Eucheuma denticulatum (PROSEA)
Eucheuma denticulatum (Burm.f.) Collins & Herv.
- Protologue: Univ. Calif. Publ. Bot. 53: 106 (1917).
- Family: Solieriaceae
- Chromosome number: 2n= 20
- Fucus denticulatus Burm.f. (1768),
- F. spinosus L. (1771),
- Eucheuma spinosum J. Agardh (1847, nom. illeg.),
- E. muricatum (S.G. Gmelin) Weber Bosse (1928).
- Usually the vernacular names are common names for all Eucheuma and Kappaphycus spp.
- Indonesia: agar-agar, agar besar (common names for all Eucheuma and Kappaphycus spp.), "spinosa" (common commercial name for all genuine Eucheuma spp., especially for E. denticulatum)
- Philippines: ruprupuuk (Ilocano), guso (Visayan), canot-canot (Ilocos Norte)
- China: chilints'ai, qilinca, gilin cai.
Origin and geographic distribution
E. denticulatum originally occurred only in the Indian Ocean (along the east coast of Africa from Natal to Djibouti, although it was probably only recently introduced into the latter country, India, Bangladesh, most island groups in the Indian Ocean, including small islands in northern Australia), in South-East Asia and in neighbouring parts of the western tropical Pacific (as far as New Caledonia). It has recently been distributed further eastward by man into the Pacific at least as far as Hawaii, Micronesia (Pohnapei) and Christmas Island in easternmost Kiribati. In South-East Asia it occurs in Peninsular Malaysia, Singapore, Indonesia (originally especially in the Moluccas), the Philippines and Vietnam. In Indonesia, farming trials with E. denticulatum carried out before 1984 failed, but nowadays the largest production area is around Bali.
E. denticulatum is a source of iota carrageenan. It appears that the carrageenan from E. denticulatum is the most valuable to industry, since it becomes an ideal iota carrageenan upon alkali modification. It is used in industrial food and beauty aid products, in pet foods, in granulated or hydrated gel components in various formulations, or prepared as a stew mixed with vegetables. E. denticulatum can also be eaten fresh or blanched in boiling water and mixed with salad garnish, or made into "Eucheuma candy" or "kue" by cooking in water until a gel is formed, whereafter sugar is added. It is used as garnish for other dishes such as fish. In Lombok (Indonesia) about 400 t (wet weight) of E. denticulatum is used annually to prepare a boiled foodstuff, wrapped in banana leaf and known as "pencok". In some areas it is also used as fertilizer. It can be applied in the control of heavy metal pollution by Pb and Cd, since this alga can accumulate these metals.
Production and international trade
E. denticulatum was exported from Indonesia to China already in the 1920s, chiefly from the southern coast of Sulawesi and adjacent islands. The Philippines and Indonesia are the two main producers of E. denticulatum. Annual production through phycoculture in the Philippines was about 8173 t in 1986 and had risen to 20 190 t by 1994 (all wet weights). In the Philippines, E. denticulatum has always been more difficult to grow than Kappaphycus alvarezii (Doty) Doty ex P.C. Silva, while in Indonesia farming of both algae seems to be equally easy. For 1987 the total production by phycoculture of E. denticulatum (dry weight) for Indonesia was 4000 t and for the Philippines 2500 t, for 1990 it reached 4500 t and 2111 t, whereas for 1991 it amounted to 10 000 t and 2000 t respectively. The estimated potentially exploitable area for "Eucheuma culture" in Indonesia (probably including Kappaphycus culture as well) is 9000-10 000 ha, with a production capacity of 45 000 t/y (dry weight). This area, however, has not yet been fully exploited, resulting in a total seaweed production in Indonesia in 1994 of less than 2700 t, including harvests of Gracilaria, Gelidium and other algae.
The FOB (Free on Board) selling price of E. denticulatum in Indonesia in the period 1986-1992 was particularly unstable, being US$ 0.32-0.43/kg in 1987. The CF (= Costs and Freight) price for dried E. denticulatum for Europe was in 1987 US$ 390/t and for the United States US$ 450/t. Increasing demand, particularly from the United States, and the resulting competition with European carrageenan processors for the limited resource, was the principal cause of the FOB price escalation to over US$ 1/kg in 1990. Added competition came from the growing E. denticulatum food market in China, for which Hong Kong buyers started activities in 1986. However, unlike the case of Kappaphycus alvarezii production, the increased demand for E. denticulatum did not result in a consistent increase in farm production. Nevertheless, prices in 1991 fell rapidly, due to a large decline in orders from foreign carrageenan processors, leaving much of the 1991 harvest unsold. Consequently, production of E. denticulatum in Indonesia in 1992 dropped to 1500-2000 t (dry weight), mainly for the more stable Chinese food market. Although 95% of the E. denticulatum crop is now farmed, in 1989 wild cropping in Indonesia was still considerable, with the largest amount, 800 t (dry weight), coming from the Aru Islands (Moluccas).
Extracts of E. denticulatum show antitumour activity against Ehrlich carcinoma with an inhibition rate of 41.2%. E. denticulatum (dry weight) contains per 100 g: crude fat 0.7-1.6 g, crude protein 5.1-6.8 g, crude iodine 2.8 g, ash 15.0 g, crude fibre 5.0 g, nitrogen 0.8 g, mannitol 25.4 g. Minerals in g/100 g of dry weight: K 12.0, N 0.5, Na 4.8, Ca 0.6, Mg 0.8, P 0.1, and in ppm: Zn 13, Cu 7.5, Fe 66 and Mn 14. The sulphate content of the iota carrageenan is often 30% or higher, while the 3,6 anhydro-galactose ester content is about 27%.
E. denticulatum produces H2O2 under oxidative stress conditions and then also releases bromoform, diiodomethane, dibromochloromethane, perchloroethylene, chloroiodomethane, chloroform, sec-butyl iodine, methyl iodide, methyl chloroform, carbon tetrachloride, trichloroethylene and butyl iodide into its growth media. These volatile halocarbons (VHCs), of which bromoform and diiodomethane are the dominant ones, are also formed under optimal growth conditions and can be efficient in catalyzing stratospheric ozone removal.
- Perennial plant with thalli forming low, rigid, caespitose clumps.
- Primary branches terete or cylindrical, bearing whorls of 1-8 mm long spinose determinate branchlets; branching at predictable intervals, forming distinct "nodes" and "internodes" especially towards terminal portion of branches; branchlets sometimes developing into secondary terete laterals.
- Cross-section of branch revealing a dense cylindrical core of thick-walled, very small rhizoidal cells at centre of medulla.
- Cystocarps borne near tips of lateral spines; tetrasporangia zonate, embedded in cortex; spermatangia forming surface sori.
Growth and development
The growth of thalli of E. denticulatum is initiated by a group of apical cells. Growth rate in laboratory culture, determined by use of the respiration method, is 1-2% per day. The average daily growth rate in open air phycoculture in the Philippines is 1-5%. The optimal growth rate is about 3.5%/d, resulting in a doubling of the crop in 28 days. Daily growth in E. denticulatum is generally lower than in Kappaphycus alvarezii.
Haploid male and female gametophytes are produced from meiospores released by tetrasporophytes, suggesting a genetic determination of sexual phenotypes. It is also suggested, however, that spores from tetrasporophytes of E. denticulatum may form germlings that grow into sporophytes again. In cultures, cystocarpic plants are often lacking, although antheridial and tetrasporic plants can be frequently found in these cultures. However, most specimens used in phycoculture are sterile and propagate by fragmentation. Plants grown from material imported from the Philippines and in phycoculture on rafts in Djibouti waters all were fertile sporophytes, except 8 of the tested 10 000 specimens, which happened to be fertile female gametophytes.
Other botanical information
The cylindrical core of rhizoidal cells distinguishes E. denticulatum from other Eucheuma spp. Several forms (cultivars) of E. denticulatum are farmed, amongst which green, brown and red ones. These forms retain their pigment characteristics after long-term laboratory culture, suggesting a genetic basis. The red forms are better adapted to high illumination ("sun"), the green and brown forms to lower illumination ("shade").
E. denticulatum is commonly found growing strongly attached to coralline gravelly-rocky or coarse sandy-rocky substrates at the intertidal to the upper (shallow) subtidal zone on the reefs exposed to moderate wave-action or strong tidal currents, where it may form thick clumps or beds. The fusion of its branches upon coming in contact with each other and its ability to form secondary holdfasts at tips of branches result in the formation of thick and strongly attached clumps or carpet-like beds which are able to withstand moderate to strong water movement. This alga has never been recorded in calm or protected habitats. Required temperatures for optimum growth rates are 24-30 °C, whereas high solar energy levels are optimal. The preferred pH is 8 and salinity should be 32‰. Nitrogen levels should be 2-4 μg/l and phosphate levels 0.5-1 μg/l.
Propagation and planting
E. denticulatum in phycoculture propagates largely through vegetative fragmentation. Laboratory grown branches, transplanted to rafts in the field in the Philippines, showed daily growth rates as high or even somewhat higher than other reported growth rates. In laboratory culture 3-5 cm long branches can be grown in inexpensive laboratory media prepared from autoclaved seawater enriched with either a commercial Philippine liquid fertilizer made from seaweed extract ("Algafer"), coconut water or soil extract.
E. denticulatum is farmed using the same methods as for Kappaphycus alvarezii, i.e. the fixed off-bottom mono-line, the raft-method or the floating long-line method. In Indonesia the two first mentioned culture methods for E. denticulatum showed no statistical significant differences, while the floating long-line method is not commonly practised in Indonesia. Polypropene rope 4 mm in diameter can also be used instead of the monofilament nylon culture lines. Generally, commercial production of E. denticulatum is found in areas with low tide ranges, allowing for a longer working period at a site than in areas with large tide ranges.
E. denticulatum has a greater tolerance to desiccation than Kappaphycus alvarezii, and thus can be farmed at sites with a longer period of tidal emergence. It can also be farmed where it is continuously submerged at relatively wave-protected sites. Productivity can be particularly high where there is freshwater run-off from land during the wet season. Such areas give poor growth of K. alvarezii. Conversely, off-shore flat shallow reef areas with moderate water movement are unfavourable for E. denticulatum farming.
Diseases and pests
One of the major problems in the culture of Eucheuma (as well as Kappaphycus) is the disease "ice-ice", which can wipe out entire crops. The early signs are slow growth, thalli becoming pale and losing their gloss, followed by white spots appearing on the branches, which finally break off at these affected spots. Entire thalli may become affected. The occurrence of ice-ice may be mainly due to adverse ecological conditions such as low light intensity, low nutrient availability, extreme water temperatures and low water movement. Whitening can also be caused by bacterial pathogens, while the high incidence of epiphytes may also affect E. denticulatum. Farm maintenance can be improved by removing heavy growth of epiphytes, such as Enteromorpha green algae. Overproduction of oxygen radicals and volatile halocarbons by the algae, which, when induced at a balanced level might protect them against epiphytes and grazers, may cause ice-ice in Eucheuma monocultures.
Another problem is "pitting" probably caused by mechanical wounding of the cortex, leading to the formation of cavities penetrating the cortex in one place and expanding into the medulla region beneath, often resulting in thallus breakage. "Tip darkening" or "tip discolouration" may occur when water is too cold or too warm. In most cases the affected parts decay, leading to fragmentation and losses.
Grazing by fish and invertebrates is one of the major causes of loss in biomass. The use of the floating methods (raft and long lines) has virtually eliminated the effect of benthic grazers such as sea urchins and starfish.
In some areas a shortage of available Mn, Fe, Cu and Zn may result in reduced plant resistance to physical stress in farmed E. denticulatum. It is suggested that destruction of seagrasses in preparing the grounds for monoculture seaweed farms may interrupt a seagrass-mediated availability of those micro-elements for cultivated algae.
Depending on the growth rate, an E. denticulatum crop of 2-3 months old may be ready for harvesting. Individual plants may then weigh about 1 kg. Often complete harvesting is practised, whereby whole plants are detached from the farm support system, placed in rafted baskets or directly transferred to a boat and brought to the drying area. In some areas growing periods of 40-50 days are still practised, resulting in the harvest of immature thalli of less than 1 kg (wet weight). This is done because it is thought that higher yields are obtained by frequent cropping. A high market demand encourages early harvesting but leads to poor "seed" selection for replanting.
Depending on the quality of a crop of E. denticulatum, the carrageenan yield varies between 30-50% of the clean anhydrous seaweed. The carrageenan content and quality of cultured material and commercial seaweed is much influenced by post-harvest treatment.
The wet (85% moisture) to dry (35% moisture) ratio for E. denticulatum is 6:1 or 17%. Carrageenan yields in E. denticulatum are usually high (up to 67%).
Handling after harvest
The harvested crop of E. denticulatum is cleaned of debris and other algae, and then sun-dried. The drying place is usually a platform made of bamboo slots lined with nylon netting material to prevent contamination. The crop is then spread evenly, and regularly turned to hasten drying. Drying may take 2-3 days during sunny wheather. The dried seaweeds are then packed in plastic sacks and stored under dry conditions.
Contact with freshwater, particularly rain, should be avoided, as this extends the drying time and reduces the salt content, both of which cause degradation of the seaweed or carrageenan. Washing in freshwater has no added value and in most cases reduces the quality of carrageenan. However, for the Chinese food market E. denticulatum material has to be rewashed in freshwater and subsequently bleached.
Inadequate drying of E. denticulatum and post-harvest contamination with sand result in poor quality and lower prices. If the alga contains more than 35% moisture the carrageenan is unstable and liable to degradation during storage. Above 40% moisture, the carrageenan may not survive transportation to the factory, resulting in too low percentages for some applications. Thus, E. denticulatum should never be stored wet. Between 25-35% moisture, the composition of the alga is relatively stable for periods of 12 months or more, and thalli are flexible enough to be baled efficiently. At lower moisture content levels thalli become too brittle, causing problems during carrageenan extraction.
To avoid degradation of the carrageenan of the harvested E. denticulatum material, fresh or recently dried seaweed can be immersed in a weak alkali solution to produce "stabilized" raw material for carrageenan production. Dried material of E. denticulatum and Kappaphycus alvarezii should never be mixed, as it is then impossible to obtain suitable carrageenan quality.
The stored seaweed should be baled before transport to promote easier handling and reduction of shipping costs. Hydraulic systems for baling are preferred over screw-type balers. Some shrinkage may occur during shipment, probably mainly due to losses of moisture.
Originally, all produced "Eucheuma" (including cultured Kappaphycus as well) was exported as raw material (dried seaweed) to processors in Europe and the United States. Since 1978, however, carrageenan has been produced in the Philippines as well, with Indonesia following suit in 1988.
Branch, micropropagule and tissue cultures as well as clonal propagation from callus of E. denticulatum have been successful. However, selection for better cultivars in E. denticulatum has not resulted in tangible improvement.
High quality iota carrageenan is much in demand on the world market. Moreover, demand for the Chinese food market is considerable and, for the farmers, often more reliable than the unstable demand from carrageenan producers. Because of the differences in post-harvest treatment (washing in freshwater is conditional for use as food and detrimental to carrageenan quality) farmers determine which part of the crop is available for each commodity. The culture of Echeumoid algae for carrageenan production is only economically viable in areas with low labour costs. In the main production areas, productivity is now generally dropping because of diminishing daily growth rates, susceptibility to stress and "ice-ice" disease. There is therefore a need to select new strains for genetic improvement of the stock. An additional problem is that intensive Eucheuma farming may have a negative ecological impact due to the production of volatile hydrocarbons.
- Azanza-Corrales, R., Mamauag, S.S., Alfiler, E. & Orolfo, M.J., 1992. Reproduction in Eucheuma denticulatum (Burman) Collins & Hervey and Kappaphycus alvarezii (Doty) Doty farmed in Danajon Reef, Philippines. Aquaculture 103: 29-34.
- Dawes, C.J. & Koch, E., 1991. Branch, micropropagule and tissue culture of the red algae Eucheuma denticulatum and Kappaphycus alvarezii farmed in the Philippines. Journal of Applied Phycology 3: 247-257.
- Dawes, C.J., Lluisma, A.O. & Trono Jr, G.C., 1994. Laboratory and field growth studies of commercial strains of Eucheuma denticulatum and Kappaphycus alvarezii in the Philippines. Journal of Applied Phycology 6: 21-24.
- Dawes, C.J., Trono Jr, G.C. & Lluisma, A.O., 1993. Clonal propagation of Eucheuma denticulatum and Kappaphycus alvarezii for Philippine seaweed farms. Hydrobiologia 260/261: 379-383.
- Doty, M.S., 1988. Prodromus ad systematica Eucheumatoideorum: a tribe of commercial seaweeds related to Eucheuma (Solieriaceae, Gigartinales). In: Abbott, I.A. (Editor): Taxonomy of economic seaweeds 2. pp. 172-184.
- Doty, M.S. & Norris, J.N., 1985. Eucheuma species (Solieriaceae, Rhodophyta) that are major sources of carrageenan. In: Abbott, I.A. & Norris, J.N. (Editors): Taxonomy of economic seaweeds 1. pp. 47-65.
- Juanich, G.L., 1988. Manual on seaweed farming. 1. Eucheuma spp. Asean/UNDP/FAO Regional-Scale Coastal Fisheries Development Project, Manila, The Philippines. Asean/SF/88/Manual 2: 1-25.
- Luxton, D.M., 1993. Aspects of the farming and processing of Kappaphycus and Eucheuma in Indonesia. Hydrobiologia 260/261: 365-371.
- Santos, G.A., 1989. Carrageenans of species of Eucheuma J. Agardh and Kappaphycus Doty (Solieriaceae, Rhodophyta). Aquatic Botany 36: 55-67.
- Trono Jr, G.C., 1993. Eucheuma and Kappaphycus: taxonomy and cultivation. In: Ohno, M. & Critchley, A.T. (Editors): Seaweed cultivation and marine ranching. First edition. Japan International Cooperation Agency, Yokosuka, Japan. pp. 75-88.
Sources of illustration
Trono, G.C. & Ganzon-Fortes, E.T., 1988. Philippine seaweeds. National Bookstore, Manila, The Philippines. Fig. 112B, p. 159 (habit); Xia, B. & Zhang, J., 1999. Flora algarum marinarum sinicarum, vol. 2, Rhodophyta, 5. Academiae Sinicae Edita, Beijing, China. Fig. 70, p. 121 (sections of thalli); Weber-van Bosse, A., 1928. Liste des algues du Siboga [List of the algae of Siboga]. Siboga-Expeditie, Monografie 59d. Brill, Leiden, The Netherlands. Fig. 164, p. 414 (section of cystocarp). Redrawn and adapted by P. Verheij-Hayes.
- G.C. Trono Jr