Recirculating Aquaculture Is Possible without Major Energy
Tradeoff: Life Cycle Assessment of Warmwater Fish Farming in
Sweden
Kristina Bergman,* Patrik J. G. Henriksson, Sara Hornborg, Max Troell, Louisa Borthwick, Malin Jonell,
Gaspard Philis, and Friederike Ziegler
Cite This: Environ. Sci. Technol. 2020, 54, 16062−16070 Read Online
ACCESS Metrics & More Article Recommendations *sı Supporting Information
ABSTRACT: Seafood is seen as promising for more sustainable
diets. The increasing production in land-based closed Recirculating
Aquaculture Systems (RASs) has overcome many local environ-
mental challenges with traditional open net-pen systems such as
eutrophication. The energy needed to maintain suitable water
quality, with associated emissions, has however been seen as
challenging from a global perspective. This study uses Life Cycle
Assessment (LCA) to investigate the environmental performance
and improvement potentials of a commercial RAS farm of tilapia
and Clarias in Sweden. The environmental impact categories and
indicators considered were freshwater eutrophication, climate
change, energy demand, land use, and dependency on animal-
source feed inputs per kg of fillet. We found that feed production
contributed most to all environmental impacts (between 67 and 98%) except for energy demand for tilapia, contradicting previous
findings that farm-level energy use is a driver of environmental pressures. The main improvement potentials include improved by-
product utilization and use of a larger proportion of plant-based feed ingredients. Together with further smaller improvement
potential identified, this suggests that RASs may play a more important role in a future, environmentally sustainable food system.
■ INTRODUCTION
To achieve future food and nutrition security without
jeopardizing the multiple functions of ecosystems and use
resources efficiently, global food production needs to trans-
form.1 There are major differences in nutritional value,
resource requirements, and environmental footprint between
food groups and food products.2,3 Increased understanding of
the environmental performance of different production
systems’ and product nutritional qualities is key to ensuring
human health while reducing environmental pressures. In this
sense, increasing global seafood production particularly at the
expense of red meat has repeatedly been identified as a
promising strategy for improved sustainability.4,5
In European countries, dietary advice often recommends an
increased consumption of seafood6,7 based on nutritional
properties. The bulk of European seafood consumption today
consists of only a handful of species, with tuna dominating
followed by cod, farmed salmon, Alaska pollock, and shrimp.
Seafood is, however, a particularly diverse food group in terms
of nutritional value and environmental footprints.2,8,9 Around
2500 species are globally harvested from the wild and 600
species are farmed, with both systems using a wide range of
production methods.10 Some species can be produced both
from fisheries and aquaculture using methods with widely
different environmental impacts. Besides seafood from capture
fisheries being a limited resource, there are also concerns over
unsustainable fishing practices, such as for cold-water shrimp,11
and the risk of spreading of nutrients, diseases, and parasites to
the surrounding ecosystems for the current production systems
(open net-pen) for farmed salmon.12 To reduce the overall
environmental impacts of the food system, these differences are
important to identify and consider in national strategies and
policies.
Consequently, the Swedish environmental legislation is
highly restrictive in giving permits for traditional open net-
pen systems due to eutrophication in coastal waters and
because aquaculture production is marginal. Closed, land-
based recirculating aquaculture systems (hereafter referred to
as RASs) have therefore attracted interest to meet national
strategies in aquaculture development as seen also in Norway,
Received: February 21, 2020
Revised: November 13, 2020
Accepted: November 16, 2020
Published: November 28, 2020
Articlepubs.acs.org/est
© 2020 American Chemical Society
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https://dx.doi.org/10.1021/acs.est.0c01100
Environ. Sci. Technol. 2020, 54, 16062−16070
This is an open access article published under a Creative Commons Attribution (CC-BY)
License, which permits unrestricted use, distribution and reproduction in any medium,
provided the author and source are cited.
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the United States, across Europe, and China.13,14 A RAS is
generally constructed with fish tanks connected to mechanical
and biological filters and with water treatment, e.g., for aeration
and disinfection.14 The treated water is recirculated back into
the farming tanks while ammonia is converted into nitrate,
which can be denitrified or gathered together with sludge.
Being completely separated from natural ecosystems, RASs
offers solutions to the main environmental issues with open
net-pens as there is no risk of spreading nutrients,
antimicrobials, parasites, or invasive species. Many of the
recently established Swedish RAS production sites produce
tropical finfish and crustacean species, such as Nile tilapia (
Oreochromis niloticus), African Clarias catfish (Clarias gar-
iepinus), and Whiteleg shrimp (Penaeus vannamei). These
warmwater species are highly productive and require low
protein inputs15 but need to be farmed in warm water (around
30 °C).
Closed farming systems offer more controlled rearing
conditions that may contribute to a lower occurrence of
disease and a more efficient Feed Conversion Ratio (FCR) in
the RAS than traditional open net-pen systems.16 The
improved FCR is achieved through healthier fish and better
control of feeding. However, RASs require more technical
input and energy to facilitate water aeration and purification in
order to create suitable conditions for the fish to live and grow
than in open farming systems. Previous LCAs of RASs have
accordingly highlighted the environmental tradeoffs when
turning to the RAS.17,18 Ayer and Tyedmers,17 for example,
concluded that abiotic depletion (the depletion of non-
renewable resources), global warming, and acidification
impacts of the RAS powered by a generic Canadian electricity
mix are over an order of magnitude higher than those of an
open net-pen system. Song et al.,19 similarly, concluded that
electricity generation, together with feed production, domi-
nated eight out of the nine impact categories (ranging 54−95%
in total).
The goal of this study is to quantify and evaluate the current
environmental performance of tilapia and Clarias produced in
a commercial RAS in Sweden, as well as their improvement
potential, using Life Cycle Assessment (LCA). This is one of
the first LCAs evaluating a commercial RAS and the first to our
knowledge to evaluate tilapia and Clarias farmed in a RAS.
Increased understanding about the efficiency of these systems
will help guide industry, policy, and research to further
improve environmental performance and can also form a basis
for strategic decisions forming a developing sector.
■ METHODS
Goal and Scope Definition. The functional unit (FU) in
this study was 1 kg of fillets without skin of tilapia and Clarias
(excluding packaging) following cradle-to-farmgate system
boundaries. The study includes fry production, transportation
of fry, grow-out in a RAS, and associated inputs (Figure 1,
Table 1). The analysis covers impacts up to farmgate, which
also include on-site slaughtering and hand filleting of the fish
(Figure 1). Impacts associated with grow-out infrastructure
and equipment were included, while the existing buildings used
for farming and their maintenance were not. The business idea
of the company is to use empty former farm buildings whose
age (>30 years) motivates excluding their construction from
the analysis. Environmental burdens were allocated among co-
products (e.g., between fish meal and fish oil) based on mass as
well as monetary value, with results presented for both
strategies to enhance transparency and usability. Farm inputs
whose use depends on space and water volume (e.g.,
electricity, freshwater, and tanks) were divided between tilapia
and Clarias by stocking density (see the Supporting
Information, Table S1) as space and freshwater are physically
needed to maintain the grow-out, is related to stocking density
(kg fish m−3). Inputs for chemicals and equipment for water
treatment were divided by fish biomass (kg) as that correlates
to the volume of fish (Table S1).
Life Cycle Inventory Analysis. Data related to fish
farming (nursery & grow-out, slaughtering, and filleting),
representing production in 2017, were gathered directly from
the largest farmer of tilapia and Clarias in Sweden. The studied
system is a closed freshwater system with recirculating water in
Figure 1. Simplified flowchart of the studied system with primary data in white boxes and secondary data in shaded boxes. Dashed lines indicate
upstream processes.
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which fish are grown in tanks connected to mechanical drum
filters and moving bed biological filters to remove solids and
ammonia. Electric pumps and fans were used to circulate and
aerate water, and heat exchangers were used to keep water
temperature around 30 °C. Fish were slaughtered in ice baths
or by hand through piercing of the head. Filleting was also
done manually. Energy (for heating and lighting in the
combined farming and processing building and for ice
production), water (for ice baths and cleaning), and cleaning
agents needed for the slaughtering and filleting were not
possible to separate from that for the grow-out. Inputs and
outputs from the hatchery operation were based on previously
published data on Chinese tilapia hatcheries,20 adjusted to
represent a Dutch hatchery by adapting the energy source and
transportation by car (see the Supporting Information, Table
S10 for details). Excretion of nitrogen (N) and phosphorus
(P) for both farm and hatchery was calculated using a mass
balance as detailed by Henriksson et al.20 A tilapia fish feed
recipe averaged over 2017 from the producer of the aquafeed
for the relevant country was obtained and only adjusted to the
specific levels of fishmeal and fish oil used on the studied farm.
Microingredients, such as vitamins and amino acids, were
excluded since detailed composition and inventory data were
lacking. The electricity used on the farm was certified
renewable electricity from wind, but the baseline scenario
was modeled using the average Swedish electricity con-
sumption mix as to better represent the potentials of upscaling
this type of farming system rather than benchmarking this
individual farm. Also, Sweden’s most prevalent renewable
energy source is hydropower. This is already fully utilized,
suggesting that an overall increase in electricity demand needs
to come from alternative energy sources. Emission estimates
from such changes in demand are often assumed to come from
peaking power plants, such as gas and oil, or imports, but since
Sweden is expanding other renewable electricity sources, our
view is that the grid average should be used.
Life Cycle Impact Assessment. Four environmental
impacts were selected as relevant to assess for the aim of
this study: freshwater eutrophication (ILCD 2011 Midpoint
method version 1.10); climate change (IPCC 201321 with a
timeframe of 100 years); energy demand (CED version
1.1022); and land use (simply estimated as the number of
square meters needed annually from cradle-to-farmgate).
Toxicological impact would also be of interest to assess for a
food production system, but it was left out given the lack of
readily available characterization factors for relevant chemicals.
Acidification was excluded due to its large overlap with climate
change.
Dependency on marine and poultry by-product ingredients
was calculated using a slightly modified Forage Fish Depend-
ency Ratio (FFDR) from the Aquaculture Stewardship Council
(ASC) salmon standard v 1.123 (see the Supporting
Information for further information).
All LCI modeling and characterization were performed using
the SimaPro 8.5 software, with secondary data on feed
ingredients from Agri-footprint (version 4.0) and the
remaining secondary data from the Ecoinvent 3.4 database.
Greenhouse gas (GHG) emissions from land use change
(LUC) are included in the Agri-footprint data. The Agri-
footprint database provides country and crop-specific emis-
sions driven by LUC based on the PAS2050-1 framework.
Sensitivity Analysis and Alternative Scenarios.
Sensitivity analyses were performed to evaluate the influence
of modeling decisions and alternative farming practices to
identify potential improvements. We investigated the outcome
of (1) excluding LUC-associated GHG emissions, (2) utilizing
entirely crop-based feed, (3) 100% utilization of filleting by-
products, (4) Swedish renewable or global consumption mix as
the electricity source, and (5) emitting waste nutrients to
nature. When evaluating the effects of the fate of waste
nutrients, no additional potential changes in the farming
system (e.g., in equipment or energy demand) were
considered. Crop-based feed options were based on the
commercial alternative recipe for tilapia obtained from the
same aquafeed producer as described above, which can
maintain the same FCR according to the manufacturer.
Comparison with Other Farmed Fish. To put the
environmental performance of this RAS into perspective and to
bring attention to environmental tradeoffs, a comparison was
made with other RAS LCAs and with fish farmed in open
systems. In addition to climate change and freshwater
eutrophication impacts, products were compared regarding
energy consumption, fuel use, FCR, FFDR, mortality, and use
of antimicrobials. Indicators were selected to capture addi-
tional relevant sustainability aspects of aquaculture. The
comparison included LCAs on an early, experimental RAS
production of Arctic char (Salvelinus alpinus),17 a more recent
large-scale RAS production of Atlantic salmon (Salmo salar),19
tilapia and pangasius (Pangasianodon hypophthalmus) farmed
in Asia in traditional ponds or cages,20 and salmon farmed in
open net-pens.25 The two products from Asia are of the same
or similar species as studied here and of relevant origin for the
Swedish market,26 whereas net-pen farmed salmon is both a
different species and production system. It was included as it is
Table 1. Farm Inputs and Outputs per Tonne Live Weight
of Tilapia and Clarias Produced (Including Energy and
Water for Slaughtering and Hand Filleting)
tilapia Clarias
economic inputs per tonne of fish
fry (pcs) 66,768 23,276
electricity (kWh) 3086 771
diesel (l) 0.09 0.02
sodium hydroxide (kg) 0.015 0.016
sodium hypochlorite (kg) 0.30 0.31
potassium hydroxide (kg) 0.002 0.002
feed (kg) 1100 1100
hydrochloric acid, conc. 20% (kg) 0.3 0.3
transportation with truck (tkm) 6 2
plastic (kg) 2.6 2.5
iron (kg) 1.4 0.7
glass fiber plastic (kg) 4.4 1.1
environmental inputs
freshwater (m3) 76 19
land, grow-out site (m2a) 33 15
economic outputs
tilapia, live (kg) 1000
Clarias, live (kg) 1000
environmental outputs
N (kg) 30 30
ammonia (kg) 0.4 0.4
dinitrogen monoxide (kg) 0.7 0.7
ammonium (kg) 26 26
nitrate (kg) 11 11
P (kg) 2 2
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currently one of the most consumed species in Sweden and
Europe27 and represents aquaculture practices that RAS
farming of omnivores aims to avoid (e.g., farming of
carnivorous fish and farming in open systems). To enable a
fair and harmonized comparison across studies using different
methodologies as far as possible, climate change and
eutrophication impacts were recalculated based on inventory
data on the two main drivers for these systems (feed and
energy). Here, the comparison stops at farmgate, disregarding
edible yield, the fate of by-products, and assuming identical
carbon footprints for energy and feed ingredients. While this is
simplified, it avoids the strong influence of different LUC
emission models and specific electricity mix, allowing a
comparison of the systems conceptually, rather than the
specific farms. The reported feed composition for each fish was
used to calculate impacts with Agri-footprint data, and all the
same assumptions and specific method choices as detailed
above were used.
■ RESULTS AND DISCUSSION
Life Cycle Inventory Results. The studied farm produced
20 tonnes of Clarias and 20 tonnes of tilapia in 2017. The
economic FCR was 1.1 for both species (Table 1). Filleting
was done by hand with fillet yields of 35% for tilapia and 50%
for Clarias. Filleting by-products (frames, heads, etc.) were not
utilized for food or feed, only for energy production (biogas).
All environmental burdens were consequently allocated to the
fillets. The farm had four employees who in total worked 9600
h in the year of production. Stocking density values before
slaughter were 60 and 250 kg m−3 for tilapia and Clarias,
respectively. Pumps were almost exclusively powered by
electricity, with a backup diesel generator only used on rare
occasions of power failure. Chemicals were used to adjust pH
and for cleaning.
Feeds are mainly constituted of plant-based ingredients,
predominantly maize gluten feed, wheat, and soybean meal. In
addition, 9−10% poultry by-products and 10−16% marine
ingredients were included for tilapia and Clarias (see the
Supporting Information, Tables S2 and S3).
Life Cycle Impact Assessment. Tilapia production was
consistently associated with higher impacts across all impact
categories (Table 2 and Table S4 for results per live weight),
mainly as a result of the lower fillet yields and lower stocking
density. The allocation strategy had a large influence on
absolute values, requiring caution if comparing with other
products. A major driver behind this was the large impact from
feed (Figure 2) in combination with using poultry by-products
that are associated with disproportionately large environmental
impacts.
Despite the low FCR, feed production was the main driver
behind all impact categories except energy demand for tilapia
and all four impacts and indicators for Clarias (Figure 2; for
economic allocation see Figures S1 and S2). Assessment of
microingredients was excluded due to the lack of data but
could potentially contribute with up to 10% to climate change
according to Hognes et al.24 The dominating contribution to
environmental impacts from feed has been widely observed
before in LCAs of conventional production of various
species.28−31 However, it is notable that we see that same
pattern for a product farmed in an RAS as previous LCA
studies of such systems have shown that the extent of energy-
and/or infrastructure requirements needed often overshadow
the impact of feed.19,32,33 Feed had a less dominating impact
on energy demand, where the grow-out operations that include
electricity use for farming accounted for 66% of the energy
needed to grow tilapia and 32% for Clarias. Previous LCA
studies of RASs have raised concerns about high GHG
emissions related to energy provision.17−19,33 However, the
current system had a considerably lower energy use despite
being located in a temperate country. Electricity consumption
only varied by ±15% throughout the year while maintaining a
water temperature around 30 °C in a climate that falls well
below freezing in winter. Well-insulated buildings and the use
of heat exchangers facilitated for efficient heat conservation. In
addition, there was no need to oxygenate the systems, which
can drive energy demand for the RAS.17 In contrast to findings
in LCAs of open net-pen production,34,35 the grow-out stage of
tilapia and Clarias had limited contributions to freshwater
eutrophication in comparison to feed production,30 which was
expected as nutrients were retrieved and utilized. Hatcheries
had only marginal contributions to overall impacts, as has been
concluded for many other systems.19,20
Production of both tilapia and Clarias relies on animal inputs
in feeds. For Clarias, the animal inputs are split equally
between poultry by-products and fish inputs, while the
production of tilapia relies more on poultry by-products.
Clarias uses 0.48 kg of whole fish and 0.19 kg of fish by-
products per kg of fillet, and tilapia uses 0.34 kg of whole fish
and 0.14 kg of by-products. Adding poultry by-products, the
relationship between total animal-in and fish-out in both cases
is just over a one-to-one ratio (1.21 kg per kg of tilapia fillets
and 1.33 for Clarias fillets).
Table 2. Life Cycle Impacts from the Production of 1 kg of Tilapia and 1 kg of Clarias Fillets Using Mass and Economic
Allocation
tilapia fillets Clarias fillets
impact category unit mass allocation economic allocation mass allocation economic allocation
f. eutrophication g P eq. 1.9 1.1 1.0 0.5
climate change kg CO2 eq. 14.7 7.0 9.3 4.3
land occupation m2a 10.2 4.5 5.9 2.2
energy demand MJ 235 207 81 63
Figure 2. Life cycle contribution of 1 kg of tilapia and Clarias fillets
using mass allocation.
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Sensitivity Analysis and Alternative Scenarios.
Assumptions related to emissions from land use change
strongly influenced results (Table 3; for economic allocation
see the Supporting Information, Table S5) as has been shown
in other LCAs of foods.3 Excluding the GHG emissions from
the land transformation, primarily driven by soy production on
deforested land in Brazil, would reduce the GHG emissions
from tilapia and Clarias roughly by half. This demonstrates the
major improvement potential of excluding this type of soy as
well as poultry fed soy from the feed.
Emitting nutrients to nature instead of using a biological
filter to use nutrients as the fertilizer would result in 4 times
larger eutrophication impacts for tilapia and 5 times larger for
Clarias. No additional changes in the farming system were
considered in the alternative scenario, but it is possible that a
farming system with less water filtering would save energy.
Holding sludge, however, also results in methane and nitrous
oxide emissions, both powerful GHG emissions, which was not
included, but could potentially give rise to considerable GHG
emissions. It is therefore critical that the sludge digestion is
done correctly and that the methane should ideally be
collected for use as biogas.36
Improving by-product utilization from filleting, using more
crop-based feed ingredients, and switching to renewable energy
would decrease the impacts of the farmed species for all impact
categories (ranked from most to least benefits). Of these, the
studied farm already sources renewable energy and alternative
feed sources are being investigated. Additional improvements
not tested include higher fillet yields and lower FCRs. The fate
of by-products strongly affects results since the fish fillets make
up only 35% of tilapia’s live weight and 50% of Clarias’. The
by-products are currently used for biogas production, which is
considered a waste treatment, thus not allocated any
environmental burdens related to fish production. If by-
products instead were used to produce feed ingredients and a
proportion of burdens were allocated to this part, climate
change impacts (mass allocated) would decrease considerably
(Table 3). Pure crop-based tilapia feed would further lower
impacts between 7 (freshwater eutrophication) and 28%
(climate change). This feed was, however, assumed to be
mainly based on soybean meal, wheat middlings, and rice bran
(Figure 3). Since soy and rice productions contribute to
considerable environmental impacts (e.g., from land trans-
formation as mentioned above), it is evident that when
replacing fish and poultry ingredients, attention is needed to
the type of crop-based ingredient used for overall reduction of
pressures. Examples of crop-based feed ingredients with a high
protein content and lower climate impact are fava beans and
peas (based on Ecoinvent and Agri-footprint databases). There
are different ways of viewing the use of processing by-products
from, e.g., poultry or fish processing. They could be viewed as
free from upstream burdens, as they would potentially
otherwise be wasted, and as they could even replace
production of another feed input. Here, we see the by-
products as an integrated part of the value chain that
contributes to the profitability of the main product supply
chain and thereby should also share its environmental burdens.
A switch to renewable energy had limited effects on the
results. This was expected since the Swedish electricity mix
used in the main results is dominated by nuclear and
hydropower sources. The difference in primary energy demand
between energy sources is explained by energy losses
accounted for in nonrenewable electricity production. The
environmental footprint would increase (with the exception of
land use) if the farm had been located elsewhere where
electricity production is based on less renewables than it is in
Sweden. Grow-out operation powered by the global electricity
production/consumption mix would, for example, outsize the
contribution to freshwater eutrophication for both tilapia and
Clarias and slightly exceed (by 2%) the contribution of feed to
GHG emissions for tilapia. This, together with lower energy
consumption, contributes to differences in GHG emissions in
earlier RAS LCA studies.
Land-Based Farming of Tilapia and Clarias in
Comparison to Other Farmed Fish. All fed aquaculture
systems have the environmental burden from feed in common,
but depending on the farming system, the overall resource use,
emissions, and pressures put on ecosystems are variable
(Figure 4). Some of the most critical challenges concerning
grow-out from net-pen farming are eutrophication and the
risks of spreading invasive species, disease, or antimicrobial
resistance.12,37 Those impacts can almost be eliminated in a
closed, land-based RAS but at the costs of energy and
potentially climate impacts.
It is essential to acknowledge that several environmental
impacts mentioned above have not been analyzed in
aquaculture LCAs or cannot be assessed by the LCA
methodological framework.37 For some concerns, national
statistics provide perspectives. For instance, the annual
production of 1.35 million tonnes of Norwegian salmonids in
net-pens (salmon and trout) generated around 160,000
Table 3. Sensitivity and Scenario Analysis of Results Using Mass Allocation (Relative Change Compared to Baseline Scenario)
freshwater eutrophication climate change land use energy demand
tilapia Clarias tilapia Clarias tilapia Clarias tilapia Clarias
by-products used −65% −50% −65% −50% −65% −50% −65% −50%
renewable electricity −13% −4% −2% −1% −11% −3% −35% −17%
global electricity mix +350% +109% +91% +25% −7% −2% +21% +10%
excluding land use change −46% −47%
nutrients emitted +312% +401%
vegetarian tilapia feed −7% −28% −18% −13%
Figure 3. Greenhouse gas emissions of the two tilapia feeds.
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escapees in 2018.38 Escapees are together with salmon lice the
most potent threat to the wild salmon stocks.39,40 Salmon lice
and the treatments used to control its occurrence are putting
additional pressure on ecosystems. Use of antimicrobials and
other therapeutants remain an issue for aquaculture sectors
including salmon farming in Chile or pangasius farming in
Vietnam.41,42 The environmental footprints of such treatments
in open sea-based production are relevant to consider ensuring
fair comparisons with RASs. An advantage of farming tropical
species in temperate regions is that there is no risk of
introducing nonindigenous species or mixing with wild fish
stocks genetically. An additional benefit with freshwater species
is that it allows for easy recirculation of wastes on agriculture
land since wastes do not contain salt.
Differences between open and closed systems, as well as
within systems and species, are shown in a comparison of
seven species and production systems of farmed fish regarding
both non-LCA indicators (e.g., mortality during grow-out and
antimicrobial use) and two critical LCA impact categories
(climate change and eutrophication) (Table 4). RAS-farmed
Clarias, tilapia, and salmon had the lowest eutrophication
impacts (for absolute values, see the Supporting Information,
Table S6), while Arctic char farmed in the RAS was associated
with the highest eutrophication potential. This was for Arctic
char driven by high electricity use, also contributing to GHG
emissions, while grow-out dominated eutrophying emissions
from net-pen and pond systems (Table S7). Salmon in net-
pen, however, had the lowest GHG emissions by assuming a
global electricity mix followed by tilapia in ponds and Clarias
in the RAS (Table 4). If grow-out processes instead were
powered by renewable electricity, the relative environmental
impact from feed increases (Table S8, Table S9) and
differences between aquaculture systems and species are to
some extent evened out. Antibiotics may be used in open cage
and pond systems but were completely absent (or in two cases
not measured) for the land-based RAS.
The RAS-farmed Clarias and tilapia had lower FCRs than all
other systems. Interestingly, the FCR for RAS salmon was
higher than that for salmon farmed in net-pens, which goes
against previous findings that RASs generally have lower
FCR.16 This could potentially reflect differences in optimiza-
tion. Tilapia and Clarias from Sweden had similar levels of
forage fish dependency to tilapia and pangasius farmed in Asia
(all below 1 kg of fish per kg of fish produced, meaning they
are net fish producers). The three salmonid systems all rely on
forage fish to a greater extent (from around 2 kg of fish per kilo
of fish produced for salmon in net-pen in Norway to around 4
for salmon in the RAS in China). Other animal-based inputs
into feed for the fish compared vary from 0 and 1 (Table S6).
Figure 4. Environmental pressures associated with closed land-based Recirculating Aquaculture Systems (RASs) versus open systems (cage or
pond aquaculture).
Table 4. Comparison of Some Performance Indicators for Farmed Fish per Tonne Live-Weight with Recalculated
Eutrophication Potential and GHGe Assuming Comparable Electricity and Feed Ingredient Data
system
energy use
grow-out,
kWh
fuel
grow-
out, l FCR
FFDR
(incl. by-
ps)
mortality
grow-out, kg
antibiotics
use, g
eutrophication,
% of highest
GHGe, GLO
electricity, % of
highest
GHGe, SE renewable
electricity, % of highest
tilapia, RASa 3084 0.10 1.10 0.5 0.20 0 41% 32% 72%
Clarias, RASa 771 0.02 1.10 0.7 0.25 0 32% 23% 67%
Arctic char,
RAS17
22,600 279.00 1.45 2.2 0.30 100% 100% 100%
salmon,
RAS19
7509 0.00 1.45 3.7 0.13 41% 42% 60%
Salmon, net-
pen,43,25,42
0 135.00 1.32 1.9 0.05 0.1 79% 16% 52%
tilapia,
ponds20,44
528 87.60 1.48 0.4 0.10 1.4 65% 22% 66%
pangasius,
ponds20,44
57 1.23 1.59 0.5 0.20 93.0 75% 27% 86%
aThis study; Ayer & Tyedmers;17 Song et al. 2019;19 Winther et al. 2020;43 Ziegler et al. 2013 (mortality);25 Henriksson et al. 2018 (antibiotics
use);42 Henriksson et al. 2015;20 Rico et al. 2013 (antibiotics use).44
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Environ. Sci. Technol. 2020, 54, 16062−16070
16067
Edible yields differ between species. The fillet yield for
tilapia in this study (35%) was considerably lower than those
for Clarias (50%) and for salmon (58−88% edible).45 The
relative environmental impacts would therefore change if
measured per edible yield instead of per live weight.
Furthermore, the nutritional profiles differ in terms of protein
and omega-3 contents.2
■ RECOMMENDATIONS
This study showed that the tradeoff between energy demand
(with associated emissions) and avoiding risk to the marine
environment (spreading of nutrients, disease, parasites,
antimicrobial resistance, and escapees) can be smaller than
previously reported for RASs. Along with the large improve-
ment potentials observed, this suggests that RAS-farmed fish
can contribute to a more sustainable food system including
more seafood.
It is essential to acknowledge that many highly relevant
environmental interactions for aquaculture are not possible to
assess using the LCA framework, many of which RAS systems
outperform open net-pen technology. This emphasizes the
need to look beyond LCA results when examining sustain-
ability of aquaculture.
Current small-scale farms could benefit from scaling-up,
especially when it comes to possibilities to filleting by-products
more efficiently. Up-scaling of RAS farms in Sweden would
however be made easier if the environmental legislation was
altered so permits were given based on environmental
pressures rather than on the amount of feed used, as is the
case today.
RAS systems are an emerging production technology under
continuous improvement. The results here should be regarded
as a snapshot of a still evolving industry in Sweden. The tilapia
and Clarias RAS exhibited major improvement potentials for
activities contributing most to climate change such as feed
choice and utilization of by-products. Farms should focus on
utilizing as much as possible fish and optimize toward using
low-impact feed ingredients. Future RAS farms in Sweden are
encouraged to buy specifically certified eco-labeled wind power
as this most likely would increase renewable generation
capacity rather than marginalizing other users. The studied
RAS already shows promise, and through development in more
sustainable directions identified here, land-based farming of
tropical fish can contribute to a sustainable future food sector
in Sweden.
■ ASSOCIATED CONTENT
*sı Supporting Information
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/acs.est.0c01100.
A detailed description of allocation for input data,
hatchery data, and aquafeed recipes is provided in the
Supporting Information. Results calculated with the
alternative allocation method, functional unit, and input
data are also provided (PDF)
■ AUTHOR INFORMATION
Corresponding Author
Kristina Bergman − RISE Research Institutes of Sweden,
Agrifood and Bioscience, 402 29 Göteborg, Sweden;
orcid.org/0000-0001-5888-4943;
Email: kristina.bergman@ri.se
Authors
Patrik J. G. Henriksson − Beijer Institute of Ecological
Economics, Royal Swedish Academy of Sciences, 104 05
Stockholm, Sweden; Stockholm Resilience Centre, Stockholm
University, 106 91 Stockholm, Sweden; Worldfish, 11960
Penang, Malaysia
Sara Hornborg − RISE Research Institutes of Sweden,
Agrifood and Bioscience, 402 29 Göteborg, Sweden
Max Troell − Beijer Institute of Ecological Economics, Royal
Swedish Academy of Sciences, 104 05 Stockholm, Sweden;
Stockholm Resilience Centre, Stockholm University, 106 91
Stockholm, Sweden
Louisa Borthwick − RISE Research Institutes of Sweden,
Agrifood and Bioscience, 402 29 Göteborg, Sweden
Malin Jonell − Beijer Institute of Ecological Economics, Royal
Swedish Academy of Sciences, 104 05 Stockholm, Sweden;
Stockholm Resilience Centre, Stockholm University, 106 91
Stockholm, Sweden
Gaspard Philis − Department of Biological Sciences,
Norwegian University of Science and Technology, 6009
Ålesund, Norway
Friederike Ziegler − RISE Research Institutes of Sweden,
Agrifood and Bioscience, 402 29 Göteborg, Sweden
Complete contact information is available at:
https://pubs.acs.org/10.1021/acs.est.0c01100
Notes
The authors declare no competing financial interest.
■ ACKNOWLEDGMENTS
The authors wish to thank the farm Gar̊dsfisk for generously
sharing their data. This work resulted from the SEAWIN
project funded by The Swedish Research Council Formas
(grant number 2016-00227) and NOMACULTURE project
(2013-1961-27044-74) funded by Formas and MISTRA.
P.J.G.H. undertook this work as part of the CGIAR Research
Programs on Fish Agri-Food Systems (FISH) led by
WorldFish and on Climate Change, Agriculture, and Food
Security (CCAFS). These programs are supported by
contributors to the CGIAR Trust Fund.
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■ NOTE ADDED AFTER ASAP PUBLICATION
This paper was published on the Web November 28, 2020
with Table 4 duplicated in the paper. The corrected version
was reposted on December 2, 2020.
Environmental Science & Technology pubs.acs.org/est Article
https://dx.doi.org/10.1021/acs.est.0c01100
Environ. Sci. Technol. 2020, 54, 16062−16070
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