Cultivation of Gracilaria on the sea-bottom in southern Chile: a review

This review contains information about the cultivation techniques, strategies, problems and new challenges faced as well as an economic analysis of the income-producing capacity of Gracilaria farming, considering the variability of environmental systems where this alga is cultivated in southern Chile. The development of Gracilaria farming in Chile was made possible by an increased market demand, as well as the existence of basic knowledge that permitted the management of wild stocks and the initiation of cultivation practices. Subtidal cultivation systems appear to be more productive than intertidal systems and are less susceptible to wave action than intertidal cultivation areas. In relation to farming practices, this difference implies that planting and harvesting methods and strategies vary between habitats where cultivation is being carried out on a commercial scale. Several problems such as the environmental impact of different cultivation methods adopted by the farmers, the management of contaminating organisms and strain selection appear to be important and new areas for future research. Finally, an analysis of the income-producing capacity indicates that environmental differences also have important consequences for the management strategies of Gracilaria cultivation.     

Environmental variation and large-scale Gracilaria production

Temporal and spatial abiotic variation in seaweed farms should be anticipated to maximize production through alternative exploitation strategies. This study describes the basic assumptions and the most relevant data used to empirically develop a production model aimed at improving prediction and increasing production of Gracilaria farms in northern Chile. Continuous light and temperature recordings since 1986 have allowed us to relate abiotic variations with high production seasons of Gracilaria or with the presence of pests and epiphytes. Much of the interannual variations in light and temperature appear as part of a predictable pattern of change between ENSO (El Niño/Southern Oscillation) and inter-ENSO years. Production has been found to be a function of stock density and harvesting frequency, two parameters that can be effectively manipulated in the field. Thus, the range of climatic change now can be anticipated to some extent which, in turn, suggests the best farming strategy. During seasons or growth periods anticipated to be highly productive, farming activities are oriented to maintain high percentage removal of the stock through frequent harvesting. During seasons anticipated to be low in production, activities are oriented to prevent biomass losses due to the blooms of epiphytes and pests and to secure stocks to renew through planting the damaged parts of the beds after the blooms.     

Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed byUlva cf.lactuca

In a previous study (Svirski et al., 1993), it was found that growth inhibition ofGracilaria spp., when cultured in the presence ofUlva cf.lactuca, was not due to shading or nutrient depletion, but seemed to be caused by competition for inorganic carbon or some type of allelopathy. In the present study, we attempted to differentiate between these two possible influences by (1) growing the two algae in biculture under various conditions, but keeping inorganic carbon levels constant and measuring net photosynthesis, respiration and growth rates, and by (2) measuring growth rates ofGracilaria spp. in the presence of extracts derived from media previously used to growUlva cf.lactuca.Both net photosynthesis and growth rates ofGracilaria spp. in biculture were inhibited, despite CO₂ (and also HCO₃ ^–) levels being kept constantly high in the culture media. It is likely that these responses were due to markedly enhanced rates of dark respiration inGracilaria spp. when grown together withUlva cf.lactuca. Growth ofGracilaria spp. was also inhibited by extracts derived from seawater in whichUlva cf.lactuca had previously been grown. The strong inhibition by ethyl acetate and chloroform extracts indicate an allelopathic effect onGracilaria spp.     

Gracilaria conferta and its epiphytes: (2) Interrelationship between the red seaweed and Ulva cf. lactuca

Ulva cf. lactuca has been a disturbing competitor of experimental Gracilaria conferta outdoor cultures in Israel. The effect of environmental conditions on the competitive ability of Ulva versus Gracilaria, and the main limiting factors for which these seaweeds compete, were studied here. Single and biculture experiments of both seaweeds showed that Ulva outgrew and damaged Gracilaria under all irradiance and temperature combinations. The higher competitive ability of Ulva cf. lactuca in bicultures was not a result of responses to shading or nitrogen shortage, but rather to a shortage of available inorganic carbon, an increase in pH and apparent excretions of Ulva which inhibited the growth of Gracilaria.     

World-wide use and importance of Gracilaria

The world's first source of agar, from the middle of the seventeenth century, was Gelidium from Japan, but by the beginning of the twentieth century demand for the phycocolloid exceeded of the supply of this alga. Since then Gracilaria has played an important role in the production of agar. Currently agars are obtained from five genera in three orders of red algae and marketed as ‘natural agar’ in squares or strips or as ‘industrial agar’ in powder form. The development of production processes through alkaline hydrolysis of sulphates has allowed a good quality food agar to be obtained from Gracilaria. This does not show the synergistic reaction with locust bean gum apparent with Gelidium agar. The term ‘agaroids’ is applied to Gracilaria agars produced without alkaline hydrolysis of sulphates, with greater sulphate content and much less gel strength. Unlike Gelidium, Gracilaria has to be processed in a short period of time and cannot be allowed to remain in storage for use during years of lower availability. Statistics of imports of agarophytes to Japan during the last 10 years give an indication of the state of the market. During this period there was a marked reduction in Gracilaria imports, mainly from Chile, but also the Philippines, Indonesia and South Africa, mainly due to the overall increase in the capacity of agar production in Gracilaria-producing countries.     

The effect of localised eutrophication on competition between Ulva lactuca (Ulvaceae,Chlorophyta) and a commercial resource of Gracilaria verrucosa (Gracilariaceae,Rhodophyta)

In spring (August) 1993 a bloom of Ulva lactuca appeared for the first time in Saldanha Bay, South Africa, and persisted through summer. Ulva wash-ups contaminated the beach and part of the commercial Gracilaria beach-cast had to be discarded. The biomass and distribution of Gracilaria and Ulva are described in relation to the seasonal water chemistry of the bay. Gracilaria survives in deeper water in summer by the pulsing of nutrients on an approximately 6-day cycle of movement of the thermocline that separates nutrient-rich bottom water from warm oligotrophic surface water. Ammonium-rich fish-factory discharge into this surface layer in a sector of the bay provided localised conditions for Ulva to out-compete Gracilaria at depths of 2–5m, demonstrating the powerful disruptive effect of eutrophication in this strongly stratified system.     

Opportunities and challenges for the development of an integrated seaweed-based aquaculture activity in Chile: determining the physiological capabilities of <Emphasis Type="Italic">Macrocystis</Emphasis> and <Emphasis Type="Italic">Gracilaria</Emphasis> as biofilters

Seaweed production is a reality in Chile. More than ten species are commercially used to produce phycocolloids, fertilizers, plant growth control products, human food or animal fodder and feed additives. These multiple uses of algae offer a number of possibilities for coupling this activity to salmon, abalone and filter-feeder farming. In this context, different experiments carried out in Chile have demonstrated that Gracilaria chilensis and Macrocystis pyrifera have great potential in the development of an integrated aquaculture strategy. The present Integrated Multi-Trophic Aquaculture (IMTA) approach study showed that Gracilaria can be cultured best at 1 m depth whereas Macrocystis has an especially good growth response at 3 m depth. Both species use available nitrogen efficiently. On the other hand, high intensities of solar radiation (UV and PAR) can be critical at low depths of cultivation, and our results indicate that both species show photosynthetic susceptibility mainly at noon during the summer. The demand of Macrocystis for abalone feeding is increasing, thus improving the opportunity for developing an integrated nutrient waste recycling activity in Chile. Although Gracilaria shows a higher nitrogen uptake capacity than Macrocystis, its market value does not yet allow a massive commercial scaling.     

Epiphytic diatoms of the inshore marine area near Davis Station

Collections of macrophytic algae from the subtidal and lower intertidal regions were processed to observe the diatom epiphytes both by light and scanning electron microscopy. For the purpose of comparison some samples of the sub-ice assemblage were also collected and processed similarly. The standing crop of epiphytes was high throughout the winter as well as the summer but the community composition varied depending upon the collection site and the morphology of the host macrophyte. The genus Cocconeis was ubiquitous achieving densities approaching 10⁵ cells cm⁻² and surpassed only by Nitzchiawith a density of twice that amount on one sample.     

Diet,food preference,and algal availability for fishes and crabs on intertidal reef communities in southern California

Synopsis Herbivory by wide-ranging fishes is common over tropical reefs, but rare in temperate latitudes where the effects of herbivorous fishes are thought to be minimal. Along the west coast of North America, herbivory by fishes on nearshore reefs is largely restricted to a few members of the Kyphosidae, distributed south of Pt. Conception. This paper presents information on natural diets and results from feeding choice experiments for two abundant kyphosids from intertidal habitats in San Diego, California —Girella nigricans andHermosilla azurea, and similar data for the lined shore crab,Pachygrapsus crassipes, which also forages over intertidal reefs. These results are compared with the availability of algae in intertidal habitats measured during summer and winter, on both disturbed and undisturbed habitats. The diets of juveniles ofG. nigricans andH. azurea collected from nearshore habitats were dominated by animal prey (mainly amphipods), but adults of these fishes, andP. crassipes, consumed algae nearly exclusively, with 26, 10, and 14 taxa of algae identified fromG. nigricans, H. azurea, andP. crassipes, respectively. Algae with sheet-like morphologies (e.g.Ulva sp.,Enteromorpha sp., members of the Delesseriaceae) were the principal algae in the diets of the fishes, and calcareous algae (e.g.Corallina sp.,Lithothrix aspergillum) and sheet-like algae (Enteromorpha sp.) comprised the greatest identifiable portion of the shore crab's diet. Feeding choice experiments indicated that the fishes preferred filamentous algae (e.g.Centroceras clavulatum, Polysiphonia sp.,Chondria californica) and sheet-like algae (e.g.Enteromorpha sp.,Ulva sp.,Cryptopleura crispa) over other algal morphologies, whereas the shore crab chose jointed calcareous algae (e.g.Lithothrix aspergillum, Corallina vancouveriensis, Jania sp.) most frequently. The diets and preferences for algae by the fishes were generally most similar to the assemblage of algae available in early successional (disturbed) habitats during summer when sheet-like and filamentous algae are abundant. The shore crab exhibited the opposite trend with a diet more similar to late successional (undisturbed) habitats.     

In vitro recruitment of Ulva sp. and Enteromorpha sp. on gametophytic and tetrasporophytic thalli of four populations of Chondracanthuschamissoi from Chile

Chondracanthus chamissoi is a red alga which is acquiring an increasing economic importance in Chile and becoming a target species for cultivation. Because epiphytism is a major problem in the mariculture of seaweeds, the recruitment of Ulva sp. and Enteromorpha sp. on gametophytic (cystocarpic) and tetrasporophytic thalli of C. chamissoi was tested in vitro on four populations from different locations in Chile. For Ulva sp., the density, cover and length of the recruits varied between the reproductive phases of the host and among the studied populations of C. chamissoi. In most experiments, a larger number of epiphytic thalli was observed on gametophytic plants of C. chamissoi; populations from Calderilla and Lechagua had a higher resistance to epiphytism. For Enteromorpha sp., its ability to grow epiphytically on both phases of the host showed a greater variability, but was inferior to that of Ulva sp. The differential resistance to epiphytism in both reproductive phases and in plant origin indicates the possibility of obtaining selected strains of C. chamissoi with lower susceptibility to epiphytism that could be utilized in planning maricultural programs.     

Changes in Epiphytic Bacterial Communities of Intertidal Seaweeds Modulated by Host, Temporality, and Copper Enrichment

This study reports on the factors involved in regulating the composition and structure of bacterial communities epiphytic on intertidal macroalgae, exploring their temporal variability and the role of copper pollution. Culture-independent, molecular approaches were chosen for this purpose and three host species were used as models: the ephemeral Ulva spp. (Chlorophyceae) and Scytosiphon lomentaria (Phaeophyceae) and the long-living Lessonia nigrescens (Phaeophyceae). The algae were collected from two coastal areas in Northern Chile, where the main contrast was the concentration of copper in the seawater column resulting from copper-mine waste disposals. We found a clear and strong effect in the structure of the bacterial communities associated with the algal species serving as host. The structure of the bacterial communities also varied through time. The effect of copper on the structure of the epiphytic bacterial communities was significant in Ulva spp., but not on L. nigrescens. The use of 16S rRNA gene library analysis to compare bacterial communities in Ulva revealed that they were composed of five phyla and six classes, with approximately 35 bacterial species, dominated by members of Bacteroidetes (Cytophaga-Flavobacteria-Bacteroides) and α-Proteobacteria, in both non-polluted and polluted sites. Less common groups, such as the Verrucomicrobiae, were exclusively found in polluted sites. This work shows that the structure of bacterial communities epiphytic on macroalgae is hierarchically determined by algal species > temporal changes > copper levels.     

Desiccation enhances phosphorylation of PSII and affects the distribution of protein complexes in the thylakoid membrane

Desiccation has significant effects on photosynthetic processes in intertidal macro‐algae. We studied an intertidal macro‐alga, Ulva sp., which can tolerate desiccation, to investigate changes in photosynthetic performance and the components and structure of thylakoid membrane proteins in response to desiccation. Our results demonstrate that photosystem II (PSII) is more sensitive to desiccation than photosystem I (PSI) in Ulva sp. Comparative proteomics of the thylakoid membrane proteins at different levels of desiccation suggested that there were few changes in the content of proteins involved in photosynthesis during desiccation. Interestingly, we found that both the PSII subunit, PsbS (Photosystem II S subunit) (a four‐helix protein in the LHC superfamily), and light‐harvesting complex stress‐related (LHCSR) proteins, which are required for non‐photochemical quenching in land plants and algae, respectively, were present under both normal and desiccation conditions and both increased slightly during desiccation. In addition, the results of immunoblot analysis suggested that the phosphorylation of PSII and LHCII increases during desiccation. To investigate further, we separated out a supercomplex formed during desiccation by blue native‐polyacrylamide gel electrophoresis and identified the components by mass spectrometry analysis. Our results show that phosphorylation of the complex increases slightly with decreased water content. All the results suggest that during the course of desiccation, few changes occur in the content of thylakoid membrane proteins, but a rearrangement of the protein complex occurs in the intertidal macro‐alga Ulva sp.     

Ceramialean epiphytism in an intertidal Gracilaria chilensis (Rhodophyta) bed in southern Chile

The cultivation of the agarophytic red alga Gracilaria has become an activity of major importance in several parts of the world. However, Gracilaria cultivation in Chile still faces problems such as epiphytism. We report ceramialean epiphytism abundance, recruitment patterns and the microscopic stages fixed on the Gracilaria thalli in an intertidal bed (Metri bay) of southern Chile. Using a factorial field experiment, we analyze the effect of intertidal elevation and the use of epiphyte free inoculum on the abundance of ceramialean epiphytic algae. This evidence is used to provide management and control recommendations for ceramialean epiphytes. The results show a summer recruitment and increase in abundance of ceramialean epiphytes. A seasonal and spatial pattern of abundance of microscopic stages of this epiphytic algae was also found, showing a significant increase from the apical (new tissues) to the central parts of the thalli (older tissues). Apical tissues are free of epiphytic propagules. The epiphyte-free tissue zone decreases significantly from winter to summer. Also, a significantly higher density of microscopic stages of ceramialean epiphytes was found on the thalli collected in the farming are a during the summer at low tidal levels. The experimental results indicated that the abundance of epiphytes was greater at the lower tidal levels than at the higher distribution limits of Gracilaria and it was not possible to control epiphytism by manual cleaning. This revised version was published online in September 2006 with corrections to the Cover Date.     

Recent trends of seaweed production in Chile

In the last fourteen years the production of seaweeds in Chile has ranged from 74 000 to 229 000 wet metric tons per year and has included about twenty species belonging to Phaeophyta and Rhodophyta. The only source of this production has been the exploitation of natural beds, except for Gracilaria, which is the only case of commercial cultivation and contributes significant quantities to total production. Initially most of the raw material was exported but currently important quantities of Gracilaria and several carrageenophytes are being processed by local industry. Changes in production of the main resources are analyzed with consideration of potential demand, level of knowledge about natural beds, and the situation of total Gracilaria farming, in order to attempt predictions for the supply. Current possibilities of applying new technologies to cultivate other economically important Chilean seaweeds are also analyzed and discussed.     

Effect of grazing by isopods and amphipods on growth of Ulva spp. (Chlorophyta)

Eutrophication of shallow coastal waters often leads to blooms of macroalgae. Grazing by crustaceans, such as amphipods and isopods, can reduce macroalgal biomass accumulation. At the same time, growth of the macroalgae can be stimulated by epiphyte removal. The role of grazing by isopods and amphipods on Ulva spp. biomass development was investigated in the Veerse Meer, a brackish lagoon situated in the southwest Netherlands. Exclusion of grazing in the field did not stimulate Ulva spp. growth. In fact, growth rates were higher in exclosures that allowed grazers to enter. Edibility tests identified the amphipod Gammarus locusta, and the isopods Idotea chelipes and Sphaeroma hookeri as potential grazers on Ulva spp. However, when epiphytic diatoms were present on the Ulva spp. thalli, Gammarus and Sphaeroma grazed on ephiphytes and not on Ulva tissue. Only Idotea continued to graze on Ulva spp. A laboratory growth experiment revealed a positive effect of Gammarus presence on Ulva spp. growth, probably caused by preferential removal of epiphytic diatoms from the Ulva spp. thalli. The growth stimulation by epiphyte removing grazers such as Gammarus may explain the higher growth rates in the presence of grazers observed in the field. When determining the potential role of invertebrate grazers in controlling macroalgal biomass accumulation, it is important to include an assessment of the epiphyte abundance on the macroalgae, as preferential removal of epiphytes may stimulate growth and thus have the opposite effect.     

Attenuation of water velocity and incident light as a function of shape parameters inGracilaria

Characteristic shape parameters, light intensities and relative water velocities were estimated in thalli of free-moving seaweeds, using threeGracilaria-like species:G. cornea, G. conferta andGracilariopsis lemaneiformis. Relative velocities over the branches were determined mostly by rotation of the algae in the water as opposed to linear translation. The tree major shape parameters of the thallus, weight, volumetric specific weight and areal specific weight, explain the differences in relative velocity. Relative velocities near the center of the thallus were about 50% to 80% of the external velocity. Light intensities at the vicinity of the center ofG. cornea ranged between 60% to 90% of the external light intensity. Light attenuation in the center was proportional to the weight of the thallus. The significance of light and velocity attenuation as a function of shape parameters is discussed.Author for correspondence     

The effect of cooling seawater effluents of a power plant on growth rate of cultured Gracilaria conferta (Rhodophyta)

The effect of cooling seawater effluents of a power plant on the growth rate of Gracilaria conferta in tanks has been studied, as a possible solution for the decrease in the winter growth rate in ambient seawater tanks. The Gracilaria cultures did not survive more than 2–8 weeks in the power plant effluents during the one-year-long repeated experiments. The major reason was the high accumulation of copper, iron, lead and chromium from the power plant effluents as compared to concentrations in Gracilaria cultured in ambient seawater. The survival increased and the copper accumulation decreased significantly when the effluents were passed through an Ulva biofilter.     

Effects of stock loading and planting distance on the growth and production ofGracilaria chilensis in rope culture

Through experimental manipulation of stock loading and planting distances in rope culture, this study evaluates the hypothesis that optimum density for growth and production ofGracilaria chilensis vary within a bed. Small packages ofGracilaria disposed at short distances exhibit higher growth and production rates in the landward ends of ropes than larger packages of seaweed disposed at longer distances. In these experiments, the landward end of ropes faces estuarine conditions, with reduced salinities and increased sediment loads during low tides. The interacting effects of stocks loading and position in the rope can affect growth and production rates so much as to nullify the 3.5-fold summer increments in production that occur in these estuarine beds of southern Chile. It is concluded that through manipulation of planting distances and stock loading, the production of this species could be increased up to 35% in some areas.     

Multiple factors promoting narrow host range in the sea hare,Aplysia californica

Summary Juvenile sea hares, Aplysia californica, utilize only the red algae Plocamium cartilagineum and Laurencia pacifica as host plants at Santa Catalina Island, CA. I tested three hypotheses which might account for this pattern of host choice: 1) A. californica specialize on the algae on which they grow best, 2) A. california specialize on algae from which they acquire secondary compounds that protect them from predators, and 3) A. californica specialize on certain algae in order to lower their encounter rates with predators. The results suggested that host range in the Aplysia californica system is affected by more than one factor. The first hypothesis was supported. A. californica of three size classes grew well on Plocamium, but could not grow at all on most other species of algae. Larger A. californica were able to grow on species of algae that smaller ones could not. The second hypothesis was also supported. Small A. californica grown on Plocamium were rich in terpenes. Small A. californica grown on Ulva sp. were terpene-free. Rock wrasses, Halichoeres semicinctus, were more likely to eat Ulva-fed A. californica than Plocamium-fed A. californica. Other fish and lobster, Panulirus interruptus, did not discriminate between the two groups. Kelp bass, Paralabrax clathratus, which were force-fed Ulva-fed A. californica regurgitated them less often, and after digesting them more completely, than did Paralabrax force-fed Plocamium-fed A. californica. The third hypothesis was rejected. A. californica located on Plocamium were not more cryptic to the opisthobranch Aglaja inermis (navanax), or to the pomacentrid fish, Hypsypops rubicundus, than were A. californica located on other algae. In addition, navanax, a specialist predator of opisthobranchs, was significantly more abundant on Plocamium than on other algae.