Review
Algae 2017, 32(1): 1-13
https://doi.org/10.4490/algae.2017.32.3.3
Open Access
Seaweed aquaculture: cultivation technologies, challenges and its
ecosystem services
Jang K. Kim1,2, Charles Yarish3,*, Eun Kyoung Hwang4, Miseon Park5 and Youngdae Kim5
1
Department of Marine Science, School of Natural Sciences, Incheon National University, Incheon 22012, Korea
Department of Marine Sciences, University of Connecticut, 1 University Place, Stamford, CT 06901, USA
3
Department of Ecology & Evolutionary Biology, University of Connecticut, 1 University Place, Stamford, CT 06901, USA
4
Seaweed Research Center, National Institute of Fisheries Science, Mokpo 58746, Korea
5
Southeast Sea Fisheries Research Institute, National Institute of Fisheries Science, Tongyeong 46083, Korea
2
Seaweed aquaculture technologies have developed dramatically over the past 70 years mostly in Asia and more recently in Americas and Europe. However, there are still many challenges to overcome with respect to the science and to social
acceptability. The challenges include the development of strains with thermo-tolerance, disease resistance, fast growth,
high concentration of desired molecules, the reduction of fouling organisms and the development of more robust and
cost efficient farm systems that can withstand storm events in offshore environments. It is also important to note that
seaweed aquaculture provides ecosystem services, which improve conditions of the coastal waters for the benefit of other
living organisms and the environment. The ecosystem services role of seaweed aquaculture and its economic value will
also be quantitatively estimated in this review.
Key Words: ecosystem services; Eucheuma; Gracilaria / Gracilariopsis; Kappaphycus; kelp; Pyropia / Porphyra; Sargassum; seaweed aquaculture
INTRODUCTION
According to an archaeological study, cooked and partially eaten seaweeds have been found at a 14,000-yearold site in southern Chile, suggesting seaweed have been
part of the human diet in the Western Hemisphere for
a very long time (Dillehay et al. 2008). In the past four
hundred years, seaweeds have been an important part
in Asian cuisine more so than in western cultures. Global
seaweed aquaculture production occupies approximately 20% of the total world marine aquaculture production
by weight, with an annual value of US $6.7 billion in 2013
(Bjerregaard et al. 2016, Cottier-Cook et al. 2016, FAO
2017). Most production occurs in Asia. Seaweed aquacul-
ture production is dominated (>81% of total production)
by relatively few species: the brown kelps, Saccharina japonica and Undaria pinnatifida; and the red seaweeds
including Pyropia / Porphyra spp. (‘nori’ in Japanese or
‘gim’ in Korean), Kappaphycus alvarezii and Eucheuma
striatum (carrageenophytes) and Gracilaria / Gracilariopsis spp. (agarophytes).
Currently 54,000 tons of seaweed are cultivated in the
Americas and Europe with an annual value of US $51
million in 2014 (FAO 2017), which is less than the value
of seaweed products that Korea exported to the United
States during the same period (US $67 million) (Meekyi-
This is an Open Access article distributed under the
terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which
permits unrestricted non-commercial use, distribution, and reproduction
in any medium, provided the original work is properly cited.
Received December 13, 2016, Accepted March 3, 2017
Copyright © 2017 The Korean Society of Phycology
*Corresponding Author
E-mail: charles.yarish@uconn.edu
Tel: +1-203-251-8432, Fax: +1-203-251-8592
1
http://e-algae.org pISSN: 1226-2617 eISSN: 2093-0860
Algae 2017, 32(1): 1-13
ung Kim, Korea Agro-Trade Center personal communication). Although seaweed aquaculture is a relatively new
industry in North America and Europe, the demand by
western markets is expected to increase rapidly due to
consumer desire for new protein sources and healthy
food supplements, plus food industry’s interest in sustainable textural additives and food security.
Seaweed aquaculture technologies have developed
dramatically in Asia, but there are still many challenges
to overcome. These challenges vary for different species
and in different countries. In this study, we will discuss
the challenges to seaweed cultivation of major aquacultured species. Seaweed aquaculture also provides ecosystem services through nutrient removal upon harvest. This
ecosystem services role by seaweed aquaculture will also
be addressed in this study.
and some Korean and Japanese farms use desiccation
control methods by exposing the Pyropia / Porphyra nets
to the air to kill epiphytes and competing organisms (e.g.,
Ulva spp.), while most Korean and Japanese farmers prefer to use a pH control method by applying organic acids
onto the nets (Pereira and Yarish 2010, Kim et al. 2014a)
but this is a costly approach. There are no additional (or
minimal) costs using the desiccation method and this
method may even increase the protein content in tissue
(Kim et al. 2013b). However, the desiccation method is
not as efficient as the pH control method. Uncontrolled
fouling organisms reduce the quality of production. Recent reports even suggest that the source of the world
largest macroalgal blooms originated from Ulva grown
on the rafts of Pyropia farms in the Southern Yellow Sea
of China (Liu et al. 2009, Hu et al. 2010, Zhang et al. 2014,
2016, Huo et al. 2016).
Pyropia / Porphyra has been cultivated in the western
countries since 1980s; however, production has had limited success. In 1994, the first commercial attempt to cultivate Pyropia yezoensis (‘Porphyra’) in open water in the
State of Maine (Chopin et al. 1999, McVey et al. 2002) was
unsuccessfully attempted by Coastal Plantations International (later incorporated into PhycoGen, Inc., Portland,
ME, USA). The aquaculture site had insufficient nutrients to support vigorous growth of Py. yezoensis. In 1996,
this company moved its nori nets adjacent to an Atlantic
salmon (Salmo salar) farm at the Connors Aquaculture
Inc. facilities (Deep Cove, Eastport, ME, USA). This open
water cultivation was successful and ultimately lead to
the development of Integrated Multi-Trophic Aquaculture (IMTA). However, PhycoGen, Inc., went bankrupt
due to the downturn in the investment environment.
More recently, Porphyra umbilicalis cultivation is in process in Maine by Brawley and her colleagues (Blouin et al.
2011, Brawley, University of Maine, personal communication). A cultivation manual has also been published for
seedstock production of Pyropia / Porphyra in the United
States (Redmond et al. 2014a) with accompanying videos
in English and Spanish. These efforts reflect that the western countries are interested in Pyropia / Porphyra cultivation. However, Pyropia / Porphyra cultivation is still in
its nascent stage in the western countries, and there currently are no commercial Pyropia / Porphyra growers in
the United States. Therefore, it is critical to develop local
cultivars and cultivation techniques suitable for the local
environments and boutique markets. Selective (intraspecific and inter-specific) breeding of cultivated Pyropia
/ Porphyra has been intensively studied in Asia (Miura
1984, Shin 1999, 2003, Niwa et al. 2009). Genetic improve-
CULTIVATION TECHNOLOGIES AND CHALLENGES IN MAJOR AQUACULTURED SPECIES
Pyropia / Porphyra (‘nori’ or ‘gim’)
Pyropia / Porphyra has been cultivated for the past
several hundred years in Japan and has become one of
the most successful aquaculture industries in Japan, Korea, and China (Mumford and Miura 1988, Pereira and
Yarish 2008). Its current annual value is nearly $0.95 billion (FAO 2017). Pyropia / Porphyra has the highest commercial value per unit mass ($523 per wet metric ton) in
comparison to other aquacultured species, kelp, $141
per wet ton; Gracilaria, $273 per wet ton; Kappaphycus
/ Eucheuma, $172 per wet ton; and Sargassum, $460 per
wet ton (FAO 2017). Although total 138 species of Pyropia
and Porphyra are currently accepted taxonomically (Guiry and Guiry 2016), only 3 major species (Py. yezoensis,
Py. tenera, and Py. haitanensis) have been commercially
cultivated, mostly in China, Korea, and Japan (99.99%
of total production) (FAO 2017). The culture methods of
Pyropia / Porphyra in these three countries are basically
similar, with minor modifications (see Sahoo and Yarish
2005, Pereira and Yarish 2008, 2010, Pereira et al. 2013 for
more details). For example, some farmers use free-living
conchocelis for seeding while others use conchocelis on
oyster shells (He and Yarish 2006, He et al. 2008). Seedlings may be outplanted in the open water farms using
one of three cultivation methods: fixed pole, semifloating
raft, or floating raft (see Sahoo and Yarish 2005 for details). The epiphyte control techniques are also different
based on the cultivation techniques. Most Chinese farms,
https://doi.org/10.4490/algae.2017.32.3.3
2
Kim et al. Seaweed Aquaculture
ment has developed superior strains with higher growth
capacity, better flavor, darker color and higher tolerance
to diseases (Chen et al. 2015).
The effects of climate change may be an incentive to
do more research in genetic manipulations. Recently,
National Aeronautics and Space Administration (NASA)
and National Oceanic and Atmospheric Administration
(NOAA) reported the year 2016 ranks as Earth’s warmest since 1880. The 17 warmest years on record, with the
exception of 1998, have occurred since 2000. Since 1880,
Earth’s average surface temperature has risen by about
1.1°C and the majority of that warming has occurred in
the past three decades (NASA 2017). Therefore, development of new strains with high thermo-tolerances will be a
must for the development of a sustainable seaweed aquaculture industry.
tank cultures (see Oliveira et al. 2000, Sahoo and Yarish
2005, Pereira and Yarish 2008 for more details). In any of
these methods, providing sustainable seedstock is critical.
Currently, most Gracilaria / Gracilariopsis seedstock has
been supplied from the wild (either collection of healthy
branches of Gracilaria / Gracilariopsis from natural stock
or selection of reproductive plants to collect spores (either carpospores or tetraspores) for seeding (Buschmann
et al. 2008a). Dependence on natural stocks may cause
some serious problems including physiological variations (e.g., growth, agar content, etc.) in the seedstock.
Adequate measures should be taken to protect natural
stocks of Gracilaria / Gracilariopsis from over-exploitation of donor populations. Another methodology that
could be used is nursery (tank culture) systems to provide sufficient seedstock through vegetative propagation
(Hanisak 1987, Abreu et al. 2011a, 2011b, Kim and Yarish
2014). One important advantage of tank cultivation is the
ease of controlling the culture system (Abreu et al. 2011b,
Pereira et al. 2013). This ensures that production meets
high quality standards and biosafety for human consumption and other high value production applications
for the cosmeceutical and pharmaceutical industries. A
limitation for tank culture, however, is high management
costs (Hanisak and Ryther 1984, Caines et al. 2014). Recently, Abreu et al. (2011b) have used tank cultivation to
mitigate fish effluent, therefore reducing the production
costs. Kim and Yarish (2014) has also suggested other cost
efficient resources, such as injecting CO2 and using commercial fertilizers. The use of LED lighting could further
reduce tank cultivation costs (Kim et al. 2015c). There was
an intensive study on genetics, mutation, selective breeding and even genetic engineering in Gracilaria / Gracilariopsis by van der Meer and his collaborators a few dacades
ago (see Patwary and van der Meer 1992 and references
therein). More recently in Chile, strains of Gracilaria
chilensis were established and maintained without sexual reproduction. These strains are homogeneous clonal
cultures (Buschmann et al. 2008a, Guillemin et al. 2008,
Robinson et al. 2013), which can be more susceptible
to diseases outbreaks and environmental changes. The
quality of wild Gracilaria / Gracilariopsis in recent years
has been diminished due to declines in the cultivation
environments and increase in diseases (Alamsjah 2010).
Using asexually derived branches may lead to a reduction
in genetic variability but more work needs to be done on
the population genetics of these taxa.
Therefore, the technology development combining hybridization, genetic material establishment while maintaining genetic diversity will become very important in
Gracilaria / Gracilariopsis
The red algae Gracilaria / Gracilariopsis are two of the
world’s most cultivated seaweeds with over 3.8 million
tons of annual production and worth annually about
US $1 billion (FAO 2017). Gracilaria / Gracilariopsis have
been mostly cultivated in two Asian countries (China 70%
and Indonesia 28% of global production). In the Americas, Chile is the most productive country, producing
more than 12.8 tons per year with an annual value of US
$29 million (FAO 2017). Most of the biomass is used in the
phycocolloid industry as the main source of food grade
agar (Pereira and Yarish 2008) and as an animal feed (Qi
et al. 2010, Johnson et al. 2014). Gracilaria / Gracilariopsis
contribute approximately 66% of the total agar production (Pereira and Yarish 2008). Currently 185 Gracilaria
and 24 Gracilariopsis species are accepted taxonomically (Guiry and Guiry 2016). Gracilaria / Gracilariopsis
include warm temperate to subtropical eurythermal species. These species are easy to propagate (asexually and
sexually), and have relatively high growth rates (Abreu et
al. 2011a, Kim and Yarish 2014, Kim et al. 2015c, 2016, Wu
et al. 2015, Gorman et al. 2017). Gracilaria / Gracilariopsis are also euryhaline species, which can tolerate a wide
range of salinities, from about 10-40 psu, though they
grow best in ranges of 25-33 psu (Yokoya et al. 1999, Weinberger et al. 2008, Kim et al. 2016, Gorman et al. 2017).
They can survive temperature ranges from 0-35°C but
have an optimal range of 20-28°C (Yokoya et al. 1999, Raikar et al. 2001, Abreu et al. 2011a, Kim et al. 2016).
Gracilaria / Gracilariopsis have been cultivated mainly
in four different ways, including open water rope cultivation, near shore bottom cultivation, pond culture and
3
http://e-algae.org
Algae 2017, 32(1): 1-13
Gracilaria / Gracilariopsis aquaculture. Another challenge
in Gracilaria / Gracilariopsis aquaculture is to develop
technologies and strategies to reduce fouling problems.
Fouling organisms (e.g., epiphytes, tunicates, hydroids,
etc.) have been observed at Gracilaria farms in Long Island Sound (CT), Bronx River estuary (NY), and Waquoit
Bay (MA) (Kim et al. 2014b, Lindell et al. 2015). A few successful solutions to these problems include fresh water
rinses, the use of tank grown fresh Gracilaria seedstock,
determination of optimal stocking density and photon
fluence levels. However, more studies are needed for sustainable production and to understand the genetic variability of the seedstocks.
pearance of white segments on the thalli, causing them
to break (Largo et al. 1995, Ask and Azana 2002, Vairappan et al. 2009). It is still unknown what vector causes
this disease, but a bacterial or viral infection, and / or
physical stresses have been suggested as the potential
sources (Vairappan et al. 2009). Farmers also need to remove epiphytes 2-3 times each and every week, which
requires intensive labor (Hurtado et al. 2006). Therefore,
it is extremely important to develop new strains that are
light and thermally tolerant and disease resistant. More
efficient epiphyte control also needs to be developed. In
addition, storm damage due to typhoons is problematic
in tropical regions where cultivation occurs. The simplest solution to minimize storm damage is the removal
of all cultivation systems prior to the typhoon season (~3
months per year). Development of more robust and cost
efficient farm systems are needed especially in the offshore environment.
Kappaphycus and Eucheuma
The red algae Kappaphycus and Eucheuma, major
sources of carrageenan, account for over 80% of world’s
carrageenan production (Pereira and Yarish 2008, Hayashi et al. 2010). Approximately 10.75 million tons of these
species were produced worth over US $1.9 billion in 2014
(FAO 2017). Kappaphycus and Eucheuma have been cultivated mostly in Indonesia (over 9.0 million tons, over 83%
of global production, mostly Eucheuma), followed by the
Philippines (nearly 1.4 million tons, 13% of global production, mostly Kappaphycus). Approximately 340,000
tons of these carrageenophytes were also cultivated in
Malaysia, Cambodia / Vietnam, China, Tanzania / Madagascar, Belize and Brazil (Valderrama et al. 2015, Bjerregaard et al. 2016, FAO 2017).
Of six species taxonomically accepted as Kappaphycus
and 30 Eucheuma species, Kappaphycus alvarezii and Eucheuma denticulatum are most often cultivated. Both of
these taxa are cultivated using the same methodologies
including the fixed, off-bottom line method, the floating raft method and basket method (see Ask and Azanza 2002, Pereira and Yarish 2008, Hayashi et al. 2010 for
more details). The steps in the farming of these genera
include 1) site selection, 2) selection of cultivation methodology, 3) farm maintenance, and 4) harvesting and drying. Among these steps, site selection is most important
due to the herbivory of siganids (rabbitfish) and puffers.
Turtles are also problematic because they take large bites
and also crawl through a farm, causing physical damage
to the farm systems. Long-spined sea urchins may also be
a pest and can cause injuries to the farmers as they try
to remove them. There is no simple solution except moving to another site where these animals are not prevalent.
Diseases are also a challenge. The most common disease
of the euchemoid spp. is called “ice-ice” because the ap-
https://doi.org/10.4490/algae.2017.32.3.3
Kelp (Saccharina and Undaria)
Over 8.0 million tons of kelp were cultivated and harvested in 2014 with a value of about US $1.4 billion annual values (FAO 2017). Nearly all kelp production occurred
in Asia: China 88.3%; Korea (south) 6.6%; and Korea
(north) 4.4% (FAO 2017). Kelp has been utilized mostly
for human consumption, but recently, it also has been
increasingly utilized as abalone feed due to low production costs (Hwang et al. 2012, 2013). Since the early part
of this decade, Undaria and Saccharina production have
continuously increased due to demand for abalone feeds
in Korea (Hwang et al. 2012). Over 60% of total production of Saccharina and Undaria was used in the abalone
industry in 2012 (Hwang et al. 2012).
In Western countries, kelp species (primarily the sugar
kelp, Saccharina latissima and winged kelp, Alaria esculenta) have been cultivated during the last two decades in
the North Atlantic Ocean (e.g., the United States, Canada,
Iceland, Norway, Scotland, Ireland, Sweden, and Germany, etc.) (Buck and Buchholz 2004, Barrington et al. 2009,
Broch et al. 2013, Kraemer et al. 2014, Kim et al. 2015b,
Marinho et al. 2015) and Macrocystis, Saccharina latissima, and Alaria esculenta in the eastern Pacific Ocean
(e.g., Chile: Buschmann et al. 2008b, 2014, Camus et al.
2016, Correa et al. 2016, Valero et al. 2017; Alaska: Stekoll
and Peeples 2016). The kelp aquaculture industry in the
western countries has become one of the fastest growing
industries (Cottier-Cook et al. 2016).
For both Saccharina and Undaria, cultivation begins
with zoospores (meiospores) for seeding. The seeding
4
Kim et al. Seaweed Aquaculture
methods are a bit different between Asia (use of seed
frames) and the West (use of seedspools) (Pereria and Yarish 2008, Redmond et al. 2014a) mainly due to the nursery
capacities and the scale of operations of the open water
farms. However, the open water cultivation techniques
using longlines are very similar. Once the seedstring is
outplanted at open water farms the kelp thalli will grow
up to 2-5 m in length, but sometimes may grow up to 10
m (see Pereira and Yarish 2008, Redmond et al. 2014a,
SINTEF 2014 for details).
Dealing with climate change will be a challenge for
cultivation of cool temperate species of kelp (Park et al.
2017). Efforts to develop strains of kelp with traits of fast
growth, disease resistance and high temperature tolerance are needed. Selective breeding and intensive selection of kelp strains in Asia, however, have reduced the genetic diversity and narrowed the germplasm base of the
varieties in cultivation (Kawashima and Tokuda 1993, Li
et al. 2007, 2016, Robinson et al. 2013), therefore jeopardizing the industry expansion in Asia.
In the United States, Canada and Europe, strain development will be a challenge. Meiospore “seeds” (zoospores) have relied mostly on natural populations. Development of “seedbanks” for the kelp species will provide a
sustainable and reliable source of seedstock without impacting the natural beds of the kelp. Having the seaweeds
with desirable morphological and physiological traits will
also enhance production capacity of the seaweed industry. Another challenge in these countries is permitting
and the social syndrome known as NIMBY (“Not In My
Back Yard”) reactions. For example, in the United States
at least 120 federal laws were identified that affect aquaculture either directly (50 laws) or indirectly (70 laws) and
more than 1,200 state statutes regulate aquaculture in 32
states (Getchis et al. 2008). Regulatory complexity is further increased when towns or counties are given jurisdiction over local waters. Social resistance has also been major factor limiting the growth of aquaculture in the United
States (Getchis et al. 2008). The nearshore waters of the
United States are heavily used, having both recreational
(boating, fishing, swimming) and aesthetic (ocean and
bay views from waterfront homes) values. Due to this reason, offshore cultivation has been suggested as an alternative to avoid stakeholder conflicts (Langan and Horton
2005, Rensel et al. 2011).
Recently, the U.S. Department of Energy’s Advanced
Research Projects Agency-Energy (ARPA-E) has expressed
interest in offshore seaweed aquaculture for the production of feeds, fuels and chemicals. The potential species
discussed include Saccharina in the Northeast (Western
Atlantic Ocean), Northwest (eastern Pacific Ocean of
Washington and Alaska) and Sargassum spp. in the Gulf of
Mexico and Caribbean. To achieve success in these ventures, technology development will be required, including breeding for suitable strain development, cultivation,
harvesting, transport, storage, processing, ecosystem services and product opportunities for long-term financial
viability of a United States-based macroalgae industry on
the path to biofuels. The nutrients for the growth of seaweeds may also be limited in the offshore environment.
To resolve this issue, site selection for cultivation will be
critical, such as in upwelling areas. The offshore seaweed
farms are unlikely to experience conflicts with other economic and recreational uses, which may result in fewer
restrictions on farm size and greater economies of scale.
Considering current cultivation techniques, the kelp will
be most the appropriate species to cultivate offshore due
to its low requirement for maintenance and harvest in
comparison to other aquacultured species. For example,
an endemic kelp phenotype, known as Saccharina latissima forma angustissima (F. S. Collins) A. Mathieson could
be an ideal candidate for the offshore cultivation. This
endemic form grows only at wave-impacted locations
in Maine (Mathieson et al. 2008, Augyte et al. in press).
Unlike the common Saccharina latissima plants, this endermic form grows very narrow (2-5 cm) and long (~5 m),
which is probably induced by hydrodynamic forces and
mechanical stress from breaking waves and strong currents (Fowler-Walker et al. 2006, Koehl et al. 2008). These
features will make Saccharina latissima forma angustissima more suiatable for the offshore cultivation.
Sargassum
Sargassum is the most common brown macroalgae
found in temperate, tropical, and subtropical waters
worldwide. These seaweeds are adapted to many different oceanic environments with a wide variety of forms
and reproductive strategies (Guiry and Guiry 2016). Sargassum species have traditionally been utilized for food
and medicine in Asia. They continue to be wild harvested
and cultivated in Japan, China, and Korea, for human
consumption as sea vegetables and for use as a medicinal
“seaweed herbs.” Locally known as the “black vegetable”
in China, Sargassum is valued for its high nutritional
content and nutty flavor. It is added to salads, soups or
vegetable dishes (Xie et al. 2013). Sargassum is utilized in
Chinese medicine as an expectorant for bronchitis, and
to treat laryngitis, hypertension, infections, fever, and
goiter (Hou and Jin 2005). Sargassum fusiforme (formally
5
http://e-algae.org
Algae 2017, 32(1): 1-13
“Hizikia fusiformis”) cultivation was initiated in the early
1980s. Thus, the production and economic value is still
low, approximately 175,000 tons of production worth US
$80 million in 2014 (FAO 2017). Nearly all Sargassum is
produced in China. Although still low in production, its
commercial value per unit mass is very high (US $460 per
wet ton), which is the highest amongst the aquacultured
brown seaweeds. It is even comparable to Pyropia / Porphyra (US $523 per wet ton). Currently, several Sargassum
species are cultured in Asia, including S. thunbergii, S.
fulvellum, S. muticum, and S. horneri in China (Xie et al.
2013), and S. fusiforme and S. fulvellum in Korea (Hwang
et al. 2006a).
Traditional culture methods initially relied on the use
of wild seedlings collected from natural beds. Groups of
3-4 seedlings, 5-10 cm in length, were inserted into seeding rope at intervals of 5-10 cm. This smaller seeding line
was then attached to a main longline placed at depths of
2-3 m, and cultivated from November to May (Sohn 1998,
Hwang et al. 2006a, Redmond et al. 2014b). This dependence on wild seedlings resulted in overharvesting natural beds, so new culture methods were developed. Holdfast-derived seeding was the first step towards developing
culture techniques for Sargassum. This type of culture
takes advantage of the perennial nature of the holdfast,
allowing farmers to reuse the holdfasts from the previous
year’s crops (Hwang et al. 1998). While plants may still be
sourced from wild beds, the attached holdfasts can be reused for the next season’s crop by over-summering in the
sea after harvest until the next growing season. While this
allows for reuse of existing cultured plants, the resulting
harvestable biomass tends to diminish after each year.
Today, Sargassum lines are seeded with juvenile plants
obtained from reproductive adults. Obtaining seedlings
through sexual reproduction allows for mass production
of new plants for seeding, and results in higher biomass
yields (Hwang et al. 2006b, Peng et al. 2013, Redmond
et al. 2014b). Fertilized eggs are gathered from mature
fronds and “seeded” onto seedstring by allowing juveniles to attach to seed lines with newly forming rhizoids.
Once attached, seedlings are cultured in a nursery until
ready for out-planting at sea, where they are transferred
to submerged long lines until harvest. The attached holdfasts can also be re-used for multiple years without any
further initiation of culture ropes. This is economically
reasonable cultivation method, but fouling organisms are
problematic. Technology development to reduce fouling
is an urgent need for the sustainable production and the
growth of the Sargassum aquaculture industry.
https://doi.org/10.4490/algae.2017.32.3.3
ECOSYSTEM SERVICES
Seaweeds are valued as food in many parts of Asia and
in the western countries. Seaweeds are also used to produce animal feed, chemicals, paper, fertilizer, biofuel, and
other renewable, derivative products, and even to test
biological toxicity for human and environmental health
(Han et al. 2011, Johnson et al. 2014, Hafting et al. 2015,
Kerrison et al. 2015, Park et al. 2016, Wells et al. 2016).
One goal for the development of sustainable aquaculture
is to ensure that commercial aquaculture has minimal
adverse effects on the environment. One way to achieve
this goal is through development of improved methods of
waste management for land based and coastal / offshore
aquaculture. IMTA combines the fed aquaculture (e.g.,
fish or shrimp) with the extractive aquaculture (seaweed
and shellfish) to create a more balanced ecosystem. In
coastal waters, high levels of these nutrients can trigger
harmful algal blooms and contribute to excessive growth
of nuisance or opportunistic macroalgae, which in turn
have negative consequences on coastal ecosystems and
economies (Neori et al. 2004, Buschamann et al. 2008a,
Chopin et al. 2008, Pereira and Yarish 2008, Abreu et al.
2009, 2011b, Kim et al. 2015a). Nutrient bioextraction is
a similar concept but without the fed aquaculture component. The concept of nutrient bioextraction can be applied to urbanized estuaries, where the excess nutrients
are already problematic. In the IMTA and the nutrient
bioextraction systems (whether land based, coastal or offshore) seaweed can be used as an extractive component
to remove inorganic nutrients and mitigate potentially
adverse environmental impacts (Neori et al. 2004, 2007,
Corey et al. 2012, 2014, Kim et al. 2013a, 2014b, 2015b,
Rose et al. 2015, Wu et al. 2017). Seaweeds take up nitrogen, phosphorus and carbon dioxide, which they use for
growth and production of energy storage products. When
seaweeds are harvested from the IMTA or nutrient bioextraction systems, the nutrients are also being removed
from the water.
Considering the global seaweed production and tissue carbon and nitrogen contents in each species, total
extractive nitrogen and carbon by seaweed aquaculture
can be estimated. Considering average values of nitrogen
(Pyropia / Porphyra 5.5%, Gracilaria 3.0%, Kappaphycus
/ Eukeuma 1.7%, kelp 2.0%, and Sargassum 4.1%) and
carbon (Pyropia / Porphyra 38%, Gracilaria 28%, Kappaphycus / Eukeuma 29%, kelp 30%, and Sargassum
34%) (Asare and Harlin 1983, Gerald 1997, Schaffelke
and Klumpp 1998, Gevaert et al. 2001, Schaffelke 2001,
Chung et al. 2002, Rawson et al. 2002, Sahoo and Ohno
6
Kim et al. Seaweed Aquaculture
2003, Dean and Hurd 2007, Kim et al. 2007, 2014b, 2015b,
Buschmann et al. 2008b, Abreu et al. 2009, RobertsonAndersson et al. 2009, Levine and Sahoo 2010, Broch et al.
2013), the total nitrogen and carbon removal by these five
major aquaculture groups is approximately 65,000 tons
of nitrogen per year and 760,000 tons of carbon per year
(to 2.8 million tons of CO2), respectively. Over 120 million
tons of fertilizer was used in 2014 and approximatelty 1530% of it entered the ocean (FAO 2015). Recently, Bjerregaard et al. (2016) reported that seaweed aquaculture
could remove approximately 30% of the introduced nitrogen if seaweeds were aquacultured in 0.03% of the ocean
surface area, producing 500 million tons DW. They also
estimated that approximately 135 million tons of carbon
could be removed by the same amount of aquacultured
seaweed. This carbon removal is approximately 3.2% of
the carbon input to seawater from greenhouse gas emissions annually. The ecosystem services role provided by
seaweed aquaculture often falls unnoticed by coastal
managers, partly because the seaweeds are hidden underwater, and partly because the services themselves
are not yet accurately valued by markets (Barbier 2013,
Costanza et al. 2014). The additional ecosystem benefits
of seaweed aquaculture need further study and dissemination via print and social media channels.
ACKNOWLEDGEMENTS
This study was supported by grants to C. Yarish and
J. K. Kim from the U.S. EPA Long Island Sound Study’s
Long Island Sound Futures Fund, National Fish and
Wildlife Foundation (NFWF/Legacy Grant Project ID:
1401.12.03305), Connecticut Sea Grant College Program
(R/A-38 and R/A-39), the U.S. EPA Long Island Sound
Study’s Long Island Sound Futures Fund, National Fish
and Wildlife Foundation (NFWF/Legacy Grant Project ID: 1401.13.039525), NOAA SBIR I and II (Contract #
WC133R10CN0221), USDA/National Institute of Food
and Agriculture (NIFA) Award # 2014-70007-22546), the
United States-Israel Binational Agricultural Research and
Development Fund (BARD; US- 4599-13 R), and a grant to
M. Park, Y. Kim and J. K. Kim from the National Institute of
Fisheries Science (R2017015), Republic of Korea.
The authors would like to acknowledge NOAA-Ministry of Oceans and Fisheries (MOF) of Korea Joint Project
Agreement on Integrated Multi-Trophic Aquaculture,
through the Joint Coordination Panel for Aquaculture Cooperation for US-Korea.
REFERENCES
Abreu, M. H., Pereira, R., Buschmann, A. H., Sousa-Pinto, I. &
FUTURE DIRECTIONS
Yarish, C. 2011a. Nitrogen uptake responses of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined
Seaweed aquaculture technologies have developed
dramatically over the last several decades, but there are
still challenges to overcome. New strain development by
advanced breeding tools is the most urgent challenge.
Superior strains will allow the growers to expand growing seasons and enhance production. Considering the
global climate challenges, development of thermo-tolerant strains may be needed. Also the strains with disease
resistance, fast growth, high concentration of desired
molecules, the reduction of fouling organisms also need
to be developed. Development of advanced cultivation
technologies which are more robust and cost efficient
farm systems is very important. This new system will be
even more critical for highly exposed, off-shore environments since most seaweed aquaculture have occurred
nearshore. With offshore aquaculture, new designs and
approaches to macroalgae cultivation will be required,
including strain development, harvesting, transport and
processing. The offshore aquaculture system may leverage new material and engineering solutions, autonomous and robotic technologies, as well as advanced sensing and monitoring capabilities.
and single addition of nitrate and ammonium. J. Exp.
Mar. Biol. Ecol. 407:190-199.
Abreu, M. H., Pereira, R., Yarish, C., Buschmann, A. H. &
Sousa-Pinto, I. 2011b. IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance
of the seaweed in a land-based pilot scale system. Aquaculture 312:77-87.
Abreu, M. H., Varela, D. A., Henríquez, L., Villarroel, A., Yarish,
C., Sousa-Pinto, I. & Buschmann, A. H. 2009. Traditional
vs. integrated multi-trophic aquaculture of Gracilaria
chilensis C. J. Bird, J. McLachlan & E. C. Oliveira: productivity and physiological performance. Aquaculture
293:211-220.
Alamsjah, M. A. 2010. Producing new variety of Gracilaria sp.
through cross breeding. Res. J. Fish. Hydrobiol. 5:159167.
Asare, S. O. & Harlin, M. M. 1983. Seasonal fluctuations in tissue nitrogen for five species of perennial macroalgae in
Rhode Island Sound. J. Phycol. 19:254-257.
Ask, E. I. & Azanza, R. V. 2002. Advances in cultivation technology of commercial eucheumatoid species: a re-
7
http://e-algae.org
Algae 2017, 32(1): 1-13
view with suggestions for future research. Aquaculture
culture activity in Chile: determining the physiological
206:257-277.
capabilities of Macrocystis and Gracilaria as biofilters. J.
Augyte, S., Yarish, C., Redmond, S. & Kim, J. K. Cultivation
Appl. Phycol. 20:571-577.
of a morphologically distinct strain of the sugar kelp,
Caines, S., Manríquez-Hernández, J. A., Duston, J., Corey, P.
Saccharina latissima forma angustissima, from coastal
& Garbary, D. J. 2014. Intermittent aeration affects the
Maine, USA, with implications for ecosystem services. J.
bioremediation potential of two red algae cultured in
Appl. Phycol. (in press).
finfish effluent. J. Appl. Phycol. 26:2173-2181.
Barbier, E. B. 2013. Valuing ecosystem services for coastal
Camus, C., Ballerino, P., Delgado, R., Olivera-Nappa, Á., Ley-
wetland protection and restoration: progress and chal-
ton, C. & Buschmann, A. H. 2016. Scaling up bioethanol
lenges. Resources 2:213-230.
production from the farmed brown macroalgae Mac-
Barrington, K., Chopin, T. & Robinson, S. 2009. Integrated
rocystis pyrifera in Chile. Biofuels Bioprod. Biorefin.
multi-trophic aquaculture (IMTA) in marine temperate
10:673-685.
waters. In Soto, D. (Ed.) Integrated Mariculture: A Global
Chen, T. T., Lin, C. M., Chen, M. J., Lo, J. H., Chiou, P. P., Gong,
Eeview. FAO Fisheries and Aquaculture Technical Paper,
H. Y., Wu, J. L., Chen, M. H. C. & Yarish, C. 2015. Prin-
No. 529. Food and Agriculture Organization of the Unit-
ciples and application of transgenic technology in ma-
ed Nations, Rome, pp. 7-46.
rine organisms. In Kim, S. -K. (Ed.) Handbook of Marine
Bjerregaard, R., Valderrama, D., Radulovich, R., Diana, J.,
Biotechnology. Springer, Berlin, pp. 387-412.
Capron, M., Mckinnie, C. A., Cedric, M., Hopkins, K., Yar-
Chopin, T., Robinson, S. M. C., Troell, M., Neori, A., Bus-
ish, C., Goudey, C. & Forster, J. 2016. Seaweed aquacul-
chmann, A. H. & Fang, J. 2008. Multitrophic integration
ture for food security, income generation and environ-
for sustainable marine aquaculture. In Jørgensen, S. E. &
mental health in Tropical Developing Countries. Report
Fath, B. D. (Eds.) Encyclopedia of Ecolog. Vol. 3. Ecologi-
#107147. Available from: http://documents.worldbank.
cal Engineering. Elsevier, Oxford, pp. 2463-2475.
org/curated/en/947831469090666344/Seaweed-aqua-
Chopin, T., Yarish, C., Wilkes, R., Belyea, E., Lu, S. & Mathie-
culture-for-food-security-income-generation-and-en-
son, A. 1999. Developing Porphyra/salmon integrated
vironmental-health-in-Tropical-Developing-Countries;
aquaculture for bioremediation and diversification of
jsessionid=4sLY8b149Hwa-8ramT5do35G. Accessed Jan
the aquaculture industry. J. Appl. Phycol. 11:463-472.
23, 2017.
Chung, I. K, Kang, Y. H., Yarish, C., Kraemer, G. P. & Lee, J. A.
Blouin, N. A., Brodie, J. A., Grossman, A. C., Xu, P. & Brawley,
2002. Application of seaweed cultivation to the bioreme-
S. H. 2011. Porphyra: a marine crop shaped by stress.
diation of nutrient-rich effluent. Algae 17:187-194.
Trends Plant Sci. 16:29-37.
Corey, P., Kim, J. K., Duston, J. & Garbary, D. J. 2014. Growth
Broch, O. J., Ellingsen, I. H., Forbord, S., Wang, X., Volent, Z.,
and nutrient uptake by Palmaria palmata integrated
Alver, M. O., Handå, A., Andresen, K., Slagstad, D., Reit-
with Atlantic halibut in a land-based aquaculture sys-
an, K. I., Olsen, Y. & Skjermo, J. 2013. Modelling the culti-
tem. Algae 29:35-45.
vation and bioremediation potential of the kelp Saccha-
Corey, P., Kim, J. K., Garbary, D. J., Prithiviraj, B. & Duston, J.
rina latissima in close proximity to an exposed salmon
2012. Bioremediation potential of Chondrus crispus (Ba-
farm in Norway. Aquac. Environ. Interact. 4:186-206.
sin Head) and Palmaria palmata: effect of temperature
Buck, B. H. & Buchholz, C. M. 2004. The offshore-ring: a new
and high nitrate on nutrient removal. J. Appl. Phycol.
system design for the open ocean aquaculture of mac-
24:441-448.
roalgae. J. Appl. Phycol. 16:355-368.
Correa, T., Gutiérrez, A., Flores, R., Buschmann, A. H., Corne-
Buschmann, A. H., Hernández-González, M. C. & Varela, D.
jo, P. & Bucarey, C. 2016. Production and economic
A. 2008a. Seaweed future cultivation in Chile: perspec-
assessment of giant kelp Macrocystis pyrifera cultiva-
tives and challenges. Int. J. Environ. Pollut. 33:432-456.
tion for abalone feed in the south of Chile. Aquac. Res.
Buschmann, A. H., Prescott, S., Potin, P., Faugeron, S., Vásquez,
47:698-707.
J. A., Camus, C., Infante, J., Hernández-González, M. C.,
Costanza, R., de Groot, R., Sutton, P., van der Ploeg, S., Ander-
Gutíerrez, A. & Varela, D. A. 2014. The status of kelp ex-
son, S. J., Kubiszewski, I., Farber, S. & Turner, R. K. 2014.
ploitation and marine agronomy, with emphasis on
Changes in the global value of ecosystem services. Glob.
Macrocystis pyrifera, in Chile. Adv. Bot. Res. 71:161-188.
Environ. Change 26:152-158.
Buschmann, A. H., Varela, D. A., Hernández-González, M. C.
Cottier-Cook, E. J., Nagabhatla, N., Badis, Y., Campbell, M.
& Huovinen, P. 2008b. Opportunities and challenges for
L., Chopin, T., Dai, W., Fang, J., He, P., Hewitt, C. L., Kim,
the development of an integrated seaweed-based aqua-
G. H., Huo, Y., Jiang, Z., Kema, G., Li, X., Liu, F., Liu, H.,
https://doi.org/10.4490/algae.2017.32.3.3
8
Kim et al. Seaweed Aquaculture
Liu, Y., Lu, Q., Luo, Q., Mao, Y., Msuya, F. E., Rebours, C.,
electronic publication, National University of Ireland,
Shen, H., Stentiford, G. D., Yarish, C., Wu, H., Yang, X.,
Galway. Available from: http://www.algaebase.org. Ac-
Zhang, J., Zhou, Y. & Gachon, C. M. M. 2016. Safeguard-
cessed Jun 21, 2016.
ing the future of the global seaweed aquaculture industry.
Hafting, J. T., Craigie, J. S., Stengel, D. B., Loureiro, R. R., Bus-
United Nation University (INWEH) and Scottish Associ-
chmann, A. H., Yarish, C., Edwards, M. D. & Critchley, A.
ation for Marine Science Policy Brief, South Hamilton,
T. 2015. Prospects and challenges for industrial produc-
ON, 12 pp.
tion of seaweed bioactives. J. Phycol. 51:821-837.
Dean, P. R. & Hurd, C. L. 2007. Seasonal growth, erosion rates,
Han, T., Kong, J. A., Kang, H. G., Kim, S. J., Jin, G. S., Choi, H. &
and nitrogen and photosynthetic ecophysiology of Un-
Brown, M. T. 2011. Sensitivity of spore germination and
daria pinnatifida (Heterokontophyta) in southern New
germ tube elongation of Saccharina japonica to metal
Zealand. J. Phycol. 43:1138-1148.
exposure. Ecotoxicology 20:2056-2068.
Dillehay, T. D., Ramírez, C., Pino, M., Collins, M. B., Rossen, J.
Hanisak, M. D. 1987. Cultivation of Gracilaria and other mac-
& Pino-Navarro, J. D. 2008. Monte Verde: seaweed, food,
roalgae in Florida for energy production. In Bird, K. T. &
medicine, and the peopling of South America. Science
Benson, P. H. (Eds.) Seaweed Cultivation for Renewable
320:784-786.
Resources. Elsevier, New York, pp. 191-218.
FAO (Food and Agriculture Organization of the United Na-
Hanisak, M. D. & Ryther, J. H. 1984. Cultivation biology of
tions). 2015. World fertilizer trends and outlook to 2019.
Gracilaria tikvahiae in the United States. Hydrobiologia
Available from: http://www.fao.org/3/a-i5627e.pdf. Ac-
116/117:295-298.
cessed Jan 23, 2017.
Hayashi, L., Hurtado, A. Q., Msuya, F. E., Bleicher-Lhonneur,
FAO (Food and Agriculture Organization of the United Na-
G. & Critchley, A. T. 2010. A review of Kappaphycus farm-
tions). 2017. The state of world fisheries and aquacul-
ing: prospects and constraints. In Israel, A., Einav, R. &
ture. Available from: http://www.fao.org/fishery/en. Ac-
Seckbach, J. (Eds.) Seaweeds and Their Role in Globally
cessed Jan 23, 2017.
Changing Environments: Cellular Origin, Life in Extreme
Fowler-Walker, M. J., Wernberg, T. & Connell, S. D. 2006. Dif-
Habitats and Astrobiology. Springer, New York, pp. 251-
ferences in kelp morphology between wave sheltered
283.
and exposed localities: morphologically plastic or fixed
He, P., Xu, S., Zhang, H., Wen, S., Dai, Y., Lin, S. & Yarish, C.
traits? Mar. Biol. 148:755-767.
2008. Bioremediation efficiency in removal of dissolved
Gerard, V. A. 1997. The role of nitrogen nutrition in high-tem-
nutrients by the red seaweed, Porphyra yezoensis, culti-
perature tolerance of the kelp, Laminaria saccharina
vated in open sea. Water Res. 42:1281-1289.
(Chromophyta). J. Phycol. 33:800-810.
He, P. & Yarish, C. 2006. The developmental regulation of
Getchis, T. S., Rose, C. M., Carey, D., Kelly, S., Bellantuono,
mass cultures of free-living conchocelis for commer-
K. & Francis, P. 2008. A guide to marine aquaculture per-
cial net seeding of Porphyra leucosticta from Northeast
mitting in Connecticut. Connecticut Sea Grant College
America. Aquaculture 257:373-381.
Program, Groton, CT, 140 pp.
Hou, J. & Jin, Y. 2005. The healing power of Chinese herbs and
Gevaert, F., Davoult, D., Creach, A., Kling, R., Janquin, M. -A.,
medicinal recipes. Haworth Press, Inc., New York, 662 pp.
Seuront, L. & Lemoine, Y. 2001. Carbon and nitrogen
Hu, C., Li, D., Chen, C., Ge, J., Muller-Karger, F. E., Liu, J.,
content of Laminaria saccharina in the eastern English
Yu, F. & He, M. -X. 2010. On the recurrent Ulva prolifera
Channel: biometrics and seasonal variations. J. Mar.
blooms in the Yellow Sea and East China Sea. J. Geophys.
Biol. Assoc. U. K. 81:727-734.
Res. 115:C05017.
Gorman, L., Kraemer, G. P., Yarish, C., Boo, S. M. & Kim, J.
Huo, Y., Han, H., Hua, L., Wei, Z., Yu, K., Shi, H., Kim, J. K.,
K. 2017. The effects of temperature on the growth and
Yarish, C. & He, P. 2016. Tracing the origin of green mac-
nitrogen content of Gracilaria vermiculophylla and
roalgal blooms based on the large scale spatio-temporal
Gracilaria tikvahiae from LIS, USA. Algae 32:57-66.
distribution of Ulva microscopic propagules and settled
Guillemin, M. L., Faugeron, S., Destombe, C., Viard, F., Cor-
mature Ulva vegetative thalli in coastal regions of the
rea, J. A. & Valero, M. 2008. Genetic variation in wild and
Yellow Sea, China. Harmful Algae 59:91-99.
cultivated populations of the haploid-diploid red alga
Hurtado, A. Q., Critchley, A. T., Trespoey, A. & Bleicher Lhon-
Gracilaria chilensis: how farming practices favor asexual
neur, G. 2006. Occurrence of Polysiphonia epiphytes in
reproduction and heterozygosity. Evolution 62:1500-
Kappaphycus farms at Calaguas Is., Camarines Norte,
1519.
Phillippines. J. Appl. Phycol. 18:301-306.
Guiry, M. D. & Guiry, G. M. 2016. AlgaeBase. World-wide
Hwang, E. K., Cho, Y. C. & Sohn, C. H. 1998. Reuse of holdfasts
9
http://e-algae.org
Algae 2017, 32(1): 1-13
in Hizikia cultivation. J. Korean Fish. Soc. 32:112-116.
nitrogen release and alteration of nitrogen metabolism
Hwang, E. K., Gong, Y. G., Hwang, I. -K., Park, E. -J. & Park,
in the intertidal genus Porphyra. PLos ONE 8:e69961.
C. S. 2013. Cultivation of the two perennial brown algae
Kim, J. K., Kraemer, G. P. & Yarish, C. 2014b. Field scale evalu-
Ecklonia cava and E. stolonifera for abalone feeds in Ko-
ation of seaweed aquaculture as a nutrient bioextraction
rea. J. Appl. Phycol. 25:825-829.
strategy in Long Island Sound and the Bronx River Estu-
Hwang, E. K., Gong, Y. G. & Park, C. S. 2012. Cultivation of
ary. Aquaculture 433:148-156.
a hybrid of free-living gametophytes between Undari-
Kim, J. K., Kraemer, G. P. & Yarish, C. 2015b. Use of sugar kelp
opsis peterseniana and Undaria pinnatifida: morpho-
aquaculture in Long Island Sound and the Bronx River
logical aspects and cultivation period. J. Appl. Phycol.
Estuary for nutrient extraction. Mar. Ecol. Prog. Ser.
24:401-408.
531:155-166.
Hwang, E. K., Ha, D. S., Baek, J. M., Wee, M. Y. & Park, C. S.
Kim, J. K., Mao, Y., Kraemer, G. & Yarish, C. 2015c. Growth and
2006a. Effects of pH and salinity on the cultivated brown
pigment content of Gracilaria tikvahiae McLachlan un-
alga Sargassum fulvellum and associated animals. Algae
der fluorescent and LED lighting. Aquaculture 436:52-
21:317-321.
57.
Hwang, E. K., Park, C. S. & Baek, J. M. 2006b. Artificial seed
Kim, J. K. & Yarish, C. 2014. Development of a sustainable
production and cultivation of the edible brown alga,
land-based Gracilaria cultivation system. Algae 29:217-
Sargassum fulvellum (Turner) C. Agardh: developing a
225.
new species for seaweed cultivation in Korea. J. Appl.
Kim, J. K., Yarish, C. & Pereira, R. 2016. Tolerances to hypo-
Phycol. 18:251-257.
osmotic and temperature stresses in native and invasive
Johnson, R. B., Kim, J. K., Armbruster, L. C. & Yarish, C. 2014.
species of Gracilaria (Rhodophyta). Phycologia 55:257-
Nitrogen allocation of Gracilaria tikvahiae grown in ur-
264.
banized estuaries of Long Island Sound and New York
Koehl, M. A. R., Silk, W. K., Liang, H. & Mahadevan, L. 2008.
City, USA: a preliminary evaluation of ocean farmed
How kelp produce blade shapes suited to different flow
Gracilaria for alternative fish feeds. Algae 29:227-235.
regimes: a new wrinkle. Integr. Comp. Biol. 48:834-851.
Kawashima, Y. & Tokuda, H. 1993. Regeneration from the cal-
Kraemer, G. P., Kim, J. K. & Yarish, C. 2014. Seaweed aqua-
lus of Undaria pinnatifida (Harvey) Suringar (Laminari-
culture: bioextraction of nutrients to reduce eutrophica-
ales, Phaeophyta). Hydrobiologia 260/261:385-389.
tion. Association of Massachusetts Wetland Scientists
Kerrison, P. D., Stanley, M. S., Edwards, M. D., Black, K. D. &
Newsletter 89:16-17.
Hughes, A. D. 2015. The cultivation of European kelp for
Langan, R. & Horton, F. 2005. Design, operation and eco-
bioenergy: site and species selection. Biomass Bioen-
nomics of submerged longline mussel culture in the
ergy 80:229-242.
open ocean. Bull. Aquac. Assoc. Can. 103:11-20.
Kim, G. H., Moon, K. -H., Kim, J. -Y., Shim, J. & Klochkova, T.
Largo, D. B., Fukami, K. & Nishijima, T. 1995. Occasional
A. 2014a. A revaluation of algal diseases in Korean Py-
pathogenic bacteria promoting ice-ice disease in the
ropia (Porphyra) sea farms and their economic impact.
carrageenan-producing red algae Kappaphycus alvare-
Algae 29:249-265.
zii and Eucheuma denticulatum (Solieriaceae, Gigarti-
Kim, J. K., Duston, J., Corey, P. & Garbary, D. J. 2013a. Marine
nales, Rhodophyta). J. Appl. Phycol. 7:545-554.
finfish effluent bioremediation: effects of stocking den-
Levine, I. A. & Sahoo, D. 2010. Porphyra: harvesting gold from
sity and temperature on nitrogen removal capacity of
the sea. I.K. International Publihing House Pvt. Ltd.,
Chondrus crispus and Palmaria palmata (Rhodophyta).
New Delhi, 92 pp.
Aquaculture 414-415:210-216.
Li, X., Cong, Y., Yang, G., Shi, Y., Qu, S., Li, Z., Wang, G., Zhang,
Kim, J. K., Kottuparambil, S., Moh, S. H., Lee, T. K., Kim, Y. -J.,
Z., Luo, S., Dai, H., Xie, J., Jiang, G., Liu, J. & Wang, T. 2007.
Rhee, J. -S., Choi, E. -M., Kim, B. H., Yu, Y. J., Yarish, C. &
Trait evaluation and trial cultivation of Dongfang No. 2,
Han, T. 2015a. Potential applications of nuisance micro-
the hybrid of a male gametophyte clone of Laminaria
algal blooms. J. Appl. Phycol. 27:1223-1234.
longissima (Laminariales, Phaeophyta) and a female
Kim, J. K., Kraemer, G. P., Neefus, C. D., Chung, I. K. & Yar-
one of L. japonica. J. Appl. Phycol. 19:139-151.
ish, C. 2007. Effects of temperature and ammonium on
Li, X., Zhang, Z., Qu, S., Liang, G., Sun, J., Zhao, N., Cui, C.,
growth, pigment production and nitrogen uptake by
Cao, Z., Li, Y., Pan, J., Yu, S., Wang, Q., Li, X., Luo, S., Song,
four species of Porphyra (Bangiales, Rhodophyta) native
S., Guo, L. & Yang, G. 2016. Improving seedless kelp (Sac-
to the New England coast. J. Appl. Phycol. 19:431-440.
charina japonica) during its domestication by hybrid-
Kim, J. K., Kraemer, G. P. & Yarish, C. 2013b. Emersion induces
https://doi.org/10.4490/algae.2017.32.3.3
izing gametophytes and seedling-raising from sporo-
10
Kim et al. Seaweed Aquaculture
phytes. Sci. Rep. 6:21255.
of the agar-producing Gracilarioid red algae. Rev. Fish.
Lindell, S., Green-Beach, E., Bailey, D., Beals, M., Kim, J. K. &
Sci. 8:345-377.
Yarish, C. 2015. Multi-cropping seaweed Gracilaria tik-
Park, J., Jin, G. -S., Hwang, M. S., Brown, M. T. & Han, T. 2016.
vahiae with oysters for nutrient bioextraction and sea
Toxicity tests using the kelp Undaria pinnatifida for
vegetables in Waquoit Bay, MA. In National Shellfisher-
heavy metal risk assessment. Toxicol. Environ. Health.
ies Association 107th Annual Meeting, National Shell-
Sci. 8:86-95.
fisheries Association, Monterey, CA.
Park, J., Kim, J. K., Kong, J. -A., Depuydt, S., Brown, M. T. &
Liu, D., Keesing, J. K., Xing, Q. & Shi, P. 2009. World’s larg-
Han, T. 2017. Implications of rising temperatures for ga-
est macroalgal bloom caused by expansion of seaweed
metophyte performance of two kelp species from Arctic
aquaculture in China. Mar. Pollut. Bull. 58:888-895.
waters. Bot. Mar. 60:39-48.
Marinho, G. S., Holdt, S. L., Birkeland, M. J. & Angelidaki, I.
Patwary, M. U. & van der Meer, J. P. 1992. Genetic and breed-
2015. Commercial cultivation and bioremediation po-
ing of cultivated seaweeds. Algae 7:281-318.
tential of sugar kelp, Saccharina latissima, in Danish
Peng, Y., Xie, E., Zheng, K., Fredimoses, M., Yang, X., Zhou,
waters. J. Appl. Phycol. 27:1963-1973.
X., Wang, Y., Yang, B., Lin, X., Liu, J. & Liu, Y. 2013. Nutri-
Mathieson, A. C., Hehre, E. J., Dawes, C. J. & Neefus, C. D.
tional and chemical composition and antiviral activity
2008. An historical comparison of seaweed populations
of cultivated seaweed Sargassum naozhouense Tseng et
from Casco Bay, Maine. Rhodora 110:1-102.
Lu. Mar. Drugs 11:20-32.
McVey, J. P., Stickney, R. R., Yarish, C. & Chopin, T. 2002.
Pereira, R. & Yarish, C. 2008. Mass production of marine mac-
Aquatic polyculture balanced ecosystem management:
roalgae. In Jørgensen, S. E. & Fath, B. D. (Eds.) Encyclo-
new paradigms for seafood production. In Stickney, R.
pedia of Ecology. Vol. 3. Ecological Engineering. Elsevier,
R. & McVey, J. P. (Eds.) Responsible Marine Aquaculture.
Oxford, pp. 2236-2247.
CABI Publishing, Wallingford, pp. 91-104.
Pereira, R. & Yarish, C. 2010. The role of Porphyra in sustain-
Miura, A. 1984. A new variety and a new form of Porphyra
able culture systems: physiology and applications. In Is-
(Bangiales, Rhodophyta) from Japan: Porphyra ten-
rael, A. & Einav, R. (Eds.) Role of Seaweeds in a Globally
era Kjellman var. tamatsuensis Miura, var. nov. and P.
Changing Environment. Springer Publishers, New York,
yezoensis Ueda form. narawaensis Miura, form. nov. J.
pp. 339-354.
Tokyo Univ. Fish. 71:1-37.
Pereira, R., Yarish, C. & Critchley, A. T. 2013. Seaweed aquacul-
Mumford, T. F. & Miura, A. 1988. Porphyra as food: cultivation
ture for human foods in land based and IMTA systems.
and economics. In Lembi, C. A. & Waaland, J. R. (Eds.)
In Meyers, R. A. (Ed.) Encyclopedia of Sustainability Sci-
Algae and Human Affairs. Cambridge University Press,
ence and Technology. Springer, New York, pp. 9109-9128.
London, pp. 87-117.
Qi, Z., Liu, H., Li, B., Mao, Y., Jiang, Z., Zhang, J. & Fang, J.
NASA. 2017. NASA, NOAA data show 2016 warmest year on
2010. Suitability of two seaweeds, Gracilaria lemaneifor-
record globally. Available from: https://www.nasa.gov/
mis and Sargassum pallidum, as feed for the abalone
press-release/nasa-noaa-data-show-2016-warmest-
Haliotis discus hannai Ino. Aquaculture 300:189-193.
year-on-record-globally. Accessed Jan 12, 2017.
Raikar, S. V., Ima, M. & Fujita, Y. 2001. Effects of temperature,
Neori, A., Chopin, T., Troell, M., Buschmann, A. H., Kraemer,
salinity and light intensity on the growth of Gracilaria
G. P., Halling, C., Shpigel, M. & Yarish, C. 2004. Integrated
spp. (Gracilariales, Rhodophyta) from Japan, Malaysia
aquaculture: rationale, evolution and state of the art em-
and India. Indian J. Mar. Sci. 30:98-104.
phasizing seaweed biofiltration in modern aquaculture.
Rawson, M. V. Jr., Chen, C., Ji, R., Zhu, M., Wang, D., Wang, L.,
Aquaculture 231:361-391.
Yarish, C., Sullivan, J. B., Chopin, T. & Carmona, R. 2002.
Neori, A., Troell, M., Chopin, T., Yarish, C., Critchley, A. & Bus-
Understanding the interaction of extractive and fed
chmann, A. H. 2007. The need for a balanced ecosystem
aquaculture using ecosystem modeling. In Stickney, R.
approach to blue revolution aquaculture. Environment
R. & McVey, J. P. (Eds.) Responsible Marine Aquaculture.
49:36-43.
CABI Publishing, Wallingford, pp. 263-296.
Niwa, K., Iida, S., Kato, A., Kawai, H., Kikuchi, N., Kobiyama,
Redmond, S., Green, L., Yarish, C., Kim, J. & Neefus, C. 2014a.
A. & Aruga, Y. 2009. Genetic diversity and introgression
New England seaweed culture handbook: nursery sys-
in two cultivated species (Porphyra yezoensis and Por-
tems. Connecticut Sea Grant CTSG-14-01. Available
phyra tenera) and closely related wild species of Porphy-
from: http://seagrant.uconn.edu/publications/aqua-
ra (Bangiales, Rhodophyta). J. Phycol. 45:493-502.
culture/handbook.pdf. Accessed Jan 23, 2017.
Oliveira, E. C., Alveal, K. & Anderson, R. J. 2000. Mariculture
Redmond, S., Kim, J. K., Yarish, C., Pietrak, M. & Bricknell, I.
11
http://e-algae.org
Algae 2017, 32(1): 1-13
2014b. Culture of Sargassum in Korea: techniques and
4caf8b4d0a36020dc0/2014-sintef---seaweed-in-the-
potential for culture in the U.S. Orono, ME: Maine Sea
bioeconomy.pdf. Accessed Jan 23, 2017.
Grant College Program. Available from: http://seagrant.
Sohn, C. H. 1998. The seaweed resources of Korea. In Critch-
umaine.edu/extension/korea-aquaculture. Accessed
ley, A. T. & Ohno, M. (Eds.) Seaweed Resources of the
Jan 23, 2017.
World. Japan International Cooperation Agency, Yoko-
Rensel, J., Bright, K., King, G. & Siegrist, Z. 2011. Integrated
suka, pp. 15-33.
fish-shellfish mariculture in Puget Sound. NOAA Final
Stekoll, M. S. & Peeples, T. N. 2016. Marine plant aquaculture
report. 3-31-2011. NA08OAR4170860. NOAA National
in southeast Alaska. Annual Meeting of the Phycologi-
Marine Aquaculture Initiative, Rensel Associates, Arling-
cal Society of America. pp. 38-39. Available from: http://
ton, WA, 82 pp.
static1.squarespace.com/static/543d47aee4b0f40897fde
Robertson-Andersson, D. V., Wilson, D. T., Bolton, J. J., An-
705/t/5790efa11b631be8a7a1f64a/1469116323834/
derson, R. J. & Maneveldt, G. W. 2009. Rapid assessment
Full+Final+Program.pdf. Accessed Jan 23, 2017.
of tissue nitrogen in cultivated Gracilaria gracilis (Rho-
Vairappan, C. A., Chung, C. S., Hurtado, A. Q., Soya, F. E.,
dophyta) and Ulva lactuca (Chlorophyta). Afr. J. Aquat.
Lhonneur, G. B. & Critchley, A. 2009. Distribution and
Sci. 34:169-172.
symtoms of epiphytic infection in major carrageeno-
Robinson, N., Winberg, P. & Kirkendale, L. 2013. Genetic im-
phyte-producing farms. In Nineteenth International
provement of macroalgae: status to date and needs for
Seaweed Symposium, Vol. 2, Springer, Amsterdam, pp.
the future. J. Appl. Phycol. 25:703-716.
27-33.
Rose, J. M., Bricker, S. B., Deonarine, S., Ferreira, J. G., Getchis,
Valderrama, D., Cai, J., Hishamunda, N., Ridler, N., Neish,
T., Grant, J., Kim, J. K., Krumholz, J. S., Kraemer, G. P.,
I. C., Hurtado, A. Q., Msuya, F. E., Krishnan, M., Naray-
Stephenson, K., Wikfors, G. H. & Yarish, C. 2015. Nutrient
anakumar, R., Kronen, M., Robledo, D., Gasca-Leyva, E.
bioextraction. In Meyers, R. A. (Ed.) Encyclopedia of Sus-
& Fraga, J. 2015. The economics of Kappaphycus sea-
tainability Science and Technology. Springer, New York,
weed cultivation in developing countries: a compara-
pp. 1-33.
tive analysis of farming systems. Aquac. Econ. Manag.
Sahoo, D. & Ohno, M. 2003. Culture of Kappaphycus alvarezii
19:251-277.
in deep water and nitrogen enriched medium. Bull. Mar.
Valero, M., Guillemin, M. -L., Destombe, C., Jacquemin, B.,
Sci. Fish. 22:89-96.
Gachon, C. M. M., Badis, Y., Buschmann, A. H., Camus,
Sahoo, D. & Yarish, C. 2005. Mariculture of seaweeds. In An-
C. & Faugeron, S. 2017. Perspectives on domestication
dersen, R. A. (Ed.) Phycological Methods: Algal Culturing
research for sustainable seaweed aquaculture. Per-
Techniques. Academic Press, New York, pp. 219-237.
spect. Phycol. Advanced online publication. https://doi.
Schaffelke, B. 2001. Surface alkaline phosphatase activities
org/10.1127/pip/2017/0066.
of macroalgae on coral reefs of the central Great Barrier
Weinberger, F., Buchholz, B., Karez, R. & Wahl, M. 2008. The
Reef, Australia. Coral Reefs 19:310-317.
invasive red alga Gracilaria vermiculophylla in the Baltic
Schaffelke, B. & Klumpp, D. W. 1998. Nutrient-limited growth
Sea: adaptation to brackish water may compensate for
of the coral reef macroalga Sargassum baccularia and
light limitation. Aquat. Biol. 3:251-264.
experimental growth enhancement by nutrient addition
Wells, M. L., Potin, P., Craigie, J. S., Raven, J. A., Merchabnt,
in continuous flow culture. Mar. Ecol. Prog. Ser. 164:199-
S. S, Helliwell, K. E., Smith, A. G., Camire, M. E. & Braw-
211.
ley, S. H. 2016. Algae as nutritional and functional food
Shin, J. -A. 1999. Crossing between Porphyra yezoensis and P.
sources: revisiting our understanding. J. Appl. Phycol.
tenera. Algae 14:73-77.
Advanced online publication. https://doi/org/10.1007/
Shin, J. -A. 2003. Inheritance mode of some characters of
s10811-016-0974-5.
Porphyra yezoensis (Bangiales, Rhodophyta) II. Yield,
Wu, H., Huo, Y., Han, F., Liu, Y. & He, P. 2015. Bioremediation
photosynthetic pigment content, red rot disease-resis-
using Gracilaria chouae co-cultured with Sparus macro-
tance, color, luster and volatile sulfur compounds con-
cephalus to manage the nitrogen and phosphorous bal-
centration. Algae 18:83-88.
ance in an IMTA system in Xiangshan Bay, China. Mar.
SINTEF. 2014. A new Norwegian bioeconomy based on cul-
Pollut. Bull. 91:272-279.
tivation and processing of seaweeds: opportunities and
Wu, H., Kim, J. K., Huo, Y., Zhang, J. & He, P. 2017. Nutrient
research and development needs. SINTEF Fisheries
removal ability of seaweeds on Pyropia yezoensis aqua-
and Aquaculture, Norway. Available from: http://www.
culture rafts in China’s radial sandbanks. Aquat. Bot.
innovasjonnorge.no/contentassets/95273c625e1c4b
137:72-79.
https://doi.org/10.4490/algae.2017.32.3.3
12
Kim et al. Seaweed Aquaculture
Xie, E. Y., Liu, D. C., Jia, C., Chen, X. L. & Yang, B. 2013. Artifi-
Zhang, J., Huo, Y., Wu, H., Yu, K., Kim, J. K., Yarish, C., Qin,
cial seed production and cultivation of the edible brown
Y., Liu, C., Xu, R. & He, P. 2014. The origin of the Ulva
alga Sargassum naozhouense Tseng et Lu. J. Appl. Phy-
macroalgal blooms in the Yellow Sea in 2013. Mar. Pollut.
col. 25:513-522.
Bull. 89:276-283.
Yokoya, N. S., Hirotaka, K., Obika, H. & Litamura, T. 1999. Ef-
Zhang, J., Kim, J. K., Yarish, C. & He, P. 2016. The expansion of
fects of environmental factors and plant growth regula-
Ulva prolifera O.F. Müller macroalgal blooms in the Yel-
tors on growth of the red alga Gracilaria vermiculophylla
low Sea, PR China, through asexual reproduction. Mar.
from Shikoku Island, Japan. Hydrobiologia 398/399:339-
Pollut. Bull. 104:101-106.
347.
13
http://e-algae.org