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975
J. Phycol.
37,
975–986 (2001)
MINIREVIEW
INTEGRATING SEAWEEDS INTO MARINE AQUACULTURE SYSTEMS: A KEY
TOWARD SUSTAINABILITY
1
Thierry Chopin
2
University of New Brunswick, Centre for Coastal Studies and Aquaculture and Centre for Environmental and Molecular Algal
Research, P.O. Box 5050, Saint John, New Brunswick, E2L 4L5, Canada
Alejandro H. Buschmann
Universidad de Los Lagos, Departamento de Acuicultura, Casilla 933, Osorno, Chile
Christina Halling
Stockholm University, Department of Systems Ecology, 106 91 Stockholm, Sweden
Max Troell
Beijer International Institute of Ecological Economics, The Royal Swedish Academy of Sciences, Box 50005, 104 05
Stockholm, Sweden
Nils Kautsky
Stockholm University, Department of Systems Ecology, 106 91 Stockholm, Sweden
Amir Neori
Israel Oceanographic & Limnological Research Ltd., National Center for Mariculture, P.O. Box 1212, Eilat 88112, Israel
George P. Kraemer
State University of New York, Purchase College, Division of Natural Sciences, Purchase, New York, 10577, USA
José A. Zertuche-González
Universidad Autonoma de Baja California, Instituto de Investigaciones Oceanologicas, Ens. Apdo. Postal #453, C.P. 22830, Ensenada,
Baja California, Mexico
Charles Yarish
University of Connecticut, Department of Ecology and Evolutionary Biology, 1 University Place, Stamford, Connecticut,
06901-2315, USA
and
Christopher Neefus
University of New Hampshire, Department of Plant Biology, Office of Biometrics, G32 Spaulding Life Science Center, Durham,
New Hampshire, 03824, USA
The rapid development of intensive fed aquacul-
ture (e.g. finfish and shrimp) throughout the world
is associated with concerns about the environmental
impacts of such often monospecific practices, espe-
cially where activities are highly geographically con-
centrated or located in suboptimal sites whose assim-
ilative capacity is poorly understood and, consequently,
prone to being exceeded. One of the main environ-
mental issues is the direct discharge of significant
nutrient loads into coastal waters from open-water
systems and with the effluents from land-based sys-
tems. In its search for best management practices,
the aquaculture industry should develop innovative
and responsible practices that optimize its efficiency
and create diversification, while ensuring the reme-
diation of the consequences of its activities to main-
tain the health of coastal waters. To avoid pro-
nounced shifts in coastal processes, conversion, not
dilution, is a common-sense solution, used for centu-
ries in Asian countries. By integrating fed aquacul-
ture (finfish, shrimp) with inorganic and organic ex-
tractive aquaculture (seaweed and shellfish), the wastes
of one resource user become a resource (fertilizer
1
Received 15 July 2001. Accepted 27 September 2001.
2
Author for correspondence: e-mail tchopin@unbsj.ca.
976
THIERRY CHOPIN ET AL.
or food) for the others. Such a balanced ecosystem
approach provides nutrient bioremediation capabil-
ity, mutual benefits to the cocultured organisms, eco-
nomic diversification by producing other value-added
marine crops, and increased profitability per cultiva-
tion unit for the aquaculture industry. Moreover, as
guidelines and regulations on aquaculture effluents
are forthcoming in several countries, using appropri-
ately selected seaweeds as renewable biological nu-
trient scrubbers represents a cost-effective means
for reaching compliance by reducing the internaliza-
tion of the total environmental costs. By adopting inte-
grated polytrophic practices, the aquaculture industry
should find increasing environmental, economic, and
social acceptability and become a full and sustain-
able partner within the development of integrated
coastal management frameworks.
Key index words:
assimilative capacity; bioremedia-
tion; coastal health; environmental impacts; integrated
aquaculture; integrated coastal management; nutrifi-
cation; salmon; seaweeds; sustainability
According to Food and Agriculture Organization of
the United Nations figures, the total world capture ma-
rine fisheries annual production has been nearly level
since 1986 (Anonymous 2000). During the same pe-
riod, global marine finfish and shellfish aquaculture
production has increased by nearly 10% per year, mak-
ing aquaculture the fastest growing global food produc-
tion sector. In the past decade, the increase in global
demand for seafood has been met by increased aqua-
culture, which provided 26.4% of the world fisheries
production in 1998 (Anonymous 2000). As a result of
this rapid production increase, it is not unreasonable to
conceive that aquaculture activities might have affected
the environment in a variety of ways, especially fish and
shrimp aquaculture, which needs to be supplemented
with an exogenous source of energy (food) (Beveridge
1996). Many authors have demonstrated that organic
and inorganic inputs of food to fish culture have a sub-
stantial impact on organic matter and nutrient loading
in coastal areas (Beveridge 1984, Brown et al. 1987,
Gowen and Bradbury 1987, Rosenthal et al. 1988, López
et al. 1988, Folke and Kautsky 1989, Handy and Poxton
1993, Chopin et al. 1999b), affecting the sediments be-
neath the culture installations and producing variations
in the nutrient composition of the water column. This
can lead, for example, to enhanced sediment metabo-
lism, anoxia, sulfate reduction, and sulfide accumu-
lation, high nitrogen and phosphorus flux, acidifica-
tion, turbidity, and all other processes associated with
eutrophication (Troell and Berg 1997). These environ-
mental modifications can also affect the benthic fauna
(Rodhouse et al. 1985, Hargrave et al. 1993, Nunes and
Parsons 1998, Angel et al. 2000), fish abundance (Carss
1990), bird populations (Dankers and Zuidema 1995),
macroalgal growth and diversity, epiphytic load and
chemical composition (Ruokolahti 1988, Rönnberg et
al. 1992, Chopin et al. 1999b, Bates et al. 2001), shifts
in phytoplanktonic and zooplanktonic communities
(Granéli et al. 1989, Carlsson et al. 1990, Capriulo et
al. in press), and the composition and abundance of
bacteria (Husevåg et al. 1991, Capriulo et al. in press).
Species that do not require exogenous feeding for
their cultivation, like shellfish, can also affect the envi-
ronment by changing local communities and food
chain patterns, enhancing sedimentation, and alter-
ing water current direction and velocity (Kaspar et al.
1985, Tenore et al. 1985, Baudinet et al. 1990, Hatcher
et al. 1994, Grant et al. 1995). Seaweed cultivation can
modify the environment by changing sediment com-
position and dynamics, the meiobenthos, and by in-
troducing exogenous materials (e.g. plastic), fertiliz-
ers, or pesticides (Olafsson et al. 1995, Buschmann et
al. 1995, 1996a). Nevertheless, the effects of shellfish
and seaweed cultivation are less dramatic than those
associated with intensive fish and shrimp cultures be-
cause the latter result in a net addition of organic ma-
terial and dissolved nutrients to the environment
(Hopkins et al. 1995). The cultivation of shrimp and
carnivorous fish species also appropriates very large
ecosystem areas, that is, a large ecological footprint,
to sustain their production (Kautsky et al. 1997b,
Folke et al. 1998). This dependence on both local ec-
osystem support (e.g. clean water) and external eco-
system support (e.g. larvae and feed production) is
not accounted for in the calculation of market prices
and seldom included in models of fisheries and aqua-
culture management. Intensive aquaculture is, for this
reason, not a substitute for fisheries because it largely
depends on fisheries to harvest resources that are
given to the cultured species in the form of feed pel-
lets (Folke and Kautsky 1989, 1992). Feed companies
are now developing new research and development
structures to identify alternative sources of oil (espe-
cially of polyunsaturated fatty acids) and protein to
counter diminishing supplies of raw material. Food
supply stability, food safety, and traceability are be-
coming key worldwide issues. Notwithstanding the sig-
nificant improvements in feed quality and the fact
that land- and sea-vegetable substitutes have to some
extent been obtained during recent years, it is still
necessary to develop incentives and research pro-
grams to prevent the further misuse of marine ecosys-
tems (Naylor et al. 1998, 2000).
In the above context, integrated aquaculture has
been proposed as a means to develop environmen-
tally sound aquaculture practices and resource man-
agement through a balanced ecosystem approach to
avoid pronounced shifts in coastal processes. Fed
aquaculture (e.g. finfish, shrimp) needs to be inte-
grated with organic and inorganic extractive aquacul-
ture (e.g. shellfish and seaweed). Conversion, not di-
lution, is the solution to pollution so that the wastes of
one resource user become a resource (fertilizer or
food) for the others. Integrated aquaculture provides
nutrient bioremediation capability, mutual benefits
to the cocultured organisms, economic diversification
977
SEAWEEDS IN SUSTAINABLE INTEGRATED AQUACULTURE
by producing other value-added marine crops, and
increased profitability per cultivation unit for the
aquaculture industry (Chopin et al. in press). Integrat-
ing seaweeds into fish/shrimp aquaculture not only
counterbalances nutrient inputs but also other meta-
bolic aspects, such as dissolved oxygen, acidity, and
CO
2
levels, in one step. In contrast, nitrification filters
compete with fish/shrimp for dissolved oxygen and
alter alkalinity, thus requiring complex additional me-
chanical monitoring (electrodes) and control (aera-
tors, pumps) devices.
The use of seaweeds integrated with fish cultures
has been studied in open-water system conditions in
Canada, Japan, Chile, and the United States (Petrell
et al. 1993, Hirata and Kohirata 1993, Hirata et al.
1994, Petrell and Alie 1996, Troell et al. 1997, Chopin
and Yarish 1998, Chopin et al. 1999b); in enclosed
floating systems in Norway (Bodvin et al. 1996); and
in land-based cultures in the United States (Ryther et
al. 1975), Israel (Vandermeulen and Gordin 1990,
Cohen and Neori 1991, Neori et al. 1991, 2000, Shpi-
gel et al. 1993, Krom et al. 1995), Spain (Jimenez del
Río et al. 1994, 1996), Sweden (Haglund and Peder-
sén 1993), and Chile (Buschmann 1996, Buschmann
et al. 1994, 1996b). This review summarizes these re-
sults, provides a critical analysis, and determines a
general conceptual framework. To achieve these goals,
we analyze some key concepts, provide a summary of
results obtained with marine open-water and land-
based systems, introduce financial tools that permit
internalization of environmental costs, and finally dis-
cuss their future applicability, especially for countries
experiencing major finfish aquaculture development.
integrated aquaculture is not a new concept
Asian countries, which provide more than two thirds
of the world’s aquaculture production, have been
practicing integrated aquaculture, through trial and
error and experimentation, for centuries (Li 1987,
Tian et al. 1987, Wei 1990, Liao 1992, Edwards 1992,
1993, Chan 1993, Chiang 1993, Qian et al. 1996). In-
terestingly, civilizations most successful at developing
integrated aquaculture systems are the ones that treat
wastes as valuable resources to be reused as they have
understood the meaning of the word
recycling
for cen-
turies. Integrated farming, especially in freshwater
and brackish pond systems, is an ancient practice in
China, which has become more refined as a conse-
quence of the agricultural and rural development pol-
icies implemented since 1949. These policies were
motivated by the need to maximize productivity per
unit of land and water bodies and were based on di-
versified self-reliance in food and basic raw material
production and the philosophy that the by-products
(wastes) from one resource use must become an in-
put into another use of resources (Ruddle and Zhong
1988). Western countries are regularly reinventing
the wheel (Ryther et al. 1979, Indergaard and Jensen
1983, Kautsky et al. 1996, Chopin et al. 1999b). How-
ever, the determination to develop integrated aqua-
culture systems will only come about if there is a ma-
jor change in the attitude of consumers toward eating
products cultured on wastes and in political, social,
and economic reasoning by seeking sustainability,
long-term profitability, and responsible management
of coastal waters.
The Western world tends to focus on high value
and high production monoculture. Interestingly, this
trend can now be observed among Asian newcomers
to aquaculture as well, especially those involved with
marine species, who are forgetting the good old prin-
ciples of integrated aquaculture because of the temp-
tation of short-term financial gain with only fish or
shrimp aquaculture. Fortunately, nature does not take
long to remind people of the common sense princi-
ples on which it functions (Rawson et al. in press).
When an innovative aquaculture practice is success-
fully (i.e. economically profitable) developed by a few
people, others follow in the same region, which often
leads to geographically highly concentrated, high-den-
sity monoculture systems. This approach to aquacul-
ture eventually leads to a deterioration of the quality
of the environment, on which fish health is so depen-
dent, because disease outbreaks are facilitated by the
concentration of organisms and stressful environmen-
tal conditions. When aquaculture takes place in pub-
lic waters (the Commons), to whom the primary re-
sponsibility falls for maintaining a balance between
environment quality and aquaculture production very
often becomes an unresolved issue, which is often
handed, by default, to one or more government re-
source management agencies faced with a formidable
task and often criticized by all sides.
One of the most difficult tasks of resource manag-
ers and policy advisors is understanding the assimila-
tive capacity of coastal ecosystems under cumulative
pressure as competing anthropogenic activities in-
crease in the coastal zone (sewage effluents, urban/
rural effluents, precipitation, agricultural/industrial
runoffs, aquaculture, etc.). Most impact studies on
aquaculture operations have typically focused on or-
ganic matter/sludge deposition because they are eas-
ily noticeable and measurable. Inorganic effluents,
such as nitrogen and phosphorus, which are neither
visible nor easily measured, have generally received
much less attention because of the common human
attitude of “out of sight, out of mind.” Moreover, it is
difficult to measure small long-term changes, and past
studies, focusing on local measurements, have often
failed to document dispersal patterns of dissolved nu-
trient fractions. The inorganic output of aquaculture
is emerging as a pressing issue as nutrification of
coastal waters is a worldwide phenomenon (Beveridge
1996, Kautsky et al. 1997a, Chopin et al. 1999b). As an
example, a seaweed monitoring program in the Bay of
Fundy, Canada, has demonstrated that seaweeds can be
excellent bioindicators of nutrification/eutrophication
and reveal that certain sites in the Bay of Fundy show
symptoms of environmental stress (Bates et al. 2001).
978
THIERRY CHOPIN ET AL.
Seaweeds can also be useful tools for measuring
the zone of influence of an aquaculture site, because
they are integrators of bioavailable nutrients over
time (Troell et al. 1997, Chopin, unpublished data).
The Atlantic salmon (
Salmo salar
Linnaeus) aquacul-
ture industry in New Brunswick, Canada, is geograph-
ically highly concentrated in the Quoddy Region.
Eighty-seven sites produced 20,230 tons in 1999 (Egan
2000) and 30,000 tons in 2000 (N. Halse, New Bruns-
wick Salmon Growers Association, personal communi-
cation). With improvements in feed composition, di-
gestibility, and conversion efficiency in recent years,
the annual discharge per ton of salmon has been re-
duced: from 78 kg nitrogen and 9.5 kg phosphorus in
the early 1990s (Ackefors and Enell 1994) to current
estimates of 35.0 kg nitrogen and 7.0 kg phosphorus
(ICES 1996, Department of Fisheries and Oceans
Canada 1997, Chopin et al. 1999b, H. Ackefors, per-
sonal communication). Consequently, the exogenous
nitrogen and phosphorus inputs into coastal waters
through aquaculture operations in the region were
1,050 and 210 ton, respectively, in 2000. Contrary to
common belief, even in regions of exceptional tidal
and apparent flushing regimes like the Bay of Fundy,
water mixing and transport may be limited and water
residency time can be locally prolonged (Page 2001).
Hence, nutrient bioavailability remains significant in
some areas for a relatively long period of time in
terms of assimilative processes. The finfish aquacul-
ture industry should not be singled out because it is
the “new kid on the coastal block.” However, as a rela-
tively new contributor to the overall nutrification of
coastal waters, it should not be exempt from develop-
ing innovative practices that ensure the remediation
of the consequences of its activities.
This is precisely when one of the contributions of
seaweeds to coastal ecosystems must be recognized
and used. Unfortunately, it is striking to realize that—
especially in the marine biology community in the
Western world, historically dominated by zoologists
who have been “kingdomly incorrect” for decades—
the fundamental roles and contributions of seaweeds
to coastal processes have frequently been either ig-
nored or misunderstood and that seaweeds are rarely
factored into modeling equations of coastal systems.
Seaweeds are frequently cataloged as alternative or
new species for aquaculture by many agencies. It is,
however, worth noting that these biological systems
have been withstanding the pressure and selection of
evolution over a considerable period of time. For ex-
ample, the genus
Porphyra
, a taxon selected for inte-
grated aquaculture development (Chopin et al. 1999b),
is considered one of the most ancient red algae, with
fossils dating from 425 million years ago (Campbell
1980). The organismal morphological design of
Por-
phyra
has been well engineered in the evolutionary
process for nutrient uptake and rapid growth. The
mono- or distromatic thalli are typically 20–160
m
thick (Bird and McLachlan 1992, Chopin et al. 1999b),
giving them a very high surface area to volume ratio
(more membrane surface for uptake) and placing cells
very close to pools of inorganic nutrients.
Moreover, seaweeds are definitely not new species
to aquaculture. For example, the culture of
Porphyra
was established in Japan ca. 400 years ago (Ohno and
Largo 1998). Considering the large quantity of sea-
weeds produced through aquaculture, many times
surpassing in tonnage, and sometimes also in reve-
nue, many animal aquaculture productions, seaweeds
deserve more conspicuous exposure and recognition.
In 1996, the brown alga
Laminaria japonica
Areschoug
was the top species in terms of annual production of
all types of aquaculture (fresh water, brackish water,
and marine environments) and third in terms of an-
nual economic value (Table 1). In 1998, of the 39.4
million ton of aquaculture production valued at US$53
billion, seaweeds contributed 8.6 million ton (21.7%)
valued at US$5.9 billion (11.1%; Hanisak 1998, Anon-
ymous 2000). In the marine environment, 44% of the
1998 annual production was provided by seaweeds (47%
by mollusks, 8% by finfish, and 1% by crustaceans).
In 1995, China produced more than 4.8 million
tons of cultivated seaweeds, mainly of the brown algae
Laminaria
and
Undaria
and of the red algae
Porphyra
,
Gracilaria
,
Kappaphycus
, and
Betaphycus
, which together
represented 70.6% of the world’s seaweed aquacul-
ture production (6.8 million tons, itself representing
87.1% of the worldwide commercial harvest of sea-
weeds, estimated at 7.8 million tons; Hanisak 1998,
Fei et al. 1998). Such a tremendous biomass certainly
provides a significant buffer capacity along the Chi-
nese coast in terms of nutrient assimilation and con-
version. Physiologically, seaweeds can be viewed as re-
newable biological nutrient scrubbers that take up
nutrients very much like sponges absorb water. How-
ever, like any sponge, they can become saturated.
This validates the sustainable harvesting of seaweeds
and their cultivation integrated into fed-type opera-
tions (periodic removal of saturated tissues and there-
fore of significant amounts of nutrients to allow re-
growth of new material to continue the scrubbing
process). The target should be the development of
enough competition for nutrients by cultivation of de-
Table
1. Worldwide annual production and economic value of
top species in aquaculture in 1996 (Hanisak 1998, Anonymous
1999).
Species
Annual production Annual value
Million tons Rank Billion US$ Rank
Laminaria japonica
(kelp) 4.17 1 2.95 3
Crassostrea gigas
(Pacific cupped oyster) 2.92 2 3.23 2
Hypophthalmichthys molitrix
(silver carp) 2.88 3 2.79 4
Penaeus monodon
(giant tiger prawn)
0.60
10 3.93 1
Salmo salar
(Atlantic salmon)
0.60
10 1.87 7
979
SEAWEEDS IN SUSTAINABLE INTEGRATED AQUACULTURE
sirable and profitable algal crops to reduce nutrient
concentrations in seawater and the biomass of prob-
lem species below the threshold of devastating and
costly hypertrophic events such as green tides (exten-
sive blooms of macroalgae such as
Enteromorpha
,
Ulva
,
and
Cladophora
), red or brown tides of harmful mi-
croalgal blooms, and blooms of short-lived filamen-
tous algae such as
Ectocarpus
and
Pilayella
(Bruno et al.
1989, Merrill 1996, Schramm and Nienhuis 1996, Bates
et al. 2001).
application of algal nutrient physiology to
integrated aquaculture
General concepts about nutrient uptake can be
found in Lobban and Harrison (1994). Nutrient up-
take kinetics, assimilation, storage, response to nutri-
ent additions, response to different forms of nutrients
(e.g. nitrogen as ammonium versus nitrate, nitrite or
urea), nutrient ratios, critical tissue nutrient contents,
and growth kinetics were discussed by Harrison and
Hurd (2001) with respect to aquaculture. To optimize
the seaweed component of an integrated aquaculture
system, particular attention should be given not only
to physical and chemical factors (such as light, tem-
perature, effluent nutrient concentration and flux,
water motion, etc.) but also to biological factors such
as interplant variability (hence the need for selec-
tion), nutrient prehistory, type of tissue in culture, life
history stages/age, control of parameters triggering
reproduction stages, surface area to volume ratio of
thalli, and morphological changes induced by cultiva-
tion techniques (e.g. ruffling, tendency to obtain sphere-
shaped plants, production of hairs).
Seaweed cultivation in open and tank cultures have
been extensively discussed (Hanisak 1987, Santelices
and Doty 1989, McLachlan 1991, Craigie and Shack-
lock 1995, Friedlander and Levy 1995, Chopin and
Yarish 1998, Craigie et al. 1999). However, it is impor-
tant to note that from a bioremediation point of view,
several concepts must be clearly defined, because they
have different interpretations and meanings. The nu-
trient uptake efficiency is the average reduction (%)
in nutrient concentration in water (also estimated by
the nutrient accumulation in algal tissues). Nutrient
uptake rate is the amount of nutrients removed per
unit of time. A variant can be the nutrient area uptake
rate, which is the amount of nutrients removed per
unit of seaweed-covered area (such as a pond) per
unit of time.
These variables depend on the environmental con-
ditions experienced by the culture during a specific
period of time and on culture parameters such as the
nutrient prehistory of the plants, growth rate and
stocking density, tank depth, water turnover rate, and
biomass harvesting frequency. For example, Vander-
meulen and Gordin (1990), Cohen and Neori (1991),
Neori et al. (1991), and Jimenez del Río et al. (1994)
found that increasing ammonium loading rates per
unit area of
Ulva
tank cultures fed with fish effluents
led to decreased dissolved nitrogen uptake efficiency
but increased nitrogen area uptake rate.
Ulva
yield
and protein content also increased with increasing
rates of ammonium supply per unit area. Studies car-
ried out in Chile came to the same conclusion, as am-
monium uptake efficiency decreased with the water
turnover rate, but the uptake per gram of
Gracilaria
per time increased (Muñoz and Varas 1998). Both
Ulva
and
Porphyra
perform better as nitrogen scrub-
bers with ammonium than with nitrate, which is excel-
lent in the context of intensive fish aquaculture,
where most of the nitrogen is released as ammonium
(Neori 1996, Carmona et al. 2001).
The relative importance of nutrient uptake effi-
ciency and rate depends on the purpose of the cultiva-
tion system. If the aim is to have clean effluent dis-
charges, nutrient uptake efficiency is important. If the
aim is to increase biomass production, resulting in a
comparatively smaller reduction of nutrients in the
water being discharged, then nutrient uptake rate
should be monitored. Neori et al. (1996) showed,
however, that by recycling the water of a fish pond
through a seaweed pond, it was possible to simulta-
neously achieve high nutrient uptake efficiency and
rate. This requires adjusting the seaweed pond area,
with its known average daily uptake rate (in the case
of
Ulva
, over 40 kg ammonium-N per hectare per day)
to the expected rate of fish nutrient production
(about 45 kg ammonium-N per 100 tons of sea bream
per day). Recycling the water between the two ponds,
at the proper rate, exerts high nutrient loading rates
on the seaweed biofilter and results in both high nu-
trient removal efficiency and rate. The addition of
one or several seaweed ponds, in series of decreasing
size, at the outflow of the culture system as a final pol-
ishing step can increase the overall efficiency of am-
monium removal even further.
review of results obtained with marine
open-water and land-based systems
Systems using seaweeds for the removal or conver-
sion of wastes fall into two groups: open-water or land-
based cultivation systems. In open-water systems,
waste disposal and removal are difficult to monitor
and control. Despite the fact that such systems have
been operating in an empirical manner for centuries
in Asia, our understanding is limited by the restricted
number of scientific studies on such integrated sys-
tems, because of the complex multidisciplinary ap-
proach they require, rendered even more complex by
often unpropitious commercial and regulatory set-
tings (Petrell et al. 1993, Newkirk 1996, Petrell and
Alie 1996, Troell et al. 1997, 1999b, Chopin et al.
1999a,b). Chopin et al. (1999b) developed an aqua-
culture project integrating
Porphyra
(nori) and salmon.
For rapid growth and appropriate marketable pig-
mentation,
Porphyra
requires constant availability of
nutrients, especially in the summer when temperate
waters are generally nutrient depleted. Cultivation of
980
THIERRY CHOPIN ET AL.
nori in the proximity of salmon alleviates this nutrient
depletion by using the constant nutrient supply of the
fish farm, which is then valued and managed. This
represents a clear case of mutual benefits for the co-
cultured organisms when meaningful developments
in integrated coastal zone management are sought: sea-
weeds use the nutrients required for their growth, while
contributing to water quality improvement around fish
for their health enhancement. Chopin et al. (1999b)
calculated that 27 and 22 nori nets (18 m
1.8 m)
would be necessary for the complete removal of phos-
phorus and nitrogen released per ton of fish per year,
respectively. However, the ultimate goal should be to
reduce nutrient concentrations in seawater below the
threshold triggering hypertrophic events, thus requir-
ing fewer nets. Unfortunately, such triggering levels
are often unknown, highly site specific, and many
other environmental factors may be involved in the
development of hypertrophic conditions. Some brown
algae (Subandar et al. 1993, Ahn et al. 1998) and red
algae (Buschmann et al. 1996b, Troell et al. 1997,
Chopin et al. 1999b) show a high capacity for remov-
ing nutrients from fish effluents, and seaweed produc-
tion is higher in areas surrounding fish cages than in
areas remote from aquaculture operations (Troell et
al. 1997). Nonetheless, modeling research still needs
to be conducted to define the nutrient uptake effi-
ciency and assimilative capacity of these systems. By
using the red alga
Gracilaria chilensis
Bird, McLachlan
et
Oliveira, Troell et al. (1997) concluded that a sus-
pended culture of 1 ha, at a stocking density of 1 kg
WW
m
2
(0.5 kg WW at the two depths,
1 m and
3 m), removes 5% of the dissolved inorganic nitro-
gen and 27% of the dissolved inorganic phosphorus
released from a 227-ton mixed fish farm (coho salmon,
Oncorrhynchus kisutch
Walbaum, and rainbow trout,
O. mykiss
Walbaum), equivalent to a reduction of 1,020
kg and 375 kg, respectively. One thing to keep in mind
is that fish culture is three dimensional (sea cages),
whereas seaweed culture is almost bidimensional (sur-
face nets or shallow rope cultures) because it is de-
pendent on the solar radiation reaching the first few
meters underwater. Because fish are cultivated in a
relatively small surface area, achieving a significant re-
moval of fish dissolved wastes requires that seaweed
cultivation is carried out at high densities and increas-
ing depths, which may be advantageous in the sum-
mer to avoid pigment photodestruction and can fa-
cilitate the operation of vessels for the fish-related
activities of a farm. Nevertheless, from an economic
point of view, suspended seaweed farming appears to
be commercially interesting (Petrell et al. 1993, Troell
et al. 1997, Chopin et al. 1999b). The agarophytic alga
G.
chilensis showed higher agar yields and increased
gel strength when cultivated near salmon cages (Weid-
ner and Bello 1996).
Porphyra purpurea
(Roth) C. Agardh
and
Porphyra umbilicalis
(Linnaeus) J. Agardh had higher
phycoerythrin and phycocyanin contents when culti-
vated in the proximity of salmon cages (Chopin et al.
1999b).
A common misconception is that all present aqua-
culture nutrification impacts will disappear when oper-
ations move on land, a solution presented by some as
the way of the future for the aquaculture industry. It
will certainly alleviate the problem of dilution of the
nutrient loading in bodies of water that becomes very
difficult to monitor and treat. Concentrated effluents
from on-land aquaculture operations will remain,
however, to be channeled through pipes and to be ap-
propriately and profitably treated—mechanically, chem-
ically, and, most economically, by biological means—
before being reused (closed systems) or discharged
(open systems). Fish effluents produced by land-based
systems are comparatively easier to treat than those
from open systems (Seymour and Bergheim 1991,
Troell et al. 1999a). Experimental projects began in
the 1970s (Haines 1975, Ryther et al. 1975, Tenore
1976, Langton et al. 1977, Fralick 1979, Harlin et al.
1979). During the last decade, renewed interest in in-
corporating macroalgae as the biofilter link in inte-
grated carnivore–herbivore polyculture systems has
produced new approaches and practical technologies
(Vandermeulen and Gordin 1990, Cohen and Neori
1991, Neori et al. 1991, 1996, 1998, 2000, Haglund
and Pedersén 1993, Buschmann et al. 1994, 1996b,
Krom et al. 1995, Martínez and Buschmann 1996,
Shpigel and Neori 1996, Neori and Shpigel 1999, Nel-
son et al. 2001). These studies indicate that seaweeds
can assimilate as much as 90% of the ammonium pro-
duced by intensive fish culture (Cohen and Neori 1991,
Neori et al. 1991, 1996, Jimenez del Río et al. 1994,
Buschmann et al. 1996b, Neori and Shpigel 1999).
Enander and Hasselström (1994) integrated the cul-
ture of prawn (
Penaeus monodon
), mussel (
Mytilus edu-
lis
), and the red alga
Gracilaria
sp.; they recorded a re-
duction in the effluent of 81% for ammonium, 19%
for nitrate, 72% for total nitrogen, 83% for phos-
phate, and 61% for total phosphorus.
The main issue in the effective implementation of
these systems is their optimal functioning, which re-
quires an in-depth understanding of the physiology
and nutrition of the selected species. With seaweeds,
like with many organisms, the different physiological
processes taking place have different requirements
and optima (Lobban and Harrison 1994, Harrison
and Hurd 2001). Consequently, the optimization of
the overall efficiency of a cultivation system can be
complex because it will require finding of a compro-
mise between apparently conflicting objectives (e.g.
biomass or particular compound production versus
bioremediation efficiency; Chopin and Yarish 1998).
For example, growth, nutrient (nitrogen and phos-
phorus) uptake, carrageenan or agar production, and
phycocolloid quality respond differentially to nutrient
enrichment (Neish et al. 1977, Chopin et al. 1990,
1995, Chopin and Wagey 1999, Buschmann et al. 2001).
In tank culture, nutrient availability can be con-
trolled by changing the water flow. By increasing the
water flow nutrient flux increases, which allows a high
biomass production of nutrient-sufficient seaweeds;
981
SEAWEEDS IN SUSTAINABLE INTEGRATED AQUACULTURE
however, the nutrient uptake efficiency is low and nu-
trient concentrations remain high in the effluents.
On the other hand, if the water flow is low, nutrients
become limiting and macroalgal biomass production
decreases, but the nutrient uptake efficiency is higher
and the nutrient concentrations in the effluents can
be lower. Of course, this is within the physiological as-
similative capabilities of the cultivated organisms. This
emphasizes that to optimize a system not only should
its main target(s) be clearly established, but the ap-
propriate species should be selected based on a thor-
ough understanding of the organism (Hanisak 1998).
If a seaweed is only used as a biofilter, previously iden-
tified low commercial value species like
Ulva
can be
used to depurate fish effluents (Cohen and Neori
1991, Hirata and Kohirata 1993, Jimenez del Río et al.
1994). However, this apparent bioremediation merely
shifts the problem of waste disposal as the algal scrub-
ber will in turn need to be disposed of or treated. On
the other hand, species like
Gracilaria
,
Porphyra
,
Pal-
maria, Chondrus
, or
Laminaria
offer both high biore-
mediation efficiency and commercial value in estab-
lished markets (phycocolloids, human consumption,
etc.) or developing ones (diets for other high-valued
aquaculture organisms [herbivorous fish, abalone, sea
urchin] and other niche markets; Haglund and Ped-
ersén 1993, Buschmann et al. 1996b, Hanisak 1998,
Yarish et al. 1998, Chopin et al. 1999a). Recently,
Neori and Shpigel (1999) demonstrated that
Ulva lac-
tuca
Linnaeus, rendered protein-rich through its use
as fish pond biofilter, acquires nutritional value that
increases the overall profitability of an aquaculture
operation per cultivation unit as well as per resource
unit (water, food, energy, and labor). The recycling
Sparus aurata
(gilthead sea bream)/
Ulva lactuca
(sea
lettuce) system developed by Neori et al. (2000) al-
lows for the reduction of seawater consumption and
energy by 75%, while also producing 7 kg of
Ulva lac-
tuca
per kg of fish, which are then converted into 0.5
kg of the lucrative macroalgivore abalone (a similar
approach can be used with sea urchin).
When the value added for the service of improving
water quality and coastal health is finally recognized,
quantified and combined with that of the principal
crop (the traditional finfish or shrimp aquaculture), the
seaweed component of an integrated aquaculture sys-
tem will be understood to significantly improve the
success of a diversified operation. An accrued benefit
to operators of this type of aquaculture is the fact that
the currently discharged (unassimilated and/or ex-
creted) phosphorus and nitrogen, which represent a
loss of money in real terms, will be captured and con-
verted into the production of salable biomass and bio-
chemicals, hence generating revenues that may more
than compensate for the expenses. Additionally, as
legislative guidelines, standards, and controls regard-
ing the discharge of inorganic nutrients into coastal
waters become more stringent in many countries, bio-
remediation via the production of seaweeds will help
the fish aquaculture industry avoid noncompliance.
internalizing environmental costs
The technical and economic cost–benefit analysis of
a land-based center for the production of salmon and
seaweeds in Chile was conducted by Alvarado (1996).
The cost of producing salmon depends largely on the
stocking density achieved in the fish culture. For ex-
ample, the investment for 200 tons of fish production
increases from US$250,000 to US$6,500,000 when the
stocking density declines from 60 to 15 kg
m
3
. The
operational cost also increases with increasing culture
size but decreases with the stocking density because of
the water requirements, which leads to different costs
for each fish culture density. With an average price of
US$4.8
kg
1
for salmon, the income for 600 tons of net
production is US$2,880,000. Considering the water flow
requirements for 200 and 600 net tons of salmon, the
production of seaweed increases from 500 to 1,700 wet
tons (Buschmann et al. 1996b). Assuming a conserva-
tive price of US$1.00
kg
1
(dry) for
Gracilaria
, the ad-
ditional income in a 600-ton salmon culture unit can
reach US$550,000.
Considering the production of solid and dissolved
wastes based on the amount of nitrogen and phospho-
rus incorporated to the system given by Buschmann et
al. (1996b) and applying a cost to nutrients released to
the environment based on calculations from Folke et
al. (1994; US$6.4 to 12.8
kg
1
for nitrogen and US$2.6
to 3.8
kg
1
for phosphorus, based on treatment costs in
Swedish sewage treatment plants), it is possible to inter-
nalize the total environmental cost for 250 tons of gross
fish production at US$201,411. However, when consid-
ering the savings realized by integrating the culture of
Gracilaria
to minimize the disposal of nitrogen and
phosphorus to the environment, the total environment
cost is only US$64,000, which represents a reduction of
68.2%. Table 2 shows the different levels of profitability
that can be reached, with farms of different net pro-
ductions and different stocking densities, when envi-
ronmental costs are not internalized (present situation
Table
2. Profitability analysis using the net present value (NPV
in US$) and internal rate of return (IRR in %) of a culture
system simulating three different net salmon productions (200,
400, and 600 tons) and four different fish stock densities (15, 30,
45, and 60 kg
m
3
) without internalizing the total environmental
costs.
Profitability indicators
Fish net production Stocking density NPV IRR
200 15 n.p. n.p.
30 n.p. n.p.
45 455,692 24.1
60 685,939 30.0
400 15 n.p. n.p.
30 814,882 21.9
45 1,965,197 34.3
60 2,498,356 42.2
600 15 n.p. n.p.
30 2,065,330 26.2
45 3,743,201 40.0
60 4,569,269 47.8
n.p., no profit.
982 THIERRY CHOPIN ET AL.
throughout the world). If laws or regulations were im-
plemented to have aquaculture operations responsibly
internalize their environmental costs, a significant re-
duction of their profitability would occur (Table 3). By
integrating the culture of the nutrient scrubber Gra-
cilaria, environmental costs of waste discharges are sig-
nificantly reduced and profitability is significantly in-
creased (Table 4). Even if it does not reach the
profitability of the first case scenario in the short term,
it gains stability and sustainability for the culture system
and reduced environmental and economic risk in the
long term, which should make financing easier to ob-
tain (Brzeski and Newkirk 1997).
conclusions
The accelerated development of intensive fed aqua-
culture throughout the world is not without regional-
ized impacts, especially when the activities are highly
concentrated or located in suboptimal sites. Unfortu-
nately, impacts are often realized after environmental
stresses become obvious because of our general lack
of understanding of the assimilative capacity of coastal
waters and its predictive modeling (Rawson et al. in
press). Responsible aquaculture practices should be
based on a balanced ecosystem management ap-
proach, the basic premise of which is to incorporate
the biological and environmental functions of a di-
verse group of organisms into a unified system that
maintains the natural interactions of species and al-
lows an ecosystem to function sustainably.
One common sense solution is the development of
integrated systems by combining fed and extractive
aquaculture at several trophic levels. By significantly
reducing the total environmental costs of aquaculture
operations, this approach should find increasing envi-
ronmental, economic, and social acceptability, espe-
cially if the “user pays” concept gains momentum as a
tool in integrated coastal management (Soley et al.
1994, Buschmann et al. 1996a, Coastal Zone Canada
Association 2001). The development of such practices
would certainly be less expensive and less labor inten-
sive than implementing and respecting regulations or
laws on conventional waste treatment enacted by state
or governing agencies (Folke et al. 1994).
To successfully develop integrated aquaculture sys-
tems, much research and development remains to be
undertaken, particularly in the following areas:
• Transfer and modification of cultivation tech-
nologies to local environments and socioeco-
nomics;
• Development of the cultivation of native species
of marketable value that will be fast growing at
different times of the year and in diverse habi-
tats;
• Site-specific biological, chemical, physical, and
socioeconomic modeling to define the appro-
priate proportions between the different cocul-
tured organisms;
• Development of a regulatory and legislative
management framework with enough flexibility
to allow experimental and innovative practices
at a meaningful preindustrial scale.
Pivotal for the success of the aquaculture industry
in the future will be the wise investment in research
and development (not development and research, as
is seen too often) and the implementation of current
novel technologies and concept, to move in new di-
rections to optimize its efficiency through diversifica-
tion, while maintaining the health of coastal waters.
The aquaculture industry is here to stay in our “coast-
alscape”: it has its place in the global seafood supply
and demand and in the economy of coastal communi-
ties. To help ensure its sustainability, however, it needs to
responsibly change its too often monotrophic practices
by adopting polytrophic ones to become better inte-
grated into a broader coastal management framework.
Table 3. Profitability analysis using the net present value (NPV
in US$) and internal rate of return (IRR in %) of a culture
system simulating three different net salmon productions (200,
400, and 600 tons) and four different fish stock densities (15, 30,
45, and 60 kgm3), considering the internalization of the total
environmental costs.
Profitability indicators
Fish net production Stocking density NPV IRR
200 15 n.p. n.p.
30 n.p. n.p.
45 n.p. n.p.
60 n.p n.p.
400 15 n.p. n.p.
30 n.p. n.p.
45 n.p. n.p.
60 339,186 19.2
600 15 n.p. n.p.
30 n.p. n.p.
45 505,167 18.6
60 1,330,517 25.4
n.p., no profit.
Table 4. Profitability analysis using the net present value
(NPV in US$) and internal rate of return (IRR in %) of an
integrated culture system simulating three different net salmon
productions (200, 400, and 600 tons) and four different fish
stock densities (15, 30, 45, and 60 kgm3), considering the
internalization of the total environmental costs reduced by the
nutrient scrubbing capacity of Gracilaria chilensis and its
conversion into another commercial marine crop.
Profitability indicators
Fish net production Stocking density NPV IRR
200 15 n.p. n.p.
30 n.p. n.p.
45 39,982 15.8
60 270,230 20.8
400 15 n.p. n.p.
30 n.p. n.p.
45 1,133,772 25.7
60 1,666,931 32.2
600 15 n.p. n.p.
30 818,195 19.4
45 2,496,785 30.3
60 3,322,135 37.5
n.p., no profit.
983
SEAWEEDS IN SUSTAINABLE INTEGRATED AQUACULTURE
Supported by the Natural Sciences and Engineering Research
Council of Canada (research grants and AquaNet Network of
Centres of Excellence in Aquaculture), FONDECYT 1940816
and Project C.I.C.S.-EULA Genova-P.U.C. Ch. from Chile, the
Swedish International Development Cooperation Agency (Sida),
the Israeli Department for Energy and Infrastructure, Euro-
pean Union and Israeli Department of Science joint programs,
and a USA-Israel BARD grant, and the State of Connecticut
Critical Technology Grant Program, and the Connecticut, New
Hampshire and New York Sea Grant College Programs, USA.
This paper is contribution no. 60 from the Centre for Coastal
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