Enteromorpha (PROSEA)
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Introduction |
Enteromorpha Link
- Protologue: in Nees, Horae phys. berol.: 5 (1820).
- Family: Ulvaceae
- Chromosome number: x= 10
Major species and synonyms
- Enteromorpha clathrata (Roth) Grev., Alg. brit. 66: 181 (1830), synonym: Conferva clathrata Roth (1806). Accepted name is now: Ulva clathrata (Roth) C.Agardh (1811).
- Enteromorpha compressa (L.) Nees, Horae phys. berol., index 2 (1820), synonyms: Ulva compressa L. (1753), Enteromorpha complanata Kütz. (1845). Accepted name is now: Ulva compressa L. (1753).
- Enteromorpha flexuosa (Wulfen) J. Agardh, Acta Univ. Lund. 19(2): 126-128 (1883), synonyms: Ulva flexuosa Wulfen (1803), Enteromorpha tubulosa (Kütz.) Kütz. (1856). Accepted name is now: Ulva flexuosa Wulfen (1803).
- Enteromorpha intestinalis (L.) Nees, Horae phys. berol., index 2 (1820), synonym: Ulva intestinalis L. (1775). Accepted name is now: Ulva intestinalis L. (1753).
- Enteromorpha lingulata J. Agardh, Acta Univ. Lund. 19(2): 143 (1883), synonym: E. compressa (L.) Nees var. lingulata (J. Agardh) Hauck (1884). Accepted name is now: Ulva flexuosa Wulfen (1803).
- Enteromorpha linza (L.) J. Agardh, Acta Univ. Lund. 19(2): 134 (1883), synonym: Ulva linza L. (1753). Accepted name is now: Ulva linza L. (1753).
- Enteromorpha prolifera (O.F. Müll.) J. Agardh, Acta Univ. Lund. 19(2): 129 (1883), synonym: Ulva prolifera O.F. Müll. (1778). Accepted name is now: Ulva prolifera O.F.Müller (1778).
Vernacular names
General:
- green laver (En)
- Indonesia: lumut benang
- Philippines: lagot, lumot bitukang-manok (Tagalog), ruprupu.
E. clathrata :
- light green aonori (En)
- Philippines: habol-habol.
E. compressa :
- yellow-green aonori (En).
E. intestinalis :
- green aonori (En).
E. prolifera :
- dark green aonori (En).
Origin and geographic distribution
Enteromorpha is a common genus of green algae distributed widely in South-East Asian waters.
Uses
Enteromorpha is widely used throughout the world, including Asia, for food, feed (especially for fish (milkfish) and pigs), as a fertilizer and medicine. It is also applied as fish bait. The dried and crushed fronds can be used as topping for many foods, in soups and as a coating. It is available in Japan in powdered form for similar uses or as a green colourant.
In Chinese herbal medicine Enteromorpha is used against goitre and scrofula, as an antipyretic, to prepare a refreshing liquid and to treat sunstroke, bronchitis, cough and asthma.
Collections from wild populations are not appreciated because these consist of thalli of different ages. The young fronds are tender and tasty, while the mature ones are cartilaginous, fibrous and somewhat bitter. When cultured, the algae can be collected in the desirable stage, based on consistency, form and colour.
Production and international trade
Information on the production and international trade of Enteromorpha is scanty. It is collected from the wild and cultivated in small quantities for local consumption in Indonesia, Malaysia, and the Philippines. Several Enteromorpha spp. are recorded from 1953 on as being cultured for milkfish food in brackish water ponds in the Philippines. Here, E. clathrata, E. compressa and E. intestinalis are cultured for animal feed (especially milkfish) and as a source of tocopherols (vitamin E). In Tagalog the word "lumot" is used for a large assemblage of filamentous algae found in shallow ponds, and used as natural food in milkfish cultivation together with "lab-lab" (a mixture of mainly filamentous microalgae). Enteromorpha can usually be found in this assemblage, although green filamentous algae such as Chaetomorpha and Cladophora spp. are present as well.
Properties
Information on the properties of Enteromorpha varies considerably, probably because it is not always indicated which species has been analyzed. Enteromorpha spp. contain (per 100 g dry weight): protein 12-15(-20) g, fat 0.3-1.5 g, carbohydrates 46-53 g, and ash 21-22.6 g. The most common lipid found is the unsaturated fatty acid sitosterol, which can help to reduce the plasma cholesterol level in cells. The carbohydrates are mostly glucides and starch. It is stated that all essential amino acids are present, together with chondrine, cysteine, D-cysteinolic acid, glutamic acid and proline. Especially data on vitamin contents are variable, indicating for 100 g Enteromorpha (dry weight): vit. A 500-1300 IU, vit. B1 0.04-0.6 mg, vit. B2 0.52-2.05 mg, niacine 1-6 mg, vit. C 10-43.2 mg, vit. B12 1.3 μm and folic acid 42.9 μm. Data on tocopherols (vitamin E) are not available. Minerals (mg/g dry weight) include: Ca 840-910, P 740-800, Fe 10-35, Na 530-570, and K 3200-3500.
Description
- Thalli inflated or tubular, crisped, contorted, or bandshaped, branched or unbranched, consisting of a single layer of cells around an open central lumen filled with water or air.
- Cells usually fairly uniform, except rhizoidal cells in the lower parts, irregularly arranged or more regularly in longitudinal or transverse rows.
- Life cycle diplo-haplontic and isomorphic.
- Gametophytes probably dioecious, forming two kinds of isogametes.
E. clathrata.
- Thalli 1-10(-45) cm long and 3-10 mm wide, forming light to grass-green dense mats of soft, delicate, flattened, hollow tubes, branched or unbranched, unattached or when attached with fragile stipe and small disciform holdfast.
- Determinate branchlets uniseriate at or near their tips, hair-like.
- Cells rather large, subquadrangular in surface view, 15-36 μm in diameter, fairly regularly arranged in longitudinal rows.
- Chloroplasts very thin or contracted, usually not obscured by starch grains.
- Pyrenoids 2-6 per cell.
E. compressa.
- Thalli 1-35 cm long and 2-20 mm wide, attached by fragile stipe and small disciform holdfast, with bright to dark green bushes of tubular, strap-shaped, more or less compressed branches, not differing from the principal ones, expanded above, as well as many short, more or less filiform branchlets, intercalated between the larger ones.
- Branching concentrated at basal region of thalli.
- Cells small, rounded to irregularly polygonal in surface view, 10-15 μm in diameter, irregularly arranged or arranged in longitudinal rows.
- Chloroplasts parietal, with numerous large starch grains, often having a cap-like appearance.
- Pyrenoids 1(-2) per cell.
E. flexuosa.
- Thalli 2-3(-60) cm long and up to 1 cm wide, usually smaller, with small disciform holdfast, forming light to yellowish-green thick tufts; individual thalli densely to sparsely branched.
- Branches tubular, strap-shaped to filiform, narrow in basal portions but enlarged to inflated towards their distal portions.
- Cells square to rectangular in surface view, 9-12 μm in diameter, regularly arranged in basal regions in longitudinal and short transversal rows, becoming irregularly arranged towards the distal regions.
- Chloroplast forming central transverse band, usually not obscured by starch grains.
- Pyrenoids 2-5 per cell.
E. intestinalis.
- Thalli 6-20(-50) cm long, with short stipe attached by discoid holdfast, forming bright to yellowish bushes of usually unbranched, constricted and/or contorted, erect, tubular fronds, tapering below and inflated above.
- Cells small, polyhedral or rounded in surface view, 8-18 μm in diameter, irregularly arranged, filled with spherical to oval parietal chloroplast, often having a cap-like appearance, with numerous large starch grains.
- Pyrenoids 1 per cell.
E. lingulata.
- Thalli up to 7(-15) cm long and usually not over 1-2 mm wide, attached by conspicuous basal disc, forming medium green tufts or turfs of fronds sparingly to abundantly branched in basal regions, above tubular, very slender and gradually dilated, below subsolid.
- Cells sharply rectangular, 9-28 μm in diameter, arranged in clear longitudinal rows.
- No published data available on chloroplasts, starch grains and/or pyrenoids.
E. linza.
- Thalli up to 37 cm long and to 30 cm wide, attached by short stalk and stout disciform holdfast, with erect, strap-shaped, flat, linear to lanceolate, simple, unbranched, often gregarious, yellowish-green to medium green blades with tapering base.
- Blades hollow at base, in flat portions the two layers united to a membrane of a combined thickness of 35-50 μm, with a hollow margin.
- Cells irregular polygonal in surface view, in middle and upper regions characteristically quadrangular to rectangular or irregularly polygonal, arranged in short to long longitudinal and transverse cell rows, 10-22 μm in diameter.
- Chloroplast completely covering outer cell wall, usually obscured by numerous large starch grains.
- Pyrenoids 1(-2) per cell.
E. prolifera.
- Thalli up to 60 cm long and 5-10 mm wide, attached by long, slender stipe with small disciform holdfast, with solitary or tufted, light yellowish-green or medium green, strap-shaped, undulating, wrinkled and lubricous fronds with a gradually narrowing base, with membrane 15-18 μm thick.
- Branches along the whole axis small; uniseriate branchlets mostly concentrated on the base.
- Cells irregularly polygonal to subangular in surface view; 8-19 μm in diameter, arranged in long to short longitudinal rows and short transverse rows.
- Chloroplast centrally situated, obscured by numerous starch grains.
- Pyrenoids 1(-2) per cell.
Growth and development
Most Enteromorpha grow fast in natural habitats as well as in cultures. They attach to stones (epilithic), ropes or nets and also to other marine organisms. They are present throughout the year in the form of successive, short-living generations.
In fertile thalli parts degrade when their contents transform into gametes or zoospores. When these zoids are released, only the walls of the original cells remain. This release usually occurs around spring tide (lunar cycle). Biflagellate isogametes of opposite mating types fuse and the quadriflagellate zygotes stay motile during a short period only. They anchor themselves at their anterior end to solid substrates and to other algae, withdraw their flagella and secrete a cell wall. They then each divide into two cells, the basal one forming the holdfast, and the apical cell divides and re-divides to produce vegetative cells of the thallus. Quadriflagellate zoospores are produced by diploid sporophytic thalli. They behave like zygotes and develop to form haploid gametophytic thalli.
When cultures of Enteromorpha are enriched by adding ammonium or nitrate, tissue growth is accelerated and the algae can stock nitrate in the form of dipeptides which form 3-7% of total dry weight. They can use this nitrogen source later to grow faster than the normally available nutrients should allow. The algae absorb the extra nitrogen mainly during the day, while rhodophytes usually mainly absorb nutrients during the night. Enteromorpha can still fix bicarbonates at pH values above 9, while many red algae cannot. Enteromorpha can also accumulate polyphosphates and these deposits can be easily used under conditions of phosphorus depletion.
Other botanical information
Seventeen Enteromorpha species have been listed for the Indian Ocean, while a total of 21 species have been listed for the Pacific coast of North America and 16 species have been described from the eastern tropical and subtropical coasts of the Americas. The individual species are very difficult to distinguish. E. compressa and E. intestinalis are considered to be synonyms by several authors, although others prefer to keep them as separate species.
Ecology
Several Enteromorpha spp. tolerate a wide range of salinity and some can even survive in almost pure fresh water. They occur often in brackish estuaries, in sandy areas with freshwater seepage and in rock pools. They are also common inhabitants of upper intertidal areas, where they attach to rocks and coral pieces exposed to air during low tide. They can also be found lying loose, especially in sheltered habitats. The cell walls of estuarine E. intestinalis are thinner and hence stretchier than those of marine rockpool plants of the same species, allowing the cells to swell with the influx of water in low-salinity conditions and to decrease again in the presence of waters of higher salinity.
Enteromorpha thalli can survive water temperatures of about 28°C and even higher air temperatures. They can also grow in water with high turbidity, although growth is much better under full sunlight.
Occasionally, large masses of green algae, consisting mainly of Enteromorpha and Ulva spp., wash up on the coast forming a "green tide". In many stressful situations (e.g. freshwater seepage, oil spills) Enteromorpha spp. quickly colonize the empty surfaces. Because spores and zygotes of these algae can quickly attach, germinate and grow on almost any substrate, Enteromorpha spp. are notorious biofouling organisms. They are difficult to control because of their tolerance to copper, a mineral often used in antifouling coatings. Their growth can, however, be prevented by using organotins as an antifouling compound. These compounds are now included into self-polishing copolymers (SPC) used extensively as paint on seagoing vessels and pleasure crafts.
Propagation and planting
Mature fronds of Enteromorpha can be collected from natural populations and placed in small water tanks with filtered sea water. After keeping them for some time in the dark, dense spore solutions are obtained after about 30 minutes exposure to daylight. These spore solutions can be transferred to large tanks containing nets or other substrates in filtered sea water. During further dark treatment, the spores will settle on the substrates and on the following day these can be transferred to the growing areas. This method is known as "artificial seed collection". Another method, known as "natural seed collection", is practised by placing suitable substrates near natural Enteromorpha populations during spring tides in September-October, when the sporophytes form their quadriflagellate zoospores. These substrates (usually the same nets as used for Porphyra cultivation in Japan and Korea) are secured in such a way that they are not exposed at low tide. The nets can be transferred to the culture grounds when juveniles are observed, usually after a few weeks. When cultivated for food production, Enteromorpha can best be grown on nets, either fixed by poles at shallow depths (not exposed) or in floating systems. The mixture of green algae grown as "lumot" in milkfish ponds in the Philippines can be propagated in separate ponds as algal nurseries and later planted in fish ponds. The algae for transplant have to be transported in a moist or semi-dried state and the ponds to be planted should preferably be cleaned and drained thoroughly beforehand. Planting can be done by staking (transplanting of patches of algae by hand), sowing (broadcasting of fragments) or spreading (producing fragments by shaking bunches of algae in the fish pond water). The latter method is considered to be unsuitable for transplanting Enteromorpha. The ponds with algal cultures must not dry out and the water has to be changed regularly.
Protoplasts have been used successfully for propagation in laboratory culture experiments.
Phycoculture
In Japan, E. prolifera is cultured for commercial purposes. Elsewhere, cultivation is mostly in the experimental phase, and trials are also being carried out on other Enteromorpha species.
Diseases and pests
So far, Enteromorpha in culture is not vulnerable to diseases.
Harvesting
When Enteromorpha is grown on nets, both hand-picking and machine collecting are possible. Hand-picking normally produces the highest quality product, but machine collecting is faster.
Handling after harvest
The collected fronds of Enteromorpha are washed in freshwater and dried in the sun or in a drier. For food use the dried thalli are often lightly toasted and crushed. Fronds of the best quality are dark green and are produced under stable environmental conditions. Changes in environmental factors, especially lowering of salinity and enhanced turbidity, due to rain or human activities, result in a decrease of biomass production and quality.
Genetic resources
Sterile strains of Enteromorpha are preferable for obtaining good quality biomass because of loss of living cells with the release of spores and gametes.
Prospects
Enteromorpha is considered suitable for human food as well as animal feed (especially for fish). The demand for human food is expected to rise, especially in Japan.
Literature
- FAO, 1974. A catalogue of cultivated aquatic organisms. FAO Fisheries Technical Paper No 130, FIRI/T130. Food and Agriculture Organization of the United Nations, Rome. 83 pp.
- Ohno, M., 1993. Cultivation of the green algae Monostroma and Enteromorpha. "Aonori". In: Ohno, M. & Critchley, A.T. (Editors): Seaweed cultivation and marine ranching. 1st Edition. Japan International Cooperation Agency, Yokosuka, Japan. pp. 7-15.
- Polne-Fuller, M. & Gibor, A., 1987. Tissue culture of seaweeds. In: Bird, K.T. & Benson, P.H. (Editors): Seaweed cultivation for renewable resources. Elsevier, Amsterdam, The Netherlands. pp. 219-239.
- Rabanal, H.R. & Montalban, H.R., 1953. The growing of algae or "lumot" in Bañgos fishponds. Fisheries Gazette 5: 3-12.
Sources of illustration
Koeman, R.P.T. & van den Hoek, C., 1984. The taxonomy of Enteromorpha Link (Chlorophyceae) in the Netherlands. 2. The sections Flexuosae and Clathratae and an addition to the section Proliferae. Cryptogamie, Algologie 5: figs. 144 & 146, p. 54 (habit and basal portion of E. clathrata); Taylor, W.R., 1960. Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor, Michigan, United States. Plate 1, fig. 3, p. 665 (habit of E. lingulata); Trono, G.C., 1986. Philippine seaweeds. In: Guide to Philippine flora and fauna. Vol. 1. Natural Resources Management Center, Ministry of Natural Resources and University of the Philippines. Goodwill Bookstore, Manila, The Philippines. Fig. 1, p. 209 (details E. clathrata); fig. 2, p. 210 (habit E. intestinalis); van den Hoek, C., Mann, D.G. & Jahns, H.M., 1995. Algae. An introduction to phycology. Cambridge University Press, Cambridge, United Kingdom. Fig. 22, p. 406 (habit and details of E. compressa). Redrawn and adapted by P. Verheij-Hayes.
Authors
- W.S. Atmadja
