Prospects and challenges for industrial ... - Wiley Online Library

J. Phycol. 51, 821–837 (2015) © 2015 Phycological Society of America DOI: 10.1111/jpy.12326

REVIEW PROSPECTS AND CHALLENGES FOR INDUSTRIAL PRODUCTION OF SEAWEED BIOACTIVES1 Jeff T. Hafting,2 James S. Craigie Acadian Seaplants Limited, 30 Brown Avenue, Cornwallis, Nova Scotia, Canada

Dagmar B. Stengel Botany and Plant Science, School of Natural Sciences & Ryan Institute for Environmental, Galway, Ireland

Rafael R. Loureiro Department of Biology, Ave Maria University, Ave Maria, Florida, USA

Alejandro H. Buschmann Centro i-mar & CeBiB, Universidad de Los Lagos, Puerto Montt, Chile

Charles Yarish Department of Ecology & Evolutionary Biology, University of Conneticut, Stamford, Connecticut, USA

Maeve D. Edwards National University of Ireland, Galway, Ireland

and Alan T. Critchley Acadian Seaplants Limited, 30 Brown Avenue, Cornwallis, Nova Scotia, Canada

Both internal concentrations and composition of bioactive compounds can fluctuate seasonally, geographically, bathymetrically, and according to genetic variability even within individual species, especially where life history stages can be important. History shows that successful expansion of seaweed products into new markets requires the cultivation of domesticated seaweed cultivars. Demands of an evolving new industry based upon efficacy and standardization will require the selection of improved cultivars, the domestication of new species, and a refinement of existing cultivation techniques to improve quality control and traceability of products.

Large-scale seaweed cultivation has been instrumental in globalizing the seaweed industry since the 1950s. The domestication of seaweed cultivars (begun in the 1940s) ended the reliance on natural cycles of raw material availability for some species, with efforts driven by consumer demands that far exceeded the available supplies. Currently, seaweed cultivation is unrivaled in mariculture with 94% of annual seaweed biomass utilized globally being derived from cultivated sources. In the last decade, research has confirmed seaweeds as rich sources of potentially valuable, health-promoting compounds. Most existing seaweed cultivars and current cultivation techniques have been developed for producing commoditized biomass, and may not necessarily be optimized for the production of valuable bioactive compounds. The future of the seaweed industry will include the development of high value markets for functional foods, cosmeceuticals, nutraceuticals, and pharmaceuticals. Entry into these markets will require a level of standardization, efficacy, and traceability that has not previously been demanded of seaweed products.

Key index words: bioactive; cosmeceutical; cultivation; efficacy; fuctional food; nutraceutical; pharmaceutical; seaweed; standardization; traceability; valueadded

OVERVIEW

The global seaweed industry has seen many shifts in focus over the course of its history, from exploiting seaweeds as fertilizers and a source of potash via iodine production to hydrocolloid extraction (Synyt-

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Received 25 September 2014. Accepted 9 June 2015. Author for correspondence: e-mail [email protected]. Editorial Responsibility: M. Graham (Associate Editor)

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sya et al. 2015). At all stages the future of the industry has always been viewed as containing “potential”; this is no less relevant today than it was 100 years ago or more when the industry looked very different. Future casting for an industry that is global in scale but local in structure can be notoriously difficult, yet it is a useful exercise to examine historical examples (Section 2). Relevant current trends, known challenges and opportunities can be used to anticipate future requirements for the complex network of researchers, producers, product processors, and developers. Recent trends show that applied phycological research has shifted somewhat, from basic biology (e.g., life history elucidation) and hydrocolloid studies toward the identification and assay of specific bioactive compounds and their effects on plant, animal, and human health (Pangestudi and Kim 2015). This change of focus has not been driven by a reduction in market viability for commodity production, rather it has been a function of a matured industry which now requires more attention to applications development, engineering, and management than to phycologically based research (Bixler and Porse 2010). Commodity here is defined as high-volume, low-unit value production, as represented by the food and food-ingredient hydrocolloid industries. Within these industries, there are certain products that can be considered as value-added and not as commodities (i.e., high value foods and specialty hydrocolloids; Cho and You 2015) but, in general, seaweed cultivation has produced low cost commodities to satisfy consumer demand. Many investigators foresee a future where seaweeds are grown for high value functional product markets such as cosmeceuticals (Balboa et al. 2015), nutraceuticals (Humaya and Kim 2015), and pharmaceuticals (Section 3). Entry into these science-based markets entails significant challenges, as these industries demand more rigorous quality and standardization of biomass than has previously been expected for seaweeds. Current cultivation technologies also may not be suitable for the production of standardized biomass (Section 4), and seaweed cultivars selected as commodity producers will not necessarily be optimal as raw materials for bioactive compound extraction (Section 5). Genomics and perhaps genetic engineering will most certainly play a role in the improvement of future seaweed cultivars. Past successes in large-scale seaweed cultivation came through a combination of excellent scientific and engineering work, coupled with large consumer demand that was under-supplied with raw materials (Section 2). The development of more value-added and efficacious products will require the concomitant development of markets for these functional products. The past informs the future here and success will not be achieved without coupling multidisciplinary scientific and technological research

with a thorough understanding of existing and emerging markets for seaweeds. Currently, the development of value-added products for human health is generally research-driven, and not pulled by consumer demand, with some exceptions. Success will require sophisticated marketing to create demand for health products, informed by a solid scientific understanding of the many benefits of seaweed product usage and consumption. The cultivation of seaweeds for commodities such as foods and food-ingredient hydrocolloids has been and will continue to be highly successful in the future. Total seaweed hydrocolloid sales worldwide in 2009 amounted to US$ 1.018 billion (Bixler and Porse 2010). Our intention is not to detract from the success of these commodity-based industries, or to suggest that they will be replaced by more lucrative value added products. However, increasingly difficult economic conditions have made the concept of “value-addition” attractive as a means for producers to capture a larger share of the consumer dollar. Value addition can be effected in several ways (Section 3), but the greatest promise for return on investment comes from the development of new products, marketed for their effects on human health (Mouritsen 2013). A BRIEF HISTORY OF SEAWEED CULTIVATION

The history of cultivating macroalgae (seaweeds) is brief relative to the time humans have harvested and utilized these organisms to benefit society. In Asian cultures, seaweed utilization is long standing, and their societal value led to augmentation of the limited natural supply of highly regarded members of genera such as Pyropia (formerly Porphyra or nori; Sutherland et al. 2011) and Saccharina (formerly Laminaria, haidai or kombu; Waaland 1981, Nisizawa 1987, Pereira and Yarish 2008). Seaweeds of economic value listed by Tseng (1981) comprise some 493 species from 107 genera, including two species of cyanobacteria. Fewer than 20 species from 11 genera are cultivated commercially, and only ~6 can be considered as true crop plants in that their cultivated biomass exceeds that harvested from nature. Seaweed cultivation today is practized globally where maritime coastlines are suitable, although it originated in, and continues to be dominant in, the Asian-Pacific region (Naylor 1976, Tseng and Fei 1987, Buchholz et al. 2012, Valderrama 2012, Mazarrasa et al. 2013, Valderrama et al. 2013). The success of the most widespread seaweed cultivation industries (i.e., nori, kelps, carrageenophytes and agarophytes), as discussed below, can be attributed to the partnership of basic science, and consumer demand for products. Nori. Japanese nori production rarely reached one billion sheets per year prior to the discovery of the life cycle of Pyropia (Porphyra) by Kathleen M. Drew (Baker) (Drew 1949). In the subsequent

INDUSTRIAL PRODUCTION OF SEAWEED BIOACTIVES

weed farming (Li et al. 2007). Fertilization of the sea farms to improve yield and quality of the kelp was adopted in the late 1950s as reviewed by Tseng (1981) but is no longer in use in China. In Japan, the ability to halve the 2-year production cycle for kombu by forced cultivation was introduced in 1968 (Hasegawa 1972, 1976); the technique revolutionized commercial production of S. japonica (Ohno 1990). Carrageenophytes. Demand for the unique red seaweed hydrocolloid, carrageenan, drove mariculture development as it became apparent in the 1960s that natural beds of Irish moss (Chondrus crispus and Mastocarpus stellatus) could not meet the escalating market requirements. Alternative sources of carrageenans were sought and commercial cultivation of Betaphycus gelatinus (formerly Eucheuma gelatinae) in the Hainan Island area of China dates from 1960 (Tseng 1981, Rawson et al. 2002). Major developments occurred a decade later in the southern Philippines where Max Doty, collaborating with staff from Marine Colloids Ltd. (Rockland, ME, USA), fostered mariculture of Kappaphycus alvarezii (formerly Eucheuma cottonii) for kappa-carrageenan extraction (Deveau and Castle 1976, Doty 1987, Pereira and Yarish 2008, Hurtado et al. 2015). Strain selection was the critical advance. Following introduction of the naturally selected Tambalang strain of “cottonii,” production went from a negligible amount in 1971 (0–6 tonnes) to 10,000 tons wet harvest in 1974 with a corresponding reduction in wild harvest from 534 to 75 tons. The export value rose from US$ 168,210 to US$ 4,533,750 raising a farming family income to more than three-fold the Philippine average (Deveau and Castle 1976). The intervening 40 years has seen Eucheuma spp. (e.g., E. denticulatum) and Kappaphycus spp. farming spread to many countries accounting for much of the 7.5% annual growth of seaweed aquaculture worldwide (FAO 2013, Mazarrasa et al. 2013, Hurtado et al. 2014). Particularly rapid development occurred in the Philippines and especially in Indonesia where production now greatly exceeds that in the Philippines (FAO 2012). Lesser quantities are produced in the Solomon Islands, Malaysia, India, Tanzania and Mexico (Valderrama 2012). A detailed and comprehensive country-by-country review of these developments in the aquaculture of carrageenophytes and their socio-economic impacts is available (Valderrama et al. 2013). Agarophytes. The discovery of agar in Japan in 1658 initiated the increase of agarophyte harvesting; industrialization of the agar extraction process in the 18th century resulted in a dry stable agar called kanten in Japan (McHugh 1987). Cultivation of Gracilaria verrucosa (now G. gracilis) was initiated in the late 1950s in Guangdong, China by outplanting frond fragments in bamboo sticks and, more recently, in floating nets and long-lines (Tseng 1981, Yang and Yarish 2011). Pond culture of G. ver-

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decade, Japanese and Chinese scientists established large-scale production of conchospores through controlled cultivation of the conchocelis phase of Py. tenera and later of other Pyropia spp. Exotic Pyropia species were introduced and numerous strains were selected to improve the crop and broaden the geographic area used for cultivation (Saito 1976). Freezing ( 20°C) small seedlings germinated on nets was a major technical innovation in 1965–1966 that stabilized nori production and greatly extended the farming season. These sciencebased advances allowed seeding of culture nets at will and with additional species or cultivars more suited to the environmental conditions pertaining at a particular farm site. Nori production followed an almost exponential increase from 1 billion (B) sheets prior to 1949 to >9 B sheets per year by 1973 (Kito 1982, citing Miura 1975). Global nori production in 2008 was 21.6 billion sheets (Japan, 8.98 B; Korea, 8.6 B; and China, 4.0 B) representing ~65,000 dry tonnes or 1.81 million tonnes of wet biomass (Levine and Sahoo 2010). Control of cropfouling species and the alleviation of both physiological and microbial diseases of nori and other macroalgae resulted from intense research efforts over decades to the present time (Tseng 1981, Chiang 1984, Largo 2002, Neil et al. 2008 and references therein). Kelp. Although cultivation of Undaria pinnatifida or wakame had begun as early as ~1940 in Japan, shortages of supply led to improved cultivation technology beginning around 1955. A two-step process was developed of cultivating gametophytes on synthetic yarn seeded with zoospores from mature sporophylls, followed by transfer of the twine to ropes for outplanting in the sea where the embryos would develop into the harvestable sporophytes (Saito 1976). By 1968, the world production of wakame well exceeded that obtained from the natural harvest (69,680 vs. 48,300 tonnes), reaching >500,000 tonnes by 1993 and 1.7 million tonnes in 2010 (Tseng 1981, Yamanaka and Akiyama 1993, Sahoo and Yarish 2005, FAO 2012). Innovations in Saccharina japonica (kombu) cultivation arose from the intense research efforts in Japan and especially in post-revolutionary China (MacFarlane 1968, Cheng 1969, Mathieson 1975, Hasegawa 1976, Ling 1990, McHugh 2003, Pereira and Yarish 2008). In general, the research related to the physiology, life cycle, and management of diseases and fouling of the species. Notable were the hybridization experiments initiated by Professor Fang et al. (1962, 1966) (Li et al. 1999) which led to larger, sturdier plants, high iodine producers, and to higher temperature tolerant strains that permit S. japonica to be cultivated as far south as Fujian province in China (Zhang et al. 2011). A recent hybrid, Dongfang 2, out-produced two commercial varieties by 26% and 62% in large-scale field trials demonstrating the benefits of hybrid vigor in sea-

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rucosa either alone or in polyculture with suitable animal species dates from 1967 in Taiwan (Briggs and Funge-Smith1993, Sahoo and Yarish 2005). The agarophytes, Gelidium, Gracilaria, Pterocladia and Gelidiella are widely distributed globally and natural sources supply the largest portion of biomass destined for the agar market. An exception occurs in Chile where commercial cultivation of Gracilaria chilensis began in 1982 in response to increasing demand for agar and depleted local seaweed resources. By 1991, the farmed alga accounted for 84% of the Gracilaria produced in the country (Buschmann et al. 2001). The seeding of farms traditionally required a stock of vegetative Gracilaria that was planted in the sea bottom or on lines or on nets held in the water column (Santelices and Doty 1989). Details on Gracilaria cultivation including a discussion of the problems of epiphytes, grazers, and frond aging have been reported (Westermeier et al. 1993, Buschmann et al. 1994, 1995, 2001, Redmond et al. 2014). A new approach to mass cultivation employed cystocarpic G. chilensis to seed polypropylene rope. After a brief incubation period to permit spore germination, the ropes were out-planted in the sea. The technique was successful and has been adopted by one commercial grower in Chile (Buschmann et al. 2001). This new technology now has been extended to the culture of G. edulis in India (Jayasankar and Ramamoorthy 1997). Summary. The value of farmed seaweeds at US > $6.0 billion in 2012 (FAO 2014) has increased by three orders of magnitude during the past century, and continues to grow at an annualized rate of 6.84% from 2003 to 2012 (Loureiro et al. 2015). It is therefore not surprising that current research should be directed to seaweeds as alternative sources of sustainable foods, fuels. and bioactive substances to improve health and to counter diseases in both humans and animals (Dhargalkar and Pereira 2005, Winberg et al. 2009, Buchholz et al. 2012, Mohamed et al. 2012, Periyasami et al. 2013). History shows that successful cultivation was achieved with intensive research into seaweed physiology, life cycle, disease, fouling prevention, and strain selection (e.g., hybridization). Equally important was the development of ready markets for the products of limited supply. Development of both new cultivars and new markets will continue to be critical to the success of a future higher value seaweed industry. FROM COMMODITY TO VALUE ADDITION

Value addition can come in many forms and here refers to an increase the difference between unit cost and generated revenue. Currently many researchers are working on elucidating bioactive and functional properties of extracted seaweed compounds for value addition. Bioactivity here is

defined as having a dosage dependent interaction or biological effect when applied to living cells, beyond simple nutritive effects. A functional product is one that contains bioactive compounds that have clinically documented health benefits upon consumption. Efficacious products are those with the capacity to produce beneficial effects consistently. Seaweed based products that have known and clinically documented bioactivity have potential to become value-added functional products as cosmeceuticals, functional foods, nutraceuticals, and pharmaceuticals. Bioprospecting. Although the modern pharmaceutical industry is based on terrestrial plants, marinesourced bioactive compounds from sponges, tunicates, bryozoans, soft corals, molluscs, and microalgae have been explored for their therapeutic potential during the last 50 years or so, but only a few marine algae have been investigated (Jha and Zi-Rong 2004, Blunt et al. 2015). Seaweeds, a late addition to the bioprospecting efforts around the globe, are highlighting the potential for efficacybased products for human consumption (Demunshi and Chugh 2009). While a number of academic researchers have surveyed local seaweed flora from the perspective of potential utility in the health industry by broadly screening specific extracts with established bioassays (Kim 2014), the development of a seaweed industry based upon bioactive compounds is truly in its infancy. In vitro and animal studies suggest the potential for human health promotion that may include antiviral, anticancer, anticoagulant, gut health promotion, and prevention of metabolic syndrome (Teas et al. 2009, 2013, Holdt and Kraan 2011, Kulshreshtha et al. 2014, 2015, Murphy et al. 2014). Seaweeds contain unique bioactive compounds not found in terrestrial sources, including proteins polyphenols and polysaccharides (Nisizawa 2002). The few human trials and general lack of clinical evidence to support cell-based and animal evidence (Brown et al. 2014) remain as significant barriers to the development of value added functional products for human consumption. Value added product spectrum. Research intensity required to achieve returns on investment increases along the following spectrum: food, cosmeceutical, functional food, nutraceutical, and pharmaceutical products. Foods (and food ingredients) and cosmeceuticals are well developed industries, with globally marketed products of high quality with well-established supply chains (Kim 2012). The functional food, nutraceutical, and pharmaceutical sectors require higher levels of evidence of effectiveness than foods and cosmeceuticals, and there are few success stories within these higher product categories. Regulatory agencies require that very high levels of standardized efficacy are demonstrated clinically before health claims can be made to aid marketing. Without health claims, the highest


SEAWEED CHEMICAL DIVERSITY

Marine macroalgae provide a broad palette of natural chemicals with many potential applications in biotechnology. However, the chemical richness available for exploitation (Stengel et al. 2011) needs to be appreciated in view of the taxonomic diversity of algae. Macroalgae belong to three major independent lineages (Ochrophyta, Rhodophyta and Chlorophyta) and vast chemodiversity exists between and within the major algal groups (Baurain et al. 2010). Additionally, considerable genetic diversity exists within and between natural seaweed populations as documented over the last 20–25 years (Billot et al. 2003). Compounds of particular

interest for food and health applications include those with antioxidant (Cornish and Garbary 2010) and anti-cancer (Teas et al. 2009, 2013, Fedorov et al. 2013) attributes. Such bioactivities have been attributed to a range of compounds (e.g., polysaccharides including major phycocolloids, fucoidans and laminarans, pigments, phenolics, lipids and fatty acids; Nishino et al. 2002, Ozawa et al. 2006, Prasanna et al. 2007, Zubia et al. 2008, Schmid et al. 2014). Natural variations in chemical diversity and bioactivity. Stengel et al. (2011) have reviewed the implications of chemical diversity within seaweeds from natural stocks as it affects commercial applications. Some examples of the effects of various environmental influencers on the content of commercially interesting seaweed compounds and bioactivities are summarized in Table 1. Environmental factors such as light climate (depth, turbidity, UV exposure), nutrient availability (eutrophication), sampling location, sampling season, grazing pressure, salinity, biomass density, water motion, and temperature all influence seaweed tissue composition and thus their bioactivities. Chemical variability occurs on different scales at the population and the individual levels. On a geographical scale, chemical diversity may be due to both genetic differentiation into locally adapted strains, or phenotypically acclimated individuals exposed to combinations of environmental variables. Recently, with improved analytical techniques, several detailed profiling studies (Craigie et al. 2008, Young et al. 2013) have documented the natural chemical diversity within and between populations, further demonstrating the richness of wild raw material derived from different natural populations. For example, genetically different strains of the same species from different locations may exhibit different adaptive features to local environments with regard to phycobilin and chlorophyll contents (Zhang et al. 2012). In-sea cultivation for standardized efficacy challenges. Seaweed production is dominated by traditional “in-sea” cultivation techniques that typically produce large amounts of monospecific harvestable biomass at relatively low cost (i.e., commodity production such as Pyropia species; Pereira and Yarish 2010). They have the great advantage of low-cost, and research will continue to improve quality and cost of commodity-type products as their markets are expected to grow (Bixler and Porse 2010). Further, in-sea methods are particularly suited for cultivars with large thalli (e.g., Laminariales) used mainly for food and fodder. In the future, bioactive compounds from these could be produced using in-sea methods as on-land (Section 5.3) cultivation may be unsuitable for the grow-out of large mature fronds. Seaweed biomass derived from in-sea cultivation is subject to spatial and seasonal variation as documented above except where temporal and spatial

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returns on investment made by developers cannot be realized and their development costs may not be rewarded sufficiently. The development of seaweedbased products within these categories is currently being researched worldwide. Formulators of functional foods, nutraceuticals, and pharmaceuticals have specific requirements for raw materials that must be satisfied. These demands often are not given the consideration they deserve during the development process. Seaweed products that would be marketed based on efficacy must attract the attention of formulators who are limited by regulatory considerations to approved sources of raw materials. Botanical formulators are usually unfamiliar with seaweeds, as there are few available seaweed species on the market (compared to terrestrial plants). In addition, seaweeds that are available have not been optimized for efficacy (i.e., they are commodity products, optimized for biomass production at low cost) and therefore can be expected to be highly variable in effectiveness (see Section 4). Factors considered by nutraceutical formulators include: cost, efficacy (mode of action and human clinical trials), sourcing (adulteration, contamination, environmental sustainability, standardization), quality assurance, regulatory requirements (these differ by country, as does the definition of novel ingredients), and procurement/purchasing (e.g., availability of biomass to meet demand on an on-going basis; Gellenbeck 2012). A major barrier to the inclusion of seaweeds in functional products results from regulatory limitations on seaweeds that have not traditionally been used by humans in the local jurisdictions. Hazard Analysis Critical Control Points and ISO22000 safety protocols are also being developed for the production of seaweeds, and adherence to these protocols will become mandatory. The development process for seaweed inclusion in nutraceutical markets is therefore long and complex. However, potential rewards are foreseen for efficacious, standardized, sustainably sourced raw materials available to experienced formulators ready to invest in developing markets for novel, innovative, seaweed-based products.

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TABLE 1. Research on factors known to influence seaweed tissue content and bioactivity. Compound/bioactivity

Mineral content Proteins

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Carbohydrates

Influencer

Sampling season Eutrophication (light, turbidity) Nutrient availability Salinity Reproductive stage

Blade age

Alginic acids Carrageenans, agars

Salinity Sampling season Light climate Nutrient availability Sampling location Biomass density Water motion Temperature Grazing pressure Sampling season

Fatty acids

Light harvesting pigments

Life history stage Sampling season

Light climate Eutrophication (light, turbidity) Diurnal light level Nutrient availability

Seaweed

Eisenia arborea Gracilaria cervicornis Sargassum vulgare Gracilaria sp. Gracilaria sp. Sargassum sp. Himanthalia elongata Ascophyllum nodosum Saccharina japonica Undaria pinnatifida Saccharina latissima Fucus serratus Fucus vesiculosus Myagropsis sp. Sargassum sp. Gelidium pulchellum Chondrus crispus Gelidium crinale Gelidium robustum Pterocladia capillacea G. pulchellum G. pulchellum G. crinale Hypnea musciformis Gracilaria verrucosa C. crispus Gracilaria conferta Gelidiella acerosa P. capillaceae C. crispus Cystoseira nodicaulis Cystoseira tamariscifolia A. nodosum F. serratus F. vesiculosus H. elongata Pelvetia canaliculata Laminaria digitata S. latissima Pyropia dioica Ceramium virgatum C. crispus Palmaria palmata Gracilaria gracilis Codium fragile Ulva lactuca A. nodosum A. nodosum Pyropia laciniata C. crispus Ulva rotundata Gelidium latifolium Phyllariopsis purpurascens Laminaria solidungula S. latissima A. nodosum Gracilaria chilensis

Reference

Herna´ndez-Carmona et al. (2009) Marinho-Soriano et al. (2006) Bird et al. (1982) Marinho-Soriano et al. (2006) Jones (1957), Brenchley et al. (1997), Stengel et al. (1999) Aberg and Pavia (1997) Aberg and Pavia (1997) Skirptsova et al. (2010) Black (1954) Kremer (1975) B€ack et al. (1992) Kim and Park (1985) Sousa-Pinto et al. (1999) Chopin et al. (1995), Boulus et al. (2007) Hurtado et al. (2011), Oliveira et al. (1996) Sousa-Pinto et al. (1999) Sousa-Pinto et al. (1999) Boulus et al. (2007), Durako and Dawes (1980) Cancino et al. (1987) Chopin et al. (1995) Friedlander et al. (1987) Mouradi-Givernaud et al. (1992), Roleda et al. (1997) Oliveira et al. (1996) McCandless et al. (1973) Schmid et al. (2014)

Ramus et al. (1976), Stengel and Dring (1998), Aguilera et al. (2002) Stengel and Dring (1998) L opez-Figueroa (1992) Henley et al. (1991), Rico and Fernandez (1996), Flores-Moya et al. (1995), Henley and Dunton (1995), Cousens (1982), Abreu et al. (2009)

(continued)

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TABLE 1. (continued) Compound/bioactivity

Phycobilins

Carotenoids

Influencer

Eutrophication (light, turbidity) Sampling season Sampling location Nutrient availability Light

Mycosporine-like amino acids Polyamines Phenolics

Phlorotannins

UV exposure UV exposure Nutrient availability UV exposure UV exposure Light climate Reproductive stage Grazing pressure Eutrophication (light, turbidity) Nutrient availability Grazing pressure Salinity Light climate

Antioxidant capacity

Sampling location Genotype Sampling season Grazing pressure

Grazing pressure Sampling location Thallus section

Antifouling capacity Agriculture extract NMR Profile

Salinity Grazing pressure Sampling season Commercial process

Reference

Rico and Fernandez (1996)

Pyropia yezoensis Pyropia sp.

Zhang et al. (2012) Carmona et al. (2006), Kim et al. (2007), Pedersen et al. (2012) Abreu et al. (2011a,b) Stengel and Dring (1998), Colombo-Pallotta et al. (2006) Stengel and Dring (1998), Colombo-Pallotta et al. (2006) Karsten et al. (1999) Korbee et al. (2005) Figueroa et al. (2008) Schweikert et al. (2014) Swanson and Fox (2007) Connan et al. (2004) Ragan and Jensen (1978), Swanson and Fox (2007) Abdala-Diaz et al. (2006) Koivikko et al. (2005)

Gracilaria vermiculophylla A. nodosum Macrocystis pyrifera A. nodosum Macrocystis sp. Devaleraea ramentacea Pyropia leucosticta Asparagopsis armata Pyropia cinnamomea Laminariales Fucoids Fucoids C. tamariscifolia F. vesiculosus A. nodosum F. vesiculosus A. nodosum F. vesiculosus S. latissima Nereocystis luetkeana Sargassum muticum F. vesiculosus Caulerpa racemosa Codium capitatum Halimeda cuneata Ulva fasciata Amphiroa bowerbankii Amphiroa ephedraea Dictyota humifusa Caulerpa taxifolia S. muticum Laminaria sp. A. nodosum S. muticum Gracilia sp. S. vulgare A. nodosum

management of biomass can be implemented to avoid unfavorable conditions, or where annual life cycle development can be avoided or shortened. Even though variation due to genetic heterogeneity can be reduced using particular strains or clones, most macroalgae exhibit considerable physiological plasticity and thus result in spatial (e.g., within the water column) and temporal fluctuations in biochemical content. A future industry based on the production of high value products from cultivated seaweed biomass will face the challenge of delivering these products in a standardized manner. In-sea cultivation management for quality. Studies of different commercial or pre-commercial scale cultivation conditions have predominantly concentrated on Gracilaria and Gelidium and different strains of

Pavia and Toth (2000) Connan and Stengel (2011) Swanson and Fox (2007) Tanniou et al. (2013) Honkanen and Jormalainen (2005) Stirk et al. (2007)

Box et al. (2008) Tanniou et al. (2013) Connan et al. (2006) Kumar et al. (2011) Plouguern e et al. (2010) Craigie et al. (2008)

C. crispus (Chopin et al. 1995, Zertuche-Gonzalez et al. 2001, Boulus et al. 2007, Friedlander 2008a, Xu et al. 2009). Seasonal and spatial variation in relation to natural environmental fluctuations have significant impacts on biomass production but only a few studies have assessed the product quality, mainly focusing on phycocolloid quality (FreilePelegrın and Robledo 1997, Sousa-Pinto et al. 1999). Few in-sea locations can provide conditions that allow for predictable chemical composition seasonally; however, several laboratory or pilot-scale studies have highlighted the potential of adjusting cultivation methods to optimize agar or carrageenan content, for example (Bird et al. 1981, Martinez and Buschmann 1996, Boulus et al. 2007, Friedlander 2008a).

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Thallus section

Seaweed

G. latifolium

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Limited manipulation of macronutrients can be achieved by suitable site selection or seasonal growth under naturally fluctuating nutrient conditions (Martınez and Rico 2008) but the effectiveness of this management is also impacted by light and temperature. Macroalgal cultivation at elevated nutrient levels can encourage epiphyte growth. This has resulted in targeted research on epiphyte control under otherwise favorable growth conditions for the desired species (L€ uning and Pang 2003). For example, nutrient application to Gracilaria was most effective when added in pulses to avoid wasteful application and limit competitors’ growth (Hanisak 1990). Alternatively, sites can be chosen for nutrient inputs (such as near fish farms) or water motion that have positive effects on bioactivity. However, insea cultivation does not permit fine levels of control, and producers use data averaging to coordinate harvesting with bioactive peaks. Natural light environments can be modified to a limited extent by regulating seaweed biomass density, cultivation rope design and the depth along ropes or within cages (Thirumaran and Anantharaman 2009). Some control over desiccation and irradiance can be achieved by creative methods of anchoring nets and lines at various depths or by exposing them to air (http://www.seaweed.i.e/aquaculture/noricultivation.php). The potential for changes in biochemical composition of the target species through the use of grazers to control epiphytes (e.g., Shacklock and Doyle 1983, L€ uning and Pang 2003) has not fully been assessed even though epi-fauna can alter agar quality of in natural populations of Gracilaria (Cancino et al. 1987). Altered bioactive profiles can result from changes in anti-grazing defenses (e.g., polyphenol levels) as modulated by grazing intensity, and increased antioxidant capacity has been reported in response to infection (e.g., Caulerpa taxifolia; Box et al. 2008). Several reports on the molecular genetic diversity of commercial genera such Pyropia, Kappaphycus and Eucheuma, highlight the fact that selection based on morphology and product quality can be supplemented by molecular techniques (Park et al. 2008, Abe et al. 2010, Chan et al. 2012a). The documented genetic diversity of wild and cultivated strains or ecotypes available for aquaculture (Zuccarello et al. 2007) is currently not being fully exploited (Halling et al. 2013). Summary. Because bioactivity is intrinsically linked to chemical composition, it is reasonable to assume that bioactivity of cultivated algae will vary according to location, depth, and season (Kim et al. 2014), but few have investigated the standardization of bioactivity with cultivated biomass as commodity production is the main objective in most cases. Achieving consistent bioactive profiles in cultivated seaweed biomass is thus a major challenge to future producers wishing to enter the higher value markets. The production of seaweeds for these high

value food and health applications may be best accomplished with newer cultivation technologies such as on-land tank cultivation systems (Friedlander 2008b, Hafting et al. 2012). FUTURE SEAWEED CULTIVATION FOR HIGH VALUE PRODUCTS

Cultivar optimization. Cultivars currently developed for maximal biomass production are those upon which natural product researchers base their work. The higher value markets for seaweeds will demand high and consistent yields of bioactive compounds. This is a fundamental challenge that must be addressed before success can be achieved in this sector. An overall improvement of genetic stocks will benefit both commodity (e.g., greater productivity, better disease resistance) and high-value markets (e.g., optimized bioactive content). An example of how little has been performed to improve available strains is Pyropia haitanensis cultivated extensively in China. The cultivar used has been in production for close to 50 years and accounted for over 75% of China’s seaweed production in 1996. No efforts to selectively improve the cultivar had been initiated until the 1980s. Inbreeding among other factors led to decreased yield and quality in recent years. Hybridization using naturally occurring color mutants resulted in the development of high-temperature tolerant cultivars. Such simple techniques improved temperature tolerance of germlings by up to 5°C over the wild-type, thus allowing the new strains to grow well during periods when the wild-type plants were deteriorating on the nets (Yan et al. 2009). Hybridization has also been used with Saccharina japonica, where growth rates of strains have been improved and, interestingly, the iodine content of some improved strains can be 20%–58% higher than that of the parent plants (Wu and Guangheng 1987). Traditional selection techniques have been very successful in maximizing tonnage and profits from cultivated seaweeds (e.g., Pyropia spp.; Saito 1976). Non-native species have also been selected for tolerance of local conditions, resulting in the establishment of seaweed cultivation industries where none previously existed (e.g., Philippines and Indonesia; FAO 2013). Some of these non-native introductions have been successful in areas where local macroalgal flora was sparse and was not utilized by local populations before the introduction of seaweed cultivation. Other introductions have been more negative in their impacts on local flora and fauna (e.g., Undaria pinnatifida; Williams and Smith 2007). The gains in productivity due to the use of traditional strain-selection methods have been impressive. However, there is a requirement for continuous improvement of biomass yield, disease resistance, and development of new regions for expanded seaweed cultivation worldwide.


Phycopathology research began more than two decades ago through ecological surveys that were able to identify the induced antiherbivore behavior of some species (Amsler 2001, Amsler and Fairhead 2006, Toth and Pavia 2007, Weinberger 2007). These pioneering studies have helped to provide a better understanding of how induced defense mechanisms in macroalgae work and how they could be applied to microscopic pathogens such as bacteria (mostly from the genera Vibrio, Alteromonas, Pseudoalteromonas, Cytophaga and Flavobacterium) and other microbes (viruses, fungi and other eukaryotes; Largo 2002, Gachon et al. 2010, Fernandes 2011). Microbes can grow at high densities as the aquatic environment is ideal for the development of biofilms where macroalgae, being part of the sessile benthic community, serve as hosts (Weinberger et al. 1999, Engel et al. 2002, Weinberger 2007, Fernandes 2011). A number of microbes are known to endow their hosts, not exclusively algae, with beneficial functions such as protection from other organisms and nutrient inputs (Matsuo et al. 2005, Zheng et al. 2005, Weinberger 2007) suggesting some level of coevolution (Hollants et al. 2013). However, it is known that other microorganisms can cause numerous diseases some of which result in major outbreaks in macroalgae crops worldwide (Correa 1996, Largo 2002, Gachon et al. 2010). Bacteria, endophytes and fungi have been identified in northeastern U.S.A. as potentially problematic for in-sea culture (Getchis 2014). Many recent reports describe disease outbreaks in the Philippines, Malaysia, Zanzibar (Kappaphycus alvarezii, Eucheuma denticulatum) and in Japan, China and South Korea. The latter are related to noneucheumatoid algae, especially those cultivated for direct human consumption (e.g., Pyropia spp., Gracilaria spp. and Saccharina spp.). Current reports indicate the damaging impact these diseases have had and can be expected to have in the seaweed industry and for communities that derive their main source of income from macroalgae farms (Table 2). The potential for crop damage points to the need to develop disease resistant seaweed cultivars, and the emerging field of phycopathology will help to inform their development. On-land seaweed cultivation. On-land cultivation was pioneered in the 1970s–1980s with the first attempts to produce C. crispus for carrageenan extraction (Craigie and Shacklock 1995). It is a highly technical method for intensive production of seaweed biomass, and it offers the highest level of control over the interaction of environmental conditions and genetic potential for seaweed bioactive production (Friedlander 2008b, Hafting et al. 2012). It also has the advantage of offering the possibility for real-time adjustments of these interactions as the growing season progresses. On-land cultivation systems use unattached, freely suspended

REVIEW

Traditional plant crossing techniques are especially effective when bioactive production is regulated by multiple gene interactions and when the genetic regulation of a particular bioactive is not known. The general lack of information on the genetic regulation of bioactive compound production in seaweeds has limited the ability to enhance their bioactive components through genetic transformation although this is an attractive concept (Chen et al. 2014, Charrier et al. 2015). The seaweed industry has so far avoided negative public opinion directed toward genetically modified foods from corn to fish, although consumer pressure is building and regulatory bodies are beginning to legislate guidelines for the labeling of GMO products (http://www.inspection.gc.ca/food/labelling/foodlabelling-for-industry/method-of-production-claims/gefactsheet/eng/1333373177199/1333373638071). Most likely GMO seaweeds will be developed for enhanced disease resistance or bioactive production, but this technology is a double edged sword. Macroalgal genes responsible for bioactive compound production, once identified, could potentially be transferred to bacterial or fungal hosts, bypassing the necessity for seaweed production. Little has been performed to improve existing cultivars through selective breeding (as is carried out in conventional agriculture and aquaculture at higher trophic levels). Exceptions exist (e.g., Saccharina in China; Zhang et al. 2007 and Pyropia in Japan; Halling et al. 2013), but much could be performed using traditional selective breeding methods to improve commodity yields, and to produce highly bioactive seaweeds (Robinson et al. 2013). New genomics information will inform the development of improved genetic stock and advances in transcriptomics will be central to the development of new optimized cultivars (Gantt et al. 2010, Chan et al. 2012a,b, Stiller et al. 2012, Coll en et al. 2014). Such work is time consuming and costly, so clearly identified marketing opportunities will have to be identified before this effort is enthusiastically championed by industry (the classic “chicken and egg” scenario); it remains as a critical hurdle to be overcome if the nascent seaweed bioactive industry is to mature. Phycopathology. The study of disease as it pertains to marine algae (i.e., phycopathology) has grown in importance in recent years (Andrews 1976, Steinberg and Denys 2002, Weinberger 2007, Harley et al. 2012). Seaweed cultures have a natural tendency to display similar disease symptoms regardless of where or how far they are located from each other. This is mainly due to the fact that cultivars come from a restricted genetic background and farms tend to be located in areas having similar environmental conditions that provide the basic necessities for the species according to its physiology (e.g., water temperature, salinity, irradiance; Largo 2002, Gachon et al. 2010).

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TABLE 2. Most common macroalgal diseases and their pathogens. Species

Disease syndrome

Pathogen

Reference

Saccharina japonica

Hole-rotten disease; Red Spot disease; Green Decay disease and malformation diseases

Uchida and Nakayama (1993), Jingying et al. (1997), Sawabe et al. (1998, 2000), Wang et al. (2004), Fernandes (2011)

Pyropia leucosticta

Kappaphycus sp. and Eucheuma sp.

Suminori disease; White Rot disease Anaaki; Green Spot rotting disease Rotten thallus syndrome (Gracilaria verrucosa); White Tips disease (G. chilensis) Ice disease, Goose Bumps disease

Vibrio (Vibrio logei), Halomonas sp., Pseudoalteromonas (Ps. bacteriolytica and Ps. elyakovii) Flavobacterium sp.; Vibrio sp. Vibrio sp.; Pseudomonas sp. Most likely - Vibrio sp.

Chondrus crispus

Green Rot disease

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Pyropia yezoensis Gracilaria sp.

CytophagaFlavobacterium group Still unknown

seaweeds, increasing the production of biomass per unit area and are highly efficient in their use of available space. Again, site selection and harvest timing is critical, but within these limitations much finer control is achievable. On-land sites can be chosen near deep water, where pipeline intakes can be installed to supply cold deep water which then can be combined with warmer surface water to regulate temperature regardless of season (e.g., Hawaiian Ocean Science and Technology Park in Kailua Kona Hawaii). Salinity can also be controlled by blending fresh/seawater ratios within on-land tanks. Light can be controlled, either by shading tanks, or by manipulation of tank depth and plant density (i.e., light exposure is a function of the ambient surface irradiance and the degree of light penetration to the biomass present). Light quality also can be manipulated artificially by the use of greenhouse coverings and light sources (LED/HID lights available with various spectral outputs). Photoperiod can be manipulated if necessary as is carried out with the cultivation of Pyropia conchocelis in greenhouses. Nutrient inputs can be finely adjusted to coordinate with real-time seaweed tissue levels of the bioactive compounds of interest and can be adjusted to maximize bioactive production while minimizing discharge, deleterious to the environment. Bacterial and microalgal growth is often described as either exponential or stationary but growth phase is a factor that receives little attention in the context of seaweed production. In certain cases bioactive compounds are not accumulated by microalgae until stationary phase (Fehling et al. 2004). The growth rate of individual cells therefore can profoundly affect bioactive accumulation. The same can be true in seaweeds. With land-based culture, stocking densities can be manipulated so that per area production levels can be maximized by either rapidly growing or slowly growing individuals. In

Tsukidate (1983), Kusuda et al. (1992), Kozo et al. (2009), Fernandes (2011) Tsukidate (1983), Fujita (1990), Sunairi et al. (1995), Fernandes (2011) Lavilla-Pitogo (1992), Weinberger et al. (1994), Correa and Flores (1995), Largo (2002) Largo et al. (1995, 1998), Vairappan (2006), Vairappan et al. (2009) Craigie and Correa (1996)

this way the physiological status of the seaweed can be manipulated. Control of pH and CO2 is readily achieved with on-land cultures and pH stress may be an effective tool for influencing real-time bioactivity content (Kim and Yarish 2014). Other chemical stresses have been implicated in bioactive content variability and some of these can ethically and cost effectively be applied during on-land cultivation (e.g., oxidants). Acadian Marine Plant Extract Powder (made from Ascophyllum nodosum) has been reported to enhance the phenolic content of Kappaphycus (Hurtado et al. 2012) and to enhance the natural pathogen defence mechanisms of Kappaphycus (Loureiro et al. 2012). Well-documented herbivory effects on phenolic compounds have been shown, but the importance of endophytes (e.g., fungal associations within A. nodosum) are less well known. Endophytes, epiphytes and the effects of herbivory all influence the chemical components of seaweeds, but their mechanisms of action are poorly understood (Jormalainen and Honkanen 2008). However, if a chemical signal can be used to simulate the effects of herbivory on seaweed bioactivity, this could be used with on-land techniques to maximize bioactivity in a cost-effective way. Microbial interactions (fungal algal, bacterial and viral) with their seaweed hosts although poorly understood at present may hold considerable promise for the future of seaweed cultivation. Specific microbes have profound effects on morphology as with the Ulva/Entermorpha complex (Hayden et al. 2003), but also may impact bioactivity. It is conceivable that future on-land tanks might be seeded with beneficial microbes (i.e., probiotic for cultivation) at some stage in the production cycle to enhance production of bioactive constituents. On-land cultivation techniques have specific challenges such as production and capital costs, with the availability of suitable coastal land being a significant limitation to development. However, if marketing efforts can establish a high value market


CONCLUSIONS

History shows both cultivar improvement and market development to be necessary components of a seaweed industry based upon the sale of efficacious products in the functional food, cosmeceutical, nutraceutical and pharmaceutical sectors. In the past, research progressed from an understanding of the basic biology, to the development of selected cultivars. In-sea techniques were developed from this knowledge base to produce commodity biomass to supply a large market with products including foods. Evolution of the seaweed industry into functional products will require the development of new markets and cultivars selected for efficacy. The partnership of industry and academia in this costly undertaking may be modeled on that developed during the burgeoning seaweed mariculture sector beginning in the 1950s. Intensive on-land systems will become more common so that the consistency and quality of the resulting biomass can be more closely controlled to provide enhanced return on the investments made to develop these new cultivars. The increased use of on-land systems could facilitate crop management to realize the full genetic potential of cultivars which, coupled with market development, will allow a new science-based, functional seaweed industry to flourish. Currently, the drive to develop efficacious seaweed products is

generally research-driven, but it will require marketpull to achieve the global successes of the past. The authors thank Drs. W. F. Farnham and M. Friedlander for their comments and editing before submission of the manuscript. AHB thanks the Basal Program of Conicyt (FB0001). The support of the Phycological Society of America in hosting the applied phycology meeting in Orlando is also acknowledged. CY thanks The Connecticut Sea Grant College Program (R/A-38; R/A-39). Abdala-Diaz, R. T. A., Cabello-Pasini, A., Perez-Rodrıguez, E., Conde Alvarez, R. M. & Figueroa, F. L. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar. Biol. 148:459–65. Abe, M., Kobayashi, M., Tamaki, M., Fujiyoshi, E. & Kikuchi, N. 2010. Rapid discrimination of Porphyra tenera Kjellman var. tamatsuensis Miura by PCR-RFLP. J. Appl. Phycol. 22:405–8. Aberg, P. & Pavia, H. 1997. Temporal and multiple scale spatial variation in juvenile and adult abundance of the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 158:111–9. Abreu, M. H., Pereira, R., Sousa-Pinto, I. & Yarish, C. 2011a. Nitrogen uptake response of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J. Exp. Mar. Biol. Ecol. 407:190–9. Abreu, M. H., Pereira, R., Sousa-Pinto, I. & Yarish, C. 2011b. Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro lagoon, Portugal. Eur. J. Phycol. 46:453–64. Abreu, M. H., Varela, D. A., Henrıquez, L., Villarroel, A., Yarish, C., Sousa-Pinto, I. & Buschmann, A. H. 2009. Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis. Aquaculture 293:211–20. Aguilera, J., Dummermuth, A., Karsten, U., Schriek, R. & Wiencke, C. 2002. Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biol. 25:432–41. Amsler, C. D. 2001. Induced defences in macroalgae: the herbivore makes a difference. J. Phycol. 37:353–6. Amsler, C. D. & Fairhead, V. A. 2006. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res. 43:1–91. Andrews, J. H. 1976. The pathology of marine algae. Biol. Rev. 51:211–53. B€ack, S., Collins, J. C. & Russell, G. 1992. Comparative ecophysiology of Baltic and Atlantic Fucus vesiculosus. Mar. Ecol. Prog. Ser. 84:71–82. Balboa, E. M., Conde, E., Soto, M. L., Perez-Armanda, L. & Domίnguez, H. 2015. Cosmetics from marine sources. In Kim, S. K. [Ed.] Handbook of Marine Biotechnology. Springer, Berlin Heidelberg, pp. 1015–42. Baurain, D., Brinkmann, H., Petersen, J., Rodrıguez-Ezpeleta, N., Stechmann, A., Demoulin, V., Roger, A. J., Burger, G., Lang, B. F. & Philippe, H. 2010. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 27:1698–709. Benemann, J. R. 2009. Microalgae Biofuels: A Brief Introduction. Available at: https://www.adelaide.edu.au/biogas/renewable/biofuels_introduction.pdf (accessed accessed February 28, 2014). Billot, C., Engel, C. R., Rousvoal, S., Kloareg, B. & Valero, M. 2003. Current patterns, habitat discontinuities and population genetic structure: the case of the kelp Laminaria digitata in the English Channel. Mar. Ecol. Prog. Ser. 253:111–21. Bird, K. T., Habig, C. & Debusk, T. 1982. Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). J. Phycol. 18:344–8. Bird, K. T., Hanisak, M. D. & Ryther, J. 1981. Chemical quality and production of agars extracted from Gracilaria tikvahiae grown in different nitrogen enrichment conditions. Bot. Mar. 24:441–4.

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share for functional seaweed-based products from highly bioactive cultivars, on-land cultivation will become more common as a viable production method. One only has to look at the success of microalgae producers such as Cyanotech, Earthrise, and others to see the future of seaweed cultivation. Open pond technology has allowed the industry to progress from the production of food (e.g., Spirulina), to nutraceuticals (astaxanthin production from Haematococcus). The revival of interest in cultivating microalgae with high lipid content as feedstock for biofuel production (Benemann 2009, SEI 2009) is an interesting example. The promise of algae-diesel remains unfulfilled, mainly due to high costs associated with these intensive (on-land, open raceway or closed bioreactor systems) systems, coupled with the low value of the commodity (fuel). For example, lipids from Nannochloropsis are valued within the cosmeceutical industry in purified form at US$ 260 per L compared to biofuel at US$1 per L with little refinement (Gellenbeck 2012). The recent trend of targeting higher value products (neutral-/pharmaceutical) rather than commodity production allows these intensive cultivation systems to become attractive income generators. Ultimately, the success and growth of land-based systems will depend on consumer demand for high value products. Without market pull for high value products, the economics for in-sea versus on-land cultivation benefits the former for most seaweed products.

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