Caulerpa (PROSEA)

Plant Resources of South-East Asia Introduction

List of species

Caulerpa fergusonii - 1, habit. C. serrulata (Forssk.) J. Agardh - 2, habit. C. sertularioides - 3, habit. C. okamurae - 4, fertile ramuli with liberation tube (arrow), female gametangial network (light grey in this figure, orange in vivo) and male gametangial network (darker in the figure, light green in vivo); 5, macrogamete, with reddish eye-spot; 6, microgamete.

Caulerpa J.V. Lamour.

Protologue: Nouv. Bull. Sci. Soc. Philom. Paris, sér. 2, 1: 332 (1809); J. Bot. (Desvaux) 2: 141-142 (1809).

Family: Caulerpaceae

Chromosome number: 2n= unknown

Major species and synonyms

• Caulerpa brachypus Harv., Proc. Amer. Acad. Arts Sci. 4: 333 (1859), synonym: C. stahlii Weber Bosse (1898).

• Caulerpa cupressoides (Vahl) C. Agardh, Syn. Alg. Scand. XXIII (1817), synonym: Fucus cupressoides Vahl (1802).

• Caulerpa fergusonii G. Murray, Trans. Linn. Soc. London, ser. 2. Bot. 3: 212 (1891).

• Caulerpa lentillifera J. Agardh - see separate article.

• Caulerpa okamurae Weber Bosse, (as C. okamurai) in Okamura, Bot. Mag., Tokyo 11: 5-7 (1898).

• Caulerpa peltata J.V. Lamour., see C. racemosa.

• Caulerpa racemosa (Forssk.) J. Agardh - see separate article.

• Caulerpa serrulata (Forssk.) J. Agardh, Mus. Senckenb. 2: 174 (1837), syonyms: Fucus serrulatus Forssk. (1775), Caulerpa freycinetii C. Agardh (1822).

• Caulerpa sertularioides (S.G. Gmelin) M. Howe, Bull. Torrey Bot. Cl. 32: 576 (1905), synonyms: Fucus sertularioides S.G. Gmel. (1768), Caulerpa plumaris Forssk. (1775).

• Caulerpa taxifolia (Vahl) C. Agardh - see separate article.

• Caulerpa urvilleana Mont., in Hombr. & Jacquinot, Voy. Pôle Sud Bot. 1: 21 (1843) (as C. urvilliana ), synonyms: C. serrata Sond. (non Kütz.) (1817), C. microdonta J. Agardh (1872), C. tristicha J. Agardh (1872).

Vernacular names

General:

• caulerpa
• Indonesia: sayur laut (used for many edible algae).

C. serrulata :

• Philippines: galgalacgac (Luzon, Ilocos).

C. sertularioides :

• Philippines: lukay-lukay (also for C. taxifolia), lato (also for C. lentillifera and C. racemosa) (Visayan), salsalamagi.

Origin and geographic distribution

Caulerpa is widely distributed in tropical to subtropical seas, with the greatest diversity in the tropics and on the coasts of Australia. In South-East Asia, all Caulerpa spp. that are listed here, except C. okamurae, are regularly recorded in Indonesia, the Philippines and Papua New Guinea. C. serrulata and C. sertularioides have also been recorded in Burma (Myanmar), Thailand, Vietnam, Malaysia (usually mainly from Peninsular Malaysia) and Singapore, while additional records for C. fergusonii are limited to Burma (Myanmar) and Malaysia only. In Vietnam also C. brachypus has been recorded. For C. cupressoides and C. urvilleana additional records are known from Thailand (C. urvilleana only from the Pacific coast). In Indonesia both species occur mainly in the eastern parts, and in Papua New Guinea at the northern coast. C. okamurae is often considered to be restricted to East Asia (Japan, Korea), but recently it has been recorded on the Indonesian islands of Java, Bali, Sulawesi and Halmahera.

Uses

Most Caulerpa are eaten raw or blanched as fresh salad in coastal areas of most countries in South-East Asia. Usually, after cleaning the algae, the frond parts are separated from the stolon and used for salad. For preservation, salt can be added. The frond parts can be dipped in vinegar (the Philippines: Ilocos Norte) or dressed with an all-spice sauce. In Indonesia some Caulerpa spp. are eaten sugar-coated, prepared as a relish, or cooked in palm sugar and soya sugar. In the Philippines C. serrulata and C. sertularioides are also stored and sold in dried form. Before being prepared as a salad the dried seaweeds are first soaked in water for a few minutes to regain succulence, then prepared in the same way as fresh fronds. Most Caulerpa spp. are also used as medicine to lower blood pressure or (in C. lentillifera and C. racemosa) to treat rheumatism, while C. sertularioides is applied to treat and prevent goitre and is listed for anti-tumour activity. Several Caulerpa spp. are used as ornamental in tropical marine aquaria. Some are also sold in pressed form as souvenirs.

Production and international trade

Most Caulerpa are only used locally and are collected by hand from natural populations. For exceptions see C. lentillifera.

Properties

Caulerpa may produce secondary compounds, such as caulerpin, caulerpicin, caulerpenyne and other terpenoids. Caulerpin, a dimer derivate of indole-3-acrylic acid, might serve as a growth regulator in these species. It has not been recorded from any source other than the Caulerpales, although it was not found in each Caulerpa specimen tested. Caulerpin is responsible for the peppery taste and is considered toxic for microorganisms, fish and humans. In some individuals, especially the compounds caulerpin and caulerpicin can function as mild anaesthetics and may cause dizziness, numbness of the tip of the tongue, weakening of the extremities and difficulty in breathing. These compounds can be concentrated in the bodies of specialized herbivores that feed on Caulerpa spp. and can thus accumulate in the food web. In Caulerpa these compounds are only present in fresh material, but not in air-dried specimens, although some diterpenes still can be isolated from this dried material. Haemagglutinic activity as well as antibacterial activities of extracts of fresh and dried Caulerpa thalli have been demonstrated. Many saturated (especially palmitic acid and stearic acid) and unsaturated fatty acids (especially myristoleic acid) are known to occur in several Caulerpa spp. Of the sterols, especially cholesterol is present in appreciable amounts. The presence of cytotoxic and antimitotic activity in methanol/toluene extracts of living specimens is documented for C. prolifera (Forssk.) J.V. Lamour., while mosquito larvicidal activity is recorded for C. scalpelliformis (R.Br. ex Turner) C. Agardh.

Long lists of identified minerals and other compounds are available for Philippine Caulerpa spp. Most of them have antibacterial and antifungal properties and several show peroxidase activity.

Description

• Thalli coenocytic, giant single multinucleate cells, with high degree of differentiation, generally characterized by a creeping stolon and erect fronds.
• Stolons rarely absent and usually bearing rhizoids, solitary, arranged in tufts or concentrated on special downwards-growing rhizophores (pillars).
• Fronds variable in form, simple or branched; internal septation completely absent; form of giant cell supported by numerous bars of cell wall material (trabeculae) transversing the cell lumen from wall to wall; central vacuole with lining cytoplasm full of green photosynthetic chloroplasts, colourless amyloplasts specialized for starch storage and many nuclei continuous throughout the alga; cell wall non-cellulosic, the structural component being xylan, embedded in a glucan matrix.
• Thalli holocarpic when fertile.

C. brachypus.

• Plant stoloniferous; stolons ovate or terete in cross-section, 0.8-2.5 mm in diameter.
• Rhizoid bearing descending branches (pillars) arising from the ventral side at irregular intervals.
• Fronds on short and cylindrical stalks, ligulate in form, 40-60 mm × 3-9 mm, margins with irregular teeth, 220-310 μm long and 500-800 μm wide at the base; branching of fronds irregular, branches arising from the margins or the surface of the fronds.

C. cupressoides.

• Plant robust; stolons ovate or terete in cross-section, 1.5-3.0 mm in diameter.
• Descending branches (pillars) emerging from the ventral surface, ending in filiform rhizoids.
• Fronds on cylindrical and rather long stalks, 6-8 cm tall, axis terete or slightly compressed, 1.0-3.0 mm wide with irregular or irregular-distichous branching, bearing multiseriate or occasionally pinnate, upward curved, compressed, conical branchlets, 0.3-2.0 mm long and 0.3-0.6 mm wide at the base, with cuspidate or mucronate tips.

C. fergusonii.

• Plant medium tall; stolons ovate in cross-section, up to 2 mm in diameter.
• Rhizoid bearing descending branches (pillars) 1-3 cm long, arising from ventral part at irregular distances.
• Fronds upright, 5-8 cm tall, with pyriform or obpyriform segments, 4-7 cm long and 3-5 mm wide, usually unbranched; segments with single or pinnate branchlets constricted at their base, rounded to clavate in form, the widest 3-6 mm in diameter.

C. okamurae.

• Plant medium tall; stolons cylindrical, glabrous, glossy, several cm long, 1-1.5 mm in diameter.
• Rhizoids emitting from ventral surface at irregular distances.
• Fronds with cylindrical axis, as thick as the stolon, 4-12 cm tall, on cylindrical, medium to long, irregularly branched stalks and clothed more or less densely with branchlets over their whole length; branchlets mostly imbricate, sometimes distichous or opposite, and obovate, oblong, or subclavate-cylindrical in form, 2-5 mm × 1.5 mm, on short stalks, and slightly constricted at the junction.

C. serrulata.

• Plant medium tall and robust; stolons stiff, ovate or terete in cross-section, 1.5-2.5 mm in diameter.
• Descending branches (pillars) terete, at irregular intervals, ending in filamentous rhizoids.
• Fronds flat or compressed, 4-9 cm tall, mostly twisted or curved upwards, 1.5-4.0 mm wide, irregularly or semi-dichotomously branched on short cylindrical stalks; branchlets on both margins arranged regularly, triangular, 1.5-2.5 mm × 1-1.5 mm, apex mucronate.

C. sertularioides.

• Plant stoloniferous; stolons tubular, naked, cylindrical, 0.25-1.5 mm in diameter.
• Rhizoid-bearing branches (pillars) emerging from the ventral side of stolons at irregular distances.
• Fronds 1-12 cm tall, on cylindrical stalks 2-10 mm long and 0.3-1 mm in diameter; axis terete, 1-2 mm wide, only rarely branched; branchlets pinnately arranged, terete, curved upwardly, with uniform diameter of about 0.5 mm, not constricted at the base, with mucronate tips.

C. urvilleana.

• Plant large and robust; stolons terete or ovoid in cross-section, 1.5-3.5 mm in diameter.
• Descending branches (pillars) few to many, cylindrical, with branched rhizoids at the ends.
• Fronds erect, 8-20 cm tall, on cylindrical stalks 2-7 mm × 1.5-2.5 mm, axis terete to compressed, 2-3.5 mm wide; branching repeatedly dichotomous or alternate; branchlets mamillate, arranged on both margins or multiseriately, 1.5-3 mm × 1 mm, apex pointed or mucronate.

Growth and development

Most Caulerpa can be found all year round, although several are most luxuriant in shallow tide pools and lagoons during the warmest and quietest months of the year.

The life cycle is not yet completely understood. Most species are considered to be monoecious and all are holocarpic, releasing their total content in the form of microscopic, mobile, biflagellated presumed anisogametes. There are indications that all Caulerpa spp. have a haplontic life cycle, in which a multinucleate, coenocytic and presumably haploid gametophyte alternates with a microscopic zygote stage, but evidence concerning the ploidy of the various stages in the life cycle is incomplete. The supposed anisogametes develop inside the coenocytic thalli. Gametogenesis is a relatively inconspicuous process involving the migration of the cytoplasm into a net-like lattice of unspecialized gametangia concentrated at the terminal ends of the fronds. Migration of the cytoplasm occurs overnight, about 2 days before gamete release, resulting in transparency of the stolons. Within 12 hours before gamete release many species typically acquire a yellowish-green appearance. Light green sections of gametangia release the small microgametes, whereas brownish-orange-coloured gametangia release slightly larger macrogametes. Siphonous shedding tubes, 5-15 mm long, develop 12-36 hours prior to gamete release. Recent studies in the Caribbean Sea show that most Caulerpa species there release all gametes within a short period of 5-15 minutes, mainly during the annual shift from dry season to wet season. Each species seems to use a fixed and characteristic time relative to sunrise, resulting in release periods that differ for related species. In the resultant gamete clouds these gametes fuse usually rapidly, but embryogenesis of zygotes has only very occasionally been observed and is remarkably slow.

Several Caulerpa spp. are stenohaline and cannot grow in areas which become brackish. The long, creeping stolons produce dense upright fronds in favourable circumstances and less dense fronds in less favourable environments. In culture, near the growing tip of the stolons, tufts of downward-growing rhizoids (often on rhizophorous pillars) are formed at regular distances and, when circumstances do not change, in each individual at a constant speed. In nature, however, changing environmental conditions usually result in irregular distances between the rhizoids. Upright fronds are formed at more irregular distances and further back from the growing tip of a stolon. The growth of stolons, rhizoids and upright fronds does not differ significantly in the various Caulerpa spp. that have been studied in detail. The direction is controlled by gravity. In all cases the different parts of the thalli extend only at their tips or from newly formed growing points, but never intercalary. The growth rate for stolons is 2-9 mm/day in C. prolifera from Italy and from the Caribbean.

A specific wound response in Caulerpa enables the giant multinucleate thalli to cope with the cell integrity when the outer wall is damaged. As soon as damage occurs, wound plug formation is initiated, thus preventing the giant cell from losing its entire content, although in general some cytoplasm will stream out into the sea water. A new wall will be laid down behind the wound plug, sealing off the remainder of the coenocytic thallus. Wound plug formation can be induced by pressing together opposite walls of the cell, resulting in the formation of a special wall. This protective response happens often within minutes and can be used to prepare fragments for propagation. The pressure technique is commonly used in the cultivation of Caulerpa as ornamental plants for aquaria. After formation of these special walls, called pression walls, regeneration of the alga begins. In nature regeneration of whole plants from even small pieces often occurs and can be considered an important means of vegetative propagation. When these algae become fertile, however, normally all contents of these holocarpic coenocytes are used to produce the gametes. The empty outer walls usually degrade quickly. Depending on wave action and currents, all remnants may disappear within two hours, or shreds of the yellowish-whitish husks of emptied thalli persist for one or two more days. In aquarium practice this phenomenon is known as "fatal bleeding" of Caulerpa.

Other botanical information

There are more than 180 taxa (i.e. species, varieties and formae) recognizable in Caulerpa , of which at least 100 occur in South-East Asia. Most of these entities show high adaptability to changing environmental conditions. As a result, these entities may persist under unfavourable conditions but exhibit different morphological characters. This phenomenon is called morphological plasticity and the entities are known as ecophenes or ecads.

Ecology

Sheltered and semi-protected coastal areas are the best habitats for the settlement of Caulerpa. The water in such areas is relatively clear, the current is not too strong and the bottom is largely soft due to sedimentation. In the tropical areas, the wide eulittoral zone has the highest species diversity of Caulerpa, while in the deeper zone the diversity becomes much less. In the sublittoral zone to a few metres deep, Caulerpa lives amongst living corals or creeping under the acropora coral canopy. C. brachypus lives in large colonies mixed with C. racemosa in the mid to lower eulittoral zone where the bottom consists of mud and sand. It occurs also in deeper water, growing solitarily on dead corals. C. serrulata grows on sandy bottoms and may reach 1 m in length, a greater length than it reaches on hard substrates. C. cupressoides and C. urvilleana commonly grow on loamy bottom and coexist in the seagrass meadow. A large C. urvilleana colony in a seagrass meadow may become 30 cm tall. The vertical distribution of Caulerpa is very wide. Reports indicate that C. cupressoides, C. fergusonii and C. racemosa are found at 20-30 m depth, C. webbiana Mont. even at 50 m depth, and C. taxifolia up to 90 m depth in the Mediterranean Sea.

The occurrence of heterotrophic assimilation by rhizoids has been suggested for several Caulerpa spp. For C. taxifolia it has been shown that endocellular bacteria in the cell lumen of rhizoids can take up inorganic phosphorous and organic carbon and nitrogen from substrata and can translocate nutrient products to the photoassimilatory organs. This rhizoid uptake of nutrients provides an explanation for the successful growth of these large coenocytic organisms in oligotrophic tropical waters.

Propagation and planting

In nature Caulerpa may propagate in two ways: sexually and vegetatively. In culture, however, vegetative propagation is more important than sexual propagation. A small detached piece of a plant will quickly recover in a few days and grow into a small complete plant. The initiation of the sexual reproductive phase of Caulerpa is strongly influenced by environmental conditions and physiological stress.

Phycoculture

There are no reports of any of the above mentioned Caulerpa spp. being commercially cultivated. Information on Caulerpa culture refers to C. racemosa and C. lentillifera , which have recently been successfully exploited and cultured on a large scale in the Philippines and Japan.

Diseases and pests

Caulerpa spp. are generally not favoured for feed by grazers, although some sacoglossan opisthobranch snails are specialized feeders on these algae.

Harvesting

Caulerpa spp. are collected by hand from wild populations and for local use only.

Handling after harvest

Caulerpa spp. are sold and used fresh and/or sun-dried; occasionally they are preserved in salt.

Prospects

The trend of increasing seaweed consumption in archipelagic countries (e.g. Indonesia and the Philippines) will provide opportunities for the development of Caulerpa culture to supply a fresh sea vegetable. There is also potential use for fine chemicals and medical products.

Literature

• Aliya, R. & Shameel, M., 1998. Phycochemical investigations on air-dried material of five species of Caulerpa. (Bryopsidaceae). Botanica Marina 41: 124-132.
• Ballesteros, E., Martín, D. & Uriz, M.J., 1992. Biological activity of extracts from some Mediterranean macrophytes. Botanica Marina 35: 481-485.
• Chisholm, J.R.M., Dauga, C., Ageron, E., Grimont, P.A.D. & Jaubert, J.M., 1996. “Roots” in mixotrophic algae. Nature 381: 382.
• Doty, M.S. & Aguilar-Santos, G., 1970. Transfer of toxic algal substances in marine food chains. Pacific Science 24: 351-355.
• Goldstein, M. & Morrall, S., 1970. Gametogenesis and fertilization in Caulerpa. Annals of the New York Academy of Science 175: 661-672.
• Jacobs, W.P., 1994. Caulerpa. This tropical alga is the world's largest single-celled organism. Scientific American, December 1994: 66-71.
• Menzel, D., 1988. How do giant plant cells cope with injury? The wound response in siphonous green algae. Protoplasma 144: 73-91.
• Prud'homme van Reine, W.F., Verheij, E. & Coppejans, E., 1996. Species and ecads of Caulerpa (Ulvophyceae, Chlorophyta) in Malaysia (South-East Asia): taxonomy, biogeography and biodiversity. Netherlands Journal of Aquatic Ecology 30: 83-98.
• Schwede, J.G., Cardellina, H., Grode, S.H., James, T.R. & Blackman, A.J., 1987. Distribution of the pigment caulerpin in species of the green alga Caulerpa. Phytochemistry 26: 155-158.
• Subramonia Thangam, T. & Kathiresan, K., 1991. Mosquito larvicidal effect of seaweed extracts. Botanica Marina 34: 433-435.
• Svedelius, N., 1906. Ecological and systematic studies of the Ceylon species of Caulerpa. Reports of the Ceylon Marine Biological Laboratory 2: 81-144.

Sources of illustration

Hatta, A.M. Original drawings of the habits of C. fergusonii and C. serrulata; Hori, T. (Editor), 1994. An illustrated atlas of the life history of algae. Vol. 1. Green algae. Uchida Rokakuho Publishing Company, Tokyo, Japan. Plate 133, p. 270 (fertile stages of C. okamurae); Trono, G.C. & Ganzon-Fortes, E.T., 1980. An illustrated seaweed flora of Calatagan, Batangas, Philippines. University of the Philippines Marine Science Center & Filipinas Foundation, Manila, The Philippines. Fig. on p. 23 (habit C. sertularioides). Redrawn and adapted by P. Verheij-Hayes.

Authors

• A.M. Hatta