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Seaweed extract stimuli in plant science and agriculture
James S. Craigie
Received: 26 March 2010 /Revised and accepted: 5 July 2010 /Published online: 29 July 2010
# Springer Science+Business Media B.V. 2010
Abstract Both micro- and macroalgae have long been used
to augment plant productivity and food production in various
regions of the world through their beneficial effects when
applied to soils. Interactions of algae with the soil community
undoubtedly are complex and benefits are dependent on the
crop and the local environmental conditions. This has resulted
in much speculation as to mechanisms involved as well as the
validity of the results reported. It is now 60 years since the first
commercial seaweed extract was manufactured for agricul-
tural use. These aqueous extracts allowed for the first time the
direct application of soluble seaweed constituents to specific
plant organs such as leaves and roots. The earlier concept that
benefits of seaweeds and their extracts were due mainly to
their manurial value or to their micronutrient suites is no
longer tenable. Seaweeds likewise have been used for
millennia as fodder supplements to improve animal nutrition
and productivity. Recent research is focusing on their mode of
action, specific health benefits, and the mechanisms of action
in animals. Improved analytical techniques and instrumenta-
tion coupled with the use of molecular genetic tools are
establishing that seaweed extracts can modify plant and
animal responses at a fundamental level. It therefore seems
appropriate to review key developments over the years and to
remark on novel findings. A new and exciting vista has
opened for seaweed extracts in both plant and animal
applications.
Keywords Algae . Growth hormones .
Pathogen resistance . Animal health . Polymers
Introduction and background
This, the “XX International Seaweed Symposium”, covers
some 58 years of usually triennial meetings. For the benefit
of new colleagues, I should like to point to a “Conference
on Utilization of Seaweeds” convened by the National
Research Council of Canada (NRCC) in September 1948.
That conference, held in Halifax, Nova Scotia, attracted
scientists and industrialists from Canada and the USA with
an interest in seaweed developments. At that time, some 18
countries were developing their seaweed resources for
chemicals, medicinals, animal fodder, and fertilizers. Dr.
W.H. (Bill) Cook (Division of Applied Biology, NRCC,
Ottawa) and others proposed that the Institute of Seaweed
Research (Inveresk, Scotland) should arrange a meeting to
consider questions important to the industry such as
seaweed supply, utilization and conservation. The outcome
was the “First International Seaweed Symposium” held in
Edinburgh, July 14–17, 1952. The meeting was attended by
almost 200 members from 21 countries who presented 53
papers. The successful formula they developed continues to
the present under the aegis of the International Seaweed
Association.
A major turning point for seaweed research can be traced
to World War II with the creation of the Scottish Seaweed
Association Limited in June of 1944 under the directorship
of Dr. F.N. Woodward. The Association goals were to
conduct and foster research on seaweeds in Botanical–
Ecological, Chemical, Chemical Engineering, and Agricul-
tural areas of potential interest to industry. The Institute was
wound up on March 31, 1969 due to the reallocation of
government research funding (Scottish Seaweed Associa-
tion, Annual Reports 1945–1968). The excitement and
interest in seaweed research elsewhere also was waning by
the 1970s as funding was shifted to programs deemed of
J. S. Craigie (*)
Acadian Seaplants Limited,
30 Brown Avenue,
Dartmouth, Nova Scotia B3B 1X8, Canada
e-mail: james.craigie@nrc-cnrc.gc.ca
J Appl Phycol (2011) 23:371–393
DOI 10.1007/s10811-010-9560-4
greater national interest. The long established and excellent
Norwegian Institute for Seaweed Research in Trondheim
changed research directions and, by 1995, seaweed research
programs at the National Research Council laboratory in
Halifax were terminated (Ragan 1996). It is a pleasure to
report that research on algae, including some on macro-
algae, has been reinitiated recently at the Institute for
Marine Biosciences, NRCC, Halifax. The foci are on
biofuels from phytoplankton, algal constituents beneficial
to human health, and collaboration with industry to
commercialize the research. Presentations at the recent
Seventh Asia-Pacific Conference on Algal Biotechnology
(2009) show clearly the breadth and vitality of research
now being pursued in Asia and India. The trend is to
research both phytoplankton and seaweeds for biofuels,
bioremediation of soils, water and sewage, and particularly
to investigate potential biomedical applications of constit-
uents such as polyphenols and polysaccharides.
Photosynthetic algae must be considered the true
survivors amongst the Plantae as they have survived
dramatic changes in climatic conditions from a hot, CO2-
and methane-rich nitrogen atmosphere to presently occupy
virtually all niches on Earth from the tropics to the cold,
dry, frozen deserts of Antarctica. The key requirement is
that there be liquid water, even if only intermittently.
Gradually, they produced the oxygen necessary to support
animal life and, perhaps more importantly, participated in
the evolution of macroalgae and the eukaryotic plants upon
which we depend for our survival (Rousé 2006).
The world’s oceans contain a ubiquitous, tiny, unicellular
green alga, Ostreococcus tauri, isolated in 1994 from the
Thau Lagoon in the Mediterranean region of southern
France. Being of bacterial dimensions (∼1 μm in size), it is
considered to be the world’s smallest free-living eukaryotic
cell possessing a single chloroplast, one nucleus, one
mitochondrion, and one Golgi body. Its fully sequenced
nuclear genome is ∼12 Mb with 20 chromosomes ranging
from 120 to 1,500 kb with some 7,885 genes coding for
proteins (Derelle et al. 2006). Phylogenetic analysis
establishes O. tauri as an early chlorophyte (Prasinophy-
ceae) originating ∼1 B years ago. Its gene structure and
organization are being compared with some green algae and
mosses as well as Arabidopsis thaliana and rice, Oryza
sativa, to better understand the evolution of plants and their
signaling systems (Pigenau et al. 2009; Pils and Heyl 2009;
Rensing et al. 2008; Rensink and Buell 2004).
Multicellular algae such as seaweeds are evolutionarily
more recent than O. tauri and have developed unique
strategies to permit their survival. Researching their
biology, chemistry, and molecular genetics can be expected
to generate novel findings, some of which may result in
more innovative ways to utilize this great resource for the
benefit of society.
Utilization of seaweeds by humans
It was reported recently that seaweeds formed an important
resource for humans in pre-historic times, ∼14,000 BP
(Dillehay et al. 2008). Archeological excavations at Monte
Verde (near Puerto Montt, Chile) have revealed nine species
of algae from marine, estuarine and terrestrial/littoral habitats
(Durvillaea antarctica, Macrocystis pyrifera, Sargassum sp.,
Gigartina sp., Gracilaria sp., Porphyra sp., P. columbina,
Sarcothalia crispata (probable name), and Trentepholia sp.).
Their association with hearths, stone tools, and presence in
masticated cuds suggest that they were used in the diet,
probably for their medicinal value. The same species
continue to be used for medicinal purposes by the local
indigenous populations of today. S. crispata, previously
Iridaea ciliata, is a major Chilean carrageenophyte.
The history of seaweed utilization and the development
of relevant commercial utilization processes by industry
have been reviewed (Chapman and Chapman 1980; Lembi
and Waaland 1988; Newton 1951; Tressler and Lemon
1951). Briefly, an important schism between the Oriental
approach to seaweed utilization and the European or
Western views is evident as the latter seem to have been
influencedby Roman ideas that seaweeds were trash forms
of marine life having little value. A notable exception was
the use of dulse or “sol” by the Norse in Iceland which
dates at least to the year 961 (Hallsson 1964).
In contrast, coastal Asian populations have long used
algae (seaweed) both as foods and medicines. The use of
agar weeds is described in a book by Chi Han about A.D.
300 (Newton 1951), and the food value of Porphyra sp. in
the Chinese diet was described as early as 533–544 (Tseng
1981). In her discussion of European usage, Newton (1951)
pointed out that the monks of St. Columba harvested dulse
1,400 years ago, and that the gathering of it for the poor is
recorded in a Gaelic poem attributed to St. Columba.
Camden’s Brittanica, written in 1607, is cited in Newton
(1951) as describing its harvest and the manufacture of a
food called Lhavan or Lhawvan (black butter). Porphyra
laciniata or laver still appears in the markets of South
Wales, and dulse is sold in regions of Europe and North
America. Utilization of seaweed as a human food in the
West remains both small-scale and local compared to that in
the Orient.
The industrial uses of seaweeds (reviewed by Jensen
1979) have followed a “boom and bust” cycle in the west
beginning ca. 1690 with soda ash production. Other major
uses of brown algae in the iodine and potash industries
largely disappeared following World War I. Notable is the
sometimes prodigious quantities ranging from 200,000 to 4
million tonnes of wet seaweed that were harvested annually
to sustain these industries. The current alginate and
carrageenan industries began only in 1930s and 1940s.
372 J Appl Phycol (2011) 23:371–393
Indeed, in reference to the European situation, Booth
(1974) stated that “In 1950, seaweed was a curiosity. Today
almost a million tons are collected annually”. Thus, large-
scale use of algae in the west is a relatively recent
phenomenon mostly related to industrial components
extracted from them. Interest in agricultural uses of
seaweeds is increasing rapidly as judged by the number of
related publications appearing since 1950 (Fig. 1). The
number of species involved is small, but the volumes of
biomass can be sizeable.
Seaweeds in agriculture and development of liquid seaweed
extracts
The comprehensive review by Chopin and Sawhney (2009)
values the global seaweed industry at just under US$6
billion in 2004 (Soto 2009). Three major subcomponents
were identified as sea vegetables, phycocolloids, and
phycosupplements (Table 1). However, Bixler and Porse
(2010) place the current world phycocolloid value at US
$1.02 B. Products relating to agriculture comprised $50 M
and were represented as soil additives, agrochemicals
(fertilizers and biostimulants) and animal feeds (supple-
ments, ingredients; Table 1). The numbers indicate a
relatively slow rate of growth in the agriculture component
as Jensen (1979) estimated the world’s seaweed meal
production at approximately US$10 million (∼30,000
tonnes/annum, mostly from Ascophyllum nodosum). He
concluded that about half was used in fodder with the
balance going to the alginate industry. The agricultural uses
of seaweeds thus comprise less than 1% of the overall value
of the current seaweed industry.
A key prerequisite for creating an industry continues to
be the availability of a steady source of raw material, in our
case seaweeds. The resource must be renewable and
sustainable and so requires enlightened management of
the seaweed harvest. Conditions found in the coastal
temperate and sub-Arctic zones of the oceans foster the
development of an extensive biomass of seaweeds consist-
ing mainly of laminarians and fucoids, and particularly of
A. nodosum in the North Atlantic. The development of a
soluble seaweed extract based on this species is an
interesting study of several factors that come into play
when a new industry is created.
In this case, a major advance in the utilization of
seaweeds in agriculture resulted from research conducted
during World War II on new sources of fiber. One of the
main sources of fiber at that time was jute from northeast-
ern India, and, by 1944, the war in Asia had threatened to
interdict this source. A significant amount of fiber was
required for netting to camouflage assemblages of aircraft,
factories, and other potential targets important to the war
effort. The British government focused research efforts to
develop local sources of fiber, and a biochemist, Dr.
0
500
1000
1500
2000
2500
1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000
Decades
N
um
be
r o
f p
ub
lic
at
io
ns
 b
y 
de
ca
de
Fig. 1 Number of publications
related to seaweed use by
decade for 1900–2000.
CAPLUS and BIOSIS data
bases were searched. Courtesy
of B. Kennedy, CISTI, NRCC
Table 1 Value of the world’s seaweed industry in 2004
Products Value (US$, millions)
Sea vegetables 5,290
Phycocolloids 650a
Phycosupplements 53
(Soil additives) (30)
(Agrochemicals) (10)
(Animal feeds) (10)b
(Other) (3)
Total 5,993
Adapted from Chopin and Sawhney (2009)
a Bixler and Porse (2010) give US$1.02 billion for phycocolloids.
b Seaweed meal, used principally as a vitamin and mineral supplement, is
produced mainly from the kelps Ascophyllum nodosum, Fucus spp.,
Laminaria spp., and Macrocystis spp.
J Appl Phycol (2011) 23:371–393 373
Reginald F. Milton, was tasked with the challenge. Large
tonnages of kelps were known to be available in Scotland,
and Stanford already had discovered alginate in the 1880s
as a major component of these seaweeds. Factories were
built in Scotland to extract alginate and produce seaweed
rayon for the netting. Functional nets were produced as
tensile strength was not important. Unfortunately, the nets
failed as the calcium and beryllium alginate fibers biode-
graded and dissolved rather rapidly in the prevailing wet
climate. The project was terminated.
Milton then moved to Birmingham where he purchased
property with a large garden and glasshouse, and set up a
small laboratory to investigate methods for liquefying kelp
for use as a fertilizer. By 1947, he had succeeded in making
a liquid product. His method, based on a hot pressurized
alkaline process, was patented and formed the basis for the
Maxicrop process (Milton 1952). During that period,
Milton became acquainted with W. A. (Tony) Stephenson,
an accountant, who was making a career change by moving
to the countryside to indulge his gardening hobby. Thus,
each could test the various iterations of the early liquefied
seaweed products in his own plot. The chemistry worked
for both men and, one night in 1949 over a bottle of brandy,
the name Maxicrop was born (Stephenson 1974).
The start-up presented the expected challenges of
financial difficulties, sales volumes and technical problems.
The last included sticky clumps of sludge in the liquid as
well as fermenting and exploding vessels (Stephenson
1974). Arrangements with a large grain company possess-
ing the requisite processing skills allowed Maxicrop to
expand. The production in 1953 was approximately
45,460 L (10,000 gallons) rising 20-fold to about
909,200 L (200,000 gallons) by 1964. The advent of leaf
spraying (foliar application) to supply plant nutrients was
the likely driver for this increased production.
Stephenson soon realized that an additional product line
was important to his business so he undertook to market
seaweed meal for stockfeed and for manure (name Neptune’s
Bounty). By 1952, he had formed the company Maxicrop
Limited to sell both the liquid seaweed extract (previously
sold by Plant Productivity Ltd.) and the meal products. The
combined businesses permitted him to support a year-round
sales staff to further develop the market.
General nature of seaweed manure and extracts used
in agriculture
Seaweeds have been used since antiquity either directly or
in composted form as a soil amendment to improve the
productivity of crops in coastal regions (Chapman and
Chapman 1980; Lembi and Waaland 1988; Metting et al.
1990; Newton 1951). Accordingto Newton (1951), the
earliest reference to seaweed manure is in the second half of
the first century when the Roman Columella recommended
that cabbages be transplanted at the sixth leaf stage and
their roots be mulched and manured with seaweed. She also
references a recommendation of Palladius, in the fourth
century, to apply March marine algae to the roots of
pomegranate and citron trees. Pre-Roman Britons also
added seaweed to soil as manure. Depending on regional
practices, seaweeds were mixed directly with sand or soil,
or composted with straw, peat, or other organic wastes for
later use. A common practice was to heap seaweed in fields
and to turn it periodically in a process called “weathering”
which aerates it and reduces the production of toxic
sulfhydryl compounds (Milton 1964).
A method, published more than 150 years ago, for
compressing seaweeds or marine plants into a compact,
transportable form indicates the value placed on seaweed
manure and the need to transport the product over long
distances (Gardissal 1857). An alkaline seaweed extract was
produced almost a century ago in recognition of the fact that
it was uneconomical to transport seaweeds more than a few
kilometers from the coastline for use as manure (Penkala
1912). The first practical method for liquefying seaweed for
agricultural use was developed by 1949 (Milton 1952).
It is interesting at this point to summarize the informa-
tion available at that time (Table 2). According to Milton
(1964), an immediate inhibition of plant growth and
nutrition occurs when seaweeds are added to soils even if
they are finely ground. The inhibitory effects on seed
germination and growth are overcome after ∼15 weeks.
During this latent period, the ionic soil nitrogens decrease
but the total N tends to increase as soil microorganisms
proliferate selectively. Liquefying the seaweed (species can
be varied, but are principally laminarians and those with
fucoidin and other sulfate esters) provides an immediate
plant response similar to the application of composted
seaweed. The liquid product contains partially hydrolyzed
fucoidan which maintains Cu, Co, Mn, and Fe in soluble
form due to the sulfate esters; the N is reduced and P is
partially precipitated by Mg. The rich, humin-like pig-
mented liquid (almost black in color) can be applied to soils
in diluted form (ca. 1/500). Milton further recognized that
the quantitative aspect of plant nutrients cannot be very
marked when extracts are used at such dilutions. He
suggested that adding strongly polar degraded fucoidan,
algin, etc., to soils improved crumb structure and aeration,
thus stimulating microorganisms and root systems which
improved plant growth.
The current commercial extracts are manufactured
mainly from the brown seaweeds A. nodosum, Laminaria
spp., Ecklonia maxima, Sargassum spp., and Durvillaea
spp., although other species such as Fucus serratus,
Enteromorpha intestinalis, Ulva lactuca, and Kappaphycus
alvarezii have been used (Gandhiyappan and Perumal 2001;
374 J Appl Phycol (2011) 23:371–393
Nabti et al. 2009; Rathore et al. 2009; Stirk and van Staden
1996, 1997). The extracts in today’s marketplace are aqueous
preparations ranging in color from almost colorless to an
intense dark brownish-black. Likewise, odors, viscosities,
solids, and particulate matter contents vary widely. The
methods of manufacture are rarely published, being held as
proprietary information. In general, extracts are made by
processes using water, alkalis or acids, or by physically
disrupting the seaweed by low temperature milling to give a
“micronized” suspension of fine particles (Hervé and
Rouillier 1977). Micronized seaweed suspensions are green-
ish to greenish-brown in color and are mildly acidic.
Alternatively, the algal cells are ruptured using a high-
pressure apparatus and the soluble cytosolic components
recovered in the filtered liquid (Hervé and Percehais 1983;
Stirk and van Staden 2006). Physical disruption avoids the
use of organic solvents, acids or alkalis to make extracts with
properties different from alkaline extracts.
The most widely used process involves heating the seaweed
with alkaline sodium or potassium solutions. The reaction
temperature may be elevated by pressurizing the vessel as in
the high temperature process developed for Maxicrop (Milton
1952) and similar processes developed later by Algea and
others. Alternatively, the seaweed may be liquified at ambient
pressure as in the case of the Acadian Seaplants extracts. All
such extracts are intensely colored due to their high content of
humic-like polyphenols or phlorotannins. The final product
may either be dried or prepared in various liquid formats
generally in the pH 7–10 range. Liquids for special
applications can be produced at an acid pH (∼4).
Depending on the application, extracts frequently are
fortified with common plant fertilizers and micronutrients
to take advantage of the natural chelating properties of the
seaweed extracts which prevent trace metal ions from
precipitating (Milton 1962). Such fortified extracts usually
are tailor-made by formulators for specific crops.
Unique features of A. nodosum
Ascophyllum nodosum is recognized as the dominant
intertidal seaweed of the North Atlantic coastline where
water temperatures do not exceed ∼27°C (Keser et al.
2005). For example, the current standing crop in Nova
Scotia is 71.3 wet tonnes/ha over some 4,960 ha of suitable
substratum (Ugarte et al. 2010). The large perennial frond is
capable of surviving more than 20 years, while its holdfast
may survive for a century or longer (Xu et al. 2008). A
significant feature for industry is the ability of A. nodosum
fronds to regenerate repeatedly provided that harvesting is
carefully managed to ensure the viability of this renewable
resource (see Ugarte et al. 2010).
Ascophyllum nodosum, the most studied of the Phaeo-
phyceae, is unique amongst seaweeds and continues to yield
surprises. The association of the alga with Mycophycias
(formerly Mycosphaerella) ascophylli has long been known,
and the possibility of a lichenous relationship with the
ascomycete has been raised (Kohlmeyer and Kohlmeyer
1972). Significant new details of the biology and ultrastruc-
ture of their intricate symbiotic relationship have emerged
over the past 20 years through the investigations of Garbary
and colleagues (Garbary and Gautam 1989). They have
shown that infection of the Ascophyllum zygote markedly
improves sporeling growth, and that all Ascophyllum
collected in nature is infected with M. ascophylli (Garbary
and Deckert 2001). The fungal mycelium surrounding the
algal cells forms a heavy and pervasive network providing
an intimate association of the two entities. There is, however,
no evidence of penetration of the algal protoplasts by the
mycelium (Xu et al. 2008). Indeed, there was no indication
of “resistance” on the part of the alga to the fungal
endophyte. Formation of asci and ascospore production
coincide with receptacle maturation in A. nodosum. The term
proposed for this unusual obligate and mutualistic symbiosis
is a symbiotum (Deckert and Garbary 2005).
A further remarkable and unique feature of Ascophyllum
biology concerns the meristoderm and the mechanism
developed for sloughing and regeneration of the epidermal
layer of cells. This mechanism provides for the shedding of
epibiota which is important for a long-lived perennial
seaweed. Garbary et al. (2009) present evidence that cells
of the meristoderm undergo a unique type of cell division
(cytokinesis) without mitosis. In this process, the distal 30%
of a meristodermal cell is walled off to become an epidermal
cell that is destined for elimination. These new epidermal
Table 2 Properties of liquid seaweed extract versus seaweed meal applied to soils as described in 1961
Liquefied Whole or meal
Plant response is immediate and positive (1:500 dilution) Must be turned or “weathered” to reduce toxic sulfhdryl compounds
Cu, Co, Mn and Fe remain soluble at high pH Immediateinhibition of seed germination and growth
Chelation effect is due to partly hydrolyzed, sulfated polysaccharides Decreases ionic nitrogen, later N increases due to microbial action
Degraded polar compounds algin, fucoidin improve soil crumb structure ∼15 weeks to overcome germination and growth inhibitions
Stimulates microorganisms, root systems, plant growth
After Milton (1964)
J Appl Phycol (2011) 23:371–393 375
cells contain minimal cytoplasm, lack nuclei and functional
chloroplasts, and are shed simultaneously in large sheet-like
masses. It is noteworthy that there is no association of the
mycobiont mycelium with these moribund epidermal cells.
Ascophyllum also hosts an obligate red algal epiphyte,
Vertebrata (formerly Polysiphonia) lanosa, and numerous
opportunistic species including diatoms, several filamen-
tous brown algae and an associated chironomid population
(cited in Xu et al. 2008). The biomass of these biota
however is small compared to that of the host seaweed. It
can be safely said that A. nodosum is a unique and very
special brown seaweed.
Seaweeds in plant agriculture
Seaweeds and to a lesser extent microalgae have been
applied to soils as a manure and as soil conditioning agents
(Chapman and Chapman 1980; Guiry and Blunden 1981;
Hong et al. 2007; Metting et al. 1988, 1990). The observed
benefits to the growth, health and yields of plant crops were
traditionally attributed to the supply of essential nutrients
and to improved soil texture and water holding capacity.
The ability of liquefied seaweed extracts to maintain
enriched trace metal mixtures (Cu, Co, Zn, Mn, Fe, Ni as
well as Mo and B) in a soluble form for application to soils
or for use as foliar sprays was clearly understood (Milton
1962). However, development of liquefied seaweed extracts
and their relatively low application rates (<15 L/ha) led to
an examination of the extracts for components other than
fertilizer nutrients that would promote plant growth.
Accumulation of our current knowledge of seaweed
extracts can be grouped into three main periods, 1950 to the
early 1970s, 1970s to 1990s, and 1990s to the present.
Information acquired in the early period derived from practical
trials and bioassays, with chemical analyses being greatly
hampered by the lack of suitable technology. The middle
period was one in which chromatographic techniques such as
gas chromatography (GC) and high-performance liquid
chromatography (HPLC) improved markedly. These, coupled
with mass spectrometry (MS), were applied to the identifica-
tion of specific components present in seaweeds and related
commercial extracts. Nuclear magnetic resonance (NMR)
spectroscopy became widespread and was applied to the
structural identification of extracted seaweed components.
Bioassay technology, however, remained essentially un-
changed. The current or modern period brought continued
improvements in analytical methods of chromatography,
tandem mass spectrometry with single ion measurement, and
the advent of quantitative NMR spectroscopy. These, coupled
with principal components analysis and methods of metab-
olomics, are now being applied to seaweed extracts and
extract treated plants to detect and compare changes in
metabolites.
Early information on the bioefficacy of seaweed extracts
was derived mainly from observations made in field and
greenhouse trials using Maxicrop, first as a soil additive and
beginning in the early 1960s as a foliar spray. A major
contributor involved in this work was Ernest Booth of the
Institute of Seaweed Research in Scotland. Three additional
research groups later became prominently active examining
seaweeds and their commercial extracts for applications in
agriculture. Beginning in 1959, an independent research
program led by T. L. Senn, Professor of Horticulture, was
established at Clemson University, SC. The results over the
next two decades from this group on the effects ofA. nodosum
and its extracts on fruits, vegetables, and ornamentals have
been summarized (Senn and Kingman 1978). By the late
1960s, G. Blunden, Professor of Pharmacy, began to focus
research on seaweed extracts at Portsmouth Polytechnic, UK.
He and his colleagues continue that research to the present.
A third independent group focusing on the effects of
seaweed extracts on crop plants was established in South
Africa in the early 1980s by Professor J. van Staden, Botany
Department, University of Natal, Pietermaritzburg. These
researchers focused extensively on the effects of a commer-
cial extract, Kelpak, manufactured from E. maxima by a cell
burst process. Work begun in the late 1980s by Bernard
Kloraeg and colleagues at CNRS, Station Biologique de
Roscoff, France, in association with Goëmar S.A., Saint-
Malo, have revealed in seaweed extracts the presence of
elicitors of defense responses in plants (Klarzynski et al.
2000, 2003; Patier et al. 1993).
In addition to Maxicrop, other commercial firms began to
produce seaweed extracts. Algea (now Valagro) began
making an alkaline Ascophyllum extract similar to Maxicrop
in Norway around 1962. A novel extraction process based
on cryo-milled seaweeds was developed in France in the
early 1970s (Hervé and Rouillier 1977) and was commer-
cialized by Goëmar S.A. Acadian Seaplants Limited began
commercial extract production in the early 1990s based
solely on A. nodosum. Table 3 lists a selection of commercial
manufacturers.
Bioassays
A continuing limitation is the availability of convenient,
rapid, and robust bioassays. Currently these are laborious,
require specialized facilities and frequently exhibit wide
variances in the data. For example, simple root initiation
bioassays require a week while a soya bean or tobacco
callus assay for cytokinins requires approximately four
weeks. As discussed by Jameson (1993), the radish
cotyledon bioassay can return extremely high cytokinin
values (up to 4,000 mg L−1 of benzyl adenine equivalents
for Maxicrop) when unfractionated extracts are tested, so
cytokinin values obtained in this way must be considered
376 J Appl Phycol (2011) 23:371–393
unreliable. The same Maxicrop product showed cytokinins
at 1 mg/L in the more specific soybean bioassay. Values an
order of magnitude less (0.115 mg L−1) were reported as the
total for the ten cytokinins detected in Seasol, a commercial
alkaline extract of Durvillaea potatorum, when GC-MS and
deuterium labeled internal reference standards were used in
the analyses (Tay et al. 1985, 1987).
Assays such as the betacynanin pigment formation in
Amaranthus can respond differentially making it an
unsuitable method for determining the cytokinins isopen-
tenyl adenine and isopentenyl adenosine (Lough and
Jameson 1990). Similarly, quantitation by immunoassays
can be imprecise due to cross-reactivity and interference
from other compounds in the samples.
Despite slow response times and variability frequently
encountered in the data, bioassays are essential as they are the
only method for detecting bioactive compounds. Valuable
comparative information can be gained from simple growth
measurements using fast-growing plants as demonstrated by
Challen and Hemmingway (1966). They measured plant
height, and fresh and dry weights of mustard seedlings
(Sinapis alba) to compare the commercial seaweed extract S.
M.3 against a fertilizer mixture and simple aqueous extracts
prepared from specific dried seaweeds (A. nodosum, F.
serratus, F. vesiculosus and Saccharina latissima as Lami-
naria saccharina). The commercial extract significantly
increased the height and fresh weights of the seedlings over
the fertilizer and water controls, however, the improvement
could not be attributed to the N, P, K, or Mg content of the S.
M.3 extract. Differences in dry weights were less clear
between S.M.3 and the fertilizer-treated group. The mustard
performed poorly when treated with simple water extracts of
the seaweeds; inhibition was noted for those from L.
saccharina and F. serratus. Hydrophyllic inhibitors in
Laminaria and Ascophyllum have beenreported (Hussain
and Boney 1973). Interestingly, the water extract of A.
nodosum meal was the least inhibitory of the seaweed
extracts tested by Challen and Hemmingway (1966). As
noted earlier (Blunden 1977), there remains a great need to
develop rapid bioassays for plant growth regulators that are
more compatible for use in bioassay-directed analysis of
seaweed extracts.
A most exciting new biological development is the
application of molecular genetics to investigate the responses
of an intact organism to seaweed extracts. This approach
permits the identification of specific genes or suites of genes
that may be either up- or down-regulated when an organism is
challenged with a seaweed extract or a bioactive subfraction
of it. Two well-studied classical organisms, the flowering
plant, A. thaliana, and the nematode, Caenorhabditis
elegans, are among the valuable biological tools being
newly used with seaweed extracts to investigate biological
responses (Durand et al. 2003; Fan et al. 2010; Rayorath et
al. 2008). The genomes of these organisms have been
mapped and their cell ontogenies described (C. elegans
Sequencing Consortium 1998; Ceron and Swoboda 2008;
The Arabidopsis Genome Initiative 2000; Theologis et al.
2000). Both species are readily mutagenized and a very large
number of transgenic clones are available for research.
Bioassaying with C. elegans combines a high throughput
capacity with the potential for direct application of the results
in vertebrate physiology as demonstrated by the discovery of
a new calcium channel antagonist during drug screening
(Burns et al. 2006; Burns et al. 2010; Kwok et al. 2006).
Larger producers Country Smaller producers Country
Acadian Seaplants Ltd Canada AfriKelp South Africa
Algea Norway Agrocean France
Arramara Teo Ireland Agrosea New Zealand
Atlantic Labs USA Brandon Products Ireland
Beijing Leili P R China Cytozyme USA
Bioatlantis Ireland Dash Egypt
China Ocean University P R China Fairdinkum Australia
Goëmar France Fartum Chile
Kelpak South Africa Gofar P R China
Seasol Australia Natrakelp Australia
Nitrozyme USA
Plantalg France
Sammibol France
Seagold Australia
Setalg France
Thorvin Iceland
West Coast Marine Products Canada
Table 3 Some larger and smaller
producers of commercial seaweed
extracts for agricultural uses
J Appl Phycol (2011) 23:371–393 377
Application of these tools to seaweed extracts will generate
new insights and opportunities applicable to both plants and
animals of agricultural importance.
Effects of seaweed fertilizers and seaweed extracts on plants
The general assumption amongst those using seaweed extracts
is that hormones native to the seaweeds would be present and
active in the manufactured extracts. Plants grown in soils
treated with seaweed manures, or extracts applied either to the
soil or foliage, exhibit a wide range of responses that have
been well documented in a number of reviews (Abetz 1980;
Blunden 1972, 1977, 1991; Booth 1965, 1966, 1969, 1981;
Hong et al. 2007; Metting et al. 1990; Myklestad 1964; Senn
and Kingman 1978; Stephenson 1974; Stirk and van Staden
2006; Verkleij 1992). Positive responses include improved
germination, root development, leaf quality, general plant
vigor and resistance to pathogens (reviewed in Kahn et al.
2009). Benefits in flower set, fruit production and marketable
qualities of fruit are recorded for a large number of both
herbaceous and woody crop species. Increases in fresh and
dry mass were recorded for tomatoes grown in jiffypots
presoaked with both water and alkaline extracts of A.
nodosum (Povolny 1981). A proprietary marine extract has
been shown to improve the leaf content of macronutrients,
promote growth, and impart resistance to drought stress in
grapes (Mancuso et al. 2006). The key point is that there
should be an increased economic benefit to the growers
(Norrie andHiltz 1999; Norrie and Keathley 2006; Stephenson
1981). Some cytokinin- and IAA-like responses for seaweed
extracts are presented in Table 4. A significant improvement
in the size of olives and the quality of olive oil was recorded
in trees sprayed with an A. nodosum extract fortified with
added nitrogen and boron (Chouliaras et al. 2009). Iron,
copper, and boron contents of the leaves were increased with
seaweed extract treatment, and the fatty acid content in the
olive oil was significantly enriched in linolenic and oleic acids
while palmitoleic, stearic, and linoleic acids were decreased.
The variable responses with different cultivars is well
shown with apples in a multi-year study involving the
seaweed preparations Goëmar BM 86® and Kelpak® (Basak
2008). Trees repeatedly sprayed with 1:500 or 1:400
dilutions of these biostimulators exhibited stronger vegeta-
tive growth than controls, and both products improved
flower quality and prolonged blooming. Sometimes fruit set
and apple size were improved, but the yield of marketable
apples was higher especially with the Goëmar product. The
red coloration of the fruit was either diminished or improved
depending on the cultivar, and sometimes the internal quality
was negatively affected after storage. No effect on return
bloom was observed for either product.
Germination of pepper seeds was examined after priming
seeds in a 10% Maxicrop solution at dilutions up to 1:1,000
(Sivritepe and Sivritepe 2008). A clear inhibition of the
germination rate occurred with the seaweed extract at
concentrations of 1:250 and higher when compared against
control seeds primed with water alone. The data show no
improvement in germination rates with the more dilute
extracts relative to their water parallels. Benefits of the
priming on seedling development were not assessed;
however, it was earlier shown that repeated foliar applica-
tions of Maxicrop increase length, diameter and fruit yields
in peppers while affording an earlier first harvest of the crop
(Eris et al. 1995). Fertilizer plus a simple autoclaved extract
of the brown seaweed, Rosenvigea intricata, stimulated
lateral root development, increased pigment content and the
number of leaves and vegetables over the fertilizer controls
when tested with the crop plant Abelmoschus esculentus
(Thirumaran et al. 2009).
The degree of response exhibited varies with the species
and even the variety of cultivars grown, and under certain
conditions an extract may even be inhibitory (Reitz and
Trumble 1996). The least response to seaweed products is
generally observed with plants raised under near optimal
conditions as might be expected. Application rates, frequency
and timing of the treatments vary with species, season,
geographical location, and local environmental variables.
Important ancillary benefits of seaweed products for crop
production include the amelioration of damage caused by
insects and bacterial or fungal diseases.
The earlier assumption that plant hormones and related low
molecular weight organic compounds native to the seaweeds
Product and algae Cytokinins (CK) CK-like activity IAA-like activity
Seasol Ecklonia + +
Maxicrop Ascophyllum + +
Kelpak E. maxima 0.115 μg L−1 + + Best no. of roots
Marinure Ascophyllum ∼5.4 μg L−1
6.63 μg g−1 powder
+ + 2nd best
Redicrop + 2nd best +
Seamac Ascophyllum + Best for callus +
S.M.3 Laminariaceae, Fucaceae + +
Table 4 Cytokinin- and indole-
3-acetic acid (IAA)-like
responses in six commercial
seaweed extracts
Adapted from Stirk and van
Staden (1996). Cytokinins were
determined in a 28 day soya bean
callus assay, and IAA with an
8 day mung bean rooting assay;
+ indicates a positive response
378 J Appl Phycol (2011) 23:371–393
are mainly responsible for the bioactivities observed in extract
treated plants now requires revision. It is evident that larger
molecules (oligomers and polysaccharide elicitors) in the
extracts can be biologically potent (see the “Polymers” section
below). A high chemical consistency with respect to site and
season of harvesting of A. nodosum has been shown for its
commercial extracts (Craigie et al. 2008). Bioassaysof these
extracts over all seasons show a remarkable degree of
consistency in promoting root initiation and development in
seedlings (Neily, unpublished data). Such consistency in
bioactivity should not be expected given that the phytohor-
mone content of seaweeds can vary widely as the physiology
of the seaweed changes over time (Featonby-Smith and van
Staden 1984; Mooney and van Staden 1984; Jameson 1993).
However, a strong positive bioactivity in these assays has
been exhibited with a high polymer fraction isolated from
these commercial products (Craigie and Neily, unpublished
data). As all water-soluble low molecular weight constituents
had been removed, we must conclude that the polymer
content is an important functional component of alkaline
seaweed extracts.
Effects on diseases and insect pests
The alkaline hydrolyzed seaweed extract, Maxicrop,
sprayed weekly on turnips and strawberries suppressed the
spread of powdery mildew on leaves of the former, and that
of gray mold (Botrytis cinerea) on strawberry fruit.
Improved yields were noted for both crops (Stephenson
1966). Loss of tomato seedlings due to damping-off was
greatly reduced if watered weekly with a 1:120 dilution of
the hydrolyzed extract.
A more recent study evaluated the liquefied seaweed
products Goëmar BM 86® and Kelpak SL for their effects on
two strawberry cultivars (Elkat and Salut) in Poland (Masny et
al. 2004). Two-year field trials for each revealed that Goëmar
BM 86® increased the marketable yield of Elkat fruit by
17% and 43% for 1- and 2-year-old plants, respectively; it
had no effect on fruit weights of either cultivar. Neither
seaweed product influenced the yield of strawberries with the
Salut cultivar, although Kelpak SL reduced the fruit weight
in this, but not in the Elkat cultivar. Both seaweed sprays
reduced fruit firmness in both cultivars. Although B. cinerea
infected up to 24% of the fruit, neither seaweed preparation
reduced the incidence of the gray mold. Clearly, varietal
differences are of significance in the response of a crop, and
the nature of the seaweed extract is itself a variable as shown
in the Mansy et al. (2004) study. The Goëmar product was
manufactured from A. nodosum while Kelpak was from
Ecklonia and, unlike Maxicrop made from A. nodosum, both
were prepared using cell burst technologies. Processing
methods therefore must be considered when assessing the
relative bioefficacy of seaweed extracts.
Treating a plant with a plant systemic inducer or elicitor
such as salicylic acid, jasmonic acid, arachidonic acid, a
seaweed extract, or humic acid and a reactive oxygen donor
provides an increase in pathogenesis-related proteins (PR1,
phenylalanine ammonium lyase PAL, or hydroxyproline rich
glycoproteins) thereby affording protection from diseases
(Moon and Anderson 2003, 2006). Liquid fertilizer from A.
nodosum (GYFA 17, Goëmar) contains laminaran which has
been shown to upregulate the production of PAL, caffeic acid
O-methyl transferase, lipoxygenase and salicylic acid as
defense responses in tobacco (Klarzynski et al. 2000; Patier
et al. 1993; Potin et al. 1999), and of antifungal compounds
in alfalfa (Kobayashi et al. 1993). Strong elicitor responses
were recorded in tobacco leaves treated with λ-carrageenan
solutions (Mercier et al. 2001).
Cotton seedlings challenged with Xanthomonas campestris
developed considerable resistance to the bacterial pathogen if
the seeds were soaked prior to germination for 12 h in a 1:500
solution of Dravya, an aqueous formulation of Sargassum
wightii extract (Raghavendra et al. 2007). Greater resistance to
bacterial attack was exhibited in developing cotton seedlings
sprayed with the seaweed extract, with the greatest reduction
in blight (up to 74% after 80 days) occurring when seed
treatment was combined with a spraying protocol. Evidence
from peroxidase measurements and increased total levels of
phenolics in treated plants suggested that a systemic resistance
had been developed. The seaweed extract was superior to
streptocycline treatment in that it also promoted greater plant
vigor, increased stem girth and higher boll yields without the
disadvantage of releasing an antibiotic into the environment.
Alcohols and polyunsaturated esters have been implicated as
antibacterial agents in chloroform extracts of red and brown
seaweeds (Vallinayagam et al. 2009). Low levels of glycine
betaine known to be present in seaweed extracts confer some
resistance to Uromyces phaseoli in beans (Blunden et al.
2009). Creeping bentgrass showed increased superoxide
dismutase and a reduction in dollar spot disease (Sclerotinia
homoeocarpa) when treated with A. nodosum extract and
humic acids (Zhang et al. 2003). Increases in phenolic
components, flavonoids and antioxidant levels were reported
in leaves from spinach plants watered with soluble A.
nodosum extract (Acadian Seaplants; Fan et al. 2010).
Stephenson (1966) reported a significant reduction in
black bean aphid (Aphis fabae) infestations on broad bean
leaves sprayed with Maxicrop compared to water sprayed
controls. In addition, she remarked that fewer winged adults
settled on extract sprayed leaves of sugar beets than on the
controls suggesting an aversion response of the aphids rather
than an insecticidal effect of the extract. Similarly, the
population of red spider mites (Tetranychus telarius) in
orchards was held to a low level on trees sprayed with the
hydrolyzed seaweed extract relative to the unsprayed trees.
The mites appeared to actively avoid settling on extract
J Appl Phycol (2011) 23:371–393 379
treated apple leaves when offered the choice of untreated
leaves. The reduction of spider mites and eggs on glasshouse
chrysanthemums sprayed fortnightly with Maxicrop was
greater than for controls receiving the normal acaricide
protocol. Two-spotted red spider mite (Tetranychus urticae)
populations on strawberries grown in high polyethylene
tunnels were significantly reduced following a twice weekly
spraying with Maxicrop Triple essentially confirming the
earlier observations (Hankins and Hockey 1990). The
mechanism of action remains unknown although chelated
metals applied to leaves can reduce fecundity of two-spotted
spider mites (Terriere and Rajadhyaksha 1964). Increased
levels of anthocyanins and phenolic constituents in leaves
may alter the palatability or acceptability of leaves to insect
predators.
A seaweed extract, Kelpak 66, is reported to reduce root
damage from nematode (Meloidogyne incognita) predation in
tomatoes whether applied to the foliage or as a soil drench in
a 1:500 dilution (Featonby-Smith and van Staden 1983). The
greatest improvement in roots, leaves, and fruits of heavily
infected plants was with a single soil drench at the time of
transplantation. Interestingly, the nematode population in the
soil increased over the control level when the seaweed
extract was applied, but the number of nematodes recovered
from inside the roots was significantly below that in the
infected controls. Reduction in fecundity of the root-knot
nematode M. javanica occurred when Arabidopsis seedlings
were inoculated in vitro with juvenile nematodes if the
seedlings were treated with Maxicrop or an equivalent
concentration of a betaine mixture (Wu et al. 1998). The
alleviation of biotic stress by seaweed products is discussed
in Kahn et al. (2009).
Plant hormones
The modern concept of plant hormones requires that they be
naturally occurring organic substances which influence phys-
iological processes at low concentrations, far below those
where nutrients or vitamins affect those processes (Davies
2004). There is no requirement that the hormone be trans-
ported within the plant. A plant growth regulator is a term
commonly used in the agrochemical industry to distinguish
synthetic plant growth regulators from the endogenous ones.
Following the first report of auxin in marine algae (van
Overbeek 1940), attention focused on plant growth regulators
that could be detected in algae. Conclusive identification ofIAA, however, remained questionable until the 1970s
although Avena coleoptile bioassays revealed several indole-
type compounds released by alkaline hydrolysis of several
seaweeds including Fucus vesiculosus and A. nodosum
(Buggeln and Craigie 1971). It is now recognized that many
of the common higher plant hormones (abscisic acid, auxins,
cytokinins) occur in algae including brown seaweeds (Table 5;
Jameson 1993; Tarakhovskaya et al. 2007; Zhang et al.
1993). Other growth regulators also are reported from brown
algae (Table 6). The presence of IAA, phenylacetic acid and
its para-hydroxy derivative were reported for Undaria
pinnatifida using chromatographic, IR, and MS techniques
(Abe et al. 1972; 1974), but the quantity of IAA found in the
harvested seaweed was small (∼10 μg kg−1 wet weight). The
commercial extracts Maxicrop (A. nodosum) and Kelpak 66
(E. maxima) were examined by GC-MS and found to contain
IAA (Crouch et al. 1992; Sanderson et al. 1987). Cell burst
concentrates of both E. maxima and M. pyrifera contained
indole-amino acid and other indole conjugates in addition to
IAA (Stirk and van Staden 2004). The auxin content,
however, declined following a fortnight of storage at 54°C.
Abscisic acid (ABA) is widely distributed in algae being
detected in 64 species from nine divisions by ELISA (Hirsch
et al. 1989). Of particular interest is its occurrence in ten
genera of brown algae including A. nodosum, a commercial
extract of it, and E. maxima and Laminaria spp. (Boyer and
Dougherty 1988; Hirsch et al. 1989). The function of ABA
in the algae remains to be discovered although it induces
genes for protein synthesis required for drought tolerance of
seeds in terrestrial plants (Rensing et al. 2008; Verslues et al.
2006). Abscisic acid induces stomatal closure in drought,
protein storage in seeds, gene transcription for proteinase
inhibitors, inhibits shoot growth, and induces some seed
dormancy effects (Davies 2004).
Evidence for ethylene production in brown seaweeds is
tenuous although 1-aminocyclopropane-1-carboxylic acid,
a potential ethylene precursor, was reported in Kelpak 66, a
commercial extract of E. maxima (Nelson and van Staden
1985).
Results from paper chromatography and a dwarf pea
bioassay indicated that gibberellin-like substances (possibly
GA1, GA3, and GA6) occur in F. vesiculosus (Radley
1961). Gibberellin-like bioactivity was observed in a lettuce
hypocotyl elongation assay of freshly prepared commercial
extracts of Ascophyllum; however, the activity was unstable
and disappeared within 4 months of storage (Williams et al.
1981). Direct chemical evidence for gibberellins does not
appear to exist for brown algae, although traces of GA4
were identified by MS in a soluble extract produced by
Acadian Seaplants Limited from A. nodosum (R.P. Pharis,
pers. comm.).
Cytokinin-like bioactivity was reported in the early
1970s in commercial seaweed extracts (Williams et al.
1981). Experimental trials with these extracts resulted in
increased potato yields, elevated protein content of grass,
and a pronounced retardation in the loss of green color in
ripening lime fruits, effects attributed to cytokinin activities
of the extracts (Blunden 1977). Cytokinins and zeatin
riboside are reported to improve heat tolerance in creeping
bentgrass (Zhang et al. 2010).
380 J Appl Phycol (2011) 23:371–393
Evidence that cytokinins are widely distributed in
seaweeds was presented by Stirk et al. (2003) who used
immunoaffinity chromatography, HPLC-MS, and single ion
measurements to investigate five green, seven brown, and
19 red species of seaweeds (Table 7, Table 8). All 31
species contained isoprenoid cytokinins, principally cis-
and trans-zeatins, their ribosides and O-glucosides, and
isopentenyl adenine and -adenosine. Quantitative measure-
ments referenced to deuterated cytokinin standards revealed
that cis-zeatins generally predominated over the trans-
zeatins. In addition, benzyladenine was present in all
species but at concentrations usually lower than those of
its ortho- and meta-hydroxylated derivatives (topolins). It is
interesting to note that the topolins can act as substrates for
zeatin-O-glucosyl transferases (Mok et al. 2005), and that
trans-ZOG and meta-topolin are dominant cytokinins in
cell burst seaweed concentrates (Stirk et al. 2004).
Qualitative and quantitative changes relating to seasonal
and lunar cycles were reported for endogenous cytokinins
in E. maxima, and Sargassum heterophyllum (Featonby-
Smith and van Staden 1984; reviewed in Jameson 1993).
The cytokinin concentrations in S. heterophyllum also were
greatest at the onset of vegetative growth and during
gamete production (Mooney and van Staden 1984).
Cytokinins in M. pyrifera were most concentrated
(23.4 ng g−1 fresh weight) in the intercalary meristem of
young blades (de Nys 1990).
Cytokinin metabolism is evolutionarily old as the
signaling molecules (N6-substituted adenine derivatives)
occur in bacteria (Barciszewski et al. 2007); however, the
structure of the active sites of the histidine phosphotransfer
(HPt) proteins differs from that of higher plants (Sugawara
et al. 2005). At least one gene coding for HPts and a
regulatory protein involved in a cytokinin feedback
signaling system have been reported in the green algae O.
tauri, Chlamydomonas reinhardtii, and Volvox carteri (Pils
and Heyl 2009). By comparison there were two HPts in
rice, ten in poplar, and five in Arabidopsis. Nuclear HPt
activates response regulators (RRs) which are involved in
negative feedback regulation of cytokinin signaling path-
ways. There are two to four RRs in the algae, seven or 14 in
mosses, 23 in rice, 32 in poplar, and 22 in Arabidopsis.
However, proteins of the CHASE domain responsible for
binding a cytokinin ligand to a receptor were not detected
in the algae, although two to five were identified in the
other species (Pils and Heyl 2009).
Betaines, while not traditionally included among the
classical plant hormones, are widely distributed in plants
including seaweeds (Table 6) and are found in seaweed
extracts (Blunden et al. 1982, 1984, 1986; MacKinnon et
al. 2010). Glycine betaine, γ-amino butyric acid betaine,
δ-aminovaleric acid betaine and laminine have been
reported in A. nodosum and F. serratus (Blunden et al.
1984). These N-methylated compounds are good potential
sources of formaldehyde in biological systems and have
been implicated in a double-immune response of beans to
bean rust, Uromyces phaseoli (Tyihák 2006). Concentra-
tions of glycine betaine as low as 10−12 M reportedly
Classic PGH Reported in genera
Abscisic acid Ascophyllum, Laminaria
Auxins Ascophyllum, Fucus, Laminaria, Macrocystis, Undaria
Cytokinins Ascophyllum, Cystoseira, Ecklonia, Fucus, Macrocystis, Sargassum
Ethylene Not reported
Gibberellins Cystoseira, Ecklonia, Fucus, Petalonia, Sargassum
Table 5 Classic plant growth
hormone (PGH) occurrence in
brown seaweeds
After Jameson (1993) and
Tarakhovskaya et al. (2007)
PGR Genusa Physiological functions in terrestrial plantsb
Betaines Ascophyllum, Fucus,
Laminaria
Osmoregulation, drought and frost resistance,
disease resistance
Brassinosterols nrc Cell division, elongation, vascular differentiation,
promotes ethylene production, inhibits root growth,
Jasmonates Fucus?d Induces defense and stress responses, and synthesis
of proteinase inhibitors, promotes tuber formation
and senescence, inhibits growth and seed germination
Polyamines Dictyota Influence growth, cell division and normal development
Salicylates nr Induces defense response in pathogenesis, reverses ABA
effects, blocks wound response, inhibits ethylene
production and seed germination
Signal peptides nr Initiate defense response, self-incompatibility recognition
Table 6 Hormone-like plant
growth regulators and reports
for brown algae
a Adapted from Jameson (1993),
Tarakhovskaya et al. (2007)
b After Davies (2004)
c nr Not reported
d Jasmonate-induced phlorotannin
production (Arnold et al. 2001)
J Appl Phycol (2011) 23:371–393381
confer some immunity in bean plants to infection by the
fungus U. phaseoli (Blunden and Tyihák 2009). The
principal betaine in both A. nodosum and the Acadian
Seaplants’ commercial extract was γ-amino butyric acid
betaine at 0.019–0.035% and 0.014–0.027% of their
respective dry weights (MacKinnon et al. 2010). As also
observed by Blunden et al. (2009), for diverse collections
of brown seaweeds, no significant seasonal variation in
betaine content was detected by MacKinnon et al., (2010),
although a yellowish, small morphotype of A. nodosum
contained lower betaine levels than its normal ecotype.
However, this result may have been related to the local
microenvironment of the morphotype.
Physiologically betaines are cytoplasmic osmoticants, but
they also elicit a number of responses in plants similar to those
of cytokinins (Blunden 1977; Blunden et al. 1996). The
salinity range of the halophobic bacterium Klebsiella pneu-
monia was increased by crude seaweed extracts or by added
glycine betaine, proline betaine, 3-dimethylsulphiopropionate,
and choline, but not by proline (Mason and Blunden 1988).
Their role in alleviating abiotic stresses such as drought, frost,
and salinity in plants has been discussed (Kahn et al. 2009).
Polymers
Seaweeds synthesize polymers such as agars, alginates,
carrageenans, fucans, phlorotanins and others not found in
terrestrial plants (Connan et al. 2006; Khan et al. 2009).
These polymers show a variety of biological activities in
both plant and animal systems and are involved in host
defense mechanisms (Ideo et al. 2009; Li et al. 2008; Myers
et al. 2010; Nakayasu et al. 2009; Wang et al. 2009a). Of
particular interest in agriculture are those that elicit defensive
responses resulting in protection against pathogens or insect
damage. A reduction in bean root rot caused by Fusarium
solani f. phaseoli was observed in soils amended with chitin,
laminarin, or Laminaria (Mitchell 1963). An A. nodosum
extract (GYFA 17, Goëmar) was shown to contain lami-
naran, a D-glycanase elicitor (Patier et al. 1993). Linear β-1,
3-glucan elicited four families of pathogenesis-related pro-
teins in tobacco leaves providing resistance to soft rot caused
by Erwinia carotovora; the minimum effective glucan
polymer length was laminaripentaose (Klarzynski et al.
2000). Systemic resistance to tobacco mosaic virus was
elicited by sulfated fucan oligosaccharides (Klarzynski et al.
Table 7 Isoprenoid cytokinin distribution in 31 species of seaweeds
Acronym Isoprenoid cytokinins Present in spp. pMol g−1 dry wt pMol g−1 distribution in G, B, and R spp.a
iP iso-Pentenyladenine 31 3.0–82 >25 in 3B, 3R
iPR iso-Pentenyladenosine 31 1.3–133 >25 in 1G, 6R
iPR5MP Iso-Pentenyladenosine-5′-monophosphate 11 1.6–43 >5 in 1G, 2B, 2R
cZ cis-Zeatin 31 0.2–76 >15 in 1G, 4R
cZR cis-Zeatin riboside 28 0.1–28 >5 in 2G, 6R
cZOG cis-Zeatin-O-glucoside 24 0.1–29 >5 in 2G, 2R
cZROG cis-Zeatin riboside-O-glucoside 20 0.13–7.5 >5 in 2G
cZR5MP cis-Zeatin riboside-5′-monophosphate 11 0.1–6.9 >5 in 1B, 2R; 3B and 3R had tZ>cZ
tZ trans-Zeatin 31 0.2–12 >5 in 1B, 2R 6 spp. had tZ>cZ; 3B, 3R
tZR trans-Zeatin riboside 20 0.01–0.7 3 spp. had tZ>cZ
tZOG trans-Zeatin-O-glucoside 30 0.3–44 >15 in 2B, 3R
tZR5MP trans-Zeatin riboside-5′-monophosphate 11 0.1–6.9 >5 in 1G, 1B, 1R
DHZ Dihydrozeatin 8 0.15 max In 1G, 2B, 5R spp.
Adapted from Stirk and van Staden (2003)
a Ranges of cytokinin content in brown (B), green (G), and red (R) seaweeds
Abbreviation Aromatic cytokinins Present in spp. pMol g−1 dry wt pMol g−1 distribution
in G, B, and R spp.a
BA Benzyl adenine 31 0.4–2.0 <1.0 in most spp.
mT meta-Topolin 30 1.0–4.8
mTOG meta-Topolin-O-glucoside 29 1.9–9.9 >5 in 1G, 1R
oT ortho-Topolin 30 2.0–22.5 >5 in 2B, 1R
oTR ortho-Topolin riboside 14 0.1–3.5
oTOG ortho-Topolin-O-glucoside 30 0.1–3.3
Table 8 Aromatic cytokinin
distribution in 31 species of
seaweeds
Adapted from Stirk and van
Staden (2003)
a Ranges of cytokinin content in
brown (B), green (G), and red (R)
seaweeds
382 J Appl Phycol (2011) 23:371–393
2003). The heavily sulfated λ-carrageenan also can trigger
signaling pathways in tobacco leaves mediated by ethylene,
jasmonic and salicylic acids as well as inducing several
defense related genes (Mercier et al. 2001). Seaweed
polymers also elicit responses in animals as discussed below.
Alkali, widely used in the liquefaction of seaweeds, has the
potential to generate compounds not native to the original
seaweeds through degradation, rearrangement, condensation,
and base catalyzed synthetic reactions. The principal polymers
of brown seaweeds are mainly polysaccharides (alginates,
several types of fucose containing polymers, laminarans),
phlorotannins, proteins and nucleic acids (Table 9).
Polyuronides such as pectin and alginic acid are well
known to undergo depolymerization and β-elimination
reactions in dilute alkali (BeMiller and Kumari 1972; Haug
et al. 1963, 1967). A unique detailed analysis of the mono-
and dicarboxylic acids generated during hydrolysis of
alginate with NaOH (0.1 M and 0.5 M) at 95°C and 135°C
was reported by Niemela and Sjöström (1985). They
identified and quantified eight to ten monocarboxylic acids
which comprised 9.8% to 14.2% of the starting mass of
alginic acid (Table 10). Lactic, formic, and acetic acids were
the principal monocarboxylic acids formed together with
smaller amounts of glycolic and other acids. Dicarboxylic
acids identified ranged from 15 to 21 and accounted for
17.3% to 42.2% of the initial alginic acid mass. The higher
numbers were produced with the higher alkali concentration.
The main components were various isomeric saccharinic,
pentaric, and tetraric acids with lesser amounts of malic,
succinic, oxalic, and several other minor dicarboxylic acids.
Thus, dilute alkali can convert 27% to 56% of purified
alginic acid into a variety of products, some of which are
known plant metabolites.
Phlorotannins Polymeric polyphenols or phlorotanins are
important components of many brown algae (Glombitza et al.
1975; Ragan and Craigie 1976; Schoenwaelder 2008;
Schoenwaelder and Clayton 1999; Steinberg 1989). Detailed
chemical investigations initiated during the 1970s have
provided considerable information on the highly variable
chemical structures of these polyphenols (comprehensively
reviewed in Ragan and Glombitza 1986). As the monomeric
unit is phloroglucinol, they are termed phlorotannins, and
they can range in mass from 320 to 400,000 Da (Ragan and
Glombitza 1986). Those of higher molecular weight are
astringent, bind to hide powder and have been used as a mild
tanning agent for leather.
The chemical linkages between successive phloroglucinol
units were proposed as a basis for a system of nomenclature
(Glombitza 1981; Ragan and Glombitza 1986). The units
may be linked through aryl–aryl or diaryl ether bonds, and
combinations of these structures appear as polymerization
proceeds (Table 11). The number of isomers can be very
large given the numerous potential linkage sites available for
polymerization.
The richest sources are found in the Fucaceae, especially A.
nodosum and F. vesiculosus where phlorotannins can account
for up to 15% of the algal dry mass (Ragan and Glombitza
1986). A. nodosum from Norway and Nova Scotia had 15–
25% of extractable polyphenols as high molecular weight,
non-dialyzable components. Phloroglucinol itself was
detected in low levels in 17 of 26 species of brown
seaweeds, but was not detected in A. nodosum (Glombitza
1981). Sulfated polyphenols are widely distributed in brown
algae, but have not been well studied (Ragan and Jensen
1979). Various monohalogenated (I, Br, Cl) phloroethols
have been isolated in low amounts. Notable is Laminaria
Table 9 Major constituents of Ascophyllum nodosum
Compound Content
(% dry wt.)a
Content
(wt.%)b
Content
(% dry wt.)c
N-free carbohydrates 46–60
Alginic acid 15–30
Laminaran 0–10
Fucoidan 4–10
Other carbohydrates ca. 10
Protein 5–10 5–10 4.9
Fats 2–7 5.0
Tannins 2–10
Organic matter65.7
Moisture 12–15
Crude ash 17–20 21.1
Klason lignin 18.6
Total dietary fiber 50.3
Sugars Fuc=6.60; Xyl=1.68;
Gal=0.69; Glc=4.48;
Man=3.84;
Uronic acids=14.44;
Ara=Rha=0
a After Baardseth (1970); Indergaard and Minsaas (1991) for Norwegian A.
nodosum
b After Jensen (1972)
c After Dierick et al. (2009) for Irish A. nodosum
Table 10 Acids produced during alkaline degradation of alginic acid
NaOH
(M)
Temperature
(°C)
Dicarboxylic
acids (% w/w)
Monocarboxylic
acids (% w/w)
Total acids
(% w/w)
0.1 95 17.3 9.8 27.1
0.1 135 22.0 14.2 36.2
0.5 95 38.7 11.2 49.9
0.5 135 42.2 14.2 56.4
Adapted from Niemela and Sjöström (1985)
J Appl Phycol (2011) 23:371–393 383
ochroleuca which has organically bound Cl at 4% of the
acetylated high molecular weight phlorotannins (Ragan and
Glombitza 1986).
The polyphenols are regarded as allelochemicals accounting
for ∼1% of the photoassimilated carbon in these algae; their
production may be stimulated by methyl jasmonate (Arnold
and Targett 1998; Arnold et al. 2001). Phlorotannin extracts
from A. nodosum are reported to have potential in the
treatment of diabetes (Zhang et al. 2006) while those from
Ecklonia cava are now marketed for potential health benefits
due to their powerful antioxidant activities (Seanol® 2008;
Ventree Co. Ltd. 2002, 2004).
Alkali is also known to act on polyphenols to produce a
complex spectrum of reaction products, the nature of which
depends on the hydroxylation pattern of the original polyphe-
nol. Ragan and Glombitza (1986) have summarized some of
the rearrangements that occur when natural phlorotannins are
reacted with dilute alkali. The tannins of Halydris siliquosa
(fuhalol type) heated at pH 10 for 15 to 120 min are
degraded to give various dibenzofurans. Similar treatment of
polymeric tannins of Sargassum muticum yields similar
products. Also Pelvetia canaliculata phlorotannins treated
with mild alkali yield a complex mixture of dibenzofurans,
the structures of which have been only partly established.
Requirements for dibenzofuran formation from phloroglu-
cinol polymers were studied by Glombitza and his colleagues
using model compounds (see Ragan and Glombitza 1986). A
diphenyl ether with 2,4,6-trihydroxy substitution on one ring
(ring A) must have at least one hydroxyl in the meta position
on the second ring (ring B) for dibenzofuran to be formed. If
a second hydroxyl on ring B is para to the meta hydroxyl,
no benzofuan is formed. Also, if ring B is hydroxylated,
ortho or para to the ether function, the ether bond of ring A
will be cleaved without forming benzofuran.
When cleavage of the ether linkage occurs, phloroglucinol,
resorcinol, or pyrogallol will be formed depending on the
hydroxyl substitution patterns of the aromatic ring systems.
This knowledge was used to determine that the polymeric
polyphenols of S. muticum were essentially the same as the
low molecular weight polyphenols in the seaweed. P.
canaliculata also yields primarily dibenzofurans when
similarly treated with mild alkali.
These examples show that the use of alkali to liquefy
seaweed components can generate a variety of compounds not
present in the parent seaweeds. As the above studies were
conducted on isolated polymers, care should be exercised in
directly extrapolating the results to the exceedingly complex
reaction mixture that pertains when the entire seaweed is
subjected to alkaline hydrolysis during the liquefaction and
extraction processes. However, novel and biologically inter-
esting compounds will be formed and these will appear in
commercial extracts. Some are normal metabolites, while
others may be expected to be biologically active either
positively or negatively. The nature and quantities of these
reaction by-products will depend on the composition and
chemical structure of the polymers originally in the seaweed
as well as on the processing conditions used to manufacture
the soluble extract. It follows that various commercial
seaweed extracts are not equivalent so can be expected to
exhibit differences in biological activity when applied to
agricultural crop species.
Seaweeds and extracts in animal diets
Meal European usage of seaweeds in animal husbandry dates
at least to Roman times (for horses) and seaweed was fed
regularly to domestic animals in Iceland, France, and Norway.
The main constituents of A. nodosum, the principal species
Table 11 Phloroglucinol-based structures recognizable in brown algal phlorotannins
Name Structure Comments Sources
Fucols Dehydrooligomers with aryl–aryl bonds Prefixes di-, tri- etc.
designate the number
of phloroglucinol units
Fucus vesiculosus (Fucaceae)
Phloroethols Dehydrooligomers with diaryl ether bonds Common in Fucales
and Laminariales.
Fucophloroethols Dehydrooligomers with combinations
of the above linkages
Common in Fucales;
sporadic in Laminariales
Fuhalols Ether linked units bearing an additional
hydroxyl on either ring forming a vicinally
trihydroxylated structure
Bifuhalol to tridecafuhalol Bifurcaria bifurcata (Sargassaceae);
oligomers in Halidrys siliquosa
(Cystoseiraceae)
Isofuhalol Contains at least one supernumerary hydroxyl
with phloroglucinol units linked para and meta
Chorda filum (Chordaceae)
Eckols Dehydrooligomers with three phloroglucinol
ether links with further cyclization to form
dibenzo[1,4]dioxin
Two ether-linked eckols
is a dieckol; if C–C linked
they are bieckols
Ecklonia kurome, E. maxima and
Eisenia arborea (all Alariaceae)
Adapted from Glombitza (1981) and Ragan and Glombitza (1986)
384 J Appl Phycol (2011) 23:371–393
used for modern seaweed meal, are shown in Table 9. Jensen
(1972) also provided data for ascorbic acid, tocopherols, a
suite of B-vitamins, and mineral elements including iodine.
Extensive trials with chickens, hogs, sheep, and dairy cows
were reported (Jensen 1972; Nebb and Jensen 1965). A 3–
7% A. nodosum meal supplement improved growth and
production with vitamin A or riboflavin deficient poultry.
Back fat was reduced in swine compared to the controls, and
there was a noticeable reduction in liver parasites in the
animals fed a 3–5% ration of seaweed meal. The significant
increase in wool production recorded in the sheep fed
seaweed meal was attributed to the prevention of molting.
Responses to A. nodosum meal fed as a 10% replacement
in the diet differed markedly among animal species being
highly toxic to rabbits, but without effect on weight gain,
blood parameters (hematocrit, hemoglobin content, or iron
concentration) or causing observable changes on autopsy of
rats after a 100-day trial (Jones et al. 1981). Pigs also fed
10% of the meal showed no significant change in measured
blood parameters during an 84-day study, however, weight
gain was significantly reduced (15% relative to the controls;
the pig weights in their Table 3 appear to be in kilograms
rather than grams) for the A. nodosum-fed animals. Further,
the authors cite Jones’ 1973 thesis as showing that A.
nodosum from a separate location also was toxic to rabbits,
while only mild toxicity resulted with F. serratus meal fed at
the same 10% inclusion rate. No deleterious effects were
exhibited in parallel experiments incorporating meals from
either Laminaria digitata or L. hyperborea in the rabbit
diets.
The brown seaweeds M. pyrifera and Sargassum spp.
recently have been evaluated as extenders or fodder supple-
ments in goat and sheep diets. Ten 43-week-old Nubian
goats were fed balanced diets and ten were fed diets in which
sun-dried Sargassum spp. flour replaced 25% of the ration
(Casas-Valdez et al. 2006a). The seaweed flour contained
89% dry matter, 8% protein, 39% carbohydrates, 31% ash,
and significant amounts of ω-3 and ω-6 fatty acids. Body
weights, feed intake, and feed conversion rates did not differ
from the controls over the 60-day trial. Evaluation of M.
pyrifera flour was conducted using four rumen cannulated
goats held in metabolism cages (Castro et al. 2009). During
four 15-day experimental periods, the goats were fed diets
consisting ofa balanced control and diets in which seaweed
flour replaced 10%, 20%, and 30% of the standard diet. No
significant differences in animal performance or digestibility
of the diets were found. Water intake and urine output again
increased as did the ruminal pH as the seaweed content in
the diet rose. As no deleterious effects were observed, it was
concluded that M. pyrifera also could serve as a partial
replacement fodder for goats.
Using a similar experimental protocol with four fistulated
Pelibuey sheep, Marin et al. (2009) determined that feed
intake was unaffected by the addition of M. pyrifera flour to
the diets. Water intake and urine production were increased
as the seaweed content was raised. Dry matter digestibility
(74–79%) and protein digestibility (85–88%) were similar
for all treatments. Digestibility of both the acid detergent and
neutral detergent fiber fractions was increased in the seaweed
fed animals. Analysis of rumen fluids showed that volatile
fatty acids decreased in the seaweed fed sheep while the pH
increased toward neutrality. As deleterious effects were
absent, it was concluded that M. pyrifera could replace up
to 30% of the normal sheep diet.
Notable was a 7-year experiment during which one cow
of each of seven monozygotic twins was fed 200 g day−1 of
A. nodosum meal over 23 lactation periods (Jensen 1972).
The remaining twins (controls) were fed a standardized diet
including a mineral supplement. The seaweed fed animals
produced a significant 6.8% increase in milk (4% fat
corrected) over the controls (p=0.01). A reduction in
mastitis and improved conception performance also were
observed as side benefits in the seaweed-meal-fed cows.
The effect of a ration containing 1% Tasco meal fed for
45 days in reducing body temperature of steers during heat
stress was investigated using temperature and humidity
controlled environmental chambers (Williams et al. 2009).
Eight of 24 steers were fitted with ruminal cannulae to
measure in situ disappearance of neutral detergent fiber
during the four experimental periods. Rectal temperatures
and respiration rates were recorded as were dry matter intake
and body weight changes. The maximum day temperatures
were 36°C and night temperatures were 25°C or 31°C in
different stress periods. The responses of the animals were
complex, changing somewhat across the three different heat-
stress periods. Dry matter intake declined after ∼4 days
under heat stress for both Tasco and control animals and
returned to normal in ∼10 days after removal of the stress.
Heat load had no effect on in situ neutral fiber disappear-
ance; however, Tasco may increase this rate under some
conditions. Rectal temperature of the steers was reduced by
Tasco for 3 or 4 days early in a heat-stress period, but Tasco
showed no effect under a higher heat-stress load.
Improvements in carcass properties of cattle, particularly in
the shelf life of steaks, were measured following treatment
with 2% Tasco meal for two 2-week intervals during the
feedlot finishing period (Braden et al. 2007). Changes in fat
deposition resulted in greater marbling of the lean muscle
which also exhibited a lower percentage of protein than in
the control animals without Tasco. The preferred red color of
steaks was maintained significantly longer in samples held in
a simulated retail display for up to 38 days. The color
retention was attributed to a combination of higher oxy-
myohemoglobin and lower metmyoglobin levels measured
in the lean muscle of the seaweed-treated animals compared
to the controls. Steaks from the Tasco fed group were
J Appl Phycol (2011) 23:371–393 385
generally more uniform and did not exhibit the same degree
of browning and off-flavor as the control steaks. It was
concluded that short-term feeding of Tasco prior to slaughter
of feedlot cattle was beneficial.
The performance and carcass condition of newly weaned
lambs fed the A. nodosum product Tasco-14™ at 10 or
20 g kg−1 of diet weight was determined (Bach et al. 2008).
The dose rate and time offered varied from 7 days to a
maximum of 28 days for the 10 g/kg supplement. Carcass
weight, dressing proportion, grade rule fat, and conforma-
tion scores were unaffected by the Tasco feeding. The fecal
E. coli level for the seaweed fed lambs was lower than for
the controls after the 28 d treatment. No O157:H7 infection
was detected in the lambs.
The benefits of A. nodosum meal (Tasco® 14) in cattle
diets include a reduction in enterohemorragic E. coli in
fecal samples and on hides after two 14-day periods of
supplementation prior to slaughter (Barham et al. 2001).
Salmonella spp. also was reduced relative to the post-
slaughter control samples. This effect was essentially
confirmed by Braden et al. (2004) who supplied 2% of
Tasco-14 meal to heifers and steers for 14 days immediately
before slaughter. The incidence of both E. coli O157 and
O157:H7 was reduced significantly in feces and on hides
compared to the respective controls. Although the incidence
of Salmonella spp. increased during the trial, the terminal
scores for Tasco-treated animals were lower for feces and
hides than those for the control animals.
The shedding of enterohemorragic E. coli O157:H7 by
Tasco-14™ fed cattle was investigated further using
experimentally infected animals (Bach et al. 2008). Year-
ling steers were inoculated with E. coli O157:H7 and 7 days
later were fed the seaweed meal at 10 and 20 g kg−1 for
14 days, or 20 g kg−1 of diet for 7 days. The fecal shedding
patterns of the E. coli were followed for 14 weeks.
Detection of the fecal pathogen was significantly less
frequent for the seaweed fed steers than for the controls
indicating that the A. nodosum meal was effective in
reducing shedding of the bacterium. As volatile fatty acids
and pH of the feces were similar among treatments, it was
suggested that no fecal alterations had occurred antagonistic
to the pathogen survival.
An interesting application for seaweed meal is its
incorporation into shrimp feed. Brown shrimp were fed a
commercial diet and one containing 4% of Sargassum meal
(Casas-Valdez et al. 2006b). Shrimp in the two treatments
did not differ in weight increments, size, survival rates, and
feed conversion over the 45-day trial. No detrimental
effects were seen. Analysis of the muscle tissue showed
that cholesterol content had decreased by 29% for shrimp
on the seaweed diet compared to the controls. The
hypocholesterolemic activity of brown seaweed fractions
when fed to vertebrates has long been known (Tsuchiya
1969). Broad applications are currently being considered
for functional ingredients from both micro- and macroalgae
(Plaza et al. 2009; Myers et al. 2010).
Beneficial changes in gut flora have been demonstrated
with 6-week-old rats fed diets containing up to 5% of either
alginate oligomers or inulin fructooligosaccharides for
14 days (Wang et al. 2006). The alginate oligomers
increased both cecal and fecal levels of the benefical
bifidobacteria and lactobacilli significantly over those in
the controls or the fructooligosaccharide fed group. Both
types of oligosaccharides decreased the cecal pH relative to
the controls. At the same time, they also decreased the
populations of enterobacteriaceae and enterococci leading
to the conclusion that the alginate oligomers were acting as
prebiotics.
Extracts Experiments conducted with an A. nodosum extract
(Tasco-Forage, Acadian Seaplants) sprayed on tall fescue
(Festuca arundinacea) pasture which was grazed by lambs
or cattle demonstrated long term beneficial effects on the
animals (Fike et al. 2001; Saker et al. 2001). The effects
were most noticeable when the fescue was infected with the
endophyte Neotyphodium coenophialum. This common
ascomycete synthesizes ergot-type alkaloids which, when
ingested by grazers, result in reduced weight gain, higher
body temperature, heat intolerance, and generally poorer
condition of the animals relative to those feeding on
uninfected fescue. Lambs and yearling beef steers grazing
the treated