.
treatment of lung cancer, tumours and AIDS j
a=(Dobretsov and Qian, 2002), b=(Dobretsov, 2005), c= (Egan et al., 2000), d= (Egan et al., 2001), e=(Holmstrom et al., 2002), f=(Boyd
et al., 1999), g=(Murata and Nakazoe, 2001), h=(Mayer et al., 2007), i=(Bartsch et al., 2008a), j=(Smit, 2004), k=(Boyd et al., 1999)
Porphyosin
Vercoyosin
Terpenoid
Meroditerpene
Halogen
The antifouling effect has also been found in extracts of seaweed without any coupling to a
specific compound that courses the effect. See next chapter and Table 26.
9
Tannic acid, a specific commercial form of tannin, is a polyphenol. Its weak acidity (pKa around 6) is due to
the numerous phenol groups in the structure. Its structure is based mainly on glucose esters of gallic acid,
and it contains a mixture of related compounds (Wikipedia, 2010).
63
Extracts or powder of seaweed
Various extraction methods have been used to release identified and unidentified bioactive
substances from marine algae. Powder derived from dried seaweed has also been tested.
Antioxidant effect
The result of 16 lipophilic extracts suggests that seaweed can be considered as a potential
source for the extraction of lipophilic antioxidants, which might be used as dietary
supplements or in production in the food industry. The results indicated an increase in
antioxidative property with increasing content of unsaturated fatty acid (Huang and Wang,
2004). Seaweed of the Sargassum family might be a valuable natural antioxidative source
containing both water and fat soluble antioxidative components preventing oxidative
damages of food oils (Siriwardhana et al., 2003; Siriwardhana et al., 2004).
Peroxidation of fatty acids
Addition of 2 % and 1 % Undaria powder to diets decreased serum and liver triglycerol
levels, respectively, compared to control. It is known that the synthesis and oxidation of
fatty acids by the liver control the concentration of triacylglycerol in the serum and liver.
The enzyme activities involved in the synthesis or the oxidation of fatty acids shows
changes in rats with Undaria powder in diets. Addition of 5-10 % Undaria powder
decreased glucose-6-phosphate dehydrogenase activity; however 10% wakame increased
several activities of other enzymes and co-enzymes. These results indicate that the
decrease in concentration of triacylglycerol in serum and liver by dietary Undaria powder in
rats is due to the promotion of fatty acid oxidation in rat liver. So Undaria may play a role in
prevention and treatment of arteriosclerosis. In addition, since the decrease in
concentration of triacylglycerol in the serum and liver by dietary Undaria is associated with
the promotion of oxidation of fatty acids in the liver, Undaria may become a food material
for prevention of obesity (Table 26;(Murata et al., 1999)).
It was furthermore found that fish oil in rat diets decreased the concentration of
triacylglycerols in serum and liver significantly compared to control, but this decrease
became even more conspicuous in a diet with both fish oil and Undaria powder (Murata et
al., 2002).
Methanol extract from the brown algae Sargassum inhibits oxidation in rat liver
homogenates (Mori et al., 2003; Kumar et al., 2008b).
64
Other effects
Extracts of seaweed with different solvents such as water, ethanol, dichloromethane, and
chloroform have shown anti-bacterial, anti-fouling, anti-inflammatory, anti-pathogenic
(Table 26).
The anti-bacterial effect of seaweed extracts was seen in several gram-negative bacteria
strains and the extracts were non-toxic against non-targeted larvae (Andersson et al.,
1983; Hellio et al., 2002; Zubia et al., 2008). However, anti-fouling properties were found in
extract of Ulva was toxic to some invertebrate larvae (Hellio et al., 2002). Antiinflammatory effect was seen in edema and erythema of mice, but rodents could also get
decreased motor activity when seaweed extract was added to their diet (Andersson et al.,
1983). Another study on rodents improved the survival of stroke-prone hypertensive rats
when given 5 % seaweed powder in the diet (Ikeda et al., 2003). Similar, Undaria powder
supplemt in rat diet (5 % of wet weight) attenuated the development of hypertension and
its related diseases and improved survival rates (Ikeda et al., 2003). Decrease in
symptoms of osteoarthritis of the knee was seen in experiments where an aqueous extract
of several species of seaweed was taken orally by humans (Myers et al., 2010).
Methanol or enzymatic extracts of Sargassum species were furthermore
preventive against DNA damage, respectively (Park et al., 2005; Cho et al., 2007). The
latter effect was also seen by enzymatic extracts of other brown seaweed (Heo et al.,
2005).
Sargassum muticum (photo: Holdt, 2010)
65
Table 26. Effects of extracts from the seaweed species or genera of interest in Denmark.
Effect
Species
Detail on effect or extract
Anti-fungicidal a, b
Laminaria digitata b, s
Seaweed conditioned seawater had anti-fungal effect on fungal-specific PCR primers s
Anti-ulcerative activity a
Anti-oxidation c, d
Laminaria digitata d, e
Synergistic effect as antioxidant with vitamin E at given concentration e
Intermediate antioxidant activity d
Sargassum fusiforme f
Saccharina latissima t
Laminaria digitata b, s, t
Laminaria orchroleuca i
Chondrus crispus i
Ascophyllum nodosum i
Fucus serratus t
Sargassum muticum i
Sargassum mangarevense g
Palmaria palmata i
Laminaria orchroleuca k
Laminaria saccharina x
Sargassum muticum k, j
Ulva lactuca k
Laminaria digitata j
Gracilaria chilensis m
Gracilaria cornea n
Ulva pertusa o
Undaria pinnatifida p
Ulva linza p
Mix: F. vesiculosus (85 %),
Macrocystis pyrifera (10 %),
L. japonica (5 %)
Sargassum fusiforme f
Sargassum micracanthum q
Sargassum thunbergii r
Laminaria digitata t
Heat- and UV-light resistant antioxidants f
Petroleum ether and methanol extract active against Escherichia coli t
Ethanolic extract anti-bacterial and non-toxic against non-targeted larvae i
Chloroform extract active against Proteus vulgaris t
Seaweed conditioned seawater reduced the community composition of bacteria (bacteria-specific PCR primers s
Ethanolic and dichloromethane extract anti-bacterial. The first non-toxic against non-targeted larvae i
Petrolium extract active against Streptococcus pyogenes t
Ethanolic and dichloromethane extract. Both non-toxic against non-targeted larvae i
Against Staphylococcus g
Dichloromethane extract anti-bacterial and non-toxic against non-targeted larvae i
Inhibits macroalgae k
Biofilm and wash-outs repelled blue mussel larvae
Inhibits micro-and macroalgae k
Toxic against oyster and sea urchin larvae k
Strong fish pathogenic bacterial activity at 31mg dw/mL j
Agar degrading micro organisms m
Against Vibrio anguillarum and Pseudomonas anguilliseptica n
Against E. coli and Pasteurella piscicida with 5 % Ulva feed supplement o
Mice edema and erythema p
Anti-bacterial b, g, h, j, t
Anti-fouling j, k, x
Anti-pathogenic bacterial l, m
Anti-inflammatory p
Lipid peroxidation
Preventive against DNA-damage r
Reactions in rodents t
The aqueous extract including fucoidan and polyphenols decreased the symptoms of osteoarthritis of the knee
when taken orally by humans over twelve weeks experiment v
Better than vit A and E q
Chloroform extract inhibited the contractions of the stimulates guinea pig ileum at a concentration of 100 μg/mL
and water extract decreased motor activity, weak loss of screen grip, enophthalmus and cyanosis with death
occuring several hours later t
Fucus serratus t
Water extract decreased motor activity and pilomotor erection in the hippocratic screening of mice t
t
Ascophyllum nodosum
Water extract decreased motor activity and pilomotor erection in the hippocratic screening of mice and induced
fearful behaviour t
Undaria pinnitifida u
5 % powder (wet weight of diet) significantly delayed the development of stroke signs and significantly improved
the survival rates of stroke-prone hypertensive rats u
a= (Plaza et al., 2008), b= (Lam et al., 2008) c= (Murata and Nakazoe, 2001), d= (Huang and Wang, 2004), e= (Le Tutour, 1990), f= (Siriwardhana et al., 2004), g= (Zubia et al., 2008), h= (Freile-Pelegrín and
Morales, 2004), i= (Hellio et al., 2001), j= (Plouguerne et al., 2008), k= (Hellio et al., 2002), l= (Dubber and Harder, 2008), m= (Weinberger, 2007), n= (Bansemir et al., 2006), o= (Satoh et al., 1987), p= (Khan
et al., 2008), q= (Mori et al., 2003), r= (Park et al., 2005), s= (Lam et al., 2008), t= (Andersson et al., 1983), u= (Ikeda et al., 2003), v= (Myers et al., 2010), x= (Dobretsov, 1999)
66
Feed supplement
Animals such as sheep, cattle and horses that live in the coastal areas have eaten
seaweed washed ashore. Today, seaweed is dried and milled to fine seaweed meal
powder especially from the main raw material Ascophyllum, because of accessibilty of this
species. Analyses show that it contains useful amounts of minerals (K, P, Mg, Ca, Na,
chlorine and S), trace metals and vitamins. Because most of the carbohydrates and
proteins are not digestible, the nutritional value of seaweed has traditionally been assumed
to be in its contribution of minerals, trace elements and vitamins to the diet of animals. In
Norway it has been assessed as having only 30 % of the feeding value of grains. Feeding
trials with added Ascophyllum meal to poultry and pigs, an increase in the ion content of
the eggs and no effect was observed, respectively. However, positive results were
reported with increase in milk production in dairy cows and better maintenance in sheep
weight during winter feeding, increase in lamb’s birth weight and gave greater wool
production (McHugh 2003; pers. comm. on birth weight of lambs Ole Hertz, Nordic
Seaweed Project 2008).
Recent research on seaweed used as supplement of either protein,
polysaccharides or enriched with PUFAs gives promising results. Either the fishmeal
protein can be supplemented with no effect or even with a beneficial effect on growth, feed
conversion ratio, colour etc. (Table 27).
For instance, results suggest that Porphyra dioica can effectively be included in
diets for rainbow trout up to 10% without significant negative effects on weight gain and
growth performance. The pigmentation effect of the fish flesh by adding the Porphyra meal
to the feed is of a considerable interest to the organic salmon-farming industry (Soler-Vila
et al., 2009). Another result showed that when Ulva meal replaced 5% of the diet lipids to
an equal of the lipid levels, the growth performance, feed efficiency, nutrient utilization, and
body composition of Nile tilapia were improved (Ergün et al., 2008). In addition, seaweed
meal elevated body weight gain of sea bream, and tended to increase feed efficiency and
muscle protein deposition. Algae-fed groups were higher in liver glycogen and triglyceride
accumulation in muscle. Feeding Porphyra showed the most pronounced effects on
growth and energy accumulation, followed by Ascophyllum and Ulva. The results suggest
the practical efficacy of using algae as a feed additive for the effective use of nutrients in
cultured sea bream (Mustafa et al., 1995).
Especially experiments on pigs (including weanling and grower-finisher) fed on
seaweed have had much attention and only some are mentioned here. In this animal there
is great attention on soling the stomach and intestinal problems when the piglets go from
suckling to solid diet. Seaweed extract feed to pigs may provide a dietary means to
improve gut health and potentially reduce pathogen carriage in finishing pigs. However,
the effect on growth performance in healthy animals was negative (Gardiner et al., 2008).
67
Table 27. Seaweed species used as feed supplement or replacement. Species of the genera available in Denmark are included. Percentage replaced by
seaweed according to the reference compound. Effects of seaweed on test organism are described. Ref= reference.
Test organism
Species
Replacement of feed (%)
Effect
Ref
Sea bass juveniles
Gracilaria bursa-pastoris
Gracilaria cornea
Ulva rigida
Ascophyllum nodosum
Porphyra yezoensis
Ulva pertusa
Porphyra>Ascophyllum>Ulva
Ascophyllum nodosum
Protein 10 %
Protein 5 %
Protein 10 %
No negative consequences on growth performance, nutrient utilisation or body composition
No negative consequences on growth performance, nutrient utilisation or body composition
No negative consequences on growth performance, nutrient utilisation or body composition
Increased body weight
(increased) feed efficiency and muscle protein deposition
a
a
a
c
c
d
Ulva pertusa
Lipid
Up to 5 %
Ascophyllum nodosum
Undaria pinnatifida
Ulva sp.
5%
Growth and energy composition
Increased muscle protein in response to the algae level
Response to air-dipping and recovery time from anesthesia with 2-phenoxyethanol
Not effect growth
Accumulated triglycerides
Low fatty acid composition
Activated lipid mobilization
Suppressed protein breakdown
Improved growth and feed efficiency
Sea bream
Nile tilapia
0, 2.5, 5 %
e
f
Lipid 5 %
Increased specific growth rate (SGR)
g
Increased feed conversion ratio (FCR)
Increased protein efficiency ratio (PER)
Ulva sp.
Protein 5 %
Increased growth, specific growth rate, FCR and PCR
h
Rainbow trout
Porphyra dioica
Protein and lipid
No difference in weight gain and growth performance
i
Up to 10 %
Increased pigmentation
Sea urchin
Sargassum linearifolium
Feeding stimulant
b
Increase protein and energy consumption
Pigs
Palmaria palmata (Pp)
Dietary fibres
Pp no effect
n
Laminaria digitata (Ld)
Alginate
Ld increased the ileal viscosity of digesta and their intestinal hydration capacity
Weanling pigs
Laminaria hyperborea
Contained laminaran and fucoidan
Decrease in intestinal bacteria
j
Laminaria digitata
Reduction in intestinal ammonia concentration
Marginal effect on immune response
Laminaria sp.
Contained laminaran and fucoidan
May alleviate use for high-lactose diets
k
Alleviate some of the common problems that occur post weaning
Ascophyllum nodosum
Extract
Reduction in intestinal E. coli
m
Iodine
Increases iodine concentration in several tissues
Grower-finisher pigs
Ascophyllum nodosum
Extract
Reduced daily weight gain, but no effects on feed intake, FCR, or carcass characteristics
l
Change in intestinal bacterial communities
Sheep
Ascophyllum nodosum
2%
Lowered body temperature during transport
o
Suppressed antibody titer, which could leave animals susceptible to bacterial infection
Ascophyllum nodosum
35 g
Less body weight reduction of ewes
p
Increased number of lambs born per ewe and increased growth rate of lambs
Increased wool production (20 %), prevented moulting
Cattle
Ascophyllum nodosum
158 g
Higher milk yield (6 %) and no influence on fat content of milk
q
Increase in iodine content of milk (100 in control to 600 μg/L in test)
Less body weight gain during barn feeding periods
No difference in reproduction performance and the weight of new-born calves
Less incidence of mastitis
Ascophyllum nodosum
>2 %
Main effect: increasing the shelf life of meat
r
Chicken
Porphyridium sp.
Polysaccharides
No difference in body weight, egg number and egg weight
s
PUFA and EPA
Consumed less food (10 %)
5 % and 10 %
Lower cholesterol level (decrease of 28 %)
Reduced cholesterol but increased fatty acids and darker colour of egg yolk
a=(Valente et al., 2006), b=(Dworjanyn et al., 2007), c=(Mustafa et al., 1995), d=(Zhang et al., 2007), e=(Nakagawa and Kasahara, 1986), f=(Yone et al., 1986), g=(Kotake-Nara et al., 2001), h=(Ergün et al., 2008),
i=(Soler-Vila et al., 2009), j=(Reilly et al., 2008), k=(Gahan et al., 2009), l=(Gardiner et al., 2008), m=(Dierick et al., 2009), n=(Hoebler et al., 2000), o=(Archer, 2005), p=(Sæter and Jensen, 1957), q=(Jensen et al.,
1968), r=(Gravett, 2000), s=(Ginzberg et al., 2000)
68
Plant stimuli
Seaweed has been used directly or in composted form as soil enrichment since antiquity
to increase produtivity of crops in coastal regions. Farmers have collected storm toss of or
harvest seaweed, but the use is also commercialised. Seaweed is sold for fertilizer or soil
enrichment purposes as meal (powder) or liquified (extracts) by several companies
worldwide; Acadian Seaplants ltd, Arramara Teo, Göemar, Kelpak, Seasol just to mention
a few of the larger producers. The current commercial extracts are manufactured mainly
from species of the brown seaweed Ascophyllum nodosum, Laminaria spp., Ecklonia
maxima, Sargassum spp., Fucus serratus, but also species such as Enteromorpha
intestinalis, Ulva lactuca and Kappaphycus alvarezii have been used (Craigie, 2010). The
differences between meal and liquified seaweed are especially the delayed respons of the
meal on the plant crop (Table 28).
Table 28. Properties of liquid seaweed extract versus seaweed meal applied to soils (Craigie, 2010; Milton,
2010)
Liquified
Whole or powder
Stimulates microorganisms, root system plant growth
Immediate positive response in plants (1:500 dilution)
Stimulates growth and germination of plant. However, immediate
inhibition (~15 wk to overcome)
Soil must be turned (aerated) to reduce toxic sulfhydryl
compounds
Decreases inonic N and later total N increases, because of
microbial activity
Improves soil crumb structure because of degraded polar
compounds
Chelation effect* because of partly hrydrolyzed, sulfated
polysaccharides. Hereby, trace metal ions are prevented
from precipitating
Cu, Co, Mn and Fe soluble at high pH
* formation of stabile and soluble complex mplecules with certain metal ions
Seaweed is, as mentioned, rich in minerals and trace metals and this makes the extracts
rich in trace metal mixtures (Cu, Co, Zn, Mn, Fe, Ni as week as Mo and B (boron)) among
other things. The observed benefits to the growth, health and yields of plant crops were
traditionally attributed to this supply of essential nutrients, together with the improvement
of soil texture and water holdning capacity. However, the development of liquified extracts
and their relatively low applications (<15 L/ha) led to examinations of the extracts for other
components that would promote growth (Maxicrop Limited, 1962; Craigie, 2010). The plant
can be treated with seaweed extract by arial application (seed treatment, seedling dip,
foliar spray (directly sprayed on leaves)) or soil application (incorporation of marine bioproducts, soil drenching, addition of extracts to hydroponics) (Khan et al., 2009).
Some of the other components, that have been found to affect plant crops, are
hormones like absissic acid, auxins or hormon-like plant regulators like betaines
(Table 29). Polymers such as polysaccharides are also bioactive in regard to plants. The
effects of these compounds or extracts are growth responses (increased yield and root
growth), biotic stress resistence (fungal, bacterial and viral pathogens) improved tolerance
to abiotic stress (salt, drought, fresszing), enhanced nutritional quality, suppression of soil
borne diseases and nematodes, etc. (Table 29) (Khan et al., 2009).
Seaweed extracts are considered an organic farm input because they are
environmentally friendly and safe for the health of animals and humans (Khan et al., 2009).
.
69
Table 29. Some bioactive compounds of seaweed and effect on plant crops.
Compound
Species
Bioactivity
Plant growth hormone
Absissic acid
Auxins- or auxin
like activity
Cytokinins- or
cytokinin like
activities
Gibberellins
Hormone-like plant
growth regulators
Betaines
Laminaria a
Ascophyllum a
Laminaria a,
Fucus a , c
Ascophyllum a, c
Undaria a, c
Macrocysti s a, c
Ecklonia c
Fucus a
Ascophyllum a, t
Sargassum a
Macrocystis a
Ecklonia a
Fucus a
Ascophyllum n
Sargassum a
Ecklonia a
Laminaria e
Fucus e
Ascophyllum e:
0.0080.014 % of dw seaweed,
0.014-0.027 %
of
dw
commercial extract u
Induce genes for protein synthesis required for drough
tolerance of seeds b
Root growth c
Cell elongation d
Cell division d
Increased yield of potatos m
Elevated protein conten in grass m
Lime fruits stayed green longer m
Increase in the reporter gene β-glucuronidase (cytokininlike activity) in arabidopsis plants (3 ml/L) t
Elongation of germinating seedlings of lettuce (unstabile,
and no effect after 4 months storage) n
Anti-fungal e
Osmoregulation f
Drought and frost resistance f
Disease resistance f
Induces defence and stress responses f
Inhibits growth and seed germination f
Induces synthesis of proteinase inhibitors f
Unknown
Seaweed liquid extract o
Increased height, root length, shoot length and number of
flowers and fruits of tomato plants, together with
biochemical constituents o
g, j
Polymers
Laminaran
Ascophyllum
Upregulate the production of phenylalanine ammonium
Sargassum wightii i
lyase, lipoxygenase and salicyclic acid g
Ecklonia k
Anti-fungal respons in alfalfa (plant in the pea family) h
Resistance to bacterium pathogen in cotton seeds and
seedlings i
Higher boll yields in cotton i
Reduction in plant louse and mites j
Reduction of root damage from nematodes k
λ-carrageenan
Trigger signaling pathways in tobacco l
Inducing several defense related genes l
Reduced fungal pathogens in the arabidopsis plant v
Potential inducer of resistance in tomato plants against
tomato chlorotic dwarf viroid replication x
Ulvan
Ulva y
Induces a gene expression signature similar to that
observed upon methyl jasmonate treatment (MeJA) y
Extract: bioactive
Ascophyllum p, q, r, s
Increased yield and quality of table grapes p
compound unknown
Reduction in fungal diseases in carrot and greenhouse
cucumbers q
Improved freezing tolerance in the plant aradiopsis,
because of lipophillic components r
Increased the total phenols, flavonoids, and antioxidant
activity in spinach leaves (1.0 g/L) s
a= (Jameson, 1993), (Tarakhovskaya et al., 2007), b= (Rensing et al., 2008), (Verslues et al., 2006), c= (Stirk and Van Staden, 1996), d= (Wikipedia,
2010), e= (Blunden and Tyihák, 2009), f= (Craigie, 2010), g= (Klarzynski et al., 2000), (Patier et al., 1993), (Potin et al., 1999), h= (Kobayashi et al.,
1993), i= (Raghavendra et al., 2007), j= (Stephenson, 1966), k= (Featonby-Smith and VanStaden, 1983), l= (Mercier et al., 2001), m= (Blunden,
1977), n= (Williams et al., 1981), o= (Reeta et al., 2010), p= (Norrie et al., 2010), q= (Jayaraj et al., 2010), r= (Rayirath et al., 2010), s= (Fan et al.,
2010), t= (Khan et al., 2010), u= (MacKinnon et al., 2010), v= (Sangha et al., 2010a), x= (Sangha et al., 2010b), y= (Jaulneau et al., 2010)
Jasmonates
Fucus (maybe) f
70
Heavy metals and other undesirable compounds
Attention should be drawn to the positive effect that seaweed accumulates compounds.
Not only the desired minerals are concentrated in seaweed, but also metals in toxic
concentrations, heavy metals and compounds. Examples are e.g. Cadmium (Cd), Cu, Mn,
Zn and if present in the ambient environment, the explosive compound trinitrotoluene
(TNT) (Ronnberg et al., 1990; Sandau et al., 1996; Mehta and Gaur, 2005; Greger et al.,
2007; Cruz-Uribe et al., 2007b; Besada et al., 2009b). Concentrations factors of 103 to 104
for the mentioned heavy metals and even up to 10 6 can be reached in chromium
(references in Lobban and Harrison 1994). This accumulating effect of seaweed can be
exploited to remediate for undesired compounds in sea- and waste water or use seaweed
as bio-indicator (Mehta and Gaur, 2005; Cruz-Uribe et al., 2007a; Boubonari et al., 2008).
However, undisered metals and compounds should be taken into account and tested for if
seaweed is to be used as food product. The concentrations of e.g. heavy metals depend
on the surrounding environment, and variations can be very local.
Inorganic arsenic accumulation in seaweed is an example of another problem
because it has an effect on the human nervous system. Marine organisms take up the
inorganic arsenic, but usually the biological system transforms it to organic and the nontoxic form of arsenic. Arsenic concentrations are generally considerably higher in brown
seaweed than in red or green (Francesconi and Edmonds, 1997). In most species of
seaweed, the concentrations are below 54 mg/kg dw, and more than half the arsenic is
organic, primarily in the form of various arseno-sugars (Table 18; (Francesconi and
Edmonds, 1997; Almela et al., 2002)). Fucus readily accumulates arsenate and transforms
it into several arsenic compounds depending on the exposure concentration, and other
major arsenic species. These arsenosugars are arsenate, arsenite, methylarsonate,
dimethylarsinate (Geiszinger et al., 2001). However, the seaweed species Sargassum
fusiforme (and possibly other species in the Sargasso family concentrate) huge amounts
of the inorganic form (88 mg/kg dw, up 72 % of total As content; Table 30). This edible
brown seaweed Sargassum fusiforme (former Hizikia fusiformes) from Japan sold as Hijiki
or Hiziki and the other Sargassum seaweed S. muticum (invasive species in Denmark
located in Limfjorden) may only contain 38 to 75 % of their arsenic in organic forms (Yasui
et al., 1978; Shinagawa et al., 1983; Almela et al., 2002). Arsenic in Sargassum is
removed by 89-92 % (w/w) by the cooking process. In addition, arsenic could effectively be
removed just by soaking the edible brown seaweed. These experiments were tested on
mice (Ichikawa et al., 2006). However, this is not observed in vegetables where cooking is
only of a very limited value as a means of reducing metal concentrations (arsenic,
cadmium, mercury, and lead) (Perelló et al., 2008). Figures of these compounds in
seaweed sold as food are shown in Table 30.
71
Table 30. Total arsenic, inorganic arsenic, lead, cadminum, and mercury in seaweed. Seaweed put on market
and Irish seaweed from nature. Free after (Almela et al., 2002; Besada et al., 2009a; Durcan et al., 2010)
refered to as a, b, and d respectively.
Type Species
Description of product
Total
Inorg.
Pb
Cd
Hg
As
As
green
red
Enteromorpha sp.
Ulva sp.
Ulva pertusa
Ulva rigida
Porphyra sp.
Porphyra tenera
Porphyra umbilicalis
Palmaria palmata
brown
Chondrus crispus
Eisenia bicyclis
Undaria pinnatifida
Laminaria japonica
Laminaria spp
Saccharina
latissima
Fucus vesiculosus
Hizikia fusiformis
Himanthalia
elongate
Green nori flakes (dried edible algae)a
From Irish coast d
AO nori (dried edible algae) a
Sea lettuce b
From Irish coast d
Nori (dried edible algae) a
Nori (dried edible algae) a
Toasted nori (dried edible algae) a
Nori b
Atlantic dulse (dried tender Japanese
algae) a
From Irish coast d
Irish moss b
Ise wild arame (dried tender Japanese
algae) a
Ise wild arame (dried tender algae) a
Arame (dried edible algae) a
Arame b
Wakame (dried edible algae) a
Wakame (dried edible algae) a
Japanese wakame (dried tender algae) a
Wakame b
Japanese kombu (dried tender algae) a
Kombu (dried algae) a
Kombu b
From Irish coast d
2.3±0.1
6.39±0.59
5.17±0.05
6.61-7.06
11.5±9.75
23.7±0.5
28.3±0.5
30±1
28.9-49.5
7.56±0.02
0.37±0.07
1.33±0.03
0.03±0.01
20.6±0.4
0.36±0.06
0.151-0.177
<0.15
0.57±0.04
0.19±0.02
0.314±0.005
0.132-0.338
0.44±0.06
0.93±0.02
1.00-1.05
0.17±0.01
0.03-0.03
18±2
18-19
0.31±0.06
0.289±0.004
0.29±0.02
<0.01-0.27
1.1±0.2
0.35±0.01
0.18±0.02
0.38±0.01
0.25-3.10
0.70±0.03
14±2
4±1
11.3±0.4
8-32
10.5±0.4
12.8±0.46
23.2-25.5
23.8±0.5
0.217-0.225
0.17±0.02
0.403-0.726
0.15±0.08
0.72-0.74
0.75±0.01
6-7
33.6±0.2
29±1
30.0±0.1
27.9-34.1
32±1
42±2
34.6±0.3
42.1-76.9
47±1
53±1
51.7-68.3
49.5
0.185±0.005
0.15±0.06
0.041-0.170
0.15±0.10
0.26±0.03
0.18±0.05
0.05-0.346
0.297±0.001
0.254±0.005
0.052-0.443
0.18±0.01
0.19±0.02
0.029-0.096
<LOD a
<LOD
<LOD
<0.01-1.28
<LOD
<LOD
<0.01-0.46
0.67±0.03
0.74±0.02
0.59-0.83
1.5±0.1
0.13±0.03
1.9±0.1
0.27-4.82
0.15±0.02
0.30±0.02
0.09-1.83
42±3
38±3
23-47
12±1
23±3
14±1
10-57
30±5
37±4
1-5
Alga fucus a
Irish coast d
Iziki a
Hijik a i
Japanese hijiki (dried tender Japanese
algae) a
Hiziki b
Seaweed spaghetti b
50.0±0.3
31.2±8.42
128±5
141±6
115±12
0.34±0.04
0.51±0.04
0.55±0.01
36±6
88±6
85±6
83±5
0.63±0.08
0.89±0.15
0.53±0.06
1.45±0.14
1.46±0,02
1.0±0.1
35±3
25.9±0.2
30.32±0.03
103-147
32.9-36.7
32.1-69.5
0.166-0.245
<0.01-0.53
0.20-0.26
0.99-2.50
0.31-0.33
15-50
8-16
From Irish coast d
42.8
Three subsamples were analysed for each typ of macroalgae. Values are expressed as mean ± SD. Results of As, Pb and Cd are expressed in mg/kg dry weight (dw).
a
Results for Hg are expressed in µg/kg dw. LOD, limit of detection: Pb=0.05 mg/kg dw.
Kainic acid is another compound to be aware of. It is a kainoid amino acid and neurotoxin
similar to domoic acid10. Kainic acid is a natural marine acid present in some seaweed. It is
a potent central nervous system stimulant, and has been developed as the prototype
neuroexcitatory amino acid for the induction of seizures in experimental animals, at a
typical dose of 10-30 mg/kg in mice. Kainic acid is neuroexcitotoxic and epileptogenic,
acting through specific kainate receptors. It is a specific agonist for the kainate receptor
used as an ionotrophic glutamate receptor which mimics the effect of glutamate. It is used
in experiments to distinguish a receptor from the other ionotropic receptors for glutamate.
Because of the supply shortage in 2000, the price of kainic acid has risen significantly
(Wikipedia, 2010). The concentration of kainic acid was higher in wild harvested
populations of Palmaria palmata (12 mg/kg dw in Ireland and 130 mg/kg dw in France)
compared to cultivated material (2.5 mg/kg dw). This neurotoxin is not transferred to
abalones fed on Palmaria (pers. comm.. Lüning, 2008).
10
Domoic acid (DA), the neurotoxin which causes amnesic shellfish poisoning (ASP), is an amino acid
associated with certain harmful algal blooms (Wikipedia, 2010)
72
Legislations
Seaweed and their components must meet certain consumer safety regulations. In France
the seaweed species authorized for human consumptions have even been defined
(Table 31). Indeed, maximum allowed levels of toxic minerals (lead, cadmium, tin,
mercury, mineral arsenic and iodine) have been defined for all edible seaweed. These low
levels are considered a high guarantee of food safety; in fact, heavy-metal norms for
certain fish and shellfish are much higher (e.g. 1 mg/kg dry weight for mercury in tuna in
the USA; 0.7 mg/kg in France) (Mabeau and Fleurence, 1993).
No legislation regarding contaminants in algae food products is currently present
in Spain. Some samples analysed from legalised seaweed food products did however
reveal cadmium and inorganic arsenic (As) levels higher than those permitted by
legislation in other countries (Table 31). Given the high concentrations of inorganic arsenic
found in Sargassum fusiforme, a daily consumption of 1.7 g of the product would reach the
Provisional Tolerable Weekly Intake recommended by the WHO for an average body
weight of 68 kg (Table 31;(Almela et al., 2002)).
Table 31. Seaweed authorized in France for human consumption (Burtin, 2003)
Phyllum
Name
Brown seaweed
Ascophyllum nodosum
Fucus serratus
Fucus vesiculosus
Himanthalia elongata
Undaria pinnatifida
Porphyra umbilicalis
Palmaria palmata
Chondrus crispus
Gracilaria verrucosa
Enteromorpha spp.
Ulva spp.
Red seaweed
Green seaweed
In other European countries, seaweed is not submitted to particular regulations. In several
countries (Ireland, Denmark and The Netherlands), seaweed use is directed by general
food regulations. However, in other countries (e.g. Greece), seaweed is not considered as
food, and thus are not authorized. The use of seaweed as a spice is allowed by the Food
and Drug Administration in the USA. Algal products have to comply with the following
upper level limits given in Table 32 (Mabeau and Fleurence, 1993).
Table 32. Quality criteria applied to edible seaweed sold in France (Burtin, 2003), regulations in USA
(Mabeau and Fleurence, 1993), and for dietary supplements in Denmark (EU)(EU, 2008).
Criteria
Toxic minerals
Inorganic Arsenic
Lead
Cadmium
Tin
Mercury
Iodine
Heavy metals
Limit
(mg/kg dry matter)(ppm)
France
<3.0
<5.0
<0.5
<5.0
<0.1
<0.5
USA
Denmark (EU-regulation)
< 3.0
<10
No regulation
<3.0
<3.0
<0.1
<5000
<40
The maximal content of neurotoxins (not specified) is of 20 ppm on fresh weight basis of
mussels but no resulations are found for seaweed (pers. comm.. Lüning, 2008).
73
Summary and conclusion
This review summarised the potential of nine genera or species that could be of interest for
utilisation of specific compounds or extracts in Denmark. The compound of industrial
interest needs to be identified before making the choice of which species to make extracts
from or specifically extraction of a single compound. One species may be high in one
compound, but low in another.
The chapters are summarised in the following and some of the compounds that seem
interesting due to their bioactivity and their concentration are pointed out in the following.
In addition, the species with highest concentration of these compounds are mentioned.
Compounds
The polysaccharide content of seaweed species varies seasonally and the type of
polysaccharides are species-specific. To generalise, the total polysaccharide content is
highest in the perrenial seaweed species in late summer and autumn. The increased
daylength makes summer suitable for photosynthesis and thereby assimilation of carbon.
The polysaccharide storages are build up which increase the weight of biomass, but length
growth will occure during winter when nutrients are available. Incorporation of nutrients is
not dependent on light. However, this seasonal growth pattern does not apply for species
like Sargassum and Ulva. These species grow from a small survival structure pass the
winter and grow in biomass (weight and size) during summer.
The large brown seaweed species are well represented in the studies
characterising the biochemical composition of the polysaccharides. This biomass is also a
major standing feedstock/crop and easily available on a rocky or boulder shore.
Sargassum is an annually species and in large quantities during summer and especially in
Limfjorden in Denmark.
Most of the polysaccharides stimulate human health, either by the e.g. creation of
a better intestinal environment or anti-viral properties. As an example, fucans are in large
concentrations in the large brown seaweed, are easy to isolate and have numerous health
benefits, which gives them the potential to serve as a valuable bioactive ingredients in
natural health foods.
The choice of species to exploit bioactive compounds relies on the aim and
property of the polysaccharide. The species should be exploited in late summer or autumn
to achieve the maximum content of stored carbon for extraction. However, these large
stores of carbon make the seaweed very slimy when cut fresh. The slimy look is not
delicate and if seaweed is to be exploited as a fresh vegetable another harvest season
should be chosen.
The total content of proteins was highest in Ulva and Porphyra. These species
are ephemeral and only grow during summer. Spring should however, be the season with
the highest content in perennial species. The seasonal variation was only examined in the
large brown seaweed, but also taking into account the larger availability of nutrients during
fall and winter stimulating production of building blocks.
Proteins, peptides and amino acids from seaweed have shown positive bioactive
effects in diabetes, cancer, AIDS, agglutination of blood cells and prevention of vascular
diseases.
74
The amino acid profile of some seaweed species is similar to that of animal foods. Extracts
of valuable amino acids for feed supplement could be of potential, because essential
amino acids cannot be replaced by other compounds. The essential amino acids need to
be present in the right quanteties in order to make proteins. The genera Ulva,
Laminaria/Saccharina, Sargassum (also ephemeral) and Chondrus have the best profiles
compared to amino acids needed in fish feed. As mentioned, Ulva also has the highest
total protein content taking the four species into account.
The lipid content of seaweed species of interest is highest in Palmaria and Sargassum
and these species also have the best (lowest) n-6/n-3 ratio. Seaweed is especially rich in
eicosapentaenoic acid (EPA). The hisghest lipid contents of seaweed are found during
winter (low temperature environment), however summer for Fucus. Seaweed lipids have
been tested positive as immune stimulant and fucosterol decreases the concentration of
cholesterol in animal and humans. In addition to this, other general effects of PUFAs are
e.g. anti-arteriosclerosis, anti-hypertension, anti-inflammation and immunoregulation.
The content of pigments in the seaweed of interest was highest during spring in
the few species tested. The Porphyra generus was outstanding in carotenoid content
(precursor of vitamin A) followed by Palmaria. Fucoxanthin content was high in the brown
algae and with maximal content in Fucus serratus.
The pigments have shown bioactivity effect towards e.g. cancer, obesity,
decreasing blood glucose and as an anti-oxidant.
The species of Laminaria/Saccharina and Ulva were the species of interest in
Denmark with the highest content in most minerals. Seaweed is very good accumulators
of minerals. Seaweed is even better source of minerals than vegetables. Iodine can even
be concentrated in great concentrations that this should be taken into account, together
with heavy metals.
Porphyra species have the best vitamin profile in regard to highest concentration and
profile for human consumption. This species had highest concentrations in most vitamin
species followed by Palmaria, Ascophyllum, Ulva and then Fucus species. Winter and
spring seemed to be the best season to harvest seaweed for the content of vitamins with
regard to the tested C, B3, B7 and B12 in the investigated species.
Phenol content is highest (up to 14 % of dry weight) in the large brown seaweed
species that is available in large quantities at the shores of Danish. The seasonal
variations in concentration are pronounced, from less than 1 % to 14 % of dry weight.
These variations can be different due to species (reproductive state in different seasons)
and differences in the same species due to differences in habitat. As a source of phenols
for antioxidant purposes the Fucus, Ascophyllum and Sargassum is the best, however
Fucus has the advantage that it is abundant as far as the Baltic.
The phlorotannins (phenolic group) shows bioactive effectssuch as anti-oxidant
activity, radiation protection, antibiotics, anti-diabetes and antifouling. Phlorotannins would
be potential candidates for the development of natural antioxidants for further industrial
applications such as functional foods, cosmetics and pharmaceuticals.
The scarce data on seaweed with antifoulant properties from other metabolites
point on the species Ulva and Laminaria as potential candidates of the seaweed species of
interest in Denmark.
Powder and extract of seaweed has shown bioactive effects such as antioxidant, peroxidation of fatty acids, anti-bacterial, anti-fungical and anti-inflammatory.
Almost all genera of seaweed have shown effect.
75
Effects on animals fed on seaweed mainly as a source of lipids, proteins, dietary fibres or
other polysaccharides. These include higher milk yield in cattle, increased growth rate of
lambs, increased iodine concentration in tissues and change in intestinal bacterial
communities of pigs, and accumulation of triglycerides in sea bream. In several of the
experiments the growth performances are increased or with no effect. Seaweed is a
potential candidate for feed supplement with beneficial effects on the health or the desired
properties of the animal and product.
Seaweed not only accumulates the desired minerals and trace metals, but also
possible metals and heavy metals from the surrounding environment. This can be
exploited, and seaweed can be used as biofilter. Kainic acid and high inorganic arsenic are
toxic and accumulated and reported in species such as Palmaria palmata and Sargassum
sp.
Legislation and limiting values of e.g. heavy metals in seaweed for human
consumption is absent in Denmark. Regulations by EU on food (non-specified) should be
followed.
Feedstock
Feedstock is important. Large quantities and year round supply are preferred. This is in
regard to seaweed as fresh salad in the stores but also when biorefineries of the future
relies on seaweed as feedstock for their industry.
Natural harvest in Denmark is not an optimal choice for feedstock supply. The
shores are not rocky, however some with boulders. The inner Danish waters are short of
large forests of seaweed and handraked harvest is not possible due to the lack of tides.
Feedstock for natural harvest at shores could be Sargassum in summer in especially
Limfjorden, Gracilaria in e.g. Horsen fjord and Fucus in most of the Danish shores.
Cultivation of seaweed in Denmark is possible. Tank cultivation is possible with
most of the species mentioned; however expenses are high, because of pumps,
maintenance and high labour costs. This means that a candidate species should either be
very valuable or have a very high productivity. The valuable Chondrus has been tested in
tank cultivation in Denmark ((Bruhn et al., 2008)) and Ulva is being tested at present. The
conclusion in the outdoor Chondrus pilot and demonstration experiment was that energy
expenses were 6-fold higher than the income. Off shore cultivation is of great potential in
Denmark. Candidate species are Saccharina, Laminaria and Palmaria. These species fulfil
the criterias; native, low labour intensive productionsuch as rope cultivation and
sporulation techniques are developed. The species Ulva and Porphyra are not appropiate
for rope cultivation in Denmark as biomass are either lost or labour intensive, respectively.
The only question is if the salinity is high enough in the inner Danish waters for such off
shore cultivation. One producer has recently started a production of Saccharina latissima
South of Århus, and the first year of production was a success. Production has previously
been tested near a fish farm in Great belt (Birkeland, 2008) and S. latissima can also be
produced in the canal of Kiel.
Cultivation-wise in large scale off-shore production Laminaria would be preferable
with the specific growth rate, controllable lifecycle and well known seedling method;
however, I also believe that the Fucus species would be of interest. This species is already
very abundant even in the low salinity southern parts of Denmark, in large quantities and is
now just thought of as a weed.
76
Conclusions are not possible to make on the decition of which species to choose for
extraction of specifically compounds or exploitation of the entire seaweed biomass in a
biorefinery of the future. However, this report is meant as a reference book for future
utilisation of seaweed biomass of Denmark or other countries with the mentioned species.
The Tables of each biochemical compound makes good overwievs and summarises
worldwide scientific research. This is supported by text and explanations of the chemistry
of the compounds. The reference book can be used for the search of a bioactive
compound in certain seaweed feedstock or if a special compound is desired for extraction,
what species should be harvested or cultivated.
Saccharina latissima on mussel (photo: Holdt, 2010)
77
Reference List
Almela,C., Algora,S., Benito,V., Clemente,M.J., Devesa,V., Suner,M.A., Velez,D., Montoro,R.,
2002. Heavy metal, total arsenic, and inorganic arsenic contents of algae food products.
Journal of Agricultural and Food Chemistry 50(4), 918-923.
Alveal,K., Romo,H., Werlinger,C., Oliveira,E.C., 1997. Mass cultivation of the agar-producing alga
Gracilaria chilensis (Rhodophyta) from spores. Aquaculture 148, 77-83.
Amano,H., Kakinuma,M., Coury,D.A., Ohno,H., Hara,T., 2005. Effect of a seaweed mixture on
serum lipid level and platelet aggregation in rats. Fisheries Science 71, 1160-1166.
Amsler,C.D., Fairhead,V.A., 2005. Defensive and sensory chemical ecology of brown algae. In:
Callow,J.A. (Ed.), Advances in Botanical Research
Incorporating Advances in Plant Pathology. Academic Press, pp. 1-91.
Andersson,L., Lidgren,G., Bohlin,L., Magni,L., Ogren,S., Afzelius,L., 1983. Studies of Swedish
marine organisms .1. Screening of biological-activity. Acta Pharmaceutica Suecica 20(6),
401-414.
Arasaki,S., Arasaki,T., 1983. Low calorie, high nutrition vegetables from the sea. To help you look
and feel better. Japan Publication, Inc, Tokyo.
Arbona,J.F., Molla,M., 2006. Cultivation of brown seaweed-Alaria esculenta. Rep 21, 1-50, BIM.
Archer,G.S., 2005. Reducing stress in sheep by feeding the seaweed Ascophyllum nodosum. Texas
A&M University, pp. 1-129.
Arnold,T.M., Targett,N.M., 2000. Evidence for metabolic turnover of polyphenolics in tropical
brown algae. Journal of Chemical Ecology 26(6), 1393-1410.
Ask,E.I., Azanza,R.V., 2002. Advances in cultivation technology of commercial eucheumatoid
species: a review with suggestions for future research. Aquaculture 206, 257-277.
Astorg,P., 1997. Food carotenoids and cancer prevention: An overview of current research. Trends
in Food Science & Technology 8(12), 406-413.
Athanasiadis,A., 1996. Taxononisk litteratur och biogeografi av skandinaviska rödalger och
brunalger. ALGOLOGIA.
Athukorala,Y., Lee,K.W., Kim,S.K., Jeon,Y.J., 2007. Anticoagulant activity of marine green and
brown algae collected from Jeju Island in Korea. Bioresource Technology 98(9), 1711-1716.
Baardseth,E., 1958. A method of estimating the physode content in brown algae-reprint of report
20. Rep 20, 1-6.
Baardseth,E., Haug,A., 1953. Individual variation of some constituents in brown algae, and
reliability of analytical results. Rep 2, 1-23, Akademisk Trykningssentral.
78
Bansemir,A., Blume,M., Schröder,S., Lindequist,U., 2006. Screening of cultivated seaweeds for
antibacterial activity against fish pathogenic bacteria. Aquaculture 252(1), 79-84.
Barbarino,E., Lourenço,S., 2005. An evaluation of methods for extraction and quantification of
protein from marine macro- and microalgae. Journal of Applied Phycology 17(5), 447-460.
Bartsch,I., Wienke,C., Bischof,K., Buchholz,C.M., Buck,B.H., Eggert,A., Feuerpfeil,P., Hanelt,D.,
Jacobsen,S., Karez,R., Karsten,U., Molis,M., Roleda,M.Y., Schubert,H., Schumann,R.,
Valentin,K., Weinberger,F., Wiese,J., 2008a. The genus Laminaria sensu lato: recent
insights and developments. European Journal of Phycology 43(1), 1-86.
Bartsch,I., Wiencke,C., Bischof,K., Buchholz,C.M., Buck,B.H., Eggert,A., Feuerpfeil,P., Hanelt,D.,
Jacobsen,S., Karez,R., Karsten,U., Molis,M., Roleda,M.Y., Schubert,H., Schumann,R.,
Valentin,K., Weinberger,F., Wiese,J., 2008b. The genus Laminaria sensu lato: recent
insights and developments. European Journal of Phycology 43(1), 1-86.
Baweja,P., Sahoo,D., García-Jiménez,P., Robaina,R.R., 2009. Seaweed tissue culture as applied to
biotechnology: Problems, achievements and prospects. Phycological Research 57, 45-58.
Berteau,O., Mulloy,B., 2003. Sulfated fucans, fresh perspectives: structures, functions, and
biological properties of sulfated fucans and an overview of enzymes active toward this class
of polysaccharide. Glycobiology 13(6), 29R-40R.
Besada,V., Andrade,J.M., Schultze,F., Gonzalez,J.J., 2009a. Heavy metals in edible seaweeds
commercialised for human consumption. Journal of Marine Systems 75(1-2), 305-313.
Besada,V., Andrade,J.M., Schultze,F., Gonzlez,J.J., 2009b. Heavy metals in edible seaweeds
commercialised for human consumption. Journal of Marine Systems 75(1-2), 305-313.
Bhaskar,N., Hosokawa,M., Miyashita,K., 2004. Comparative evaluation of fatty acid composition
of different Sargassum (Fucales, Phaeophyta) species harvested from temperature and
tropical waters. Journal of Aquatic Food Product Technology 3, 53-70.
Bidwell,R.G.S., McLachlan,J., Lloyd,N.D.H., 1985. Tank cultivation of Irish Moss, Chondrus
crispus Stackh. Bot. Mar. 28, 87-97.
Bird,K.T., Chiles,T.C., Longley,R.E., Kendrick,A.F., Kinkema,M.D., 1993. Agglutinins from
marine macroalgae of the Southeastern United-States. Journal of Applied Phycology 5(2),
213-218.
Birkeland,M.J., 2008. Nitrogen accumulation and primary production by Saccharina latissima
(Phaeophyceae) estimated from mathematical modelling and experimental cultivation near a
sea cage farm: a case study-MSc thesis. University of Copenhagen-Biological Institute, pp.
1-35.
Black,W.A.P., 1950. The seasonal variation in the cellulose content of the common Scottish
Laminariaceae and Fucaceae. Journal of the Marine Biological Association of the United
Kingdom 29(2), 379-387.
79
Blouin,N., Xiugeng,F., Peng,J., Yarish,C., Brawley,S.H., 2007a. Seeding nets with neutral spores of
the red alga Porphyra umbilicalis (L.) Kntzing for use in integrated multi-trophic
aquaculture (IMTA). Aquaculture 270(1-4), 77-91.
Blouin,N., Xiugeng,F., Peng,J., Yarish,C., Brawley,S.H., 2007b. Seeding nets with neutral spores of
the red alga Porphyra umbilicalis (L.) Kntzing for use in integrated multi-trophic
aquaculture (IMTA). Aquaculture 270(1-4), 77-91.
Blunden,G., 1977. Cytokinin activity of seaweed extracts. In: Faulkner,D.J., Fenical,W.H. (Eds.),
Marine Natural Products Chemistry. Plenum Press, New York, pp. 337-344.
Blunden,G., Tyihák,E., 2009. The biochemical basis of immunity of plants treated with seaweed
extracts. pp. Poster.
Bobin-Dubigeon,C., Lahaye,M., Barry,J.L., 1997. Human colonic bacterial degradability of dietary
fibres from sea-lettuce (Ulva sp). Journal of the Science of Food and Agriculture 73(2), 149159.
Boubonari,T., Malea,P., Kevrekidis,T., 2008. The green seaweed Ulva rigida as a bioindicator of
metals (Zn, Cu, Pb and Cd) in a low-salinity coastal environment. Botanica Marina 51(6),
472-484.
Boyd,K.G., Adams,D.R., Burgess,J.G., 1999. Antibacterial and repellent activities of marine
bacteria associated with algal surfaces. Biofouling 14(3), 227-236.
Browne,K.L., 2001. Mariculture of the edible red alga Palmaria palmata. Queen's University of
Belfast, UK, pp. 1-186.
Bruhn,A., Rasmussen,M.B., Olesen,B., Worm,T., 2008. Kommerciel dyrkning af carrageentang
(Chondrus crispsu) i danske farvande. 1-62, Danmarks Miljøundersøgelser.
Buck,B., Buchholz,C., 2005. Support device for the cultivation of macroorganisms in marine
waters. Patent, EP 1720403.
Buck,B.H., Buchholz,C.M., 2004a. The offshore-ring: A new system design for the open ocean
aquaculture of macroalgae. J. Appl. Phycol. 16, 335-368.
Buck,B.H., Buchholz,C.M., 2004b. The offshore-ring: A new system design for the open ocean
aquaculture of macroalgae. Journal of Applied Phycology 16(5), 355-368.
Burtin,P., 2003. Nutritional value of seaweeds. Electronic Journal of Environmental, Agricultural
and Food Chemistry 2(4), 498-503.
Cáceres,P.J., Carlucci,M.J., Damonte,E.B., Matsuhiro,B., Zúñiga,E.A., 2000. Carrageenans from
chilean samples of Stenogramme interrupta (Phyllophoraceae): structural analysis and
biological activity. Phytochemistry 53(1), 81-86.
Cardozo,K.H.M., Guaratini,T., Barros,M.P., Falcão,V.R., Tonon,A.P., Lopes,N.P., Campos,S.,
Torres,M.A., Souza,A.O., Colepicolo,P., Pinto,E., 2007. Metabolites from algae with
80
economical impact. Comparative Biochemistry and Physiology Part C: Toxicology &
Pharmacology 146(1-2), 60-78.
Cérantola,S., Breton,F., Ar Gall,E., Deslandes,E., 2006. Co-occurrence and antioxidant activities of
fucol and fucophlorethol classes of polymeric phenols in Fucus spiralis. Botanica Marina
49(4), 347-351.
Chapman,V.J., 1970. Seaweeds and their uses, 2 ed. Methuen & Co. ltd., London.
Chen,Y.H., Tu,C.J., Wu,H.T., 2004. Growth-inhibitory effects of the red alga Gelidium amansii on
cultured cells. Biological & Pharmaceutical Bulletin 27(2), 180-184.
Chernomorsky,S., Segelman,A., Poretz,R.D., 1999. Effect of dietary chlorophyll derivatives on
mutagenesis and tumor cell growth. Teratogenesis Carcinogenesis and Mutagenesis 19(5),
313-322.
Chkhikvishvili,I.D., Ramazanov,Z.M., 2000. Phenolic substances of brown algae and their
antioxidant activity. Applied Biochemistry and Microbiology 36(3), 289-291.
Cho,S.H., Kang,S.E., Cho,J.Y., Kim,A.R., Park,S.M., Hong,Y.K., Ahn,D.H., 2007. The antioxidant
properties of brown seaweed (Sargassum siliquastrum) extracts. Journal of Medicinal Food
10(3), 479-485.
Choi,H.G., Kim,Y.S., Lee,S.J., Nam,K.W., 2007. Growth and reproductive patterns of Undaria
pinnatifida sporophytes in a cultivation farm in Busan, Korea. Journal of Applied Phycology
19(2), 131-138.
Choi,J.-S., Cho,J.-Y., Jin,L.-G., Jin,H.-J., Hong,Y.-K., 2002. Procedures for the axenic isolation of
conchocelis and monospores from the red seaweed Porphyra yezoensis. J. Appl. Phycol. 14,
115-221.
Chopin,T., Gallant,T., Davison,I., 1995. Phosphorus and nitrogen nutrition in Chondrus crispus
(Rhodophyta): Effects on total phosphorus and nitrogen content, carrageenan production,
and photosynthetic pigments and metabolism. J. Phycol. 31, 283-293.
Chopin,T., Sharp,G., Belyea,E., Semple,R., Jones,D., 1999a. Open-water aquaculture of the red
alga Chondrus crispus in Prince Edward Island, Canada. Hydrobiologia 398/399, 417-425.
Chopin,T., Sharp,G., Belyea,E., Semple,R., Jones,D., 1999b. Open-water aquaculture of the red
alga Chondrus crispus in Prince Edward Island, Canada. Hydrobiologia 398-399(0), 417425.
Christensen,L., 2007. Cultivation of algae in bubble column photobioreactors-PhD-thesis.
Department of Biochemistry and Molecular Biology, University of Southern Denmark, pp.
1-131.
Cloughley,G., Burbridge,E., Kraan,S., Guiry,M.D., Smyth,P.P.A., 2008. Iodine uptake and efflux
by macroalgae. pp. 81.
81
Connan,S., Delisle,F., Deslandes,E., Ar Gall,E., 2006. Intra-thallus phlorotannin content and
antioxidant activity in Phaeophyceae of temperate waters. Botanica Marina 49(1), 39-46.
Connan,S., Goulard,F., Stiger,V., Deslandes,E., Ar Gall,E., 2004. Interspecific and temporal
variation in phlorotannin levels in an assemblage of brown algae. Botanica Marina 47(5),
410-416.
Craigie,J.S., 2010. Seaweed stimuli in plant science and agriculture.
Cruz-Uribe,O., Cheney,D.P., Rorrer,G.L., 2007b. Comparison of TNT removal from seawater by
three marine macroalgae. Chemosphere 67(8), 1469-1476.
Cruz-Uribe,O., Cheney,D.P., Rorrer,G.L., 2007a. Comparison of TNT removal from seawater by
three marine macroalgae. Chemosphere 67(8), 1469-1476.
Darcy-Vrillon,B., 1993. Nutritional aspect of the developing use of marine macroalgae for the
human foods industry. International Journal of Food Science and Nutrition 44, 23-35.
Dawczynski,C., Schubert,R., Jahreis,G., 2007. Amino acids, fatty acids, and dietary fibre in edible
seaweed products. Food Chemistry 103(3), 891-899.
Dembitsky,V.M., Pechenkinashubina,E.E., Rozentsvet,O.A., 1991. Glycolipids and fatty-acids of
some seaweeds and marine grasses from the Black-sea. Phytochemistry 30(7), 2279-2283.
Dembitsky,V.M., Rozentsvet,O.A., 1990. Phospholipid composition of some marine red algae.
Phytochemistry 29(10), 3149-3152.
Dembitsky,V.M., Rozentsvet,O.A., Pechenkina,E.E., 1990. Glycolipids, phospholipids and fattyacids of brown-algae species. Phytochemistry 29(11), 3417-3421.
Deville,C., Damas,J., Forget,P., Dandrifosse,G., Peulen,O., 2004. Laminarin in the dietary fibre
concept. Journal of the Science of Food and Agriculture 84(9), 1030-1038.
Deville,C., Gharbi,M., Dandrifosse,G., Peulen,O., 2007. Study on the effects of laminarin, a
polysaccharide from seaweed, on gut characteristics. Journal of the Science of Food and
Agriculture 87(9), 1717-1725.
Dierick,N., Ovyn,A., De Smet,S., 2009. Effect of feeding intact brown seaweed Ascophyllum
nodosum on some digestive parameters and on iodine content in edible tissues in pigs.
Journal of the Science of Food and Agriculture 89(4), 584-594.
Dietrich,C.P., Farias,G.G.M., de Abreu,L.R.D., Leite,E.L., da Silva,L.F., Nader,H.B., 1995. A new
approach for the characterization of polysaccharides from algae: presence of four main
acidic polysaccharides in three species of the class Phaeophycea. Plant Science 108(2), 143153.
Dobretsov,S., 2005. Suppression of settlement of larvae of fouling organism by water-soluble
substances from epibiotic bacteria. Russian Journal of Marine Biology 31(6), 367-372.
82
Dobretsov,S.V., 1999. Effects of macroalgae and biofilm on settlement of blue mussel (Mytilus
edulis L.) larvae. Biofouling 14(2), 153-165.
Dobretsov,S.V., Qian,P.-Y., 2002. Effect of bacteria associated with the green alga Ulva reticulata
on marine micro-and macrofouling. Biofouling 18(3), 217-228.
Douady,D., Rousseau,B., Caron,L., 1994. Fucoxanthin-Chlorophyll a/c light-harvesting complexes
of Laminaria saccharina: Partial amino acid sequences and arrangement in thylakoid
membranes. Biochemistry 33(11), 3165-3170.
Dubber,D., Harder,T., 2008. Extracts of Ceramium rubrum, Mastocarpus stellatus and Laminaria
digitata inhibit growth of marine and fish pathogenic bacteria at ecologically realistic
concentrations. Aquaculture 274(2-4), 196-200.
Durcan,J., Stengel,D., Cave,R., Tyrrell,L., McGovern,E., 2010. Determination of total and
inorganic arsenic in Irish macroalgae. XX International Seaweed Symposium, Mexico.
Dworjanyn,S.A., de Nys,R., Steinberg,P.D., 1999. Localisation and surface quantification of
secondary metabolites in the red alga Delisea pulchra. Marine Biology 133(4), 727-736.
Dworjanyn,S.A., de Nys,R., Steinberg,P.D., 2006. Chemically mediated antifouling in the red alga
Delisea pulchra. Marine Ecology-Progress Series 318, 153-163.
Dworjanyn,S.A., Pirozzi,I., Liu,W., 2007. The effect of the addition of algae feeding stimulants to
artificial diets for the sea urchin Tripneustes gratilla. Aquaculture 273(4), 624-633.
Edwards,M., 2007a. The cultivation of the edible red alga, Palmaria palmata for aquaculture-PhD
thesis. The Queen's University Belfast-Northern Ireland, pp. 1-169.
Edwards,M., 2007b. The cultivation of the edible red alga, Palmaria palmata for aquaculture. The
Queen's University Belfast-Northern Ireland, pp. 1-169.
Egan,S., Holmstrom,C., Kjelleberg,S., 2001. Pseudoalteromonas ulvae sp nov., a bacterium with
antifouling activities isolated from the surface of a marine alga. International Journal of
Systematic and Evolutionary Microbiology 51, 1499-1504.
Egan,S., Thomas,T., Holmstrom,C., Kjelleberg,S., 2000. Phylogenetic relationship and antifouling
activity of bacterial epiphytes from the marine alga Ulva lactuca. Environmental
Microbiology 2(3), 343-347.
Enoki,T., Sagawa,H., Tominaga,T., Nishiyama,E., Komyama,N., Sakai,T., Yu,F.G., Ikai,K.,
Kato,I., 2003. Drugs, foods or drinks with the use of algae-derived physiologically active
substances.
Ergün,S., Soyutürk,M., Güroy,B., Güroy,D., Merrifield,D., 2008. Influence of Ulva meal on
growth, feed utilization, and body composition of juvenile Nile tilapia (Oreochromisániloticus) at two levels of dietary lipid. Aquaculture International.
Eriksen,N.T., 2008. The technology of microalgal culturing. Biotechnol. Lett 30, 1525-1536.
83
Eriksen,N.T., Poulsen,B.R., Iversen,J.J.L., 1998. Dual sparging laboratory-scale photobioreactor for
continuous production of microalgae. J. Appl. Phycol. 10, 377-382.
EU, 2008. KOMMISSIONENS FORORDNING (EF) Nr. 629/2008, af 2. juli 2008, om ændring af
forordning (EF) nr. 1881/2006 om fastsættelse af grænseværdier for bestemte forurenende
stoffer i fødevarer. pp. 6-9.
Fan,D., Hodges,D.M., Zhang,J., Wang-Pruski,G., Kirby,C.W., Ji,X., Locke,S.J., Critchley,A.T.,
Prithiviraj,B., 2010. Commercial Ascophyllum nodosum extract enhances phenolic
antioxidant content of spinach (Spinacia oleracea L.) that imparts protective effects on
Caenorhabditis elegans against oxidative stress and thermal stress.
FAO, 2008. FAO-statistics.
Featonby-Smith,B.C., VanStaden,J., 1983. The effect of seaweed concentrate on the growth of
tomato plants in nematode-infested soil. Scientia Horticulturae 20(2), 137-146.
Fernandez,L.E., Valiente,O.G., Mainardi,V., Bello,J.L., Velez,H., Rosado,A., 1989. Isolation and
characterization of an antitumor active agar-type polysaccharide of Gracilaria
dominguensis. Carbohydrate Research 190(1), 77-83.
Fleurence,J., 1999. Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends in
Food Science & Technology 10(1), 25-28.
Fleury,N., Lahaye,M., 1991. Chemical and physicochemical characterization of fibers from
Laminaria digitata (Kombu Breton) - A physiological approach. Journal of the Science of
Food and Agriculture 55(3), 389-400.
Floreto,E.A.T., Teshima,S., 1998. The fatty acid composition of seaweeds exposed to different
levels of light intensity and salinity. Botanica Marina 41(5), 467-481.
Foster,G.G., Hodgson,A.N., 1998. Consumption and apparent dry matter digestibility of six
intertidal macroalgae by Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae).
Aquaculture 167(3-4), 211-227.
Foti,M.C., 2007. Antioxidant properties of phenols. Journal of Pharmacy and Pharmacology 59(12),
1673-1685.
Francesconi,K.A., Edmonds,J.S., 1997. Arsenic and marine organisms. ACADEMIC PRESS INC,
SAN DIEGO.
Freile-Pelegrín,Y., Morales,J.L., 2004. Antibacterial activity in marine algae from the coast of
Yucatan, Mexico. Botanica Marina 47(2), 140-146.
Freile-Pelegrín,Y., Robledo,D., 1997. Effects of season on the agar content and chemical
characteristics of Gracilaria cornea from Yucatan, Mexico. Botanica Marina 40(4), 285290.
84
Gahan,D.A., Lynch,M.B., Callan,J.J., O'Sullivan,J.T., O'Doherty,J.V., 2009. Performance of
weanling piglets offered low-, medium- or high-lactose diets supplemented with a seaweed
extract from Laminaria spp. Animal 3(1), 24-31.
Galland-Irmouli,A.V., Fleurence,J., Lamghari,R., Luçon,M., Rouxel,C., Barbaroux,O.,
Bronowicki,J.P., Villaume,C., Guéant,J.L., 1999. Nutritional value of proteins from edible
seaweed Palmaria palmata (dulse). The Journal of Nutritional Biochemistry 10(6), 353-359.
Ganesan,P., Kumar,C.S., Bhaskar,N., 2008. Antioxidant properties of methanol extract and its
solvent fractions obtained from selected Indian red seaweeds. Bioresource Technology
99(8), 2717-2723.
Gao,J., Qin,S., Zhang,Y., 2006b. Rapid optimization of process conditions for cultivation of
transgenic Laminaria japonica gametophyte cells in a stirred-tank bioreactor. Chemical
Engineering Journal 122(1-2), 11-14.
Gao,J., Qin,S., Zhang,Y., 2006a. Rapid optimization of process conditions for cultivation of
transgenic Laminaria japonica gametophyte cells in a stirred-tank bioreactor. Chemical
Engineering Journal 122(1-2), 11-14.
Garbary,D.J., DeWreede,R.E., 1988. Life history phases in natural populations of Gigartinaceae
(Rhodophyta): quantification using resorcinol. In: Lobban,C.S., Chapman,D.J., Kremer,B.P.
(Eds.), Experimental phycology : A laboratory manual. Cambridge University Press, pp. 1291.
Garcia-Jimenez,P., Marian,F.D., Rodrigo,M., Robaina,R.R., 1999. Sporulation and sterilization
method for axenic culture of Gelidium canariensis. J. Biotechnol. 70, 227-229.
Gardiner,G.E., Campbell,A.J., O'Doherty,J.V., Pierce,E., Lynch,P.B., Leonard,F.C., Stanton,C.,
Ross,R.P., Lawlor,P.G., 2008. Effect of Ascophyllum nodosum extract on growth
performance, digestibility, carcass characteristics and selected intestinal microflora
populations of grower-finisher pigs. Animal Feed Science and Technology 141(3-4), 259273.
Geiszinger,A., Goessler,W., Pedersen,S.N., Francesconi,K.A., 2001. Arsenic biotransformation by
the brown macroalga Fucus serratus. Environmental Toxicology and Chemistry 20(10),
2255-2262.
Gessner,F., 1971. Wasserpermeabilitit und Photosynthese bei marinen Algen. Botanica Marina 14,
29-31.
Gessner,F., Schramm,W., 1971. Salinity: Plants. In: Kinne,O. (Ed.), Marine Ecology. Wiley, New
York, pp. 705-820.
Ghosh,T., Chattopadhyay,K., Marschall,M., Karmakar,P., Mandal,P., Ray,B., 2009. Focus on
antivirally active sulfated polysaccharides: From structure-activity analysis to clinical
evaluation. Glycobiology 19(1), 2-15.
Ginzberg,A., Cohen,M., Sod-Moriah,U.A., Shany,S., Rosenshtrauch,A., Arad,S., 2000. Chickens
fed with biomass of the red microalga Porphyridium sp. have reduced blood cholesterol
85
level and modified fatty acid composition in egg yolk. Journal of Applied Phycology 12(35), 325-330.
Glenn,E.P., Moore,D., Fitzsimmons,K., Azevedo,C., 1996. Spore culture of the edible red seaweed,
Gracilaria parvispora (Rhodophya). Aquaculture 142, 59-74.
Goemar, 2010. Goemar. www.goemar.fr.
Gordillo,F.J.L., Matthew,J.D., Graham,S., 2002. Nitrate and phosphate uptake characteristics of
three species of brown algae cultured at low salinity. Mar Ecol Prog Ser 234, 111-118.
Gravett,R.B., 2000. The effect of Ascophyllum nodosum on immune function, performance, and
carcass characteristics of sheep and cattle. Graduate Faculty of Texas Tech University,
pp. 1-86.
Greger,M., Malm,T., Kautsky,L., 2007. Heavy metal transfer from composted macroalgae to crops.
European Journal of Agronomy 26(3), 257-265.
Guist,G.G., 1990. Applications for seaweed hydrocolloids in prepared foods. In: Akatsuka,I. (Ed.),
Introduction to Applied Phycology. SPB Academic Publishing, The Hague, The
Netherlands, pp. 391-400.
Haddad,A.M.G., Ormond,R.F.G., 1994. Use of photography and image analysis for In situ
monitoring of growth rates of intertidal fucoid algae. Journal of the Marine Biological
Association of the UK 74(03), 727-730.
Hammerstrom,K., Dethier,M.N., Duggins,D.O., 1998. Rapid phlorotannin induction and relaxation
in five Washington kelps. Marine Biology Progress Series 165, 263-305.
Han,J.G., Syed,A.Q., Kwon,M., Ha,J.H., Lee,H.Y., 2008. Antioxident, immunomodulatory and
anticancer activity of fucoidan isolated from Fucus vesiculosus. Journal of Biotechnology
136(Supplement 1), S571.
Haug,A., Jensen,A., 1954. Seasonal variation in the chemical composition of Alaria esculenta,
Laminaria saccharina, Laminaria hyperborea and Laminaria digitata from Northern
Norway. Rep 4, 1-14, Akademisk Trykningssentral.
Haug,A., Larsen,B., 1957. Carotene content of seaweed and seaweed meal. Rep 16, 1-19,
Akademisk Trykningssentral.
Haug,A., Larsen,B., 1958. Brunfarging av tangmel og tangekstrakter (The formation of brown
coloured substances in seaweed and seaweed extracts). Rep 22, 1-18, N.T.H. TRYKK.
Haugan,J.A., Liaaen-Jensen,S., 1989. Algal carotenoids .43. Improved isolation procedure for
fucoxanthin. Phytochemistry 28(10), 2797-2798.
Haugan,J.A., Liaaen-Jensen,S., 1994. Algal carotenoids .54. Carotenoids of brown-algae
(Phaeophyceae). Biochemical Systematics and Ecology 22(1), 31-41.
86
Hayashi,L., Yokoya,N.S., Ostini,S., Pereira,R.T.L., Braga,E.S., Oliveira,E.C., 2008. Nutrients
removed by Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in integrated cultivation
with fishes in re-circulating water. Aquaculture doi:10.1016/j.aquaculture.2008.02.024 (in
press).
Hellio,C., Berge,J.P., Beaupoil,C., Le Gal,Y., Bourgougnon,N., 2002. Screening of marine algal
extracts for anti-settlement activities against microalgae and macroalgae. Biofouling 18(3),
205-215.
Hellio,C., De La Broise,D., Dufosse,L., Le Gal,Y., Bourgougnon,N., 2001. Inhibition of marine
bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling
paints. Marine Environmental Research 52(3), 231-247.
Hemmingson,J., Falshaw,R., Furneaux,R., Thompson,K., 2006. Structure and antiviral activity of
the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta). Journal of
Applied Phycology 18(2), 185-193.
Heo,S.J., Park,E.J., Lee,K.W., Jeon,Y.J., 2005. Antioxidant activities of enzymatic extracts from
brown seaweeds. Bioresource Technology 96(14), 1613-1623.
Heo,S.J., Jeon,Y.J., 2008. Protective effect of fucoxanthin isolated from Sargassum siliquastrum on
UV-B induced cell damage. Journal of Photochemistry and Photobiology B: Biology In
Press, Accepted Manuscript.
Herbreteau,F., Coiffard,L.J.M., Derrien,A., DeRoeckHoltzhauer,Y., 1997. The fatty acid
composition of five species of macroalgae. Botanica Marina 40(1), 25-27.
Hoebler,C., Guillon,F., Darcy-Vrillon,B., Vaugelade,P., Lahaye,M., Worthington,E., Duee,P.H.,
Barry,J.L., 2000. Supplementation of pig diet with algal fibre changes the chemical and
physicochemical characteristics of digesta. Journal of the Science of Food and Agriculture
80(9), 1357-1364.
Hoffman,R., Paper,D.H., Donaldson,J., Alban,S., Franz,G., 1995. Characterization of a laminarin
sulfate which inhibits basic fibroblast growth-factor binding and endothelial-cell
proliferation. Journal of Cell Science 108, 3591-3598.
Holdt,S.L., 2009. Nutrient reduction in aquaculture waste by macroalgae production. University of
Southern Denmark, Odense, pp. 1-80.
Holmstrom,C., Egan,S., Franks,A., McCloy,S., Kjelleberg,S., 2002. Antifouling activities expressed
by marine surface associated Pseudoalteromonas species. FEMS Microbiology Ecology
41(1), 47-58.
Honya,M., Kinoshita,T., Ishikawa,M., Mori,H., Nisizawa,K., 1994. Seasonal-variation in the lipidcontent of cultured Laminaria-japonica - fatty-acids, sterols, beta-carotene and tocopherol.
Journal of Applied Phycology 6(1), 25-29.
Horn,S.J., 2000. Bioenergy from brown seaweeds. Department of Biotechnology, Norwegian
University of Science and Technology NTNU, NTNU, pp. 1-82.
87
Hou,X.L., Yan,X.J., 1998. Study on the concentration and seasonal variation of inorganic elements
in 35 species of marine algae. Science of the Total Environment 222(3), 141-156.
Huang,H.L., Wang,B.G., 2004. Antioxidant capacity and lipophilic content of seaweeds collected
from the Qingdao coastline. Journal of Agricultural and Food Chemistry 52(16), 4993-4997.
Ichikawa,S., Kamoshida,M., Hanaoka,K., Hamano,M., Maitani,T., Kaise,T., 2006. Decrease of
arsenic in edible brown algae Hijikia fusiforme by the cooking process. Applied
Organometallic Chemistry 20(9), 585-590.
Ikeda,K., Kitamura,A., Machida,H., Watanabe,M., Negishi,H., Hiraoka,J., Nakano,T., 2003. Effect
of Undaria pinnatifida (Wakame) on the development of cerebrovascular diseases in strokeprone spontaneously hypertensive rats. Clinical and Experimental Pharmacology and
Physiology 30(1-2), 44-48.
Indergaard,M., Minsaas,J., 1991. Seaweed resources in Europe: Uses and potential. In: Guiry,M.D.,
Blunden,G. (Eds.), Animal and human nutrition. John Wiley and Sons, Chichester, pp. 2164.
Ishihara,K., Murata,M., Kaneniwa,M., Saito,H., Komatsu,W., Shinohara,K., 2000. Purification of
stearidonic acid (18 : 4(n-3)) and hexadecatetraenoic acid (16 : 4(n-3)) from algal fatty acid
with lipase and medium pressure liquid chromatography. Bioscience Biotechnology and
Biochemistry 64(11), 2454-2457.
Ishihara,K., Murata,M., Kaneniwa,M., Saito,H., Shinohara,K., Maeda-Yamamoto,M., 1998.
Inhibition of icosanoid production in MC/9 mouse mast cells by n-3 polyunsaturated fatty
acids isolated from edible marine algae. Bioscience Biotechnology and Biochemistry 62(7),
1412-1415.
Jameson,P.E., 1993. Plant hormones in the algae. Biopress Ltd. {a}.
Jaulneau,V., Lafitte,C., Jacquet,C., Fournier,S., Salamagne,S., Briand,X., Esquerre-Tugaye,M.T.,
Dumas,B., 2010. Ulvan, a sulfated polysaccharide from green algae, activates plant
immunity through the jasmonic acid signaling pathway. Journal of Biomedicine and
Biotechnology.
Jayaraj,J., Norrie,J., Punja,Z.K., 2010. Commercial extract from the brown seaweed Ascophyllum
nodosum reduces fungal diseases in carrot and greenhouse cucumber.
Je,J.-Y., Park,P.J., Kim,E.K., Park,J.S., Yoon,H.D., Kim,K.R., Ahn,C.B., 2009. Antioxidant activity
of enzymatic extracts from the brown seaweed Undaria pinnatifida by electron spin
resonance spectroscopy. LWT - Food Science and Technology 42(4), 874-878.
Jensen,A., 1969b. Tocopherol content of seaweed and seaweed meal .2. Individual, diurnal and
seasonal variations in some Fucaceae. Journal of the Science of Food and Agriculture 20(8),
454-&.
Jensen,A., 1969a. Tocopherol content of seaweed and seaweed meal .3. Influence of processing and
storage on content of tocopherols, carotenoids and ascorbic acid in seawood meal. Journal of
the Science of Food and Agriculture 20(10), 622-&.
88
Jensen,A., 1966. Carotenoids of Norwegian brown seaweeds and of seaweed meals. Rep 31, 1-138,
TAPIR.
Jensen,A., 1960. Produksjon av tangmel. Rep 24, 1-23, N.T.H. TRYKK.
Jensen,A., 1956. Component sugars of some common brown algae. Rep 9, 1-8, Akademisk
Trykningssentral.
Jensen,A., Haug,A., 1956. Geographical and seasonal variation in the chemical composition of
Laminaria hyperborea and Laminaria digitata from the Norwegian coast. Rep 14, 1-8,
Akademisk Trykningssentral.
Jensen,A., Nebb,H., Sæter,E.A., 1968. The value of Norwegian seaweed meal as a mineral
supplement for dairy cows. Rep 32, 1-35, TAPIR-TRYKK.
Johnson,C.R., Mann,K.H., 1986. The importance of plant defence abilities to the structure of
subtidal seaweed communities: The kelp Laminaria longicruris de la Pylaie survives
grazing by the snail Lacuna vincta (Montagu) at high population densities. Journal of
Experimental Marine Biology and Ecology 97(3), 231-267.
Jones,A.L., Harwood,J.L., 1992. Lipid composition of the brown algae Fucus vesiculosus and
Ascophyllum nodosum. Phytochemistry 31(10), 3397-3403.
Jormalainen,V., Wikstrom,S.A., Honkanen,T., 2008. Fouling mediates grazing: intertwining of
resistances to multiple enemies in the brown alga Fucus vesiculosus. Oecologia 155(3), 559569.
Kaeffer,B., Benard,C., Lahaye,M., Blottiere,H.M., Cherbut,C., 1999. Biological properties of ulvan,
a new source of green seaweed sulfated polysaccharides, on cultured normal and cancerous
colonic epithelial tells. Planta Medica 65(6), 527-531.
Kanazawa,K., Ozaki,Y., Hashimoto,T., Das,S.K., Matsushita,S., Hirano,M., Okada,T., Komoto,A.,
Mori,N., Nakatsuka,M., 2008. Commercial-scale preparation of biofunctional fucoxanthin
from waste parts of brown sea algae Laminalia japonica. Food Science and Technology
Research 14(6), 573-582.
Kang,K., Park,Y., Hwang,H.J., Kim,S.H., Lee,J.G., Shin,H.C., 2003. Antioxidative properties of
brown algae polyphenolics and their perspectives as chemopreventive agents against
vascular risk factors. Archives of Pharmacal Research 26(4), 286-293.
Karlström,O., 1963. The vitamin B12 content of marine algae. Rep 29, 1-10, N.T.H. TRYKK.
Kawai,H., Motomura,T., Okuda,K., 2005. Isolation and purification techniques for macroalgae. In:
Anderson,R.A. (Ed.), Algal culturing techniques. Phycological Society of America, pp. 133143.
Khan,M.N.A., Cho,J.Y., Lee,M.C., Kang,J.Y., Park,N.G., Fujii,H., Hong,Y.K., 2007. Isolation of
two anti-inflammatory and one pro-inflammatory polyunsaturated fatty acids from the
brown seaweed Undaria pinnatifida. Journal of Agricultural and Food Chemistry 55(17),
6984-6988.
89
Khan,M.N.A., Suk-Choi,J., Lee,M.C., Kim,E., Nam,T.J., Fujii,H., Hong,Y.K., 2008. Antiinflammatory activities of methanol extracts from various seaweed species. Journal of
Environmental Biology 29(4), 465-469.
Khan,W., Hiltz,D.A., Critchley,A.T., Prithiviraj,B., 2010. Detection of cytokinin-like activity in a
commercial, liquid extract of Ascophyllum nodosum using an Arabidopsis thaliana
cytokinin response reporter plant.
Khan,W., Rayirath,U.P., Subramanian,S., Jithesh,M.N., Rayorath,P., Hodges,D.M., Critchley,A.T.,
Craigie,J.S., Norrie,J., Prithiviraj,B., 2009. Seaweed extracts as biostimulants of plant
growth and development. Journal of Plant Growth Regulation 28(4), 386-399.
Khotimchenko,S.V., 1991. Fatty-acid composition of 7 Sargassum species. Phytochemistry 30(8),
2639-2641.
Khotimchenko,S.V., 2005. Lipids from the marine alga Gracilaria verrucosa. Chemistry of Natural
Compounds 41(3), 285-288.
Khotimchenko,S.V., 2003. The fatty acid composition of glycolipids of marine macrophytes.
Russian Journal of Marine Biology 29(2), 126-128.
Khotimchenko,S.V., Levchenko,E.V., 1997. Lipids of the red alga Gracilaria verrucosa (Huds.)
Papenf. Botanica Marina 40(6), 541-545.
Kim,I.H., Lee,J.H., 2008. Antimicrobial activities against methicillin-resistant Staphylococcus
aureus from macroalgae. Journal of Industrial and Engineering Chemistry 14(5), 568-572.
Kim,M.K., Dubacq,J.P., Thomas,J.C., Giraud,G., 1996. Seasonal variations of triacylglycerols and
fatty acids in Fucus serratus. Phytochemistry 43(1), 49-55.
Kiriyama,S., Okazaki,Y., Yoshida,A., 1969. Hypocholesterolemic effect of polysaccharides and
polysaccharide-rich foodstuffs in cholesterol-fed rats. Journal of Nutrition 97(3), 382-&.
Klarzynski,O., Plesse,B., Joubert,J.M., Yvin,J.C., Kopp,M., Kloareg,B., Fritig,B., 2000. Linear
beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol. 124(3), 10271037.
Kobayashi,A., Tai,A., Kanzaki,H., Kawazu,K., 1993. Elicitor-active oligosaccharides from algal
laminaran stimulate the production of antifungal compounds in alfalfa. Zeitschrift fur
Naturforschung C-A Journal of Biosciences 48(7-8), 575-579.
Kotake-Nara,E., Kushiro,M., Zhang,H., Sugawara,T., Miyashita,K., Nagao,A., 2001. Carotenoids
affect proliferation of human prostate cancer cells. J. Nutr. 131(12), 3303-3306.
Kumar,C.S., Ganesan,P., Bhaskar,N., 2008a. In vitro antioxidant activities of three selected brown
seaweeds of India. Food Chemistry 107(2), 707-713.
Kumar,C.S., Ganesan,P., Suresh,P.V., Bhaskar,N., 2008b. Seaweeds as a source of nutritionally
beneficial compounds - A review. Journal of Food Science and Technology-Mysore 45(1),
1-13.
90
Kuznetsova,T.A., Krylova,N.V., Besednova,N.N., Vasiléva,V.N., Zviagintseva,T.N.,
Krashevskii,S.V., Eliakova,L.A., 1994. The effect of translam on the natural resistance
indices of the irradiated organism. Radiatsionnaia Biologiia, Radioecologiia 34, 236-239.
Lahaye,M., 1991. Marine-algae as sources of fibers - determination of soluble and insoluble dietary
fiber contents in some sea vegetables. Journal of the Science of Food and Agriculture 54(4),
587-594.
Lahaye,M., Kaeffer,B., 1997. Seaweed dietary fibres: structure, physico-chemical and biological
properties relevant to intestinal physiology. Sciences des Aliments 17(6), 563-584.
Lahaye,M., Michel,C., Barry,J.L., 1993. Chemical, physicochemical and in vitro fermentation
characteristics of dietary-fibers from Palmaria palmata (L) Kuntze. Food Chemistry 47(1),
29-36.
Lahaye,M., Robic,A., 2007. Structure and functional properties of Ulvan, a polysaccharide from
green seaweeds. Biomacromolecules 8(6), 1765-1774.
Lam,C., Stang,A., Harder,T., 2008. Planktonic bacteria and fungi are selectively eliminated by
exposure to marine macroalgae in close proximity. FEMS Microbiology Ecology 63, 283291.
Lamare,M.D., Wing,S.R., 2001. Calorific content of New Zealand marine macrophytes. New
Zealand Journal of Marine and Freshwater Research 35(2), 335-341.
Lamela,M., Anca,J., Villar,R., Otero,J., Calleja,J.M., 1989. Hypoglycemic activity of several
seaweed extracts. Journal of Ethnopharmacology 27(1-2), 35-43.
Larsen,B., 1958. The influence of season, habitat and age of tissue on the niacin content of some
brown algae. Rep 19, 1-13, N.T.H. TRYKK.
Larsen,B., 1961. The biotin content of marine algae. Rep 26, 1-18, N.T.H. TRYKK.
Larsen,B., Haug,A., 1958. The influence of habitat on the chemical composition of Ascophyllum
nodosum (L.) Le Jol.-reprint of report 20. Rep 20, 29-38, Norwegian Institute of Seaweed
Research.
Larsen,J.C.G., Hansen,P.J., 1986. Tang. Naturhistorisk Museum, Århus.
Le Tutour,B., 1990. Antioxidative activities of algal extracts, synergistic effect with vitamin E.
Phytochemistry 29(12), 3759-3765.
Le Tutour,B., Benslimane,F., Gouleau,M.P., Saadan,B., Quemeneur,F., 1998. Antioxidant and prooxidant activities of the brown algae, Laminaria digitata, Himanthalia elongata, Fucus
vesiculosus, Fucus serratus and Ascophyllum nodosum. Journal of Applied Phycology
10(2), 121-129.
Lee,J.B., Hayashi,K., Hashimoto,M., Nakano,T., Hayashi,T., 2004. Novel antiviral fucoidan from
sporophyll of Undaria pinnatifida (Mekabu). Chemical & Pharmaceutical Bulletin 52(9),
1091-1094.
91
Li,B., Lu,F., Wei,X.J., Zhao,R.X., 2008a. Fucoidan: Structure and bioactivity. Molecules 13(8),
1671-1695.
Li,N., Zhang,Q.B., Song,J.M., 2005. Toxicological evaluation of fucoidan extracted from
Laminaria japonica in Wistar rats. Food and Chemical Toxicology 43(3), 421-426.
Li,Y., Qian,Z.J., Le,Q.T., Kim,M.M., Kim,S.K., 2008b. Bioactive phloroglucinol derivatives
isolated from an edible marine brown alga, Ecklonia cava. Journal of Biotechnology
136(Supplement 1), S578.
Li,Y., Qian,Z.J., Ryu,B., Lee,S.H., Kim,M.M., Kim,S.K., 2009. Chemical components and its
antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorganic &
Medicinal Chemistry In Press, Accepted Manuscript.
Lim,S.N., Cheung,P.C.K., Ooi,V.E.C., Ang,P.O., 2002. Evaluation of antioxidative activity of
extracts from a brown seaweed, Sargassum siliquastrum. Journal of Agricultural and Food
Chemistry 50(13), 3862-3866.
Lobban,C.S., Harrison,P.J., 1994. Seaweed ecology and physiology. Cambridge University Press.
Lüder,U.H., Clayton,M.N., 2004. Induction of phlorotannins in the brown macroalga Ecklonia
radiata (Laminariales, Phaeophyta) in response to simulated herbivorythe first
microscopic study. Planta 218(6), 928-937.
Lüning,K., Pang,S., 2003. Mass cultivation of seaweeds: current aspects and approaches. J. Appl.
Phycol. 15, 115-119.
Mabeau,S., Fleurence,J., 1993. Seaweed in food products: biochemical and nutritional aspects.
Trends in Food Science & Technology 4(4), 103-107.
MacArtain,P., Gill,C.I.R., Brooks,M., Campbell,R., Rowland,I.R., 2007. Nutritional value of edible
seaweeds. Nutrition Reviews 65(12), 535-543.
MacKinnon,S.L., Hiltz,D.A., Ugarte,R.A., Craft,C.A., 2010. Improved methods of analysis for
betaines in Ascophyllum.
Maeda,H., Tsukui,T., Sashima,T., Hosokawa,M., Miyashita,K., 2008a. Seaweed carotenoid,
fucoxanthin, as a multi-functional nutrient. Asia Pacific Journal of Clinical Nutrition 17,
196-199.
Maeda,H., Hosokawa,M., Sashima,T., Miyashita,K., 2008b. Antiobesity effect of fucoxanthin from
edible seaweeds and its multibiological functions. A. C. S. symposium series 993, 376-388.
Maeda,H., Hosokawa,M., Sashima,T., Funayama,K., Miyashita,K., 2005. Fucoxanthin from edible
seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white
adipose tissues. Biochemical and Biophysical Research Communications 332(2), 392-397.
Maher,W.A., 1985. Selenium in macroalgae. Botanica Marina 28(7), 269-273.
92
Mai,K., Mercer,J.P., Donlon,J., 1994. Comparative studies on the nutrition of two species of
abalone, Haliotis tuberculata L. and Haliotis discus Hannai Ino. II. Amino acid composition
of abalone and six species of macroalgae with an assessment of their nutritional-value.
Aquaculture 128(1-2), 115-130.
Makarov,V.N., Makarov,M.V., Schoschina,E.V., 1999. Seasonal dynamics of growth in the Barents
sea seaweeds: Endogenous and exogenous regulation. Botanica Marina 42(1), 43-49.
Marais,M.F., Joseleau,J.P., 2001. A fucoidan fraction from Ascophyllum nodosum. Carbohydrate
Research 336(2), 155-159.
Marinho-Soriano,E., Fonseca,P.C., Carneiro,M.A.A., Moreira,W.S.C., 2006. Seasonal variation in
the chemical composition of two tropical seaweeds. Bioresource Technology 97(18), 24022406.
Marsham,S., Scott,G.W., Tobin,M.L., 2007. Comparison of nutritive chemistry of a range of
temperate seaweeds. Food Chemistry 100(4), 1331-1336.
Martino,A.D., Douady,D., Quinet-Szely,M., Rousseau,B., Crépineau,F., Apt,K., Caron,L., 2004.
The light-harvesting antenna of brown algae. Highly homologous proteins encoded by a
multigene family. European Journal of Biochemistry 267(17), 5540-5549.
Maruyama,H., Tanaka,M., Hashimoto,M., Inoue,M., Sasahara,T., 2007. The suppressive effect of
Mekabu fucoidan on an attachment of Cryptosporidium parvum oocysts to the intestinal
epithelial cells in neonatal mice. Life Sciences 80(8), 775-781.
Matsubara,K., Xue,C., Zhao,X., Mori,M., Sugawara,T., Hirata,T., 2005. Effects of middle
molecular weight fucoidans on in vitro and ex vivo angiogenesis of endothelial cells.
International Journal of Molecular Medicine 15(4), 695-699.
Mayer,A.M.S., Hamann,M.T., 2004. Marine Pharmacology in 2000: Marine compounds with
antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet,
antituberculosis, and antiviral activities; affecting the cardiovascular, immune, and nervous
systems and other miscellaneous mechanisms of action. Marine Biotechnology 6, 37-52.
Mayer,A.M.S., Rodríguez,A.D., Berlinck,R.G.S., Hamann,M.T., 2007. Marine pharmacology in
2003–4: Marine compounds with anthelmintic antibacterial, anticoagulant, antifungal, antiinflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral
activities; affecting the cardiovascular, immune and nervous systems, and other
miscellaneous mechanisms of action. Comparative Biochemistry and Physiology Part C
145, 553-581.
McCandless,E.L., Craigie,J.S., Walter,J.A., 1973. Carrageenans in gametophytic and sporophytic
stages of Chondrus crispus. Planta 112(3), 201-212.
McHugh,D.J., 1987. Production and utilization of products from commercial seaweeds. Food and
Agriculture Organization of the United States.
McHugh,D.J., 2003. A guide to the seaweed industry. Food and Agriculture Organization of the
United Nations, Rome.
93
Mehta,S.K., Gaur,J.P., 2005. Use of algae for removing heavy metal ions from wastewater:
Progress and prospects. Critical Reviews in Biotechnology 25(3), 113-152.
Mercier,L., Lafitte,C., Borderies,G., Briand,X., Esquerre-Tugaye,M.T., Fournier,J., 2001. The algal
polysaccharide carrageenans can act as an elicitor of plant defence. New Phytologist 149(1),
43-51.
Miao,H.Q., Elkin,M., Aingorn,E., Ishai-Michaeli,R., Stein,C.A., Vlodavsky,I., 1999. Inhibition of
heparanase activity and tumor metastasis by laminarin sulfate and synthetic
phosphorothioate oligodeoxynucleotides. International Journal of Cancer 83(3), 424-431.
Michel,C., Lahaye,M., Bonnet,C., Mabeau,S., Barry,J.L., 1996. In vitro fermentation by human
faecal bacteria of total and purified dietary fibres from brown seaweeds. British Journal of
Nutrition 75(2), 263-280.
Michel,C., Macfarlane,G.T., 1996. Digestive fates of soluble polysaccharides from marine
macroalgae: Involvement of the colonic microflora and physiological consequences for the
host. Journal of Applied Bacteriology 80(4), 349-369.
Miki,W., 1991. Biological functions and activities of animal carotenoids. Pure and Applied
Chemistry 63(1), 141-146.
Milton,R.F., 2010. Liquid seaweed as a fertilizer. pp. 428-431.
Miraglio,A.M., 2009. Phospholipids: Structure plus functionality.
Mishra,V.K., Temelli,F., Ooraikul,B., Shacklock,P.F., Craigie,J.S., 1993. Lipids of the red alga,
Palmaria palmata. Botanica Marina 36(2), 169-174.
Mochizuki,H., Takido,J., Oda,H., Yokogoshi,H., 1999. Improving effect of dietary taurine on
marked hypercholesterolemia induced by a high-cholesterol diet in streptozotocin-induced
diabetic rats. Bioscience Biotechnology and Biochemistry 63(11), 1984-1987.
Morgan,K., Wright,J., Simpson,F., 1980. Review of chemical constituents of the red alga Palmaria
palmata (dulse). Economic Botany 34(1), 27-50.
Mori,J., Matsunaga,T., Takahashi,S., Hasegawa,C., Saito,H., 2003. Inhibitory activity on lipid
peroxidation of extracts from marine brown alga. Phytotherapy Research 17(5), 549-551.
Morrissey,J., Kraan,S., Guiry,M.D., 2001. A guide to commercially important seaweeds on the Irish
coast. Published by Bord Iascaigh Mhara, Dun Laoghaire, Co. Dublin.
Mouritsen,O.G., 2009. Tang- grøntsager fra havet. Nyt Nordisk Forlag, Arnold Busck, Copenhagen.
Msuya,F.E., Kyewalyanga,M.S., Salum,D., 2006. The performance of the seaweed Ulva reticulata
as a biofilter in a low-tech, low-cost, gravity generated water flow regime in Zanzibar,
Tanzania. Aquaculture 254(1-4), 284-292.
Munda,I.M., Kremer,B.P., 1977. Chemical composition and physiological properties of fucoids
under conditions of reduced salinity. Marine Biology 42(1), 9-15.
94
Murata,M., Nakazoe,J., 2001. Production and use of marine algae in Japan. Jarq-Japan Agricultural
Research Quarterly 35(4), 281-290.
Murata,M., Ishihara,K., Saito,H., 1999. Hepatic fatty acid oxidation enzyme activities are
stimulated in rats fed the brown seaweed, Undaria pinnatifida (Wakame). J. Nutr. 129(1),
146-151.
Murata,M., Sano,Y., Ishihara,K., Uchida,M., 2002. Dietary fish oil and Undaria pinnatifida
(Wakame) synergistically decrease rat serum and liver triacylglycerol. J. Nutr. 132(4), 742747.
Mustafa,M.G., Wakamatsu,S., Takeda,T.A., Umino,T., Nakagawa,H., 1995. Effects of algae meal
as feed additive on growth, feed-efficiency, and body-composition in Red-sea bream.
Fisheries Science 61(1), 25-28.
Myers,S.P., Conner,J.O., Fitton,J.H., Brooks,L., Rolfe,M., Connellan,P., Wohlmuth,H.,
Cheras,P.A., Morris,C., 2010. A combined phase I and II open label study on the effects of a
seaweed extract nutrient complex on osteoarthritis. Biologics: Targets & Therapy 4, 33-44.
Nagaoka,M., Shibata,H., Kimura,I., Hashimoto,S., 2003. Oligosaccharide derivatives and process
for producing the same. In: Assigned to Kabushiki Yakult Honsha (Ed.), Tokyo/Japan.
Nakagawa,H., Kasahara,S., 1986. Effect of Ulva meal supplement to diet on the lipid metabolism of
red sea bream. Bulletin of the Japanese Society of Scientific Fisheries 52(11), 1887-1893.
Nakayasu,S., Soegima,R., Yamaguchi,K., Oda,T., 2009. Biological activities of fucose-containing
polysaccharide ascophyllan isolated from the brown alga Ascophyllum nodosum. Bioscience
Biotechnology and Biochemistry 73(4), 961-964.
Nakazawa,Y., Sashima,T., Hosokawa,M., Miyashita,K., 2009. Comparative evaluation of growth
inhibitory effect of stereoisomers of fucoxanthin in human cancer cell lines. Journal of
Functional Food 1, 88-97.
Narayan,B., Miyashita,K., Hosakawa,M., 2006. Physiological fffects of eicosapentaenoic acid
(EPA) and docosahexaenoic acid (DHA)A review. Food Reviews International 22(3),
291-307.
Neori,A., Cohen,I., Gordin,H., 1991. Ulva lactuca biofilters for marine fishpond effluents. 2.
Growth rate, yield and C-N ratio. Botanica Marina 34(6), 483-489.
Nishide,E., Uchida,H., 2003. Effects of Ulva powder on the ingestion and excretion of cholesterol
in rats. In: Chapman,A.R.O., Anderson,R.J., Vreeland,V.J., Davison,I.R. (Eds.), Proceedings
of the 17th International Seaweed Symposium. Oxford University Press, Oxford, pp. 165168.
Nishino,T., Nishioka,C., Ura,H., Nagumo,T., 1994. Isolation and partial characterization of a novel
amino sugar-containing fucan sulfate from commercial Fucus vesiculosus fucoidan.
Carbohydrate Research 255(41 ref), 213-224.
95
Nisizawa,K., Noda,H., Kikuchi,R., Watanabe,T., 1987. The main seaweed foods in Japan.
Hydrobiologia 151, 5-29.
Noda,H., 1993. Health benefits and nutritional properties of nori. Journal of Applied Phycology
5(2), 255-258.
Norrie,J., Mansilla,J., Babelis,G., Mondino,C., Ferratto,J., Melgar,R., 2010. The commercial
Ascophyllum nodosum-based seaweed extract "Stimplex®" positively affects the yield and
quality of red globe and superior seedless table grapes.
Nygård,C.A., Dring,M.J., 2008. Influence of salinity, temperature, dissolved inorganic carbon and
nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the
Baltic and Irish Seas. European Journal of Phycology 43(3), 253-262.
Nylund,G.M., Gribben,P.E., de Nys,R., Steinberg,P.D., Pavia,H., 2007. Surface chemistry versus
whole-cell extracts: antifouling tests with seaweed metabolites. Marine Ecology-Progress
Series 329, 73-84.
Okuzumi,J., Takahashi,T., Yamane,T., Kitao,Y., Inagake,M., Ohya,K., Nishino,H., Tanaka,Y.,
1993. Inhibitory effects of fucoxanthin, a natural carotenoid, on N-ethyl-N'-nitro-Nnitrosoguanidine-induced mouse duodenal carcinogenesis. Cancer Letters 68(2-3), 159-168.
Oliveira,E.C., Alveal,K., 1990. The mariculture of Gracilaria (Rhodophyta) for the production of
agar. In: Akatsuka,I. (Ed.), Introduction to Applied Phycology. SPB Academic Publishing,
The Hague, The Netherlands, pp. 553-564.
Ortiz,J., Romero,N., Robert,P., Araya,J., Lopez-Hernández,J., Bozzo,C., Navarrete,E., Osorio,A.,
Rios,A., 2006. Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible
seaweeds Ulva lactuca and Durvillaea antarctica. Food Chemistry 99(1), 98-104.
Ortiz,J., Uquiche,E., Robert,P., Romero,N., Quitral,V., Llanten,C., 2009. Functional and nutritional
value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis
pyrifera. European Journal of Lipid Science and Technology 111(4), 320-327.
Pang,S.J., Lüning,K., 2004a. Breaking seasonal limitation: year-round sporogenesis in the brown
alga Laminaria saccharina by blocking the transport of putative sporulation inhibitors.
Aquaculture 240(1-4), 531-541.
Pang,S.J., Lüning,K., 2006. Tank cultivation of the red alga Palmaria palmata: Year-round
induction of tetrasporangia, tetraspore release in darkness and mass cultivation of vegetative
thalli. Aquaculture 252(1), 20-30.
Pang,S., Lüning,K., 2004b. Tank cultivation of the red alga Palmaria palmata: Effects of
intermittent light on growth rate, yield and growth kinetics. J. Appl. Phycol. 16(2), 93-99.
Panlasigui,L.N., Baello,O.Q., Dimatangal,J.M., Dumelod,B.D., 2003. Blood cholesterol and lipidlowering effects of carrageenan on human volunteers. Asia Pacific Journal of Clinical
Nutrition 12(2), 209-214.
96
Park,P.J., Heo,S.J., Park,E.J., Kim,S.K., Byun,H.G., Jeon,B.T., Jeon,Y.J., 2005. Reactive oxygen
scavenging effect of enzymatic extracts from Sargassum thunbergii. Journal of Agricultural
and Food Chemistry 53(17), 6666-6672.
Patier,P., Yvin,J.C., Kloareg,B., Lienart,Y., Rochas,C., 1993. Seaweed liquid fertilizer from
Ascophyllum nodosum contains elicitors of plant D-glycanases. Journal of Applied
Phycology 5(3), 343-349.
Pavia,H., Cervin,G., Lindgren,A., Åberg,P., 1997. Effects of UV-B radiation and simulated
herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Marine EcologyProgress Series 157, 139-146.
Pavia,H., Åberg,P., 1996. Spatial variation in polyphenolic content of Ascophyllum nodosum
(Fucales, Phaeophyta). Hydrobiologia 326-327(1), 199-203.
Pavia,H., Toth,G.B., 2000. Inducible chemical resistance to herbivory in the brown seaweed
Ascophyllum nodosum. Ecology 81(11), 3212-3225.
Pedersen,M.F., Borum,J., 1996. Nutrient control of algal growth in estuarine waters. Nutrient
limitation and the importance of nitrogen requirements and nitrogen storage among
phytoplankton and species of macroalgae. Mar. Ecol. :Prog. Ser. 142(1-3), 261-272.
Pereira,R., Yarish,C., 2008. Mass production of marine macroalgae. In: Jørgensen,S.E., Fath,B.
(Eds.), Encyclopedia of Ecology. Elsevier, pp. 2236-2247.
Pereira,R., Yarish,C., Sousa-Pinto,I., 2006. The influence of stocking density, light and temperature
on the growth, production and nutrient removal capacity of Porphyra dioica (Bangiales,
Rhodophyta). Aquaculture 252(1), 66-78.
Perelló,G., Martí-Cid,R., Llobet,J.M., Domingo,J.L., 2008. Effects of various cooking processes on
the concentrations of arsenic, cadmium, mercury, and lead in foods. Journal of Agricultural
and Food Chemistry 56(23), 11262-11269.
Plaza,M., Cifuentes,A., Ibáñez,E., 2008. In the search of new functional food ingredients from
algae. Trends in Food Science & Technology 19(1), 31-39.
Plouguerne,E., Hellio,C., Deslandes,E., Veron,B., Stiger-Pouvreau,V., 2008. Anti-microfouling
activities in extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum.
Botanica Marina 51(3), 202-208.
Potin,P., Bouarab,K., Kupper,F., Kloareg,B., 1999. Oligosaccharide recognition signals and defence
reactions in marine plant-microbe interactions. Current Opinion in Microbiology 2(3), 276283.
Queiroz,K.C.S., Medeiros,V.P., Queiroz,L.S., Abreu,L.R.D., Rocha,H.A.O., Ferreira,C.V.,
Jucá,M.B., Aoyama,H., Leite,E.L., 2008. Inhibition of reverse transcriptase activity of HIV
by polysaccharides of brown algae. Biomedicine & Pharmacotherapy 62(5), 303-307.
97
Ragan,M.A., Jensen,A., 1978. Quantitative studies on brown algal phenols. II. Seasonal variation in
polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L.).
Journal of Experimental Marine Biology and Ecology 34(3), 245-258.
Raghavendra,V.B., Lokesh,S., Prakashl,H.S., 2007. Dravya, a product of seaweed extract
(Sargassum wightii), induces resistance in cotton against Xanthomonas campestris pv.
malvacearum. Phytoparasitica 35(5), 442-449.
Rasmussen,R.S., Morrissey,M.T., 2007. Marine biotechnology for production of food ingredients.
In: Taylor,S.L. (Ed.), Advances in Food and Nutrition Research, Volume 52. Elsevier, pp.
237-292.
Rayirath,P., Zhang,J., Kirby,C.W., Benkel,B., Hodges,M.D., Hilz,D., Critchley,A.T., Prithiviraj,B.,
2010. Lipophilic components of Ascophyllum nodosum impart freezing tolerance in
Arabidopsis thaliana through priming osmolyte accumulation and enhancing fatty acid
unsaturation.
Reddy,C.R.K., Gupta,M.K., Mantri,V.A., Jha,B., 2008. Seaweed protoplasts: status,
biotechnological perspectives and needs. Journal of Applied Phycology 20, 619-632.
Reeta,K., Inderdeep,K., Bhatnagar,A.K., 2010. Effect of seaweed liquid fertilizor on growth and
yield of Lycopersicon esculentum.
Reilly,P., O'Doherty,J.V., Pierce,K.M., Callan,J.J., O'Sullivan,J.T., Sweeney,T., 2008. The effects
of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient
digestibility, volatile fatty acid concentrations and the immune status of the weaned pig.
Animal 2(10), 1465-1473.
Renn,D., 1997. Biotechnology and the red seaweed polysaccharide industry: Status, needs and
prospects. Trends in Biotechnology 15(1), 9-14.
Renn,D.W., Noda,H., Amano,H., Nishino,T., Nishizana,K., 1994a. Antihypertensive and
antihyperlipidemic effects of funoran. Fischeries Science 60, 423-427.
Renn,D.W., Noda,H., Amano,H., Nishino,T., Nishizana,K., 1994b. Study on hypertensive and
antihyperlipidemic effect of marine algae. Fischeries Science 60, 83-88.
Rensing,S.A., Lang,D., Zimmer,A.D., Terry,A., Salamov,A., Shapiro,H., Nishiyama,T.,
Perroud,P.F., Lindquist,E.A., Kamisugi,Y., Tanahashi,T., Sakakibara,K., Fujita,T., Oishi,K.,
Shin,I., Kuroki,Y., Toyoda,A., Suzuki,Y., Hashimoto,S., Yamaguchi,K., Sugano,S.,
Kohara,Y., Fujiyama,A., Anterola,A., Aoki,S., Ashton,N., Barbazuk,W.B., Barker,E.,
Bennetzen,J.L., Blankenship,R., Cho,S.H., Dutcher,S.K., Estelle,M., Fawcett,J.A.,
Gundlach,H., Hanada,K., Heyl,A., Hicks,K.A., Hughes,J., Lohr,M., Mayer,K.,
Melkozernov,A., Murata,T., Nelson,D.R., Pils,B., Prigge,M., Reiss,B., Renner,T.,
Rombauts,S., Rushton,P.J., Sanderfoot,A., Schween,G., Shiu,S.H., Stueber,K.,
Theodoulou,F.L., Tu,H., Van de Peer,Y., Verrier,P.J., Waters,E., Wood,A., Yang,L.X.,
Cove,D., Cuming,A.C., Hasebe,M., Lucas,S., Mishler,B.D., Reski,R., Grigoriev,I.V.,
Quatrano,R.S., Boore,J.L., 2008. The Physcomitrella genome reveals evolutionary insights
into the conquest of land by plants. Science 319(5859), 64-69.
98
Rioux,L.E., Turgeon,S.L., Beaulieu,M., 2007. Characterization of polysaccharides extracted from
brown seaweeds. Carbohydrate Polymers 69(3), 530-537.
Roberts,M.A., Quemener,B., 1999. Measurement of carrageenans in food: challanges, progress, and
trends in analysis. Trends Food Sci. Technol. 10, 169-181.
Robledo,D., Freile-Pelegrín,Y., 1997. Chemical and mineral composition of six potentially edible
seaweed species of Yucatan. Botanica Marina 40(4), 301-306.
Rodrigueza,M.R.C., Montaño,M.N.E., 2007a. Bioremediation potential of three carrageenophytes
cultivated in tanks with seawater from fish farms. J. Appl. Phycol. 19(6), 755-762.
Rodrigueza,M.R.C., Montaño,M.N.E., 2007b. Bioremediation potential of three carrageenophytes
cultivated in tanks with seawater from fish farms. J. Appl. Phycol. 19(6), 755-762.
Rohde,S., Wahl,M., 2008. Antifeeding defense in baltic macroalgae: Induction by direct grazing
versus waterborne cues. Journal of Phycology 44(1), 85-90.
Ronnberg,O., Adjers,K., Ruokolahti,C., Bondestam,M., 1990. Fucus vesiculosus as an indicator of
heavy metal availability in a fish farm recipient in the northern Baltic Sea. Marine Pollution
Bulletin 21(8), 388-392.
Rorrer,G.L., Yoo,H.D., Huang,Y.M., Hayden,C., Gerwick,W.H., 1997a. Production of hydroxy
fatty acids by cell suspension cultures of the marine brown alga Laminaria saccharina.
Phytochemistry 46(5), 871-877.
Rorrer,G.L., Cheney,D.P., 2004d. Bioprocess engineering of cell and tissue cultures for marine
seaweeds. Aquacultural Engineering 32(1), 11-41.
Rorrer,G.L., Cheney,D.P., 2004c. Bioprocess engineering of cell and tissue cultures for marine
seaweeds. Aquacultural Engineering 32(1), 11-41.
Rorrer,G.L., Cheney,D.P., 2004b. Bioprocess engineering of cell and tissue cultures for marine
seaweeds. Aquacultural Engineering 32(1), 11-41.
Rorrer,G.L., Cheney,D.P., 2004a. Bioprocess engineering of cell and tissue cultures for marine
seaweeds. Aquacultural Engineering 32(1), 11-41.
Rorrer,G.L., Yoo,H.D., Huang,Y.M., Hayden,C., Gerwick,W.H., 1997b. Production of hydroxy
fatty acids by cell suspension cultures of the marine brown alga Laminaria saccharina.
Phytochemistry 46(5), 871-877.
Rupérez,P., 2002. Mineral content of edible marine seaweeds. Food Chemistry 79(1), 23-26.
Rupérez,P., Saura-Calixto,F., 2001. Dietary fibre and physicochemical properties of edible Spanish
seaweeds. European Food Research and Technology 212(3), 349-354.
Russell,G., 1988. The seaweed flora of a young semi-enclosed sea - the Baltic - salinity as a
possible agent of flora divergence. Helgolander Meeresuntersuchungen 42(2), 243-250.
99
Sæter,E.A., Jensen,A., 1957. Forsøk med tangmel som tilskuddsfôr til sau (Experiments with
seaweed meal as supplement to rations for sheep-summary in English). Rep 17, 1-30,
Akademisk Trykningssentral.
Sahoo,D., Tang,X., Yarish,C., 2002. Porphyra – the economic seaweed as a new experimental
system. Current Science 83(11), 1313-1316.
Sahoo,D., Yarish,C., 2005. Mariculture of seaweeds. In: Anderson,R.A. (Ed.), Algal culturing
techniques. Phycological Society of America, pp. 219-237.
Sanchez-Machado,D.I., Lopez-Cervantes,J., Lopez-Hernandez,J., Paseiro-Losada,P., 2004a. Fatty
acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chemistry
85(3), 439-444.
Sanchez-Machado,D.I., Lopez-Hernandez,J., Paseiro-Losada,P., Lopez-Cervantes,J., 2004b. An
HPLC method for the quantification of sterols in edible seaweeds. Biomedical
Chromatography 18(3), 183-190.
Sandau,E., Sandau,P., Pulz,O., Zimmermann,M., 1996. Heavy metal sorption by marine algae and
algae by-products. Acta Biotechnologica 16(2-3), 103-119.
Sangha,J.S., Ravichandran,S., Prithiviraj,K., Critchley,A.T., Prithiviraj,B., 2010a. The sulphated
polysaccharides, -carrageenan and i-carrageenan, differentially alter a model plant's
(Arabidopsis thaliana) resistance to Sclerotinia sclerotiorum.
Sangha,J.S., Singh,R.P., Critchley,A.T., Prithiviraj,B., 2010b. Lambda () carrageenan reduces
tomato chlorotic dwarf viroid (TCDVD) replication and symptom expression.
Sathivel,A., Raghavendran,H.R.B., Srinivasan,P., Devaki,T., 2008. Anti-peroxidative and antihyperlipidemic nature of Ulva lactuca crude polysaccharide on d-Galactosamine induced
hepatitis in rats. Food and Chemical Toxicology 46(10), 3262-3267.
Sato,M., Hosokawa,T., Yamaguchi,T., Nakano,T., Muramoto,K., Kahara,T., Funayama,K.,
Kobayashi,A., Nakano,T., 2002. Angiotensin I-converting enzyme inhibitory peptides
derived from wakame (Undaria pinnatifida) and their antihypertensive effect in
spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry 50(21), 62456252.
Satoh,K., Nakagawa,H., Kasahara,S., 1987. Effect of Ulva meal supplementation on disease
resistance of Red-sea bream. Nippon Suisan Gakkaishi 53(7), 1115-1120.
Schaeffer,D.J., Krylov,V.S., 2000. Anti-HIV Activity of Extracts and Compounds from Algae and
Cyanobacteria. Ecotoxicology and Environmental Safety 45(3), 208-227.
Shacklock,P.F., Doyle,R.W., 1983. Control of epiphytes in seaweed cultures using grazers.
Aquaculture 31(2-4), 141-151.
Shanmugam,M., Mody,K.H., 2000. Heparinoid-active sulphated polysaccharides from marine algae
as potential blood anticoagulant agents. Current Science 79(12), 1672-1683.
100
Shinagawa,A., Shiomi,K., Yamanaka,H., Kicuchi,T., 1983. Selective determination of inorganic
arsenic (III), (V) and organic arsenic in marine organisms. Bulletin of the Japanese Society
of Scientific Fisheries 49(1), 75-78.
Sieburth,J.M., Conover,J.T., 1965. Sargassum tannin, an antibiotic which retards fouling. Nature
208(5005), 52-53.
Simpson,F.J., Shacklock,P., Robson,D., Neish,A.C., 1977. Factors affecting cultivation of
Chondrus crispus (Florideophyceae). Proceedings of International Seaweed Symposium 9,
509-513.
Simpson,F.J., Shacklock,P.F., 1979. The cultivation of Chondrus crispus. Effect of temperature on
growth and carrageenan production. Bot. Mar. 22, 295-298.
Siriwardhana,N., Lee,K.W., Kim,S.H., Ha,J.H., Park,G.T., Jeon,Y.J., 2004. Lipid peroxidation
inhibitory effects of Hizikia fusiformis methanolic extract on fish oil and linoleic acid. Food
Science and Technology International 10(2), 65-72.
Siriwardhana,N., Lee,K.W., Kim,S.H., Ha,J.W., Jeon,Y.J., 2003. Antioxidant activity of Hizikia
fusiformis on reactive oxygen species scavenging and lipid peroxidation inhibition. Food
Science and Technology International 9(5), 339-346.
Skoler-Karpoff,S., Ramjee,G., Ahmed,K., Altini,L., Plagianos,M.G., Friedland,B., Govender,S.,
Kock,A.D., Cassim,N., Palanee,T., Dozier,G., Maguire,R., Lahteenmaki,P., 2008. Efficacy
of Carraguard for prevention of HIV infection in women in South Africa: a randomised,
double-blind, placebo-controlled trial. The Lancet 372(9654), 1977-1987.
Smit,A.J., 2004. Medicinal and pharmaceutical uses of seaweed natural products: A review. Journal
of Applied Phycology 16(4), 245-262.
Smith,D.G., Young,E.G., 1953. On the nitrogenous constituents of Fucus vesiculosus. J. Biol.
Chem. 205, 849-858.
Soler-Vila,A., Coughlan,S., Guiry,M.D., Kraan,S., 2009. The red alga Porphyra dioica as a fishfeed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency
and carcass composition. Journal of Applied Phycology 21(5), 617-624.
Sørensen,H.O., 2009. Marine phospholipids. pp. 14-15.
Stahl,W., Ale-Agha,N., Polidori,M.C., 2002. Non-antioxidant properties of carotenoids. Biological
Chemistry 383(3-4), 553-558.
Stahl,W., Sies,H., 2005. Bioactivity and protective effects of natural carotenoids. Biochimica et
Biophysica Acta-Molecular Basis of Disease 1740(2), 101-107.
Steen,H., Rueness,J., 2004. Comparison of survival and growth in germlings of six fucoid species
(Fucales, Phaeophyceae) at two different temperature and nutrient levels. Sarsia 89(3), 175183.
101
Stengel,D.B., Dring,M.J., 1997. Morphology and in situ growth rates of plants of Ascophyllum
nodosum (Phaeophyta) from different shore levels and responses of plants to vertical
transplantation. European Journal of Phycology 32(02), 193-202.
Stephenson,W.M., 1966. The effect of hydrolysed seaweed on certain plant pests and diseases.
International Seaweed Symposium. pp. 405-415.
Stirk,W.A., Van Staden,J., 1996. Comparison of cytokinin- and auxin-like activity in some
commercially used seaweed extracts. Journal of Applied Phycology 8(6), 503-508.
Suetsuna,K., Maekawa,K., Chen,J.R., 2004. Antihypertensive effects of Undaria pinnatifida
(wakame) peptide on blood pressure in spontaneously hypertensive rats. Journal of
Nutritional Biochemistry 15(5), 267-272.
Sugawara,T., Baskaran,V., Tsuzuki,W., Nagao,A., 2002. Brown algae fucoxanthin is hydrolyzed to
fucoxanthinol during absorption by Caco-2 human intestinal cells and mice. J. Nutr. 132(5),
946-951.
Tarakhovskaya,E.R., Maslov,Y.I., Shishova,M.F., 2007. Phytohormones in algae. Russian Journal
of Plant Physiology 54(2), 163-170.
Targett,N.M., Arnold,T.M., 1998. Minireview: Predicting the effects of brown algal phlorotannins
on marine herbivores in tropical and temperate oceans. Journal of Phycology 34, 195-205.
Tasende,M.G., 2000. Fatty acid and sterol composition of gametophytes and sporophytes of
Chondrus crispus (Gigartinaceae, Rhodophyta). Scientia Marina 64(4), 421-426.
Tititudorancea, 2009. Tititudorancea.
http://www.tititudorancea.com/z/nutrition_facts_undaria_spp_seaweed_wakame_raw.htm.
Troell,M., Halling,C., Nilsson,A., Buschmann,A.H., Kautsky,N., Kautsky,L., 1997. Integrated
marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for
reduced environmental impact and increased economic output. Aquaculture 156(1-2), 45-61.
Tseng,C.K., 2001. Algal biotechnology industries and research activities in China. Journal of
Applied Phycology 13(4), 375-380.
Urbano,M.G., 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
Chemistry 76(3), 281-286.
Vadas,S., Wright,W.A., Beal,B.F., 2004. Biomass and productivity of intertidal rockweeds
(Ascophyllum nodosum LeJolis) in Cobscook Bay. Northeastern Naturalist 11(sp2), 123142.
Valente,L.M.P., Gouveia,A., Rema,P., Matos,J., Gomes,E.F., Pinto,I.S., 2006. Evaluation of three
seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary
ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252(1), 8591.
102
van Netten,C., Hoption Cann,S.A., Morley,D.R., van Netten,J.P., 2000. Elemental and radioactive
analysis of commercially available seaweed. The Science of The Total Environment 255(13), 169-175.
Ventura,M.R., Castañón,J.I.R., 1998. The nutritive value of seaweed (Ulva lactuca) for goats. Small
Ruminant Research 29(3), 325-327.
Verslues,P.E., Agarwal,M., Katiyar-Agarwal,S., Zhu,J.H., Zhu,J.K., 2006. Methods and concepts in
quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water
status. Plant Journal 45(4), 523-539.
Vlieghe,P., Clerc,T., Pannecouque,C., Witvrouw,M., De Clercq,E., Salles,J.P., Kraus,J.L., 2002.
Synthesis of new covalently bound kappa-carrageenan-AZT conjugates with improved antiHIV activities. Journal of Medicinal Chemistry 45(6), 1275-1283.
Voet,D., Voet,J., Pratt,C.W., 1999. Fundamentals of biochemistry. John Wiley & Sons Inc, New
York.
von Elbe,J.H., Schwartz,S.J., 1996. Colorants. Food Chemistry. Marcel Dekker, Inc, New York, pp.
651-722.
Wahbeh,M.I., 1997. Amino acid and fatty acid profiles of four species of macroalgae from Aqaba
and their suitability for use in fish diets. Aquaculture 159(1-2), 101-109.
Weinberger,F., 2007. Pathogen-induced defense and innate immunity in macroalgae. Biol Bull
213(3), 290-302.
Wen,X., Peng,C.L., Zhou,H.C., Lin,Z.F., Lin,G.Z., Chen,S.W., Li,P., 2006. Nutritional composition
and assessment of Gracilaria lemaneiformis Bory. Journal of Integrative Plant Biology
48(9), 1047-1053.
Wernberg-Møller,T., Stæhr,P.A., Thomsen,M.S., 1997. Invasion and productivity of Sargassum
muticum (Yendo) Fensholt in Limfjorden, Denmark. Poster presented at the 32nd European
Marine Biology Symposium in Lysekil, Sweden, August 16.-22.
Whittaker,M.H., Frankos,V.H., Wolterbeek,A.M.P., Waalkens-Berendsen,D.H., 2000. Effects of
dietary phytosterols on cholesterol metabolism and atherosclerosis: Clinical and
experimental evidence. American Journal of Medicine 109(7), 600-601.
Wikipedia, 2010. Wikipedia. www.wikipedia.com.
Williams,D.C., Brain,K.R., Blunden,G., Wildgoose,P.B., Jewers,K., 1981. Plant growth regulatory
substances in commercial seaweed extracts. International Seaweed Symposium. pp. 760763.
Wong,K., Cheung,P.C., 2001a. Influence of drying treatment on three Sargassum species 2. Protein
extractability, in vitro protein digestibility and amino acid profile of protein concentrates.
Journal of Applied Phycology 13(1), 51-58.
103
Wong,K., Cheung,P.C., 2001b. Influence of drying treatment on three Sargassum species. 1.
Proximate composition, amino acid profile and some physico-chemical properties. Journal
of Applied Phycology 13(1), 43-50.
Wong,K.H., Cheung,P.C.K., 2001c. Nutritional evaluation of some subtropical red and green
seaweeds Part II. In vitro protein digestibility and amino acid profiles of protein
concentrates. Food Chemistry 72(1), 11-17.
Wong,K.H., Cheung,P.C.K., 2000. Nutritional evaluation of some subtropical red and green
seaweeds - Part I - proximate composition, amino acid profiles and some physico-chemical
properties. Food Chemistry 71(4), 475-482.
Yamamoto,I., Takahashi,M., Tamura,E., Maruyama,H., Mori,H., 1984. Antitumor-activity of edible
marine-algae - effect of crude fucoidan fractions prepared from edible brown seaweeds
against L-1210 leukemia. Hydrobiologia 116(SEP), 145-148.
Yan,X.J., Zheng,L., Chen,H.M., Lin,W., Zhang,W.W., 2004. Enriched accumulation and
biotransformation of selenium in the edible seaweed Laminaria japonica. Journal of
Agricultural and Food Chemistry 52(21), 6460-6464.
Yasui,A., Tsutsumi,C., Toda,S., 1978. Selective determination of inorganic arsenic (III), (V) and
organic arsenic in biological-materials by solvent extraction atomic absorption
Spectrophotometry. Agricultural and Biological Chemistry 42(11), 2139-2145.
Ye,H., Wang,K., Zhou,C., Liu,J., Zeng,X., 2008. Purification, antitumor and antioxidant activities
in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chemistry
111(2), 428-432.
Yone,Y., Furuichi,M., Urano,K., 1986. Effects of Wakame Undaria pinnatifida and Ascophyllum
nodosum on absorption of dietary nutrients, and blood sugar and plasma free amino-N levels
of red sea bream. Bulletin of the Japanese Society of Scientific Fisheries 52(10), 1817-1819.
Young,E.G., Smith,D.G., 1958. Amino acids, peptides, and proteins of Irish Moss, Chondrus
crispus. The Journal of Biological Chemistry 233(2), 406-410.
Yuan,Y.V., Carrington,M.F., Walsh,N.A., 2005. Extracts from dulse (Palmaria palmata) are
effective antioxidants and inhibitors of cell proliferation in vitro. Food and Chemical
Toxicology 43(7), 1073-1081.
Yuan,Y.V., Walsh,N.A., 2006. Antioxidant and antiproliferative activities of extracts from a variety
of edible seaweeds. Food and Chemical Toxicology 44(7), 1144-1150.
Zertuche-González,J.A., García-Lepe,G., Pacheco-Ruiz,I., Chee,A., Gendrop,V., Guzmán,J.M.,
2001. Open water Chondrus crispus Stackhouse cultivation. J. Appl. Phycol. 13, 249-253.
Zhang,J.Z., Tiller,C., Shen,J.K., Wang,C., Girouard,G.S., Dennis,D., Barrow,C.J., Miao,M.S.,
Ewart,H.S., 2007. Antidiabetic properties of polysaccharide- and polyphenolic-enriched
fractions from the brown seaweed Ascophyllum nodosum. Canadian Journal of Physiology
and Pharmacology 85(11), 1116-1123.
104
Zhao,X., Xue,C.H., Li,B.F., 2008. Study of antioxidant activities of sulfated polysaccharides from
Laminaria japonica. Journal of Applied Phycology 20(4), 431-436.
Zhi,C., Rorrer,G.L., 1996. Photolithotrophic cultivation of Laminaria saccharina gametophyte cells
in a bubble-column bioreactor. Enzyme and Microbial Technology 18(4), 291-299.
Zhou,G., Sheng,W., Yao,W., Wang,C., 2006a. Effect of low molecular [lambda]-carrageenan from
Chondrus ocellatus on antitumor H-22 activity of 5-Fu. Pharmacological Research 53(2),
129-134.
Zhou,Y., Yang,H.S., Hu,H.Y., Liu,Y., Mao,Y.Z., Zhou,H., Xu,X.L., Zhang,F.S., 2006b.
Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta)
integrated into fed fish culture in coastal waters of north China. Aquaculture 252(2-4), 264276.
Zhuang,C., Itoh,H., Mizuno,T., Ito,H., 1995. Antitumor active fucoidan from the brown seaweed,
Umitoranoo (Sargassum-thunbergii). Bioscience Biotechnology and Biochemistry 59(4),
563-567.
Zou,Y., Qian,Z.J., Li,Y., Kim,M.M., Lee,S.H., Kim,S.K., 2008. Antioxidant effects of
phlorotannins isolated from Ishige okamurae in free radical-mediated oxidative systems.
Journal of Biotechnology 136(Supplement 1), S579-S580.
Zubia,M., Payri,C., Deslandes,E., 2008. Alginate, mannitol, phenolic compounds and biological
activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria
ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). Journal of Applied
Phycology 20(6), 1033-1043.
105