Objective: Collate and summarise published and unpublished reports relevant to the taxonomy, ecology, habitat and phycocolloid contents of Fiji Gracilaria, or any other seaweed genera with known commercial potential in Fiji.
Phycological study in Fiji is still in its early stages, and the major research effort has been (and still is) focussed upon taxonomy, nomenclature and biogeography. In recent years this work has been carried out primarily by staff and visiting researchers at the Marine Studies Programme, University of the South Pacific (USP). Such taxonomic work is the necessary prerequisite to any ecological work, population studies, and commercial utilisation of Fiji's seaweeds, and will underpin any work carried out in these other areas in the future. Thorough taxonomic studies are particularly important for commercial utilisation of phycocolloid-bearing seaweeds, since phycocolloid properties vary so much between species.
The work done so far has resulted in publications that provide checklists and descriptions of the marine algae found in Fiji and Rotuma. Landmark studies include Kasahara (1985), South (1991), Garbary et al. (1991), South (1992), South and Kasahara (1992), Raj (1993), N'Yeurt (1993), and South and N'Yeurt (1994). These and many other pertinent references are listed in McLachlan et al. (1993), a most useful bibliography on seaweed utilisation in the Pacific. The handful of studies on Fiji's benthic marine algae carried out prior to those cited above are reviewed in South and Kasahara (1992).
There have been no ecological or population-biological studies of Fiji's seaweeds as yet that might provide information on seasonal trends in recruitment, abundance, productivity or sustainable yields. This type of information will be critical to an understanding of the biological processes involved in any industrial-scale harvesting or aquaculture of seaweeds. It will be possible up to a point to rely on studies of similar species overseas (Gracilaria in particular has been well researched), but local conditions and species will always have their own peculiarities.
The only publicly-available information found for the phycocolloid contents of Fiji's seaweeds is some preliminary work carried out twenty years ago by WA Booth and colleagues at USP's then Institute of Natural Resources (Solly and Booth, 1977; Singh et al., 1975). This investigation included a survey of seaweeds in Suva Harbour and Kubuna Waters, and the determination of polysaccharide content and seasonal variations for Gracilaria (the species was not named but was probably G. maramae), Hypnea and Gelidium. The unpublished reports so far sighted do not, however, include any detailed results from this survey other than to mention the fact that it was carried out.
This preliminary work by Solly and Booth (1977) also included a cultivation trial of “Eucheuma striatum var. tambalang and E. spinosum” (now known as Kappaphycus alvarezii and Eucheuma denticulatum respectively) imported from the Philippines in 1976. This trial was successful, and subsequent work on commercialisation of seaweeds in Fiji by MAFF, Coast Biologicals Ltd and The seaweeds of interest for the current project have a long history of traditional use as food by the indigenous Fijian people, and such use is documented in South (1993a). This paper provides nomenclature (including Fijian names), descriptions and illustrations, plus a discussion of harvesting, marketing and socio-economic roles, for edible seaweeds in Fiji. The most important species are Caulerpa racemosa (nama), Hypnea pannosa (lumicevata), Gracilaria maramae (lumiwawa), Codium bulbopilum (sagati), Acanthophora spicifera (lumikaro or lumikava) and Solieria robusta (lumitamana). As well as providing a checklist of the edible species, the paper provides a published record of traditional use for these species that will assist in obtaining market acceptance (for example, US FDA approvals) for any Fiji seaweed products that get marketed overseas.
Also reported were the prices paid for some of the various species sold in municipal markets in Fiji. Caulerpa prices ranged from F$0.50 – 2.00 per heap depending on quality (a “heap” may be anywhere from 0.25 to 1.0 kg), while Solieria and the other edible seaweeds were F$1.00 per heap. Between 1981 and 1991 the domestic seaweed harvesting industry in Fiji was conservatively estimated to be worth up to FJ$50,000 per year, involving up to 36 T fresh weight of product.
N'Yeurt (1993) documents the use of Meristotheca procumbens as an ingredient in traditional puddings made in Rotuma. Meristotheca is one of the most prized edible seaweeds in Japan, and demand for it is strong. Meristotheca has not yet been positively recorded as occurring in the main Fiji group.
The particular species of Gracilaria (lumiwawa) that is traditionally eaten in Fiji did not fit any of the Gracilaria species previously reported in Fiji, and was found by G. R. South (Marine Studies Programme, USP) to be an undescribed species. This has now been named Gracilaria maramae sp. nov. (South 1995), and it replaces the records of “G. sp. aff. G. parvispora Abbott” and “G. verrucosa (Hudson) Papenfuss” reported in South and Kasahara (1992).
An overview of seaweed resources in the South Pacific island nations generally is provided by South (1993b). This review article covers basic seaweed biology, distribution, traditional uses, and commercial uses (that is, Eucheuma farming). The article concludes by stating surprise that, given the world prices paid for dried Gracilaria (more than US$600 per tonne at the time of writing) there has not yet been any evaluation of Gracilaria cultivation in the South Pacific.
There is extensive literature on the biology, farming and phycocolloid extracts of Gracilaria species, and it is not possible to review it all here. Key review papers on Gracilaria biology, productivity and farming include Chiang (1981), McLachlan and Bird (1986), Hanisak (1987), Santilices and Doty (1989) and Critchley (1993). The genus is found in all tropical and temperate parts of the world, and is a major source of the gelling phycocolloid “agar” which is used as a thickening agent in all manner of industries such as foods, cosmetics, textiles, brewing, paper and biotechnology. Virtually all of the agar used by Japanese industry comes from dried Gracilaria imported from Asia and from Chile (Christeller, 1986). Japan's dependence upon imports is such that there are no import quotas or duties on dried seaweed (the raw material), however duty must be paid on any imports of processed agar products.
The commercial importance of Gracilaria has made it one of the world's most studied seaweeds. However much work remains to clarify the taxonomic relationships within the genus. This work is made difficult by the fact that all lifecycle stages (not always present year-round) need to be examined to identify a species with any certainty, and by the fact that many morphological characters can be altered by environmental conditions.
In tropical oceans, Gracilaria is found in the shallow waters surrounding high islands, and does not usually occur near atolls (Tsuda, 1982). It can be found on reef flats, sand banks, mudflats and near mangrove areas. Gracilaria is quite palatable and lacking in chemical defenses, so is likely to be heavily grazed (particularly by siganid fishes), though fragmentation from wave action is another significant factor in loss of biomass (Nelson and Tsutsui, 1981). Most Gracilaria species are fairly tolerant of brackish water, though they usually grow best in oceanic salinities.
The lifecycle goes through three phases and involves four morphologically-different forms: a diploid tetrasporophyte plant, haploid male (spermatangial) and female (cystocarpic) gametophytes, and a diploid carposporophyte that lives parasitically within the tissue of cytocarpic plants. Under the spore-reproduction cycle (which includes a sexual reproduction stage), tetrasporophytes give rise to gametophytes by releasing spores which are washed away by currents, stick to a surface, and grow into new plants attached by holdfasts. Male gametophytes release spermatia which fertilise oogonia in the female gametophytes and these develop into carposporophytes. The carposporophytes release spores which germinate into tetrasporophytes again. Gracilaria plants can also reproduce asexually through vegetative propagation, where fragments of plants are broken off and washed away to new areas where they continue growing. These fragments are not able to form new holdfasts, and are at the mercy of the currents.
Farming of Gracilaria usually makes use of the capacity for vegetative propagation. Seed plants harvested from the wild are torn up into fragments and cast into ponds to establish a new crop. Descriptions of Gracilaria cultivation and agar extraction, in environments most similar to Fiji's, can be found in work done for the Bay of Bengal Programme, in Malaysia, and in the Philippines (see for example, Anon., 1983; Bay of Bengal Programme, 1987; Trono, 1988). A farming method using lines was worked out in Malaysia supervised by Jack Fisher and Max Doty from Hawaii (Anon., 1983). Raffia and monofilament lines were seeded with Gracilaria spores in tanks, then strung out between posts driven into the mudflat at cultivation sites. However most farming in Taiwan, Hainan Island and China is done in brackish-water ponds using vegetative fragments. This can be done because the enclosed ponds (about 1 ha each) prevent the unattached plants from being washed away. Vegetative fragments in open water must be attached to lines by hand, or enclosed in cages. The use of cages or ponds involves high capital costs, and is usually only possible if subsidised by culture in the same facilities of higher value species such as fish, prawns or crabs. In brackish ponds in the Philippines, plants grew fastest during the dry season (November - April). Problems include other small seaweeds growing on and smothering the Gracilaria plants at certain times of the year.
Gracilaria contains the phycocolloid “agar”, which is the cell wall material that gives structural strength to the plant (it performs a similar function to cellulose in the cells of land plants). Agar can be extracted by boiling the plants in water. The resulting liquid, on cooling, sets into a jelly. This jelly can be dried down to a solid and be finely ground up, to produce a powder that is easily stored and which can be dissolved in water again to make a new jelly. Good quality agar has a high gel strength (resistance to rupture by a probe) and good physical and chemical properties such as elasticity, melting and gelling temperatures, milk and sugar reactivities. The chemical structure can be altered and improved through various treatments, for example with caustic soda. International standards for agar quality are set by the Japanese Specifications for Processed Agar (JSPA), United States Pharmacopoeia (USP) and Food Chemical Codex (FCC). The food industry also has its own detailed specifications and recipes for particular end uses.
Agar is a spectrum of chain-like polymers, being a mix of pre-cursors and “mature” molecules often with various types of chemical groups attached as side-chains. The length of the polymers (that is, their molecular weight) and the types of chemical substitution groups attached to them affect the properties of the agar. These properties differ between species (Hurtado-Ponce and Umezaki, 1988; de Castro, 1994), and differ within a species between seasons (Whyte et al., 1981; Miller and Furneaux, 1987; Pickering, 1990), between lifecycle stages (Whyte et al., 1981), between plants grown in different nutrient conditions (Bird et al., 1981; Craigie et al., 1984; Cote and Hanisak, 1986), and between young and old portions of the same plant (Craigie and Wen, 1984; Christiaen et al., 1987).
Since agar quality can differ between seasons, it is important to know the best time to harvest plants. However there are contradictory reports in the literature. In temperature climates, agar gel strengths have been reported as higher during summer or when plants are growing quickly (Asare, 1980; Whyte et al., 1981; Friedlander and Zelikovich, 1984; Rotem et al., 1986; Friedlander et al., 1987; Bird, 1988), or lower during summer or in high water temperatures (Craigie and Wen, 1984; Cote and Hanisak, 1986; Christiaen et al., 1987). There is obviously a complex interplay of environmental factors that determine agar quality, that include temperature, light, and salinity, and no predictive model has yet been devised. The seasonal variations in agar quality in Fiji will only become known if a study is carried out upon it.
Hurtado-Ponce and Umezaki (1988) tested agar quality from seven Philippine Gracilaria species, four of which (G. coronopifolia, G. verrucosa, G. edulis and G. eucheumoides) have also been recorded in Fiji (South and Kasahara, 1992; but note that the Fiji G. verrucosa record is to be replaced by G. maramae and is not necessarily the same as the Philippine G. verrucosa). G. edulis was found to have the lowest agar yield (24%) of the species tested, while G. coronopifolia and G. eucheumoides had 33% and 35% yields (the highest was G. arcuata at 49%). These three species all had the lowest of the gel strengths measured (126 – 135 g). The data was not expressed as g cm-2 and a comparitively small (8 mm diameter) gel tester probe was used, which makes comparison with other studies difficult. Even so, their figures probably equate to JSPA Grade 2 agar (<350 g cm-2), and the authors considered these species to be potential sources of food-grade agar. The strongest gels were from G. verrucosa and G. sp. (266 g and 464 g), which probably equates to Grade 1 (>350 g cm-2) and Superior Grade (>600 g cm2) respectively. It will be interesting to find out if any Fiji Gracilaria species bear any resemblance to either of these two stronger-gelling Philippine species.
Like Gracilaria, Hypnea seaweeds are pantropical in distribution and have been studied as sources of phycocolloid (Rao, 1977a). They contain the phycocolloid “carrageenan” (usually kappa-carrageenan), however the genus has not been as well studied as Gracilaria nor is it intensively farmed. Its lifecycle is similar to that for Gracilaria. The species Hypnea musciformis is the main source of raw material for kappa-carrageenan production in Brazil. Supplies are harvested from widely dispersed natural beds and are often found growing attached to Sargassum plants (Berchez et al., 1993). Hypnea is also cultured in Senegal (Mollion, 1983). Erratic natural production in Brazil, and interest in phycocolloids generally in places like India, Israel and Florida (USA) has led to several studies on the cultivation and phycocolloid yield of Hypnea species. There have also been reports of various compounds found in Hypnea plants that have medical and pharmaceutical uses such as muscle relaxants and blood agglutinins (reviewed in Schenkman, 1989). The most recent information available from unpublished sources indicates that Hypnea genus is not highly regarded as a source of phycocolloid by companies like FMC, because of technical problems in getting the extract out of the seaweed (Erik Ask, pers.comm.)
Seasonal reproductive cycles have been studied for H. musciformis and H. valentiae by Rao (1977b) in India, who found that H. musciformis tetrasporophytes and sterile plants predominated throughout the year. Plants can also reproduce vegetatively from regrowth of fragments which, in contrast to Gracilaria, are able to re-attach themselves by forming hooked tendrils around other plants or objects. Rao (1977b) implies that only tetrasporophyte plants have this ability. H. valentiae showed seasonal peaks of tetrasporophytes in winter months and cystocarpic plants in summer months, while male plants were always rare.
Durako and Dawes (1980) examined seasonality of growth and chemistry of H. musciformis in Florida, and found plants were larger and more abundant during winter months, similar to patterns observed elsewhere in India and Hawaii. Dry matter content was typical of many algae in that highest values (between 12.3 and 19.7%) were observed in summer when plants did not appear to be growing well, and was least (8.7 – 10.2%) during winter when plants were large and abundant. Carrageenan levels were highest (20 – 30% of dry matter) in late spring and early summer, and lowest in autumn (15%). Humm and Kreuzer (1975) investigated growth of the same species at American Virgin Islands, and found growth was extremely rapid (doubling in weight every 2 days) in short-term experiments during the month of August where plants were attached to lines. Guist et al. (1982) grew H. musciformis in tanks and recorded growth of 20% per day when water temperatures were between 18 and 24°C and nitrogen fertiliser was added. Carrageenan content was inversely proportional to growth rate.
Friedlander and Lipkin (1982) grew H. musciformis and H. cornuta alongside Gracilaria cf. verrucosa and Pterocladia cappillacea in sandy-bottomed ponds. Both Hypnea species grew either the same as or faster than Gracilaria, and did best from May-June to October. The chemical contents of plants harvested in summer were 10.2 and 11.0 % dry weight, and 31.1 and 32.7 % carrageenan for H. musciformis and H. cornuta, respectively. A follow-up study by Friedlander and Zelikovich (1984) confirmed that Hypnea can grow more rapidly than Gracilaria, with fastest growth during summer (growth appeared most related to water temperature). Carrageenan contents for both Hypnea species were highest in late winter and early spring, and was positively correlated with plant growth rate. This result differed from other culture studies for H. musciformis in Florida (for example, Guist et al., 1982).
Thomas and Subbaramaiah (1994) studied Hypnea pannosa seasonality at Mandapam in India, and found growth was best at lower water temperatures and higher salinities. Carrageenan contents were higher when plants were fast-growing, and were higher when there was more wave action. Schenkman (1989) studied ecological influences on H. musciformis in Brazil, and found biomass was most affected by high temperatures (such as during low spring tides on sunny days) followed by rough seas, and grazing by amphipods and sea-hares. Growth was best during the cool season when seawater temperatures were less than 25°C. Other factors that affected abundance were the availability of substrate (surfaces to cling to) and predation by herbivores. Phycocolloid content varied from 48% to 66% of dry weight, with seasonal maxima in spring (September - October) and autumn (March - April) and minima in winter (July, when plants were most fertile) and summer (January, when biomass declines).
Most of the cultivation studies of Hypnea have been experimental, in tanks or ponds, or using plants tied to lines on rafts (for example, Wallner et al., 1992), while commercial utilisation has relied upon wild harvest. The most serious attempt at development of a cost-effective commercial aquaculture system is described in Berchez et al. (1993). Their system takes advantage of the ability for Hypnea fragments to re-attach themselves to objects using hooked tendrils. Rope lines were stretched between cement blocks and arranged perpendicular to the down-shore current. Some ropes had pieces of plastic netting attached. The idea was that naturally occurring Hypnea fragments would snag and attach onto the ropes, thereby eliminating the labour involved in seeding plants onto lines (as must be done for Gracilaria). Seeding by spores would also occur. They found that plants could be harvested within 15 – 30 days of placing the lines in the water.
There are even fewer studies of Acanthophora species than of Hypnea, and most of these studies had other seaweed species as their main focus. Parekh et al. (1989) has isolated carrageenan from Acanthophora spicifera in India, and found its IR spectral features were similar to standard lambda-carrageenan. The species has been experimentally cultivated in the Gulf of Mannar in India (Kallaperumal et al., 1986), by tying vegetative fragments into clusters with raffia and attaching these to monofilament lines. Using this method, plant biomass increased 2.6-fold in 25 days. Kilar and McLachlan (1986) studied natural dispersal mechanisms of Acanthophora on a reef in Panama, and found that fragmentation processes accounted for its standing crop and distribution. Fragments broken off by wave action would snag and become attached or entangled in seagrass meadows or backreefs. Connor (1983) found that plant size and condition of Panamanian Acanthophora decreased (as did several other species) during the hot, windless season (November - January) in combination with extreme low tides.