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Hurtado, A.Q. 2022. Genetic resources for farmed seaweeds – Thematic background study. Rome. FAO. https://doi.org/10.4060/cb7903en

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Contents

Acknowledgements

Abbreviations and acronyms

Introduction

1. PRODUCTION, CULTIVATION TECHNIQUES AND UTILIZATION

1.1 Species and varieties

1.2 Farming systems

1.3 Major seaweed producing countries

1.4 Volume and value of farmed seaweeds

1.5 Utilization

1.6 Impact of climate change

1.7 Future prospects

2. GENETIC TECHNOLOGIES

2.1 Sporulation (tetraspores and carpospores)

2.2 Clonal propagation and varietal selection

2.3 Somatic embryogenesis

2.4 Micropropagation

2.5 Hybridization and crossbreeding

2.6 Genetic transformation

3. MAJOR PROBLEMS OF FARMING SEAWEEDS

3.1 Disease and epiphytism

3.2 Social and financial

4. IMPACT OF SEAWEED FARMING

4.1 Socio-economic impact

4.2 Ecological and environmental impact

5. DRIVERS OR MOTIVATIONS TO PURSUE OR EXPAND FARMING

5.1 Food

5.2 Feed (aquaculture)

5.3 Fuel

6. CONSERVATION AND SUSTAINABLE USE STRATEGIES

7. CAPACITY BUILDING

7.1 Education

7.2 Research and training

8. ROLE OF INTERNATIONAL AND REGIONAL ASSOCIATIONS IN THE DEVELOPMENT AND MANAGEMENT OF FARMED SEAWEEDS

9. SOURCES OF INFORMATION

9.1 Regional and international centres

9.2 Dissemination, networking and linkages

10. EXCHANGE PROGRAMMES

10.1 Information

10.2 Scientists and experts

10.3 Test plants

11. CONCLUSIONS

References

Tables

1. Summary of seaweeds currently farmed

2. English and local names of farmed seaweed

3. Summary of the different culture techniques and species farmed by country

4. Organisms suitable for IMTA in temperate waters

5. Sea-based IMTA practices in different countries

6. Land-based IMTA practices in different countries

7. Major seaweed producing countries

8. Major seaweeds farmed in Japan and the Republic of Korea

9. Summary of utilizations of farmed seaweeds

10. Earlier reports on the regeneration of plants from callus

11. Summary of protoplast isolation and regeneration of farmed seaweeds

12. Summary of seaweeds that were hybridize

13. Summary of farmed seaweeds that were genetically transformed

14. Summary of seaweed diseases and epiphytism

15. Conservation and sustainable strategies for farmed seaweeds

16. International, regional and local associations, organizations and societies engaged in seaweed research and other related activities

17. Some international algae centres

18. Various networks involved in seaweed farming and allied activities

Figures

1 Photos of commercially farmed red seaweeds

2 Photos of commercially farmed brown seaweeds

3 Photos of commercially farmed green seaweeds

4 Conceptual diagram of an IMTA operation

5. Seaweed carrageenan (Eucheuma spinosum) production, 2015 (tonnes, dry weight)

6. Gracilaria production by region, 2015 (tonnes, dry weight)

7. Gracilaria production by country, 2014 (tonnes, dry weight)

8. Gelidium production by region, 2015 (tonnes, dry weight)

9. Infection triangle

10. Pyramid schematic of seaweed product markets

11. Sustainability paradigm

Acknowledgements

The author is thankful to the following colleagues: Prof Yusho Aruga of Japan for providing data on seaweed production; Dr E.K. Hwang of the National Fisheries Research and Development Institute, Republic of Korea, for the latest seaweed production and photos of farmed seaweeds; and Dr Tong Pang of the Chinese Academy of Sciences Institute of Oceanology and Prof Show-Mei Lin for the information provided about the Chinese Phycological Society and the Taiwanese Phycological Society, respectively.

Abbreviations and acronyms

AmCFP humanized cyan fluorescent protein AMPEP

AMT aminomethyltransferase

AmCFP humanized cyan fluorescent protein AMPEP

ASP12-NTA synthetic medium with added vitamins

BA 6-benzyladenine

BAL Bio Architecture Lab

BAP 6-benzylaminopurine

BAPs Best Aquaculture Practices

CaMV 35S cauliflower mosaic virus 35S promoter CAT

CIMTAN Canadian Integrated Multi-Trophic Aquaculture Network

CaMV 35S cauliflower mosaic virus 35S promoter CAT

CIMTAN Canadian Integrated Multi-Trophic Aquaculture Network

CO2 carbon dioxide

DIN dissolved inorganic nutrients

EFA epiphytic filamentous algae

EGFP enhanced green fluorenscent protein

ESS Erd-Schreiber’s Seawater

ESS/2 Erd-Schreiber’s Seawater (half strength)

F_1 First generation

F_2 Second generation

FAO Food and Agriculture Organization of the United Nations

FCP fucoxanthin chlorophyll a/c-binding protein

GUS glucuronidase

HBsAg human hepatitis B surface antigen

IAA indole-3-acetic acid

IacZ bacterial beta-galactosidase

IBA indole-3-butyric acid

IFREMER L’Institut Français de Recherche Pour l’Exploitation de la Mer

IMTA integrated multi-trophic aquaculture

ISAV infectious salmon anaemia virus

mESCs mouse embryonic stem cells

N nitrogen

NAA 1-naphthaleneacetic acid

(NH4)2HPO4 diammonium phosphate

(NH4)NO_3 ammonium nitrate

NSE natural seaweed extract

NTNU Norwegian University of Science and Technology

OA ocean acidification

P phosphorous

PAA phenylacetic Acid

PES Provasoli’s enriched seawater

PGRs plant growth regulators

PI protoplast isolation

POM particulate organic matter

PR plant regeneration

PtHSP70 Porphyra tenera promoter

PyAct1 P. yezoensis actin 1 (promoter)

PyGAPDH P. yezoensis glyceraldehyde-3-phosphate dehydrogenase

PyGUS P. yezoensis glucuronidase

Rt-PA recombinant human tissue plasminogen activator

S65T Mutated threonine

SABs Seaweed Aquaculture Beds

SEA Southeast Asia

SES Seaweed Energy Solutions AS

sGFP superfolder green fluorescent protein

SINTEF Stiftelsen for industriell og teknisk forskning ved Norges tekniske høgskole

SSW sterile seawater

SV40 a promoter

SWM3 seawater enrichment

UBI ubiquitin (as gene promoter)

UprbcS Ulva pertusa ribulose-1,5-bisphosphate carboxylase/oxygenase (gene promoter)

VS 50 von Stosch’s (half strength)

ZsGFP humanized green fluorescent protein

ZsYFP humanized yellow fluorescent protein

Introduction

The increasing global population needs to source food from the ocean, which is a much greater area than the land. The ocean is rich with diversified flora and fauna, and both are sources of proteins, vitamins, minerals, phytohormones and bioactive compounds. Thousands of species of macroalgae (seaweed) dominate the vegetation of the sea floor from the intertidal to the subtidal zone.

The domestication of several economically important seaweed such as Saccharina, Undaria and Pyropia in China, Japan and the Republic of Korea, and Kappaphycus and Eucheuma in Indonesia, Malaysia, the Philippines and the United Republic of Tanzania led to intensive commercial cultivation of these seaweeds. Except for the United Republic of Tanzania, the commercial farming of seaweed, both temperate and tropical species, is centred in Asia. Despite the presence of several economically important seaweeds outside Asia, commercial farming is practised only in a few of non-Asian countries. These include Chile for Gracilaria and Macrocystis (Buschmann et al., 2001); France for Palmaria palmata, Porphyra umbilicalis and Undaria pinnatifida (Netalgae); and Canada for Saccharina latissima in integrated multi-trophic aquaculture (IMTA) (Chopin et al., 2013) and Chondrus crispus. Trial cultivation of Saccharina spp. and P. palmata is now taking place in Western Europe.

Seaweeds are farmed mainly for food as sea vegetables and food ingredients (Bixler and Porse, 2011), as well as feed (Wilke et al., 2015; Norambuena et al., 2015). However, there is increasing interest for their use for biorefinery products that require a vast amount of biomass which must be farmed.

The world is experiencing climate change, and several reports have shown that seaweeds are an efficient CO_2 sink. Seaweed aquaculture beds (SABs) provide ecosystem services similar to those seaweed beds existing in the wild. The use of SABs for potential CO2 mitigation has been established, with commercial seaweed production in China, India, Indonesia, Japan, Malaysia, the Philippines, the Republic of Korea, Thailand and Viet Nam, and it is also in the developmental stage in Australia and New Zealand (Chung and Lee, 2014). Seaweed farming is no doubt an aquaculture endeavour that can be socially and economically sustainable (= equitable); socially and environmentally sustainable (= bearable); and economically and environmentally sustainable (= viable) (Circular Ecology, 2016). Every stakeholder has an important role along the value chain to make it sustainable.

1. PRODUCTION, CULTIVATION TECHNIQUES AND UTILIZATION

For more than 100 years, China and other countries in Asia have grown seaweeds (also known as macroalgae) at a large industrial scale for the production of food, animal feed, pharmaceutical remedies and for cosmetic purposes. Commercial cultivation of seaweeds has a long history in Asia; in fact, the major source of cultivated seaweeds comes from this region. Despite being described as a low technology endeavour, it is highly successful and efficient. However, there is a newly emerging sector based on investment from petrochemical companies and governments for projects in Asia, Europe and the Americas aimed at extracting sugars from seaweed for ethanol, bio-based diesel, advanced biofuels, drop in fuels, biobutanol, biochemical and biopolymers.

Low technology cultivation can become highly advanced and mechanized, requiring on-land cultivation systems for seeding some life stages before grow-out at open-sea aquaculture sites. Cultivation and seedstock improvement techniques have been refined over the centuries, mostly in Asia, and can now be highly sophisticated. Advanced technologies and on-land cultivation systems have been developed in a few cases, mostly in the western world, wherein commercial viability can usually be reached only when high value-added products are obtained, their markets secured (not necessarily in response to a local demand, but often for export to Asia), and labour costs reduced to balance the significant technological investments and operational costs.

1.1 Species and varieties

Among the farmed seaweeds, Chondrus crispus, Eucheuma denticulatum, Kappaphycus alvarezii and K. striatus have different colour morphotypes, which range from brown, green, red, yellow and purple. Table 1 shows the different genera and species commercially farmed, which is composed of: 11 genera and over 25 species of red seaweeds with two varieties; 7 genera and 12 species of brown seaweeds; and 5 genera and 10 species of green seaweeds with one variety. Among the red seaweeds, Gracilaria has 11 species, followed by Pyropia with 5 species. In the brown seaweeds, Sargassum has 4 species while the green seaweeds are dominated by the genus Ulva, with 6 species (Figures 1–3). Figures 1, 2 and 3 provides pictures of some of the most important commercial species for the red, brown and green seaweeds respecitively.

English and local names of some farmed seaweeds are reported in Table 2.

1.2 Farming systems

1.2.1 Sea based farming

Sea-based farming may be classified according to location: coastal; deep sea; and offshore. Coastal and deep-sea farming are common in Asia, and to a little extent in Latin America and in the Western Indian Ocean regions. The fixed off-bottom line, the hanging longline, single and multiple raft longlines and spider-web techniques of cultivating Eucheuma and Kappaphycus and sometimes Gracilaria in the coastal and deep-sea waters are well documented (Hayashi et al., 2014; Hurtado et al., 2014; Msuya et al., 2014). Gracilaria and Macrocystis are also commercially farmed in Chile (Buschmann et al., 2001; Gutierrez et al., 2006). On the other hand, offshore farming is confined to Western Europe (Watson, 2014) and Eastern Canada (Chopin and Sawhney, 2009), mainly the monoculture of Saccharina and Undaria. Seaweed cultivation is currently in its infancy in Europe. Commercial aquaculture of seaweed is found in France (Brittany, six farms) and Spain (Galicia, two farms), and on an experimental basis in Ireland, Asturias (Spain), Norway, and the United Kingdom of Great Britain and Northern Ireland. The main cultivated species are Saccharina latissima and Undaria pinnatifida. In Ireland, Palmaria palmata farming is being experimented with on the West coast, but the results seem limited. However, with the fast development of IMTA as a culture system in Europe, farming of Alaria esculenta, P. palmata, S. latissima and Laminaria japonica is gaining much attention in this region (Chopin et al., 2001; Ridler et al., 2007).

China is known as the superpower in seaweed production and has decades of experience in seaweed cultivation, innovation and production. IMTA started in China about 2 000 years ago with a different system, called spontaneous integrated culture. Most of the culture systems in the country, however, are still single species intensive culture. China is well known in the field of marine aquaculture. More than 30 important aquaculture species, including kelp, scallops, oysters, abalone and sea cucumbers, are grown using various culture methods, such as longlines, cages, bottom sowing and enhancement, pools in the intertidal zone, and tidal flat culture (Zhang et al., 2007).

The concept of IMTA was coined in 2004 and refers to the use of species from different trophic positions or nutritional levels in the same system (Chopin and Robinson, 2004). IMTA, however, has been successfully practiced in Sanggou Bay in North China since the late 1980s (Fang et al., 1996). There are several IMTA modes in the bay, with benefits at the ecosystem level. For instance, the co-culture of abalone and kelp provides combined benefits as a food source and for waste reduction: abalone feed on kelp, and the kelp take up nutrients released from the abalone (Tang et al., 2013). The co-culture of finfish, bivalves and kelp links organisms from different trophic levels so that the algae absorb nutrients released from finfish and bivalves and bivalves feed on suspended faecal particles from the fish. Since kelp and Gracilaria lemaneiformis are cultured from December to May and from June to November, respectively, nutrients are absorbed by the algae throughout the year. These examples of multi-trophic culture maximize the utilization of space by aquaculture as they combine culture techniques in the pelagic and benthic zones. Implementation of IMTA in Sanggou Bay has improved economic benefits, maintained environmental quality, created new jobs, and led to culture technique innovations (Fang and Zhang, 2015).

Table 3 presents a summary of the different culture techniques of the different farmed seaweeds per country, all of which are in the commercial stage, with the exception of the land based IMTA in Portugal. Apparently, hanging longline is common both to red and brown seaweeds. Except for Caulerpa, Eucheuma, Gracilaria and Kappaphycus, the source of propagules for commercial farming comes from spores that are grown first in hatcheries and then planted out when reaching the juvenile stage during favourable sea temperatures. In contrast, the four genera above use vegetative cuttings as propagules for commercial farming.

One of the most discussed types of aquaculture in Western Europe, Eastern Canada and the United States of America is IMTA, which is the farming, in proximity, of several species at different trophic levels (Figure 4). The species selected should be well adapted to these conditions and be appropriately chosen at multiple trophic levels, based on their complementary functions in the ecosystem as well as for their existing, or potential, economic value. Proximity should be understood as not necessarily considering absolute distances, but connectivity in terms of ecosystemic functionalities in which management at the sea-area level is paramount.

IMTA is an ecologically engineered ecosystem management approach, which, in fact, does nothing more than mimic a simplified natural trophic network. IMTA creates a balanced system for increased environmental sustainability (ecosystem services and green technologies for improved ecosystem health); economic stability (product diversification, risk reduction and job creation in coastal communities); and societal acceptability (better management practices, improved regulatory governance, and appreciation of differentiated and safe products). IMTA programmes, in different states of development and configuration, are taking place in at least 40 countries (Barrington et al., 2009).

IMTA has gained recognition after 16 years of existence in the Western world and has slowly been developing in other regions. The most advanced IMTA systems, near commercial or at commercial scale, can be found in the temperate waters of Canada, Chile, China, Israel and South Africa, for example (Chopin et al., 2008; Barrington et al., 2009). Table 4 presents the genera selected based on their established husbandry practices, habitat appropriateness, biomitigation ability and economic life. Developments of IMTA projects have been started in France, Ireland, Japan, the Republic of Korea, Mexico, Norway, Portugal, Spain, Thailand, Turkey, the United Kingdom of Great Britain and Northern Ireland (mostly Scotland), and the United States of America (see Table 5 for sea-based practices and Table 6 for land-based practices) (Barrington et al., 2009). IMTA offers many advantages compared with the monoculture system (Barrington et al., 2009), such as:

i. Effluent biomitigation: the mitigation of effluents through the use of biofilters (e.g. seaweeds and invertebrates), which are suited to the ecological niche of the farm.

ii.Disease control: prevention or reduction of disease among farmed fish can be provided by certain seaweeds due to their antibacterial activity against fish pathogenic bacteria (Bansemir et al., 2006), or by shellfish that reduce the virulence of infectious salmon anaemia virus (Skar and Mortensen, 2007).

iii. Increased profits through diversification: increased overall economic value of an operation from the commercial by-products that are cultivated and sold.

iv. Increased profits through obtaining premium prices: potential for differentiation of the IMTA products through ecolabelling or organic certification programmes.

v. Improving local economy: economic growth through employment (both direct and indirect) and product processing and distribution.

vi.Form of “natural” crop insurance: product diversification may offer financial protection and decrease economic risks when price fluctuations occur, or if one of the crops is lost to disease or inclement weather.

Seaweed is a growing category in Europe, although it is far behind Asia, where marine plants are part of a longstanding traditional culinary culture.

In France, the largest producer of seaweed is Algolesko, which began harvesting seaweed in May 2014. Interestingly, two of its partners are oyster growers, which, apart from their obvious expertise in aquaculture, also demonstrates the complementary nature of seaweed culture with other types of aquaculture. Future aquaculture production will see more IMTA practices, which optimizes interaction between species while reducing environmental impact, leading to sustainable production systems that will supply healthy sustainable seafood for future generations. The potential of seaweed for bioenergy production and a strong interest in developing IMTA have given a new dimension to seaweed aquaculture.

1.2.2 Land-based farming

There are only a few successful commercial land-based tanks/raceways of seaweed farming that have been reported. These are: Chondrus crispus (three different colour morphotypes) in Canada as sea vegetables (direct source of human food) grown in raceways; Ulva pertusa, in Israel, grown in raceways using deep seawater from the Mediterranean Sea and used in diversified food preparations such as pasta, salads, drinks, and abalone feed (SEAKURA); Ulva pertusa in South Africa, grown in raceways as the primary food of abalone (Bolton et al., 2006; Robertson-Anderson et al., 2008), and SeaOr Marine Enterprise in Israel using fish (Sparus aurata), seaweeds (Ulva and Gracilaria) and molluscs (Haliotis discus hannai).

1.3 Major seaweed producing countries

Except for Chile, which farms Gracilaria and Macrocystis, and the United Republic of Tanzania, which cultivates Eucheuma, seaweed production is mainly concentrated in Asia (Table 7).

1.4 Volume and value of farmed seaweeds

As of 2016, recent production data on Saccharina, Undaria and Pyropia from China were not available. The author communicated with colleagues in academia and industry, but only Japan and the Republic of Korea responded to the request. Table 8 shows the volume of farmed seaweeds in Japan and the Republic of Korea.

Indonesia and the Philippines are the world’s two major producing countries of Kappaphycus alvarezii (cottonii) but while Indonesia continues to increase its production, in the Philippines it has decreased since 2009. The sudden increase of production in Indonesia since 2008 is mainly due to the opening of new cultivation areas, considering the presence of thousands of islands in the country. However, the country’s productivity is only 11 tonnes dry weight (dwt) ha-1 year-1. Despite the geographic location of the Philippines, which every year is exposed to several cyclones that often destroy farming structures and propagules, the country’s productivity is 18 tonnes dwt ha-1 year-1 (Porse and Rudolph, 2017). Malaysia, though it is within the Coral Triangle and has vast areas suitable for farming, is still facing challenges to increase its production. In 2014 and 2015, 26 076 tonnes and 24 533 tonnes of Kappaphycus, respectively, were produced (Suhaimi, personal communication).

Production of Kappaphycus in other Southeast Asian countries, such as Cambodia, China, India, Myanmar, Viet Nam, and in Latin America are still small at present and data are not available.

The shallow areas in the coastal zone of the United Republic of Tanzania and Zanzibar allow favourable cultivation of Eucheuma denticulatum; hence, these locations are major producing areas. Figure 5 shows the latest production of spinosum (common vernacular name of E. denticulatum) in the three major producing countries.

Gracilaria and Gelidium are two genera of seaweed suitable for the processing of agar, the former being more appropriate for food applications while the latter for bacteriological and biotechnological applications.

Gracilaria is a ubiquitous seaweed, which can be found both in tropic and temperate waters, while Gelidium is more confined to temperate waters. The capacity of Gracilaria to grow in euryhaline areas and to regenerate from fragments are characteristics that favour intensive cultivation from brackish-water to full seawater areas (Hurtado-Ponce et al., 1992; Hurtado-Ponce, 1993; Hurtado-Ponce et al., 1997).

Asia-Pacific is the largest producing region of Gracilaria, followed by the Americas (mainly Chile), and Africa and Europe (Figure 6). A more detailed graph is presented in Figure 7, which shows the countries that produce Gracilaria, with Indonesia being the major producer. Africa is the leader for the production of Gelidium (Figure 8).

1.5 Utilization

Farmed seaweeds have been mainly used as sources of direct food in Asia for many centuries; however, in the past two to three decades, western countries have started including seaweeds in their diet for health reasons. Several single species have various applications, as reflected in Table 9. A total of 59 species are currently farmed and dominated by red seaweed (54.3 percent), followed by brown seaweeds (23.7 percent), and finally green seaweeds (22 percent). Seaweeds are prime candidates for the integrated biorefinery approach, both for the production of high-value compounds (such as edible food, food and feed ingredients, biopolymers, fine and bulk chemicals, agrichemicals, cosmetics, bioactives, pharmaceuticals, nutraceuticals, botanicals) and low-value bioenergy compounds (e.g. biofuels, biodiesels, biogases, bioalcohols, biomaterials).

1.6 Impact of climate change

Seaweeds are a key source of carbon in the reef ecosystem, and they are involved in other important processes, including the construction of reef frameworks, coral settlements and creation of habitats. They are a direct food source for herbivorous fish, crabs and sea urchins. The carbon they fix in photosynthesis enters the food chain via microbes.

Seaweeds are subject to both regional and global environmental changes in coastal waters, where environmental factors fluctuate dramatically because of high biological production and land runoff. Ocean warming and ocean acidification (OA) caused by climate changes can influence coastal environments and consequently affect the physiology, life cycles and community structures of seaweeds. According to Ji et al. (2016), some species showed enhanced growth and/ or photosynthesis under elevated CO_2 levels or ocean acidification conditions, possibly due to increased availability of CO_2 in seawater with neglected influence of pH drop. Nevertheless, OA can harm some macroalgae because of their high sensitivity to the acidic perturbation to intracellular acid-base stability. Mild cean warming has been shown to benefit most macroalgae examined. OA may positively affect gametogenesis because of increased availability of CO_2 and may neutrally influence germination due to the counteractive effects of decreased pH (Roleda et al., 2012). OA can impact photosynthesis and respiration differently in some macroalgae. While it is important to look into responses of macroalgae to fluctuating pH under OA (common in coastal waters) (Cornwall et al., 2012), the impact of OA can affect productivity of sea-farmed macroalgae that experience dramatic diel pH variations. Altered chemistry under OA may reduce growth, photosynthesis and even lead to death of some macroalgal species (Israel and Hophy, 2002; Martin and Gattuso, 2009). Ultraviolet B, which penetrates only several metres in coastal waters, is harmful for macroalgae throughout their life cycles.

Sea level rise may create more available habitat space for macroalgae to grow as more land area will be inundated with water. In general, the macroalgae are not particularly vulnerable to the impact of sea level rise, even if in some cases the increase in sea level could negatively impact some species that live in shallow waters by reducing their exposure to sunlight (increased depth will mean more distance for sunlight to travel to reach the macroalgae).

The predicted increase in the frequency of severe weather events such as cyclones, storms and floods will bring an influx of nutrients into the reef ecosystem, which will increase macroalgae growth and reproduction. Cyclones and storms can also destroy coral reef structures, increasing habitat areas for macroalgae to grow.

The most notable impact of rising temperature and concomitant elevated salinity has been reported on farmed Kappaphycus. The high incidence of “ice-ice”, a disease affecting Kappaphycus and Eucheuma production, as well as epiphytic filamentous algae, were reported in Southeast Asia by Critchley et al. (2004), Hurtado and Critchley (2006), Vairappan (2006), Vairappan et al. (2008), Tisera and Naguit (2009), Borlongan et al. (2011); in China by Pang et al. (2011, 2012, 2015); and in Madagascar by Ateweberhan et al. (2015) and Tsiresy et al. (2016).

Low productivity and production and the unavailability of propagules for the next growing cycles were the major problems for seaweed farmers as a result of rising temperatures. Sometimes the seaweed farmers stopped cultivating Kappaphycus and, consequently, their economic life was severely affected. While there are possible positive effects of ocean warming for some warm seawater-grown species, the rise of temperature may still represent a threat for the cold seawater-grown species by reducing their living space and ecological niche.

1.7 Future prospects

Farmed seaweeds in the tropics and subtropics will continue to grow and expand, not only because of their economic significance among coastal fishers, but also because of the development of more product applications in food industries as well as in pharmaceuticals, nutraceuticals, cosmetics and personal care. The combination of increasing production, innovative products and consumer demand for natural and organic products will no doubt lead to bright days for seaweed in Europe and other parts of the globe.

In Western Europe, Northeastern Canada and the United States of America, the brown seaweed Alaria, Laminaria and Saccharina will experience a tremendous expansion in terms of sea cultivation, both as monocultures and as part of the IMTA, mainly for biorefineries. Further, sea vegetables like Chondrus crispus, Palmaria palmata, Pyropia yezoensis and Ulva pertusa will be cultivated extensively in land-based systems both as a monoculture and in IMTA.

IMTA will find its way in countries where intensive fish cage and pond shrimp farming are practised, as in Southeast Asia, India and South America. IMTA is considered more sustainable than the common monoculture systems, a system of aquaculture where only one species is cultured, in that fed monocultures tend to have an impact on their local environments due to their dependence of supplementation with an exogenous source of food and energy without mitigation (Chopin et al., 2001). For some twenty years now, many authors have shown that this exogenous source of energy (e.g. fish feed) can have a substantial impact on organic matter and nutrient loading in marine coastal areas (Gowen and Bradbury, 1987; Folke and Kautsky, 1989; Chopin et al., 1999; Cromey et al., 2002), affecting the sediments beneath the culture sites and producing variations in the nutrient composition of the water column (Chopin et al., 2001).

2. GENETIC TECHNOLOGIES

The global seaweed industry produced 23–24 million tonnes of wet seaweed from aquaculture in 2012 (FAO, 2014), as the demand for seaweed based-products exceeds the supply of seaweed raw material from natural stocks. Aquaculture of seaweed offers advantages over the harvest of natural stocks for the following reasons: stable supply and reliable access of raw material; uniformity of quality of the raw material; and selection of germplasm with desired traits. Seaweed cultivation must be technically feasible, environmentally friendly, economically equitable, and socially acceptable in order to be sustainable.

Traditional selection of varieties based on growth performance and resistance to “disease” is still used in propagating farmed species. The breakthrough in the hybridization of Laminaria japonica in China paved the way to massive cultivation of this species globally. In vitro cell culture techniques have also been employed, as these facilitate development and propagation of genotypes of commercial importance. There are more than 85 species of seaweeds for which tissue culture aspects have been reported.

Initially, the aim of these techniques focused mostly on genetic improvement and clonal propagation of seaweeds for mariculture; however, recently, the scope has been extended for use in bioprocess technology for the production of high-value chemicals of great importance in pharmaceuticals and nutraceuticals, and more recently, in biorefinery.

2.1 Sporulation (tetraspores and carpospores)

All brown seaweeds commercially cultivated (Hizikia, Macrocystis, Saccharina and Undaria) use strings for the attachment of zoospores in hatcheries during summertime until they reach 1 mm long, and then they are out planted into the sea in autumn. When these stocks attain a size of more than 1 m long, they are ready to be harvested. The growth stage from the land-based hatchery to grow-out is nine to ten months.

A number of reports have been conducted on the trial use of spores from Gracilaria for possible commercial cultivation, but as of 2016 no one has adopted the use of spores for commercial propagation. Likewise, the use of carposporelings from Kappaphycus alvarezii as possible propagules for field cultivation (Azanza and Aliaza, 1999; Azanza-Corrales, Aliaza and Montano, 1996; Azanza and Ask, 2003) did not gain much success compared with the carposporelings from K. striatus, which were field cultivated in Guimaras Island, the Philippines (Luhan and Sollesta, 2010). Further, the use of tetrasporelings from K. alvarezii (de Paula, 1999; Bulboa et al., 2007) also did not gain much attention among the seaweed farmers for use in commercial cultivation compared with other species, such as Laminaria digitata, Palmaria palmata, Pyropia yezoensis, Saccharina latissima and Undaria pinnatifida. This is probably due to the low germination rate under laboratory/hatchery conditions for mass field cultivation. Hatchery production of the conchocelis and/or spores for out planting purposes is already well developed in China, Japan and the Republic of Korea and is still practised today.

2.2 Clonal propagation and varietal selection

Clonal propagation is the most common and simplest approach to select superior varieties from wild populations to improve the performance of cultivated crops (Santelices, 1992), as done for Chondrus (Cheney et al., 1981), Gigartina (Sylvester and Waaland, 1983), Gracilaria (Patwary and van der Meer, 1982, 1983), and Kappaphycus (Doty and Alvarez, 1973), all cases where it was exploited the organogenetic potential of seaweeds in isolating superior clones for cultivation. Clonal propagation of Chondrus crispus in raceways in Canada is the only known successful cultivation of this red seaweed. Its commercial cultivation has been perfected after more than ten years of trial cultivation.

2.3 Somatic embryogenesis

Somatic embryogenesis is an asexual form of plant propagation that mimics many of the events of sexual reproduction. This process may be reproduced artificially by the manipulation of tissues and cells in vitro. Some of the most important factors for a successful plant regeneration are the culture medium and the environmental incubation conditions. In vitro somatic embryogenesis is an important prerequisite for the use of many biotechnological tools for genetic improvement as well as for mass propagation.

Whole plants are regenerated from culture via two different processes: somatic embryogenesis, in which cells and tissues develop into a bipolar structure containing both root and shoot axes with a closed vascular system (essentially, the type of embryogenesis that occurs in a seed); and organogenesis, in which cells and tissues develop into a unipolar structure, namely a shoot or a root with the vascular system of this structure often connected to parent tissues.

2.4 Micropropagation

2.4.1 Tissue and callus culture

Tissue culture is the science of maintaining cells and/or tissues in vitro in a sterile environment that regulates specific growth and development patterns. Culture conditions requiring control include: physical conditions (controlled with an environmental chamber or walk-in culture room), light, temperature, photoperiod and aeration; and chemical conditions (controlled by the culture media), all essential nutrients, minerals, pH and quality of water. Culture media is either solid (agar) or liquid. Plant growth regulators (PGRs) are essential to induce developmental changes in cells to create specific tissues. There are five classes of PGR, namely: auxins, promoting both cell division and cell growth; cytokinins, promoting cell division; gibberellins, for cell division; abscisic acid, inhibiting cell division; and ethylene, controling fruit ripening.

Plants can be regenerated in tissue culture either from tissue explants or from isolated cells. When plant cells and tissues are cultured in vitro, in most cases they exhibit a very wide range of plasticity. Regeneration of the whole plant from any single cell depends on the concept that each cell, if given the appropriate stimuli, has the genetic potential to divide and differentiate into all types of tissues. This genetic potential by plant cells is referred to as totipotency. Several species of red, brown and green macroalgae have been reported to regenerate from callus, as shown in Table 10. Although several successful studies were reported on the regeneration of plantlets of Kappaphycus and Eucheuma from callus through micropropagation using different culture media, their economic viability in the field has yet to be tested further, though initial trials have been started.

2.4.2 Protoplast isolation and fusion

Protoplasts are living plant cells without cell walls that offer a unique uniform single cell system that facilitates several aspects of modern biotechnology, including genetic transformation and metabolic engineering. Protoplasts isolation from macrophytic benthic marine algae was reported as early as 1970 using mechanical methods (Tatewaki and Nagata, 1970; Enomoto and Hirose, 1972; Kobayashi, 1975). However, the success in producing a large number of viable protoplasts became possible only after the development of an enzymatic method by Millner et al. (1979) for Enteromorpha intestinalis (Linnaeus) Nees. Plantlet regeneration from the same species was reported by Rusing and Cosson (2001).

Only a few species among the farmed seaweeds were tested for protoplast isolation and its possible regeneration to plantlets. Among the brown seaweeds, only Laminaria japonica (Saga and Sakai, 1984; Tokuda and Kawashima, 1988; Sawabe et al., 1993; Sawabe and Ezura, 1996; Inoue et al., 2008); L. saccharina and L. digitata (Butler et al., 1989); Macrocystis pyrifera (Kloareg et al., 1989); and Undaria pinnatifida (Tokuda and Kawashima, 1988) were reported. Only the works of Kloareg et al. (1989) on Macrocystis pyrifera and Matsumura et al. (2000) on L. japonica were successful in the regeneration of plantlets from protoplasts.

Early protoplast isolations from Kappaphycus alvarezii were made with the purpose of improving the genetic characteristics of this species as a source of propagules for possible commercial cultivation (Zablackis, et al., 1993). Digestions with cellulase and kappa-carrageenase produced only a few cortical cell protoplasts, while digestions with cellulase and iota-carrageenase only produced epidermal cell protoplasts. When both carrageenases were used in the digestion media with cellulase, protoplasts were released from all cell types and yields ranged from 1.0 to 1.2 × 10^7 cells g-1 with sizes from 5 to 200 mm diameter. Protoplasts were subsequently cultured to study cell wall regeneration; however, no regeneration of plantlets was observed.

Attempts to isolate protoplast from tissue fragments (<1 mm2) of three Philippine cultivars of Kappaphycus alvarezii, namely the giant cultivar, the cultivar L and the Bohol wild type, by enzymatic dissolution of cell walls was reported by Salvador and Serrano (2005). The yields of viable protoplasts from young and old thalli (apical, middle, basal segments) were compared at various temperatures, duration of treatment and pH using eight combinations of commercial enzymes (abalone acetone powder and cellulase), and prepared extracts from fresh viscera of abalone (Haliotis asinina) and a terrestrial garden snail. Though viable protoplasts formed radially expanded discs and filaments arising from the disc, no regeneration to a plantlet was reported. Table 11 shows a summary of earlier reports on protoplast isolation and regeneration. As of 2016, protoplast isolation and regeneration are not being used commercially and all applications remain in the research and development phase.

2.5 Hybridization and crossbreeding

Among the commercial farmed seaweeds, only a few brown and red seaweed species were subjected to hybridization and crossbreeding.

For example, S. japonica in China was bred by crossing gametophytes and self-crossing the best individuals and selecting the best self-crossing line (Li et al., 2016). Its sporophytes were reconstructed each year from representative gametophyte clones, from which seedlings were raised for farming. As stated by the Authors, “such strategy ensured Dongfang No. 7 against a variety of contamination due to cross-fertilization, and occasional mixing and inbred depletion due to self-crossing number-limited sporophytes matured year after year”. Dongfang No. 7 is derived from a crossbreeding of different lines of S. japonica through four rounds of self-crossing and selection and retains a certain degree of genetic heterozygosity, and thus it is relatively immune to inbreeding depression caused by the reduction of genetic variability. The farming of Dongfang No. 7 increased the air-dry yield by 43.2 percent over two widely farmed controls on average. This value was however less than the value obtained with the interspecific hybrids or the varieties derived from them.

The successful work of Hwang et al. (2014) on the hybridization of female U. pinnatifida and male U. peterseniana led to the extended period of availability of Undaria for abalone feed and cultivation in the Republic of Korea. Using free-living gametophyte seeding and standard on-growing techniques, the second generation (F_2) hybrids were found to have longer pinnate blades and narrower midribs than the first generation (F_1) hybrid and formed only sporophylls. The growth and morphology of F_2 hybrids originating from the sporophyll or sorus of the F_1 hybrids were not morphologically different from each other. Both of the F_2 hybrids exhibited late maturation, with the early stages of sporophylls appearing in April.

An attempt to hybridize Kappaphycus alvarezii and Eucheuma denticulatum was successful, as reported by Wang (1993), using a somatic cell-fusion method to produce hybrids of non-filamentous or anatomically complex algae as evidenced by isoenzyme electrophoresis. However, this was not pursued further for its mass production for possible commercial cultivation (Table 12).

2.6 Genetic transformation

Genetic transformation occurs at the cellular level and can be used to introduce trait altering genes into the host genome. Cells must be regenerated into plants to recover the transgenic plant. Genetic transformation is a powerful tool not only for elucidating the functions and regulatory mechanisms of genes involved in various physiological events, but also for establishing organisms that efficiently produce biofuels and medically functional materials, or that carry stress tolerance under uncertain environmental conditions (Torney et al., 2007; Bhatnagar-Mathur et al., 2008). As of 2016 no genetically transformed seaweeds are being sold or used commercially for food, biofuel or any other applications; this technology is only used for research and development purposes.

Donald P. Cheney is the pioneer in researching red algal transformation. He and his colleague performed transient transformation of the red alga Kappaphycus alvarezii using particle bombardment, which was the first report about the transient transformation of seaweeds (Kurtzman and Cheney, 1991). Since then, there have been recent developments in macroalgal transformation. The report of Wang et al. (2010a) showed a viable way of producing stable transformants to eliminate chimeric expression, and to achieve transgenic breeding in K. alvarezii using SV40 promoter-driving lacZ gene into cells of K. alvarezii through particle bombardment of epidermal and medullary cells at 650 psi (pounds per square inch) at a distance of 6 cm. In another report, a transgenic K. alvarezii was successfully produced when a binary vector pMSH1-Lys carrying a chicken lysozyme (Lys) gene was transformed into Agrobacterium tumefaciens LBA4404 by triparental mating (Handayani et al., 2014). The percentage of pMSH1-Lys transformation on K. alvarezii was 23.5 percent, while the efficiency of regeneration was 11.3 percent. PCR analysis showed that three of the regenerated thalli contained the lysozyme gene, which has the ability to break down the bacterial cell wall, a significant result in the prevention of “ice-ice” disease in K. alvarezii.

Among the red industrially important macroalgae such as Chondrus, Gelidium, Kappaphycus and Pyropia, the transient gene expression system has not yet been developed in these red macroalgae other than P. yezoensis. Optimization of codon usage in coding regions of the reporter gene and recruitment of endogenous strong promoters (pPyAct1-PyGUS and pPyAct1-GUS plasmids) are important factors in the transient gene expression system. Furthermore, the use of particle bombardment is the proven method of gene transfer into red algal cells (Mikami et al., 2011) (Table 13).

According to Mikami (2013), genetic transformation is reported in red and brown seaweeds using the SV40 promoter; however, isolation of transgenic clone lines produced from distinct single transformed cells, which is the final goal of the genetic transformation of seaweeds as a tool, has not been reported, and seaweed genetic transformation is thus not fully developed. Due to the problems with efficient genetic transformation systems, the molecular biological studies of seaweeds are currently progressing more slowly than are the studies of land green plants. Since a genetic transformation system allows the performance of genetic analysis of gene function via inactivation and knock-down of gene expression by RNAi and antisense RNA suppression, its establishment will enhance both biological understanding and genetical engineering for the sustainable production of seaweeds and also for the use of seaweeds as bioreactors.

Though in vitro culture techniques as described above are currently being developed for seaweeds, which can create new genetic variants or promote clonal propagation in photobioreactors for high-end applications, most commercial seaweed cultivation, especially in the subtropical to tropical waters, is currently based on simple vegetative propagation because of economic and farming advantages.

3. MAJOR PROBLEMS OF FARMING SEAWEEDS

3.1 Disease and epiphytism

When a seaweed is suffering, we call it diseased. A seaweed is diseased when it is continuously disturbed by some causal agents that results in an abnormal physiological process that it disrupts its normal structure, growth, function or other activities. The concepts of disease are the following (Singh, 2007): the normal physiological functions of seaweed are disturbed when they are affected by pathogenic living organisms and/or by some environmental factors; initially, seaweed reacts to the disease causing agents, particularly in the site of infection; later, the reaction becomes more widespread and histological changes take place; such changes are expressed as different types of symptoms of the disease which can be visualized macroscopically; and as a result of the disease, seaweed growth is reduced, deformed or even dies.

Disease occurrence is generally driven by the interactions of three factors (Agrios, 2005; Garret et al., 2009): a susceptible host population; the presence of a competent endophyte/malaise; and a conducive (biotic and abiotic) environment (Figure 9).

Despite the advances in seaweed farming, disease occurs, especially in areas where stocking is intensive. Table 14 shows a summary of seaweed diseases caused by bacteria, fungi and epiphytes.

3.2 Social and financial

Issues on social problems pertinent to seaweed farming stem from the unacceptability by the community to the introduction of a novel farming system. This is brought on mainly if such farming system affects the immediate environment.

One of the biggest problems of seaweed carrageenan farming is the accessibility to financial assistance, especially in areas where cyclones or typhoons occur, such as the Philippines. Normally, farming structures and propagules are destroyed when the typhoon signal is No. 2 or higher. The capacity to rehabilitate is a major problem. The need to have crop insurance in seaweed aquaculture activity is important so that in times of calamities seaweed farmers can claim a certain amount of the lost crop and structures to restart farming.

4. IMPACT OF SEAWEED FARMING

4.1 Socio-economic impact

The comprehensive report of Valderamma et al. (2013), which includes six case studies of carrageenan seaweed farming in six different countries (India, Indonesia, Mexico, the Philippines, Solomon Islands and the United Republic of Tanzania), attests to the economic benefits of Kappaphycus farming in the tropics and subtropics. In the temperate countries, reports include an economic analysis of Laminaria digitata farming in Ireland by Edwards and Watson (2011); a cost analysis for ethanol produced from farmed seaweeds by Philippsen et al. (2014); a new bioeconomy for Norway by SINTEF (2014); and economic feasibility of offshore seaweed production in the North Sea by Van den Burg et al. (2013). All these reports clearly show that seaweed farming is economically beneficial to farmers in particular and the local and national economy in general.

4.2 Ecological and environmental impact

Seaweed farming is an extractive aquaculture whose process of production of valuable biomass renders various ecosystem services with ecological and economic values (Chopin et al., 2008, 2010; Neori et al., 2007; Radulovich et al., 2015). Seaweed farming adds oxygen during photosynthesis and cleans seawater from excess nutrients (nitrogen, phosphorus and others). Nutrient extraction, or uptake, cleans water effectively and thoroughly through a process known as bioremediation (Forster, 2008). Seaweed farming enhances biodiversity and fisheries (Radulovich et al., 2015). Seaweeds are carbon sinks that can reduce ocean acidification through uptake of CO_2 from water.

Among the red seaweeds being farmed, Kappaphycus is drawing much attention in places where it is being introduced. The literature shows that this seaweed is endemic in the tropics such as Indonesia, Malaysia and the Philippines; its first successful commercial farming was reported in the Philippines in the early 1970s (Doty, 1973; Parker, 1974; Doty and Alvarez, 1981). Since then, it has been introduced in almost 30 countries worldwide. Such introduction without prior scientific and quarantine protocols and proper management led to some negative impacts in Hawaii, United States of America (Rodgers and Cox, 1999; Smith et al., 2002; Conklin & Smith, 2005), and in India (Chandrasekaran et al., 2008), where the plant became invasive.

5. DRIVERS OR MOTIVATIONS TO PURSUE OR EXPAND FARMING

The expansion or increase in seaweed farming in terms of production is mainly due to increasing demand for food, feed (animal) and, recently, fuel. The global demand for seaweed biomass is rising. Large companies using algae in their products require a regular and reliable supply of the material, both in quantity and quality. Western Europe, for example, will continue to improve farming techniques to increase production, mainly because of the high market value of the different products derived from seaweeds (Holdt, 2011). Figure 10 shows the pyramid of the seaweed product markets.

5.1 Food

Asian countries will continue to consume seaweeds as part of their daily diet. There is a rising awareness of health and nutritional benefits from seaweeds in western countries. Likewise, there is a growing use by food processors in new applications that include seaweed pasta, mustard, rillettes and pâtés. Also, there is a high demand from the catering and food service sector that requires seaweed recipes. Hence, cultivation of economically important seaweed will expand as the population grows.

5.2 Feed (aquaculture)

The commercialization of land- and sea-based IMTA in Western Europe will open more opportunities to an immense use of seaweed as part of the diet of fish such as salmon, rainbow trout, cod, sea bass and other high-value fish. This is simply because several earlier studies have demonstrated the positive effects not only in terms of the increased growth rate, but more importantly, on the prevention of diseases (Wan et al., 2016; Walker et al., 2009; Valente et al., 2006). Likewise, hogs fed with seaweed resulted in higher milk production, decreased mortality by 50 percent, reduction in the use of antibiotics by 50 percent, generally improved health, reduced feed intake (gut health), earlier maturation, improved taste (industrial taste panel), and doubled omega-3 content (Kraan, 2015). The high demand of seaweed-fed abalone will continue, as the growing population prefers traceable marine food. The newly emerged application of seaweed in the shrimp diet will be developed and refined further. For these reasons, responsible and sustainable farming of seaweed will increase in the next few years.

5.3 Fuel

Traditionally, seaweeds have not been considered as feedstock for bioenergy production, but have been used in food, in medicine or as fertilizer, and in the processing of phycolloids and chemicals (Bixler and Porse, 2011). The cultivation of algal biomass for the production of third-generation biofuels has received increasing attention in recent years, as seaweeds can be produced in the marine environment and on non-arable lands. Production yields of algae per unit area are significantly higher than those for terrestrial biomass (Wei, Quarterman and Jin, 2013; Schenk et al., 2008). The chemical composition of algae makes it suitable for conversion into biofuels, especially the subtidal large brown kelps of the order Laminariales (Hughes et al., 2013) and Ulva (Bruton et al., 2009).

Seaweeds are already farmed on a large scale in Asia and to a lesser extent in Europe, primarily in France, and on a research scale in Scotland (Kelly and Dworjanyn, 2008). Western Europe, Ireland in particular, is becoming aggressive in research and development for a marine bioenergy and biofuel industry (Roberts and Upham, 2012). Biofuel production from macro-algae is in its infancy. There is a strong collaboration in the private sector, such as Statoil ASA, which entered into a partnership with Seaweed Energy Solutions AS (SES) and Bio Architecture Lab (BAL) to develop a macroalgae-to- ethanol system in Norway. The aim of the partnership is to develop a 10 000 ha seaweed farm off the coast of Norway, which will produce 200 000 tonnes of ethanol (equivalent to 2 percent of the European Union’s ethanol market) (Ystanes and Fougner, 2012). SES is developing the technology for large-scale cultivation and harvesting technology, while BAL is responsible for developing the technology and the process to convert the macro-algae into ethanol (Murphy et al., 2013).

Though several preliminary investigations have been conducted to assess the technical feasibility, environmental viability and economic profitability of seaweed farming for fuel (Watson, 2014; Valderamma et al., 2013; Watson et al., 2012), numerous parameters (such as method of cultivation, species of seaweed, yields of seaweed per hectare, time of harvest, method of harvesting, suitability of seaweed to ensiling the gross and net energy yields in biogas, carbon balance, cost of the harvested seaweed, and cost of the produced biofuel) have to be developed economically to obtain viable algae biofuel production.

6. CONSERVATION AND SUSTAINABLE USE STRATEGIES

Conservation is a careful preservation and protection of resources that includes a well-planned management of the natural resources to prevent exploitation, destruction or neglect. There is biodiversity of seaweeds within species, between species, and ecosystems, with each species having its own peculiar characteristics to adapt in a certain habitat. Seaweeds, both harvested and farmed, are important sources of livelihood to humans. Conserving and sustaining these resources for the benefit of mankind are imperative.

A sustainable livelihood is one that can be carried out over the foreseeable future without depleting the resources it depends upon and without depriving others of a livelihood. In order for a livelihood to be sustainable, there should be: economic development; social equity; and environmental protection. Sustainable development can be achieved if decisions are made to be economically profitable, biologically appropriate and socially acceptable (Figure 11) (Eigner-Thiel et al., 2013) (Circular Ecology, 2016).

Currently, intensive fed aquaculture (finfish and shrimp) throughout the world is rapidly increasing, making environmental impact the main concern. This concern pertains to the direct discharge of significant nutrient loads into coastal waters from open waters and with the effluents from land-based systems. The only way to mitigate this environmental concern is to adopt an aquaculture system that is sustainable and balanced, a system known as integrated multi-trophic aquaculture (IMTA) (Chopin et al., 2001). Aquaculture is the world’s fastest growing food production sector, and is associated with environmental, economic and societal issues. IMTA offers an innovative solution for environmental sustainability, economic stability, and societal acceptability of aquaculture by taking an ecosystem-based management approach. IMTA is the farming, in proximity, of aquaculture species from different trophic levels and with complementary ecosystem functions, so that one species’ excess nutrients are recaptured by the other crops and synergistic interactions among species occur (Chopin et al., 2013). By integrating fed aquaculture (finfish, shrimp) with inorganic and organic extractive aquaculture (seaweed and shellfish), the wastes of one resource user becomes a resource (fertilizer or food) for the others. Such a balanced ecosystem approach provides nutrient bioremediation capability, mutual benefits to the co-cultured organisms, economic diversification by producing other value-added marine crops, and increased profitability per cultivation unit for the aquaculture industry.

In order for seaweed farming to be sustainable, the following actions are to be implemented: expansion of farming areas, wherever possible and profitable, and subject to the needs of other sectors and environmental health; improvements in productivity through the development and wide adoption of better aquaculture practices, to include improved quality of seed supply, establishment of land-sea based nurseries, including innovative approaches such as IMTA; increased investment in research, development and extension (RD&E) to meet expected challenges, including disease risks, climate change and introductions of non-indigenous species; and strong collaboration among government agencies, academia and the private sector. Table 15 presents the conservation and sustainability strategies for farmed seaweeds.

7. CAPACITY BUILDING

7.1 Education

Development of human resources through scholarships and fellowships is encouraged, especially in developing countries, to pursue professional and personal advancement in the different fields of specialization in seaweeds for graduate and post-graduate programmes. Such education will prepare students to embark in tougher responsibilities needed in the community and the industry. A number of scholarships are being offered by developed countries, such as Australia, European countries, Japan, United Kingdom of Great Britain and Northern Ireland, and the United States of America, and are highly competitive.

7.2 Research and training

Skills training is designed both to improve student effectiveness as researchers and to equip them with the skills they will need in a career after graduating, whether to choose to follow an academic or a non-academic career path. The structure and design of PhD programmes should incorporate generic skills and be formulated with direct engagement with employers and enterprises where appropriate.

Worldwide, state universities and colleges as well as research centres have good programmes for seaweed research and training. Students and trainees are given the opportunity to conduct research according to the needs of the industry under the supervision of a professor or a scientist. They are trained to: conceptualize and write a proposal; conduct the study with little supervision; collect, analyse and interpret the data; make conclusions; write a manuscript for publication; and share the results with the scientific community through attendance at symposia and congresses.

It is in the stage of research and training that individuals will establish a strong working relationship with their mentor, peers, the private sector and the scientific community.

8. ROLE OF INTERNATIONAL AND REGIONAL ASSOCIATIONS IN THE DEVELOPMENT AND MANAGEMENT OF FARMED SEAWEEDS

There are several international and regional associations that are involved in the development and management of farmed seaweeds, as shown in Table 16. These associations have different mandates to fulfil for the betterment of the community and industry.

9. SOURCES OF INFORMATION

9.1 Regional and international centres

Only a few countries and regions have their own seaweed centres that cater to the needs of the industry and community. The western countries have centres dedicated mainly for basic and applied research on algae that may be absent in the developing countries. However, a small research laboratory is normally present in the university or in fisheries institutions. Table 17 lists international centres that have strong collaboration with other institutions/academia or industry in and out of the region with their respective mandates.

The biggest storage of seaweed information in terms of taxonomy, description and distribution is found in www.algaebase.org. All universities and research institutions that have seaweed programmes have a herbarium of their local species, as well as algae journals and books in their libraries.

9.2 Dissemination, networking and linkages

Scientific knowledge coming from research can be disseminated through the following ways: publication in peer-reviewed journals, symposium proceedings and books; presentation of results in different symposia and congresses; and writing in popularized magazines, newsletters, brochures and flyers for the industry.

Networking is important in the seaweed community. There is a need to work together to develop sea agriculture, or sea farming, in order to cater to the needs of the industry. Vertically integrated supply chains request a lot of energy from small companies. There is a need to improve the value chain for better efficiency and maximize shared benefits among the seaweed community. There are mutual benefits and assistance derived from linkages and networking activities with both local and international organizations. Linkages and networking are different in the degree of commitment by the partners. In linkages, the relationship between partner organizations is quite loose. It intends to serve the members of both sides according to their respective needs, interests and objectives. It creates bonds together to solicit support and assistance for purposeful activities. Networking, on the other hand, is much stronger, usually because the groups and agencies have common objectives and beneficiaries. Networking is basically about extending the outreach of the resources in different ways so as to increase the effectiveness of the programme. The areas of operation can also be increased through networking. A network is composed of several institutions, universities or research centres that bind together for a common goal. They work together to attain common objectives, undertake innovative practices, and update members regarding breakthroughs in different disciplines. Table 18 lists some of the active networks in different regions.

10. EXCHANGE PROGRAMMES

10.1 Information

Science and technology provide critical tools that help address national and global needs. Freedom of scientific exchange and stronger scientific collaboration to benefit humankind is of paramount importance. Open exchange of information and ideas is critical to scientific progress. To achieve this end, there should be: promotion of a strong, non-governmental, scientific publishing enterprise that ensures access to information and exchange of scientific ideas and information among all parties with legitimate uses while appropriately protecting copyright and security-related information; assurance of the quality of science and technological advancement through open, rigorous and inclusive peer review scientific publishing; and open interactions among scientists, engineers and students from across the globe.

Developments in computer technology have opened many opportunities to gain access to multiple systems to gather data or exchange information. Open access and exchange of information is one of the core values of academics. Open access is part of the open science movement and covers various initiatives and projects across the globe to make academic studies and results available to a wider readership. As open access publications are available free of charge throughout the world, even people in poorer countries who usually lack the financial means can access and use them.

Regular members of the International Seaweed Association have free access to the Journal of Applied Phycology, a journal that publishes articles on microalgae and macroalgae (seaweeds) with four issues each year.

10.2 Scientists and experts

Scientists and experts play crucial roles in the exploitation, management, conservation and sustainability of seaweed resources. Results of their scientific studies are used to formulate policies for the government to adapt for implementation.

According to Dr Houde of the Chesapeake Biological Station, United States of America, scientists have the difficult task of walking the fine line between traditional “science-worthy” science or making the news. Traditional science takes time, as the peer review process is typically a slow one, even though it helps to minimize errors. Often, it moves too slowly for policy, which has now begun to turn to “post normal” science, which pools the collective advice of experts.

Seaweed farming is centred on the management of the environment and sustainability of the commodities. It takes several years for scientists and experts to transfer the science-based technology to the industry. Trials of farming Kappaphycus and Eucheuma in the Philippines started in 1965 and it was only in 1971 that the first harvest of seaweed for export purposes was attained (Doty and Alvarez, 1981). Also, the introduction of IMTA in Canadian waters started as early as 2000 and became commercial several years after. Though biological and economic results were positive, social acceptability was a critical component in aquaculture sustainability (Barrington, Chopin and Robinson, 2009). Scientists and experts, together with the different stakeholders, met several times to discuss the importance and significance of IMTA. All agreed that IMTA has the potential to reduce the environmental impacts of salmon farming, benefit community economies, and improve industry competitiveness and sustainability. This successful aquaculture system is currently being replicated either on an experimental or near commercial stage in Western Europe (Holdt and Edwards, 2014; Lamprianidou, Telfer and Ross, 2015; Freitas, Morrondo and Ugarte, 2016).

Scientific and technological development is impossible without efficient communication between scientists or technologists and the community. Such that, a higher level of scientific research can be achieved through collaboration.

10.3 Test plants

Only test plants preserved in silica gels and dried samples previously soaked in 10 percent formaldehyde and later drained are allowed to be sent by courier to other universities or institutions outside from its point of origin for collaborative work. This is especially true in developing countries, which lack the facilities to analyse the samples for a specific test. The test plants serve as the share of the collaborative study, and ultimately, part of the authorship when the results are written and submitted to a peer-reviewed journal for possible publication. No fresh test plants are allowed by courier for scientific studies. However, live test plants can be brought by a scientist personally after proper documents from point of origin to final destination are in order. If no prior agreement is made with the provider of test plants for research and scientific purposes, a due recognition through acknowledgement at the end of the report or paper is appropriate.

11. CONCLUSIONS

The farming of economically important seaweeds for food has been predominantly in Asia for the past several decades and will continue to increase as population increases. On the other hand, the farming of seaweed for feed and fuel purposes will be centred in the western countries. Also, people in western countries are increasing their seaweed consumption as part of their diet for health reasons.

China, Japan and the Republic of Korea are the leading producing countries of brown seaweeds (Saccharina and Laminaria) and red seaweed (Pyropia), while Indonesia and the Philippines are the top leading producers of Kappaphycus and Eucheuma. It is surprising to learn that Indonesia has surpassed China and Chile in the production of Gracilaria since 2013. Indonesia is presently the world’s number one producer of farmed red seaweeds, notably Eucheuma, Gracilaria and Kappaphycus.

Innovations in farming systems are being done because of disease and epiphytism problems brought on by climate change. Seaweed farmers with the technical assistance of scientists and experts will continue to work together for the improvement of crop management, productivity and production. One example of a culture farming modification is the traditional farming of Kappaphycus, which has now shifted from shallow waters to deeper waters to avoid elevated surface water temperature that adversely affects productivity and production.

The use of plantlets from spores remains to be used in the laboratory for out planting purposes with improvements in nutrition-temperature-light requirements. Although several successful studies were reported on the regeneration of plantlets of Kappaphycus and Eucheuma from callus through micropropagation using different culture media, their economic viability in the field needs additional testing, though initial trials have been started. Likewise, the use of seaweed extract as a biostimulant in the micropropagation of Kappaphycus has proven successful and field trials are in progress. At present, vegetative propagation still dominates the commercial farming of Kappaphycus and Eucheuma. The successful crossbreeding of Saccharina japonica using gametophytes and sporophytes (Dongfang No. 7) may provide a model for domestication to be used with other brown seaweeds (kelp).

Currently, seaweed genetic transformation is not fully developed despite several studies reported. Because a genetic transformation system would allow to perform genetic analysis of gene function via inactivation and knock-down of gene expression by RNAi and antisense RNA suppression, its establishment will enhance both our biological understanding and genetical engineering for the sustainable production of seaweeds and also for the use of seaweeds as bioreactors.

IMTA as a holistic aquaculture system has been tested to be technically feasible, environmentally friendly, economically viable and socially acceptable in the western countries and China. Its replication in other countries, especially in countries engaged in intensive shrimp and finfish aquaculture, has yet to be introduced or developed.

Conservation and sustainability of farmed seaweeds are the ultimate goals to ensure that the biomass needed for its final product is maintained commercially.

Seaweed international centres, societies, organizations and associations, and networking among scientists and experts will continue to play important and significant roles in the further development and ultimate sustainability of farmed seaweeds, which are good for food, feed and fuel.

References

Agrios, G.N. 2005. Plant pathology. Fifth edition. Elsevier B.V. 922 pp.

Akaike, S., Takiya, A., Tsuda F., Motoya, A. & Takahashi, K. 2002. Seasonal occurrence of a kelpboring amphipod, Ceinina japonica along the coasts of Hokkaido from 1997 to 2001. Scientific Reports of Hokkaido Fisheries Experimental Station, 61: 25–28.

Akiyama, K. 1977. Preliminary report on Streblonema disease in Undaria. Bulletin of Tohoku Regional Fisheries Research Laboratory, 37: 39–41.

Andrews, J.H. 1976. The pathology of marine algae. Biological Review, 51(2): 211–253.

Apt, K.E. 1988. Galls and tumor-like growths on marine macroalgae. Diseases of Aquatic Organisms, 4: 211–217.

Araki, T. & Morishita, T. 1990. Fusion of protoplasts from wild type Porphyra yezoensis and green type P. tenera thalli (Rhodophyta). Nippon Suisan Gakkaishi, 56(7): 1161.

Araújo, P.G., Schmidt, E.C., Kreusch, M.G., Kano, C.H., Guimarães, S.M.P.B., Bouzon, Z.L., Fujii, M.S. & Yokoya, N.S. 2014. Ultrastructural, morphological, and molecular characterization of Colaconema infestans (Colaconematales, Rhodophyta) and its host Kappaphycus alvarezii (Gigartinales, Rhodophyta) cultivated in the Brazilian tropical region. Journal of Applied Phycology, 26(5): 1953–1961.

Ateweberhan, M., Rougier, A. & Rakotomahazo, C. 2015. Influence of environmental factors and farming technique on growth and health of farmed Kappaphycus alvarezii (cottonii) in south-west Madagascar. Journal of Applied Phycology, 27(2): 923–934.

Azanza, R.V. & Aliaza, T. 1999. In vitro carpospore release and germination in Kappaphycus alvarezii (Doty) Doty from Tawi-Tawi, Philippines. Botanica Marina, 42(3): 281–284.

Azanza-Corrales, R., Aliaza, T.T. & Montano, N.E. 1996. Recruitment of Eucheuma and Kappaphycus on a farm in Tawi-Tawi, Philippines. Hydrobiologia, 326(1): 235–244.

Azanza-Corrales, R. & Ask, E. 2003. Kappaphycus alvarezii (Doty) Doty carposporeling growth and development in the laboratory. In A. Chapman, R.J. Anderson, V. Vreeland & I. Davison, eds. Proceedings of the XVII International Seaweed Symposium, pp. 95–99. New York, USA, Oxford University Press.

Bansemir, A., Blume, M., Schröeder, S. & Lindequist, U. 2006. Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture, 252(1): 79–84.

Barrington, K., Chopin, T. & Robinson, S. 2009. Integrated multi-trophic aquaculture (IMTA) in marine temperate waters. In D. Soto, ed. Integrated mariculture: a global review, pp. 7–46. FAO Fisheries and Aquaculture Technical Paper No. 529. Rome, FAO.

Benet, H., Bruss, U., Duval, J.C. & Kloareg, B. 1994. Photosynthesis and photoinhibition in protoplasts of the marine brown alga Laminaria saccharina. Journal of Experimental Botany, 45(2): 211–220.

Benet, H., Gall, A.E., Asensi, A. & Kloareg, B. 1997. Protoplast regeneration from gametophytes and sporophytes of some species in the order Laminariales (Phaeophyceae). Protoplasma,199(1–2):39–48.

Bernasconi, P., Cruz-Uribe, T., Rorrer, G., Bruce, N. & Cheney D.P. 2004. Development of a TNT-detoxifying strain of the seaweed Porphyra yezoensis through genetic engineering. Journal of Phycology, 40(Suppl_1): 31

Bhatnagar-Mathur, P., Vadez, V. & Sharma K.K. 2008. Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Reports, 27(3): 411–424.

Bixler, H.J & Porse, H. 2011. A decade of change in the seaweed hydrocolloids industry. Journal of Applied Phycology, 23(3): 321–335.

Bjork, M., Ekman, P., Wallin, A. & Pedersen, M. 1990. Effect of growth rate and other factors on protoplast yield from four species of Gracilaria (Rhodophyta). Botanica Marina, 33(5): 433–439.

Bolton, J.J., Robertson-Andersson, D.M., Troell, M. & Halling, C. 2006. Integrated systems incorporate seaweeds in South African abalone culture. Global Aquaculture Advocate, 9(4): 54–55.

Borges, M.T., Silva, P., Moreira, L. & Soares, R. 2005. Integration of consumer-targeted microalgal production with marine fish effluent biofiltration – a strategy for mariculture sustainability. Journal of Applied Phycology, 17(3): 187–197.

Borlongan, I.A.G., Tibudos, K.R., Yunque, D.A.T., Hurtado, A.Q. & Critchley, A.T. 2011. Impact of AMPEP on the growth and occurrence of epiphytic Neosiphonia infestation on two varieties of commercially cultivated Kappaphycus alvarezii grown at different depths in the Philippines. Journal of Applied Phycology, 23(3): 615–621.

Bouarab, K., Potin, P., Correa, J.A. & Kloareg, B. 1999. Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell, 11(9): 1635–1650.

Bouarab, K., Potin, P., Weinberger, F., Correa, J.A. & Kloareg B. 2001. The Chondrus crispus-Acrochaete operculata host-pathogen association, a novel model in glycobiology and applied phycopathology. Journal of Applied Phycology, 13(2): 185–193.

Brown, P., Plumb, J., Sanchez-Baracaldo, P., Hayes, P.K. & Brodie, J. 2003. Sequence heterogeneity of green (Chlorophyta) endophytic algae associated with a population of Chondrus crispus (Gigartinaceae, Rhodophyta). European Journal of Phycology, 38(2): 153–163.

Bruton, T., Lyons, H., Lerat, Y., Stanley, M. & Rasmussen M.B. 2009. A review of the potential of marine algae as a source of biofuel in Ireland. Dublin, Ireland, Sustainable Energy Ireland.

Bulboa, C.R., De Paula, E.J. & Chow, F. 2007. Laboratory germination and sea out-planting of tetraspore progeny from Kappaphycus striatum (Rhodophyta) in subtropical waters of Brazil. Journal of Applied Phycology, 19(4): 357–363.

Burkhardt, E. & Peters, A.F. 1998. Molecular evidence from nrDNA ITS sequences that Laminariocolax (Phaeophyceae, Ectocarpales sensu lato) is a worldwide clade of closely related kelp endophytes. Journal of Phycology, 34(4): 682–691.

Buschmann, A.H., Hernandez-Gonzalez, M.C., Aroca, G. & Gutierrez, A. 2001. Seaweed farming in Chile: A review. The Advocate, 4: 68–69.

Buschmann, A.H., Troell, M., Kautsky, N. & Kautsky, E. 1996. Integrated tank cultivation of salmonids and Gracilaria chilensis (Gracilariales, Rhodophyta). Hydrobiologia, 326(1): 75–82.

Butler, D.M. & Evans, L.V. 1990. Cell and tissue culture of macroalgae. In I. Akatsuka, ed. Introduction to applied phycology, pp. 629–645. The Hague, The Netherlands, SPB Academic Publishing.

Butler, D.M., Ostgaard, K., Boyen, C., Evans, L.V., Jensen, A. & Kloareg, B. 1989. Isolation condition for high yields of protoplasts from Laminaria saccharina and L. digitata (Phaeophyceae). Journal of Experimental Botany, 40(11): 1237–1246.

Carmona, R., Kraemer, G.P. & Yarish C. 2006. Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture, 252(1): 54–65.

Chandrasekaran, S., Nagendran, N.A., Pandiaraja, D., Krushnankutty, N. & Kamalakannan B. 2008. Bioinvasion of Kappaphycus alvarezii on corals in the Gulf of Mannar, India. Current Science, 94(9): 1167–1172.

Chen, L.C. & Taylor, A.R. 1978. Medullary tissue culture of the red alga Chondrus crispus. Canadian Journal of Botany, 56(7): 883–886.

Chen, Y.C. & Shih, H.C. 2000. Development of protoplasts of Ulva fasciata (Chlorophyta) for algal seed stock. Journal of Phycology, 36(3): 608–615.

Cheney, D. 1990. Genetic improvement of seaweeds through protoplasts fusion. In C. Yarish, C. Penniman & P. Van Patten, eds. Economically important marine plants of the Atlantic: their biology and cultivation, pp. 15–25. Storrs, USA, University of Connecticut Sea Grant Program.

Cheney, D.P., Mathiesen, A. & Schubert, D. 1981. The application of genetic improvement techniques to seaweed cultivation: I. strain selection in the carrageenophyte Chondrus crispus. International Seaweed Symposium, 10: 559–567.

Cheney, D., Metz, B. & Stiller, J. 2001. Agrobacterium-mediated genetic transformation in the macroscopic marine red alga Porphyra yezoensis. Journal of Phycology, 37(11).

Chess, J.R. 1993. Effects of the stipe-boring amphipod Peramphithoe stypotrupetes (Corophioidea: Ampithoidae) and grazing gastropods on the kelp Laminaria setchellii. Journal of Crustacean Biology, 13(4): 638–646.

Chopin, T., Buschmann, A.H., Halling, C., Troell, M., Kautsky, N., Neori, A., Kraemer, G.P., Zertuche-Gonzalez, J.A., Yarish, C. & Neefus, C. 2001. Integrating seaweeds into marine aquaculture systems: a key towards sustainability. Journal of Phycology, 37(6): 975–986.

Chopin, T., MacDonald, B., Robinson, S., Cross, S., Pearce, C., Knowler, D., Noce, et al. 2013. The Canadian Integrated Multi-Trophic Aquaculture Network (CIMTAN– A Network for a New Era of Ecosystem Responsible Aquaculture. Fisheries, 38(7): 297–308.

Chopin, T., Robinson, S.M.C., Troell, M., Neori, A., Buschmann, A.H. & Fang, J. 2008. Multi-trophic integration for sustainable marine aquaculture. In S.E. Jørgensen., B.D. Fath, eds. The Encyclopedia of Ecology, Ecological Engineering, vol. 3, pp. 463–2475. Oxford, UK, Elsevier.

Chopin, T., Yarish, C., Wilkes, R., Belyea, E., Lu, S. & Mathieson, A. 1999. Developing Porphyra/ salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. Journal of Applied Phycology, 11(5): 463.

Chopin, T. & Sawhney, M. 2009. Seaweeds and their mariculture. In: J.H. Steele, S.A. Thorpe, K.K. Turekian, eds. The Encyclopedia of Ocean Sciences, pp. 4477–4487. Oxford, UK, Elsevier.

Chopin, T. & Robinson, S. 2004. Defining the appropriate regulatory and policy framework for the development of integrated multi-trophic aquaculture practices: introduction to the workshop and positioning of the issues. Bulletin of the Aquaculture Association of Canada, 104: 4–10.

Chou, H.N. & Lu, H.K. 1989. Protoplasts from seaweeds: isolation, culture and fusion. In S. Miyachi, I. Karube & Y. Ishida, eds. Current topics in marine biotechnology, pp. 227–230. Tokyo, Japan, Japanese Society of Mairne Biotechnology.

Chung, I.K. & Lee, J.A. 2014. Mitigation potential of seaweed aquaculture beds in Asia-Pacific countries. Paper presented at World Aquaculture 2015 Guangzhou, China. 18–21 December 2014.

Circular Ecology. 2016. Sustainable development. www.circularecology.com/sustainability-and-sustainable-development.html#.WBZjJ4WcHg8

Conklin, E.J. & Smith, J.E. 2005. Abundance and spread of the invasive red algae, Kappaphycus spp., in Kane’ohe Bay, Hawai’i and an experimental assessment of management options. Biological Invasions, 7(6): 1029–1039.

Corey, P., Kim, J.K., Duston, J. & Garbary, D.J. 2014. Growth and nutrient uptake by Palmaria palmata integrated with Atlantic halibut in a land-based aquaculture system. Algae, 29(1): 35–45.

Cornwall, C.E., Hepburn, C.D., Pritchard, D., Currie, K.I., McGraw, C.M., Hunter, K.A. & Hurd, C.L. 2012. Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. Journal of Phycology, 48(1): 137–144.

Correa, J.A. & Flores, V. 1995. Whitening, thallus decay and fragmentation in Gracilaria chilensis associated with an endophytic amoeba. Journal of Applied Phycology, 7(4): 421–425.

Correa, J.A. & McLachlan, J.L. 1991. Endophytic algae of Chondrus crispus (Rhodophyta). 3. Host specificity. Journal of Phycology, 27(3): 448–459.

Correa, J.A. & McLachlan, J.L. 1992. Endophytic algae of Chondrus crispus (Rhodophyta). IV. Effects on the host following infections by Acrochaete operculata and A. heteroclada (Chlorophyta). Marine Ecology Progress Series, 81(1): 73–87.

Correa, J.A. & McLachlan, J.L. 1994. Endophytic algae of Chondrus crispus (Rhodophyta). V. Fine structure of the infection by Acrochaete operculata (Chlorophyta). European Journal of Phycology, 29(1): 33–47.

Coury, D.A., Naganuma, T., Polne-Fuller, M. & Gibor, A. 1993. Protoplasts of Gelidium robustum (Rhodophyta). Hydrobiologia, 260/261: 421–427.

Craigie, J.S. & Correa, J.A. 1996. Etiology of infectious diseases in cultivated Chondrus crispus (Gigartinales, Rhodophyta). Hydrobiologia, 326(1): 97–104.

Critchley, A.T., Largo, D., Wee, W., Bleicher-L’honneur, G., Hurtado, A.Q. & Schubert, J. 2004. A preliminary summary on Kappaphycus farming and the impact of epiphytes. Japan Journal of Phycology, 52(Suppl): 231–232.

Cromey, C.J., Nickell, T.D. & Black, K.D. 2002. DEPOMOD-modelling the deposition and biological effects of waste solids from marine cage farms. Aquaculture, 214(1–4): 211–239.

Dai, J., Zhang, Q. & Bao, Z. 1993. Genetic breeding and seedling raising experiments with Porphyra protoplasts. Aquaculture, 111: 139–145.

Dawes, C.J. & Koch, E.W. 1991. Branch micropropagule and tissue culture of the red alga Eucheuma denticulatum and Kappaphycus alvarezii farmed in the Philippines. Journal of Applied Phycology, 3(3): 247.

Dawes, C.J., Trono, G.C. Jr. & Lluisma, A.O. 1993. Clonal propagation of Eucheuma denticulatum and Kappaphycus alvarezii for Philippine seaweed farms. Hydrobiologia, 260(1): 379–383.

De Paula, E.J., Pereira, R.T.L. & Ohno, M. 1999. Strain selection in Kappaphycus alvarezii var. alvarezii (Solieriaceae, Rhodophyta) using tetraspore progeny. Journal of Applied Phycology, 11: 111–121.

Dewey, F.M., Donnelly, K.A. & Foster, D. 1983. Penicillium waksmanii isolated from a red seaweed, Eucheuma striatum. Transactions of the British Mycological Society, 81(2): 433–434.

Dewey, F.M., Hunter-Blair, C.M. & Banbury, G.H. 1984. Isolation of Scopulariopsis brevicaulis from Eucheuma striatum and its ability to degrade seaweeds and their soluble products. Transactions of the British Mycological Society, 83(4): 621–629.

Ding, H. & Ma, J. 2005. Simultaneous infection by red rot and chytrid diseases in Porphyra yezoensis Ueda. Journal of Applied Phycology, 17(1): 51–56

Doty, M.S. 1973. Farming the red seaweed, Eucheuma, for carrageenans. Micronesica, 9(1): 59–73.

Doty, M.S. & Alvarez, V. 1973. Seaweed farms: a new approach for U.S. industry. Marine Technology Society Annual Conference Paper, 9: 701–708.

Doty, M.S. & Alvarez, V.B. 1981. Eucheuma farm productivity. International Seaweed Symposium, 8: 688–691.

Edwards, M. & Watson, L. 2011. Cultivating Laminaria digitata. Aquaculture Explained No. 26. Bord lascaigh Mhara, Irish Sea Fisheries Board. 72 pp.

Egan, S., James, S., Holmstrom, C. & Kjelleberg, S. 2001. Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. FEMS Microbiology and Ecology, 35(1): 67–73.

Eigner-Thiel, S., Schmehl, M., Ibendorf, J. & Geldermann, J. 2013. Assessment of different bioenergy concepts in terms of sustainable development. In H. Ruppert, M. Kappas & J. Ibendorf, eds. Sustainable bioenergy production – an integrated approach, 339–384. Dordrecht, Netherlands, Springer.

Enomoto, K. & Hirose, H. 1972. Culture studies on artificially induced aplanospores in the marine alga Boergesenia forbesii (Harvey) Feldman (Chlorophyceae, Siphonocladales). Phycologia, 11(2): 119–122.

Ezura, Y., Yamamoto, H. Kimura, T. 1988. Isolation of a marine bacterium that produces red-spots on the culture bed of makonbu Laminaria japonica cultivation. Nippon Suisan Gakkaishi, 54: 665–672.

Fang, J.G, Kuang, S., Sun, H., Li, F., Zhang, A., Wang, X. & Tang, T. 1996a. Mariculture status and optimizing measurements for the culture of scallop Chlamys farreri and kelp Laminaria japonica in Sanggou Bay. Fishery and Marine Research, 17(2): 95−102.

Fang, J.G., Sun, H.L., Yan, J.P., Kuang, S.H., Feng, L.I., Newkirk, G.F. & Grant, J. 1996b. Polyculture of scallop Chlamys farreri and kelp Laminaria japonica in Sungo Bay. Chinese Journal of Oceanology and Limnology, 14: 322–329.

Fang, J.G. & Zhang, J.H. 2015. Types of integrated multi-trophic aquaculture practiced in China. World Aquaculture, 46(1): 26−30.

Fang, J., Zhang, J., Xiao, T., Huang, D. & Liu, S. 2016. Integrated multi-trophic aquaculture (IMTA) in Sanggou Bay, China. Aquaculture Environment Interactions, 8: 201–205.

FAO. 2014. Fishery and Aquaculture Statistics 2012. Rome.

Folke, C. & Kautsky, N. 1989. The role of ecosystems for a sustainable development of aquaculture. Ambio, 18: 234–243

Forster, J. 2008. Offshore aquaculture: the great American debate. Global Aquaculture Advocate, 11(2): 18–20.

Freitas, J.R.C. Jr., Morrondo, J.M.S. & Ugarte, J.C. 2016. Saccharina latissima (Laminariales, Ochrophyta) farming in an industrial IMTA system in Galicia (Spain). Journal of Applied Phycology, 28(1): 377–385.

Fujimura, T., Kawai, T., Shiga, M., Kajiwara, T. & Hatanaka, A. 1989. Regeneration of protoplasts into complete thalli in the marine green alga Ulva pertusa. Nippon Suisan Gakkaishi, 55(8): 1353–1359.

Fujita, Y. 1993. Crossbreeding of green and red algae by cell fusion. Kaiyo Monthly, 25: 690–695.

Fujita, Y. & Migita, S. 1985. Isolation and culture of protoplasts from seaweeds. Bulletin Faculty of Fisheries, Nagasaki University, 57: 39–45.

Fujita, Y. & Migita, S. 1987. Fusion of protoplasts from thalli of two different color types in Porphyra yezoensis Ueda and development of fusion products. Japan Journal of Phycology, 35: 201–208.

Fujita, Y. & Saito, M. 1990. Protoplasts isolation and fusion in Porphyra (Bangiales, Rhodophyta). Hydrobiologia, 204/205: 161–166.

Gan, S.Y., Qin, S., Othman, R.Y., Yu, D. & Phang, S.M. 2003. Transient expression of lacZ in particle bombarded Gracilaria changii (Gracilariales, Rhodophyta). Journal of Applied Phycology, 15(4): 345–349.

Gan, S.Y., Qin, S., Othman, R.Y., Yu, D. & Phang, S.M. 2004. Development of a transformation system for Gracilaria changii (Gracilariales, Rhodophyta), a Malaysian red alga via microparticle bombardment. The 4th Annual Seminar of National Science Fellowship. BIO, 8: 45–48.

Garrett, K.A., Nita, M., De Wolf, E.D., Gomez, L. & Sparks, A.H. 2009. Plant pathogens as indicators of climate change. In T. Letcher, ed. Climate change: observed impacts on planet Earth, pp. 425–437. Dordrecht, The Netherlands, Elsevier.

Gong, Q., Yu, W., Dai, J., Liu, H., Xu, R., Guan, H. & Pan, K. 2005. Efficient gusA transient expression in Porphyra yezoensis protoplasts mediated by endogenous beta-tubulin flanking sequences. Journal of Ocean University of China, 6(1): 21–25.

Gowen, R.J. & Bradbury, N.B. 1987. The ecological impact of salmonid farming in coastal waters: a review. Oceanography and Marine Biology Annual Review, 25: 563–575.

Gutierrez, A., Correa, T., Muñoz, V., Santibañez, A., Marcos, R., Caceres, C. & Buschmann, A.H. 2006. Farming of the giant kelp Macrocystis pyrifera in southern Chile for development of novel food products. Journal of Applied Phycology, 18: 259–267.

Hado, M., Okauchhi, M., Murase, N. & Mizukami, Y. 2003. Transient expression of GUS gene using Rubisco gene promoter in the protoplasts of Porphyra yezoensis. Suisan Zoushoku, 51(3): 355–360.

Hafting, J.T. 1999. A novel technique for propagation of Porphyra yezoensis Ueda blades in suspension cultures via monospores. Journal of Applied Phycology, 11: 361–367.

Handå, A. 2012. Cultivation of mussels (Mytilus edulis): feed requirements, storage and integration with salmon (Salmo salar) farming. Ph.D. Dissertation at Norwegian University of Science and Technology, Trondheim, Norway. 164 pp.

Handayani, T., Alimuddin, A., Widyastuti, U., Suryati, E. & Parengrengi, A. 2014. Binary vector construction and Agrobacterium tumefaciens-mediated transformation on lyzsozome gene in seaweed Kappaphycus alvarezii. BIOTROPIA, 21: 80–90.

Hanniffy, D. & Kraan, S. 2006. BIOPURALG: reducing the environmental impact of land-based aquaculture through cultivation of seaweeds.

Hayashi, L., Bulboa, C., Kradolfer, P., Soriano, G. & Robledo, D. 2014. Cultivation of red seaweeds: a Latin American perspective. Journal of Applied Phycology, 26(2): 719–727.

Hayashi, L., Yokoya, N.S., Kikuchi, D.M. & Oliveira, E.C. 2008. Callus induction and micropropagation improved by colchicines and phytoregulators in Kappaphycus alvarezii (Rhodophyta, Solieriacea). Journal of Applied Phycology, 20: 653–659.

He, P., Yao, Q., Chen, Q., Guo, M., Xiong, A., Wu, W. & Ma, J. 2001. Transferring and expression of glucose oxidase gene in Porphyra yezoensis. Journal of Phycology, 37(Suppl): 23.

Heesch, S. & Peters, A.F. 1999. Scanning electron microscopy observation of host entry by two brown algae endophytic in Laminaria saccharina (Laminariales, Phaeophyceae). Phycological Research, 47(1): 1–5.

Hirata, H., Yamasaki, S., Maenosono, H., Nakazono, T., Yamauchi, T. & Matsuda, M. 1994. Relative budgets of pO_2 and pCO_2 in cage polycultured red sea bream, Pagrus major and sterile Ulva sp. Aquaculture Science, 42(2): 377–381.

Ho, J. & Hong, J.S. 1988. Harpacticoid copepods (Thalestridae) infesting the cultivated Wakame (brown alga, Undaria pinnatifida) in Korea. Journal of Natural History, 22(6): 1623–1637.

Holdt, S.L. 2011. Bioactive components in algae. Paper presented at Algal Plant Bioteck, Denmark Meeting. 3–4 March 2011.

Holdt, S.L. & Edwards, M.D. 2014. Cost-effective IMTA: a comparison of the production efficiencies of mussels and seaweed. Journal of Applied Phycology, 26(2): 933–945.

Huang, X., Weber, J.C., Hinson, T.K., Mathieson, A.C. & Minocha, S.C. 1996. Transient expression of the GUS reporter gene in the protoplasts and partially digested cells of Ulva lactuca L. (Chlorophyta). Botanica Marina, 39(5): 467–474.

Huddy, S.M., Meyers, A.E. & Coyne, V.E. 2013. Protoplast isolation optimization and regeneration of cell wall in Gracilaria gracilis (Gracilariales, Rhodophyta). Journal of Applied Phycology, 25(2): 433–443.

Hughes, A.D., Black, K.D., Campbell, I., Heymans, J.J., Orr, K.K., Stanley, M.S. & Kelly, M.S. 2013. Comments on “Prospects for the use of macroalgae for fuel in Ireland and UK: an overview of marine management issues”. Marine Policy, 38: 554–556.

Hurtado, A.Q. & Biter, A. 2007. Plantlet regeneration of Kappaphycus alvarezii var. adik adik by tissue culture. Journal of Applied Phycology, 19(6): 783–786.

Hurtado, A.Q. & Cheney, D.P. 2003. Propagule production of Eucheuma denticulatum (Burman) Collins et Hervey by tissue culture. Botanica Marina, 46(4): 338–341.

Hurtado, A.Q. & Critchley, A.T. 2006. Seaweed industry of the Phillipines and the problem of epiphytism in Kappaphycus farming. In S.M. Phang, A.T. Critchley & P.O. Ang, eds. Advances in seaweed cultivation and utilisation in Asia, pp. 21–28. Kuala Lumpur, Malaysia, University of Malaya.

Hurtado, A.Q., Critchley, A.T., Trespoey, A. & Bleicher-L’Honneur, G. 2006. Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Island, Camarines Norte, Philippines. Journal of Applied Phycology, 18(3–5): 301–306.

Hurtado, A.Q., Gerung, G.S., Yasir, S. & Critchley, A.T. 2014. Cultivation of tropical red seaweeds in the BIMP-EAGA region. Journal of Applied Phycology, 26(2): 702–718.

Hurtado, A.Q., Yunque, D.A., Tibubos, K. & Critchley, A.T. 2009. Use of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. Journal of Applied Phycology, 21(6): 633.

Hurtado-Ponce, A.Q. 1993. Harvesting Gracilariopsis hetroclada (Gracilariales, Rhodophyta in Iloilo), Philippines. Philippine Journal of Science, 122(4): 413–423.

Hurtado-Ponce, A.Q., Agbayani, R.F. & Samonte-Tan, G.P.B. 1997. Growth rate yield and economics of Gracilariopsis bailiniae (Gracilariales, Rhodophyta) using fixed-bottom long line method. Philippine Journal of Science, 126(3): 251–259.

Hurtado-Ponce, A.Q, Samonte, G., Luhan, G.P.B., Ma, R.J. & Guanzon, N.G., Jr. 1992. Gracilaria farming in Western Visayas, Philippines. Aquaculture, 105(3–4): 233–240.

Hwang, E.K., Hwang, I.K., Park, E.J., Gong, Y.G. & Park, C.S. 2014. Development and cultivation of F2 hybrid between Undariopsis peterseniana and Undaria pinnatifida for abalone feed and commercial mariculture in Korea. Journal of Applied Phycology, 26(2): 747–752.

Hwang, E.K., Baek, J.M., & Park, C.S. 2009. Cultivation of the green alga, Codium fragile (Suringar) Hariot) by aritificial seed production in Korea. Journal of Applied Phycology, 20(5): 19-25.

Inoue, A., Kagaya, M. & Ojima, T. 2008. Preparation of protoplasts from Laminaria japonica using native and recombinant abalone alginate lyases. Journal of Applied Phycology, 20(5): 633–640.

Ishikawa, Y. & Saga, N. 1989. Diseases of economically valuable seaweeds and their pathology in Japan. Proceedings of the First International Marine Biotechnology Conference (IMBC ’89), pp. 215–218. Tokyo, Japan.

Israel, A. & Hophy, M. 2002. Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO_2 concentrations. Global Change Biology, 8(9): 831–840.

Japan Ministry of Agriculture, Forestry and Fisheries. 2014.

Ji, Y., Xu, Z., Zou, D. & Gao, K. 2016. Ecophysiological responses of marine macroalgae to climate change factors. Journal of Applied Phycology, 28(5): 2953–2967.

Jiang, J., Ma, Y., Zhang, Z. & Xu, H. 1997. The histopathological study on “green decay diseases” of Undaria pinnatifida in Dalian. Journal of Dalian Fisheries, University/Dalian Shuichan Xueyuan Xuebao, 12: 7–12.

Jiang, P., Qin, S. & Tseng, C.K. 2002. Expression of hepatitis B surface antigen gene (HBsAg) in Laminaria japonica (Laminariales, Phaeophyta). Chinese Science Bulletin, 47: 1438–1440.

Jiang, P., Qin, S. & Tseng, C.K. 2003. Expression of the lacZ reporter gene in the sporophytes of the seaweed Laminaria japonica (Phaeophyceae) by gametophyte-targeted transformation. Plant Cell Report, 21(12): 1211–1216.

Jiang, Z., Fang, J. & Zhang, J. 2009. Nutrient budget in marine fish cage culture system and integrated multi-trophic aquaculture (IMTA) scheme. In 2nd YSLME Regional Mariculture Conference Towards Sustainability in Yellow Sea Mariculture.16–18 June. (Abstract only)

Jie, K. 1987. Protoplast fusion of Enteromorpha linza and Ulva pertusa. Marine Fisheries Research, 08.

Kakinuma, M., Ikeda, M., Coury, D.A., Tominaga, H., Kobayashi, I. & Amano, H. 2009. Isolation and characterization of the rbcS genes from a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta) and transient gene expression using the rbcS gene promoter. Fisheries Science, 75(4): 1015–1028.

Kang, J.W. 1982. Some seaweed diseases occurred at seaweed farms along the south-eastern coast of Korea. Bulletin of the Korean Fisheries Society, 14(3): 165–170.

Kawashima, Y. & Tokuda, H. 1993. Regeneration from the callus of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta). Hydrobiologia, 260(1): 385–389.

Kelly, M.S. & Dworjanyn, S. 2008. The potential of marine biomass for anaerobic biogas production: a feasibility study with recommendations for further research. The Crown Estate, 103 pp.

Kim, Y.D., Park, M.S., Min, B.H., Jeong, S.J., Kim, H.C., Yoo, H.I., Won-Chan Lee, W.C. & Choi, J.S. 2014. Study on growth characteristics of Sargassum fulvellum in the integrated multi-trophic aquaculture (IMTA) system. Journal of Environmental Science International, 23(10): 1703–1718.

Kim, J.K., Yarish, C., Hwang, E.K. Park, M., & Kim, YD. 2017. Seaweed aquaculture: cultivation technologies, challenges and its ecosystem services. Algae, 32(1): 1–13.

Kimura, T., Ezura, Y. & Tajima, K. 1976. Microbiological study of a disease of wakame (Undaria pinnatifida) and of the marine environments of wakame culture sites in Kesennuma Bay. Bulletin of the Tohoku Regional Fisheries Research Laboratory, 36: 57–65.

Kito, H., Akiyama, K. & Sasaki, M. 1976. Electron microscopic observations on the diseased thalli of Undaria pinnatifida (Harvey) Suringar, caused by parasitic bacteria. Bulletin of the Tokohu Regional Fisheries Research Laboratory, 36: 67–73.

Kito, H., Kunimoto, M., Kamanishi, Y. & Mizukami, Y. 1998. Protoplasts fusion between Monostroma nitidum and Porphyra yezoensis and subsequent growth of hybrid plants. Journal of Applied Phycology, 10(1): 15–21.

Kloareg, B., Polne-Fuller, M. & Gibor, A. 1989. Mass production of viable protoplasts from Macrocystis pyrifera (L.) C. Ag. (Pheophyta). Plant Science, 62(1): 105–112.

Klochkova, T.A., Shin, Y.J., Moon, K.H., Motomura, T. & Kim, G.H. 2016. New species of unicellular obligate parasite, Olpidiopsis pyropiae sp. nov., that plagues Pyropia sea farms in Korea. Journal of Applied Phycology, 28(1): 73–83.

Kobayashi, K. 1975. Growth of extra cellular protoplast of Bryopsis maxima in an agar medium. Bulletin of Tokyo Gakugei University, 27: 1–5.

Kohlmeyer, J. 1968. Revisions and descriptions of algicolous marine fungi. Journal of Phytopathology, 63(4): 341–363.

Korea Ministry of Oceans and Fisheries. 2015.

Kraan, S. 2010. Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production. Mitigation and Adaptation Strategies for Global Change, 18(1): 1–20.

Kraan, S. 2015. IMTA in an international context and the applications of harvested biomass. Paper presented at Horsen, Denmark, 15 June 2015.

Kuang, M., Wang, S.J., Li, Y., Shen, D.L. & Zeng, C.K. 1998. Transient expression of exogenous GUS gene in Porphyra yezoensis (Rhodophyta). Chinese Journal of Oceanology and Limnology, 16(1): 56–61.

Kurtzman, A.M. & Cheney, D.P. 1991. Direct gene transfer and transient expression in a marine red alga using the biolistic method. Journal of Phycology, 27(Suppl): 42.

Lamprianidou, F., Telfer, T. & Ross, L. 2015. A model for optimization of the productivity and bioremediation efficiency of marine integrated multitrophic aquaculture. Estuarine, Coastal and Shelf Science, 164: 253–264.

Largo, D.B., Diola, A.G. & Marabahol, M.S. 2016. Development of an integrated multi-trophic aquaculture (IMTA) system for tropical marine species in southern Cebu, Central Philippines. Aquaculture Reports, 3: 67–76.

Largo, D.B., Fukami, F., Nishijima, T. & Ohno, M. 1995a. Laboratory-induced development of the ice-ice disease of the farmed red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 7(6): 539–543.

Largo, D.B., Fukami, K. & Nishijima, T. 1995b. Occasional pathogenic bacteria promoting ice-ice disease in the carrageenan-producing red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 7(6): 545–554.

Largo, D.B., Fukami, K. & Nishijima, T. 1999. Time-dependent attachment mechanism of bacterial pathogen during ice-ice infection in Kappaphycus alvarezii (Gigartinales, Rhodophyta). Journal of Applied Phycology, 11(1): 129–136.

Lavilla-Pitogo, C.R. 1992. Agar-digesting bacteria associated with “rotten thallus syndrome” of Gracilaria sp. Aquaculture, 102(1–2): 1–7.

Lefebvre, S., Barillé, L. & Clerc, M. 2000. Pacific oyster (Crassostrea gigas) feeding responses to a fish-farm effluent. Aquaculture, 187(1–2): 185–198.

Li, F., Qin, S., Jiang, P., Wu, Y. & Zhang, W. 2009. The integrative expression of GUS gene driven by FCP promoter in the seaweed Laminaria japonica (Phaeophyta). Journal of Applied Phycology, 21(3): 287–293.

Li, H., Liu, J. & Pang. T. 2015. Callus induction and morphogenesis of callus in Kappaphycus alvarezii. Haiyang Xuebao, 37(4): 52–61.

Li, X., Zhang, Z., Qu, S., Liang, G., Sun, J., Zhao, N., Cui, C., et al. 2016. Improving seedless kelp (Saccharina japonica) during its domestication by hybridizing gametophytes and seedling-raising from sporophytes. Scientific Reports, 6(1): 1–9.

Liu, C., Wang, L., Wang, M. & Tang, X. 2002. Difference analysis of infection activity of alginic acid decomposing bacteria infecting Laminaria japonica. Marine Sciences, 26(6): 44–47.

Liu, J.G., Pang, T., Wang, L., Li, J. & Lin, W. 2009. The reasons causing catastrophic death in tropical carrageenan producing seaweeds and their difference in resistance to illness. Oceanology et Limnologia Sinica, 40(2): 235–241.

Liu, Q.Y., Chen, L.C.M. & Taylor, A.R.A. 1992. Ultrastructure of cell wall regeneration by isolated protoplasts of Palmaria palmata (Rhodophyta). Botanica Marina, 35(1): 21–34.

Liu, S., Pan, X., Wang, C. & Yue, H. 2003. Surveying and analysis of diseases of aquacultured species in Shandong. Transactions of Oceanology and Limnology/Haiyang Huzhao Tongbao, 97: 78–88.

Luhan, M.R.J. & Sollesta, H. 2010. Growing the reproductive cells (carpospores) of the seaweed, Kappaphycus striatum, in the laboratory until outplanting in the field and maturation to tetrasporophyte. Journal of Applied Phycology, 22(5): 579–585.

Lund, S. 1959. The marine algae of East Greenland. I. Taxonomic Part. Meddelser om Grønland, 156(1): 1–247.

Ma, Y., Yang, Z., Wan, L., Ge, M. & Zhang, K. 1998. Pathogenic bacteria of spot decay disease found in Undaria pinnatifida. Proceedings of International Symposium on Progress and Prospect of Marine Biotechnology (ISPPMB ’98). Qingdao, China. pp. 356–360.

Ma, Y., Zhang, Z., Fan, C. & Cao, S. 1997a. Study on the pathogenic bacteria of spot decay disease of Undaria pinnatifida in Dalian. Journal of Fishery Sciences of China/Zhongguo Shuichan Kexue, 4: 62–65.

Ma, Y., Zhang, Z., Liu, C., Fan, C. & Cao, S. 1997b. Study on the pathogenic bacteria of green decay disease of Undaria pinnatifida in Dalian. Journal of Fishery Sciences of China/Zhongguo Shuichan Kexue, 4: 66–69.

Marinho, G.S., Holdt, S.L., Birkeland, M.J. & Angelidaki, I. 2015. Commercial cultivation and bioremediation potential of sugar kelp, Saccharina latissima, in Danish waters. Journal of Applied Phycology, 27(5): 1963–1973.

Martin, S. & Gattuso, J.P. 2009. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology, 15(8): 2089–2100.

Matos, J., Costa, S., Rodrigues, A., Pereira, R. & Sousa-Pinto, I. 2006. Experimental integrated aquaculture of fish and red seaweeds in Northern Portugal. Aquaculture, 252(1): 31–42.

Matsumoto, M., Kawashima, Y. & Fukui, E. 1995. Transduction of high temperature-tolerant to Porphyra by cell fusion. Kaiyo Monthly, 27: 677–682.

Matsumura, W., Yasui, H. & Yamamoto, H. 2000. Mariculture of Laminaria japonica (Laminariales, Phaeophyceae) using protoplast regeneration. Phycology Research, 48(3): 169–176.

Metaxa, E., Deviller, G., Pagand, P., Alliaume, C., Casellas, C. & Blancheton, J.P. 2006. High rate algal pond treatment for water reuse in a marine fish recirculation system: water purification and fish health. Aquaculture, 252(1): 92–101.

Mikami, K. 2013. Current advances in seaweed transformation. In G.R. Baptista, ed. An integrated view of the molecular recognition and toxinology: from analytical procedures to biomedical applications, pp. 323–347. Rijeka, Croatia, InTech.

Mikami, K., Hirata, R., Takahashi, M., Toshiki Uji, T. & Saga, N. 2011. Transient transformation of red algal cells: breakthrough toward genetic transformation of marine crop Porphyra Species. In M.A. Alvarez, ed. Genetic Transformation, pp. 241–258. Rijeka, Croatia, InTech.

Mikami, K., Uji, T., Li, L., Takahashi, M., Yasui, H. & Saga, N. 2009. Visualization of phosphoinositides via the development of the transient expression system of a cyan fluorescent protein in the red alga Porphyra yezoensis. Marine Biotechnology, 11(5): 563–569.

Millner, P.A., Callow, M.E. & Evans, L.V. 1979. Preparation of protoplasts from the green alga Enteromorpha intestinalis (L.). Planta, 147(2): 174–177.

Mizukami, Y., Hado, M., Kito, H., Kunimoto, M. & Murase, N. 2004. Reporter gene introduction and transient expression in protoplasts of Porphyra yezoensis. Journal of Applied Phycology, 16: 23–29.

Mizukami, Y., Okauchi, M., Kito, H., Ishimoto, S., Ishida, T. & Fuseya, M. 1995. Culture and development of electrically fused protoplasts from red marine algae, Porphyra yezoensis and P. suborbiculata. Aquaculture, 132(3–4): 361–367.

Msuya, F.E., Buriyo, A., Omar, I., Pascal, B., Narrain, K., Ravina, J.J.M., Mrabu, E. & Wakibia, J.G. 2014. Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) Region. Journal of Applied Phycology, 26(2): 699–705.

Muñoz, J., Cahue-López, A., Patiño, R. & Robledo, D. 2006. Use of plant growth regulators in micropropagation of Kappaphycus alvarezii (Doty) in airlift bioreactors. Journal of Applied Phycology, 18(2): 209.

Murphy, F., Devlin, G., Deverell, R. & McDonnell, K. 2013. Biofuel production in Ireland – an approach to 2020 targets with a focus on algal biomass. Energies, 6(12): 6391–6412.

Myers, A.A. 1974. Amphitholina cuniculus (Strebing), a little-known marine amphipod crustacean new to Ireland. Proceedings of the Royal Irish Academy. Section B: Biological, Geological, and Chemical Science, pp. 463–469. Dublin, Ireland, Royal Irish Academy.

Nakao, Y., Onohara, T., Matsubara, T., Fujita, Y. & Zenitani, B. 1972. Bacteriological studies on diseases of cultured laver – I. Green spot rotting-like deterioration of laver frond by bacteria in vitro. Bulletin of the Japanese Society of Scientific Fisheries, 38(6): 561–564.

Neori, A., Troell, M., Chopin, T., Yarish, C., Critchley, A. & Buschmann, A. 2007. The need for a balanced ecosystem approach to blue revolution aquaculture. Environment: Science and Policy for Sustainable Development, 49(3): 36–43.

Neves, F.A.S., Simioni, C., Bouzon, Z.L. & Hayashi, L. 2015. Effects of spindle inhibitors and phytoregulators on the micropropagation of Kappaphycus alvarezii (Rhodophyta, Gigartinales). Journal of Applied Phycology, 27(1): 437–445.

Nielsen, R. 1979. Culture studies on the type species of Acrochaete, Bolbocoleon and Entocladia (Chaetophoraceae, Chlorophyceae). Botaniska Notiser, 132: 441–449.

Nikolaeva, E.V., Usov, A.I., Sinitsyn, A.P. & Tambiev, A.H. 1999. Degradation of agarrophytic red algal cell wall components by new crude enzyme preparations. Journal of Applied Phycology 11(4): 385–389.

Norambuena, F., Hermon, K., Skrzypczyk, V., Emery, J.A., Sharon, Y., Beard, A. & Turchini, G.M. 2015. Algae in fish feed: performances and fatty acid metabolism in juvenile Atlantic salmon. PLoS ONE 10(4): e0124042.

Okauchi, M. & Mizukami, Y. 1999. Transient β-Glucuronidase (GUS) gene expression under control of CaMV 35S promoter in Porphyra tenera (Rhodophyta). Bulletin of National Research Institute of Aquaculture, 4(Suppl): 13–18.

Pang, T., Liu, J., Liu, Q. & Lin, W. 2011. Changes of photosynthetic behaviors in Kappaphycus alvarezii infected by epiphyte. Evidence-based Complementary and Alternative Medicine, 2011: 658906.

Pang, T., Liu, J., Lin, Q. & Zhang, L. 2012. Impacts of glyphosate on photosynthetic behaviors in Kappaphycus alvarezii and Neosiphonia savatieri detected by JIP-test. Journal of Applied Phycology, 24(3): 467–473.

Pang, T., Liu, J., Qian Liu, Q., Li, H. & Li, J. 2015. Observations on pests and diseases affecting a eucheumatoid farm in China. Journal of Applied Phycology, 27(5): 1975–1984.

Paravano, L. 2015. Myths and genuine opportunities in seaweed industries, the Gracilaria case. Third Indonesia Seaweed Forum, Makassar, Indonesia. 12–14 November 2015.

Park, T.S., Rho, Y.G., Gong, Y.G. & Lee, D.Y. 1990. A harpacticoid copepod parasitic in the cultivated brown alga Undaria pinnatifida in Korea. Journal of the Korean Fisheries Society, 23: 439–442.

Parker, H.S. 1974. The culture of the red algal genus Eucheuma in the Philippines. Aquaculture, 3(4): 425–439.

Patwary, M.U. & van der Meer, J.P. 1982. Genetics of Gracilaria tikvahiae (Rhodophyceae). VIII. Phenotypic and genetic characterization of some selected morphological mutants. Canadian Journal of Botany, 60(12): 2556–2564.

Patwary, M.U. & van der Meer, J.P. 1983. Genetics of Gracilaria tikvahiae (Rhodophyceae) IX: Some properties of agars extracted from morphological mutants. Botanica Marina, 26(6): 295–300.

Pedersen, PM. 1976. Marine, benthic algae from southernmost Greenland. Meddelelser om Grønland, 199: 1–80.

Peters, A.F. 2003. Molecular identification, taxonomy and distribution of brown algal endophytes, with emphasis on species from Antarctica. Proceedings of the International Seaweed Symposium, 17: 293–302.

Peters, A.F. & Ellertsdottir, E. 1996. New record of the kelp endophyte Laminarionema elsbetiae (Phaeophyceae, Ectocarpales) at Helgoland and its life history in culture. Nova Hedwigia, 62: 341–349.

Phap, T.T. & Thuan, L.T.N. 2002. Tam Giang Lagoon aquatic systems health assessment. In J.R. Arthur, M.J. Phillips, R.P. Subasinghe, M.B. Reantaso, & I.H. MacRae, eds. Primary aquatic animal health care in rural, small-scale, aquaculture development, pp. 225–234. FAO Fisheries Technical Paper No. 406.

Phillipsen, A., Wild, M. & Verchick, A. 2014. Energy input, carbon intensity and cost for ethanol produced from farmed seaweed. Renewable and Sustainable Energy Review, 38: 609–623.

Polne-Fuller, M. & Gibor, A. 1987. Calluses and callus-like growth in seaweeds: induction and culture. Hydrobiologia, 151/152: 131–138.

Polne-Fuller, M., Rogerson, A., Amano, H. & Gibor, A. 1990. Digestion of seaweeds by the marine amoeba Trichosphaerium. Hydrobiologia, 204(1): 409–413.

Porse, H. & Rudolph, B. 2017. The seaweed hydrocolloids industry: 2016 updates, needs and outlook. Journal of Applied Phycology, 29: 2187–2200.

Potin, P., Bouarab, K., Küpper, F. & Kloareg, B. 1999. Oligosaccharide recognition signals and defence reactions in marine plant-microbe interactions. Current Opinion in Microbiology, 2(3): 276–283.

Potin, P., Bouarab, K., Salaun, J.P., Pohnert, G. & Kloareg, B. 2002. Biotic interactions of marine algae. Current Opinion in Plant Biology, 5(4): 308–317.

Putro, S.P., Widowati, W., Suhartana, S. & Muhammad, F. 2015. The application of integrated multi-trophic aquaculture (IMTA) using stratified double net rounded cage (SDFNC) for aquaculture sustainability. International Journal of Scientific Engineering, 9(2): 85–89.

Qin, S., Jiang, P., Li, X., Wang, X. & Zeng, C. 1998. A transformation model for Laminaria japonica (Phaeophyta, Laminariales). Chinese Journal of Oceanology and Limnology, 16(Suppl_1): 50–55.

Radulovich, R., Amir Neori, A., Valderrama, D., Reddy, C.R.K., Cronin, H. & Forster, J. 2015. Farming of seaweeds. In B.K. Tiwari & D.J. Troy, eds. Seaweed sustainability: food and nonfood applications, pp. 27–59. Elselvier.

Reddy, C.R.K. & Fujita, Y. 1989. Protoplast isolation and fusion of Ulva pertusa and U. conglobata. In S. Miyachi, I. Karube & Y. Ishida, eds. Current topics in marine biotechnology, pp. 235–238. Tokyo, Japan, Japan Society of Marine Biotechnology.

Reddy, C.R.K., Iima, M. & Fujita, Y. 1992. Induction of fast growing and morphologically different strains through intergeneric protoplasts fusion of Ulva and Enteromorpha (Ulvales, chlorophyta). Journal of Applied Phycology, 4(1): 57.

Reddy, C.R.K., Migita, S. & Fujita, Y. 1989. Protoplasts isolation and regeneration of three species of Ulva in axenic culture. Botanica Marina, 32: 483–490.

Reddy, C.R.K., Dipakkore, S., Rajakrishan Kumar, G., Jha, B., Cheney, D.P. & Fujita, Y. 2006. An improved enzyme preparation for rapid mass production of protoplast as seed stock for aquaculture of macrophytic marine green algae. Aquaculture, 260(1–4): 290–297.

Rheinheimer, G. 1992. Aquatic microbiology. Chichester, UK, John Wiley & Sons. 363 pp.

Rho, Y.G., Gong, Y.G., Lee, D.Y., Cho, Y.C. & Jang, J.W. 1993. On the parasitic copepod (Harpacticoida) in the cultivated brown alga, Undaria pinnatifida (Harvey) Suringar. Bulletin of National Fisheries Research and Development Institute (Korea), 47: 197–210.

Ridler, N., Barrington, K., Robinson, B., Wowchuk, M., Chopin, T., Robinson, S., Page, F., et al. 2007. Integrated multi-trophic aquaculture. Canadian project combines salmon, mussels, kelps. Global Aquaculture Advocate, 10: 52–55.

Roberts, T. & Upham, P. 2012. Prospects for the use of macro-algae for fuel in Ireland and the UK: an overview of marine management issues. Journal of Marine Policy, 36(5): 1047–1053.

Robertson-Anderson, D.V., Potgieter, M., Hansen, J., Bolton, J.J., Troell, M., Anderson, R.J., Halling, C. & Probyn, T. 2008. Integrated seaweed cultivation on an abalone farm in South Africa. Journal of Applied Phycology, 20(5): 579–595.

Rodgers, S.K. & Cox, E.F. 1999. Rate of spread of introduced rhodophytes Kappaphycus alvarezii, Kappaphycus striatum, and Gracilaria salicornia and their current distributions in Kaneohe Bay, Oahu, Hawaii. Pacific Science, 53(3): 232–241.

Roleda, M.Y., Morris, J.N., McGraw, C.M. & Hurd, C.L. 2012. Ocean acidification and seaweed reproduction: increased CO_2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Global Change Biology, 18(3): 854–864.

Rusing, A.M. & Cosson, J. 2001. Plant regeneration from protoplasts of Enteromorpha intestinalis (Chlorophyta, Ulvaphyceae) as seedstock for macroalgal culture. Journal of Applied Phycology, 13(2): 103–108.

Saga, N. 1984. Isolation of protoplasts from edible seaweeds. Botany Magazine of Tokyo, 97(3): 423–427.

Saga, N. & Sakai, Y. 1984. Isolation of protoplast from Laminaria and Porphyra. Nippon Suisan Gakkaishi, 50(6): 1085.

Saga, N., Polne-Fuller, M. & Gibor, A. 1986. Protoplasts from seaweeds: production and fusion. Beih Nova Hedwigia, 83: 37–43.

Salvador, R.C. & Serrano, A.E. 2005. Isolation of protoplasts from tissue fragments of Philippine cultivars of Kappaphycus alvarezii (Solieriaceae, Rhodophyta). Journal of Applied Phycology, 17(1): 15–22.

Sanderson, J.C. 2015. Maximizing production of Palmaria palmata (Linnaeus) Weber & Mohr, 1805. Final report to MASTS under visiting fellowship scheme.

Santelices, B. 1992. Strain selection of clonal seaweeds. Progress in Phycological Research, 8: 86–115.

Sawabe, T. & Ezura, Y. 1996. Regeneration from Laminaria japonica Areschoug (Laminariales, Phaeophyceae) protoplasts isolated with bacterial alginase. Plant Cell Report, 15(12): 892–895.

Sawabe, T., Ezura, Y. & Kimura, T. 1993. Application of an alginate lyase from Alteromonas sp. for isolation of protoplasts from a brown algae Laminaria japonica. Bulletin of Japanese Society of Science and Fisheries, 59(4): 705–709.

Sawabe, T., Ezura, Y. & Yamamoto, H. 1997. Plant regeneration from protoplasts of Laminaria japonica Areschoug (Laminariales, Phaeophyceae) in a continuous-flow culture system. Plant Cell Report, 17(2): 109–112.

Schatz, S. 1984. Degradation of Laminaria saccharina by saprobic fungi. Mycologia, 76(3): 426–432.

Schenk, P.M., Thomas-Hall, S.R., Stephens, E., Marx, U.C., Mussgnug, J.H., Posten, C., Kruse, O. & Hankamer, B. 2008. Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Research, 1(1): 20–43.

Shan, T.S., Pang, S.J. & Gao, S.Q. 2013. Novel means for variety breeding and sporeling production in the brown seaweed Undaria pinnatifida (Phaeophyceae): crossing female gametophytes from parthenosporophytes with male gametophyte clones. Phycological Research, 61(2): 154–161.

Singh, D.V. 2007. Plant pathology (introductory plant pathology). 48 pp.

Skjermo, J., Aasen, I.M., Arff, J., Broch, O.J., Carvajal, A.K., Christie, H.C., Forbord, S.et al. 2014. A new Norwegian bioeconomy based on cultivation and processing of seaweeds: Opportunities and R&D needs. Trondheim, Norway, SINTEF Fisheries and Aquaculture.

Skår, C.K. & Mortensen, S. 2007. Fate of infectious salmon anaemia virus (ISAV) in experimentally challenged blue mussels Mytilus edulis. Diseases of Aquatic Organisms, 74(1): 1–6.

Smith, J.E., Hunter, C.L. & Smith, C.M. 2002. Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pacific Science, 56(3): 299–315.

Solis, M.J.L., Draeger, S. & Dela Cruz, T.E.E. 2010. Marine-derived fungi from Kappaphycus alvarezii and K. striatum as potential causative agents of ice-ice disease in farmed seaweeds. Botanica Marina, 53(6): 587–594.

Son, S.H., Ahn, J.W., Uji, T., Choi, D.W., Park, E.J., Hwang, M.S., Liu, J.R. et al. 2012. Development of a transient gene expression system using the heat shock protein 70 promoter in the red macroalga, Porphyra tenera. Journal of Applied Phycology, 24(1): 79–87.

Song, H.S. & Chung, G.H. 1988. Isolation and purification of protoplasts from Porphyra tenera thalli. Aquaculture, 1(1): 103–108.

Stanley, S.J. 1992. Observations on the seasonal occurrence of marine endophytic and parasitic fungi.Canadian Journal of Botany, 70(10): 2089–2096.

Stirling, H. & Okumus, I. 1995. Growth and production of mussels (Mytilus edulis L.) suspended at salmon and shellfish farms in two Scottish sea lochs. Aquaculture, 134(3–4): 193–210.

Sukiman, S., Rahman, F., Rohyani, I.S. & Akhyadi, H. 2014. Growth of seaweed Eucheuma cottonii in multi-trophic sea farming systems at Gerupuk Bay, Central Lombok, Indonesia. Bioscience, 6(1): 82–85.

Sulistiani, E., Soelistyowati, D.T., Alimuddin & Yani, S.A. 2012. Callus induction and filaments regeneration from callus of cottonii seaweed (Kappaphycus alvarezii (Doty) collected from Natuna Islands, Riao Island Province. Biotropia, 19(2): 103–114.

Sutherland, G.K. 1915. New marine phycomycetes. Transactions of the British Mycological Society, 5: 147–155

Sylvester, A.W. & Waaland, R. 1983. Cloning the red alga Gigartina exasperata for culture on artificial substrates. Aquaculture, 31(2–4): 305–318.

Takahashi, M., Uji, T., Saga, N. & Mikami, K. 2010. Isolation and regeneration of transiently transformed protoplasts from gametophytic blades of the marine red alga Porphyra yezoensis. Electronic Journal of Biotechnology, 13(2): 8–9.

Tang, Q., Fang, J., Zhang, J., Jiang, Z. & Liu, H. 2013. Impacts of multiple stressors on coastal ocean ecosystems and integrated multi-trophic aquaculture. Progress in Fisheries Science, 34(1): 1−11.

Tang, X.X., Wang, Y., Huang, J., Yang, Z. & Gong, X.Z. 2001. Action of reactive oxygen species in Laminaria japonica against infection by alginic acid decomposing bacteria. Acta Botanica Sinica, 43(12): 1303–1306.

Tatewaki, M. & Nagata, K. 1970. Surviving protoplasts in vitro and their development in Bryopsis. Journal of Phycology, 6(4): 401–403.

Tisera, W. & Naguit, M.R.A. 2009. Ice-ice disease occurrence in seaweed farms in Bais Bay, Negros Oriental and Zamboanga del Norte. The Threshold, 4: 1–16.

Titlyanov, E.A., Titlyanova, T.V., Kadel, P. & Luning, K. 2006a. Obtaining plantlets from apical meristem of the red alga Gelidium sp. Journal of Applied Phycology, 18(2): 167–174.

Titlyanov, E.A., Titlyanova, T.V., Kadel, P. & Luning, K. 2006b. New methods of obtaining plantlets and tetraspores from fragments and cell aggregates of meristematic and submeristematic tissue of the red alga Palmaria palmata. Journal of Experimental Marine Biology and Ecology, 339(1): 55–64.

Tokuda, H. & Kawashima, Y. 1988. Protoplast isolation and culture from a brown alga, Undaria pinnatifida. In T. Stadler, J. Mollion, M.C. Verdus, Y. Karamanos, H. Morvan & D. Christaen, eds. Algal Biotechnology, pp. 151–157. London, UK, Elsevier Applied Science.

Torney, F., Moeller, L., Scarpa, A. & Wang, K. 2007. Genetic engineering approaches to improve bioethanol production from maize. Current Opinion in Biotechnology, 18(3): 193–199.

Troell, M., Halling, C., Nilsson, A., Buschmann, A.H., Kautsky, N. & Kautsky, L. 1997. Integrated marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for reduced environmental impact and increased economic output. Aquaculture, 156(1–2): 45–61.

Tsiresy, G., Preux, J., Lavitra, T., Dubois, P., Lepoint, G. & Eeckhaut, I. 2016. Phenology of farmed seaweed Kappaphycus alvarezii infestation by the parasitic epiphyte Polysiphonia sp. in Madagascar. Journal of Applied Phycology, 28(5): 2903-2914.

Tsukidate, J. 1971. Microbiological studies of Porphyra plants. III. Abnormality of the growth of Porphyra plants by the disturbance of the bacterial flora accompanying the plant. Bulletin of the Nansei Regional Fisheries Research Laboratory, 4: 1–12.

Tsukidate, J. 1977. Microbiological studies of Porphyra plants 5. On the relation between bacteria and Porphyra diseases. Bulletin of the Nansei National Fisheries Research Institute, 10: 101–112.

Tsukidate, J. 1991. Seaweed disease. Fish health management in Asia-Pacific. Report on a regional study and workshop on fish disease and fish health management, pp. 397–408. Bangkok, Thailand, ADB/NACA.

Uchida, T. & Arima, S. 1992. Regeneration of protoplasts isolated from the sporophyte of Cladosiphon okamuranus Tokida (Chordariaceae, Phaeophyta). Japan Journal of Phycology, 40: 261–266.

Uchida, A., Yoshikawa, T., Ishida, Y. & Saga, N. 1992. Stable protoplasts isolation and its regeneration into thallus of the marine green alga Ulva pertusa. Nippon Suisan Gakkaishi, 58(1): 153–157.

Uji, T., Takahashi, M., Saga, N. & Mikami, K. 2010. Visualization of nuclear localization of transcription factors with cyan and green fluorescent proteins in the red alga Porphyra yezoensis. Marine Biotechnology, 12(2): 150–159.

Uppalapati, S.R. & Fujita, Y. 2002. A simple method for mass isolation of protoplasts from species of Monostroma, Enteromorpha and Ulva (Chlorophyta, Ulvales). Journal of Applied Phycology, 14(3): 165–168.

Uyenco, F.R., Saniel, L.S. & Gomez, E.D. 1977. Microbiology of diseased Eucheuma striatum Schmitz. Journal of Phycology, 13: 70.

Vairappan, C.S. 2006. Seasonal occurrences of epiphytic algae on the commercially cultivated red alga Kappaphycus alvarezii (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 18(3–5): 611–617.

Vairappan, C.S., Chung, C.S., Hurtado, A.Q., Msuya, F., Bleicher-L’Honneur, G. & Critchley, A.T. 2008. Distribution and malaise of epiphyte infection in major carrageenophyte-producing farms. Journal of Applied Phycology, 20(5): 477–483.

Vairappan, C.S., Suzuki, M., Motomura, T. & Ichimura, T. 2001. Pathogenic bacteria associated with lesions and thallus bleaching symptoms in the Japanese kelp Laminaria religiosa Miyabe (Laminariales, Phaeophyceae). Hydrobiologia, 445(1–3): 183–191.

Valderrama, D., Cai, J., Hishamunda, N. & Ridler, N. 2013. Social and economic dimensions of carrageenan seaweed farming. Fisheries and Aquaculture Technical Paper No. 580. Rome, FAO.

Valente, L.M.P., Gouveia, A., Rema, P., Matos, J., Gomes, E.F. & Pinto, I.S. 2006. Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture, 252(1): 85–91.

Van den Burg, S., Bikker, P., van Krimpen, M. & van Dujin, A.P. 2013. Economic feasibility of offshore seaweed production in the North Sea. Presentation at the Aquaculture Europe Conference. Trondheim, Norway.

Walker, A.B., Fournier, H.R., Neefus, C.D., Nardi, G.C. & Berlinsky, D.L. 2009. Partial replacement of fish meal with laver Porphyra spp. in diets for Atlantic cod. North American Journal of Aquaculture, 71(1): 39–45.

Wan, A.H.L., Soler-Vila, A., O’Keeffe, D., Casburn, P., Fitzgerald, R. & Johnson, M.P. 2016. The inclusion of Palmaria palmata macroalgae in Atlantic salmon (Salmo salar) diets: effects on growth, haematology, immunity and liver function. Journal of Applied Phycology. 28(5): 3091–3100.

Wang, L.Z. 1993. Hybridization of macroscopic red algae by somatic cell fusion. Master’s Thesis in Marine Biotechnology and Biology, Northeastern University, Boston, Massachusetts, USA.

Wang, J., Jiang, P., Cui, Y., Deng, X., Li, F., Liu, J. & Qin, S. 2010a. Genetic transformation in Kappaphycus alvarezii using micro-particle bombardment: a potential strategy for germplasm improvement. Aquaculture International, 18(6): 1027–1034.

Wang, J., Jiang, P., Cui, Y., Guan, X. & Qin, S. 2010b. Gene transfer into conchospores of Porphyra haitanensis (Bangiales, Rhodophyta) by glass bead agitation. Phycologia, 49(4): 355–360.

Wang, Q.K., Shi, C.L. & Ma, J.C. 1983. Isolation and cultivation of MLO associated with coiling-stunt disease of sea tangle. Acta Microbiologica Sinica, 23: 73–74.

Wang, Y., Tang, X., Yang, Z. & Yu, Z. 2006. Effect of alginic acid decomposing bacterium on the growth of Laminaria japonica (Phaeophyceae). Journal of Environmental Science China, 18(3): 543–551.

Watson, L. 2014. Profiting from seaweed farming. Paper presented at the Farmed Irish Seaweed: An Ocean Wonder Food? Limerick, Ireland, 18–19 November 2014.

Watson, L., O’Mahony, F., Edwards, M., Dring, M.L. & Werner, A. 2012. The economics of seaweed aquaculture in Ireland Laminaria digitata and Palmaria palmata. Paper presented at AQUA 2012, Global Aquaculture Securing our Future. Prague, Czech Republic, 1–5 September 2012.

Wei, N., Quarterman, J. & Jin, Y.S. 2013. Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends in Biotechnology, 31(2): 70–77.

Weinberger, F., Pohnert, G., Berndt, M-L., Bouarab, K., Kloareg, B. & Potin, P. 2005. Apoplastic oxidation of L-asparagine is involved in the control of the green algal endophyte Acrochaete operculata Correa & Nielsen by the red seaweed Chondrus crispus Stackhouse. Journal of Experimental Botany, 56(415): 1317–1326.

Wilke, T., Faulkner, S., Murphy, L., Kealy, L., Kraan, S. & Brouns, F. 2015. Seaweed enrichment of feed supplied to farm-raised Atlantic salmon (Salmo salar) is associated with higher total fatty acid and LC n-3 PUFA concentrations in fish flesh. European Journal of Lipid Science and Technology, 117(6): 767–772.

Wilson, I.M. & Knoyle, J.M. 1961. Three species of Didymosphaeria on marine algae: D. danica (Berlese) comb. nov., D. pelvetiana Suth. and D. fucicola Suth. Transactions of the British Mycological Society, 44(1): 55–71.

Wiltshire, K.H., Tanner, J.E., Gurgel, C.F.D. & Deveney, M.R. 2015. Feasibility study for integrated multitrophic aquaculture in southern Australia. Report to the Fisheries Research & Development Corporation. South Australian Research and Development Institute (Aquatic Sciences), Adelaide. SARDI Publication No. F2015/000786-1. SARDI Research Report Series No. 883.

Wu, C.Y., Dou, C. & Jiajun, L. 1983. On the diseases of cultivated Laminaria japonica. In C.K. Tseng, ed. Proceedings of the Joint China-U.S. Phycology Symposium, pp. 211–220. Beijing, China, Science Press.

Yamada, K., Yoshimizu, M., Ezura, Y. & Kimura, T. 1990. Distribution of Alteromonas sp., the redspot causative agent on the culture bed of makonbu Laminaria japonica, in coastal areas of Hokkaido. Bulletin of the Faculty of Fisheries, Hokkaido University, 41: 221–226.

Yamaguchi, K., Araki, T., Aoki, T., Tseng, C. & Kitamikado, M. 1989. Algal cell wall degrading enzymes from viscera of marine animals. Nippon Suisan Gakkaishi, 55: 105–110.

Yamazaki, A., Nakanishi, K. & Saga, N. 1998. Axenic tissue culture and morphogenesis in Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Phycology, 34(6): 1082–1087.

Yan, Z.M. 1984. Studies on tissue culture of Laminaria japonica and Undaria pinnatifida. Hydrobiologia, 116/117: 314–316.

Yan, X.H. & Wang, S.J. 1993. Regeneration of whole plants from Gracilaria asiatica Chang et Xia protoplasts (Gracilariaceae, Rhodophyta). Hydrobiologia, 260(1): 429–436.

Yeong, H.Y., Khalid, N. & Phang, S.M. 2008. Protoplast isolation and regeneration from Gracilaria changii (Gracilariales, Rhodophyta). Journal of Applied Phycology, 20: 641–651.

Yokoya, N.S., West, J.A. & Luchi, A.E. 2004. Effects of plant growth regulators on callus formation, growth and regeneration in axenic tissue culture of Gracilaria tenuistipitata and Gracilaria perplexa (Gracilariales, Rhodophyta). Phycological Research, 52(3): 244–254.

Yokoyama, H. 2013. Growth and food source of the sea cucumber Apostichopus japonicus cultured below fish cages – potential for integrated multi-trophic aquaculture. Aquaculture, 372–375: 28–38.

Yong, W.T.L., Ting, S.H., Yong, Y.S., Thien, V.Y., Wong, S.H., Chin, W.L., Rodrigues, K.F. & Anton, A. 2014. Optimization of culture conditions for the direct regeneration of Kappaphycus alvarezii (Rhodophyta, Solieriaceae). Journal of Applied Phycology, 26(3): 1597–1606.

Yoshida, T. & Akiyama, K. 1978. Streblonema (Phaeophyceae) infection in the frond of cultivated Undaria (Phaeophyceae). Proceedings of the International Seaweed Symposium, 9: 219–223.

Ystanes, L. & Fougner, M.W. 2012. Seaweed to biofuels – future perspectives by industry presented actor. Paper presented at the Seaweed to Biofuel Workshop, 25–26 September 2012.

Yu, D.Z., Qin, S., Sun, G.Q. & Tzeng, C.K. 2002. Transient expression of lacZ reporter gene in the economic seaweed Undaria pinnatifida. High Scientific Letters, 12(8): 93–95.

Yumoto, I., Ezura, Y. & Kimura, T. 1989a. Distribution of the Alteromonas sp., the causative agent of red-spots on the culture bed of makonbu, Laminaria japonica, in the coastal area of Funka Bay. Nippon Suisan Gakkaishi, 55(3): 453–462.

Yumoto, I., Yamaguchi, K., Yamada, K., Ezura, Y. & Kimura, T. 1989b. Relationship between bacterial flora and occurrence of the Alteromonas sp., the causative agent of red-spots on the culture bed of makonbu, Laminaria japonica, in the coastal area of Funka Bay. Nippon Suisan Gakkaishi, 55(11): 1907–1914

Yunque, D.A.T., Tibubos, K.R., Hurtado, A.Q. & Critchley, A. 2011. Optimization of culture conditions for tissue culture production of young plantlets of carrageenophyte Kappaphycus. Journal of Applied Phycology, 23(3): 433–438.

Zablackis, E., Vreeland, V. & Kloareg, B. 1993. Isolation of protoplasts of Kappaphycus alvarezii var. tambalang (Rhodophyta) and secretion of iota-carrageenan fragments by cultured cells. Journal of Experimental Botany, 44(9): 1515–1522.

Zhang, D. 1983. Study on the protoplasts preparation, culture and fusion of somatic cells from two species of green algae Ulva linza and Monostroma angicava Kjellm. Journal of Shandong College of Oceanology, 13: 57–65.

Zhang, J. 1982. Some experiments and observations on the tissue and cell cultured of Undaria pinnatifida. Journal of Shandong College of Oceanology, 12: 29–38.

Zhang, Y.C., Jiang, P., Gao, J.T., Liao, J.M., Sun, S.J., Shen, Z.L. & Qin, S. 2008. Recombinant expression of rt-PA gene (encoding Reteplase) in gametophytes of the seaweed Laminaria japonica (Laminariales, Phaeophyta). Sciencia China Series, 51(12): 1116–1120.

Zhang Z.H., Lu, J.B., Ye, S.F. & Zhu, M.Y. 2007. Values of marine ecosystem services in Sanggou Bay. China Journal of Applied Ecology, 18(11): 2540–2547.

Zitta, C.S., Rover, T., Hayashi, L., Zenilda, L. & Bouzon, Z.L. 2013. Callus ontogeny of the Kappaphycus alvarezii (Rhodophyta, Gigartinales) brown tetrasporophyte strain. Journal of Applied Phycology, 25(2): 615–629.

Websites:

Acadian Seaplants. 2021. Acadian Seaplants [online]. Dartmouth. [Cited 20/4/2021]. https://www.acadianseaplants.com/sustainable-seaweed-company/

AlgaeBase. 1996. AlgaeBase [online]. Galway. [Cited 20/4/2021]. https://www.algaebase.org/

C-Weed Aquaculture. 2016. C-Weed Aquaculture [online]. Saint Méloir des Ondes. [Cited 20/4/2021]. https://www.c-weed-aquaculture.com/en/

The Fish Site. 2021. The Fish Site [online]. Cork. [Cited 20/4/2021]. https://www.thefishsite.com/