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H I G H L I G H T S G R A P H I C A L A B S T R A C T
A R T I C L E I N F O A B S T R A C T
Guest Editor: Ruben Aldaco Aquaculture is an increasingly important supplier of food worldwide. However, due to its high dependence on agricul-
tural and fishing resources, its growth is constantly constrained by environmental impacts beyond aquaculture produc-
Keywords: tion systems. Within the European Union, Spain accounts for approximately 25 % of total aquaculture production,
Aquaculture which implies that environmental impacts in rivers and marine ecosystems must be monitored to understand the
Aquafeed
role of aquaculture systems. While studies on the environmental performance of mussels or turbot production have
Climate change
Environmental impacts
been reported in the literature, Spanish rainbow trout (Oncorhynchus mykiss) has not received much attention despite
Fish processing its relative importance. In this sense, a Life Cycle Assessment (LCA) study of rainbow trout produced in a medium-sized
Water pollution plant in Galicia (NW Spain) was carried out in the present study. The study considered the production of round weight
trout, as well as some commonly produced processed products, including filleting. The life cycle modelling included a
high level of primary data in the foreground system. In addition to the widely considered environmental impact cate-
gories for this activity (e.g., global warming potential, terrestrial acidification and freshwater eutrophication), the re-
cent proposed antibiotic resistance (ABR) enrichment impact category was included to explore the potential impact of
antibiotic release in freshwater microbiota. The results highlighted the high contribution of aquafeed to most impact
categories, due to upstream agricultural and fishing processes, whereas farm operation was responsible for the larger
part of the impact in freshwater eutrophication, mainly due to direct emissions of nutrients from fish feeding. Amox-
icillin release to recipient water bodies was the main driver to the ABR enrichment category. In contrast, the processing
⁎ Corresponding author.
E-mail address: ian.vazquez@pucp.pe (I. Vázquez-Rowe).
http://dx.doi.org/10.1016/j.scitotenv.2022.159049
Received 18 April 2022; Received in revised form 11 August 2022; Accepted 22 September 2022
Available online 24 September 2022
0048-9697/© 2022 Elsevier B.V. All rights reserved.
J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
phase (i.e., gutting, freezing and packaging) showed low environmental burdens. In order to improve the environmen-
tal performance of the rainbow trout production system, decreasing the feed conversion ratio (FCR), shifting to renew-
able energy, using low environmental burden ingredients in aquafeed, and alternatives to control diseases without
antibiotics could be considered.
1. Introduction systems (Philis et al., 2019). In fact, LCA has proven to be useful to detect
improvement opportunities to increase the sustainability of aquaculture
Aquaculture has become an important source of food for the world's systems (Bohnes et al., 2019; Cao et al., 2013; Philis et al., 2019). Several
growing human population (Garlock et al., 2020), and has shown to be LCA studies in rainbow trout production systems have highlighted that
the fastest growing food sector in recent decades (Ahmed et al., 2019; feed production is the process with the highest burdens in multiple environ-
Tacon, 2020). In 2018 it contributed 48 % of global fish production and mental impacts categories, whereas the farming process is responsible of
is expected to contribute 53 % by 2030, thus surpassing capture fisheries higher burden in eutrophication than others process (Avadí and Fréon,
for the first time (FAO, 2020). 2015; Maiolo et al., 2021).
In 2018, global aquaculture produced approximately 82 million metric However, few studies have been published dealing with the environ-
tons of live weight products in inland aquaculture (62 %) and marine and mental impact linked with the use of antibiotics in aquaculture using LCA
coastal aquaculture (38 %), in different aquatic environments: freshwater, (Henriksson et al., 2012). Antibiotics inputs in most studies are excluded
brackish water and seawater (FAO, 2020). Many aquaculture products are due to lack of reliable data (Dekamin et al., 2015; Grönroos et al., 2006;
produced through inland aquaculture, mainly from freshwater environ- Samuel-Fitwi et al., 2013a). Furthermore, Chen et al. (2015) and
ments (i.e., freshwater aquaculture) (Zhang et al., 2022). The recent FAO d’Orbcastel et al. (2009) highlighted that chemicals (production and
report (2020) has highlighted that inland aquaculture is the main source transport of medicines, cleaning products and other chemicals) contributed
of finfish production in the world, being responsible of 86 % of the global with less than 1 % to several environmental impacts categories
finfish production. (e.g., acidification, eutrophication, global warming) in rainbow trout
Despite the high growth ratio of global aquaculture, the European farming. Nevertheless, a more recent study by Nyberg et al. (2021) has
Union (EU) does not seem to share this trend, thus becoming the main im- revealed the importance of antibiotics in terms of ecosystem quality
porter of aquaculture products in the global market (EUMOFA, 2019; FAO, damage, namely eco-toxicity. Hence, in their study, characterization factors
2020). In fact, the EU only produces approximately one fifth of its domestic for 14 antibiotics were proposed, based on the potential for antibiotic
fish and shellfish demand. Interestingly, 25 % of this aquaculture harvest is resistance (ABR) enrichment as a midpoint category.
produced in Spain, a member state with the second highest per capita con- In this regard, the present study aimed to assess the environmental
sumption of aquatic products and the third largest finfish producer impacts in the production of rainbow trout in a medium-sized plant in the
(APROMAR, 2020; Gutiérrez et al., 2020). The main aquaculture species region of Galicia (NW Spain) using LCA methodology. The novelty of the
produced in Spain are mussels, seabass and rainbow trout (Cavallo et al., study is based on two perspectives. On the one hand, numerous studies
2021). Rainbow trout (Oncorhynchus mykiss) is the main and most have delved into the environmental impacts of Galician fisheries, one of
commonly produced species from freshwater aquaculture in Spain with a the main fishing regions in Spain (Avdelas et al., 2021; STECF, 2021),
production of 18,995 metric tons in 2019 (APROMAR, 2020; Muñoz- such as great scallop (Cortés et al., 2021), tuna (Hospido and Tyedmers,
Lechuga et al., 2018). The main rainbow trout producing regions are Castile 2005), European pilchard (Vázquez-Rowe et al., 2014; Villanueva-Rey
and León and Galicia, contributing with 30 % and 14 % of the national et al., 2018), European hake (Vázquez-Rowe et al., 2011), or horse mack-
production, respectively, followed by Andalusia (12 %), Catalonia (11 %), erel (Vázquez-Rowe et al., 2010). Moreover, others studies focused on
La Rioja (10 %), Aragon (7 %) and Asturias (6 %) (APROMAR, 2020). marine aquaculture systems in Galicia, such as mussels (Iribarren et al.,
The difference in production levels between Castile and León and Galicia 2010a, 2010b, 2010c), and turbot (Iribarren et al., 2012), but no studies
could be linked to: a) the potential freshwater production areas, which is have analyzed freshwater aquaculture systems. On the other hand, the
three fold higher in Castile and Leon than in Galicia (Muñoz-Lechuga study provides an analysis which aims at including the most recent method-
et al., 2018); and, b) the higher fish consumption in Castile and Leon ological advances in aquaculture LCA, by computing, for instance, the
(24.8 kg/person/year) as compared to Galicia (21.1 kg/person/year) environmental impacts linked to the use of antibiotics (including impacts
(FOESA, 2014). linked to microbial resistance). The target audience of the study includes
Freshwater aquaculture generates thousands of direct and indirect stakeholders in the aquaculture sector in Spain and other trout-producing
employees, and it is recognized as an alternative food source with the po- areas in Europe, as well as academics and policy-makers.
tential to reduce pressure on wild stocks (Diana, 2009; Gutiérrez et al.,
2020). However, depending on the type of system, freshwater aquaculture 2. Materials and methods
is also linked to a wide spectrum of environmental issues, such as habitat
alteration, the escape of exotic species and competition with native species, 2.1. Goal and scope definition
water pollution through nitrogen and phosphorus release in superficial
water bodies, that may subsequently trigger eutrophication (Diana, The goal of this LCA study was to determine the environmental perfor-
2009), biotic depletion, fish diseases and parasites and greenhouse gas mance of an intensive rainbow trout production system in a plant that
(GHG) emissions from aquafeed production, among others (Ahmed et al., produces ca. 1700 metric tons of this product per year in Galicia (NW
2019). Furthermore, veterinary drugs and antibiotics from aquaculture Spain),1 identifying its main environmental hotspots and, more specifically,
systems can also be discharged to the environment, causing toxic effects understanding the contribution of antibiotics to the different impact catego-
in aquatic biodiversity, antibiotic accumulation and antibiotic resistance ries, namely those linked to toxicity. The function of the production system
(Lulijwa et al., 2020). is the delivery of a certain amount of packaged animal protein for direct
Life Cycle Assessment (LCA) is an environmental management method- human consumption. Therefore, the main functional unit (FU1) was 1
ology that allows calculating different environmental impact categories metric ton (t) of fresh rainbow trout produced at the farm gate; however,
considering the whole life cycle of a given product or service (ISO,
2006a). LCA has been used in many studies regarding freshwater aquacul- 1
The aquaculture plant, as well as some upstream providers of goods, preferred to remain
ture systems, especially salmonids, such as rainbow trout production anonymous in the present study.
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
due to the fact that the company produces a set of packaged trout-based The fish were raised in a flow through system (FS), a technology used
items for sale, other formats of the product were considered. Therefore, for salmonids farming composed by tanks or raceways, in which the
additional FUs other than FU1 were also computed to represent specific water flows and after use is discharged in a receiving water body (Ahmad
trout-related packaged processed products. These include the following et al., 2021). The mortality ratios reported by the company were as follows:
products: a) 5 kg of packaged fresh gutted fish in polystyrene (PS) box 10 % in the fry stage (except during summer when the mortality increases
(FU2); b) 5 kg of packaged frozen gutted fish in cardboard box (FU3); to ca. 25 %), and 5 % in the fattening stage. The mean water flow in the
c) 1 kg of packaged frozen fish in polyethylene (PE) bag (FU4); and, production system was 1.17 m3 s−1 collected from a nearby river. The
d) 340 g of packaged frozen gutted fish in cardboard box (FU5). wastewater is discharged downstream, after a primary treatment process.
The aquafeed production input data were obtained from the fish pro-
2.2. System boundaries ducer. Due to the lack of some feed ingredients in life cycle inventory
(LCI) databases, aminopro®, antifungals, antioxidants, appealing, betaine
The system boundary established includes activities from the hatching anhydrous, liquid choline, organic mineral were excluded from the model-
stage to the farm gate (see Fig. 1). The data used to model the rainbow ling, representing ca. 4 % by weight of total aquafeed composition. There-
trout production system were obtained from the production information fore, agriculture-based products and fishmeal and fish oil accounted for
of year 2017. The processes included aquafeed production, transport of most of the content of the aquafeed (see Table 1). Given the absence of
chemicals and aquafeed, hatchery, fattening, and slaughtering. Further- camelina and krill oil in the LCI databases available, these inputs were
more, these stages included the linked upstream processes, such as raw modeled considering the LCA studies of Li and Mupondwa (2014) and
material production of aquafeed (i.e., fishery and agricultural derived raw Parker and Tyedmers (2012), respectively. Water, energy and natural gas
materials), antibiotics, chemotherapeutics, electricity and fuel, as well as use in aquafeed production were modeled using the proportion per metric
the downstream processes linked to emissions to soil, water or air, as well ton of fresh rainbow trout provided by Maiolo et al. (2021). Furthermore,
as waste management. The production processes related to infrastructure due to the absence of specific data on the origin of each aquafeed ingredi-
(i.e., capital goods) were excluded. ent, the transport from the production place to the aquafeed producer
was only considered.
2.3. Life cycle inventory For the fry production, 70 % of eggs were obtained from a regional pro-
ducer located 210 km away, and the rest were obtained directly from repro-
2.3.1. Rainbow trout production system duction at the plant. The viability of the rainbow trout eggs was 95 %. After
The production system under analysis was an intensive monoculture of the hatching of eggs, the fry is raised until month 8 or until it reaches 50 g
rainbow trout (Oncorhynchus mykiss) with a feed conversion ratio (FCR) of before entering the fattening phase. The aquafeed consumed in the whole
1.09 in 2017. This FCR is assumed to be a constant value for rainbow trout fry production is equivalent to 25 % of aquafeed used in the production sys-
production in the plant. tem. Electricity and transport data of this process were embedded in the
Fig. 1. System boundaries of the rainbow trout system under analysis. Important to note that the functional unit FU1 represents the main system under analysis for live weight
trout, whereas FU2-FU5 represent processed packaged products for rainbow trout.
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Table 1 and petrol combustion for light commercial vehicles (European Environ-
Composition of aquafeed used in the rainbow trout production system under analy- ment Agency, 2019).
sis and datasets used for their life cycle modelling. The production input data for materials and energy, such as agricultural
Composition % Dataset and fishery products, chemicals, fuels, transportations and electric energy,
Fishmeal 65/67 % 20.8 Fishmeal, 65–67 % protein {GLO}| market for fishmeal, were retrieved from the Ecoinvent v3.6 database (Moreno Ruiz et al.,
65–67 % protein | Cut-off, Uc 2019). When inputs were not available in the aforementioned database,
Wheat bran 16.2 Wheat bran {RoW}| market for wheat bran | Cut-off, Uc these were obtained from Agri-footprint v5.0 and Agribalyse v3.0.1 data-
Wheat gluten 15.6 Wheat gluten feed, at processing/ES Energyb bases, which are based on Ecoinvent's cut-off system (Philis et al., 2021).
Fishmeal (Low 12.0 Fishmeal, 65–67 % protein {GLO}| market for fishmeal,
Temperature) 65–67 % protein | Cut-off, Uc
The combination of these databases allowed complementing the absence
Squid meal 8.6 Fish hydrolyzate (CPSP) from whole fishes, from Chile, at of certain agricultural and livestock production inputs from the Ecoinvent
feed plant/FR Se database, widely recognized by previous studies (Maiolo et al., 2021;
Camelina oil 6.2 Camelina oila Philis et al., 2021).
Sunflower oil 5.9 Crude sunflower oil (pressing), at processing/ES Energyb
Pea starch 4.7 Pea starch-concentrate, at processing/NL Energyb
Fish oil 4.2 Fish oil, from anchovy {GLO}| market for fish oil | Cut-off, Uc
Krill oil 4.2 Krill oild 2.3.2. Emission of nutrients
Lysine 1.0 L-Lysine HCl, animal feed, at retailer gate/FR Ue Nutrients (nitrogen and phosphorous) emissions to freshwater were
Threonine 50 % 0.4 L-Threonine, animal feed, at retailer gate/FR Ue calculated using the mass balance model of rainbow trout farming proposed
Vitamins 0.1 Vitamin, animal feed, at retailer gate/FR Ue by Papatryphon et al. (2005). Aquafeed consumption, protein nitrogen con-
Vitamin C 15 % 0.1 Ascorbic acid {GLO}| market for ascorbic acid | Cut-off, Uc
tent of aquafeed and the apparent digestibility coefficient of protein were as-
a
Li and Mupondwa (2014). sumed to be 95 %, 90 % and 16 %, respectively (Papatryphon et al., 2004).
b
Agri-footprint 5 - gross energy allocation. The protein and phosphorus values in aquafeed were 40 % and 1 %, respec-
c
Ecoinvent 3 - allocation, cut-off by classification – unit. tively. These data were obtained from the nutritional information provided
d
Parker and Tyedmers (2012).
e by the aquafeed producer. Furthermore, the apparent digestibility coefficient
AGRIBALYSE v3.0.1.
of phosphorus was assumed to be 65 %. Finally, the nitrogen and phosphorus
content in round rainbow trout were assumed to be 0.3 % and 0.4 %, respec-
tively, as recommended by Papatryphon et al. (2005).
inventory of the whole production system (see Table 2). However, it is rel-
evant to clarify that during transport, 0.05 g was assumed as the average
Table 2
rainbow trout egg weight (Bonnet et al., 2007).
Life Cycle Inventory of the rainbow trout production system per metric ton of fresh
Given the lack of disaggregated data linked to electricity use, a differen- round fish at farm gate. Data reported based on FU1 (i.e., 1 metric ton of fresh rain-
tiation between farming operations and processing phases could not be bow trout produced in 2017).
attained. Hence, the electricity use value of the whole facility was distrib-
Inputs Unit Amount
uted based on the inventory of rainbow trout production reported by
Maiolo et al. (2021): 76 % and 24 % for farming operation and processing, Fry Unit 3317
respectively. Despite the embedded uncertainty of these values, the deci- Feed t 1.09
Florfenicol g 0.50
sion of using the distribution of energy between farming operations and Oxytetracycline g 2.04
processing phases in the current study was based on the values reported Sulfadiazine sodium g 3.88
by Maiolo et al. (2021) taking into account: a) both production systems Trimethoprim glutamate g 0.97
are developed in the European Region with FS; b) the plant from the Amoxicillin g 6.22
Doxycycline g 1.99
study analyzed in Maiolo et al. (2021) shows similar FCR to those in the
Electric energy MJ 3212
present study; and, c) the processing phase includes the packaging process. Water m3 32,254
The modelling of antibiotic production is one of the major gaps in LCA Fertilized commercial eggs kg 0.12
studies of aquaculture production systems (Bohnes and Laurent, 2019). Fertilized eggs from in situ spawning kg 0.05
However, Nyberg et al. (2021) carried out a review on antibiotics use in Formaldehyde kg 42.22
Oxygen t 0.50
LCA studies, finding that only two studies covered the environmental im- Road transport t km 117.1
pacts linked with antibiotic production (Stone et al., 2010, 2011). Given Diesel oil A L 13.94
the lack of data on antibiotic production, it was assumed that the antibiotics Diesel oil B L 5.09
used at the plant (i.e., oxytetracycline, sulfadiazine sodium, trimethoprim, Gasoline L 0.61
Plastic kg 0.00
amoxicillin and doxycycline) were produced in the same way as chlortetra-
cycline and tylosin, following the methodological scheme suggested by Outputs Unit Amount
Stone et al. (2011). This assumption considers that the tetracycline group
Fresh round trout t 1.00
is the second most used antibiotic in the present study, representing 26 % Waterb m3 32254
of the amount (mass based) of antibiotics used. Phosphorous kg 6.51
Antibiotic emission to water was modeled assuming that 80 % of Nitrogen kg 63.43
antibiotics ingested together with the non-digested aquafeed (around Dead biomass t 0.08
Carbon monoxidea g 188.5
30 % of the provided aquafeed) are accumulated in sediments and released
Non-methane volatile organic compoundsa g 31.34
to the aquatic environment, causing selective pressure on the bacterial Nitrogen oxidesa g 244.4
diversity of this environmental component (Cabello et al., 2013, 2016; Nitrous oxidea g 0.98
Rico et al., 2017). Ammoniaa g 0.91
Florfenicol g 0.43
In terms of transport, it was assumed that antibiotics and formaldehyde
Oxytetracycline g 1.76
were transported for 200 km by freight truck (EURO 4), while rainbow Sulfadiazine sodium g 3.34
trout eggs and aquafeed were obtained from specific sites located 210 km Trimethoprim glutamate g 0.83
and 100 km away, respectively. Regarding the transport to the production Amoxicillin g 5.35
plant, it was considered that internal transport was responsible for the en- Doxycycline g 1.71
tire diesel and petrol consumption. Therefore, the emissions from this a
European Environment Agency (2019).
b
sub-process were calculated based on the emission factors (Tier 1) for diesel Water evaporation was considered negligible.
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Table 3
Life Cycle Inventory of additional FUs linked with processing phase.
Inputs Unit FU2 FU3 FU4 FU5
5 kg packaged fresh gutted fish 5 kg packaged frozen gutted fish 1 kg packaged frozen fish 340 g packaged frozen gutted fish
(PS box) (cardboard box) (PE bag) (cardboard box)
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Fig. 2. Relative contribution analysis of the rainbow trout production system in Galicia (NW Spain) in terms of selected Life Cycle Assessment impact categories. GW-1 =
global warming (IPCC method); TA = terrestrial acidification; FE = freshwater eutrophication; CED = cumulative energy demand; WC = water scarcity; Tox = freshwater
ecotoxicity.
particularly in climate change, TA and CED (Avadí et al., 2015; Chen et al., Although Table 1 shows a similar proportion based on weight for
2015; Dekamin et al., 2015; Maiolo et al., 2021; Samuel-Fitwi et al., 2013a). fishmeal and fish oil (FMFO) and agricultural-based products (∼49 %
This trend is common when aquaculture production is not based on a each), these two blocks showed different contribution levels. Thus, FMFO
recirculating system (RS), where the main hotspot tends to be electricity (including krill oil and squid meal) was the main contributor in terms of
consumption (Dekamin et al., 2015; Samuel-Fitwi et al., 2013a). When a aquafeed environmental impacts, representing 58 %, 72 % and 52 % for
zoom in is performed to analyze the results linked to aquafeed production, GW-1, TA, and CED, respectively (Fig. 3). In contrast, agriculture-based
the environmental impact results for GW-1, TA, FE, CED, WC and Tox were products were the main drivers of FE and WC, contributing with 66 %
1272 kg CO2eq, 14.2 kg SO2eq, 0.2 kg Peq, 22,222 MJ, 6298 m3, and 6.32E and 96 % of these categories, respectively. A more disaggregated level of
+06 PAF m3 day per metric ton of aquafeed, respectively. As abovemen- analysis revealed that three feed ingredients dominated all environmental
tioned, aquafeed production represents the highest environmental impact categories of aquafeed: krill oil, wheat and sunflower oil. Thus,
impacts for most categories, with values ranging from 48 % in the case of krill oil was the main contributor in GW-1, TA and CED, whereas wheat
Tox to 97 % for WC. For FE, however, the contribution of aquafeed was and sunflower oil were the main carriers for in FE and WC. Interestingly, de-
below 4 %. spite krill oil only representing 4 % of the whole aquafeed composition it
Fig. 3. Relative contribution analysis of the production of aquafeed used in rainbow trout production in Galicia (NW Spain) in terms of selected Life Cycle Assessment impact
categories. GW-1 = global warming (IPCC method); TA = terrestrial acidification; FE = freshwater eutrophication; CED = cumulative energy demand; WC = water scar-
city; Tox = freshwater ecotoxicity.
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
represents 28 %, 55 % and 24 % of GW-1, TA and CED impacts, respec- different FUs (in terms of amount of protein intake unit) may not be
tively. This high environmental burden is linked to its high levels of fuel significant.
use intensity – FUI (Parker and Tyedmers, 2012), which is the main source Previous studies have highlighted that packaging of seafood
of GHGs and acidifying substances. However, wheat (i.e., wheat bran and (e.g., anchovy, sardine, and tuna) using plastic shows better environmental
wheat gluten) represented 32 % of the whole aquafeed mass weight and performance than those that use aluminum, tinplate or glass (Almeida et al.,
contributed almost in the same proportion (35 %) in FE, mainly due to 2014, 2021; Hospido et al., 2006; Laso et al., 2017). However, the main
the phosphorous-based fertilizer use. Sunflower oil contributed with 81 % concern regarding plastic bag use is related to the release of microplastics
of the WC impact in aquafeed production, which is linked with the water in the environmental compartments due to the plastic bag waste generation
requirements in agricultural processes in water–stressed areas of the during the post-consumption phase (Tziourrou et al., 2021; Yurtsever and
world (Hussain et al., 2018). Yurtsever, 2018). Despite ongoing efforts to develop life-cycle metrics for
these impacts (Woods et al., 2021), these were not evaluated in this study.
3.2. Environmental impact results of processed rainbow trout products
3.3. Comparison with the scientific literature
The environmental impacts results linked to the processing activities to
gut and freeze trout demonstrated that these processes present low contri- As previously mentioned, a CML method-based comparison with the
bution in all impact categories. Thus, the GW-1 values of gutted and frozen scientific literature was performed, as shown in Table 6, which reveals
rainbow trout were slightly higher than GW-1 of fresh rainbow trout: 2 % that the results of the current study are in line with prior results available
and 4 %, respectively. Regarding the rest of impact categories, the environ- for rainbow trout. Thus, regarding climate change (in this case, using
mental impacts linked to gutted and frozen rainbow trout ranged from 0.2 GW-2), A and E of Galician rainbow trout, results were within the ranges re-
% to 3 % and from 0.4 % to 5 % higher than fresh rainbow trout, respec- ported by previous studies: 0.7–13.6 kg CO2eq, 3.7–52.9 g SO2eq, and
tively. 1.1–135.7 g PO4eq, respectively. Regardless of the uncertainties linked to
Table 5 shows the environmental impacts related to the final product- the use of differing inventory databases and different versions of the CML
based FUs, which include gutting and/or freezing operations, and packag- assessment method, an additional underlying reason for environmental dif-
ing. The production of frozen or gutted fish dominated all impacts catego- ferences across studies are the diverse production systems used and their
ries, whereas the materials and energy used in packaging together different FCR to produce the same FU, as also highlighted by the recent sci-
accounted for less than 10 % in all impact categories. In order to compare entific review of Philis et al. (2019). For example, our results (FS) linked
the different product presentations, the values of environmental impacts with GW-2 are similar to those obtained by Dekamin et al. (2015) and
were recalculated based on the value of protein intake recommended by slightly lower than those reported by Chen et al. (2015), and Maiolo et al.
WHO for an adult person (WHO, 2007). This analysis revealed that the en- (2021) for the same production technology and similar FCR (1.1–1.2). In
vironmental burdens of the protein consumption by a world average- contrast, when compared with other rainbow trout production systems,
weight adult for product FU5 was slightly worse than for the other FUs such as RS, our results are 7.7 and 3.4 fold lower than those reported by
(Table 5), ranging from 3 % to 7 %, mainly in GW-1, CED, and Tox. Instead, Samuel-Fitwi et al. (2013a) and Dekamin et al. (2015), respectively.
FU4 showed the lowest values, mainly in GW-1 (0.51 kg CO2eq) and TA Regarding other environmental impacts (i.e., A and E), our results to-
(4.8 g SO2eq). This trend was expected due to slightly higher amount of gether with those of other rainbow trout LCA studies that use FS systems
packaging materials used per kg of fish in FU5 than the other FUs. In (Chen et al., 2015; Dekamin et al., 2015; Maiolo et al., 2021) were higher
other words, as seen in Table 3, we can estimate the amount of packaging than those obtained in RS systems (Dekamin et al., 2015; Samuel-Fitwi
per kg of fish dividing the sum of plastic or cardboard materials by the et al., 2013a). This behavior was expected because an RS layout avoids
amount of fish in each FU. Hence, FU5 shows a consumption of package emissions of nutrient and acidifying substances to the environment, while
material per kg of fish (67.7 g of cardboard and 16.7 g of plastic per kg of consuming more energy than FS systems (Dekamin et al., 2015; Samuel-
fish) higher than for the other FUs. However, due to the uncertainty linked Fitwi et al., 2013a).
to the study, the differences between the environmental impacts from the When comparing the environmental performance of Galician rainbow
trout production with the production of other fish species (see Table 6),
the GW-2 of Galician rainbow trout was lower in comparison to Eurasian
Table 5 perch (Cooney et al., 2021), black pacu (Avadí et al., 2015; Medeiros
Comparison of environmental impacts linked with the processing phase per func-
et al., 2017), and tilapia (Avadí et al., 2015; Henriksson et al., 2017;
tional unit (FU) and amount of protein intake recommended by WHO.
Yacout et al., 2016). However, African catfish (Besson et al., 2016) pre-
Impact categories FU1 FU2 FU3 FU4 FU5 sented better results. In terms of other impact categories, E and A of Gali-
Per functional unit cian rainbow trout were slightly higher than African catfish (Besson et al.,
GW-1 (kg CO2eq) 1.78 9.66 9.57 1.91 0.67 2016), tilapia (Yacout et al., 2016) and Brazilian black pacu (Medeiros
TA (g SO2eq) 17.44 90.38 90.37 17.91 6.20
et al., 2017).
FE (g Peq) 6.87 34.49 34.59 6.91 2.36
CED (MJ) 35.42 197.9 196.5 39.27 13.84 In order to facilitate the discussion between the results of our study and
WC (m3) 7.08 36.72 36.59 7.33 2.50 those in the literature as regards environmental impacts of aquafeed ingre-
Tox (PAF m3 day) 14,330 76,081 79,206 15,728 5592 dients for rainbow trout, these different ingredients were grouped into four
Per amount of protein intake recommended by WHO categories (Fig. 4): FMFO, agricultural-based, animal-based and supple-
GW-1 (kg CO2eq) 0.48 0.52 0.51 0.51 0.53 ments. Based on this comparison, it can be noted that feed compositions
TA (g SO2eq) 4.67 4.84 4.84 4.80 4.89 across the previous studies are very heterogeneous; yet the amount of
FE (g Peq) 1.84 1.85 1.85 1.85 1.86 FMFO in the feed ranges from 35 % to 79 %, agricultural-based from
CED (MJ) 9.49 10.61 10.53 10.53 10.91
WC (m3) 1.90 1.97 1.96 1.96 1.97
21 % to 67 %, animal based between 0 % and 21 %, and supplements are
Tox (PAF m3 day) 3841 4078 4246 4216 4408 in all cases below 5 % (mass weight).
Most studies highlighted that FMFO is a hotspot both in aquafeed and
GW-1 = global warming (IPCC method); TA = terrestrial acidification; FE = fresh-
consequently in rainbow trout production (Dekamin et al., 2015; Elhami
water eutrophication; CED = cumulative energy demand; WC = water scarcity;
Tox = freshwater ecotoxicity. WHO = World Health Organization. FU1 = 1 kg et al., 2019; Silvenius et al., 2017). For example, according to study of
of fresh rainbow trout; FU2 = 5 kg of packaged fresh gutted fish in polystyrene Elhami et al. (2019), where FMFO constituted 52 % and 25 % of the mass
box; FU3 = 5 kg of packaged frozen gutted fish in cardboard box; FU4 = 1 kg of weight of feed in two different plants from Iran, this feed ingredient
packaged frozen fish in polyethylene bag; FU5 = 340 g of packaged frozen gutted group shared 72 % and 78 % in the GW-2 per metric ton of rainbow trout
fish in cardboard box. produced, respectively. Regarding A, the results of the same study reported
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J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Table 6
Comparative data on global warming (GW-2), acidification (A), and eutrophication (E) of 1 kg of fresh rainbow trout based. All results have been recalculated based on the
CML 2 baseline 2000 v.4.7.
Authors Fish species Production system GW-2 (kg CO2eq) A (g SO2eq) E (g PO4eq)
FS: Flow through system, NS: Not specified, SRS: Semi-closed recirculating system, C: Floating cages, RS: Recirculating system, P: Ponds.
that FMFO contributed 72 % and 81 %, for both production plants, respec- on the proportion of a given ingredient in the feed, but also on environmen-
tively. In contrast, the recent study by Maiolo et al. (2021) reported that ag- tal burden of the remaining ingredients. This situation could be better
ricultural and animal-based ingredients group was the main contributors in reflected when comparing our results with those obtained by Maiolo et al.
GW-2, A and E of the production of one metric ton of aquafeed produced, (2021), which reported higher levels of GW-1, TA and FE per kg of
while FMFO (which composed the third part of aquafeed biomass) only aquafeed, despite a similar FCR and lower proportion of FMFO. A reason
contributed up to 21 % in all impact categories. This suggests that the for this performance could be linked with the environmental burdens of ag-
level of contribution for the different impact categories not only depends ricultural and animal ingredients, which were not fully reported.
Fig. 4. Comparative data of ingredients groups used to produce aquafeed for rainbow trout production. LTF = aquafeed used in Lordegal trout farm, ATF = aquafeed used in
Ardal trout farm, RT09 = aquafeed with complete FMFO in 2009, RT16 = aquafeed with 50 % substitution of FMFO by alternative protein sources, FS = aquafeed used in
flow-through system, SRS = aquafeed used in semi-recirculating system, RS = aquafeed used in recirculating system, G1-G3 = aquafeed used in pan-size, mix-size, and large
size trout production system, TrComF1 = Artisanal feed, TrComF2 = Commercial feed, TrComF3 = Comercial feed based in Chilean production.
9
J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Fig. 5. Environmental impacts linked with different scenarios: (a) variations in FCR, (b) variations in energy consumption and (c) shifting from grid electricity to wind power.
FCR + 10: increasing 10 % of FCR, FCR-10: decreasing 10 % of FCR, B-20: decreasing 20 % of energy consumption, B + 20: increasing 20 % of energy consumption. GW-1 =
global warming (IPCC method); TA = terrestrial acidification; FE = freshwater eutrophication; CED = cumulative energy demand; WC = water scarcity; Tox = freshwater
ecotoxicity.
3.4. Sensitivity analysis FS, given that unlike RS, direct use of electricity at the plant is not a deter-
mining factor for its environmental profile. However, the substitution of
The sensitivity analysis showed that FCR is a key parameter to improve grid electricity to wind power reduced 15 %, 11 %, 10 %, and 9 % of
the environmental performance of fresh rainbow trout production. A varia- GW-1, CED, Tox, and TA, respectively, and to a lesser extent in FE (2 %),
tion of 10 % in FCR triggered proportional variations in the assessed impact and WC (3 %), suggesting that deep-decarbonization of the energy matrix
categories, mainly in FE and WC (see Fig. 5a). As expected, variations in the can attain relevant environmental gains in the aquaculture sector
amount of aquafeed supplied per kg of rainbow trout generate equivalent (Fig. 5c). Similar trends were reported for rainbow trout produced in RS
changes in the associated environmental impacts, since aquafeed's contri- (Dekamin et al., 2015; Samuel-Fitwi et al., 2013a).
bution is significant to total impacts. This behavior is in line with the results When fish oil is used as a substitute of krill oil (see Fig. 6a), and environ-
reported by the scientific literature (Avadí et al., 2015; Dekamin et al., mental impact reduction is attained mainly in TA, Tox, GW-1, and CED:
2015; Papatryphon et al., 2004). 52 %, 41 %, 25 %, and 20 %, respectively. This effect also extends to the
Variations in electricity consumption (20 %) produced slight variations environmental burdens of fresh rainbow trout production (Fig. 6b), consid-
in all impact categories (Fig. 5b). Thus, a more efficient energy consump- ering the importance of aquafeed contribution to the total system under
tion profile decreased all impacts category results in a range from 0.3 % analysis.
to 5 %. Therefore, this parameter would not be decisive for improving envi- To sum up, environmental impact reductions linked to the rainbow
ronmental performance in this production system, despite the fact that elec- trout production system should focus on the following key aspects. In the
tricity is the second contributor for most environmental impacts, ranging first place, improvement of FCR must be considered as a variable with di-
from 2 % to 24 %. This effect could be linked with the characteristics of rect influence on the environmental performance of fresh rainbow trout.
Fig. 6. Effect of the substitution from krill oil to fish oil on the environmental performance of (a) aquafeed and (b) fresh rainbow trout. Aquafeed-KO: Aquafeed with total
substitution of krill oil by fish oil, B-KO: Fresh rainbow trout produced with Aquafeed-KO. GW-1 = global warming (IPCC method); TA = terrestrial acidification; FE =
freshwater eutrophication; CED = cumulative energy demand; WC = water scarcity; Tox = freshwater ecotoxicity.
10
J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
This improvement could be achieved increasing aquafeed quality and Supervision. Sara González-García: Conceptualization, Methodology,
adopting best feeding management practices (Avadí et al., 2015; Maiolo Writing – review & editing, Visualization, Supervision. Ian Vázquez-
et al., 2021). In this regard, an enhanced feed formulation could improve Rowe: Conceptualization, Methodology, Formal analysis, Resources, Writ-
the nutrient intake and reduce the waste and nutrient release, through ing – review & editing, Visualization, Supervision, Project administration,
decreased use of poorly digestible feed ingredients and maximizing more Funding acquisition.
digestible ingredients (Cho and Bureau, 2001). Moreover, novel feed
additives, such as pre- and probiotics, have been reported as promising to Data availability
improve the FCR and to reduce the use of antibiotics and the nitrogen
and phosphorous discharges (Boyd et al., 2020). Nevertheless, these alter- Data will be made available on request.
natives could be carried out with further LCA studies, in order to assess
the possible environmental trade-offs. Secondly, the development of a full
Declaration of competing interest
direct electricity use decarbonization scheme for the plant, considering
the high potential of Galicia to produce onshore (Simón et al., 2019) and
The authors declare no conflict of interest.
offshore wind-based energy (Castro-Santos and Filgueira-Vizoso, 2021).
The application of this activity could be carried out in the short and me-
Acknowledgements
dium term, taking into a count the growing expansion of the wind energy
sector in Galicia (Carvalho et al., 2021; Simón et al., 2019). Finally, the
This work was supported by the EAPA_576/2018 NEPTUNUS project.
use of feed ingredients with low environmental burden in substitution of in-
The authors would like to acknowledge the financial support of the Interreg
gredients with high environmental burdens (i.e. krill oil) should be assessed
Atlantic Area.
in depth, as these can generate a “cascade effect” throughout the produc-
tion chain (Maiolo et al., 2021). However, this action must be accompanied
Appendix A. Supplementary data
by further research beyond the scope of LCA so as not to affect nutritional
and productive performance (McLaren et al., 2021) as well as on the evalu-
The Supplementary Material provides a set of tables with quantitative
ation of environmental impacts linked to biodiversity and ecosystems
data on the processes that are described in the paper. Supplementary data
(Henriksson et al., 2012) that are currently not available through life-
to this article can be found online at doi:https://doi.org/10.1016/j.
cycle methodologies.
scitotenv.2022.159049.
4. Conclusions
References
The current study is a first attempt to model the Galician rainbow trout
aquaculture and apply the novel proposal of ABR enrichment CF (Nyberg Ahmad, A., Sheikh Abdullah, S.R., Hasan, H.A., Othman, A.R., Ismail, ‘Izzati, N., 2021. Aqua-
et al., 2021) to this sector. From a global point of view, the production of culture industry: Supply and demand, best practices, effluent and its current issues and
treatment technology. J. Environ. Manage. 287, 112271. https://doi.org/10.1016/j.
Galician rainbow trout shows an environmental behavior in line with previ- jenvman.2021.112271.
ous reports in local environmental impacts. However, in terms of GHG Ahmad, A.L., Chin, J.Y., Mohd Harun, M.H.Z., Low, S.C., 2022. Environmental impacts and
emissions, lower levels were detected as compared to the scientific imperative technologies towards sustainable treatment of aquaculture wastewater: a re-
view. J. Water Process Eng. 46, 102553. https://doi.org/10.1016/j.jwpe.2021.102553.
literature. Moreover, the results revealed that the main driver of most envi- Ahmed, N., Thompson, S., 2019. The blue dimensions of aquaculture: a global synthesis. Sci.
ronmental impacts of fresh rainbow trout was the production of aquafeed, Total Environ. 652, 851–861. https://doi.org/10.1016/j.scitotenv.2018.10.163.
mainly due to the production of krill and sunflower oil, as well as wheat. Ahmed, N., Ward, J.D., Saint, C.P., 2014. Can integrated aquaculture-agriculture (IAA) pro-
duce “more crop per drop”? Food Secur. 6, 767–779. https://doi.org/10.1007/s12571-
In order to reduce the environmental burden of the production system, 014-0394-9.
some improvement alternatives have been identified, such as decreasing Ahmed, N., Thompson, S., Glaser, M., 2019. Global aquaculture productivity, environmental
the FCR through enhanced aquafeed quality and best practices in feeding sustainability, and climate change adaptability. Environ. Manag. 63, 159–172. https://
doi.org/10.1007/s00267-018-1117-3.
management, the shift from grid energy to wind energy, and using low en-
Almeida, C., Vaz, S., Cabral, H., Ziegler, F., 2014. Environmental assessment of sardine
vironmental burden-ingredients in the aquafeed formulation. (Sardina pilchardus) purse seine fishery in Portugal with LCA methodology including bi-
Regarding chemotherapeutics, antibiotic production had relatively low ological impact categories. Int. J. Life Cycle Assess. 19, 297–306. https://doi.org/10.
1007/s11367-013-0646-5.
contribution to all impact categories, whereas the ABR enrichment environ-
Almeida, C., Loubet, P., da Costa, T.P., Quinteiro, P., Laso, J., Baptista de Sousa, D., Cooney,
mental impact of antibiotic discharges to the water compartment may be R., Mellett, S., Sonnemann, G., Rodríguez, C.J., Rowan, N., Clifford, E., Ruiz-Salmón, I.,
underestimated due to the lack of CFs for all antibiotic used in the produc- Margallo, M., Aldaco, R., Nunes, M.L., Dias, A.C., Marques, A., 2021. Packaging environ-
tion system. However, new alternatives to antibiotic use must be investi- mental impact on seafood supply chains: a review of life cycle assessment studies. J. Ind.
Ecol. 1–18. https://doi.org/10.1111/jiec.13189.
gated, in order to reduce the ABR enrichment impact linked with APROMAR, 2020. Aquaculture in Spain 2020, Spanish Aquaculture Business Association.
antibiotics release to freshwater bodies. http://www.apromar.es/content/la-acuicultura-en-españa-2020.
Finally, this study identified, in line with other recent studies, some Avadí, A., Fréon, P., 2013. Life cycle assessment of fisheries: a review for fisheries scientists
and managers. Fish. Res. 143, 21–38. https://doi.org/10.1016/j.fishres.2013.01.006.
needs for the development of LCA in the aquaculture sector: i) the develop- Avadí, A., Fréon, P., 2015. A set of sustainability performance indicators for seafood: direct
ment of ABR enrichment CFs for more antibiotics used in freshwater aqua- human consumption products from peruvian anchoveta fisheries and freshwater aquacul-
culture, to improve the estimation of this impact category; ii) further ture. Ecol. Indic. 48, 518–532. https://doi.org/10.1016/j.ecolind.2014.09.006.
Avadí, A., Pelletier, N., Aubin, J., Ralite, S., Núñez, J., Fréon, P., 2015. Comparative
studies about the environmental impacts of best feeding management prac- environmental performance of artisanal and commercial feed use in peruvian fresh-
tices and new sources of proteins and oils are necessary to explore; and, water aquaculture. Aquaculture 435, 52–66. https://doi.org/10.1016/j.aquacul-
3) some methodological aspects also could be considered in future research, ture.2014.08.001.
Avdelas, L., Avdic-Mravlje, E., Borges Marques, A.C., Cano, S., Capelle, J.J., Carvalho, N.,
for example, the use of a standardized model to calculate the nutrient re-
Cozzolino, M., Dennis, J., Ellis, T., Fernández Polanco, J.M., Guillen, J., Lasner, T., Le
lease or the use of data from water quality, due the different approach Bihan, V., Llorente, I., Mol, A., Nicheva, S., Nielsen, R., van Oostenbrugge, H.,
used across the scientific literature. Villasante, S., Visnic, S., Zhelev, K., Asche, F., 2021. The decline of mussel aquaculture
in the European Union: causes, economic impacts and opportunities. Rev. Aquac. 13,
91–118. https://doi.org/10.1111/raq.12465.
CRediT authorship contribution statement Ayer, N.W., Tyedmers, P.H., Pelletier, N.L., Sonesson, U., Scholz, A., 2007. Co-product alloca-
tion in life cycle assessments of seafood production systems: review of problems and strat-
Joan Sanchez-Matos: Conceptualization, Methodology, Formal analy- egies. Int. J. Life Cycle Assess. 12, 480–487. https://doi.org/10.1065/lca2006.11.284.
Aziza, A.E., Quezada, N., Cherian, G., 2010. Antioxidative effect of dietary camelina meal in
sis, Investigation, Data curation, Writing – original draft. Leticia Regueiro: fresh, stored, or cooked broiler chicken meat. Poult. Sci. 89, 2711–2718. https://doi.
Conceptualization, Resources, Writing – review & editing, Visualization, org/10.3382/ps.2009-00548.
11
J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Besson, M., Aubin, J., Komen, H., Poelman, M., Quillet, E., Vandeputte, M., Van Arendonk, FAO, 2020. The state of world fisheries and aquaculture 2020, Sustainability in action.
J.A.M., De Boer, I.J.M., 2016. Environmental impacts of genetic improvement of growth http://www.fao.org/publications/card/en/c/CA9229EN.
rate and feed conversion ratio in fish farming under rearing density and nitrogen output FOESA, Ministerio de Agricultura, Alimentación y Medio Ambiente-Gobierno de España,
limitations. J. Clean. Prod. 116, 100–109. https://doi.org/10.1016/j.jclepro.2015.12.084. 2014. Plan Estratégico Plurianual de la Acuicultura Española 2014-2020. https://
Bohnes, F.A., Laurent, A., 2019. LCA of aquaculture systems: methodological issues and po- www.mapa.gob.es/es/pesca/temas/acuicultura/plan-estrategico/default.aspx.
tential improvements. Int. J. Life Cycle Assess. 24, 324–337. https://doi.org/10.1007/ Ford, J.S., Pelletier, N.L., Ziegler, F., Scholz, A.J., Tyedmers, P.H., Sonesson, U., Kruse, S.A.,
s11367-018-1517-x. Silverman, H., 2012. Proposed local ecological impact categories and indicators for life
Bohnes, F.A., Hauschild, M.Z., Schlundt, J., Laurent, A., 2019. Life cycle assessments of aqua- cycle assessment of aquaculture: a Salmon aquaculture case study. J. Ind. Ecol. 16,
culture systems: a critical review of reported findings with recommendations for policy 254–265. https://doi.org/10.1111/j.1530-9290.2011.00410.x.
and system development. Rev. Aquac. 11, 1061–1079. https://doi.org/10.1111/raq. Frischknecht, R., Hischier, R., Weidema, B., Althaus, H.-J., Bauer, C., Doka, G., Dones, R.,
12280. Hellweg, S., Humbert, S., Jungbluth, N., Köllner, T., Loerincik, Y., Margni, M.,
Bonnet, E., Fostier, A., Bobe, I., 2007. Characterization of rainbow trout egg quality: a case Nemecek, T., 2004. Implementation of Life Cycle Impact Assessment Methods Data
study using four different breeding protocols, with emphasis on the incidence of embry- v1.1 (2004). Ecoinvent Rep. No. 3. 116.
onic malformations. Theriogenology 67 (4). https://doi.org/10.1016/j.theriogenology. Garlock, T., Asche, F., Anderson, J., Bjørndal, T., Kumar, G., Lorenzen, K., Ropicki, A., Smith,
2006.10.008. M.D., Tveterås, R., 2020. A global blue revolution: aquaculture growth across regions,
Boulay, A.M., Bare, J., Benini, L., Berger, M., Lathuillière, M.J., Manzardo, A., Margni, M., species, and countries. Rev. Fish. Sci. Aquac. 28, 107–116. https://doi.org/10.1080/
Motoshita, M., Núñez, M., Pastor, A.V., Ridoutt, B., Oki, T., Worbe, S., Pfister, S., 2018. 23308249.2019.1678111.
The WULCA consensus characterization model for water scarcity footprints: assessing im- Grönroos, J., Seppälä, J., Silvenius, F., Mäkinen, T., 2006. Life cycle assessment of Finnish cul-
pacts of water consumption based on available water remaining (AWARE). Int. J. Life tivated rainbow trout. Boreal Environ. Res. 11, 401–414.
Cycle Assess. 23, 368–378. https://doi.org/10.1007/s11367-017-1333-8. Guinée, J.B., Gorrée, M., Heijungs, R., Huppes, G., Kleijn, R., Wegener Sleeswijk, A., Udo De
Boyd, C.E., D’Abramo, L.R., Glencross, B.D., Huyben, D.C., Juarez, L.M., Lockwood, G.S., Haes, H.a., de Bruijn, J.a., van Duin, R., Huijbregts, M.a.J., 2001. Life Cycle Assessment:
McNevin, A.A., Tacon, A.G.J., Teletchea, F., Tomasso, J.R., Tucker, C.S., Valenti, W.C., An Operational Guide to the ISO Standards, III: Scientific Background.
2020. Achieving sustainable aquaculture: historical and current perspectives and future Gutiérrez, E., Lozano, S., Guillén, J., 2020. Efficiency data analysis in EU aquaculture produc-
needs and challenges. J. World Aquac. Soc. 51, 578–633. https://doi.org/10.1111/ tion. Aquaculture 520, 734962. https://doi.org/10.1016/j.aquaculture.2020.734962.
jwas.12714. Heijungs, R., 2020. On the number of Monte Carlo runs in comparative probabilistic LCA. Int.
Cabello, F.C., Godfrey, H.P., Tomova, A., Ivanova, L., Dölz, H., Millanao, A., Buschmann, A.H., J. Life Cycle Assess. 25, 394–402. https://doi.org/10.1007/s11367-019-01698-4.
2013. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resis- Heijungs, R., 2021. Selecting the best product alternative in a sea of uncertainty. Intern. J. Life
tance and to animal and human health. Environ. Microbiol. 15, 1917–1942. https://doi. Cycle Assess. 26 (3). https://doi.org/10.1007/s11367-020-01851-4.
org/10.1111/1462-2920.12134. Helmes, R.J.K., Huijbregts, M.A.J., Henderson, A.D., Jolliet, O., 2012. Spatially explicit fate
Cabello, F.C., Godfrey, H.P., Buschmann, A.H., Dölz, H.J., 2016. Aquaculture as yet another factors of phosphorous emissions to freshwater at the global scale. Int. J. Life Cycle As-
environmental gateway to the development and globalisation of antimicrobial resistance. sess. 17, 646–654. https://doi.org/10.1007/s11367-012-0382-2.
Lancet Infect. Dis. 16, e127–e133. https://doi.org/10.1016/S1473-3099(16)00100-6. Henriksson, P.J.G., Guinée, J.B., Kleijn, R., De Snoo, G.R., 2012. Life cycle assessment of aqua-
Cao, L., Diana, J.S., Keoleian, G.A., 2013. Role of life cycle assessment in sustainable aquacul- culture systems-a review of methodologies. Int. J. Life Cycle Assess. 17, 304–313. https://
ture. Rev. Aquac. 5, 61–71. https://doi.org/10.1111/j.1753-5131.2012.01080.x. doi.org/10.1007/s11367-011-0369-4.
Carrillo, C., Cidrás, J., Díaz-Dorado, E., Obando-Montaño, A.F., 2014. An approach to deter- Henriksson, P.J.G., Dickson, M., Allah, A.N., Al-Kenawy, D., Phillips, M., 2017. Benchmarking
mine the weibull parameters for wind energy analysis: the case of Galicia (Spain). Ener- the environmental performance of best management practice and genetic improvements
gies 7, 2676–2700. https://doi.org/10.3390/en7042676. in egyptian aquaculture using life cycle assessment. Aquaculture 468, 53–59. https://doi.
Carvalho, D., Rocha, A., Costoya, X., deCastro, M., Gómez-Gesteira, M., 2021. Wind energy re- org/10.1016/j.aquaculture.2016.09.051.
source over Europe under CMIP6 future climate projections: what changes from CMIP5 to Hospido, A., Tyedmers, P., 2005. Life cycle environmental impacts of spanish tuna fisheries.
CMIP6. Renew. Sust. Energ. Rev. 151. https://doi.org/10.1016/j.rser.2021.111594. Fish. Res. 76, 174–186. https://doi.org/10.1016/j.fishres.2005.05.016.
Castro-Santos, L., Filgueira-Vizoso, A., 2021. The decarbonisation of Galicia using renewable Hospido, A., Vazquez, M.E., Cuevas, A., Feijoo, G., Moreira, M.T., 2006. Environmental assess-
marine energy. Renew. Energy Power Qual. J. 19, 115–120. https://doi.org/10.24084/ ment of canned tuna manufacture with a life-cycle perspective. Resour. Conserv. Recycl.
repqj19.231. 47, 56–72. https://doi.org/10.1016/j.resconrec.2005.10.003.
Cavallo, M., Pérez Agúndez, J.A., Raux, P., Frangoudes, K., 2021. Is existing legislation Huijbregts, M.A.J., Steinmann, Z.J.N., Elshout, P.M.F., Stam, G., Verones, F., Vieira, M., Zijp,
supporting socially acceptable aquaculture in the European Union? A transversal analysis M., Hollander, A., van Zelm, R., 2017. ReCiPe2016: a harmonised life cycle impact assess-
of France, Italy and Spain. Rev. Aquac., 1683–1694 https://doi.org/10.1111/raq.12540. ment method at midpoint and endpoint level. Int. J. Life Cycle Assess. 22, 138–147.
Chen, X., Samson, E., Tocqueville, A., Aubin, J., 2015. Environmental assessment of trout https://doi.org/10.1007/s11367-016-1246-y.
farming in France by life cycle assessment: using bootstrapped principal component anal- Hussain, M., Farooq, S., Hasan, W., Ul-Allah, S., Tanveer, M., Farooq, M., Nawaz, A., 2018.
ysis to better define system classification. J. Clean. Prod. 87, 87–95. https://doi.org/10. Drought stress in sunflower: physiological effects and its management through breeding
1016/j.jclepro.2014.09.021. and agronomic alternatives. Agric. Water Manag. 201, 152–166. https://doi.org/10.
Cho, C.Y., Bureau, D.P., 2001. A review of diet formulation strategies and feeding systems to 1016/j.agwat.2018.01.028.
reduce excretory and feed wastes in aquaculture. Aquac. Res. 32, 349–360. https://doi. IPCC, 2013. Climate Change 2013. The Physical Science Basis. Working Group I Contribution
org/10.1111/raq.12014. to the 5th Assessment Report of the IPCC. Intergovernamental Panel on Climate Change.
Cooney, R., Tahar, A., Kennedy, A., Clifford, E., 2021. The dilemma of opportunity in devel- Iribarren, D., Moreira, M.T., Feijoo, G., 2010a. Revisiting the life cycle assessment of mussels
oping a life cycle assessment of emerging aquaculture systems - a case study of a eurasian from a sectorial perspective. J. Clean. Prod. 18, 101–111. https://doi.org/10.1016/j.
perch (Perca fluviatilis) hatchery recirculating aquaculture system. Aquaculture 536, jclepro.2009.10.009.
736403. https://doi.org/10.1016/j.aquaculture.2021.736403. Iribarren, D., Moreira, M.T., Feijoo, G., 2010b. Life cycle assessment of fresh and canned mus-
Copena, D., Simón, X., 2018. Wind farms and payments to landowners: opportunities for rural sel processing and consumption in Galicia (NW Spain). Resour. Conserv. Recycl. 55,
development for the case of Galicia. Renew. Sust. Energ. Rev. 95, 38–47. https://doi.org/ 106–117. https://doi.org/10.1016/j.resconrec.2010.08.001.
10.1016/j.rser.2018.06.043. Iribarren, D., Moreira, M.T., Feijoo, G., 2010c. Implementing by-product management into
Cortés, A., González-García, S., Franco-Uría, A., Moreira, M.T., Feijoo, G., 2021. Evaluation of the life cycle assessment of the mussel sector. Resour. Conserv. Recycl. 54, 1219–1230.
the environmental sustainability of the inshore great scallop (Pecten maximus) fishery in https://doi.org/10.1016/j.resconrec.2010.03.017.
Galicia. J. Ind. Ecol. 1–14. https://doi.org/10.1111/jiec.13153. Iribarren, D., Dagá, P., Moreira, M.T., Feijoo, G., 2012. Potential environmental effects of
d’Orbcastel, E.R., Blancheton, J.P., Aubin, J., 2009. Towards environmentally sustainable probiotics used in aquaculture. Aquac. Int. 20, 779–789. https://doi.org/10.1007/
aquaculture: comparison between two trout farming systems using life cycle assessment. s10499-012-9502-z.
Aquac. Eng. 40, 113–119. https://doi.org/10.1016/j.aquaeng.2008.12.002. ISO, 2006. ISO 14040:2006. Environmental Management – Life Cycle Assessment –Principles
de Andrade, M.C., Ugaya, C.M.L., de Almeida Neto, J.A., Rodrigues, L.B., 2021. Regionalized and Framework.
phosphorus fate factors for freshwater eutrophication in Bahia, Brazil: an analysis of spa- ISO, 2006. Environmental Management-Life Cycle Assessment-Requirements and Guidelines.
tial and temporal variability. Int. J. Life Cycle Assess. 26, 879–898. https://doi.org/10. Int. Stand.
1007/s11367-021-01912-2. Laso, J., Margallo, M., Fullana, P., Bala, A., Gazulla, C., Irabien, Á., Aldaco, R., 2017. When
Dekamin, M., Veisi, H., Safari, E., Liaghati, H., Khoshbakht, K., Dekamin, M.G., 2015. Life product diversification influences life cycle impact assessment: a case study of canned an-
cycle assessment for rainbow trout (Oncorhynchus mykiss) production systems: a case chovy. Sci. Total Environ. 581–582, 629–639. https://doi.org/10.1016/j.scitotenv.2016.
study for Iran. J. Clean. Prod. 91, 43–55. https://doi.org/10.1016/j.jclepro.2014.12.006. 12.173.
Diana, J.S., 2009. Aquaculture production and biodiversity conservation. Bioscience 59, Li, H., Ma, T., Shen, Z., Li, A., Yang, J., Xiang, D., Liu, J., Deng, S., Sun, Y., 2020. Optimization
27–38. https://doi.org/10.1525/bio.2009.59.1.7. of [Bmim][HSO4]-catalyzed transesterification of camelina oil. Chem. Eng. Technol. 43,
Dodds, W.K., Smith, V.H., 2016. Nitrogen, phosphorus, and eutrophication in streams. Int. 403–411. https://doi.org/10.1002/ceat.201900477.
Waters 6, 155–164. https://doi.org/10.5268/IW-6.2.909. Li, M., Dong, J., Zhang, Y., Yang, H., Van Zwieten, L., Lu, H., Alshameri, A., Zhan, Z., Chen, X.,
Ehsani, A., Jasour, M.S., Khodayari, M., 2013. Differentiation of common marketable-size rain- Jiang, X., Xu, W., Bao, Y., Wang, H., 2021. A critical review of methods for analyzing
bow trouts (Oncorhynchus mykiss) based on nutritional and dietetic traits: a comparative freshwater eutrophication. Water (Switzerland) 13, 1–20. https://doi.org/10.3390/
study. J. Appl. Anim. Res. 41, 387–391. https://doi.org/10.1080/09712119.2013.783483. w13020225.
Elhami, B., Farahani, S.S., Marzban, A., 2019. Improvement of energy efficiency and environ- Li, X., Mupondwa, E., 2014. Life cycle assessment of camelina oil derived biodiesel and jet fuel
mental impacts of rainbow trout in Iran. Artif. Intell. Agric. 2, 13–27. https://doi.org/10. in the Canadian prairies. Sci. Total Environ. 481, 17–26. https://doi.org/10.1016/j.
1016/j.aiia.2019.06.002. scitotenv.2014.02.003.
EUMOFA, 2019. The EU Fish Market 2019 Edition. https://doi.org/10.2771/168390. Lulijwa, R., Rupia, E.J., Alfaro, A.C., 2020. Antibiotic use in aquaculture, policies and regula-
European Environment Agency, 2019. EEA Report N° 13/2019: EMEP/EEA Air Pollutant tion, health and environmental risks: a review of the top 15 major producers. Rev. Aquac.
Emission Inventory Guidebook 2019. 12, 640–663. https://doi.org/10.1111/raq.12344.
12
J. Sanchez-Matos et al. Science of the Total Environment 856 (2023) 159049
Maiolo, S., Forchino, A.A., Faccenda, F., Pastres, R., 2021. From feed to fork – life cycle assess- Silvenius, F., Grönroos, J., Kankainen, M., Kurppa, S., Mäkinen, T., Vielma, J., 2017. Impact of
ment on an italian rainbow trout (Oncorhynchus mykiss) supply chain. J. Clean. Prod. feed raw material to climate and eutrophication impacts of finnish rainbow trout farming
289, 125155. https://doi.org/10.1016/j.jclepro.2020.125155. and comparisons on climate impact and eutrophication between farmed and wild fish.
McLaren, S., Berardy, A., Henderson, A., Holden, N., Huppertz, T., Jolliet, O., De Camillis, C., J. Clean. Prod. 164, 1467–1473. https://doi.org/10.1016/j.jclepro.2017.07.069.
Renouf, M., Rugani, B., Saarinen, M., van der Pols, J., Vázquez-Rowe, I., Antón Vallejo, Simón, X., Copena, D., Montero, M., 2019. Strong wind development with no community par-
A., Bianchi, M., Chaudhary, A., Chen, C., CooremanAlgoed, M., Dong, H., Grant, T., ticipation. The case of Galicia (1995–2009). Energy Policy 133, 110930. https://doi.org/
Green, A., Hallström, E., Hoang, H., Leip, A., Lynch, J., McAuliffe, G., Ridoutt, B., 10.1016/j.enpol.2019.110930.
Saget, S., Scherer, L., Tuomisto, H., Tyedmers, P., Zanten, V.H., 2021. Integration of En- STECF, 2021. Scientific, Technical and Economic Committee for Fisheries (STECF) – Eco-
vironment and Nutrition in Life Cycle Assessment of Food Items: Opportunities and Chal- nomic Report of the EU Aquaculture sector (STECF-18-19), Publications Office of the
lenges. https://doi.org/10.4060/cb8054en. European Union, Luxembourg, EUR 26336 EN, JRC 86671. https://doi.org/10.2760/
Medeiros, M.V., Aubin, J., Camargo, A.F.M., 2017. Life cycle assessment of fish and prawn 441510.
production: comparison of monoculture and polyculture freshwater systems in Brazil. Stone, J.J., Dollarhide, C.R., Jinka, R., Thaler, R.C., Hostetler, C.E., Clay, D.E., 2010. Life cycle
J. Clean. Prod. 156, 528–537. https://doi.org/10.1016/j.jclepro.2017.04.059. assessment of a modern northern great plains U.S. Swine production facility. Environ.
Moreno Ruiz, E., Valsasina, L., FitzGerald, D., Brunner, F., Symeonidis, A., Bourgault, G., Eng. Sci. 27, 1009–1018. https://doi.org/10.1089/ees.2010.0051.
Wernet, G., 2019. Documentation of Changes Implemented in the Ecoinvent Database Stone, J.J., Aurand, K.R., Dollarhide, C.R., Jinka, R., Thaler, R.C., Clay, D.E., Clay, S.A., 2011.
v3.6 6, pp. 1–42. Determination of environmental impacts of antimicrobial usage for US northern Great
Muñoz-Lechuga, R., Sanz-Fernández, V., Cabrera-Castro, R., 2018. An overview of freshwater Plains swine-production facilities: a life-cycle assessment approach. Int. J. Life Cycle As-
and marine finfish aquaculture in Spain: emphasis on regions. Rev. Fish. Sci. Aquac. 26, sess. 16, 27–39. https://doi.org/10.1007/s11367-010-0241-y.
195–213. https://doi.org/10.1080/23308249.2017.1381832. Sultan, F.A., Routroy, S., Thakur, M., 2021. Evaluating sustainability of the surimi supply
Nyberg, O., Rico, A., Guinée, J.B., Henriksson, P.J.G., 2021. Characterizing antibiotics in LCA chain in India: a life cycle assessment approach. Int. J. Life Cycle Assess. 26,
—a review of current practices and proposed novel approaches for including resistance. 1319–1337. https://doi.org/10.1007/s11367-021-01927-9.
Int. J. Life Cycle Assess. https://doi.org/10.1007/s11367-021-01908-y. Tacon, A.G.J., 2020. Trends in global aquaculture and aquafeed production: 2000–2017. Rev.
Papatryphon, E., Petit, J., Kaushik, S.J., Van Der Werf, H.M.G., 2004. Environmental impact Fish. Sci. Aquac. 28, 43–56. https://doi.org/10.1080/23308249.2019.1649634.
assessment of salmonid feeds using life cycle assessment (LCA). Ambio 33, 316–323. Tziourrou, P., Kordella, S., Ardali, Y., Papatheodorou, G., Karapanagioti, H.K., 2021.
https://doi.org/10.1579/0044-7447-33.6.316. Microplastics formation based on degradation characteristics of beached plastic bags.
Papatryphon, E., Petit, J., Van Der Werf, H.M.G., Sadasivam, K.J., Claver, K., 2005. Nutrient- Mar. Pollut. Bull. 169, 112470. https://doi.org/10.1016/j.marpolbul.2021.112470.
balance modeling as a tool for environmental management in aquaculture: the case of Vázquez-Rowe, I., Moreira, M.T., Feijoo, G., 2010. Life cycle assessment of horse mackerel
trout farming in France. Environ. Manag. 35, 161–174. https://doi.org/10.1007/ fisheries in Galicia (NW Spain): comparative analysis of two major fishing methods.
s00267-004-4020-z. Fish. Res. 106, 517–527. https://doi.org/10.1016/j.fishres.2010.09.027.
Parker, R.W.R., Tyedmers, P.H., 2012. Life cycle environmental impacts of three products de- Vázquez-Rowe, I., Moreira, M.T., Feijoo, G., 2011. Life cycle assessment of fresh hake fillets
rived from wild-caught Antarctic krill (Euphausia superba). Environ. Sci. Technol. 46, captured by the galician fleet in the northern stock. Fish. Res. 110, 128–135. https://
4958–4965. https://doi.org/10.1021/es2040703. doi.org/10.1016/j.fishres.2011.03.022.
Payen, S., Cosme, N., Elliott, A.H., 2021. Freshwater eutrophication: spatially explicit fate fac- Vázquez-Rowe, I., Villanueva-Rey, P., Moreira, M.T., Feijoo, G., 2013. The role of consumer
tors for nitrogen and phosphorus emissions at the global scale. Int. J. Life Cycle Assess. purchase and post-purchase decision-making in sustainable seafood consumption. A
26, 388–401. https://doi.org/10.1007/s11367-020-01847-0. spanish case study using carbon footprinting. Food Policy 41, 94–102. https://doi.org/
Philis, G., Ziegler, F., Gansel, L.C., Jansen, M.D., Gracey, E.O., Stene, A., 2019. Comparing life 10.1016/j.foodpol.2013.04.009.
cycle assessment (LCA) of salmonid aquaculture production systems: status and perspec- Vázquez-Rowe, I., Villanueva-Rey, P., Hospido, A., Moreira, M.T., Feijoo, G., 2014. Life cycle
tives. Sustain. 11. https://doi.org/10.3390/su11092517. assessment of european pilchard (Sardina pilchardus) consumption. A case study for Ga-
Philis, G., Ziegler, F., Jansen, M.D., Gansel, L.C., Hornborg, S., Aas, G.H., Stene, A., 2021. licia (NW Spain). Sci. Total Environ. 475, 48–60. https://doi.org/10.1016/j.scitotenv.
Quantifying environmental impacts of cleaner fish used as sea lice treatments in salmon 2013.12.099.
aquaculture with life cycle assessment. J. Ind. Ecol. 1–14. https://doi.org/10.1111/jiec. Villanueva-Rey, P., Vázquez-Rowe, I., Arias, A., Moreira, M.T., Feijoo, G., 2018. The impor-
13118. tance of using life cycle assessment in policy support to determine the sustainability of
Pomponi, F., Li, M., Saint, R., Lenzen, M., D’Amico, B., 2022. Environmental benefits of fishing fleets: a case study for the small-scale xeito fishery in Galicia, Spain. Int. J. Life
material-efficient design: a hybrid life cycle assessment of a plastic milk bottle. Sustain. Cycle Assess. 23, 1091–1106. https://doi.org/10.1007/s11367-017-1402-z.
Prod. Consump. 30. https://doi.org/10.1016/j.spc.2022.01.028. Walpole, S.C., Prieto-Merino, D., Edwards, P., Cleland, J., Stevens, G., Roberts, I., 2012. The
Rico, A., Jacobs, R., Van den Brink, P.J., Tello, A., 2017. A probabilistic approach to assess an- weight of nations: An estimation of adult human biomass. BMC Public Health 12, 0–5.
tibiotic resistance development risks in environmental compartments and its application https://doi.org/10.1186/1471-2458-12-439.
to an intensive aquaculture production scenario. Environ. Pollut. 231, 918–928. https:// WHO, 2007. Protein and amino acid requirements in human nutrition, WHO technical report
doi.org/10.1016/j.envpol.2017.08.079. series. https://apps.who.int/iris/handle/10665/43411.
Robb, D., MacLeod, M., Hasan, M., Soto, D., 2017. Greenhouse gas emissions from aquacul- Woods, J.S., Verones, F., Jolliet, O., Vázquez-Rowe, I., Boulay, A.M., 2021. A framework for
ture: a life cycle assessment of three Asian systems. FAO Fisheries and Aquaculture Tech- the assessment of marine litter impacts in life cycle impact assessment. Ecol. Indic. 129.
nical Paper No. 609, Rome. https://doi.org/10.1016/j.ecolind.2021.107918.
Rosenbaum, R.K., Bachmann, T.M., Gold, L.S., Huijbregts, M.A.J., Jolliet, O., Juraske, R., Yacout, D.M.M., Soliman, N.F., Yacout, M.M., 2016. Comparative life cycle assessment (LCA)
Koehler, A., Larsen, H.F., MacLeod, M., Margni, M., McKone, T.E., Payet, J., of tilapia in two production systems: semi-intensive and intensive. Int. J. Life Cycle As-
Schuhmacher, M., Van De Meent, D., Hauschild, M.Z., 2008. USEtox - the UNEP-SETAC sess. 21, 806–819. https://doi.org/10.1007/s11367-016-1061-5.
toxicity model: recommended characterisation factors for human toxicity and freshwater Yurtsever, M., Yurtsever, U., 2018. Commonly used disposable plastic bags as a source of
ecotoxicity in life cycle impact assessment. Int. J. Life Cycle Assess. 13, 532–546. https:// microplastic in environment, in. Proceedings of the International Conference on
doi.org/10.1007/s11367-008-0038-4. Microplastic Pollution in the Mediterranean Sea. Springer, pp. 99–106 https://doi.org/
Salvador, S., Costoya, X., Sanz-Larruga, F.J., Gimeno, L., 2018. Development of offshore wind 10.1007/978-3-319-71279-6_14.
power: contrasting optimal wind sites with legal restrictions in Galicia, Spain. Energies Zhang, W., Belton, B., Edwards, P., Henriksson, P.J.G., Little, D.C., Newton, R., Troell, M.,
11, 2011–2020. https://doi.org/10.3390/en11040731. 2022. Aquaculture will continue to depend more on land than sea. Nature 603, E2–E4.
Samuel-Fitwi, B., Nagel, F., Meyer, S., Schroeder, J.P., Schulz, C., 2013a. Comparative life https://doi.org/10.1038/s41586-021-04331-3.
cycle assessment (LCA) of raising rainbow trout (Oncorhynchus mykiss) in different pro- Ziegler, F., Winther, U., Hognes, E.S., Emanuelsson, A., Sund, V., Ellingsen, H., 2013. The car-
duction systems. Aquac. Eng. 54, 85–92. https://doi.org/10.1016/j.aquaeng.2012.12. bon footprint of norwegian seafood products on the global seafood market. J. Ind. Ecol.
002. 17, 103–116. https://doi.org/10.1111/j.1530-9290.2012.00485.x.
Samuel-Fitwi, B., Schroeder, J.P., Schulz, C., 2013b. System delimitation in life cycle assess-
ment (LCA) of aquaculture: striving for valid and comprehensive environmental assess-
ment using rainbow trout farming as a case study. Int. J. Life Cycle Assess. 18,
577–589. https://doi.org/10.1007/s11367-012-0510-z.
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