European Journal of Phycology

ISSN: 0967-0262 (Print) 1469-4433 (Online) Journal homepage: http://www.tandfonline.com/loi/tejp20

The future of seaweed aquaculture in a rapidly

changing world

Ik Kyo Chung, Calvyn F. A. Sondak & John Beardall

To cite this article: Ik Kyo Chung, Calvyn F. A. Sondak & John Beardall (2017) The future of
seaweed aquaculture in a rapidly changing world, European Journal of Phycology, 52:4, 495-505,
DOI: 10.1080/09670262.2017.1359678

To link to this article: http://dx.doi.org/10.1080/09670262.2017.1359678

Published online: 10 Oct 2017.

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 EUROPEAN JOURNAL OF PHYCOLOGY, 2017
VOL. 52, NO. 4, 495–505
https://doi.org/10.1080/09670262.2017.1359678

The future of seaweed aquaculture in a rapidly changing world

a
Ik Kyo Chung , Calvyn F. A. Sondakb and John Beardall c

a
Department of Oceanography, Pusan National University, Busan 46241, Korea; bFaculty of Fisheries and Marine Science, Sam Ratulangi
University, Manado 95115, Indonesia; cSchool of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia

ABSTRACT
Human activities are having increasingly negative impacts on the natural environment. The rapidly expanding human
population has led to a shortage of resources and the ability to support the growing population sustainably is a major
challenge for the future. Coastal environments, including natural seaweed communities, provide a range of important
ecosystem services. Since seaweed aquaculture beds (SABs) provide many of the services associated with natural seaweed
communities they have a potential role in providing solutions such as CO2 sequestration, provision of food and the supply of
useful chemicals. However, the productivity of natural seaweed communities and SABs is under threat from the rapid changes
in climate that the planet is experiencing. Here we examine the likely effects of global change, in particular elevated CO2 and
ocean acidification, increased temperatures and elevated levels of UVB, on the performance of seaweeds. While it is clear that
rising temperatures and elevated CO2 and their interactions with other environmental factors are likely to have profound
effects on macroalgal production, such effects are likely to be species dependent. We also examine the fate of organic matter
from seaweeds and the potential for using SAB productivity as a contributor to blue carbon as a strategy for amelioration of
increases in anthropogenic CO2 emissions. There is considerable potential for increased drawdown of CO2 by SABs, though its
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effectiveness in amelioration of atmospheric CO2 increase will depend on the fate of the resulting biomass.

ARTICLE HISTORY Received 11 April 2017; Revised 6 July 2017; Accepted 18 July 2017

KEYWORDS aquaculture; blue carbon; climate change; primary productivity; seaweeds; seaweed aquaculture beds

Introduction and non-living biomass in the ocean and coastal

habitats has been termed ‘Blue Carbon’ by the
The aquaculture industry has grown at an impressive
United Nations Environment Programme (UNEP)
rate in recent years. The combined effects of improved
(Nellemann et al., 2009; Vierros, 2013; Howard
productivity and market growth have made aquacul-
et al., 2014) and such blue carbon environments
ture the world’s fastest growing animal-based food
provide many ecosystem services (Table 2). Krause-
sector of the last few decades (FAO, 2010, 2016).
Jensen & Duarte (2016) estimate that seaweeds could
Global aquaculture seaweed production has also
potentially assimilate about 173 Tg C year–1, which
increased markedly, having nearly tripled between
compares favourably with estimates for carbon burial
2000 and 2014, from 9.3 to nearly 27 million tonnes
rates for salt marshes, mangroves and seagrasses of
(Table 1), and the value of world seaweed production
up to 87.3, 24.9 and 112 Tg C year−1, respectively
has doubled over this period, from about US$3 to US$6
(Duarte et al., 2013), though how much of the carbon
billion (FAO, 2016) with more than 95% of this produc-
assimilated by seaweeds is sequestered over the long
tion being from Asian countries. Seaweeds are used for
term is debatable (Trevathan-Tackett et al., 2015).
a wide range of products from food to bioactive com-
Natural seaweed communities provide a range of
pounds for medicine and these uses are reviewed in
ecosystem services (Smale et al., 2013; Cabral et al.,
detail by several authors in this issue (Buschmann et
2016), and similar roles can be ascribed to artificial
al., in press; Busetti et al., in press; Mac Monagail et al.,
seaweed aquaculture beds (SABs) (MEA, 2005). Even
in press). Recently there has been increasing recogni-
though SABs are artificial ecosystems, they fulfil
tion of seaweed aquaculture and the many positive
many of the functions exhibited by natural kelp for-
benefits it supplies, though as the production of sea-
ests and seaweed beds (Table 2). Those functions can
weeds is limited within several Asian countries and its
be categorized as (1) Provisioning, i.e. food produc-
coverage is also restricted in those areas, the role of
tion (Sohn, 1993; FAO, 2003), raw materials
seaweed aquaculture has not been properly evaluated
(MacArtain et al., 2007) and biofuels (Roesijadi
(Sondak et al., 2016).
et al., 2010); (2) Regulating, i.e. potential CO2 seques-
Nonetheless, natural seaweed communities and
tration (Chung et al., 2011, 2013; Tang et al., 2011;
seaweed aquaculture represent a significant sink for
N’Yeurt et al., 2012), coastal protection (Jackson &
atmospheric CO2. Carbon sequestered in both living
Winant, 1983), nutrient removal (Chopin et al., 1999;

CONTACT Ik Kyo Chung ikchung@pusan.ac.kr; John Beardall john.beardall@monash.edu

© 2017 British Phycological Society
 496 I. K. CHUNG ET AL.

Table 1. World Seaweed Aquaculture Production 2005–2014. Source: FAO (2016).

2005 2010 2013 2014
Seaweed species (Thousand tonnes) (Thousand tonnes) (Thousand tonnes) (Thousand tonnes)
Kappaphycus alvarezii and Eucheuma spp. 2444 5629 10 394 10 992
Saccharina japonica 4371 5147 5942 7655
Gracilaria sp. 936 1696 3463 3752
Undaria pinnatifida 2440 1537 2079 2359
Porphyra (Pyropia) sp. 1287 1637 1861 1806
Sargassum fusiforme 86 78 152 175
Total 11 564 15 724 23 891 26 739

Table 2. Comparisons of services derived from mangroves, seagrasses, saltmarshes and SAB ecosystems (see text for details
of service types).
Mangrovesa Salt marshesb Seagrassesc SABsd
Provisioning Food Food Food Food
Water supply Fibres Raw materials
Raw materials Industrial products Industrial products
Regulating Climate regulation Climate regulation Climate regulation Climate regulation
(CO2 drawdown) (CO2 drawdown) (CO2 drawdown) (CO2 drawdown)
Coastal protection Coastal Protection Coastal protection Coastal protection
Improving air quality Improving water quality Improving water quality Improving water quality
Supporting Nutrient cycling Nutrient cycling Nutrient cycling Nutrient cycling
Refugia Refugia Refugia Refugia
Primary production Primary production Primary production Primary production
Cultural Recreation and ecotourism Recreation and ecotourism Recreation Recreation and ecotourism
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Aesthetic Aesthetic Aesthetic Aesthetic

Education Education Education Education
a
Barbier et al., 2011; Nellemann et al., 2009; Mumby et al., 2004. bBarbier et al., 2011; Nellemann et al., 2009; Waycott et al., 2009; Saintilan et al., 2007. cBarbier
et al., 2011; Nellemann et al., 2009. dJackson & Winant, 1983; Duggins et al., 1989; Sohn, 1993; Chopin et al., 1999; Levinton et al., 2002; Norderhaug et al.,
2002; FAO, 2003; Fei, 2004; Graham, 2004; Go, 2010; O’Connor & Anderson, 2010; Chung et al., 2011, 2013; Tang et al., 2011; N’Yeurt et al., 2012.

Fei, 2004) and nursery grounds (Norderhaug et al., are facing many problems (Muraoka, 2004; Dearing,
2002; O’Connor & Anderson, 2010); (3) Supporting, 2006; Regnier et al., 2013; Gao et al., 2016).
i.e. primary production (photosynthesis), nutrient Among the anthropogenic effects, the greatest
cycling and biodiversity (Duggins et al., 1989; threats result from human population growth. Our
Levinton et al., 2002; Graham, 2004); and (4) rapidly expanding population has led to a shortage
Cultural, i.e. recreational, educational, spiritual/aes- of resources, and thus sustainable growth is a cri-
thetic and scientific properties (Go, 2010). tical issue that the planet and humankind are
SABs, in contrast to natural seaweed communities, facing. In addition to restricted resources, increased
are artificial systems in which seaweeds are attached carbon dioxide in the atmosphere, mostly due to
as germlings to cultivation lines attached to buoys or fossil fuel combustion and deforestation of terres-
poles and then allowed to grow until they are of trial environments, is driving rapid climate change
harvestable size. Seaweed aquaculture beds cover (Chapin et al., 2000; Le Quere, 2010). As atmo-
extensive shallow coastal areas, particularly in the spheric CO2 increases, so does CO2 dissolved in
Asia-Pacific region, and although still accounting for seawater (Sabine et al., 2004) and this is bringing
only a small portion of global agriculture, seaweed about major changes in the oceans. In marine eco-
aquaculture is growing more rapidly than other com- systems, the rising atmospheric CO2 is associated
ponents of production (Sondak et al., 2016; Duarte with concurrent changes in the environment
et al., 2017). The future of seaweed aquaculture is (details of which are provided below), including
likely to see an increase in the total harvest produc- alterations in temperature, circulation, stratification,
tion following an increase in the number of cultiva- nutrient supply, oxygen content and ocean acidifi-
tion areas around the world. In 2012 only 33 cation, with potentially wide-ranging biological
countries and territories worldwide cultivated sea- effects (Doney et al., 2012). All these changes in
weed, but in 2015 50 countries reported the practice climate have the potential to affect the physiological
of seaweed aquaculture (FAO, 2014, 2016). performance of seaweeds and hence the productiv-
However, our planet has entered a new era, the ity of seaweed aquaculture.
Anthropocene (Monastersky, 2015), where human Furthermore, human population distribution is
activity has become one of the major agents of envir- heterogeneous, with just over half the world’s popu-
onmental change (IPCC, 2013). Human activities lation occupying a coastal strip 200 km wide (Small &
have been, and continue to be, affecting natural and Nicholls, 2003; Neumann et al., 2015). These popula-
social environments and, as a result, global systems tions have a tremendous impact on the quality of
coastal and oceanic environments, and coastal
 EUROPEAN JOURNAL OF PHYCOLOGY 497

environments are vulnerable to water pollution and The extent to which increasing CO2 concentra-
eutrophication caused by human activities, climate tions in seawater will impact seaweed productivity is
change and other stresses. Coastal areas are diverse dependent on the inorganic carbon acquisition
in function and important in terms of transportation, kinetics of different species. For example, some spe-
trade, settlement, tourism/recreation, resource extrac- cies are already CO2-saturated under present-day
tion including aquaculture, wildlife habitats, industry CO2 levels (Beardall et al., 1998; Cornwall et al.,
and defence (Clark, 1992). 2012) as they generally express active CO2 concen-
As the world’s environment is changing, we may trating mechanisms (CCMs) (Giordano et al., 2005).
need a new paradigm to evaluate our environment Nonetheless some sub-tidal species have been shown
and activities in terms of maintaining ecosystem sus- to have no, or limited, CCM activity and thus show
tainability and services. In this review, we discuss the increases in photosynthetic rate when supplied with
role of natural macroalgal communities and SABs, additional CO2 (Holbrook et al., 1988; Johnston et al.,
and the ecosystem services that they provide, in the 1992; Kübler et al., 1999). Even species that have been
context of global change. Other important aspects of demonstrated to have CCMs can show stimulated
algal-based industries, such as the uses of algae for growth rates under elevated CO2. Thus Zou & Gao
biofuels, high value biochemicals and bioactive sub- (2009) demonstrated increased growth of Gracilaria
stances, the importance of Integrated Multi-trophic lemaneiformis when supplied with 700 ppm CO2 and
Aquaculture (IMTA) and the impacts of diseases are saturating irradiance (but not when light was low).
considered elsewhere in this issue (Busetti et al., in Suárez-Álvarez et al. (2012) and Sarker et al. (2013)
press; Buschmann et al., in press; MacMonagail et al., also showed stimulation of growth of Hypnea spirella
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in press). and Chondrus crispus, respectively, by elevated CO2,

though in C. crispus the effects of CO2 were only
significant under elevated temperature or low irradi-
Seaweed physiological performance is likely to be ance. Likewise Celis-Plá et al. (2015) have shown that
affected by global environmental change elevated CO2 had positive effects on the physiological
performance of the brown algae Cystoseira compressa
Anthropogenic CO2 emissions have resulted in a
and Padina pavonica, though the nature of the
range of changes to the marine environment. These
changes was also modulated by nitrogen and light
include the effects of elevated CO2, changes in carbo-
availability. It is possible that under elevated CO2
nate chemistry (Feely et al., 2004), particularly a
levels, operation of the energetically expensive
decrease in oceanic pH (Ocean Acidification, OA),
CCMs is down-regulated, freeing up extra energy
and an increase in sea surface temperatures (Meehl
which can then be diverted into investment in growth
et al., 2007). In turn these have led to alterations in
processes (Israel & Hophy, 2002; Cornwall et al.,
stratification, resulting in impaired nutrient supply
2012). This might be especially advantageous under
from deep to surface waters (Doney et al., 2012). At
conditions of limited energy supply (light).
the same time damage to the stratospheric ozone
However, Zou et al. (2007) showed that elevated
layer is continuing to cause elevated levels of UVB
CO2 increased photosynthetic rates of Ulva lactuca,
radiation, especially, but not exclusively, at high lati-
but rendered the alga more susceptible to photoinhibi-
tudes (Hegglin & Shepherd, 2009). The impacts of
tion, possibly because of the down-regulation of the
global change on microalgae have been dealt with
CCM removing a possible mechanism for dissipation
extensively elsewhere (Beardall & Raven, 2004;
of excess energy. Young & Gobler (2016) showed that
Beardall et al., 2009, 2014; Gao et al., 2012; Johnson
in situ growth of Gracilaria and Ulva in an estuary was
et al., 2013), so here we concentrate on the impacts
stimulated by elevated CO2, though in the case of Ulva
on seaweeds, especially those of potential importance
this was also related to nutrient levels. An excellent
for the aquaculture industry, such as the kelps at
summary of the effects of elevated CO2 on a range of
higher latitudes and the range of species (dominated
processes in seaweeds is given by Ji et al. (2016),
by red algae) that are used extensively in the tropics.
though more work is needed to explore the effects of
elevated CO2 on commercially used seaweed species to
get a better picture of what the future of SABS might
Effects of CO2 levels and ocean acidification (OA)
be in relation to CO2 and OA, as these are poorly
CO2 concentrations in the atmosphere are expected to covered in the climate change literature. One effect of
reach 1000 ppm by the end of this century (IPCC, elevated CO2 on C. compressa in the presence of addi-
2013). This will cause dissolved CO2 concentrations to tional N reported by Celis-Plá et al. (2015) was a
rise by ~2.5-fold but because of the resulting drop in stimulation of phenolic content, an effect also noticed
pH (~0.4 units), bicarbonate concentrations will only in the microalga Phaeodactylum (Jin et al., 2015)
increase by ~10% and carbonate levels will approxi- though Arnold et al. (2012) have reported the opposite
mately halve (Feely et al., 2004; Raven et al., 2005). effect in seagrasses. While an increase in phenolics
 498 I. K. CHUNG ET AL.

would increase antioxidant capacity, these compounds though CCM activity in those species that possess one
taste bitter and can act as a deterrent to herbivory is likely to continue to suppress photorespiration
(Steinberg, 1988; Van Alstyne, 1988; Salimen & (Raven et al., 2017). Elevated temperature is likely to
Karonen, 2011; Sarojini et al., 2016). In microalgae at have the usual effects on metabolism and growth,
least, changes in CO2 levels affect fatty acid composi- increasing these properties up to an optimum but caus-
tion (Riebesell et al., 2000; Rossol et al., 2012; ing a decrease as the optimum temperature is exceeded.
Bermúdez et al., 2016) and this change in nutritional This may be especially important in South East Asia as
quality can have flow-on effects to copepod grazers, this region is predicted to show very significant tem-
but it is not known at present whether similar flow-on perature rises by 2065 (Guinotte et al., 2003).
of macromolecular composition to herbivores occurs Terada et al. (2016) showed optimum growth of
in the case of seaweeds. Kappaphycus alvarezii at 30.5°C, but reported 100%
Some effects of elevated CO2/OA can be indirect. mortality at 36°C. In contrast, optimal temperature
Connell & Russell (2010), for instance, have shown in for growth of Pyropia yezoensis (as Porphyra yesoen-
systems in South Australia that elevated CO2 favours sis) was reported as 12–15°C (Yamamoto et al., 1991).
turf-forming algae which outcompete the kelp species For Gracilaria, Raikar et al. (2001) reported that
Ecklonia radiata. Recruitment of non-calcifying sea- species from Malaysia, Japan and India showed
weeds in tropical seas has been shown to be positively slightly different temperature optima, with maximal
influenced by elevated CO2 as the accompanying OA growth for the Japanese species being ~20–25°C,
inhibits the recruitment of coralline species that would while those from India and Malaysia had optima
normally compete (Kuffner et al., 2008). Harley et al. around 25–35°C, though most species examined
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(2012) pointed out scenarios whereby although tem- showed damage as temperatures increased from 30
perate kelp species might be negatively impacted by to between 32.5 and 35°C. Thus for many algae, even
increases in herbivore (e.g. urchin) numbers under small shifts in temperature can have deleterious
warmer future conditions, concomitant OA would effects on growth and survival.
overcome this by inhibiting growth of urchins and In natural ecosystems, such alterations in tempera-
competing coralline algae and thereby promote kelp ture can result in changes in populations. Barry et al.
growth. In the case of tropical seaweeds, the final (1995) reported that over a 60-year period the tem-
impact of warming and OA would depend on the perature of their study zone on the Californian coast
extent of fisheries exploitation and thus top-down had increased by 2.2°C and showed increased dom-
pressure on the algae (Harley et al., 2012). inance of warm temperate, low growing, turf algal
species such as Gelidium coulteri, Gigartina canalicu-
lata, Endocladia muricata and Mastocarpus papillatus
Effects of rising sea surface temperature
at the expense of larger, colder water preferring spe-
Sea surface temperatures are expected to rise on cies such as Fucus distichus and Pelvetia fastigata.
average by ~4°C (range 2.4–6.4) under the A1F1 sce- Brodie et al. (2014) have predicted that rising tem-
nario by 2100 (Meehl et al., 2007), though the peratures in the north-east Atlantic will have major
changes will be heterogeneous across the world’s negative impacts on the highly productive kelp for-
oceans with high latitude regions likely to show ests, particularly in the southern reaches (Yesson
greater warming. Increasing sea surface temperatures et al., 2015), while OA will impact badly on maerl
may have significant direct impacts on the biology of (rhodolith-forming free-living coralline algae) in the
seaweeds used in aquaculture (Stévant et al., 2017). northern regions. In the 1990s, Breeman (1988, 1990)
Consequently, the responses to temperature by the carried out elegant work on the effects of temperature
algae used in SABs will need to be taken into account on reproductive biology and biogeography of canopy-
as they may determine where establishment of new forming kelp species, predicting a northward shift in
SABs is best directed, or may dictate that established the southern boundaries of species such as Laminaria
SABs are relocated to areas where temperature is hyperborea, Saccharina latissima (as L. saccharina)
more amenable to productivity. Natural populations and L. digitata. Fernández (2011) has shown that
used for harvest may also exceed their temperature population retreats of L. hyperborea, L. ochroleuca
optimum and thus become stressed, with subsequent and Saccorhiza polyschides from the northern
declines in harvest (Steneck et al., 2002; Israel et al., Spanish coast were related to increases in tempera-
2010). Thus an understanding of the responses of ture from the 1980s to the 2000s.
commercially important seaweeds to temperature is Temperature increases in the surface waters of the
an important issue for management of naturally open ocean will lead to more marked stratification of
occurring seaweeds and SABs into the future. the water column and this will lead to a diminished
Increased temperature will reduce solubility of O2 supply of nutrients from cold, nutrient-rich water
and CO2 and affect the kinetics of carbon fixation by below the thermocline into surface water (Doney,
Rubisco, slightly in favour of the oxygenase activity, 2006; Doney et al., 2012). Such restriction in nutrient
 EUROPEAN JOURNAL OF PHYCOLOGY 499

supply is likely to have a big impact on productivity SABs will be more prone to storm damage in a future
of phytoplankton in the open ocean, though is likely climate and consequently more attention will need to be
to be less important in near-shore coastal systems paid to constructing systems that will withstand greater
where increased storm activity in future is likely to wave and wind forces.
initiate greater mixing and increased run-off from Although many stressors are known to affect sea-
land, thereby enhancing nutrient availability (Meier, weeds, few studies have addressed interactions
2006; Beardall et al., 2009). However, SABs deployed between the various components of global change.
in deep water might be affected by the increased The data available in the literature are largely from
stratification and restriction on nutrient supply that single-stressor physiology, ecotoxicology and global
would impose. change studies (Israel et al., 2010). A few studies
(touched on above) have investigated the interactive
effects of warming, UVB and CO2-driven acidifica-
Other global change factors
tion on marine organisms. Our limited knowledge of
Levels of UVB radiation reaching the Earth’s surface are the interactive effects of climate change stressors is a
still increasing, due to complex interactions between major knowledge gap and some progress is being
breakdown of stratospheric ozone and global warming made with phytoplankton (Boyd et al., 2015).
and, although ozone ‘holes’ are still occurring annually However, similar studies on seaweeds are few and
over the Poles, increases in UVB fluxes to the Earth’s far between and if we are to truly understand how
surface are not restricted to high latitudes, though seaweeds in SABs are going to respond in the future
changes at the tropics are minimal (Hegglin & then more work on interactive effects of climate
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Shepherd, 2009; Herman, 2010). Increased UVB has a change components is necessary.
range of deleterious effects on algae (see Beardall et al., Adaptation in a changing ocean is crucial to identify
2014, and references therein) so increased UVB would potential ‘winners’ and ‘losers’ in the climate change
pose problems for seaweeds, though many can modu- stakes (Somero, 2010). Physiological responses to tem-
late levels of reactive oxygen scavenging compounds perature are known to be a major determinant of spe-
and UVB-screening compounds such as mycosporine cies distributions and can dictate the sensitivity of
amino acids (MAAs) (Richa et al., 2016). Studies of the populations to global warming (Southward et al.,
effects of UVB on seaweeds have focused more on early 1995; Pearson & Dawson, 2003; Harley et al., 2012;
developmental stages than on mature thalli (Beardall Jueterbock et al., 2013; Wernberg et al., 2013).
et al., 2014) and the effects of UV radiation appear to be However, if species can adapt to become more tolerant
very species-specific, even within a genus (see for to climate change related stressors, or if active selection
instance the work of Altamirano et al. (2003) on Fucus for tolerant strains is encouraged, then the potential
species). As described in the recent review by Beardall damage to SABs from a changing climate will be mini-
et al. (2014), UVB effects are modulated by other envir- mized. Again, although some advances in considering
onmental factors such as temperature (which appears to evolutionary adaptations to climate change-related
promote repair and reduce the overall UVB damage), changes are being made with phytoplankton, work
CO2 (both positive and negative effects on UVB sensi- with seaweeds in this respect is lagging far behind (see
tivity have been recorded) and nutrient limitation Reusch, 2014).
(which generally increases UVB sensitivity). However,
it is noteworthy that although UVB levels are higher in
The potential of seaweeds as one solution to
tropical regions than at higher latitudes, UVB levels are
ameliorating climate change
not rising significantly in the tropics and therefore may
not adversely affect seaweed performance in the Asia- The potential of seaweeds as a mitigation measure for
Pacific as the algae in this region may be better evolved increasing CO2 emissions has also been considered.
to cope with the existing, high, UVB fluxes. There have been several reports which demonstrate
One of the consequences of global warming will be the capacity for seaweeds to draw down and fix
increased storm activity (Meier, 2006) and this has the anthropogenic CO2 into organic matter (N’Yeurt
potential to affect seaweed aquaculture by (a) increasing et al., 2012; Chung et al., 2013; Duarte et al., 2017).
turbidity and decreasing productivity through light lim- There is also evidence that some of this organic
itation, (b) physical damage to macroalgal beds and carbon is in refractory forms that would resist
SABs by increased wave action (Pickering et al., 2011), decomposition and thus would not be released as
and (c) decreased water quality though increased runoff CO2 back into the atmosphere (Trevathan-Tackett
of nutrients and pollutants from terrestrial and riverine et al., 2015) and seaweeds could therefore act as a
systems (Eng et al., 1987; Fei, 2004). Given the predic- “blue carbon” sink (Hill et al., 2015).
tions (IPCC, 2013) that storm activity is likely to be Chung et al. (2013) proposed the concept of a coastal
enhanced in future, due to increased temperature dif- CO2 removal belt (CCRB) and reported a potential
ferences between the land and sea, it is very likely that sequestration capability of about 10 ton CO2eq ha−1
 500 I. K. CHUNG ET AL.

year−1 for a project in Korea. In addition to drawdown into deep water, this being the approximate time
by natural macroalgal communities, artificial seaweed scale for deep-sea circulation and the biological car-
aquaculture beds (SABs) could also provide the same bon pump (Maier-Reimer & Hasselmann, 1987;
potential CO2 removal capability. The potential use of Sabine et al., 2004).
seaweed aquaculture beds in CO2 mitigation efforts has The importance of blue carbon has been ever
been proposed for commercial seaweed production in increasing and it is now recognized as an important
Asian countries (Sondak et al., 2016). SABs and natural agent in the new era of climate change. Seaweeds are
seaweed beds and kelp forests represent very significant quite different from other blue carbon systems as
pools of aquatic vegetation and C sinks and they could they almost all grow on hard substrata and therefore
thus enhance carbon sequestration in coastal waters like are not associated with sediments in which organic
other blue carbon systems (Nellemann et al., 2009; carbon could be buried. However, because of sea-
Vierros, 2013; Howard et al., 2014). weeds’ capability for attachment to hard structures,
However, it is difficult for seaweeds to be recognized SABs could be developed in offshore waters and
as carbon sink agents under the current concept of CO2 therefore have a strong potential for expansion,
sequestration as conceived by the UN Framework beyond what is possible within coastal waters. The
Convention on Climate Change (UNFCCC). There concept of open-ocean aquaculture of seaweeds using
has been considerable debate about considering sea- structures, such as ‘the offshore-ring’, was introduced
weeds as a CO2 sink, particularly with respect to the in combination with offshore wind parks and har-
time period of sequestration of the carbon in their vesting and conversion of seaweed biomass to renew-
organic matter. It is obvious that seaweeds draw down able energy carriers and chemicals (Buck & Buchholz,
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CO2 from seawater through photosynthesis in the water 2004). Considerable system development is required,
column, but a good proportion of this carbon is easily however, to enable large-scale, economically attrac-
decomposed back to CO2 (see Hill et al., 2015; tive cultivation of seaweeds combined with offshore
Trevathan-Tackett et al., 2015). wind parks (Buck et al., 2008).
The current definition of a carbon sink in terms of Krause-Jensen & Duarte (2016) proposed a role for
turnover time has been set up for trees and forests, macroalgal carbon sequestration which accounts for
including mangroves, in the terrestrial environment accumulation of a large stock of organic carbon with
and the afforestation and reforestation process of the two modes for the transport of organic carbon to the
clean development mechanism (A/R CDM) is based deep ocean and sediments: (1) macroalgal material
on this concept (Wylie et al., 2016). When we consider drifting through submarine canyons, and (2) the sink-
seaweeds as CO2 sink agents, we have to apply a ing of negatively buoyant macroalgal detritus. Their
different time frame, applicable to the oceanic life estimations suggested that seaweeds could sequester
cycle. Thus, when we consider the time frame for the about 173 Tg C year–1 (with a range of 61–268 Tg C
oceanic environment we need to develop two different year–1) globally. About 90% of this sequestration
time frame strategies. One is based on the time to occurs through export to the deep sea, and the rest
reach the climax condition and the other is related to through burial in coastal sediments. This estimate
the displacement of organic carbon to specific regions exceeds that for carbon sequestered in angiosperm-
of the oceans for sequestration. based coastal habitats (Krause-Jensen & Duarte, 2016).
Compared to the time scale of decades, used when It is critical to provide accurate methodology to
the A/R CDM is applied to terrestrial environments, estimate the amount of carbon sequestered by SABs
turnover in the coastal environment occurs on quite and establish the measurement, reporting and verifica-
short time scales, less than 10 years (Chung et al., 2013). tion (MRV) methodology. The general techniques and
It is, however, unreasonable to apply the terrestrial time biology of seaweed culture are well known. It should
scale, for example a period of at least 50 years required therefore be easy to apply this information to projects
for afforestation, to those of oceanic blue carbon involving mass growth of seaweeds and establish the
(UNFCC, 2016). Therefore, we need to develop a new MRV system as well. When the MRV is provided, this
concept encompassing different time scales and a new can then be adopted and implemented as a measure of
paradigm for oceanic carbon sequestration. mitigation in the Nationally Determined Contribution
Alternatively, we could apply the same time frame (NDC) and/or Nationally Appropriate Mitigation
used for terrestrial CDMs if we consider draw-down Action (NAMA) registry (http://unfccc.int/coopera
of CO2 in one place (based on SABs or natural tion_support/nama/items/7476.php).
macroalgal beds in coastal regions) and displace- This is especially significant where SABs are
ment of the biomass to another place for sequestra- located in shallow waters where the natural standing
tion purpose – such as sinking them into the deep biomass of other vegetation is absent or low (Mitra
sea. If we use the same ‘terrestrial clock’, we could et al., 2014). Moreover, the services that natural sea-
develop appropriate solutions to keep the biomass weeds and SABs provide fulfil some strategies for
from SABs for more than 1000 years if introduced climate change adaptation. The ecosystem services
 EUROPEAN JOURNAL OF PHYCOLOGY 501

Table 3. The main steps to consider when planning, conducting, or evaluating seaweed farming at sea as a blue carbon sink.
(Modified from Radulovich et al., 2015).
1. Evaluating the main characteristics of each coastal-marine environment where farming is intended, including water and climate,
environmental quality and biodiversity, other uses of water, access and facilities, manpower availability, socioeconomic, cultural, and legal
characteristics;
2. Selecting the right seaweed species to farm in each environment for the purposes of bioenergy, ecosystem services and carbon sequestration;
3. Selecting the right site(s) within each environment, emphasizing local conditions in relation to the seaweed species selected;
4. Selecting and implementing reproduction/propagation techniques to secure sufficient numbers and quality of propagules with reliable timing;
5. Selecting and implementing cultivation technique (planting), populating the farmed area in optimal spatial arrangement and density of
propagules;
6. Following up during grow-out, making sure that the crop stays in place in the desired spatial arrangement during the entire project period;
7. Quantification of Corg and transport offshore to sink for sequestration or harvest for biofuel conversion.

that natural seaweed beds and SABs provide have efforts to identify species for use in SABs in future
been well documented (Table 1). In addition, coastal will need to take into account their physiological
eutrophication, deoxygenation and ocean acidifica- tolerance to environmental changes and to OA and
tion could be reduced by seaweeds. The design struc- warming in particular.
ture of SABs could also facilitate coastal protection to
reduce wave energy as currently occurs e.g. with
mangroves (Duarte et al., 2017). Acknowledgements
When a novel way of using seaweeds is developed This Festschrift review article is dedicated to Professor
Downloaded by [119.198.71.86] at 05:46 29 October 2017

to increase C assimilation as a blue carbon sink for Phang Siew-Moi, who has made a tremendous contribution
CO2, this could then be implemented as a new sea- to phycology in a wide range of topics, including algal CO2
weed-based ‘carbon capture and storage’ project sequestration, uses of algae for biofuels and dietary supple-
ments and halocarbon production by seaweeds.
(Chung et al., 2013; Sondak et al., 2016). The amount
of Corg produced could be easily monitored and
quantified. After the project period the total biomass Disclosure statement
could be taken offshore for sinking into deep waters.
No potential conflict of interest was reported by the authors.
The procedures that might be used in such projects
are described in Table 3 (modified from Radulovich
et al., 2015). However, as pointed out earlier, how Funding
successful burial efforts will be in sequestering C will
depend, inter alia, on the recalcitrance of the organic This work was supported by a grant from the National
Research Foundation of Korea (NRF), funded by the
matter to decomposition (Hill et al., 2015, Trevathan-
Korean Government (MSIP) (NRF-2016R1A2B1013637)
Tackett et al., 2015). to IKC, and a DIKTI Scholarship from the Indonesia
The estimate of Krause-Jensen & Duarte (2016) Ministry of National Education and Culture for CFAS.
of about 173 Tg C year–1 (with a range of 61–268
Tg C year–1) fixed by seaweeds globally is a rela-
tively small proportion of total oceanic primary Author contributions
production (54–59 Pg C year–1) and the increase J. Beardall: planning, drafting and editing the manuscript;
in atmospheric CO2 of 4 Pg C year−1 (Denman I.K. Chung: planning, drafting and editing the manuscript;
et al., 2007). However, SABs should prove to be C.F.A. Sondak contributed important information on eco-
system services and assisted with writing.
expandable to the offshore environment and the
open sea, in contrast to the A/R CDM which is
limited to land, unlocking a capacity to greatly ORCID
increase carbon caption in biomass. This approach Ik Kyo Chung http://orcid.org/0000-0003-2350-0473
has been termed Seaweed Carbon Capture and Sink John Beardall http://orcid.org/0000-0001-7684-446X
(‘Seaweed CCS’; analogous to terrestrial Carbon
Capture and Storage) and could also be applied as
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