PROSEA, Introduction to Algae

Plant Resources of South-East Asia
Introduction

Definition and diversity of Cryptogams

Cryptogams

The designation "Cryptogams" can be used for all organisms that were traditionally considered to be plants, except the Spermatophyta (Gymnospermae and Angiospermae). Although the term "Cryptogams" does not cover an accepted taxon, it is still the only available terminology that can be used to include all algae, fungi, mosses, ferns and fern-allies, as well as at least some of the organisms now considered to belong to the Bacteria.

The Cryptogams form a rather large and very diverse commodity group, with a wide range of uses and can be found growing in many different habitats. In modern systems, Bacteria and Fungi are usually not included with the plants, although the Fungi are still covered by the International Code of Botanical Nomenclature. Algae and Fungi are included in this volume because they are also dealt with in the basic sources (Burkill, 1966; Heyne, 1927). The Bacteria have been added to make the information even more complete.

In the Prosea volume on Cryptogams the following groups will be covered (Margulis & Schwarz, 1982):

Monera : different groups of bacteria as well as Cyanophyta (blue-green algae);
Fungi : all groups, including the lichens;
Protoctista : algal groups including Phaeophyta (brown algae), Rhodophyta (red algae) and Chlorophyta (green algae), as well as the fungus-like group Chytridiomycota;
Plantae : mosses, clubmosses, horsetails and ferns.

Marine plants (seaweeds) are included as well as organisms growing as epiphytes in the upper branches of rain forest trees, while some other organisms grow mainly subterrestrially. A minority of the species are cultivated, either under special circumstances (fermenters for bacteria and yeasts), in gardens, plantations (mycorrhizae) or in phycoculture on rafts or lines. Very few cultivars of Cryptogams are known, usually these are ornamental plants or may be seaweeds cultivated for bulk production of phycocolloids. Most of the species of Cryptogams treated here are indigenous, although some introduced species will be included.

Role of Cryptogams

Because the Cryptogams do not form a real entity, it is not possible to completely summarize the commodity use for the different taxa.

Many Cryptogams are eaten in some form, often as a salad or condiment. Others have medicinal applications or form the source of vitamins, phenols, amino acids, iodine, carbohydrates, fats, antibiotic substances or even poisons. In addition, selected species are used as a laxative, vermifuge or insect repellent. Several form sugars, alcohols or colloids; there are even some timber plants or producers of fibres, dyes and tannins found among the Cryptogams. The uses of Cryptogams as feed for animals (including molluscs, shrimps, and some fish) or as a fertilizer or "green manure" are known, as is the application of plant parts for packing and for wicker-work. Finally there are also Cryptogams that can be used as ornamental plants or as a substrate on which ornamental plants can be grown.

Cryptogams can be found in many different habitats and are often primarily used locally. In these cases they are collected for domestic use or are sold as fresh or conserved material in local markets. Only relatively few products have wider uses or are cultivated for national or international trade. These tend to be bacteria used in industrial processes; seaweeds grown for the production of colloids or for use as vegetables; edible fungi and fungi used in the production of food and drinks, and ferns and other flowerless vascular plants used as ornamentals, or (in the case of the water fern Azolla Lamk) as "green manure".

Of course collection, culture, handling and yield differ greatly, as well as the effort and capital necessary for successful production. In most cases production can be increased and improved, while sales can be increased through careful promotion and quality control of the end-product. Often the demand for Cryptogamic products is rather limited because of inadequate or lacking quality control and sudden changes in quantities offered. A stable and slowly growing demand is the best possible prospect for use as a commodity.

All representatives of the Cryptogams belong to one or more other commodity groups of the Prosea handbook, as can be seen in Table 1. These groups are listed as "secondary uses" in the basic list of species and commodity grouping (Jansen et al., 1991).

Grouping of Cryptogams

The Cryptogams in Prosea volume 15 will be treated in the following subvolumes:

- 15(1) Algae:

blue-green algae (Cyanophyta)
brown algae (Phaeophyta)
red algae (Rhodophyta)
green algae (Chlorophyta)

- 15(2) Ferns and fern-allies:

ferns
clubmosses
horsetails
mosses

- 15(3) Fungi and bacteria:

fungi (all main groups)
lichens
bacteria

Table 1. Cryptogams arranged according to their use.
Commodity groups	Algae	Ferns	Mosses	Fungi	Bacteria	Lichens
Dye and tannin-producing plants	x			x
Forages	x	x
Timber trees		x
Vegetables	x	x	x	x	x	x
Plants yielding non-seed carbohydrates	(x)	x		x	x
Auxiliary plants	x	x
Medicinal and poisonous plants	x	x	x	x	x	x
Spices	x			x	x
Vegetable oils and fats		x?
Stimulants	x			x	x
Fibre plants		x
Ornamental plants		x		x

Note: x = used, - = not used, blank = no data.

Algae: definition and delimitation

The designation "Algae" can be applied to all organisms containing the pigment chlorophyll a, except all land plants, i.e. the mosses, ferns and fern-allies and all Spermatophyta. Although the term "Algae" does not cover an accepted taxon, it is still the only available term that can be used to include all of these photosynthesizing organisms.

The algae form a group containing many different taxa, with very different uses and which grow in diverse habitats. In the broadest definition of the Algae organisms that have probably secondarily lost the ability to photosynthesize and their photosynthesizing pigments may also be included. These non-photosynthesizing organisms, however, are not included in the present Prosea subvolume 15(1).

In Prosea subvolume 15(1) on Algae the following taxonomic groups will be covered (Silva et al., 1996; van den Hoek et al., 1995):

Cyanophyta (= Cyanobacteria), with representatives of the families Mastigocladaceae, Nostocaceae and Phormidiaceae;
Phaeophyta, with representatives of the families Chnoosporaceae, Cystoseiraceae, Dictyotaceae, Sargassaceae and Scytosiphonaceae;
Rhodophyta, with representatives of the families Bangiaceae, Bonnemaisoniaceae, Caulacanthaceae, Delesseriaceae, Galaxauraceae, Gelidiaceae, Gelidiellaceae, Gracilariaceae, Halymeniaceae, Hypneaceae, Liagoraceae, Rhizophyllidaceae, Rhodomelaceae, Rhodymeniaceae and Solieriaceae;
Chlorophyta, with representatives of the families Caulerpaceae, Cladophoraceae, Codiaceae, Halimedaceae, Monostromataceae, Polyphysaceae, Selenastraceae, Siphonocladaceae, Ulvaceae and Valoniaceae.

Role of algae

Macroalgae, microalgae and their importance

Economic algae are either marine macroalgae (seaweeds) or freshwater and marine microalgae. Commercially interesting microalgae are often either blue-green algae (Cyanophyta) or members of the unicellular green algal genera Chlorella Beij. and Dunaliella Teodor. Commercial resources of algae are often only minor components of the total standing crop of an aquatic flora. These amounts could be improved by cultivation, to the extent that amounts of material under cultivation could far exceed the natural standing stocks. It has been stated that, as a whole, seaweed resources are not greatly exploited (Michanek, 1975). Only about 3.5 million t of seaweeds are used, out of a total biomass which is probably 100 times larger (Jensen, 1993).

Macroalgae

Of the marine algae 107 genera and 493 species have some economic value; mainly macroalgae are used extensively (Tseng, 1981b). The earliest records of the occurrence of Porphyra C. Agardh and its food value appeared in books in China published in the years 533-544 A.D. One thousand years ago the Chinese already regarded Porphyra as a delicacy to be presented to the emperor annually (Tseng, 1981a). Several surveys of useful seaweeds have been published (Chapman, 1950, 1970; Hoffmann, 1938; Levring et al., 1969; Sauvageau, 1920; Tressler, 1923). In recent years lists of useful seaweeds have also been made available (Arasaki & Arasaki, 1983; Bonotto, 1979; Tokuda et al., 1987). Few lists also contain vernacular names (e.g. Calumpong & Meñez, 1997; Ganzon-Fortes, 1991; Hatta et al., 1993; Zaneveld, 1955, 1959).

Microalgae

Freshwater microalgae and marine microalgae can be grown in closed systems (including heterotrophic systems), tanks, or shallow ponds for the production of health food ("nutraceuticals"), carotenoids, proteins, fine chemicals, or for medicinal uses. Several microalgae are particularly used for the hatchery cultivation of marine molluscs and prawns (de Pauw et al., 1984; Laing & Ayala, 1990; Yúfera & Lubián, 1990). The difficulty of producing economically large quantities of microalgal feeds is currently one of the major impediments to the further development of the aquaculture industry (Apt & Behrens, 1999; Gladue & Maxey, 1994). Microalgae are a genetically very diverse group with a wide range of physiological and biochemical characteristics. They comprise a large, almost unexplored group of organisms, and thus provide a virtually untapped source of products and possibilities for commercial application (Radmer & Parker, 1994). The blue-green algae Arthrospira (Spirulina) platensis Gomont and A. (S.) maxima Setch. & N.L. Gardner are at present the richest known sources of plant protein (Jassby, 1988a). In addition, they have the highest vitamin B12 content of any unprocessed plant or animal and relatively high contents of β carotene (Jassby, 1988a; Mshigeni, 1982). In relation to this carotene product, however, the species of Arthrospira Stizenb. ex Gomont are outstripped by another genus of microalgae: Dunaliella (Jassby, 1988a; Moulton et al., 1987). Free-living nitrogen-fixing blue-green algae, as well as the endosymbiotic nitrogen-fixing blue-green algae growing in the Azolla water fern are used as fertilizers for rice fields. These algae function as a "green manure" (Faridah Hanum & van der Maesen, 1997; Metting et al., 1988, 1990; Mshigeni, 1982).

The commercial significance of most other microalgae has been small up to the present, although many show much potential (Apt & Behrens, 1999; Radmer & Parker, 1994; Yamaguchi, 1996). The costs associated with growing and harvesting microalgae and, where necessary, extraction and purification of the product may prevent the success of many initiatives for nutritional uses from the outset (Regan, 1988). Nevertheless, the use of microalgae as sources of valuable chemicals is now established and it is assumed that the next few years will see a continued expansion of the range of commercially available microalgal products (Borowitzka, 1994).

Importance

In terms of utilization of algae, several commodities are of main interest: vegetables (direct human consumption), producers of phycocolloids, raw materials for feed and fertilizer and for medicinal or pharmaceutical use. In contrast, the extraction of soda and potash (in the 18th Century) and iodine, which was a thriving industry in the early parts of the 19th Century, is no longer of economic significance.

Algae as vegetables Specimens used as vegetables (or as material for medicinal or pharmaceutical use) are usually collected from nature (Hatta et al., 1993). This small-scale use results in offering the fresh specimens for sale at the local market. In South-East Asia especially, coastal inhabitants of the Philippines, Malaysia and Indonesia consume seaweeds. Only occasionally are freshwater macroalgae used as food (Arasaki & Arasaki, 1983).

Phycocolloids Production of phycocolloids is occasionally possible in small-scale ventures. In these cases washed-up specimens collected from the beach can be used, as well as material collected from wild populations or from cultivated stock. Those seaweeds can be sold as raw material, often washed and bleached, to be used for the home production of crude phycocolloids for the preparation of puddings and cakes, or as raw (often untreated) material for animal feed or fertilizer. Often small-scale traders buy dried seaweeds from collectors and farmers for export to other countries or to factories for phycocolloids. The cultivation of algae for phycocolloids takes place in family-owned seaweed farms or in larger complexes owned by cooperatives, exporters or factories.

Other uses Biomass from macroalgae can be prospected to provide environmentally and economically feasible alternatives to fossil fuels and can also be functional in pollution abatement (Gao & McKinley, 1994).

Biological and chemical products and uses

Phycocolloids

Various seaweeds are used to manufacture phycocolloids including agar, carrageenan and alginate. These water-soluble non-crystalline polysaccharides can be extracted from cell walls. They are variously designated as seaweed colloids, hydrocolloids, phycocolloids or seaweed gums. They are not found in land plants and are specific to seaweeds (Heyraud et al., 1990; Lewis et al., 1988; Tseng, 1945, 1946). However, polymers with similar properties are extracted from higher plants and all compete with pectin, gelatin and carboxymethyl cellulose (CMC) in the food additive hydrocolloid market (Bixler, 1996; Lewis et al., 1988).

Phycocolloids are extracted from red and brown algae and are included in many industrial processes. They are used to thicken aqueous solutions, to form gels or jellies of various degrees of firmness, to stabilize oil-in-water emulsions and to stabilize products such as ice-cream and whipped toppings (Guist, 1990; McHugh & Lanier, 1983). Without the phycocolloids, several biotechnological advances, many of which have the potential of being beneficial to mankind, would not have been possible (Renn, 1990). The mechanisms of gel formation differ widely for agar (heating/cooling), carrageenan (addition of monovalent ions) and alginate (addition of bivalent cations). These different properties are used in different applications in prepared food (Guist, 1990).

Phycocolloids are characterized by formation of strong and transparent gels with different viscosity, solubility and reversibility of gel formation and often by a high gel-melting temperature. Their physical behaviour (conformation of chains in solution, solubility, ion-exchange properties, gelling, viscosity) and the resulting biopolymer engineering have been described (Heyraud et al., 1990; Lewis et al., 1988; Smidsrød & Østgard, 1991). The gels usually have no acid sensitivity; they are natural and of plant origin; they have non-caloric properties, the ability to assimilate and enhance flavours and are easy to measure and use.

Agar

Agar is a hydrophyllic colloid extracted from a number of red algae, which are often collectively designated as agarophytes. Of the total global agar production in 1994, about 35% came from members of the Gelidiales (e.g. Gelidiella Feldmann & Hamel, Gelidium J.V. Lamour. and Pterocladia J. Agardh); most other agar came from members of the Gracilariales (e.g. Gracilaria Grev., including Gracilariopsis E.Y. Dawson) (Armisén, 1995; Armisén & Galatas, 1987; Chapman, 1970; Indergaard & Østgard, 1991; Lewis et al., 1988; Lobban & Harrison, 1994; Pérez et al., 1992).

Structure

Chemically, agars consist of a mixture of polysaccharides, viz. polymers which are chains of joint units of galactans. In agar the average sulphate content of these polymers is between 1.5 and 6%, while there are lesser quantities of pyruvic and guluronic residues present, varying from source to source (Armisén, 1991; Cosson et al., 1995; McHugh & Lanier, 1983). The backbone structure of both agars and carrageenans is based on repeating galactose and 3,6-anhydrogalactose residues, or is formed by aragan: alternating units of D- and L-galactopyranoses (Armisén, 1991; Craigie, 1990; Knutsen et al., 1994). Another extreme backbone structure is agarose, in which all 4-linked α-L-galactose residues are in the 3,6-anhydro form. A letter code for a shorthand nomenclature system for galactan building units and sequences, using L (for L-galactose) and LA (for anhydro-L-galactose), is considered typical for agars.

The agar group (agarocolloids) differs from the highly sulphated carrageenans by having 4-linked α-L-galactose as well as D-galactose. High content of 3,6-anhydro-L-galactose and low degrees of substitution favour gelation of agar. Fractionation into a neutral good-gelling fraction lacking sulphate and other charged groups (agarose), and a residual fraction with poor gelling properties (agaropectin) is well established commercially, but the two extremes are connected to each other by many intermediates (Craigie, 1990; Pérez et al., 1992; Smidsrød & Christensen, 1991). High gel strength is usually due to the presence of longer chains of polymers in agar samples.

Ionized agarose, where molecules are highly sulphated, is dominant in some Gracilaria, producing a flexible and elastic gel which can not, however, meet all specifications for food grade agar (Cosson et al., 1995). Treatment of the Gracilaria phycocolloid with sodium hydroxide (alkaline hydrolysis), which transforms the agaroid into real agar, makes a product that meets the specifications required (Armisén, 1995). Agar in Gracilaria has a greater tendency to become hydrolyzed during storage, even under favourable conditions. This is not only caused by agarolytic bacteria; even if these organisms are not present, adequately dried and stored warm-water Gracilaria may still undergo a reduction in their agar content over a few months in storage. Gracilaria spp. from colder waters usually have a much greater resistance to hydrolysis but, even so, they are not as resistant to hydrolysis as agar from Gelidium (Armisén, 1995).

Properties

Unique properties of agar are: very strong, stable, brittle, thermo-reversible gel formation in aqueous solution, without the presence of any additives; gelation at temperatures far below the gel melting temperature (= the sol temperature: there the phycocolloid becomes liquid again); resistance to high temperatures (a 1.5% aqueous solution gels between 32 and 43 °C and does not melt below 85 °C); usability over a wide pH range from 5 to 8; capacity to hold large amounts of soluble solids, flavours and colours; a maximum ash content of 5% (normally maintained between 2.5-4%) (Armisén & Galatas, 1987). The difference between gel and sol temperatures is called hysteresis. This difference can be as high as 50°C and is only displayed by agar (Lewis et al., 1988). While agar is the most commonly accepted term, in French-, Spanish- and Portuguese-speaking countries it is also called "gélose" or "gelosa" and in Japan the dry product is called "kanten".

Uses

Agar (commercial code E406), insoluble in cold water but soluble in boiling water, is a major additive in the food industry because of its resistance to high temperatures (it is often used to prevent dehydration in bakery products), its rigid gel (in confectionery and canned products), its gelling properties (in marmalade production, but also to prevent meats from becoming mushy and reducing damage in transit of soft meats, permitting the reduction of fat content) and its stabilizing properties (in dairy products). Agar is also often used for viscosity control and is known for its unique application as a culture medium in bacteriology and also for orchids and vegetables. The gel is used for the preparation of medical supportives and is utilized in the manufacture of photographic films, in the print industries and to prepare mould casts for use in sculpture, archaeology and dentistry. Because gel strength varies according to the species of seaweed used as a raw material, processors often use a mixture of seaweeds. Separate uses of agarose can be grouped in the broad categories of immuno-diffusion and diffusion techniques, electrophoresis, chromatographic techniques, immobilized systems technology and special growth media (Renn, 1990). Agarose has great stability and constitutes an inert support of natural origin, modifiable by organic synthesis, with the highest known gelling power among natural colloids (Armisén, 1991; Armisén & Galatas, 1987).

Carrageenan

Carrageenans are formed in the cell walls of some red algae (carrageenophytes), including the tropical genera Acanthophora J.V. Lamour., Betaphycus Doty ex P.C. Silva, Eucheuma J. Agardh, Hypnea J.V. Lamour. and Kappaphycus Doty. In Eucheuma and Kappaphycus, the sporophytes and the gametophytes always contain the same type of carrageenan within each species. This differs to the situation in carrageenophytes from temperate regions, where the life-cycle phases each contain a different type of carrageenan. Although the Malay word "agar-agar" refers to Eucheuma, it is now known that these yield carrageenans rather than agar-type polysaccharides.

Structure

Chemically, carrageenans are polysaccharides, their exact composition, however, varying from source to source. They all are formed by groups of linear D-galactans with varying amounts of 3,6-anhydro-D-galactose with alternating 1,4- and 1,3-linkages and variations in the amount and position of sulphate half-esters. The complex structure of carrageenan is an active field of research (Knutsen et al., 1994; Pérez et al., 1992; Stanley, 1987). Usually three or four main chemical types or "families" of refined carrageenan are distinguished:

Kappa carrageenan, with a rather brittle gel characterized by syneresis, a condition in which water is exuded from the gels by standing, and even more so when squeezed in a press. Originally kappa carrageenan was defined as the fraction which was precipitated by potassium chloride.
Iota carrageenan, with a less brittle and more flexible gel, showing only little syneresis and distinct precipitation by KCl.
Lambda carrageenan, which dissolves in cold water and does not form a gel at all when potassium or calcium salts are added, but provides increased viscosity and suspension capacity in products.
The beta family of carrageenans, a rather new group of carrageenans found in Betaphycus gelatinus (Esper) Doty ex P.C. Silva, Basson & R.L. Moe (= Eucheuma gelatinum (Esper) J. Agardh), is competitive with certain functions of agarose in some biotechnology applications (McHugh, 1996).

The designations beta, kappa, iota and lambda carrageenan for refined carrageenans refer to certain idealized structures with quite different physical properties, although they sometimes occur in mixed structures (Craigie, 1990; Guist, 1990; Heyraud et al., 1990).

Attempts have been made to group the different disaccharide-repeating units of carrageenans into families, but that system omitted many natural complex carrageenans (Craigie, 1990; Knutsen et al., 1994). A new nomenclatural system for red algal galactans has been proposed, in which the backbone structures in the carrageenan group of polysaccharides are separated as carrageenan in its strict chemical sense and as the component carrageenose (Knutsen et al., 1994). Commercial carrageenans are available as stable sodium, potassium, or calcium salts of unstable free acids. These commercial carrageenans are most commonly mixtures of different salts.

Properties

The unique properties of carrageenan include high-quality, highly viscous, thermo-reversible gel formation; protein reactivity (especially with casein); and it can be used together with guar (Cyamopsis tetragonoloba (L.) Taub.) and locust bean or carob seed (Ceratonia siliqua L.) gums (Anonymous, 1979; Glickman, 1987; Stanley, 1987).

Uses

Carrageenans (commercial code E407; for natural grade carrageenan in Europe the code E407a is applied) are the phycocolloids with by far the widest application in food industry (Anonymous, 1998; Bixler, 1996). They are mainly used as stabilizing, thickening, suspending and gelling agents in food such as dietary and baby foods and also in canned pet-foods, syrups, fruit drink powders and frozen concentrations, milk-based products, chocolate, pasta sauce, artificial whipped toppings, imitation coffee creams and pre-cooked, packaged meats. Carrageenans are also used in non-food products: toothpaste, cosmetics, solid gel-type air fresheners and textile paints. A preferred name in the Philippines for the locally produced carrageenan is "natural grade carrageenan" which is sometimes called "Philippines natural grade" or "PNG carrageenan" because of its country of origin. Other commonly used names are "alkaline carrageenan flour" (ACF), "alkaline-modified carrageenan" (AMC), "alkali-modified flour" (AMF), "alternatively refined carrageenan" (ARC), "alkaline-treated cottonii" or "alkali-treated cottonii" or "alkali-treated carrageenophyte" (all as ATC), "natural washed carrageenan" (NWC), "processed Eucheuma seaweed" (PES), "semi-refined carrageenan" (SRC) and "seaweed flour" (SF) (Anonymous, 1998; McHugh, 1996; Neish, 1990). In a recent survey "SRC" is used as an acronym for the total of alkali-treated chips and semi-processed powder, while "PNG" is exclusively used for the semi-processed powder alone (Anonymous, 1998). Natural grade carrageenan is not universally accepted for classification as carrageenan, although the American Food and Drugs Administration has done so. In the European Union, however, natural grade carrageenan was mainly excluded from the arbitrary definition of carrageenan as having a maximum 2% content of acid-insoluble matter (Bixler, 1996; Luxton, 1993). In the European Union therefore it has received the official separate designation "PES = Processed Eucheuma seaweed" (Anonymous, 1998; Bixler, 1996).

Alginate

Algin is often used as the name for the soluble sodium salt of alginic acid, while these and other salts and esters together are called alginates. These products are found in the cell walls of brown algae, including the tropical seaweed genera Hormophysa Kütz., Hydroclathrus Bory, Sargassum C. Agardh and Turbinaria J.V. Lamour. (Painter, 1983; Trono & Ganzon-Fortes, 1988). Most commercial alginate is produced from alginophytes occurring in temperate or even colder waters. Alginic acid itself is insoluble in water, but it swells when water is added. Alginates are also produced as microbial polysaccharides by certain bacteria (Smidsrød & Christensen, 1991).

Structure

Alginates are polysaccharides of which the exact composition varies from source to source. They form a family of linear binary copolymers containing 1,4-linked β-D-mannuronic acid (M) and its C-5-epimer α-L-guluronic acid (G). The distribution of M and G in alginate chains gives rise to three different block types, namely blocks of poly-M, blocks of poly-G and alternating blocks of the type M-G-M-G. This composition can be described in detail by using nuclear magnetic resonance (NMR) techniques (Jensen, 1995; Smidsrød & Christensen, 1991).

Gel formation or binding is an important application of alginates. A solution of 1-2% sodium alginate will stiffen to a gel by addition of calcium ions (50 mM) or other bivalent ions (Ba2+, Pb2+, Sr2+, etc.). The bivalent ions bind the alginate chains together in a three-dimensional gel network in accordance with the "egg box" model (Heyraud et al., 1990; Jensen, 1995). Alginate gels have various strengths, largely dependent on their content of polyguluronic acid blocks (Indergaard & Østgard, 1991). The alginate content of the warm-water seaweeds is usually somewhat lower than that in algae from other waters. In general the alginate of Sargassum and Turbinaria is of low viscosity but forms good gels. Turbinaria thalli usually have a higher alginic acid content (20-22% of the dry weight) than Sargassum (13-18%) (Pérez et al., 1992).

Properties

Unique properties of alginate are its cold-water solubility of sodium alginate, and its instantaneous calcium reactivity resulting in a highly water-retentive, non-melting, thermo-irreversible chemical gel formation.

Uses

Alginates are used as low-price viscosifiers or thickeners in a wide range of products. They are the most widely used seaweed colloids. The primary food products in which alginic acid and alginates (commercial codes E401-E405) are used include frozen desserts, where they regulate the formation of ice crystals and help to control over-run, providing a smooth, creamy body in products. Alginates prevent products from sticking to wrapping paper, especially bakery products. They are emulsifiers and stabilizers in salad dressings, meat, flavour sauces, canned food and beverages. In dessert gels alginates produce clear, firm, quick-setting gels, suitable for use with hot as well as cold water (Glicksman, 1987). In non-food industries alginates are also very often used in paint, cotton textile, plastics, vulcanite fibre, linoleum and imitation leather, waterproof products, glass-production and etching industries.

Chemical products

Several high-value fine chemicals are produced on the basis of microalgae grown in mass culture (Borowitzka & Borowitzka, 1988). The products derived from these microalgae include carotenoids, other pigments, fatty acids, sterols, vitamins and bioactive compounds (Apt & Behrens, 1999; Borowitzka, 1994).

Nutritional aspects

Nutritional value of marine macroalgae

Although marine macroalgae were known and prized for nutritional purposes from very early times in the Orient, most of them have rather low digestibility, containing many unfamiliar polysaccharides and minerals. It is sometimes stated that a regular intake of seaweed will help develop an intestinal bacterial flora capable of breaking down the polysaccharides, but probably the human body does not digest phycocolloids at all or only in small quantities of less than 10% (Armisén, 1991; Mori et al., 1981).

Nevertheless, major uses of seaweeds are found in human nutrition, although seaweeds can not function as a basic source for proteins or lipids, neither in man nor animals (Jensen, 1993). In the green algae, which store starch in the same way as most land plants, cell walls contain highly resistant polymers of glucose, mannose and xylose (Painter, 1983). Seaweeds are very "filling", however, which make them good diet foods. Their soft cell walls regulate bowel action without damaging intestinal walls (Indergaard & Minsaas, 1991). In terms of amino acids, seaweed protein is similar to that of egg white and legumes (in %), while sea-vegetables are low in fats but contain considerable amounts of vitamins and minerals (Arasaki & Arasaki, 1983).

Although energy values of various seaweeds are known, these values can not be thought of as physiological energy until the digestibility, and thus bio-availability of the various compounds, has been determined (Indergaard & Minsaas, 1991; Paine & Vadas, 1969; see, however, Booth, 1964). Information about algal products, e.g. seaweed meal as fodder supplement, is mainly based on uses in Europe, while detailed reports on the use of other seaweed species are few (Indergaard & Minsaas, 1991; Wong & Leung, 1979). Differences in the phenolic content of various algae seems vital, low contents favouring the protein digestibility of green and especially red algae at the expense of the browns.

Marine macroalgae as human food

Terrestrial vegetables are eaten because of their mineral and vitamin contents and their taste. In addition seaweeds may also bring colour, flavour, texture and chewiness, which make them delicacies (Arasaki & Arasaki, 1983; Madlener, 1977; Trono & Ganzon-Fortes, 1988). Some red algae have a reasonably high protein content. Algal phycocolloids are officially accepted as additives for human foodstuffs (Indergaard & Østgard, 1991).

The addition of seaweed meal as a source of iodine and other minerals to the diet of fast-growing children and pregnant women may be advisable even in countries with otherwise rationally balanced diets (Indergaard & Minsaas, 1991). Possibly a better means of introducing these elements into the diet might be to use seaweed meal as animal feed or as a fertilizer for the plants whose products are eventually consumed by humans.

In general, marine algae are rich in vitamins A and E. Niacin and vitamin C content are about the same in all groups of marine macroalgae. Concentrations of vitamins B1, B12, pantothenic acid, and folic and folinic acids are generally higher in the green and red algae than in brown seaweeds. Animal organs, especially liver, which are richest in vitamin B12, contain a lower amount (in g dry-weight basis) of this vitamin than some of the green algae. The concentrations of algal B vitamins are, in fact, comparable to those in many common fruits and vegetables. Extraordinary amounts of vitamin A are generally found in the marine algae, occasionally much more than is present even in cod liver oil (Madlener, 1977). For tropical areas, the richest source of vitamin C from algae would be Sargassum spp., which are already traditionally consumed in a number of countries including Indonesia, Malaysia, the Philippines and Vietnam (Michanek, 1979; Trono & Ganzon-Fortes, 1988). Some algae from Indonesia have been screened for active substances, mainly steroids, but also carbohydrates (Harlim, 1986). "Wild" populations of inland algae (microalgae) are only occasionally collected for use as food (Jassby, 1988a).

Marine macroalgae as feed in aquaculture

In areas where aquaculture is an important industry, seaweeds could be applied more regularly as a feed for aquatic animals. For example, Gracilaria can be grown in ponds with milkfish and shrimp. These animals graze on epiphytes on the Gracilaria, and eventually on the red alga itself if they are left in the pond for long enough or their numbers increase out of balance with the seaweed biomass (McHugh & Lanier, 1983).

Production of milkfish in fish ponds (in Indonesia: "tambaks") is best when the bottom of the production ponds is covered by a thick mat of blue-green algae such as Chroococcus, Gomphosphaeria, Lyngbya, Microcoleus, Oscillatoria, Phormidium and Spirulina spp., as well as by diatoms. This algal periphyton constitutes the main food of cultured milkfish, but filamentous green algae may also be eaten (Bardach et al., 1972). The biological complex of blue-green algae, diatoms, bacteria and various animals, which is typical of well-managed milkfish ponds, is known as "lab-lab" in the Philippines and as "kelekap" in Indonesia (Benitez, 1984; Chong et al., 1984). Red seaweeds of the genus Gracilaria can also be used as food for milkfish, but the algae are unable to withstand salinities below 5‰ (Bardach et al., 1972). It is also possible to feed molluscs on these Gracilaria seaweeds obtained from phycoculture. When labour costs are too high to make enough profit from preparing Gracilaria thalli for agar production, farmers may prefer to use these algae as a direct food for molluscs, as has been the case in Taiwan (Ajisaka & Chiang, 1993).

Microalgae as human food

The blue-green alga Arthrospira (Spirulina) platensis, which occurs in a great variety of inland waters, is renowned as being one of the richest protein sources in the world. The alga contains significant amounts of vitamin B12, other B-complex vitamins, vitamins A and E, β carotene and the essential mineral elements iron, phosphorus, magnesium, zinc and selenium (Mshigeni, 1982; Switzer, 1982; Vonshak, 1997). However, due to the production of certain toxins use of cyanobacteria as food will always entail a degree of hazard, until adequate health standards for production and marketing of cyanobacteria for single-cell protein are adopted and observed (Gorham & Carmichael, 1988).

The potential for using microalgae to combat current problems of famine and malnutrition has been reviewed. Attempts to bring small-scale microalgal production to villages for application in integrated village systems are promising (Jassby, 1988a). Arthrospira has little value as an energy source, but is interesting as a protein source, especially among malnourished human populations (Van Khuong, 1990). The palatability of small amounts is not the problem, but in larger quantities the strong colour, odour and taste are often not acceptable as a major food source (Jassby, 1988a).

Other freshwater algae, such as the unicellular green algae of the genus Chlorella, also produce a very good protein source. Its protein is especially rich in the amino acids lysine, threonine and tryptophane, which are generally poor in cereal proteins (Lee & Rosenbaum, 1987). However, Chlorella is not accepted as an attractive new food item. It is mainly available in health-food shops and in the form of chlorophyll pills, or added in powder form to various kinds of food products. In this form it increases significantly the level of vitamins and lipids without affecting the palatability of the food (Mshigeni, 1982). Members of Dunaliella are occasionally used as a protein supplement in bread (Borowitzka & Borowitzka, 1988).

Microalgae as feed in aquaculture

Most freshwater algae, as well as marine microalgae, are too small to be attractive as potential sources of human food or animal fodder, although they are indispensable as live feed in aquaculture (de Pauw et al., 1984). These feed microalgae are especially used for larvae of commercially grown crustaceans, molluscs and fish or as feed for zooplankton that in turn will be used as feed for other larval stages and juvenile fish. Several microalgae are grown for these purposes in commercial growth media (Benemann, 1992; de Pauw & Persoone, 1988; Gladue & Maxey, 1994; Shamsudin, 1992). Comparative studies of the most widely used microalgae in hatcheries worldwide have shown that their nutritional quality varies considerably (Apt & Behrens, 1999). Much of this variation can be explained by major differences in fatty acid composition, particularly with respect to the proportions of long-chain polyunsaturated fatty acids. Recent efforts have focused on the use of algal oils containing long-chain polyunsaturated fatty acids (LCPUFAs) as nutritional supplements (Apt & Behrens, 1999). The most prominent of these are the omega-3 LCPUFAs docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA). DHA is a dominant fatty acid in neurological tissue and is also abundant in heart muscle tissue and sperm cells. It is an essential nutrient during infancy. Humans are not capable of synthesizing DHA themselves. Thus, adequate supplies of DHA must be obtained from dietary sources. A number of algal groups have been identified that produce high levels of these compounds. The component EPA, however, can significantly lower growth rates of humans and animals and can also cause other developmental difficulties. Purified algal oil containing EPA is not commercially available (Apt & Behrens, 1999).

Green algae are mostly less suitable as feed, although Chlorella and Dunaliella are often used as feed for fish larvae in commercial fish farming. Several diatoms, however, are more satisfactory in many respects. Nutritional deficiencies in a diet for organisms in aquaculture can be avoided by using mixed algal diets (Volkman et al., 1989). Gross chemical and fatty acid composition of a number of tropical microalgae has been determined (Renaud & Parry, 1994; Renaud et al., 1994; Shamsudin, 1992). The greatest breakthrough in shellfish production would be the production of the right microalgae in the right quantities at the right time (Doty, 1979). Heterotrophic growth may be the solution (Apt & Behrens, 1999; Gladue & Maxey, 1994). The prospects of the green freshwater microalga Haematococcus pluvialis Flot. for the production of the keto-carotenoid astaxanthin, a natural food and feed colourant often used in the aquaculture industry, are promising (Borowitzka, 1994; Ding et al., 1994).

Medicinal and toxic aspects

Medicinal uses

The earliest information on seaweed utilization for medicinal purposes originate from the Chinese "Materia Medica" of Shên-nung, dating from 2700 B.C. (Hoppe, 1979). In many areas numerous algae are used as medicaments, especially in coastal countries. They are used in folk medicine against goitre, nephritic diseases, helminths, catarrh, etc. Several algal species contain substances of pharmaceutical interest of which the active compounds are not yet characterized. In others, however, the active principle compound has been identified like a mixture of kainic and allokainic acids responsible for vermifugal properties in the red alga Digenea simplex (Wulfen) C. Agardh (Arasaki & Arasaki, 1983; Chapman, 1970; Michanek, 1979). Substances with anticoagulant properties, with cytotoxic activity (anticancer or antineoplastic activity), antibiotic, antifungal, antiviral or antioxidant activity are known to occur in some seaweeds, as are haemagglutinins (Chapman, 1970; Fujimoto, 1990; König, 1992; Mabugay et al., 1994; Matsukawa et al., 1997; Michanek, 1979; Neushul, 1990; Pesando, 1990; Reichelt & Borowitzka, 1984; Santos & Guevara, 1988; Shiomi & Hori, 1990; Wong et al., 1994). Antibiotic activity is not present at all times and even samples of the same species, when collected from different localities, may give different results (Padmakumar & Ayyakkannu, 1997).

Fucoidan, a polymer of fucan sulphate, found in members of the Phaeophyta, contains a fairly high percentage of sulphate ester. This substance is known to have the same anticoagulant effect as heparin and a 1% aqueous solution of fucoidan obtained from a Sargassum sp. has shown greater antithrombic activity than the same concentration of heparin (Arasaki & Arasaki, 1983). Fucan sulphate, however, can not yet be stored satisfactorily; even deep-frozen material is not stable (Nishino & Nagumo, 1991). The path from discovery to commercial production of a drug is long and costly (Baker, 1984). Each investigated marine organism may yield new natural products and/or new or known compounds with biological activity (König, 1992).

Compounds that are toxic for the freshwater snail Biomphalaria glabrata (vector for schistosomiasis) have been found in marine algae, whereas some anti-malarial activity has been detected in compounds isolated from the brown algal genus Dictyota J.V. Lamour. and other seaweeds (König, 1992; Subramonia Thangam & Kathiresan, 1991).

Phycocolloids

The role of phycocolloids in pharmaceuticals as thickening or binding agents is similar to that in food. However, this role must be separated from their biochemical action, particularly as oligosaccharides. Only in a few instances may the phycocolloid component be considered as the active therapeutic agent (Chapman, 1979; Güven et al., 1991; Indergaard & Østgard, 1991).

Agar is used in emulsions with liquid paraffin for the treatment of constipation. The gelling power of agar is so high that it is generally used only in low concentrations. For this reason the ingested quantities are very small and its caloric contribution is negligible. Thus agar can be used in special diet food (Armisén & Galatas, 1987).

Aqueous extracts of several red algae, as well as carrageenans, have been recorded as active against retroviruses (Neushul, 1990). Some carrageenans show anticoagulant, fibrinolytic or antiaggregant activity. Such activities, however, have never been reported in alginates (Güven et al., 1991). Alginates, however, have strong ion-exchange affinities for bivalent cations (Tsytsugina et al., 1975). It has been proposed that these phycocolloids could be used to cleanse human bodies of unwanted heavy metals (Indergaard & Minsaas, 1991; Tanaka et al., 1972; Tanaka & Stara, 1979). If dairy products, cereals, fish or meat may be contaminated, the uptake of strontium especially could be prevented by the addition of alginate to food. Alginic acid has the ability to form insoluble complexes with strontium, which can pass through the intestines without being absorbed into the body. Alginates can even be used to reduce strontium already deposited in the bone and can also be used to inhibit absorption of lead, barium, cadmium and zinc (Michanek, 1979; Takana et al., 1972).

Calcium/sodium alginate is also produced as a thread in order to manufacture a woven fabric for wound healing. The threads are woven as calcium alginate and then modified to give a mixture of sodium and calcium alginates, resulting in a product that gels on contact with the wound and one that has good haemostatic qualities. This type of fabric is available as first-aid dressings and is particularly useful in the treatment of burns (Dixon, 1986).

Alginates are also used in pharmaceutical tableting, dental impressions, bacterial cell encapsulation and enzyme immobilization (Lewis et al., 1988). The use of alginate in slow-release systems for pharmaceuticals is developing rapidly (Jensen, 1995). Combinations of agar and alginate show promising results for dental uses (Kasloff, 1990).

Iodine

A bulk use of seaweeds as a food material with obvious therapeutic benefits (nutraceuticals) is found in the brown algae which contain iodine which combats endemic goitre. Products made from Laminaria japonica Aresch. are widely used for such purposes in China (Michanek, 1981). Endemic goitre may also possibly be eradicated by public health information and use of seaweed food, especially in Indonesia and Malaysia (Michanek, 1979). Excess intake of iodine may, however, also produce fatal effects in both humans and animals. Goitre (thyrotoxicosis) has been demonstrated as a consequence of the high intake of kelp products by children in Japan and in adults in Australia and Finland (Liewendahl, 1972; Wheeler et al., 1982; Zuzuki, 1965).

Poisonous macroalgae

Until recently, only very few macroalgae had been recorded as more or less un-wholesome, especially some Caulerpa spp. and Turbinaria ornata (Turner) J. Agardh (Russell, 1984). Caulerpa spp. have occasionally been mentioned as producing neurotoxins (Lemée et al., 1993; Paul & Fenical, 1986; Ribera et al., 1996; Schantz, 1970). Turbinaria is recorded as creating gastro-intestinal distress in humans (Russell, 1984). In comparison with the more than 1200 toxic marine organisms that were included in Russell's review of marine poisonous organisms, one must conclude that the macroalgae, as a group, are more or less non-toxic (Indergaard & Minsaas, 1991). A well-documented case where people died after eating the red alga Gracilaria tsudai (I.A. Abbott & I. Meneses) I.A. Abbott on Guam, however, indicates that this alga may form relatively high levels of previously undescribed toxic compounds at some stages of its life cycle (Yasumoto, 1993). The occurrence of toxic substances seems not related to the neurotoxins causing the marine food poisoning known as "ciguatera", which is associated with toxins formed by the dinoflagellate alga Gambierdiscus toxicus Adachi & Fukuyo and accumulated in fish and molluscs (Stadler, 1993; Steele, 1993). The latter dinoflagellate, however, may contaminate macroalgae, to which it strongly adheres (Nakahara et al., 1996; Saint-Martin et al., 1988). Around Ambon (Indonesia) these dinoflagellates occur attached to Sargassum, Turbinaria and Halimeda spp. (Sidabutar, 1996).

Although it is suggested that consuming large amounts of seaweed may be a cause of human arsenic poisoning, in most algae, arsenic is in a form that is not assimilated (Norman et al., 1988; Walkiw & Douglas, 1975).

Cyanophytes

There are several blue-green algae (Cyanobacteria) that are known to be poisonous, especially the genus Lyngbya C. Agardh ex Gomont (Madlener, 1977). In the microalgae many highly toxic species occur which have not, however, been reported, as having harmful effects on macroalgal cultivation (Correales & MacLean, 1995). Most of these microalgae are not included in the present book of plant resources, except some blue-green freshwater algae that are useful because of their nitrogen-producing capacities. Not all blue-green algae are toxic, however. Arthrospira platensis, which is often used as food or a food supplement for humans, is completely non-toxic. A list has been published of experiments on potential therapeutic applications of Arthrospira (as Spirulina Turpin ex Gomont) as well as a review of public health aspects of microalgal products (Jassby, 1988a, 1988b). The status of microalgae as sources for pharmaceutical and other biologically active molecules has been reviewed (Borowitzka, 1995). Experiments to prepare mosquitocidal cyanobacteria provide an interesting prospect (Stevens et al., 1994).

Other aspects

Fertilizers and soil conditioners

Manual harvesting of beach-cast algae, mainly members of the Phaeophyta, has been carried out since ancient times for spreading on fields as a fertilizer and for soil conditioning, especially in maritime parts of Europe. These and other stranded algae are often the result of proliferation, due to an abundant presence of nutrients, favourable meteorological conditions and accumulation in confined areas (Morand et al., 1991). In the Philippines, in the coastal area of Ilocos Norte (north-western Luzon) the use of brown seaweeds of the genera Hormophysa, Padina Adans., Sargassum and Turbinaria as a fertilizer and soil conditioner is well documented (Fortes et al., 1993; Tungpalan, 1983). A product based on composted Ascophyllum nodosum (L.) Le Jol., a North Atlantic brown alga, has been used successfully in landscaping and reclamation projects. The method used to apply the soil conditioner will depend on the nature of the site. Where topsoil is available, the composted algae are mixed with the soil at a rate of 1.5 kg/m3. However, in many cases no topsoil is available and the seaweed product must be applied to subsoils. If the site is relatively flat, the soil conditioner is worked into the top 5 cm of subsoil at a rate of 75 g/m3, and then appropriate fertilizers and seeds are added using ordinary horticultural techniques. Often, the area to be treated includes steep slopes which are impossible to cultivate using conventional equipment and thus more liable to suffer soil loss due to run-off than flat sites. In tropical regions, heavy rains often make the problem of erosion due to run-off more acute than in the temperate zones. Spraying with a mixture containing composted Ascophyllum, together with clay, fertilizer, seed, a mulch (either cellulose pulp or peat) and water has given satisfactory results, even on bare rock and in tropical countries (Blunden, 1991). Processed seaweed products for crop use are of three kinds:

meals for supplementing soil in large volumes or for blending into defined rooting media for glasshouse crops;
powdered seaweeds; and
liquid extracts and concentrates employed both as root dips (or soil drenches) and as foliar sprays (Menning et al., 1988, 1990).

Several crustose, calcareous red algae of the family Corallinaceae are used as fertilizers and soil-conditioning agents, primarily on acid soils.

The influence of microalgae on soil structure is well documented, although microalgal soil conditioners are not suited for non-irrigated soils (Metting, 1988).

Bio-fertilizers

The use of cyanobacterial bio-fertilizers, especially for growing rice, is promising (Kannaiyan et al., 1997; Venkataraman, 1994). In terms of ultimate nitrogen input in the paddy, algalization is feasible at about one-third of the cost of a chemical fertilizer. Bio-fertilization by blue-green algae can also be done indirectly by using the heterosporous floating aquatic ferns of the genus Azolla. Specialized leaf cavities in the water fern house the cyanobacterium Anabaena azollae Strasb. ex Wittr. (Faridah Hanum & van der Maesen, 1997; Metting, 1988; Metting et al., 1988, 1990). Among the known plant-cyanobacteria symbioses, only the Azolla-Anabaena associations have significant potential as alternative nitrogen source in agriculture, since the symbiont is capable of fixing atmospheric nitrogen at high rates. The utilization of these inexpensive bio-fertilizers has several advantages over chemical fertilizers: they make use of freely available solar energy, atmospheric nitrogen and water, thus utilizing renewable resources. In addition, they are non-polluting and, besides supplying nitrogen to crops, they also supply other nutrients such as vitamins and growth substances and improve the general fertility of the soil by improving the soil structure and increasing the organic matter. The benefits brought about by green manure such as Azolla are long-term, increasing grain yield during several successive crops of rice. Moreover, in low-potassium environments the application has a greater ability to accumulate potassium than does rice. Thus, when the fern decomposes, it acts indirectly as a potassium fertilizer.

Seaweed extracts

Seaweed extracts and suspensions, mainly derived from marine brown algae, are marketed for use in agriculture and horticulture. The effects of these products were traditionally explained by their content of trace elements. However, it has been shown that the amounts of trace elements form an insignificant proportion of the annual requirements of a crop. Consideration was also given to the presence of cytokinins, a diverse group of plant hormones. Results of research in this direction are not yet conclusive, although experiments in the Philippines provided good results, i.e. better growth and increased production in terrestrial crops (Fortes et al., 1993; Montaño & Tupas, 1990). There is, moreover, a sufficient body of information available to show that the use of seaweed extracts is beneficial in certain cases, even though the reasons for the benefits are not fully understood (Blunden, 1991). A survey is available of effects of commercial seaweed products on growth of plants and of cytokinins in commercial seaweed preparations (Metting et al., 1990).

Cosmetics

Several algal products are used as components of cosmetics. These include gelling substances (agar, alginates, carrageenans), algal flour and ground algae. For direct use, algal meal sachets for immersion in a bathtub are produced, as well as bath salts with algae and algal pastes to be used in thalassotherapy institutions (Arasaki & Arasaki, 1983).

Other uses

The concept of marine farms as a source of fuel was tested in the United States (Bird et al., 1990; Chynoweth et al., 1987; Flowers & Bird, 1990; Neushul, 1987; North, 1980, 1987). It is difficult, however, to attain economic profitability where energy is the only aim, although international agreements on CO2-reduction may change this conclusion (Gao & McKinley, 1994). Some reviews suggest that microalgae show great promise for the production of "biodiesel" liquid fuel. Others suggest that the CO2-binding activities may be of influence on the global climate, and similarly that the large-scale cultivation of macroalgae might be used to counteract coastal eutrophication (Jensen, 1993; Norton et al., 1996). Even more success can be expected from integrated multi-use approaches, including biomass-transformation methods and use as fertilizer, resulting in products like useful chemicals, composts and biogas apart from more well-known uses as vegetables and as sources of hydrocolloids (Morand et al., 1991). Seaweeds, as well as certain microalgae, are particularly suited for the purification of nitrogen-rich domestic and urban sewage, and also for agricultural and some industrial waste effluents (de la Noüe et al., 1992; Kumaran et al., 1994; Lincoln & Earle, 1990; Oswald, 1988a; Schramm, 1991).

The accumulation and detoxification of toxic metal elements by algae also suggest promising aspects if it were to be applied to biological detoxification and control of these elements in natural waters or in industrially polluted waters (Maeda & Sakaguchi, 1990). Metal recovery in industrial applications is also feasible (Greene & Bedell, 1990).

Production, economic value and export

Production

Access and abundance of seaweed resources are two critical factors determining their commercial viability. Other factors determining viability include the costs of cultivation and harvesting (labour and/or equipment), drying, transportation, chemicals, water supply and environmental measures (McHugh, 1991).

The following taxa of seaweeds were cultivated in South-East Asia around 1973 (FAO, 1974): Caulerpa racemosa (Forsk.) J. Agardh, Chaetomorpha antennina (Bory) Kütz., C. crassa (C. Agardh) Kütz., Cladophora spp., Enteromorpha compressa (L.) Nees, Eucheuma edule J. Agardh (probably partly Betaphycus gelatinus and partly E. serra (J. Agardh) J. Agardh), E. denticulatum (Burm.f.) Collins & Herv. (as E. spinosum J. Agardh).

Other seaweeds have been added recently as cultivated organisms: Caulerpa lentillifera J. Agardh (this is probably the correct identification of most cultivated Caulerpa racemosa), Enteromorpha clathrata (Roth) Grev., E. intestinalis (L.) Nees, Gracilaria spp., Kappaphycus alvarezii (Doty) Doty ex P.C. Silva, K. striatus (F. Schmitz) Doty ex P.C. Silva.

Until 1995 the Food and Agriculture Organization (FAO) published data on world production of all seaweeds together, thus no separation was made between data from phycoculture and from catches from natural populations. More recently these separate data have become readily available (Tables 2 and 3).

Usually FAO Fishery Statistics give seaweed quantities in metric t (wet weight). For industrial use, however, statistics are usually expressed in "dry weight". This is the mass of the seaweeds after it has been dried by natural means. These dried seaweeds usually contain about 20% moisture, but in Eucheuma and Kappaphycus, the main sources of carrageenan, buyers prefer 35% moisture for shipping convenience (McHugh, 1990). The fresh weight of seaweeds consists of 75-90% water. Of the remaining "true" dry weight, about 75% is organic matter and 25% mineral ash, consisting mainly of K, Na, Mg and Ca ions (Lüning, 1993). A conversion of dry weight versus wet weight is often necessary. Red algae especially shrink considerably during drying. The prices of dried and baled red seaweeds (in dry metric t) are thus distinctly higher than those for the fresh and wet product. The global prices for red algae are mainly influenced by the high prices and large amounts of Porphyra spp. produced in East Asia, while the high price for "miscellaneous aquatic plants" can not be explained on the basis of the available data.

Table 2. World production of seaweeds by phycoculture (t wet weight).
	Production
	1986	1990-1992	1993-1995	1996	1997
World
seaweeds total	3 400 089	4 599 520	6 789 656	7 166 780	7 241 449
Phaeophyta	2 269 880	3 230 676	4 541 362	4 909 269	4 978 402
Rhodophyta	888 246	1 109 761	1 571 875	1 750 505	1 758 348
Chlorophyta	21 476	33 514	29 695	28 479	32 989
miscellaneous	221 154	314 981	647 047	478 903	472 015
freshwater Chlorophyta	667	332	317	376	305
freshwater miscellaneous	0	11	5	0	0
Indonesia
Rhodophyta	77 462	95 000¹	104 333	148 000	157 000
The Philippines
total	168 868	307 496¹	480 438	631 387	627 105
"Eucheuma alvarezii"	4 627	9 244	10 426	12 903	4 533
"Eucheuma cottonii"	145 632	265 013	434 933	590 107	589 263
"Eucheuma spinosum"	8 173	15 408	13 472	8 551	8 149
Gracilaria	0	0	4	0	0
Chlorophyta (Caulerpa)	10 436	18 490¹	21 606	19 826	24 890
Vietnam
Gracilaria	1 700	3 333¹	6 500¹	8 500¹	12 000¹

¹ FAO estimate.
Sources: FAO, 1996, 1999c.

Table 3. World production from natural stocks (excluding phycoculture)
of seaweeds and other aquatic plants (t wet weight).
	Total catch	Phaeophyta	Rhodophyta			Chlorophyta	Miscellaneous
	Total catch	Phaeophyta	Total	Indonesia	Philippines	Chlorophyta	Miscellaneous
1990-1992	1 133 667	737 904	213 170	11 284	1 265	23 013	159 586
1993-1995	1 101 433	716 608	176 102	8 803	1 042	22 675	185 836
1996	1 138 200	765 914	167 236	13 543	884	23 409	181 646
1997	1 193 800	784 196	168 378	15 000	494	24 517	214 756

Source: FAO, 1999a.

Economic value

The global value of the seaweed industry has been estimated at US$ 1 billion (109) and world demand for seaweeds and their products has been increasing by approximately 10% per year (Ohno & Critchley, 1993).

Calculations for phycoculture alone, however, already give a US$ 4 billion of profit/year and a turnover of more than US$ 16 billion. Total revenues for worldwide utilization of seaweeds have been calculated to be US$ 3.5 billion per year (Jensen, 1993). Phycoculture in the world uses an area of 530 000 ha, providing work and income for 250 000 family industries and almost 1 million employees, including those involved in dependent industries, repair, and maintenance (Pérez et al., 1992).

Little detailed information is available on the prices paid for seaweeds. To understand the price structure, its terminology has to be explained. For seaweed the FOB (Free On Board) price is fundamental - this is what is paid to the sellers (traders and exporters) for dried seaweed accepted on board the vessel and free to leave the port to be transported to the buyer. All costs to obtain and transport the seaweed to the vessel have to be met by the seller. The CF (Cost and Freight) price includes all costs the buyer has to meet to have the product delivered to the receiving port.

Lists are available of global prices for aquaculture products (FAO, 1996, 1999c). These are the prices of one t (wet weight) calculated from the amount produced (t) and the total value. These data are presented in Table 4.

Table 4. Prices of seaweeds produced by phycoculture
in US$ per t (wet weight).
	1990-1992	1993-1995	1996	1997
Phaeophyta	719	666	626	620
Rhodophyta	1051	1015	803	829
Chlorophyta	608	464	382	335
miscellaneous	631	627	721	728
"Eucheuma alvarezii"	120	125	127	135
"Eucheuma cottonii"	141	92	95	84
"Eucheuma spinosum"	100	125	119	95
Gracilaria	406	422	417	408
Caulerpa	268	217	176	152

Source: FAO, 1999c.

Microalgae

Few quantitative data are available on the production of microalgae (Zhu & Lee, 1997). Microalgal production in 1991 was limited to approximately 2000 t, and was used primarily as health food and for the extraction of β carotene (Benemann, 1992). In 1984 the ten largest commercial Spirulina farms produced just over 700 t of food-grade Spirulina powder, the Siam Algae Company in Thailand being the leader in terms of productivity (Jassby, 1988a). Since then other producing plants have taken over the lead position (Belay et al., 1994; Venkataraman, 1989; Vonshak, 1997). The production costs, however, are rather high (Belay et al., 1994; Vonshak, 1997).

Hydrocolloids

Of the global revenues from different food hydrocolloids, the phycocolloids accounted for 40% in 1978 (US$ 148 million of total revenues of US$ 397 million) and for 33% in 1993 (US$ 472 million of total revenues of US$ 1500 million) (Bixler, 1996; Jensen, 1993).

Globally, there are 300-350 factories in the world where raw, semi-dry algae are processed to provide the many products of algal origin that are used for innumerable aspects of modern human life (Pérez et al., 1992). For "Eucheuma" alone about 30 carrageenan-producing plants were active in 1987 (Neish, 1990).

Agar and agarophytes

In 1980 about 36 000 t (dry weight) agarophytes were harvested around the world, including 18 100 t from Asia (1470 t from the Philippines), and used to produce 7000 t of agar (3500 t from Asia) in the same year. Indonesia and Thailand were already known to be producing and exporting agar-bearing seaweeds, but no data were available (McHugh & Lanier, 1983; Soegiarto & Sulistijo, 1986). In 1984 150 t of agar were produced in Indonesia, probably mainly from Gracilaria (Armisén & Galatas, 1987), rising to 450 t in 1993 (Armisén, 1995).

By 1989 the world harvest of agarophytes had increased to 48 500 t (dry weight). Of this, less than 1000 t came from Indonesia (Luxton, 1993; McHugh, 1991). World production in 1987 was 6000 t of bacteriological grade agar (Indergaard & Østgard, 1991).

In 1990 the global production of agarophytes was 180 000 t (wet weight), resulting in a production of 11 000 t agar (Jensen, 1993).

The average price for agarophytes is higher than the price for other colloid-bearing seaweeds. Of course seaweeds which give agar with a higher gel strength, like Gelidium, command a better price. Often Gelidiella is mixed with imported Gelidium seaweeds in Japan, especially in lots assigned to the Philippines and to Indonesia (Armisén & Galatas, 1987). Wide fluctuations in price occur, depending on the source and the condition of the seaweed. The latter often depends on whether there are many epiphytes on the agarophytes, whether it is mixed with foreign seaweeds, and how well it has been dried and stored. It is almost impossible to store dried Gracilaria stocks for extended periods (Armisén, 1995).

Carrageenan and carrageenophytes

The estimated world carrageenan production in 1980 was 9200 t, including 2000 t from Asia. This correlates with 40 000 and 17 900 t (dry weight) seaweeds (McHugh & Lanier, 1983). In 1989 the world harvest of carrageenophytes was 82 570 t (dry weight), of which 65 500 t was harvested in the Philippines and Indonesia (McHugh, 1991). This resulted in a production capacity in the Philippines of 9040 t of alternatively refined carrageenan and 800 t of conventionally refined carrageenan (Llana, 1990). World production of carrageenans in 1990 was 12 300 t (Pérez et al., 1992). Alternative calculations for 1990 resulted in a global production of 250 000 t (fresh weight) of carrageenophytes, to produce 15 500 t of carrageenan (Jensen, 1993). World demand in 1993 was 20 000 t of food-grade carrageenan and 5600 t of crude carrageenans or seaweed flour (Bixler, 1996), for this 80 000 and 22 000 t respectively of dried carrageenophytes were required.

The world supply scenario for carrageenan was that most of the production technology and thus manufacturing activities were in the hands of a few major manufacturers in non-tropical countries. The production of semi-refined carrageenan changed this picture completely. In 1982 the world carrageenan market size was 13 200 t, which already composed 2400 t of semi-refined carrageenan mainly produced in the Philippines. The conversion rate for 1 kg of semi-refined and refined carrageenan is 4.5 and 5.0 kg of seaweed respectively.

Apart from the dried raw seaweed, products of carrageenophytes can also be exported as alkali-treated chips (Bixler, 1996; Luxton, 1993; Trono, 1994).

It is almost impossible to find accurate information about the prices paid for carrageenan. Already more than two hundred different carrageenan blends were available before 1987, tailored to meet specific applications (Stanley, 1987). Prices for food grade carrageenan in 1990-1995 were about US$ 10 per kg, while the price of semi-refined carrageenan was about 20% less (Bixler, 1996).

The yield of carrageenan in percentage of dry weight of the seaweeds varies from 14-27% in Eucheuma gelatinum in China to 58-65% in Kappaphycus alvarezii in the Philippines (Pérez et al., 1992). A 39% yield of carrageenan for conventionally dried Kappaphycus alvarezii has been mentioned, which can be increased to a yield of 60% after first washing the dried algae with freshwater (Bixler, 1996).

Alginates and alginophytes

The estimated world production of alginates in 1980 was 190 000 t of seaweeds, which is equivalent to 22 000 t of alginate (the amounts from Asia were only 4570 and 1950 t respectively). This global estimate excludes the production (1980) of 90 000 t of dry seaweed in China that was utilized for alginate manufacture. Only a very small portion of this large output entered the world market. Estimated world production was 180 000 t of dry alginophytes in 1989, again excluding the large amount from China (McHugh, 1991). The total world production of alginates in 1987 was estimated at 27 000 t; for 1990, however, the estimate is only 24 300 t (Indergaard & Østgard, 1991; Pérez et al., 1992).

Food

The total amount of seaweeds used as food for direct human consumption in the world was 385 000 t (dry weight) in 1980 (McHugh & Lanier, 1983). In 1989 the production of Hizikia, Laminaria, Porphyra and Undaria spp. combined was 454 800 t (dry weight) (McHugh, 1991). For 1990 it was 200 000 t (dry weight) for Laminaria, Porphyra and Undaria spp. together (Jensen, 1993). Except for Porphyra, none of these algal genera occur in South-East Asia.

Export

Dried seaweeds are often exported, especially for the production of phycocolloids. In South-East Asia these seaweeds are usually exported as raw material, although in particular the production of (semi-refined) carrageenan and salted Caulerpa lentillifera is growing.

Several South-East Asian countries are participating in the expansion of production of agarophytes and carrageenophytes and their associated products. Unfortunately, the logical link of production of raw material to the manufacture of agar and carrageenan, however, has often not yet been sufficiently implemented. In this way value-added benefits could be realized to the national economies of the producing countries.

Around 1980 approximately 50% of the world supply of agar was used principally in food in Asian countries. Of the 7000 t of agar produced less than 1000 t were utilized in the European Union (McHugh & Lanier, 1983). The production technology and manufacturing activities for carrageenophytes and alginophytes are in the hands of a few manufacturers only, while the farmers and collectors (especially of carrageenophytes) are poorly organized.

Between 1988 and 1990 the 1200 known applications of carrageenans increased to 4200 (Pérez et al., 1992). In 1993 the current annual demand for carrageenan was suggested to be 20 000 t, while the world capacity was then 28 000 t.

In 1980 Japan used about 20% of the world production of carrageenan, and western Europe and North America each used about 25% annually. In 1990 utilization in Japan was still about 20% of the world production, but had been to 45% in Europe and 35% in North America. However, in 1993 Japanese utilization accounted for only 8% of the world production of food grade carrageenan, while Europe still used the largest amounts (37%), followed by North America (26%), Latin America (17%) and Australasia (13%) (Bixler, 1996). The largest production capacity for food grade carrageenan in 1993 was in Denmark (26% of the world capacity), followed by the United States (19%), France (11%), the Philippines (11%) and Chile (8%). In 1978 the latter two countries did not have any substantial carrageenan production facilities (Bixler, 1996).

The market for raw material for alginate production is not as competitive as that for other colloid-bearing seaweeds, since the major processors usually attempt to ensure supplies by buying directly from the source. The market for alginates lies principally in the textile and the food industries.

Of the microalgae produced in South-East Asia (Arthrospira mainly in Thailand but also in Vietnam), most is exported in the form of dried algal powder.

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Table 5. Import and export values of dry seaweeds during the period 1995-1997
for Indonesia, Malaysia, Singapore, the Philippines and Thailand.
Country		Import			Export
		Quantity (t)	Value (10³ US$)	Unit price (US$/t)	Quantity (t)	Value (10³ US$)	Unit price (US$/t)
Indonesia	1995	50	213	24 620	24 957	16 262	651
	1996	30	168	5 600	22 310	18 962	850
	1997	131	492	3 755	12 698	10 521	829
Malaysia	1995	1	1 005	1 005 000	3	320	106 666
	1996	1 263	1 540	1 219	477	727	1 524
	1997	353	2 588	7 331	1 299	597	460
Singapore	1995	4141	4 686	11 318	2621	1 790	6 832
	1996	8741	8 160	9 336	4941	3 274	6 627
	1997	6121	5 710¹	9 330	331¹	2 025¹	6 117
The Philippines²	1995				28 920	39 106	1 352
	1996				26 406	41 974	1 589
	1997				n.a.	54 992	n.a.
Thailand	1995	298	5 932	19 906	110	1 649	14 990
	1996	477	8 364	17 535	77	1 298	16 857
	1997	383	3 697	9 653	55	797	14 491

¹ FAO estimate (1999b); ² only carrageenophytes; n.a. = not available.
Sources: FAO, 1999a, 1999b, 1999c; Trono, 1999.

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Table 6. Import and export values of agar during the period 1995-1997
for Indonesia and Singapore.
Country		Import			Export
		Quantity (t)	Value (10³ US$)	Unit price (US$/t)	Quantity (t)	Value (10³ US$)	Unit price (US$/t)
Indonesia	1995	496	4 711	9 498	931	2 942	3 160
	1996	557	3 783	6 792	981	4 974	5 070
	1997	754	6 640	8 806	637	3 327	5 223
Singapore	1995	369	6 168	16 715	126	1 714	13 603
	1996	485	7 180	14 804	114	616	5 404
	1997	319	4 897	15 351	32	369	11 531

Source: FAO, 1999b.

The algal industry

Indonesia

Collection and use of seaweeds are done on a local basis; the market for these products is not well-developed. An up to date inventory of Indonesian seaweeds is also lacking. Due to the importance of sea plants in the economy of Indonesia several attempts have been made to set up programmes for the comprehensive investigation of marine algae and their products (Soegiarto, 1979; Soegiarto & Sulistijo, 1986). Unfortunately, none of the proposed programmes were ever fully implemented (Eisses, 1952, 1953; Rachmat et al., 1986; Soegiarto & Sulistijo, 1986; Zaneveld, 1955, 1959). Before 1985, all seaweed production was harvested from natural stocks (Istini et al., 1998). In 1986 the total export of dried seaweeds was about 7200 t, rising to 11 423 t in 1989, and to more than 20 000 t in 1995 and 1996 (Table 5).

Marine vegetables Varieties of red, brown and green seaweeds are eaten by coastal inhabitants as a salad or as cooked vegetables (Hatta et al., 1993). At least 61 species in 27 genera of marine macroalgae are consumed as food and at least 21 species are used as herbal medicine (Istini et al., 1998).

Agarophytes Much of the final product of the agarophytes is in the form of agar strips, which are used in food preparation. In 1984, 62 t (probably dry weight) of "Gelidium seaweeds" from Indonesia were imported to Japan, together with 69 t of "other agarophytes", probably mainly Gracilaria (Armisén & Galatas, 1987). However, Gelidium production (potential: 4500 t wet weight) is still only done by gathering from natural stocks (Mintardjo, 1990). Less than 1000 t (dry weight) of agarophytes are exported annually, of which in 1991 603 t of dried Gracilaria to Japan and 59 t of Gelidium to New Zealand and Italy.

In 1975 10 agar extraction companies employed 175 people and produced about 109 t agar/year. By 1993 the total number of algal extraction companies increased to 15, with a production of about 889 t agar and 980 t in 1994.

About 90% of this production was sold on domestic markets, the rest exported (McHugh, 1996). However, that is not in agreement with other published data (FAO, 1999b). Indonesia still imports agar (FAO, 1999b; Istini et al., 1998; McHugh, 1996) (Table 6). The combined capacity of the Indonesian agar production plants is 1200 t agar/year, limited by the quantity and quality of cultivated Gracilaria available. The Indonesian production levels of agar require 7200 t (dry weight) of agarophytes per year. However, only 5500 t of dried Gracilaria is produced by phycoculture, and thus demand exceeds the present supply (McHugh, 1996). The potential amount of agarophytes available from wild crops is estimated at 28 000 t (wet weight) (McHugh, 1996).

Carrageenophytes It was not until Eucheuma spp. were recognized as valuable carrageenophytes by the western carrageenan industries that large-scale export became established (Adnam & Porse, 1987; Rachmat et al., 1986; Stanley, 1987). The main species of carrageenophytes for phycoculture in Indonesia are Eucheuma denticulatum and Kappaphycus alvarezii. In the 1980s, inadequate drying and post-harvest contamination with sand resulted in poor export quality for foreign processors (Doty, 1986; Luxton, 1993; McHugh & Lanier, 1983). On the other hand, consumption by Indonesian processors and sustained demand by the Chinese food market for Eucheuma denticulatum (1500-2000 t annually) ensured a predictable base of farm production.

In 1990 between 6000 and 6500 t (dry weight) of Eucheuma denticulatum and between 4000 and 5000 t (dry weight) of Kappaphycus alvarezii were exported, to which can be added 2100 t (dry weight) of the latter species consumed by local processors (Luxton, 1993). In 1993 15 000-21 000 t (dry weight) of carrageenophytes (iota and kappa types) were exported from Indonesia for food grade carrageenan production (Bixler, 1996; McHugh, 1996). Data for 1994 give an estimated production of 26 294 t dried seaweeds, including "Eucheuma", Gracilaria, Gelidiaceae and others, of which 16 100 t was exported (Istini, 1998). In 1995 the dry weight production of Eucheuma denticulatum and Kappaphycus alvarezii together was estimated at 20 000 t (Trono, 1998).

In 1994 6 carrageenan-processing companies in Indonesia collectively produced 2300 t semi-refined carrageenan (SRC) and one company produced 120 t refined carrageenan (McHugh, 1996). The semi-refined carrageenan produced locally is not yet a final product, however, and has to be exported for final processing. None of this domestically produced, semi-refined carrageenan is consumed in the country itself and Indonesia must also import to meet its requirements for refined carrageenan (150-170 t annually), because its total produce is exported to Japan. For further information on carrageenophytes ("Eucheuma"), see Table 7.

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Table 7. Production of carrageenophytes in Indonesia and the Philippines
for the period 1990-1997.
	1990-1992	1993	1994	1995	1996	1997
Indonesia
quantity, wet (t)	95 000¹	110 000¹	102 000	102 000	148 000	157 000
value (10³ US$)	8 150	12 100	11 220	11 220	14 800	15 700
unit price (US$/t (wet)	87	110	110	110	100	100
from wild populations, wet (t)	11 284	8 395	8 438	9 575	13 543	15 000¹
The Philippines
quantity, wet (t)	289 664	376 379	454 708	545 407	611 561	602 215
quantity, dry (t)	38 677	47 844	50 614	58 324	117 511²	no data
value (quantity wet)(10³ US$)	40 017¹	37 384	41 984	49 158	58 716	50 910
unit price (US$/t (wet))	138	99	92	90	96	84
from wild populations, wet (t)	1 265	1 144	1 062	919	884	494

¹ FAO estimate; ² equivalent, calculated from produced carrageenan together with exported dry seaweed.
Sources: FAO, 1999a, 1999c.

Alginophytes Alginate has been produced by a factory in Bandung (West Java) since 1992. Production in 1992 was 300 t alginate which required 3000 t of dried Sargassum seaweed (Istini et al., 1998). Other data, however, estimate production at 100 t alginate per year and required 1000 t of dried Sargassum (McHugh, 1996). Nevertheless, Indonesian alginate imports rose from about 3700 t in 1987 to 5100 t in 1991. The estimate for 1994 was 4000 t. The main uses were in the food, brewing, pharmaceutical and textile industries (McHugh, 1996).

The farms Farming of Eucheuma denticulatum (market name: "spinosum"), Kappaphycus alvarezii (market name "cottonii") and Gracilaria is a promising activity. In 1988 22 600 ha were identified as potentially suitable sites for seaweed culture, of which 17 700 ha was considered suitable for Eucheuma culture. Of these potential sites, about 900 ha are actually used for seaweed cultivation (Mintardjo, 1990). Later figures of the estimated potential exploitable area for Eucheuma culture, however, are approximately 9000-10 000 ha, with a production capacity of 450 000 t (dry weight) per year (Istini et al., 1998). Gracilaria is mainly farmed in South Sulawesi, where about 2000 farmers produce approximately 5500 t dried seaweed per year.

Microalgae PT Sun Chlorella Indonesia Manufacturing Company in East Java, a joint venture with Japanese companies, has 16 circular culture ponds, each capable of producing 36 t of wet Chlorella. The enterprise has a total production of 150 t Chlorella powder a year. Production started in 1995 with 6 t/year. All of the production is exported to Japan for processing and packaging.

Malaysia

Malaysia is marginally involved in the seaweed trade, although surveys have been undertaken for Malaysian seaweed resources and for species which might be potential sources of phycocolloids (Phang, 1984; Phang & Vellupillai, 1990). As yet there is no seaweed industry. The biomass of natural populations of commercial algae is unable to support harvesting for commercial extraction of phycocolloids (Phang, 1998). See also Table 5.

Marine vegetables Coastal inhabitants eat green, brown and red seaweeds, sometimes as salad, or cooked as vegetables (McHugh & Lanier, 1983). Seaweeds such as Laminaria ("kombu"), Porphyra ("nori") and Undaria spp. ("wakame") are imported, mainly from Japan, Korea and China.

Agarophytes In 1993 and 1994 about 6 t (dry weight) of agar from Gracilaria was produced by a small-scale, Thai-owned processing factory in Selangor (Peninsular Malaysia) for local consumption in jelly-type sweetmeats. In 1987 about 240 t of agar, worth US$ 2 600 000, was imported, mainly from Korea and Japan (McHugh, 1996). Since trials for Gracilaria cultivation were successful, and because there is a large market for domestically produced agar strip, the country seemed to be a good choice for future development of agar strip production facilities for the region (McHugh, 1996).

Carrageenophytes Jellies are also made from carrageenan extracted from "Eucheuma" by local coastal populations. Refined carrageenan, however, in quantities of about 150 t, with a value of US$ 1 600 000 are imported annually. These carrageenans are used in industry and this market is expected to grow at 5% per year (McHugh, 1996).

Alginophytes The domestic market for alginates in 1978 was thought to be sufficiently large to support a small alginate processor. There was, however, no information available on the extent of Sargassum and Turbinaria beds in the area, nor of the quality of any alginate extracted from them (McHugh & Lanier, 1983). Some Sargassum spp. from Sabah (East Malaysia), however, have a high content of guluronic acid (Wedlock et al., 1986). Alginates of these algae are supposed to form strong gels, sought after for special applications (McHugh, 1987). Recent annual import quantities of alginate for Malaysia are estimated to be 60 t (McHugh, 1996).

The farms Farming of Gracilaria changii (B.M. Xia & I.A. Abbott) I.A. Abbott, C.F. Zhang & B.M. Xia is promising and is in an experimental stage in Peninsular Malaysia (Phang, 1998). The seaweeds are cultivated in an integrated polyculture system with shrimps (Panaeus monodon and Lates calcifer). In Sabah (East Malaysia) small-scale Kappaphycus culture takes place, which has resulted in the export 80 t (dry weight) of cultured Kappaphycus alvarezii (as Eucheuma) to Denmark in 1990 (Choo, 1990). More recently the crop (500-1800 t dry weight per year) is exported to the Philippines (FAO, 1999b; McHugh, 1996; Phang, 1998).

Microalgae Some microalgae are cultured to be used as feed for larval stages of organisms grown in aquaculture or for use in integrated systems for wastewater treatment (Phang, 1987; Shamsudin, 1992).

The Philippines

About 350 economically important seaweed species from the Philippines have been recognized (Trono & Ganzon-Fortes, 1988); the different uses of only 150 species of seaweeds have been reviewed (Llana, 1990; Trono, 1986, 1999; Trono & Ganzon-Fortes, 1988; Velasquez, 1953, 1972). These uses include, apart from being a source of phycocolloids or food, mainly horticultural and medicinal applications. Only 1% of the seaweed production is consumed locally as food (Llana, 1990).

Marine vegetables Over 40 species of seaweeds are gathered and directly utilized as food in the coastal areas of the Philippines. Production is seasonal and in small quantities and detailed information is lacking (Trono, 1998). There is, however, one exception: Caulerpa racemosa (and more recently C. lentillifera) has been produced in phycoculture ponds since as early as 1950. More than 400 ha of ponds are used for the cultivation of C. lentillifera in Mactan Island, Cebu. These algae are either sold fresh or exported as a brine-cured product to Japan. More than 20 000 t (wet weight) of these green algae are produced (FAO, 1996, 1999c). See also Table 2.

Agarophytes Of the agarophytes, mainly Gracilaria is available and utilized, although other algae are used as agarophytes as well (Montaño & Pagba, 1996). Domestically produced agar strips ("gulaman bars") are sold in 5 g pieces; there is a total agar production of about 30 t per year. Only relatively small amounts (less than 10 t/year) of agar are imported, mainly for applications in the biotechnology and pharmaceutical industries.

Farming of Gracilaria is promising (FAO, 1996, 1997) and more than a dozen species are presently grown in culture, which produced 10 t (wet weight in 1994). However, only 4 species are in commercial production: i.e. Gracilaria heteroclada C.F. Zhang & B.M. Xia (= Gracilariopsis heteroclada C.F. Zhang & B.M. Xia), G. firma C.F. Zhang & B.M. Xia and a still unidentified Gracilaria sp. are partly produced through cultivation, while G. tenuistipitata C.F. Zhang & B.M. Xia is produced mainly from natural stocks (Trono, 1998). The total amount of wild Gracilaria harvested annually is estimated at 200 t (dry weight). Apart from Gracilaria only Gelidiella acerosa is suitable for agar production, and is almost exclusively harvested through the gathering of local stocks (Trono, 1998).

Carrageenophytes The phycoculture of Eucheuma in the Philippines was pioneered and developed in the period 1968-1971. This greatly promoted the carrageenan industry (Anonymous, 1998; Laite & Ricohermoso, 1980; Lim & Porse, 1981; Ricohermoso & Deveau, 1979; Stanley, 1987). Annual production increased from 300 t dry wild seaweed in 1970 to 13 500 t dry weight seaweed (mainly from phycoculture) during the period 1978-1980 to 117 511 t dried carrageenophytes or an equivalent of 822 500 t wet weight in 1996 (Anonymous, 1998; McHugh & Lanier, 1983). Of the 15 000 t dry seaweed produced in the Philippines in 1980, only 700 t of carrageenans were produced in that country, and most of the seaweeds were exported as raw material. In 1990 1295 t (wet weight) of carrageenophytes were still collected from wild stocks. That amount declined to 494 t (wet weight) in 1997, as compared to 291 176 (1990) and 627 105 (1997) t (wet weight) produced by phycoculture (FAO, 1999a). Data from different sources are not always comparable, however (Dawes et al., 1990; Llana, 1990; McHugh, 1990; Trono, 1990, 1998). See also Tables 2, 5 and 7.

The principal species grown in the Philippines is Kappaphycus alvarezii ("cottonii"), with smaller and irregular amounts of Eucheuma denticulatum ("spinosum"). The seaweeds are either exported to carrageenan producers, or semi-refined carrageenan ("natural grade carrageenan") is produced locally. At present 10 different companies (mostly members of the Seaweed Industry Association of the Philippines, SIAP) export semi-refined carrageenan, while 3 export pure carrageenan (Anonymous, 1998). In 1990 these companies provided employment for more than 10 000 people (Trono, 1998). By 1987, more than 50% of all Philippine Eucheuma/Kappaphycus harvests were utilized by local processors in the manufacture of carrageenan products, which then generated about 60% of the country’s foreign exchange earnings. Seaweeds and their products form the third most important fishery export of the Philippines (Trono, 1999). Large quantities of semi-refined carrageenan were produced in 1995 and 1996, while 14 493 and 18 292 t respectively of semi-refined carrageenan were exported, as well as 2375 and 2252 t of refined carrageenan. The local market, however, is only small (McHugh, 1996; Trono, 1999).

In 1991 the United States Food and Drug Administration (USFDA) classified "PNG" as carrageenan. In the European Union, however, the product is known as "processed Eucheuma seaweed" (PES) and is accepted as a food additive (INS - E407a). Another designation, "Alternatively Refined Carrageenan" (ARC) is also used (Anonymous, 1998).

Alginophytes Sargassum is mainly collected sun-dried and shipped to Japan to be used as fertilizer or in powder form as a binder of heavy metals in sewage water treatment. However, the bulk of the collected Sargassum biomass is presently processed into seaweed meal and utilized in the production of animal feed, whereas a part (5000 t in 1987) is still exported to Japan (Trono, 1998). The harvest of local stock is presently limited to northern Mindanao and Visayas. There is no local alginate production in the Philippines (McHugh, 1996).

The farms Over 10 000 family-owned and commercial seaweed farms were in operation around 1991, with over 170 000 people employed (Dawes et al., 1993). For 1989 the total number of "fisher folks" directly involved in the farming of "Eucheuma" was about 70 000 people (Trono, 1990). In 1998 about 80 000 farmers were involved in seaweed cultivation and, in addition, more than 300 000 people engaged in activities related to the seaweed industry (Trono, 1998). In 1997 10 000-15 000 ha of seaweed farms were located in the shallow coastal waters of the Philippines (Anonymous, 1998). Farm sites are mainly centered in south-western Mindanao (Zamboanga), the Sulu Archipelago, Tawi-tawi and southern Palawan (Trono, 1998).

Microalgae There is no large-scale commercial production of microalgae. A company is promoting a novel concept for the contract growing of Arthrospira (Spirulina). The company provides training and materials such as Spirulina inoculum and chemicals for culture medium are sold at cost price to the contract producers. The company buys back the dried microalgae which are produced (Lee, 1997).

Singapore

The involvement of Singapore in the seaweed trade is mainly by import and export of dried seaweeds and agar (Tables 5 and 6). Nevertheless, the differences between imported and exported quantities suggest a certain amount of consumption in Singapore of both products (FAO, 1999b).

Burma (Myanmar)

Studies of the seaweed flora of Myanmar are still incomplete. Up to now 307 species of seaweeds in 122 genera have been recorded (Soe-Htun, 1998). Of these algae, experimental cultivation of Catenella nipae Zanardini, Gracilaria salicornia (as G. crassa) and G. edulis (S.G. Gmelin) P.C. Silva is being undertaken at Setse Aquaculture Research Centre, on the Tanintharyi coast.

Marine vegetables Seaweeds are not generally popular as vegetables. Nevertheless, Catenella nipae is available as a sea vegetable from the market in Yangon. Edible seaweeds in a dried form are sold on the domestic Burmese market, these include Catenella, Enteromorpha and Hypnea spp. Coastal people use Catenella Grev., Gracilaria, Halymenia C. Agardh, Hypnea, Sargassum and Solieria J. Agardh in salads (Soe-Htun, 1998).

Agarophytes There is no internal agar industry, although agar powder imported from neighbouring countries is very popular among the people. Locally farmed Gracilaria edulis did not attract enough demand to warrant continued production. If a local agar-processing industry could be initiated, both the domestic demand and the potential to farm Gracilaria are positive factors (Soe-Htun, 1998).

Carrageenophytes Carrageenan is mainly obtained from Hypnea, of which there is a standing stock of 1500 t (dry weight). About 25 small factories produce strips of carrageenan for the domestic market. However, this product is not very popular since people prefer imported agar powder for making jelly desserts (Soe-Htun, 1998).

Microalgae About 30 t of Arthrospira (Spirulina) are commercially harvested from volcanic lakes (Twyn Taun and others) near Butalin in Central Burma. Spirulina flakes are first sun-dried, then ground into fine powder and finally punched into tablets (Lee, 1997).

Thailand

The use of seaweeds is limited to only those people living in the coastal area, especially along the Gulf of Thailand and the Andaman Sea. Recent imports and exports of seaweeds are documented in Table 5.

Marine vegetables Especially Caulerpa racemosa and Porphyra are used as a vegetable. The total crop of Porphyra is less than 100 kg (dry weight) per year, while no data are available for Caulerpa. Imports in 1989 of 78 t of dried and preserved seaweeds consisted mainly of Laminaria ("kombu"), Porphyra ("nori") and Undaria spp. ("wakame"), which are used as food. These imports mainly came from Japan, China and Korea.

Agarophytes In 1985 production of 4233 t of seaweeds was recorded (FAO, 1995). Seaweed production data for later years are lacking (FAO, 1995, 1996, 1997). Up till 1989 about 100 t (dry weight) of seaweeds were annually exported from Thailand, including 30-50 t of Gracilaria, some of which was obtained from phycoculture (Saraya & Srimanobhas, 1990). Pond culture of Gracilaria fisheri (B.M. Xia & I.A. Abbott) I.A. Abbott, C.F. Zhang & B.M. Xia (also by monoline culture) and G. tenuistipitata is currently successful. The combined production of Gracilaria from natural stocks and cultivation in ponds ranged between 50-400 t/year in Pattani Province, while data on the production from the monoline cultures in Songkhla Lake are not yet available (Lewmanomont, 1998; McHugh, 1996). Most of the material is exported. In some years, Thailand imported rather large quantities of agar (1989: 275 t) for different industrial uses and re-exported much smaller amounts (e.g. 1989: 3 t) as repacked flavour agars (Saraya & Srimanobhas, 1990).

Carrageenophytes Annual imports for carrageenan are about 1100 t/year. The large pet-food industry in Thailand uses about 780 t of semi-refined carrageenan annually, valued at US$ 2 500 000. Tuna processing, the jelly and confectionery industry and toothpaste manufacturers each use more than 100 t of imported, refined carrageenan per year. To cope with its annual demand for approximately 780 t of carrageenan, Thailand could support a semi-refined carrageenan facility if it imports the raw seaweed material from neighbouring countries or established its own "Eucheuma" cultivation industry (McHugh, 1996).

Alginophytes The brown seaweed Sargassum is the most common genus of marine algae in Thailand. When these algae are used, it is mainly for fresh consumption or as a herbal medicine. The import of 316 t of alginate for different industrial uses is documented for 1989, for 1994 the figure was 400 t, the latter with a value of US$ 4 000 000.

Microalgae The two major producers of Arthrospira (Spirulina) produce 150 t and 20 t Spirulina powder per year respectively, mainly for human consumption as health food (Lee, 1997).

Vietnam

Traditional harvesting and utilization of seaweeds by coastal people has taken place for over 100 years. Seaweeds are used for human and animal food, as traditional medicine, manure and raw materials for industry (Huynh & Nguyen, 1998).

Agarophytes In 1984 a small agar production facility existed, but production data are not available (Armisén & Galatas, 1987). The main commercial seaweeds are about 15 Gracilaria spp., with a total production from natural stocks of about 9300 t wet weight (= about 800 t dry weight) in 1990. These algae were harvested from the total estimated available wild biomass of 30 000 t (wet weight). At present, the main species cultivated are G. vermiculophylla (Ohmi) Papenf. (as G. asiatica C.F. Zhang & B.M. Xia), G. tenuistipitata and Gracilariopsis heteroclada. Of these gracilarioid algae, together with some Gelidiella acerosa (Forssk.) Feldmann & Hamel collected from natural populations, 100-300 t (dry weight) were used for agar-agar processing for foodstuffs, resulting in a production of 10 t food quality agar in 1987, 20 t in 1989 and 80-100 t in 1996 and 1997 (Huynh & Nguyen, 1998). Gracilaria production has become considerable, and was estimated in 1997 at 1500-2000 t (dry weight). A large part of this material is being exported to Russia, Japan and China (FAO, 1996; 1999a; Huynh & Nguyen, 1998). See also Table 2.

Carrageenophytes Both Kappaphycus cottonii/alvarezii and Betaphycus gelatinus are grown in phycoculture, each with an annual production of about 10 t (dry weight). These algae are, up to now, mainly used for food purposes. Cultivation of K. alvarezii started recently and is expected to become economically much more important in the coming years (Huynh & Nguyen, 1998).

Alginophytes The brown seaweed genus Sargassum is the largest natural seaweed resource of Vietnam. The annual production in natural Sargassum beds is estimated to be over 5000 t (dry weight), but the total amount harvested is only 300-500 t/year (dry weight). Annual production of alginate paste and powder from Sargassum is 15-20 t. These values far from satisfy the needs of the local textile industry, for which alginate has to be imported from India (Huynh & Nguyen, 1998; Van Khuong, 1990).

The farms The area used for Gracilaria phycoculture is around 350 ha, which is only a fraction of the potential area of more than 10 000 ha thought to be available (Van Khuong, 1990).

Microalgae In Vietnam Arthrospira and some diatoms in particular are cultured. Of the diatoms Chaetoceros sp. and Skeletonema costatum are grown in culture for use in shrimp hatcheries. In 1989 Arthrospira cultivation was executed in two factories, one of which measured 1000 m2 in surface area. The two factories produced pellets or dried tablets to be used as nutritional supplements for women and children (Van Khuong, 1990).

No data are currently available for the use of algae or the algal industry in Papua New Guinea, Brunei or Cambodia.

Botany

Algae are all the autotrophic organisms other than plants, a group of 30 000 to 40 000 different and described living organisms (Norton et al., 1996). The total number of undescribed species, however, may exceed known ones by a factor of four to eight. For a long time algae have been considered as primitive plants without a strict tissue differentiation, but only some groups of green algae are related to the "real" plants. The members of the informal group called "algae" are not necessarily related. Some algae are more closely related to bacterial groups (the blue-green algae are in fact Cyanobacteria), while others are more closely related to some Protozoa or to fungus-like organisms than to other algal groups. Algae occur in an incredible variety of life forms, from uni-cellular species to giant kelp which may extend to more than 60 m in length. The algal body is designated as a "thallus" or a "frond". In general, drawing conclusions about algae by analogy with plants, or even with other algal groups, is often fraught with potentially invalid assumptions.

Pigments

Since all algae are autotrophic, they contain chlorophylls as the main photosynthetic pigments, usually together with many accessory pigments. Due to these pigments, the algae can use light energy for photosynthesis, although several microalgae are capable of heterotrophic growth as well (Gladue & Maxey, 1994). The photosynthetic algae fix over 40% of the earth's carbon (Norton et al., 1996). All that goes into and out of an algal thallus does so by diffusion, because no roots or vascular tissue are available for transport (Doty, 1979). The highest rates of net photosynthesis under optimal environmental conditions are achieved by the sheet-like and filamentous annuals. Photosynthetic rates decrease in the more bulky growth forms of perennial algae, where many cells are set aside in the thallus for purposes of storage, translocation and stability. In some algal groups calcification of cell walls occurs, probably for protection from grazing. However, the high cost of calcification is evident from the generally low photosynthetic rates of calcified algae (Lüning, 1990).

In many cell walls of brown and red algae phycocolloids serve a structural function analogous to, but differing from, that of cellulose in land plants. Whereas land plants require a rigid structure capable of withstanding the constant pull of gravity, aquatic plants must have a more flexible structure to accommodate the varying stresses of currents and wave motion. They have adapted accordingly by hydrophilic, gelatinous, structural materials having the necessary flexibility (Lewis et al., 1988; Lobban & Harrison, 1994).

Taxonomy

Seaweeds are generally classified into four main groups, largely on the basis of their structure and pigmentation: red algae (division Rhodophyta), brown algae (division Phaeophyta), green algae (division Chlorophyta) and blue-green algae (division Cyanophyta, which is a group of the Prokaryotes). However, colour is only an approximate guide, e.g. red seaweeds show a variety of colours, from pink to purple and black. Botanists use structural features of the seaweeds as an accurate guide to classification.

Brown seaweeds are, especially in temperate regions, the most familiar, conspicuous, largest and most abundant of the seaweeds, but in number and diversity they are exceeded by the red seaweeds, of which there are 4000-6000 recognized species (McHugh & Lanier, 1983; Norton et al., 1996). Red seaweeds are usually smaller than brown seaweeds, with even some unicellular species occurring. The red seaweeds of commercial interest, however, are usually rather robust organisms. Of the green algae the majority is formed by microscopic members, but in the marine environment often multicellular representatives occur, as well as multinucleate (siphonous) thalli, in which the many nuclei are not separated by cell walls. The morphology of these green algae is very diverse, showing complicated coenocytic structures as well as plate-like or tubular thalli.

Several surveys of Philippine seaweeds have been made, including most of the economic species (Calumpong & Meñez, 1997; Trono, 1997; Trono & Ganzon-Fortes, 1988). A catalogue of the Philippine seaweeds is available (Silva et al., 1987). For Indonesia the old list of the Siboga-Expedition is still the most complete survey, supplemented by a number of more regional surveys (Coppejans & Prud'homme van Reine, 1992; Verheij & Prud'homme van Reine, 1993; Weber-van Bosse, 1913-1928). There are surveys for Malaysia (Phang, 1998; Phang & Wee, 1991) and Singapore (Teo & Yee, 1983), Vietnam (Nguyen & Huynh, 1993; Pham, 1969) and Thailand (Lewmanomont et al., 1995; Lewmanomont & Ogawa, 1995). A series of papers has recently been published for Papua New Guinea (Coppejans et al., 1995a, 1995b; Millar et al., 1999).

For a broader area, e.g. the Indian Ocean, another catalogue is available (Silva et al., 1996). For freshwater algae very few recent data are available, although there is a survey of the freshwater algae of Thailand (Lewmanomont et al., 1995).

The blue-green algae are morphologically the most diverse and complicated of the Prokaryotes. Both unicellular and filamentous representatives occur, while the cells may also grow together to form colonies. Species with the potential to be used as bio-fertilizers have heterocystous filaments. Arthrospira platensis is an important source of protein in some inland tropical areas.

Growth and development

The numerous different algal groups show a broad variation in life cycles. In many groups there is only one major kind of life cycle present, but in other groups (e.g. in the Phaeophyta) several major kinds of life cycles exist, often with an alternation of generations (van der Hoek et al., 1995). These generations, known as sporophytes and gametophytes, can be isomorphic to each other or heteromorphic. In the latter case the dimensions of the thalli of the different generations may be very different and then microstages and macrostages can be distinguished. These heteromorphic generations can greatly differ in morphology and are often given separate scientific names. In several cases it has only been detected quite recently that morphologically very different algae in fact belong to a single species and are only stages or generations in the life cycle of that species.

All algae have unicellular spores and gametes, but occasionally vegetative propagules are also present in some species. Once the spores and propagules of benthic algae have been released from the parent generation, they must find a surface and stick to it. The microscopic stages of most seaweeds are inconspicuous. Resting spores or resting zygotes seldom form thick walls in marine macroalgae, while in many microalgae thick-walled resting spores and cysts are of frequent occurrence. Many seaweeds are perennial, but some opportunistic algae often occur as short-living annuals. In several seaweeds, the combined effects of temperature and photosynthesis regulate development and reproduction (Lobban & Harrison, 1994).

Productivity

Although the biomass of natural algal vegetation in tropical marine waters is not usually very impressive, the annual primary productivity can be very high. Turnover rates (total renewal of biomass) for some tropical seaweeds are 1-1.5 months, resulting in maximum values for annual primary productivity that are higher than in tropical rain forests (Harlin & Darley, 1988; Lüning, 1990). High productivity occurs especially on coral reefs and in benthic Sargassum vegetations. Most nutrients there remain in a relatively closed environment with many herbivores and predators, resulting in a quick recirculation. In contrast to temperate regions, where about 90% of the seaweed biomass is thought to be decomposed and finally mineralized in detritus food chains, in tropical regions much of the seaweed biomass is consumed by grazers (Lüning, 1990). Primary productivity in the marine waters of South-East Asia is generally high, although the surrounding open oceans have much lower primary productivity values (Lembi & Waaland, 1988; Rodin et al., 1975).

Ecology

Blue-green algae and green algae, although also present in salt water, are more commonly associated with freshwater and on land (for example, on tree trunks, in soils, etc.). The largest forms of the green algae, however, occur in the sea. Red and brown algae are usually associated with marine environments, often rocky shores, although some representatives of these groups occur in freshwater. Blue-green algae are ubiquitous members of the soil microflora. Brown seaweeds are particularly abundant in cold and temperate waters and most species of commercial interest grow best in waters below 20°C, usually at or below the intertidal zone (McHugh & Lanier, 1983). Few species are found in tropical regions, of which members of the genera Sargassum and Turbinaria, however, may be locally dominant and also of commercial interest.

Red seaweeds often grow in deeper waters than the brown ones, e.g. from just above the low tide level down to more than 50 m. Many species occur in temperate to tropical waters, amongst which are several of considerable commercial interest.

Green seaweeds may become dominant in pools and in the intertidal, especially in eutrophic situations. In tropical regions, the multinucleate genera (Caulerpa J.V. Lamour., Halimeda J.V. Lamour. and others) especially form important constituents of both seagrass meadows and coral reefs.

Temperature

Temperature, and particularly water temperature, is the main abiotic factor governing the geographical distribution of seaweeds, although interactions amongst environmental variables are the rule rather than the exception. Many marine seaweeds can not survive seawater temperatures higher than 33-35 °C. Some, however, can tolerate much lower seawater temperatures than occur in their own environment (Lüning, 1990). The edaphic Cyanobacteria generally grow and fix nitrogen optimally between 30-35 °C; thus temperature is not limiting to their growth in the tropics. Several blue-green algae are unique in the microbial world for their ability to simultaneously fix nitrogen in aerobic habitats and carbon by the oxygenic eukaryotic plant mechanism (Metting et al., 1988).

Light

Algae, being autotrophic organisms, need light to be able to survive and for that reason they can only occur in locations where at least some light will reach them. As a rule, macroalgae live attached to the seabed between the top of the intertidal zone and the maximum depth to which adequate light for growth can penetrate (Lobban & Harrison, 1994). In very transparent tropical or subtropical marine waters some algae may reach depths of around 200 m, but most of them prefer much more light and occur close to the surface of the water, often protected from strong irradiance and desiccation by canopy seaweeds that shade the understory algae. This protection is important to the survival of understory algae, including germlings of larger species (Lobban & Harrison, 1994).

Water movements

Water movements are necessary for the adequate supply of nutrients and removal of silt, detritus and excretion products from the surface of seaweeds. These water movements can increase the steepness of the diffusion gradient for all nutrients and excretion products, while both too much and too little outward-diffusion may depress growth rates (Doty, 1979). Water motion can also become excessive, resulting in the physical removal of algae from a given site.

Desiccation

Most subtidal seaweeds do not survive desiccation, but intertidal ones often exhibit a remarkable desiccation tolerance. Such algae are unable to avoid desiccation, and thus simply tolerate it and survive the related osmotic stress (Lüning, 1990).

Soil surfaces in deserts are commonly consolidated by cryptogamic communities, of which algal crusts can be important constituents. Functions of algal crusts include consolidation of the crust, mediation of infiltration and retention of water, and nitrogen input. The desert surfaces are consolidated by the combined aggregating effects of mucilaginous sheaths and the filamentous nature of dominant blue-green algae. Ensheathed blue-green algae retain water, which buffers against rapid desiccation and promotes water infiltration (Round, 1981).

Salinity

Many microalgae, and certainly all the marine ones, have a low tolerance of salinity change. Some, however, occur typically in a wide salinity range. In inland saline lakes, only few microalgal species occur and these are especially well-suited for mass culture since most of the potential contaminating and competing aerial algal spores and cysts will not be able to germinate in such extreme saline environments. Marine microalgae can also be found in an aerial environment, but they usually do not contaminate open air mass cultures in hyper-saline situations (Borowitzka & Borowitzka, 1988; Round, 1981).

Most marine macroalgae grow optimally at salinities of approximately 30‰, but there are exceptions such as Gracilaria spp. and the mangrove algae of the red algal genera Bostrychia Harv. and Caloglossa J. Agardh. These species often show maximum growth at much lower salinities (Lüning, 1990). In the species of the latter two genera brackish-water ecotypes may also occur; these do not tolerate high salinities (Lüning, 1990). In these euryhaline ecotypes respiration and photosynthesis decline only slightly with decreasing salinity.

Competition

Algae may experience considerable competition with other organisms, as there are other algae and phototrophic organisms (e.g. competition for space, light, carbon and nutrients), or parasites, pathogens and herbivores (Lobban & Harrison, 1994; Olson & Lubchenco, 1990). Therefore, many algae have developed toxins, digestive inhibitors, or unpalatable substances. In particular, anti-herbivore substances are often found in seaweeds; there are phenol-like substances in brown algae and halogenated substances in red algae (Lüning, 1990). Inhibiting substances might also explain the clean appearance of some brown and red algae in the field, since most epiphytic organisms are unable to settle or grow on these thalli. Most epiphytic organisms attach only superficially to the surface of their host. For this reason, some seaweeds slough their outer layers to inhibit the growth of epiphytes. Epiphytic algae decrease the growth rate of their host, increase the probability of breakage of the thalli of the host and may decrease reproductive output. Epiphytic animals may also cover large parts of the thalli of seaweeds. In epiphytic animals their larvae are chemically attracted by the preferred host alga.

Epiphytes can be removed by small herbivores which specialize in browsing on epiphytic organisms (Lüning, 1990). Most epiphytes are not specific to their host, and are not parasitic, but there are notable exceptions of specialized epiphytes and even parasitic algae.

Exploitation and cultivation

Marine agriculture has a relatively short history (approximately 250 years), especially when compared to approximately 8000-10 000 years of terrestrial agriculture. In the years 1970-1972 almost nobody would have predicted any future growth in marine agronomy and South-East Asia was barely covered in handbooks on aquaculture (Bardach et al., 1972; Doty, 1979). Gracilaria and other algae as food for milkfish were mentioned and the culture of Caulerpa in the Philippines for the fresh vegetable market was also listed. The advanced experimental culture of Eucheuma and Hypnea spp. in the Philippines was then mentioned for the first time (Bardach et al., 1972).

Traditionally, the seaweed industry has relied on the gathering of wild seaweeds to meet its raw material requirements. The accelerating pace of advances in seaweed culture techniques, however, combined with the expanding demand for seaweed products and the rising costs of operation in industrialized countries are creating forces that have potential to alter the global distribution of this industry in the foreseeable future. This in particular holds true for the seaweed colloid manufacturing sectors (McHugh & Lanier, 1983). It has been proposed that the term "phycoculture" be used for farming of algae in general, and thus "marine phycoculture" as the commercial farming of seaweeds (Tseng, 1981a).

Production systems

The natural productivity of many seaweeds is only about 1t (dry weight)/ha/year in nutrient-poor water, the actual productivity depending, of course, on many parameters and on the species (Wise, 1981). Productivity may, however, exceed 40 t (dry weight)/ha/year under good cultivation conditions (Morand et al., 1991).

Collection of wild resources

Harvesting techniques for wild resources of marine macroalgae vary, depending on circumstances. They can, however, be classified as follows:

gathering of seaweeds washed to the shore;
gathering seaweeds by cutting or uprooting them from their beds, often by scuba divers (Armisén & Galatas, 1987).

In all cases where seaweed industries expand, over-exploitation and eventual loss of local stocks are considerable risks. Thus development and commercialization of phycoculture of the exploited seaweeds is usually a necessity.

When harvesting wild populations of the microalga Arthrospira (Spirulina) several technical, ecological, and public health issues require serious evaluation before any large-scale venture can be undertaken (Jassby, 1988a).

Extensive field production of macroalgae

Seaweeds grown in open lagoons and cultivation where natural populations are supported (as in Betaphycus gelatinus in Hainan, China) can be considered as a form of extensive field production, although transitions to more intensive forms of cultivation frequently occur.

Intensive market gardening

For most algae that are cultivated, intensive phycoculture methods are used, for which tanks, ponds, rafts or systems of lines have to be installed and maintained. Different types of phycoculture may be characterized on the basis of the methods used (Pérez et al., 1992):

- Fragmentation by hand and growing the fragments to mature plants (vegetative propagation). This is the case in cultivation of Caulerpa, Eucheuma, Gracilaria and Kappaphycus.

In tropical regions marine phycoculture for the production of food or of phycocolloids is either by pond culture, by fixed, off-bottom monoline methods or by floating methods, where either rafts or longlines are used. The methods to be preferred depend on the species to be cultivated and the local circumstances, as well as on the conceptual framework for marine phycoculture (Santelices, 1999). In general Gracilaria spp. and Caulerpa lentillifera are grown in ponds, while Eucheuma, Kappaphycus and several other Gracilaria spp. are cultured attached to monolines, rafts, longlines or off-bottom systems (Luxton, 1993). To account for and avoid the possible devastating actions of tropical storms, the areas within about 6° of the equator are considered to be the most favourable for potential seaweed cultivation sites (Doty, 1979).

Basically, a seaweed farm for Eucheuma, Kappaphycus or line-grown Gracilaria comprises networks of lines suspended either from mangrove stakes and then immersed a short distance below the low-tide level, or from (bamboo) rafts. Fixed bottom monoline phycoculture (constant depth farming) is an inexpensive and easy method to establish and maintain. It needs bi-filament polythene twine, either No 5 (2.5 mm) or No 6 (3.0 mm) and mangrove stakes. The "seedlings" are inserted between the twines to start farming. A plot can be 10 m × 10 m in area (two plots of 5 m × 10 m are better), with a maximum of 32 lines, each about 32 cm apart. The lines are stretched and tied to the stakes, which are positioned approximately 5 or 10 m apart (Trono, 1990).

Material costs of the floating rafts are higher than those of off-bottom systems (Luxton, 1993). Floating raft monoline phycoculture can be used in places where the cultivated algae can be submerged in 30 cm of seawater at all times. In addition, the raft must be able to withstand the weight of the seaweeds near harvest time. Recommended material for the raft is bamboo measuring 2.5 m × 5.0 m or 5.0 m × 5.0 m. The lines are stretched within the rafts which need to be well anchored.

"Sprigs" (cuttings) of the algal seedstock are suspended from the lines. They may be pruned back when mature, with growth continuing from the remaining thalli (Lewis et al., 1988). Alternatively, farmers may harvest the whole plants and replant the farm with cuttings. The best plants from the harvest are selected and used for the next crop. The built-in mechanism of "seed improvement" by selection is a great advantage of this practice and is not possible with the pruning method of harvesting (Trono, 1994).

- In the second group of intensive cultivation methods, parts of the culture work is undertaken indoors, where microscopic stages of the life cycle of the cultivated algae are handled (Pérez et al., 1992). These techniques are not yet commonly applied in South-East Asia (Trono, 1994). Indoor cultivation methods, however, can also be used in micro-propagation in Eucheuma denticulatum and Kappaphycus alvarezii (Dawes et al., 1993).

- In the third group of intensive phycoculture methods all actions are on land, and the cultivated algae are grown in tanks. Up to now results with seaweeds in tanks are not very promising, but cultivation of several species of microalgae can be successful and occurs, albeit not frequently, in some countries in South-East Asia.

Cultured microalgae

Unicellular freshwater algae are often grown in special facilities consisting of shallow cultivation tanks located in dry land areas with much sunshine. Blue-green algae, for direct use as agricultural fertilizer, are also grown in similar shallow cultivation tanks or ponds. When the water is allowed to evaporate in the sun, these blue-green algae form dry flakes that can be scraped off, stored in bags and be used as inoculum for rice fields after rice transplantation (Metting et al., 1988, 1990; Mshigeni, 1982).

Large-scale algal culture systems for microalgae need engineering designs of a size sufficient to produce tonnes of algae or algal products daily (Oswald, 1988b). This involves consideration of not only the application desired, but also many other factors, such as media requirements of the species to be grown and various media inputs as a function of quality and availability for economic production. Local climatological conditions must also be taken into account, including variation in illumination, temperature, precipitation and evaporation. The following must also not be forgotten: physical properties of the design area, including slopes, drainage, water quality and quantity and the specific physical requirements for cultures, e.g. mixing, depth, residence time and power inputs needed (Oswald, 1988b). These factors, together with attainable efficiencies and productivities, harvesting and processing and the costs need to be related to the specific application to ensure success. This may be cultivation of microalgae on organic residues as the basis for production of fish and other animals or use as oxygen generators for waste oxygenation and nutrient control as well as systems for production of high-value fine chemicals or health food products (Belay et al., 1994; Borowitzka, 1992; Laing & Ayala, 1990).

Carbonation (CO₂-supply) of microalgal cultures is usually required, as well as continuous mixing in all shallow outdoor cultures (Vonshak, 1997). In some cases cultivation of freshwater algae in seawater-based culture media is feasible (Tseng & Xiang, 1993). Continuous flow mixing in shallow channelized ponds, driven by propeller or screw pumps, by air lift pumps or by paddle wheels are methods often chosen, particularly in tropical areas (Oswald, 1988b). However, not all microalgae can be grown adequately in such ponds. A fairly new development is the use of tubular photo-bioreactors (Borowitzka, 1994; Materassi, 1994; Torzillo, 1997). Another possibility is the vertical alveolar panel reactor (VAP), which can also be used in combination with open raceway ponds (Materassi, 1994; Pushparaj et al., 1997; Tredici & Chini Zittellii, 1997). A third alternative is heterotrophic growth of microalgae (Day & Tsavalos, 1996; Gladue & Maxey, 1994; Johns, 1994).

Domestication of algae

Seaweeds versus land plants

The difficulties involved in the domestication of seaweeds, transforming them from wild plants into crops, are many. The most fundamental is that in the farming of seaweeds one is dealing with a very different organism than in the case of farming of land plants. First of all, there is a big difference between the reproductive units of seed plants and algae. Terrestrial crops mostly reproduce by seeds which are multicellular, macroscopic and generally can be preserved by drying and eventually sown into the soil. The algae reproduce by microscopic unicellular spores and gametes which usually can not be preserved by drying or stored in any form. However, propagation using vegetative fragments is often possible in multicellular algae. The spore-liberating algae should be brought as close to the desired substrate as possible, so that the liberated spores and fertilized eggs will find the necessary place to attach and grow (Tseng, 1981a).

Tissue culture

Tissue culture is a method of propagation of sterile plants that is frequently used in terrestrial agronomy. The technique has also special problems when used in phycoculture (Polne-Fuller & Gibor, 1987). As a consequence of the aquatic habitat and unique chemical composition, seaweeds present the biotechnologist with problems which are very different from those encountered with land plants.

The aquatic habitat

Another fundamental difference between cultivation of terrestrial and phycoculture crops involves the growth media. Land crops grow on soil and in air, whereas the aquatic crop plants grow in water, usually attached to some sort of substrate. In the case of the land crop plants, the air is relatively gentle and the plant is stationary with respect to the source of light. In the case of aquatic crop plants, water is constant, but there is often vigorous motion with perpetual pounding of waves and ever-changing tidal levels. In addition, the substrates to which the algae attach must be able to withstand the continuous water motion and remain stable enough to ensure that the algae remain at a particular level where it can receive adequate light for photosynthesis. The water movements also replenish nutrients and cleanse the algae of silt, detritus and other sediments. All these and other differences naturally lead to differences in the technical methods of cultivation (Tseng, 1981a); many of the techniques have to be modified for site-specific conditions.

Marine phycoculture

Phycoculture techniques have been successfully applied to several seaweed species. The successful establishment of a large phycoculture industry in the Philippines based on seaweed had its genesis in an agar supply crisis in Japan around 1960. This eventually resulted in the collection of seaweeds in hitherto untapped areas around the world and precipitated appreciation of the fact that inadequate seaweed supplies were hindering the growth of the seaweed colloid manufacturing industry. Seaweed culture offered the best solution to raw material supply problems. Development of marine phycoculture in tropical areas especially developed as a pioneering effort in the Philippines from 1965 onwards. Farming of Eucheuma species required the identification of suitable sites, identifying the people who would farm and obtaining the stability of return on the investment that would keep the farmers active and industry interested in continuing use of the farm-produced material (Doty, 1979).

The phycoculture of Gracilaria is now well-established in several South-East Asian countries (McHugh & Lanier, 1983; Trono, 1994). Nevertheless, only species from about 15 genera of seaweeds are at present grown in marine phycoculture (Ohno & Critchley, 1993; Pérez et al., 1992). The indications are, however, that most commercially important seaweeds will be produced by phycoculture before long. In fact, this is largely already the case. Virtually all commercial brown seaweeds, as well as 63% of the commercial red seaweeds and 68% of the commercial green seaweeds are now cultivated (Ohno & Critchley, 1993). For Eucheuma and Kappaphycus it is even stated that over 95% of the crop is farmed (Lobban & Harrison, 1994). Of the total 3.9 million t (wet weight) of seaweeds used in 1991 in the seaweed industry, 2.8 million t were provided by phycoculture (Pérez et al., 1992).

Site "fertility"

To obtain improved yields, a rational adaptation of appropriate working methods in relation to environmental factors of the area, is advocated. The importance of the site "fertility" and the role of water require special consideration as well as an understanding of the variations in environmental factors at the site. A multi-factorial compensation hypothesis for physical control of site "fertility" has been formulated (Doty, 1979). This takes into consideration the factors of light, water motion, water quality and temperature, in relation to algal fertility. This fertility can then be calculated in terms such as mass per unit area per unit time. Any change in one or more physical factors changes the relative position of all of the other factors when plotted in a multi-factorial figure and thus can be expected to affect the overall "fertility" of the site. This hypothesis has merit in that it provides a conceptual explanation for the short-term, almost random changes in standing crop and production potential often found in natural habitats and it also allows controlled laboratory results to be contrasted with the variability found in the field. The concept leads to an easier understanding of the essence of marine phycoculture (Santelices, 1999).

After a site has been identified, test planting of the desired species (or, in some species, the desired cultivar) is recommended. For Eucheuma, Kappaphycus and some Gracilaria spp. test plots consisting of a few monolines planted with 50-100 test plants each are constructed at different strategic locations in the area. The growth of the test plants must be monitored at weekly intervals and their daily growth rates determined. Areas supporting daily growth rates of 2-5% or higher are potentially good sites. A 2-3 months long monitoring period of growth rate may be enough to start a small family farm, but for commercial farms a year-round monitoring programme is necessary, considering the possibility of problems associated with the seasonality of algal growth.

Space, labour and costs

About 530 000 ha in the world are already occupied by the existing 250 000 seaweed farms, many of which are small family enterprises, which provide employment for approximately 950 000 individuals. These developments augur well for the countries in South-East Asia with phycoculture potential in that the cultivation, harvesting and processing of seaweeds are highly labour-intensive activities (Doty, 1977). The farming of tropical algae is not a periodic activity, rather it is continuous and an alternative means of sustainable employment based on renewable resources. Incentive and free enterprise can be considered to be major factors in farm productivity (Doty, 1987). A large, successful farm could require several people for its proper operation and a smaller farm might be successful even though it may not require all the time of even one person. The cost of production of Eucheuma and Kappaphycus is much lower from family farms than from farms with paid employees (Doty, 1987; Trono, 1990). Although large and semi-intensive farms produce the highest yields, they are also the most expensive to maintain. The extensive farms derive higher net profits than the semi-intensive and intensive farms. Small farms generally obtain higher net profit, because of lower total costs (Llana, 1990).

Details of necessary investments and the costs of phycoculture of Kappaphycus alvarezii are readily available from the literature. These investments include the structures (poles, etc.) to fix the cultivation units, the living quarters for the farmers and the labourers, the drying house, boats, lines and nets and further miscellaneous equipment. The operating costs include mainly labour (for selecting and obtaining "seed", planting, maintenance and weeding, harvesting, drying and washing, packing, baling and shipping) as well as some costs for materials such as polythene ties and freshwater. Overhead costs such as salaries, boat and transportation rentals, communications, representation expenses, repairs, fuel and oil also have to be taken into account. Estimates of farmer returns and future farming costs can also be calculated (Doty, 1986; Llana, 1990; McHugh, 1990).

National distribution and marketing structure

Success will not necessarily come to those who simply establish good methods of phycoculture. These efforts must be tied to the establishment and maintenance of a national distribution and marketing structure which equitably rewards and sustains seaweed collectors/farmers and ensures a necessarily more stable seaweed price and demand structure, thereby motivating investment and the production of consistent and reliable seaweed supplies (McHugh & Lanier, 1983; Trono & Ganzon-Fortes, 1988).

Culture of microalgae

The concept of mass production of microalgae was first tested around 1940 in Germany, resulting in advanced techniques for the continuous cultivation of large quantities of microalgal biomass (Burlew, 1953). Selection of promising microalgal species, strains and products requires evaluation of the cost structure of the microalgal production process, the suitability of the alga for mass culture, the value of the product, its concentration within the alga, the size of the market for the products and existing and/or future alternative sources (Borowitzka, 1992, 1994). The costs associated with growing and harvesting microalgae, extraction and purification of the products are often disappointingly high (Jassby, 1988a; Regan, 1988). The amount of free sun energy in tropical countries, however, provides interesting possibilities for cultivation of autotrophic organisms, especially when the microalgae can be grown in seawater (Tseng & Xiang, 1993).

The utilization of blue-green algae as bio-fertilizers has a long history and is inherently attractive. There is widespread interest in developing technologies for mass culture and their use with crops other than rice. A methodology for accurate, rapid estimation of standing crop or productivity of filamentous blue-green algae (Cyanobacteria) does not exist (Metting et al., 1988). Important physical factors influencing growth and nitrogen fixation include light, pH, temperature and cycles of wetting and drying. Soil cyanobacteria grow best under neutral to alkaline conditions. Nutrients and agro-chemicals also influence their activities and growth, in particular the availability of phosphate in the soil. The addition of lime (CaCO₃) to rice often stimulates the growth of blue-green algae. The effects of herbicides on growth and N2-fixation by free-living cyanobacteria are variable and differ widely among strains. Many components are inhibitory at high concentrations, but are stimulatory when diluted.

Planting material

Although algae are never really "planted", most macroalgae need to be attached to a substrate in order to ensure survival. Cultures can be started from vegetative cuttings, spores or propagules, or by bringing young plants in from nurseries. These young plants can be seeded directly onto nets, as is usually the case with Porphyra cultures, or onto special nursery cord to be later attached to other substrates for further cultivation. The latter method is normally used in the phycoculture of large brown algae (kelps) in non-tropical waters (e.g. Laminaria spp., Undaria spp.), but is also used to grow Gracilaria sporelings. In pond cultures of Caulerpa and Gracilaria one end of a small bundle of cuttings is often buried into the mud at the bottom of the pond. When algae are to be attached to lines, this has to be done by hand. The cuttings are attached either individually or in small bundles (Trono, 1994).

In several forms of seaweed culture cuttings are used for propagation instead of spores. These cuttings, which should be prepared from healthy plants, can be broadcast in shallow pools or they can be tied to lines or nets or to dead coral branches. These substrates have to be positioned in the best possible way according to local conditions. Vegetative propagules may also be produced in well-equipped laboratories (Dawes et al., 1993).

For commercial cultivation of microalgae, sufficient amounts of fresh and healthy specimens must be added to the culture medium. Some microalgae can be preserved for many years by cryo-preservation, while cyanobacteria can be immobilized in polyurethane foam or sugar-cane waste to be used as bio-fertilizer (Day et al., 1997; Kannaiyan et al., 1997).

Phycoculture

Phycoculture can only be successful when cultivation methods are based on scientific research. The many differences with the agronomy of land crop plants involve various important factors and practices. Competition with other local activities may restrict the possibilities for phycoculture.

Substrate

The importance of the substrate is merely to provide a suitable attachment base for the algae. Rhizoids of algae are generally not responsible for the absorption of water or nutrients. All parts of the algae are involved in absorption as the algae are immersed in an aquatic medium.

For the seaweed farmers, however, the selection of the substrate is important from the point of view of convenience, availability, durability and economics.

The growth medium for seaweed cultivation is seawater, which contains salts that may be quite corrosive. Therefore, the substrate should be able to resist this corrosive action of the seawater, while it must also be strong enough to withstand the wave action and currents. As a result of tidal amplitude, the positioning and anchorage of the substrate should also be able to adapt to these changes. The locality where a cultivation site is established must be selected with utmost care. Thus the substrate and its positioning are of primary importance. The substrate may be natural, such as rocks and reefs, or artificial, such as ropes and wooden or bamboo structures.

Selection of locality

Other important factors in the selection of locality and position are salinity (no culture of stenohaline species near to a freshwater outlet, but euryhaline species may even need some additional freshwater), pollution (especially for species to be used as food), water movement and mobility of the bottom substrate (causing turbidity, burial of the algae or even erosion of the bottom). Water movement must be strong enough to provide the necessary minerals and gaseous exchange, but not so strong as to cause breakage and spoilage by losing pieces of the crop before harvest. In areas where strong currents occur, a retaining fence made of nylon netting (with approximately 10 cm mesh size) should be constructed on the leeward side of the farm in order to catch thalli washed away by the current. In some areas about a third of the daily harvest may consist of thalli carried out by currents (Trono, 1998).

Nitrogen normally occurs at such low concentrations in seawater that it may become the limiting nutrient. The same may be the case for phosphorus. This is especially evident in clear "blue" waters of the tropics. In areas with upwelling, growth of most seaweeds is much better. In areas where water movement is low (with a low exchange of gas and ions), supplementation with additional nutrients may be necessary for successful phycoculture.

Spores

Algal spores are very delicate unicellular structures which can die as soon as they are removed from their medium. Therefore, it is imperative that in the "seeding" process (i.e. the collection of spores), the substrates must be brought close enough to the seaweed fronds so that the liberated spores will have the best chance to adhere in the shortest time possible. In general, spores of seaweeds germinate only after adhering to the substrate (Tseng, 1981b). Thallus fragments used as vegetative propagules are often also designated as "seed stocks".

Competition

Biotic competition with other algae, with epiphytic organisms, parasites and pathogens and with predators (herbivores) is an important factor determining the success of phycoculture. Weeding and regular pruning are necessary activities in the maintenance of every seaweed farm. If senescence of the stocks is apparent, the lines should be re-stocked with fresh "seed". Decreasing productivity of the stocks is an important problem in farming of tropical seaweeds (Dawes et al., 1993; Trono, 1994). Research on periphyton communities used as food in abalone culture in Pacific Canada has shown that nutrient enrichment usually does not change the competition of these periphyton communities. However, both productivity and protein concentrations increased (Austin et al., 1990). This may also be the case in pool polyculture of milkfish and Gracilaria, which is also mainly based on the food value of the periphyton to the fish.

Environmental effects of seaweed farming

The effects of seaweed farming on a coral reef environment are generally positive, especially when reef flats are used in areas with good tidal currents. However, the implementation of suitable legislation, as well as strict observance of the laws by the farmers are essential (Trono, 1993, 1994).

Crop protection

Destructive grazing by finfish, snails, sea urchins, limpets and starfish are problems in many tropical as well as temperate areas (Pringle et al., 1989). Finfish may eat large quantities of algae and a visit by a shoal can result in considerable damage. Sea urchins may almost completely destroy the vegetation of natural algal beds (Doty, 1986; Tseng, 1981b). Epiphytes can also reduce productivity.

Monocultures of seaweeds tend to be susceptible to mycoses, bacterial activity and/or viruses. Large parts of a farm can be infected, especially where plants in phycoculture are overcrowded. Literature on diseases of tropical algae is scant, except for "ice-ice", a disease of Eucheuma and Kappaphycus (Trono, 1994). This disease is characterized as one of the "malaises" of Eucheuma cultivation (Doty, 1987). It is probably not a real disease, but a symptom of poor growing conditions (Pringle et al., 1989). "Ice-ice" can be induced by manipulation in laboratory studies, although bacteria most probably accelerate the expression of the "disease" (Correa, 1997; Largo et al., 1995a, 1995b). In species that are only propagated vegetatively, ageing of the stocks may result in reduction of growth and productivity (Dawes et al., 1993; Pérez et al., 1992; Trono, 1994).

Successful maintenance in outdoor mass culture of microalgae requires constant feedback on the state of the culture (Belay et al., 1994; Richmond, 1988). In several microalgae, especially in Dunaliella salina Teodor. and some strains of Arthrospira, the ability of the algae to withstand high salt concentrations makes extensive open-air cultivation possible (being relatively free of competitors, pathogens and predators) (Borowitzka & Borowitzka, 1988; Tseng & Xiang, 1993).

Harvesting and post-harvest handling

Maturity indices

These differ for the various species in cultivation. Some culture methods allow Eucheuma plants to grow to one kg or more, while other methods allow less full-grown specimens. In addition, the optimum harvest for Eucheuma and Kappaphycus varies between different locations, depending on a number of factors including the level of loss from physical damage as thalli increase in size. A short 40-45 days growing period, with the harvesting of immature thalli of less than one kg (wet weight) is still practised in some localities, in the belief that higher yields are obtained by frequent cropping. A longer harvest interval of 50-60 days, however, produces a crop which is usually more suitable for carrageenan production (Luxton, 1993). It has been suggested that higher prices should be paid for thalli with a basal diameter greater than a given size. This may result in a better quality of the seaweeds that are offered for sale (Doty, 1986).

Harvesting

One of the advantages of phycoculture is the relative ease of harvesting and crop control. Harvest of whole plants is in some cases considered favourable to the often-used pruning methods. Over-harvesting must be avoided; this may occur frequently in the collection of wild seaweed stocks, resulting in a fluctuation of seaweed supplies. A tool to assess the best harvesting strategy for natural populations can be provided by using a simulation with the aid of a projection matrix model, which is based on studies of phenology, recruitment and mortality of the seaweed species (Ang, 1987).

Cultures of microalgae usually have a low solid content and many algal cells are very small. This means that large volumes of water have to be processed in order to extract the algal biomass. This is a major cost factor in most algal processing. The options available for harvesting include centrifugation, filtration, or flocculation (Belay et al., 1994; Borowitzka, 1994; Mohn, 1988).

Grading and drying

The need for collectors and farmers to improve post-harvest treatment (cleaning, sorting, washing, drying) is crucial to provide products with a consistently high quality (Doty, 1986; Luxton, 1993; McHugh & Lanier, 1983; Trono, 1994). The algae must be well-dried shortly after collection and as rapidly as possible. Dehydration must be sufficient to guarantee preservation of the alga, otherwise anaerobic fermentation will occur, causing high temperatures and even carbonization of the seaweeds during storage in the warehouse. In general, the moisture content is best reduced to about 20% (for Eucheuma and Kappaphycus 35%) by natural or artificial drying ("bone-dry"). Commercial seaweeds are often mixed with significant quantities of impurities such as stones, shells, sand, other seaweeds, epiphytes, as well as other products added during gathering, drying and packing (such as land weeds, leaves, wood and plastic). It is important to prevent this type of contamination of the raw material. Contact with freshwater, particularly rain, should be avoided, especially for Eucheuma and Kappaphycus. Sand causes severe problems during carrageenan extraction due to its abrasive properties (Blakemore, 1990).

The existing literature on the evaluation of seaweeds as an industrial source of phycocolloids is often confusing because the contributions generally come from scientists who often are unfamiliar with specific requirements, the different grades of phycocolloids and the analytical methods used. These evaluations usually have been made from seaweeds which are perfectly dry and clean, like herbal samples, and therefore the data have little similarity to that obtained by the manufacturers who process hundreds or thousands of tonnes of commercial seaweeds during the industrial process (Armisén & Galatas, 1987). In phycoculture the average phycocolloid yields can be improved by using more sophisticated harvesting procedures (Adnam & Porse, 1987). For microalgae usually spray-drying is used (Belay et al., 1994; Switzer, 1982).

Packing, transport and storage

Large-scale seaweed processing requires that the raw material is well stabilized in order that it can be transported over long distances, at the least possible cost, and stored for long periods before use. After dehydration, the dried seaweed is compressed with a hydraulic press into bales. Obviously it is necessary to avoid wetting during transportation and/or storage (Armisén & Galatas, 1987). All storage should be in clean, cool, dry and well-ventilated places.

In some cases the problem of storage is more difficult to solve. In Gracilaria enzymatic hydrolysis of agar may occur spontaneously, even at a relatively low moisture content. The rates of hydrolysis are variable depending on the species, its origin and conditions. This prevents long-term storage of stocks. Agar in Gelidium, however, can be preserved indefinitely in seaweeds, provided they have been well-treated (Armisén, 1995; Armisén & Galatas, 1987). When the gathered seaweeds are treated with NaOH at an adequate concentration and for the correct duration, destruction of microbial contaminants takes place, perhaps also resulting in the in-activation of hydrolytic enzymes. Sterilization by gamma irradiation, however, often causes loss of gel strength characteristics (Armisén, 1995).

For Eucheuma and Kappaphycus it is known that the material is unstable and undergoes degradation during storage above a moisture content of 35%. Above 40% moisture content the carrageenan in the seaweed may not survive transportation to the factory, arriving with characteristics unsuitable for some applications. At 25-35% moisture content seaweeds are relatively stable for periods in excess of 12 months and the thalli are also flexible which is ideal for efficient baling. At 15-25% moisture content Eucheuma thalli are extremely stable, but are too brittle and resist compression or snap during baling. Below 15% moisture content thalli remain stable, but can cause processing problems during carrageenan extraction (Blakemore, 1990). Careful drying and good baling are essential for well-packed seaweeds and lower freight costs (McHugh, 1990).

Processing and utilization

Biological products

Phycocolloids

The technical requirements for the manufacture of seaweed colloids, involving production techniques and expertise of effective marketing, put up certain barriers for producers who wish to enter the trade. However, the production technology for agar and semi-refined carrageenan is not so complex, that the development of the requisite technology is beyond the resources of most countries in South-East Asia (Bixler, 1996; McHugh, 1996; McHugh & Lanier, 1983). When used in combination with other gums different forms of phycocolloids, especially agar, may behave differently in relation to gel strength (Armisén & Galatas, 1987). Due to synergism, mixtures of Gelidium agar with "locust bean gum" (LBG) produce a more elastic gel; but this is not the case with Gracilaria agar (Armisén, 1995). Some sources of kappa carrageenan, however, show even greater synergism when mixed with LBG.

New business

When establishing a phycocolloid industry, a pilot-plant should be the first step in the evaluation of feasibility. This pre-supposes that results have been obtained from preliminary evaluations and quality control tests have been performed. Detailed knowledge of the industrial manufacturing process is essential for this evaluation, as well as knowledge of actual gel specifications required by the different markets and the practical applications of the product (Heyraud et al., 1990; Jensen, 1995). It is essential that the required seaweeds be correctly evaluated before operations start in countries or areas of potential interest. As soon as the quantities of useful algae from a part of the coast have been estimated, the quantity and quality of the colloid in the seaweeds should be evaluated in terms of its practical use. Representative sampling is very important and samples should be immediately packed in strong, waterproof, well-fastened bags. As soon as samples are received in the control laboratory, the impermeability of the polythene bags is verified and registered in the protocol. Next, aliquots need to be taken in such a way that their homogeneous composition is guaranteed, so that determinations can be made on moisture, content of pure seaweed and extraction of an aliquot part of the sample (Armisén & Galatas, 1987). It is impossible, however, to assign a general extraction method which is valid for any phycocolloid.

Tests

Gels of algal polysaccharides are generally made with 0.5-2% polymer per weight. Besides being characterized for gel and sol temperatures, these gels are tested for break force or gel strength and penetration. These parameters are measured on devices aptly called gel testers. These are machines which determine, by various means, the force necessary to break the surface of a gel (i.e. break force, expressed in g/cm²) and the amount of deformation of the surface of the gel at break point (i.e. penetration, expressed in cm) (Lewis et al., 1988).

Methods for structural analysis as well as a simple laboratory test for the determination of gel strength are available (Cosson et al., 1988; Czapke, 1979; Heyraud et al., 1990; Lewis et al., 1988).

Agar

The freeze-thaw method

The discovery (around the year 1658) of the "freeze-thaw" extraction of agar is attributed to Japan (Booth, 1979). Agar extraction is a fairly simple process. Frozen agar gel liberates water as it thaws, profiting from the insolubility of agar in the cold (Armisén, 1995). Alternatively, synaeresis is often applied, especially in agars produced from Gracilaria . The term synaeresis is used in agar technology to describe the process whereby pressure is used to exclude liquid from the gel. Boiling is necessary to dissolve agar in water. The insoluble residue is usually removed by some means of filtration and the liquid, when cooled, forms a gel. Solutions with 1-1.5% agar stiffen to a firm gel when cooled to between 36 - 42 °C and the gel will not melt below 85-90 °C (Indergaard & Østgard, 1991). By alternately freezing and thawing the gel several times, the water is removed and a dried "strip" of agar is produced. Agar is sold in strip form, but also in powder form (McHugh, 1996). Details on processing techniques and analysis of physico-chemical properties of agar are widely available (Armisén, 1995; Armisén & Galatas, 1987; McHugh & Lanier, 1983; Montaño & Pagba, 1996). Agar manufacturing has the advantage of being feasible on both small or large scales, with the corresponding capital outlay.

Gelidium and Gracilaria

Originally only Gelidium agar constituted what was considered genuine "agar", assigning the term "agaroids" to the products extracted from other seaweeds. This differentiation is no longer accepted. In 1984 approximately half of all agar produced came from members of the Gelidiaceae, the other half were mainly from Gracilaria (Armisén & Galatas, 1987). The different seaweeds used as raw material in agar production gave rise to products with differences in their behaviour. For this reason, when agar is mentioned, it is customary to indicate its original raw material as this can influence its application. To describe the product more accurately, it is usual to mention the origin of the seaweeds, since Gracilaria agar from one area of the world has different properties from Gracilaria agar from another area.

Chemical treatments

An increase in agar gel strength was obtained through improvement of the industrial process. Treatments of the seaweeds prior to extraction are very important as they will determine to a high degree the characteristics of the agar obtained. Strong alkaline conditions increase gel strength, especially in Gracilaria agar (Armisén & Galatas, 1987). The treatment, called sulphate alkaline hydrolysis, must be adapted to the seaweed used, to obtain as much desulphation as possible whilst avoiding the yield losses that this process can cause (Armisén & Galatas, 1987; Villanueva et al., 1997). Other corrective treatments using an alkaline solution eliminate a large quantity of foreign substances. This alkaline treatment uses sodium carbonate and is milder than the alkaline treatment with sodium hydroxide which used to improve gel strength. Pre-treatment with acetic acid, however, may also result in higher agar yields and gel strength (Roleda et al., 1997).

The gelification process in agars may be blocked by chaeotropic agents, which prevent the formation of hydrogen bonds. This reversible process occurs when urea, guanidine, potassium iodide, tannic acid or sodium thiocyanate are present. The addition of glycerol in moderate quantities avoids this effect.

The market

Agar, contrary to industrial grades of other phycocolloids, is marketed pure, without any mixture. There are different types of agar available on the world market (Montaño & Pagba, 1996; Ohno & Critchley, 1993):

Native and natural agar (from Gracilaria) usually can not be classified as bacteriological grade agar, as there is a high content of methoxyl groups and consequently high gelling temperatures (Murano, 1995). Half of the world supply of agar is directly used in food. In Asia there is considerable household consumption of "natural agar", mainly in traditional cooking, which is often marketed in "strips", in bar-like "squares" or in pill form. These are mixtures in which Gelidium agar dominates, but which can not be used for industrial food agar (Armisén, 1995; Armisén & Galatas, 1987).
Industrial agar is sold world-wide in powder form, as pharmacological grade, biotechnological grade, bacteriological grade and purified agar. The source of these grades is mainly Gelidium (Armisén, 1995).
Food-grade industrial agar is mainly marketed in powder form and comes mostly from Gracilaria. A food-grade agar should have a moisture content of less than 18%, ash content of less than 5%, gel strength greater than 750 g/cm2 (Nikan-Sui method) and a bacterial count below 10 000 bacteria/g. Usually the lead content is specified as less than 5 ppm and arsenic less than 3 ppm (Armisén & Galatas, 1987). Food-grade agar is the least valuable of the industrial agars, because it meets neither the standards for bacteriological agar nor those for sugar-reactive agar. Demand for food-grade agar can easily decline due to replacement of the gel by other phycocolloids, especially carrageenans.
Bacteriological agar (also known as "standard agar") needs strict physical-chemical control and requires the absence of haemolytic substances and bacterial inhibitors. Nevertheless, there are no official general specifications for universal categorization as bacteriological agar (Armisén & Galatas, 1987). It must have a good transparency in sol and gel forms and a consistent gel strength from lot-to-lot. Uses in microbiology are based on special properties: a gelling temperature of 36 ± 1.5 °C, a melting temperature of 87 ± 2.5 °C and lack of hydrolysis by bacterial exo-enzymes. The above temperatures refer to culture media which contain 10-11 g agar/l. Requirements are a low content of oligomers and proteins (so that these can not form a source of nutrients for microorganisms), a low and regular content of electro-negative groups that could cause differences in diffusion of electro-positive molecules (e.g. antibiotics, nutrients, metabolites), freedom from toxic (bacterial inhibitors) and haemolytic substances that might interfere with normal haemolytic reactions in culture media as well as free from contamination by thermophilic spores (Armisén, 1991). Bacteriological agar, which is the highest agar grade, is prepared from Gelidium (and Pterocladia), since Gracilaria and Gelidiella give agars with gelling temperatures above 41 °C.
Sugar-reactive agar: gel strength, with very low sulphate content and high molecular weight, increases when sugar is added (Armisén, 1995). Sugar-reactive agar is able to form a good gel in strong sugar solutions.
Purified agar is produced in much smaller quantities. This expensive agar is a bacteriological agar that could also be used in biochemistry for electrophoresis or immunodiffusion. It can be considered as an agarose fore-runner, which is still being used for economic reasons (Armisén & Galatas, 1987).

Agarose

Interest in agarose resumed with the search for an electrically neutral polysaccharide suitable for use in electrophoresis and chromatography. Agarose is a derivate of high-quality agar. Its yield can be 70-80% of that of agar. The rather small market for this special product is expanding because of its current use in tissue culture and as a medium for electrophoresis. Demand is expected to remain high due to biotechnological and biochemical needs. A technique for agarose preparation using polyethylene glycol results in a product of good purity (Armisén & Galatas, 1987; Russell et al., 1964). Good commercial agarose is considered to have less than 0.35% sulphate; the pyruvate content is likewise very low (Armisén, 1991). The agar of Philippine Gracilariopsis heteroclada is a potential source of agarose (Hurtado-Ponce, 1994).

Modern commercial agaroses for use in biochemical separation techniques have to be chemically modified (Armisén & Galatas, 1987).

Bacteria

Some bacteria (e.g. Cytophaga and Pseudomonas spp.) can produce agar-degrading enzymes (Forro, 1987).

Carrageenan

Traditional production methods

The first mention of the use of carrageenan in the food industry is from the mid-19th Century as a fining agent in beer brewing (Booth, 1979). The traditional, refined products are made by dissolving the carrageenan out of the seaweed, filtering off the unwanted residue, precipitating the carrageenan from the extract, then separating and drying it. Before the extraction process, the seaweeds are digested with hot water under alkaline conditions to extract all of the carrageenan. The algae, however, also may be soaked in sodium, potassium or calcium chloride according to the type of gel required. In general, treatment with sodium salts results in a viscous product with low gel strength; calcium salts give an elastic gel and potash salts produce a firm gel. The solution of carrageenan is separated from the seaweed solids by filtration, or by centrifugation followed by filtration (McHugh & Lanier, 1983; Stanley, 1987).

Semi-refined carrageenan

In the Philippines "semi-refined" carrageenan is produced from seaweeds known as Kappaphycus alvarezii. There are many different names and acronyms for this "semi-refined" carrageenan. The method used was introduced in the Philippines by Japanese chemists in 1978 (Llana, 1990). Baskets full of seaweed fronds are immersed and cooked in hot, aqueous potassium hydroxide 8.5% solutions and soaked 5-6 times in freshwater to extract most of the residual alkali. In the production process most of the non-carrageenan matter in the seaweed is dissolved and removed, leaving a solid residue of cellulose and carrageenan, which is dried and milled (Stanley, 1987). The product contains some insoluble material, and thus will not yield clear gels (Neish, 1990). Material handling in the production process is greatly reduced and energy costs are lower than in the case of the full industrial process. Thus production costs are only 25-50% for that of refined carrageenan (McHugh, 1996). Therefore, the price of semi-refined carrageenan is about 50% of that of the refined product (McHugh & Lanier, 1983). With the advantages of being easier and cheaper to manufacture, it is feasible for an entrepreneur to develop the semi-refined carrageenan-processing technology on an experimental scale for a modest capital outlay, and then gradually increase the scale of operation as is done in the Philippines (Anonymous, 1998; Neish, 1990). The process is most effective when using Kappaphycus alvarezii, but with careful control it is also possible to treat Eucheuma denticulatum and its iota carrageenan. Usually, however, kappa carrageenan is the active component in semi-refined carrageenan.

Refined carrageenan

The production of refined carrageenan involves a very complex industrial process (Anonymous, 1998; Bixler, 1996; Luxton, 1993; McHugh, 1996; Neish, 1990).

Problems

The quality of carrageenan has been decreasing recently; this is thought to be the result of hybridization with native plants in the farming areas in the Philippines (Lobban & Harrison, 1994). Some bacteria, (e.g. Pseudomonas sp.) are capable of degrading carrageenans (Forro, 1987).

Alginate

Although alginate was already manufactured in 1881 in Scotland, the first commercial production of alginate was launched in 1929, and its use in food was patented just after 1930 (McHugh & Lanier, 1983). There is, however, only limited information available on the manufacture of sodium alginate (Lewis et al., 1988). Alginate is probably the most difficult of all the three colloids to manufacture. Chemically, its extraction is a simple process but the physical separation of insoluble cellulose from thick solutions presents formidable difficulties.

In general, alginates are manufactured in five basic operations (McHugh & Lanier, 1983):

Removal of soluble matter by washing with water and reduction of the seaweeds to a size suitable for further processing.
Extraction of alginate with sodium carbonate and filtration; the product may be bleached at this stage.
Precipitation of the calcium salt by adding calcium chloride.
Conversion of the calcium salt to alginic acid by treating it with hydrochloric acid.
Conversion of alginic acid to its sodium salt by using a suitable alkali; the salt is then dried.

Usually the quality of Sargassum alginate is thought to be rather poor and not good enough to be used by the textile printing industry (McHugh & Lanier, 1983). Nevertheless, a local alginate producer in Indonesia sells about 100 t of locally produced Sargassum alginate to the textile industry (McHugh, 1996). Comparative research, moreover, suggests that alginate produced from Malaysian Sargassum is of a high quality (Fasihuddin & Siti, 1994).

Bacteria

Several bacteria, in particular Cytophaga spp., are capable of degrading alginates, especially under anaerobic conditions (Forro, 1987).

Chemical products

The potential of microalgae as a commercial source of carotenoids has been recognized for some time and extensive research and development of β carotene production using Dunaliella salina is underway in various parts of the world. After harvesting, the biomass must be processed to extract either glycerol or β carotene (Chen & Chi, 1981; Ruane, 1974). Microalgae are ideally suited as a source of stable isotopically labelled compounds (Apt & Behrens, 1999).

Genetic resources and breeding

For species grown in phycoculture the possibility arises for cultivation of improved seaweed strains with predictable and better yields. In the Kappaphycus alvarezii group several cultivars are now known. It might be possible to cross these to provide better yields, although hybridization has not yet succeeded (Trono, 1994). In Eucheuma denticulatum all crossing experiments have also so far failed (Pérez et al., 1992). References to tropical species are generally lacking in the literature on genetic studies in marine algae (van der Meer & Patwary, 1995). However, the presence of numerous unknown Gracilaria spp. in particular offers tremendous opportunities for the development of ideal seedstock strains for the agarophytes (Shen & Wu, 1995; Trono, 1994).

Genetic engineering of microalgae has provided promising results, that are not yet fully applicable (Craig et al., 1988). Highly sophisticated molecular systems are being used to include recombinant techniques especially in Cyanobacteria and some unicellular eukaryotic algae, but these new techniques have not yet contributed directly to a commercial product.

Prospects

There is a general tendency to deplete natural resources and algae are not an exception. To counteract this, better resource management, with closer studies of the economic interactions and information on indigenous algal species are required. Algae are able to provide sustainable raw materials that are well-suited to applications in science and technology. Such uses can contribute to the industrial transformation of countries in South-East Asia as well as to the sustainable use of the available biodiversity (Frankenberg, 1986). The role of education and training of farmers, researchers, employees and businessmen is essential to these mutual developments. Realization of the full potential of the seaweed industry must result in the provision of financial resources, incentives and proper training. Furthermore, there is a requirement for increased research into harvesting, cultivation of algae and improvement in the quality of the algal products. Finally, the absence of adequate and up-to-date international market information obstructs the trade in algae and tends to reduce profits to the producers (Pringle et al., 1989).

The long distances between the centres of phycocolloid production and its markets will become an unsustainable luxury. The phycocolloid industry must work with producers to develop refined products within the areas of seaweed production. If the processing plants can be decentralized and constructed on a smaller scale, some of the problems of disposing the waste might be solved by incorporation of both waste water and biomass residue into agricultural production (Kapraun, 1999). Discussions on the introduction of cultivars of foreign species as an alternative to depletion of natural populations of target species should be continued.

Good prospects for algal products exist, especially in the fields of fine chemicals, antibiotic substances, anticancer medicines, herbicides, vermifuges, insecticides, etc. Several algal-derived substances are very different from those that can be obtained from terrestrial organisms and therefore have different applications (Apt & Behrens, 1999). Cultivation of selected algae for production of proteins, lipids, carbohydrates, vitamins, etc. can be expected and will be augmented. Moreover, phycoculture can also be used to obtain large amounts of biomass that can be used for methanization for energy production, an option that becomes more feasible because of international agreements on CO2-reduction (Gao & McKinley, 1994).

In recent years, developments in biotechnology have swiftly transformed laboratory discoveries into commercially useful products. Algae offer promise as direct and indirect renewable biological resources. A special application is being developed in the production of high-performance paper from seaweeds, mainly alginate fibres (Kobayashi, 1990). Promising prospects for microalgae are presented in the literature (Borowitzka, 1994; Gladue & Maxey, 1994; Lee, 1997; Radmer & Parker, 1994; Stevens et al., 1994; Vonshak, 1997).

Research

Phycoculture in South-East Asia is usually represented by one person in an academic department. This specialist in phycoculture must have the training of a plant physiologist, agronomist, aquatic ecologist, oceanographer or limnologist, sociologist, agricultural economist and phycologist, hopefully also with a little natural products chemistry and reasonable writing skills (Doty, 1979). There is a distinct lack of multi-disciplinary research teams in phycoculture. Problems are also encountered due to the limited availability of information about phycoculture due to both political and commercial factors and linguistic barriers (Critchley & Ohno, 1998; Ohno & Critchley, 1993; Pérez et al., 1992; Trono, 1994).

Commercial cultivation of all promising species is not yet possible, especially cultivation of several agar-producing species in the genera Gelidiella, Gelidium and Pterocladia. In addition, there are erratic results in the production of algae bearing iota carrageenan which still require more attention. Nevertheless, attempts to increase production from natural beds of Gelidium, by increasing the area of rocky substrates, farming it with ropes and rafts, and even cultivating free-floating plants in onshore tanks have met with some success (Lobban & Harrison, 1994; Melo et al., 1990).

The production of semi-refined carrageenan is promising, but may also need some adjustments (Anonymous, 1988; Bixler, 1996; Luxton, 1993).

Many new developments in biotechnology would not have been possible without phycocolloids and their derivates (Renn, 1990). Phycotechnology now constitutes a special branch of biotechnology and algae form the main focus of interest.

Main research institutions in phycology

The following main institutions in South-East Asia are involved in phycological research (usually research on seaweeds):

Indonesia

Research and Development Center for Oceanology, PPPO-LIPI, Jakarta
Marine Station of PPPO-LIPI, Ambon (not active at the moment)
Agency for the Assessment and Application of Technology, Seaweed Research and Development Team, BPP Teknologi, Jakarta

Malaysia

Institute of Advanced Studies, University of Malaya, Kuala Lumpur

The Philippines

Marine Science Institute, University of the Philippines, Diliman, Quezon City
Marine Laboratory, Silliman University, Dumaguete City
Marine Biological Section, University of San Carlos, Cebu City
Mindanao State University, Naawan
Many universities and national organizations have phycologists in their staff, whereas industrial laboratories involved in the production of seaweed products are often active in seaweed research

Singapore

Department of Microbiology, National University of Singapore (specialized in research on microalgae)

Thailand

Faculty of Fisheries, Kasetsart University, Bangkok

Vietnam

Nha Trang Institute of Materials Science, Production of Seaweeds, Nha Trang City

Marketing infrastructure

The marketing distribution system for seaweeds and their products in countries such as Indonesia, Malaysia and the Philippines was poorly organized in the early years of development of seaweed cultivation (Doty, 1986; McHugh & Lanier, 1983; Trono & Ganzon-Fortes, 1988). Small traders acted as middlemen to the large traders. The buyers were the exporters of the phycocolloid industry, who often established strict product specifications, upon which sales and acceptance were dependent. But exporters' purchase requirements and prices were also heavily influenced by the buying policies of foreign users. Thus, during periods of short supplies and rising prices, seaweed collection and farming was stimulated and quality requirements were lowered. The lack of stability in buyer policy induced farmers to take less care with their crops, resulting in production of inferior seaweed. This pattern of market fluctuation seemed to be more or less cyclical and applied to carrageenan-bearing seaweeds as well as the agar-bearing ones (Luxton, 1993; McHugh & Lanier, 1983). However, several of the Philippine producers, mainly making and marketing semi-refined carrageenan for human consumption, have now formed a trade association (SIAP) to represent their interests (Anonymous, 1998; Bixler, 1996). This will hopefully result in more stable prices for the seaweed farmers and improvements in the quality of raw materials.

Phycocolloids

The market for phycocolloids largely depends on relatively low prices. Agar, carrageenan and alginate may compete directly with one another in some end-use markets. Specialty gums, such as carrageenans, are sold on the basis of their functionality in specific applications. For this reason carrageenan manufacturers have to devote a substantial portion of their budget to maintaining active applications and technical marketing groups to serve the ever-changing needs of their customers. In that way the carrageenan industry tries to sustain the growth that it has enjoyed for the last 30 years. A survey of market factors (food product innovations, especially different forms of liquid diets and fat substitutes) and the successful application of carrageenan in further-processed poultry and meat has been documented (Bixler, 1996). Phycocolloids compete with gums from flowering plants, such as guar gum and locust bean gum and cheaper cellulose derivates. A variety of agar substitutes have been developed for gel media in microbiology, including alginate and polysaccharides of non-algal origin, such as plantgar and gellan. For a number of important food uses, however, no synthetic or other natural gums have been found that can replace phycocolloids on a cost-effective basis. This fact seems to assure the continued viability of the industry. New food applications will require gums which demonstrate pH and temperature stability, salt tolerance and cold stability; these properties are found in seaweed extracts (Guist, 1990).

Agar

The instability of the world agar market has resulted in price levels that have priced agar out of several end-use markets. A stable supply of seaweed from phycoculture would help to stabilize the price of agar. On the other hand, labour costs and manpower shortages may result in all harvested Gracilaria crop being used for the production of mollusc feed (Ajisaka & Chiang, 1993). Agar was used as a gelling agent in canned pet food until price rises led to its replacement by carrageenan. The agar market, however, still presents good potential for countries in South-East Asia. A global marketing approach to agar includes identification of all possible uses for agar by consumers and preparation of a good product launch (Becker & Rotman, 1990).

Carrageenan

The potential for culturing carrageenan-bearing seaweeds in countries in South-East Asia is very large. However, expansion in the number of growers has resulted already in an over-supply of certain forms of carrageenan and may lead only to the spreading of sales among a greater number of producers (at lower prices) as well as to disputes amongst the different carrageenan producers (McHugh & Lanier, 1983).

In many cases, price is not the determining factor in a buyer's choice of a seaweed colloid. Quality, and its reproducibility from one batch to another may be more important. Many buyers of seaweed colloids, satisfied with one particular brand or grade will stay with it, despite a higher price, because the risks of changing may not seem worth the savings. Thus brands already established in a market place often hold a very strongly entrenched position (McHugh & Lanier, 1983). Economic practices to encourage better-quality farmed seaweed should include bonuses or higher prices paid by industry for value-added or higher-quality seaweeds due to on-site post-purchase treatment, better drying practices and basal diameter standards for the harvested thalli, resulting in a fair partitioning of the export prices (Doty, 1986; Trono, 1990).

Biotechnology

The algal biotechnology industry needs to continue to develop more markets for algal products. Not only does this require the raising of awareness that algal products are suitable alternatives to other products, but standards of quality for algal products have to be set and the appropriate registration achieved (Borowitzka, 1994).

Differentiation of products

Phycocolloids

New markets for phycocolloids will be found in pharmaceutical applications such as vaccines, drug delivery, anticancer, antirhombogenic applications and antiadhesive drugs and diagnostics. The volume of phycocolloids needed for such purposes will be relatively small, but chemical purity and precisely identified structural composition will definitely be reflected in increased prices (Indergaard & Østgard, 1991). Cells entrapped in phycocolloid gels have many potential applications in biotechnology, ranging from biocatalysts in fermentation and immobilized algae for metal recovery to artificial seeds in agriculture and carrier materials for transplantation of living tissue (Jensen, 1993; Skjak-Bræk & Martinsen, 1991).

Agar

Demand is expected to increase for bacteriological agar and for agar strips for food. The high-quality agar required for bacteriological use can only be made from a limited number of seaweeds, notably Gelidium and Pterocladia. These seaweeds are in short supply and, as a result, production of bacteriological grade agar may be restricted in the future (McHugh & Lanier, 1983). However, agar from Gracilaria can be improved by treatment with alkali, resulting in better gel strength at the cost of lower agar yields (Armisén & Galatas, 1987). There is an urgent need, however, for the agar industries to develop studies for the promotion of agar use in food applications (Armisén, 1995).

Carrageenan

Use of carrageenan, especially semi-refined carrageenan, in further-processed poultry and meat is a proliferating market. For all carrageenan producers there is a constant need to seek new applications for these phycocolloids. They must be willing to invest in both basic carrageenan research and development and in its applications (Bixler, 1996). In the future, carrageenan may be used to produce nearly fat-free hamburgers (Lobban & Harrison, 1994). New methods for rapid screening of carrageenan composition of carrageenophytes are being developed (Vreeland et al., 1992).

Alginate

There is likely to be an increase in demand from tropical countries for alginate for use in the cotton textile printing processes. The market for industrial textile applications of alginates is, however, already covered by dominating western industries. The steady global growth of the alginate industry by some 5% annually is nevertheless expected to continue (Jensen, 1993).

Microalgae

The use of microalgae as sources of valuable chemicals is especially promising and the next few years will probably see a continued expansion of the range of commercially available microalgal products (Borowitzka, 1994; Lee, 1997; Vonshak, 1997). The development of an automated microalgal culture system in Malaysia is an attractive prospect (Ho et al., 1994).

W.F. Prud'homme van Reine