Towards Environmental Sustainability in Marine Finfish - Editedriri

REVIEW
published: 21 April 2021

doi: 10.3389/fmars.2021.666662
Towards Environmental
Sustainability in Marine Finfish
Aquaculture
Carlos Brais Carballeira Braña 1* , Kristine Cerbule 2 , Paula Senff 3,4 and
Insa Kristina Stolz 5
1
School of Marine Science, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile, 2 Faculty of Biosciences,
Fisheries and Economics, UiT the Arctic University of Norway, Tromsø, Norway, 3 Leibniz Centre for Tropical Marine
Research, Bremen, Germany, 4 Faculty of Biology/Chemistry, University of Bremen, Bremen, Germany, 5 GEOMAR Helmholz
Centre for Ocean Research Kiel, Kiel, Germany
Aquaculture is one of the fastest growing food production sectors and has
great potential for food security and livelihoods. However, it generates concerning
consequences for the environment, including chemical and biological pollution,
disease outbreaks, unsustainable feeds and competition for coastal space. Recent
investigations are focusing on sustainable techniques (e.g., polyculture, offshore
facilities) to improve the relationship between the industry, environment and society. This
review provides an overview of the main factors of ecological concern within marine
Edited by: finfish aquaculture, their interactions with the environment, and highlights sustainable
Viola Liebich, alternatives that are currently in use or development. Adequate environmental
Bremen Society for Natural Sciences,
Germany
monitoring and location of farms, the reduction and exploitation of wastes and chemicals
Reviewed by:
being used is crucial to ensure the growth and continuity of aquaculture production.
Christina Hoerterer,
Keywords: IMTA, finfish farms, environmental pollution, environmental assessement, eutrophication
Alfred Wegener Institute Helmholtz
Centre for Polar and Marine Research
(AWI), Germany
Kilian Toledo-Guedes, INTRODUCTION
University of Alicante, Spain
Aquaculture can be traced back as far as 4000 years in Egypt (Chimits, 1957) and more than
*Correspondence:
Carlos Brais Carballeira Braña
2000 years in China (Beveridge and Little, 2002; Edwards, 2004; Lu and Li, 2006) and Europe
carlos.carballeira@pucv.cl (Beveridge and Little, 2002; Buschmann and Muñoz, 2019). Aquaculture was further developed
because the capacities of traditional aquatic ecosystems could not support the human population
Specialty section: growth (Costa-Pierce, 2002), thus, it became a social necessity. The rapid development of the
This article was submitted to aquaculture sector by producing great amounts of diverse fish products for human consumption
Global Change and the Future Ocean, has been called the “Blue Revolution” (Costa-Pierce, 2002) which started during the 1960s in
a section of the journal Asia (Thia-Eng, 1997) and in the West in the late 1970s and early 1980s (MacKay, 1983). Since
Frontiers in Marine Science
then, the aquaculture sector is continuing to significantly develop towards new diversification and
Received: 10 February 2021 intensification (Ahmed and Thompson, 2018). The economic demand for fish protein is increasing,
Accepted: 17 March 2021
however, capture fisheries production remains static or is diminishing (depending on the species in
Published: 21 April 2021
question) during the last decades (FAO, 2018). Currently, aquaculture produces more than 30% of
Citation: the total fish consumed worldwide (FAO, 2018).
Carballeira Braña CB, Cerbule K,
In recent years, society has become increasingly concerned about the effects that anthropogenic
Senff P and Stolz IK (2021) Towards
Environmental Sustainability in Marine
activities have on the environment. The assessment of impacts from aquaculture farm activities has
Finfish Aquaculture. not been examined extensively enough to cope with the growth of this industry (Bostock et al., 2009;
Front. Mar. Sci. 8:666662. Bohnes and Laurent, 2021). These assessments are mostly based on physical-chemical measures
doi: 10.3389/fmars.2021.666662 and/or sediment characteristics with comparably limited focus on environmental carrying capacity
Frontiers in Marine Science | www.frontiersin.org 1 April 2021 | Volume 8 | Article 666662

Carballeira Braña et al. Environmental Sustainability Marine Finfish Aquaculture
studies, required for aquaculture sustainability. Environmental Worldwide, there are many developed co-operational projects
characteristics of the receiving environment define the that are or have been researching for more sustainable methods
Environmental Carrying Capacity (ECC) of the selected (Table 1). The main topics studied address general sustainable
site, which will determine the discharge load (i.e., dissolved and intensification of aquaculture, educational purposes, animal
particulate organic matter, chemicals) that might be assimilated welfare, alternative feeds, land-based and aquaponics systems.
by the affected ecosystem. These environmental characteristics According to Life Cycle Assessment studies (a tool to assess the
include bathymetry conditions, physical-chemical characteristics environmental impacts to get a product, including processing,
of water and substrate, trophic status, and colonizing capacity transport, use and disposal), fish feed and burning of fossil
(fouling) (Garmendia et al., 2012). fuels (required for mobility and electricity) are the main
Since its appearance on the international agenda, the concept environmental impacts from net cage aquaculture (Samuel-
of sustainability has been the topic of much debate, both Fitwi et al., 2012; Ramos et al., 2019). From a feed efficiency
in terms of how to achieve it as well as how to define point of view, aquatic livestock use less energy than terrestrial
it. A popular definition is the one coined by the 1992 livestock to grow and, therefore, produce less greenhouse gasses
United Nations Conference on Environment and Development (Ayer and Tyedmers, 2009; Pelletier et al., 2009). For example,
report Our common future in the context of sustainable eutrophication is not considered due to the inexistence of specific
development: “meeting the needs of the present without impact methodologies for the marine environment (Samuel-
compromising the ability of future generations to meet their Fitwi et al., 2012; Woods et al., 2016; Winter et al., 2017; Ramos
own needs” (Brundtland, 1987). However, not all ecosystems et al., 2019). Nevertheless, more research is needed to measure
can be conserved unaltered (Brundtland, 1987). Principles of life cycles covering all environmental aspects (Samuel-Fitwi et al.,
sustainability include three dimensions: (1) the economy (ability 2012; Woods et al., 2016; Winter et al., 2017).
to be maintained without an outside influx of money; Copus and Optimal environmental monitoring plans help to understand
Crabtree, 1996), (2) the society [equity and cultural capital that the impacts of waste management, their utilization and
can be passed to succeeding generations (Copus and Crabtree, possibilities of how it can be reduced. The exploitation of
1996)], and (3) the environment [maintenance of an ecosystem’s farming wastes implies a double benefit; less environmental
characteristic diversity, productivity and biogeochemical cycling contamination and higher economic profits. Thus, polycultures
(Amundsen and Osmundsen, 2018)]. In this chapter, we focus on and technological advances should help the aquaculture industry
environmental aspects of sustainability. and are necessary towards aquaculture sustainability.
Environmental aspects of sustainability in aquaculture may This review focuses on marine finfish aquaculture. The
not be achieved until several problems are solved: eutrophication majority of world aquaculture occurs inland, producing nearly
of receiving ecosystems, destruction of natural habitats, twice as much as coastal and marine aquaculture (Li et al., 2018).
dependence on fishmeal and fish oil, introduction of exotic However, these are mostly small operations while multinational
species and inadequate medication practices (Martinez-Porchas companies are mainly focused on marine farming. Those
and Martinez-Cordova, 2012; Figure 1). companies highly contribute to aquaculture research (including
minimizing economic losses from uneaten feed or ineffective
chemical treatment), define best management practices, develop
more detailed monitoring studies and help governments in
defining environmental regulations. Marine aquaculture, also
known as mariculture, includes those cultures located in the
sea while coastal aquaculture implies human-made structures in
areas close to the sea (e.g., coastal ponds and gated lagoons). Most
of the finfish aquaculture from the Americas, Europe and Oceania
is produced through mariculture (FAO, 2018). Most African
production belongs to inland aquaculture because infrastructure,
technical expertise and investment are needed to promote marine
culturing (FAO, 2020). In terms of live weight, molluscs represent
the most biomass from mariculture. Nevertheless, when edible
animal-source food is considered, a conversion factor of 6
and 1.15 is applied to the commonly reported weight from
molluscs and finfish, respectively. Therefore, finfish are the main
contributor from whole aquatic animal production to human
nutrition (FAO, 2018; Edwards et al., 2019).
Mariculture concerning finfish production is dominated by
salmonid aquaculture, especially Atlantic salmon (Salmo salar),
which is also the most cultured carnivorous fish worldwide (Føre
et al., 2018; Filgueira et al., 2019; Figure 2).
FIGURE 1 | The main pollution sources from marine finfish aquaculture and
From an ecological point of view, intensive fish farming
their related effects on the environment.
represents the highest environmental risk when compared to

TABLE 1 | Summary about co-operational projects (ongoing or finished) concerning sustainable methods in aquaculture.
Acronym Project goals Website Countries involved Project duration
Aquaculture intensification
GAIN Green Aquaculture Intensification in https://www.gain2020.com/ United Kingdom, Germany, Ireland, 2018 – 2021
Europe Spain, Portugal, Norway, Netherlands,
TAPAS Tools for Assessment and Planning of http://tapas-h2020.eu/ Poland, Italy, Canada, China
BLUEEDU Aquaculture Sustainability http://www.blueedu.eu/ United Kingdom, Malta, France, Spain, 2016 – 2020
MefANIG Fostering growth in the blue economy http://www.susaquastirling.net/blog/ Netherlands, Hungary, Greece, 2016 – 2019
EURASTIP by developing an action plan for 2017/2/22/mefanig-kicks-off-in- Sweden, Norway, Ireland, Scotland
innovative European aquaculture VET khulna-bangladesh Faroe Islands, Finland, Iceland, Ireland,
and harmonized qualifications https://cordis.europa.eu/project/id/ Norway, Scotland, Croatia, Cyprus,
(2016-2019) 728030 France, Greece, Italy, Spain finished
MedAID Metric for Aquaculture Nutrition Impact http://www.medaid-h2020.eu/ Bangladesh, Scotland, Denmark 2017 – 2019
for Girls https://www.giz.de/en/worldwide/ Belgium, United Kingdom,
63918.html Netherlands, Norway, Ireland, 2017 – 2021
MYSAP Promoting Multi- Stakeholder http://performfish.eu/ Malaysia, Vietnam, Thailand 2017 – 2021
PerformFISH Contribution to international Croatia, Denmark, Egypt, France,
Cooperation on Sustainable Solutions Greece, Italy, Netherlands, Norway,
for Aquaculture Development in Portugal, 2017 –2022
South-East Asia Spain, Tunisia, Turkey, United Kingdom
Mediterranean Aquaculture Integrated Myanmar, Germany
Development. Supporting sustainable Greece, Spain, Italy, France, Norway,
intensification of aquaculture sector, Denmark, Portugal, Slovenia,
helping to realize its potential for food United Kingdom, Ireland, and Croatia
security, nutrition and employment.
Consumer Driven Production:
Integrating Innovative Approaches for
Competitive and Sustainable
Performance across the Mediterranean
Aquaculture Value Chain
Feed sourcing
PROteINSECT Insects as sustainable sources of https://www.proteinsect.eu/ China, Africa, Europe (7 countries) finished
INvertebrateIT protein https://invertebrateitproject.eu/ https: Ireland, Belgium, France, Spain, 2017 – 2019
IFFO Disruptive and forward-looking //www.iffo.net/fishery-improvement-projects Portugal 2017 – 2019
Ento-Prise opportunities for competitive and www.prise.odi.org United Kingdom, Peru, China finished
sustainable aquaculture United Kingdom, Senegal, Pakistan,
Fishery Improvement Projects Central Asia, Kenya, Burkina Faso
Pathways to Resilience in Semi-Arid
Economies
Integrated Multitrophic Aquaculture
iDREEM Increasing Industrial Resource http://www.idreem.eu/ United Kingdom, Scotland, Israel, 2012- 2016
KEEP Efficiency in European Mariculture https://www.keep.eu/project/418/ Norway, Ireland, Cyprus, Italy, 2007 – 2013
IMPAQT Project - Sustainable and sustainable-and-environmentally-friendly- Netherlands 2018 – 2021
Environmentally friendly Aquaculture aquaculture-for-the-atlantic-region-of-europe Ireland, United Kingdom, France,
For the Atlantic Region of Europe https://impaqtproject.eu/ Spain, Portugal Ireland, Greece,
Intelligent Management Systems for Luxembourg, Netherlands, Turkey,
Integrated Multi-Trophic Aquaculture France, Portugal, United Kingdom,
Poland, Spain, Italy, China
Education, training, networking
AQUAEXCEL AQUAculture infrastructures for https://www.aquaexcel2020.eu/ Norway, Ireland, Scotland, Denmark, 2015 – 2020
EXCELlence in European fish research https://cordis.europa.eu/project/id/ Netherlands, France, Spain, Portugal, 2008 – 2011
towards 2020 213143 https://cordis.europa.eu/project/id/ Czech Republic, Hungary, Greece, 2009 – 2013
SARNISSA 222889/reporting http://www.aquatnet.com/ Belgium 2011 – 2014
https://www.sustainablefish.org/ United Kingdom, France, Egypt, since 2006
SEAT Sustainable Aquaculture Research https://sustainableseafood Thailand, Malawi, Cameroon, since 2018
AQUA-TNET Networks in Sub-Saharan Africa consumption.wordpress.com/ Netherlands finished
Sustainable trade in ethical https://www.susaquastirling.net/ Bangladesh, China, Thailand, Vietnam
aquaculture s/ThirdBontheAnnualOysterFestival 26 countries
SFP European Thematic Network in the MarketTrials__26Jul19.pdf United States
SSCI field of aquaculture, fisheries and United Kingdom
SWOMA aquatic resources management. United Kingdom, Sierra Leone
Rebuild depleted fish stocks and
reduce the environmental and social
impacts of fishing and fish farming
The Sustainable Seafood Consumption
Initiative worked with remote
communities in Sierra Leone to offer
sustainable income for local women
through the culture, processing and
marketing of native mangrove oysters.
Economic sustainability
PrimeFish Developing Innovative Market https://cordis.europa.eu/project/id/ Denmark, Iceland, Germany, Norway, 2015 – 2019
ClimeFish Orientated Prediction Toolbox to 635761 Canada, Vietnam, Faroe Islands, 2016 –2020
Strengthen the Economic Sustainability https://climefish.eu/ United Kingdom, Spain, Greece
and Competitiveness of European Norway
Seafood on Local and Global Markets
Developing production scenario
forecasts to serve as input to
socio-economic analysis to identify
risks and opportunities within fisheries
and aquaculture related to climate
change.
(Continued)

TABLE 1 | Continued
Acronym Project goals Website Countries involved Project duration
Animal and human health
IMAQulate Probiotics in Aquaculture http://www.stir.ac.uk/imaqulate India, Bangladesh, Kenya, 2015 – 2019
PEDIGREE increase awareness of issues around https://www.pedigree.stir.ac.uk/ United Kingdom 2019 – 2020
BOLTI risk & efficacy of prophylactic health http://www.susaquastirling.net/blog/2017/2/ Scotland, Bangladesh, finished
EGYPT product (based on findings of 22/bolti-egypt https://sniph.stir.ac.uk/ Egypt, United Kingdom finished
SNIPH IMAQulate) United Kingdom, India, Kenya and
Behavioral Prophylaxis Project Tanzania
Sustainable New Ingredients to
Promote Heath
Private consultancy
WORLDFISH Building capacity, coordination and https://www.worldfishcenter.org/ Nepal, China, Bangladesh, 2018 – 2022
SAS communication for collective action on http://www.sasnet.nl/ https://www.tunatech.de/ United States, Cambodia, Vietnam, since
TUNATECH small-scale fisheries Philippines. Zimbabwe. Uganda, 2005
Sustainable Aquaculture Solutions Myanmar, Nigeria, Singapore, since 2008
Bluefin Tuna Project in Egypt (Mersa Thailand, Mozambique, Netherlands,
Gargub) Cameroon, Malawi, Laos, Zambia,
United Kingdom, Germany, Norway,
Egypt, Tanzania, Australia, Zambia,
Ghana, Indonesia, South Africa
Netherlands
Germany
Land-based recirculation systems
VEOLIA Sustainable Water Solutions for https://www.veolia.com/en/solution/ United States, Canada na
AQUAOPTIMA Aquaculture treatment-recycling-of-wastewater-aquaculture- Norway since 1993
CLEWER Optimal water quality - ideal fish health industry Finland since 1984
MAT Greece, Turkey since 2012
LSS Urban Protein Production with https://aquaoptima.com/en Poland, Slovak Republic na
AGROFIM Innovative Recirculating Aquaculture Denmark since 2009
Blue Unit Systems https://www.clewer.com/aquaculture/ Ireland na
Nova Q Aquarium filtration systems and ?lang = en
engineering
Indoor Recirculating Aquaculture https://matlss.com/
System with Integrated Greenhouses https://www.agrofim.com/
Consultancy specializing in water http://blue-unit.com/
quality management for land-based https://www.nova-q.ie
fish farms
Driving Innovation in RAS Water
Quality
Offshore systems
SalMar ASA Offshore fish farming- Passion for https://www.salmar.no/ Norway since 1991
Salmon
Aquaponics
AQUAPONIC SOURCE Growing fish and plants together https://www.theaquaponicsource.com/ United States na
SMART AQUAPONIC Development of intelligent http://www.smart-aquaponics.com/ Belgium na
AGROFIM management tools for aquaponics https://www.agrofim.com/ Poland, Slovak Republic na
Aquaponic in action
other aquaculture sectors due to the feeding needs and the However, it must be noted that there are also other direct effects,
chemicals used associated with the production process (Tornero such as landscape visual impact, noise, odor, and marine litter
and Hanke, 2016). This chapter will further describe the from intensively farmed areas (Figure 3; Martinez-Porchas and
main effects that the marine finfish aquaculture creates for Martinez-Cordova, 2012; Radford and Slater, 2019). Untreated
the environment. wastewater from fish farms includes elevated nutrient levels, but
also chemicals used to prevent diseases. In the case of open net
cages, the ability to prevent these contaminants from entering the
MAIN ENVIRONMENTAL AQUACULTURE surrounding water is very limited. The focus of this chapter is on
EFFECTS the main sources of contamination in marine finfish aquaculture
(as highlighted, e.g., by Duarte et al., 2009).
As the aquaculture sector is developing and expanding, it has an
increasing effect on the surrounding environment. These effects
include nutrient pollution from uneaten feed and metabolic Nutrient Pollution
waste, chemical pollution from various substances used in During the production process, uneaten feed and the metabolic
the production process (such as medical treatments, including waste of fish release nitrogen and phosphorus into the water.
antibiotics and antiparasitics) as well as the spread of farmed fish This process causes problems in intensive farming areas where
genes, parasites, and diseases to wild populations (Sarà, 2007; food sources from a broader region are concentrated in a smaller
Burridge et al., 2010; Little et al., 2016; Weitzman, 2019). An area (Dempster and Sanchez-Jerez, 2008). Waste originated from
important indirect effect of the production process is the high aquaculture farms may create a significant source of excess
impact on aquatic ecosystems through the need to use wild fish nutrients within the coastal areas. These excess nutrients are
to feed carnivorous species of farmed fish (Little et al., 2016). mainly related to the proliferation of primary producers that

FIGURE 2 | Main finfish species produced in marine aquaculture globally, salmonid species on the right (percentages extracted from FAO, 2018).
FIGURE 3 | Intensive marine land-based fish farm discharging effluents directly into the sea (NW Spain). Authorship: Carlos Carballeira.
may trigger micro- and macroalgal blooms that may be toxic at pisciculture facilities. Up to 50% of supplied feed can be
(Wang et al., 2018). The causes of emergence of toxic algae lost to the surrounding water and sediment, posing not only
are still unknown and seem to be more related with natural an economic, but also an environmental threat (Ballester-Moltó
or anthropogenic nutrient and silica fluxes from terrestrial et al., 2017b). Particulate waste from aquaculture farms, such as
sources (Masó and Garcés, 2006; Kumar et al., 2018), but feeds, feces, and other organic material, traps harmful lipophilic
nutrients are required for algal blooms and they may originate compounds, increasing their incorporation into the trophic

chain, elevates water turbidity and, thus, decreases photic depth, medicines such as antiparasitics and antibiotics to disinfectants
and is finally deposited close to fish farms, modifying chemical (Burridge et al., 2010; Martinez-Porchas and Martinez-Cordova,
and biochemical properties of the sediment (Price et al., 2015; 2012; Ozbay et al., 2014; Rico et al., 2018). Antifouling chemicals
Brager et al., 2016; Ballester-Moltó et al., 2017a). are also being used at aquaculture facilities to avoid the
Nitrogen species make up the largest volume of aquaculture clogging of meshes.
contaminants and provide a source of nutrients for primary Chemicals used in aquaculture enter surrounding marine
producers. When discharged into the surrounding environment, environments and may be toxic to non-target organisms in
they affect the trophic balance and can lead to eutrophication at proximity of the farming sites because they are not highly
low hydrodynamic sites, where less mixing occurs (Price et al., selective, e.g., benzoylurea pesticides affect naupliar development
2015; Urbina, 2016; Herrera et al., 2018). Ammonia is excreted of copepod Tisbe battagliai (Macken et al., 2015). Moreover, the
directly by the fish and produced through decomposition of effectiveness of most chemical treatments is low within high fish
uneaten food. It is toxic to animals, especially at high pH densities because of increased host availability. This is especially
levels, and when levels of unionized ammonia are also high, the case in open cage systems where chemical inputs are directly
this reduces fertility and increases susceptibility to diseases (Ip released to the marine environment.
and Chew, 2010). Ammonia is rapidly taken up by primary Antibiotics are used in aquaculture to control the spread
producers because of the higher preference for reduced forms of pathogenic bacteria (Burridge et al., 2010; Martinez-Porchas
of nitrogen or oxidized by Nitrobacteraceae bacteria into nitrite, and Martinez-Cordova, 2012; Rico et al., 2018). This raises
which is 50 to 100 times more toxic to freshwater animals concerns about the possible effects on biological diversity and of
than those from seawater (Kroupova et al., 2005). Nitrification selection of antibiotic resistant bacteria when antibiotics are used
continues when nitrite is oxidized into nitrate, which is less excessively over time, e.g., Erythromycin and bacterial kidney
toxic than its previous forms. At low levels of oxygen as disease (Burridge et al., 2010). Moreover, the use of a single
found in sediment, nitrate is reduced into dinitrogen gas, pharmaceutical can cause insignificant consequences while it may
then sulfate-reducing bacteria transfer electrons to sulfur forms have a highly adverse effect when acting in combination with
(sulfate, thiosulfate, and elemental sulfur) releasing toxic sulfides other chemical substances (Fent et al., 2006). It is estimated that
(Wang and Chapman, 1999). around 70 - 80% of antibiotics given as medicated feed ends up
Nitrogen and phosphorous support and limit the growth in the marine environment around the farming sites (Ferreira
of aquatic primary producers because they are needed et al., 2007). Another environmental risk is associated with
for the synthesis of proteins, DNA, RNA, and the energy parasiticides, which contaminate the water column and seabed
transfer, respectively (Conley et al., 2009). The vast majority, either as uneaten medicated feed, fecal material or in soluble form
about 80%, of phosphorus contained in fish feed has been in urine (Tornero and Hanke, 2016). Additionally, parasiticides
found to be lost to surrounding waters, with a large that are being used in aquaculture to control ectoparasite
portion ending up in the sediment (Holby and Hall, 1991). infestations can lack specificity to target organisms thereby
Phosphorous introduced from aquaculture pollution can posing a threat to non-target species including small crustaceans
be more mobilizable (more easily released to the overlying in the proximity of the farm site (Burridge et al., 2010).
water and posteriorly taken up by primary producers) Due to increasing resistance, the approach in some cases is
than what is usually found in the environment, hindering to use even larger concentrations of chemical treatments. Use
recovery and increasing the potential to cause eutrophication of antibiotics is subjected to reporting but quantities are not
(Jia et al., 2015). always publicly accessible (e.g., Chile) (Burridge et al., 2010).
However, there are examples of diseases that classically have
Chemical Pollution been considered as occurring only in freshwater but today cause
Numerous chemicals are being used in aquaculture production problems in marine aquaculture, e.g., furunculosis (Aeromonas
(Table 2) to prevent and treat disease outbreaks, ranging from salmonicida), bacterial kidney disease (Renibacterium
salmoninarum) and some types of streptococcosis in such
species as salmonids and turbot (Toranzo et al., 2005).
TABLE 2 | Main chemical pollution sources in marine finfish aquaculture and their Antifouling products are used in aquaculture on submerged
related effects on the environment. structures (cage nets and supporting infrastructure) to avoid
Antibiotics Affect biodiversity increase risk of selection of biofouling by various epibiotic organisms, such as marine
antibiotic resistant bacteria, can affect food safety algae, barnacles, bivalves, bryozoans and others. Marine finfish
(Ferreira et al., 2007; Burridge et al., 2010) aquaculture biofouling can result in compromised cage structures
Parasiticides Can affect non-target organisms (Tornero and and have negative effects on farmed fish lowering water flow
Hanke, 2016) through cages, leading to poor oxygen availability or increased
Antifouling products Can affect non-target organisms (Fitridge et al., risk of disease (Fitridge et al., 2012). Antifouling products are
2012; Tornero and Hanke, 2016)
associated with increased copper levels, which are toxic to several
Disinfectants Can have negative effects on fish health and other
marine organisms (difficult to assess) (Buschmann
marine invertebrates, especially molluscs (Fitridge et al., 2012).
et al., 2006) In addition, the immune defense of exposed organisms around
Anesthetic Few associated negative effects (Burridge et al., farming sites is affected by antifouling and copper-based products
2010) (Fitridge et al., 2012; Tornero and Hanke, 2016).

There is little information available regarding disinfectant compared to the abundance of their wild conspecifics as is the
quantities and particular substances, and not so much research case with wild Atlantic salmon (S. salar) (Thorstad et al., 2008).
has been performed on the effect of disinfectants, which are used Negative effects to the wild populations are related to ecological
on land-based facilities, nets, platforms, boats, ponds, and other interactions, such as possible genetic impacts in case of inter-
surfaces (Buschmann et al., 2006). breeding and competition for both food and habitat (Izquierdo-
Anesthetics are being used in marine aquaculture to reduce Gómez et al., 2017). Around 80-83% of the European aquaculture
stress during handling and to improve the efficiency of production originates from selective breeding to improve growth
procedures (Sneddon, 2012). However, the use of those chemicals performance (Janssen et al., 2017). In the wild, farmed fish
does not pose significant risks to the environment due to may transmit these genetic characteristics, which may result in
infrequent and limited use and practically no discharge into reduced life span, increased susceptibility to diseases and lower
the environment when good management practices are followed individual fitness leading to a lower survival rate of future wild
(Burridge et al., 2010). populations (Glover et al., 2017; Faust et al., 2018).
Fish farms are considered as fish aggregation devices (FAD)
due to the significant increase of surrounding populations after
Disease Outbreak and Biological installation of facilities because their wastewater is a source
Pollution of food and their structure acts as artificial reefs (Dempster
Outbreaks of fish diseases are a result of the interaction between et al., 2006; Grigorakis and Rigos, 2011; Sanchez-Jerez et al.,
the pathogen, the host, and the environment. Several drivers may 2011; Aguado-Giménez et al., 2016; Riera et al., 2017; Figure 4).
cause a disease outbreak: high fish density, compressed rearing Cage aquaculture is colonized similarly to artificial and rocky
cycle and a limited genetic diversity (Kennedy et al., 2016). reefs but unique fish assemblages have been observed around
Considering the high stocking densities within aquaculture deployed aquaculture facilities. The combination of both floating
farms, bacterial, viral, and fungal diseases as well as the spread and bottom artificial structures (e.g., Integrated multi-trophic
of parasites is taking place at an increasing rate. For example, aquaculture, IMTA) enhances the population of local species and
in marine aquaculture such spread of diseases occurred during increases the complexity of fish assemblages (Wang Y. et al.,
Infectious Salmon Anemia outbreaks (Lyngstad et al., 2018). 2015). However, artificial reefs for sea cucumber cultivation
Another recently growing problem is dealing with parasites (e.g., may trigger the settlement of polyps whose jellyfish blooms
salmon lice Leopephtheirus salmonis) (Overton et al., 2018). may generate severe gill problems on farmed fish (e.g., salmon)
While the culture period is shortened to minimize the production (Purcell et al., 2007). Furthermore, microbial densities are
costs, this may lead to higher pathogen virulence due to evolution increasing, as a result of the medusae preying on the predators
(Kennedy et al., 2016). In addition, the limited genetic diversity of microbes like small copepods and ciliates (Turk et al., 2008).
due to selective breeding may lead to the development of a Wild organisms may improve the quality of sediment and water
pathogen specialization towards a particular group of hosts by reducing the organic load released by farms (Katz et al.,
(Kennedy et al., 2016). 2002; Vita et al., 2004). However, fishing in the vicinity of farms
Another issue concerning aquaculture-based negative effects must be restricted because of public health concerns (disease
on the environment is the risk of biological pollution. Biological and antibiotic transmission) and ecological reasons. Fishing at
pollution can be caused by the farming of exotic species, which FADs will reduce local populations and subsequently adjacent
also act as vectors for new parasites and diseases, and of native populations that are attracted by the empty ecological niches
but cultured individuals with a reduced genetic diversity that and the food supply (Riera et al., 2017). Other wild populations
may also pose a threat to wild populations. After shipping, are attracted by the increased biomass and may damage farming
aquaculture is the second largest sector causing the introduction facilities (e.g., sea lions, dolphins, cormorants, and bluefish)
of exotic species worldwide and likely to increase because of the easing biological pollution (Aguado-Giménez et al., 2016).
spread of farms into more pristine areas (Hewitt and Campbell,
2007). Although some escaped fish have shown homing behavior
(remaining in the vicinity of the cages), other studies found POLLUTION ASSESSMENT
escaped fish dozens of kilometers away from the place of
cultivation (Toledo-Guedes et al., 2014; Dempster et al., 2016). The control of the main marine aquaculture production
Recapture methods have been only partially effective, therefore, by multinational companies helps the development of
efforts should be focused on preventive measures. environmental regulations and technological breakthroughs,
Biological pollution can take place as the accidental release improves feeding techniques by reducing feed losses, and
of fish during operation, damage to cages (e.g., caused by harsh decreases the usage of antibiotics by the increasing utilization
weather conditions), or attacks by wild predators. It may also of vaccines (Føre et al., 2018). However, these regulations
occur during spawning when farmed fish are kept in open are mainly based on the economically dominant type of
cages to a size in which they can become sexually mature (e.g., fish farming; net cages on protected coasts. This is why
Atlantic cod (Gadus morhua)), allowing drifting of fertilized Environmental Monitoring Plans (EMPs) are usually based on
eggs into the surrounding environment (Jensen et al., 2010). the assessment of water and sediment changes. Meanwhile,
Although accidental escapes (especially large scale) do not occur the location of farms at high dispersive sites (high flow
often, the number of individuals escaping can be large when velocities and great depths) may disable this type of monitoring

FIGURE 4 | Opportunistic species from turbot land-based farms: (a) mullets [Nerga, Cangas do morrazo (Spain)], (b) birds [Quilmas, Carnota (Spain)], (c) green
algae [Grove, Salnés (Spain)]. (a,d) Recreational fishermen are usually found in the dumping area, attracted by the high concentration of fish [d – Aguiño, Barbanza
(Spain)]. Authorship: Carlos Carballeira.
(Sutherland et al., 2018). Changes on physicochemical properties Li and Liu, 2018). Nevertheless, these methods are either under
of the water column are most times undetectable (Sarà, development or expensive.
2007) even between input and output water from land-based
farms. Sediment is a matrix that integrates and concentrates
contaminants from the water column and facilitates studies Chemical Pollution Assessment
of ecological integrity of benthic communities (Caeiro et al., Chemical treatments used in aquaculture depend on several
2012) but this may not be present at hard bottom coastal factors - disease, the location of the facility, system parameters,
areas and offshore sites because organic waste is highly treatment type, and legislation. There are specific regulations
dispersed (Carballeira et al., 2012). The following sections concerning the use and quantities of specific substances
describe the current type of assessment, monitoring plans in aquaculture but this highly differs between countries
and methods, and how to improve and adapt it to different (Burridge et al., 2010). These include mandatory risk
types of facilities. evaluation and authorization processes before a particular
substance can be used. There are also various modeling
tools, based on the assessment of dilution and dispersion
Nutrient Pollution Assessment of both chemical treatments and particles (from medicated
Nutrient release may affect water quality (e.g., water turbidity, feed), that calculate chemical exposure and ecotoxicological
dissolved oxygen), increase trophic resources, and modify risks close to cages (Rico et al., 2018). Even though there
the geochemical properties of sediment (Qi et al., 2019). are only few monitoring and control requirements regarding
Nevertheless, most times the effect of a fish farm on the water accumulation of chemicals used, their components and
column is negligible due to the high dilution and recycling derivatives (FAO, 2009).
of nutrients at sites where farms are established (Soto and Authorities are setting regulations concerning allowed
Norambuena, 2004). For this reason, environmental impact substances but also routes of delivery, dosage by fish species
assessments are mainly based on the study of sediment, and other limitations (Dawood et al., 2018). Fish do not
but this is not possible in hard-bottom sites. To reach metabolize antibiotics efficiently; releasing a large part
sustainable alternatives, effective assessment methods must of the substance to the marine environment that should
be used without being sediment dependent. Traditional be posteriorly monitored or reused within polycultures
water monitoring measures physicochemical parameters (Burridge et al., 2010).
mainly related with organic contamination (dissolved oxygen, Overall, the use of antimicrobials in aquaculture has declined
nitrogen forms, phosphorus, salinity, turbidity, pH, chlorophyll, because of improved rearing practices and hygienic conditions,
temperature, sulfides, and redox potential). When a parameter as well as the development of vaccines. Also, the use of antibiotics
represents a certain pollution threshold, the water sample as growth promoters is not practiced in aquaculture (Burridge
is sent to a laboratory for further analysis. Every step is et al., 2010; Done et al., 2015; Watts et al., 2017; Okocha et al.,
performed manually, which is time- and cost-consuming, 2018). Producers in the largest farming countries are required
and contamination episodes might be missed (Li and Liu, to report particular diseases and the chemicals prescribed to
2018). New sensors that utilize fiber optics, laser technology, avoid their outbreaks and minimize chemical treatments, e.g.,
biosensors, optical sensors, and microelectronic mechanical allowable number of salmon lice (L. salmonis) per fish in Atlantic
systems to detect different water quality parameters in situ salmon (S. salar) farming which is monitored regularly during
and in real-time are being developed (Simbeye et al., 2014; the production process (Hjeltnes et al., 2018).

Biological Pollution Assessment aimed at favoring farmers’ production (e.g., feed efficiency and
Fish from open net cages may escape and enter directly into the absence of anoxic sediments) and regulate food standards (FAO,
surrounding environment. The ability to assess the escape rate 2009; Weitzman and Filgueira, 2019). Determination of ECC of
depends on factors determined by species behavior, including the an aquatic ecosystem is a complex process generally based on
time escaped fish are spending close to the aquaculture facilities mathematical models, making difficult to assess and implement
after the escape and their mortality rates. These behaviors are standards (Silva et al., 2012; Bueno et al., 2017).
important for calculating the efficiency of potential recapture
methods (Izquierdo-Gómez and Sanchez-Jerez, 2016; Dempster Open Land-Based Farming
et al., 2016; Arechavala-Lopez et al., 2017). Recapture is said to be Environmental monitoring programs for marine open land-
mostly ineffective (around 50% of escaped fish) although required based aquaculture effluents are generally based on maximum
in many jurisdictions (Dempster et al., 2016). According to that, percentages of increase or decrease of several physicochemical
a contingency plan consisting of notification of the escape to parameters between input and output water. These parameters
responsible authorities, recapture actions and a final report must are related to the eutrophication risk by measuring nutrient
be carried out (Arechavala-Lopez et al., 2018). content (ammonia, nitrites, nitrates, and phosphorus) and related
Recapture methods are similar to those that have been used parameters such as turbidity, dissolved oxygen, chlorophyll, and
in wild fisheries and include the identification of farmed fish pH (Carballeira et al., 2012).
(Dempster et al., 2016). Farmed fish can be tagged and thereby One of the most critical problems from marine land-based
identified in case of escape using acoustic telemetry or mark and aquaculture monitoring is the absence of sensitive methods
recapture techniques (Arechavala-Lopez et al., 2017). Methods able to determine the amount and toxic effects of pollutants
to detect escaped fish are based on genetic differences (Karlsson in highly diluted seawater discharges. This is because there
et al., 2011) and external characteristics, as a consequence of high are no industries with similar discharges; moreover, intensive
crop densities and handling (fin erosion, opercular deformities aquaculture is relatively modern and was previously considered
and body lesions) (Fiske et al., 2005). A simple and less expensive as a non-polluting activity (Carballeira et al., 2018). This is
method includes the identification of scales based on the fact that not the case with net cages and soft bottom samples, because
fish in aquaculture lose some scales when handling or during there is usually sediment underneath and its integrative capacity
feeding. These lost scales are then regenerated, and this can be concentrates contaminants from the water column and allows its
detectable on the farmed fish (Izquierdo-Gómez et al., 2017). determination (Caeiro et al., 2012).
Triploid organisms are being used in commercial farming
(e.g., oysters and trout) but triploidy attempts with some species
have been unsuccessful with an increase in deformities, e.g., Net Cages
Atlantic salmon (S. salar) (Lovatelli et al., 2013). Triploidy Net cages involve higher: (i) losses of nutrients (feed and
might be a potential solution to prevent interbreeding but it biological waste) and chemicals; (ii) emergence and transmission
will not solve the problem of potential disease transmission or of diseases; (iii) risk of escapees and attraction of predators;
competition for food and space. The location of the farm (to and (iv) greater problems in the shared use of waters (Price
avoid harsh weather conditions) is important as a preventive and Morris, 2013). The environmental requirements of cage
measure for escapes. The same is said about the provision of production are very similar worldwide; they are based on
appropriate technical standards for the operation of facilities the same parameters of study, by focusing the study on the
(e.g., appropriate mooring and netting of the cages) and ecosystemic effects in the benthic macrofauna of the sediment
development of farming routines (Arechavala-Lopez et al., 2017). and the appearance of bacterial mats (Holmer et al., 2008;
Wilson et al., 2009). Moreover, implications of EIA’s and routine
monitoring involve high costs and time because there is a
Environmental Monitoring Plans lack of harmonization between federal and regional roles in
The effects of marine aquaculture on the surrounding regulating aquaculture activities, and appropriately qualified
environments (especially in open production systems) may be scientific personnel (particularly in the area of benthic ecology
limited to a minimum. To establish these limits, monitoring data and this is regarded as a major issue for the EIA).
are needed at different levels of organization, so that, ecological Norway, being the largest salmon producer in the world,
changes can be detected and Ecological Quality Standards is developing the aquaculture practice that is based on the
can be defined and included within an Environmental Impact sustainable development (one that does not exceed the carrying
Assessment (EIA) (Telfer and Beveridge, 2001; Holmer et al., capacity of the ecosystem) (Hersoug, 2015; Michaelsen-Svendsen,
2008). Monitoring techniques must be effective, scientifically 2019). Even if each particular farming site meets the requirements
rigorous, cost-effective, dynamic, and regionally/site adapted independently, overall, they may exceed the load capacity in the
to facilitate their usage and avoid unwanted damage to the area in question and cause environmental problems. Therefore,
ecosystem. Research is still needed to improve the monitoring the presence of salmon lice (L. salmonis) in salmon farming is
programs, in particular those related to eutrophication at considered as an important factor relating to the ECC. Overall,
different scales and the ecosystem approach at larger scales close cooperation between the Norwegian government and
(Holmer et al., 2008). Only few countries apply the ECC producers allows better enforcement of sustainable measures, but
approach (e.g., Norway) and regulations from the majority are this approach does regulate production carrying capacity instead

of ECC (Chapman and Byron, 2018). The first may not guarantee However, there are no standardized protocols for the selection
long-term sustainability. Thus ECC should be considered. of indicator species (Carballeira et al., 2019), and biotic indices
need to be regionally adapted and may show higher biodiversity
Monitoring Methods at transitional zones of disturbances than reference sites because
Unfortunately, EMPs do not usually consider ECC measures and of low-medium concentrations of organic matter (Galand et al.,
there are problems associated with current monitoring methods 2016). Thus, it might be hindering the interpretation of results.
regarding sampling, selection of indicator species, use of biotic Moreover, sampling and the studies related to benthic fauna
indices and the absence of sediment (hard-bottom sites). Most are very onerous, and very little has been done regarding the
of the time methods lack standardization and effectiveness at combined effects of pollutants and the ecological preferences of
different aquaculture scenarios. marine indicator species, impeding the development of sensitive
biomonitoring tools (Belando et al., 2017). The application of
Sampling frequency analysis techniques, the calculation of specific renewal
Before and After Control Impact (BACI) is a common design rates along environmental gradients and multiple regression
proposed to evaluate anthropogenic perturbations on ecological techniques allow to select the explanatory variables and define the
variables. Using powerful statistics, different approaches allow physicochemical thresholds that best characterize the significant
adjusting to the particular real conditions (Underwood, 1993). changes in the ecological status of the system represented by the
However, the BACI method depends on the preoperational community of polychaetes (Martinez-Garcia et al., 2013).
study (which is only done once just before starting the activity) Sessile organisms are good candidates for indicator species
and requires choosing control sites arbitrarily and assumes because they cannot change their habitat, have to deal with
the control and impact sites to be similar before the impact. and/or adapt to shifts to less favorable conditions (Scheu et al.,
When a contaminant disperses with distance from a point 2011). Being bioaccumulators, the study of their body burdens
source it is suggested that a gradient design will be more and pollution effects allow the determination of influence area
sensitive to change than BACI sampling designs (Rubio-Portillo and extent of impact, respectively (Carballeira et al., 2012).
et al., 2019). Gradient designs avoid the problem of arbitrarily The uptake of organic matter from fish farms by associated
selecting a control site, enable chemical, physical, and biological invertebrates can be traced by examining changes in their fatty
changes to be assessed as a function of distance, and results acid profile due to the assimilation of terrestrial-based oils
are easier to interpret and to use in public policy decisions used in fish feed (Gonzalez-Silvera et al., 2015; White et al.,
(Ellis and Schneider, 1997). 2019). Additionally, metabolomics is emerging as a technique to
assess the impact of aquaculture effluents on wild populations
Indicator Species and Biotic Indices (Maruhenda-Egea et al., 2015).
Geochemical changes of the sediment due to organic enrichment
alter the composition and structure of the infauna, favoring Stable Isotope Analysis
the dominance of the tolerant-generalist versus the sensitive- Deducing the fate of nutrients in an aquaculture or natural system
specialized species (Resende et al., 2010; Martinez-Garcia et al., can be done based on balance calculations of the nutrient content
2013). The effects of the farms on the benthic communities in plants or animals (Vandermeulen and Gordin, 1990; Brown
are widely studied, especially on the communities of macro et al., 1999; Shpigel et al., 2013).
and meio invertebrates from the infauna, and occasionally on However, there are shortcomings to this technique when
the benthic microbial communities (Verhoeven et al., 2016; trying to account for all nutrient transformation in the system
Weitzman, 2019). It is usual to determine the degradation of the (Gribsholt et al., 2005). A more detailed view can be obtained
sediment by using the formation and coverage of Beggiatoa spp., through stable isotope analysis (SIA), a widely accepted tool to
a chemotrophic filamentous bacterium common in sulfur-rich reconstruct diets and trophic relationships of organisms and their
environments (Verhoeven et al., 2016; Weitzman, 2019). food (DeNiro and Epstein, 1978; Middelburg, 2014). The analysis
Benthic communities (e.g., bacterial mats, polychaetes, of stable isotopes is often applied in marine or estuarine sciences
amphipods) are the most studied group as they are those that and can be used to examine fluxes of carbon and nitrogen from
manifest the greatest changes when environmental conditions ecosystems and pollution from coastal aquaculture (Peterson and
are altered (Buschmann et al., 2006; Borja et al., 2009; Keeley Fry, 1987; Herbeck et al., 2014; Viana et al., 2015). Compared
et al., 2012; Martinez-Porchas and Martinez-Cordova, 2012; to the natural aquatic ecosystem, aquaculture derived nutrients
Ozbay et al., 2014; Martinez-Garcia et al., 2013; Weitzman, are usually enriched in their δ15 N and depleted in their δ13 C
2019; Verhoeven et al., 2016). It is very common to use them values, allowing this source to be traced along gradients and into
as bioindicators of the state of the benthic ecosystem (both sinks (Holmer et al., 2007; Watai et al., 2015). In case larger
indicator species and communities), such as the increase of isotopic differences are needed, isotope labeling (the introduction
opportunistic species (e.g., Capitella capitata or Malacoceros of compounds high in the heavy isotope) can be applied to
fuliginosus) (Maldonado et al., 2005) or the reduction of sensitive trace the fate of the labeled matter over time, through specific
species (e.g., Pennatula phosphorea) (Wilding, 2011) up to metabolic pathways or along trophic chains (Berthold et al.,
macroscopic parameters (e.g., ABC Curves, Shannon-Wiener 1991; Burford et al., 2002; Gribsholt et al., 2005; Barrón et al.,
Index, ITI, AMBI, OSI, BHQ) of the invertebrate community 2006). A number of studies have worked with labeled feed in an
(Borja et al., 2009; Cromey et al., 2012; Keeley et al., 2012). aquaculture context, tracing the fate of feed derived nutrients in

the vicinity of fish cages (Felsing et al., 2006; Gonzalez-Silvera issues, and/or overproduction (Aguilar-Manjarrez et al., 2017;
et al., 2015; White et al., 2017, 2019), monitoring nutrient uptake Shetty et al., 2018).
in different fish tissues (Felip et al., 2012; Maruhenda-Egea et al., Geographic Information Systems (GIS), remote sensing, and
2015), or identifying uptake of cyanobacteria in an aquaculture modeling are commonly used for aquaculture site selection
pond (Wang Z. et al., 2015). because they provide preliminary information on site assessment.
Establishing a monitoring system based on isotope values of However, they are mainly based on physical variables, e.g., water
an indicator species gives the opportunity to trace the impact of temperature and chlorophyll a concentration (chl a) (Huber
aquaculture effluents in the surrounding ecosystem and check the et al., 2016; Stelzenmüller et al., 2017). From a sustainable
effectiveness of mitigation measures (Costanzo et al., 2005). point of view, the location of farms must consider the ECC
of the waterbody and get in situ background information
Hard Bottom Sites (e.g., isotopic signal 15 N, biodiversity and metal contents)
Eutrophication and toxicity assessment methods of hard bottom to enable the necessary production with the least possible
sites should always integrate physicochemical and biological adverse impact on the environment and consequently, the farm
indicators as a basis for management decisions although some itself. For this reason, assessment of suitability must consider
methods use only selected water column parameters (Ferreira conservative estimates (i.e., precautionary principle), presence of
et al., 2011). Contaminant concentrations may not be useful predators, spacing between the proposed site and other farms,
parameters (most times below the detection limits of analytical industries, recreational activities, cultural or ecological assets, and
methods) while properly selected indicators should show a environmental characteristics (FAO, 2018).
gradient that reflects the level of human-induced impairment. In general, more carrying capacity will be achieved at
No single set of indicators will meet the needs worldwide oligotrophic sites with higher coastal exposure, waves, seafloor
so general guidelines for the selection of indicator species must slope, depth, current speed, salinity, dissolved oxygen and
be established, both for soft and hard substrates (Rice et al., lower temperature, suspended solids, and colonizing capacity
2012). Hard substrates sites require the selection of sensitive or (Garmendia et al., 2012). However, the multifactorial nature
tolerant sessile organisms (Scheu et al., 2011), such as macroalgae, of the ecological capacity makes it difficult to evaluate it
bivalves, cnidarians, and defined ecological state groups for both theoretically. Moreover, the contribution of other specific or
unpolluted and contaminated situations. diffuse sources of pollution (e.g., wastewater treatment plants,
Other indicator species, such as sponges (Porifera) have shown agricultural activities, river mouths) that occur in a specific
to be strong indicators of environmental changes (Luter et al., physical space must also be considered.
2014) and are highly sensitive to environmental shifts (Holmes, The requirements for appropriate sites are directly related
2000; Hill and Hill, 2002). to the interplay of the farm with the surrounding environment.
In the case that no sessile organisms or study matrices (apart Recirculating Aquaculture Systems (RAS) provide the possibility
from the water column) are present, studies on accumulation as to cultivate fish in a closed system, minimizing the threat of
well as on diversity or abundance of species could be focused parasites, diseases, and changing environmental conditions.
on the study of the colonizing communities of artificial surfaces It also allows for the immediate treatment of waste. As
previously placed in areas affected by aquaculture activities. land-based facilities, RAS may be located almost everywhere
while net cages must be located at protected coasts with high
dispersive capacity and far from other sources of pollution.
SITE SELECTION However, RAS operations require specific infrastructure
and know-how of the system and have high starting and
One of the main challenges for the sustainable development operational costs (Badiola et al., 2012). While they are becoming
of aquaculture is the distribution of water, land, and other increasingly important in the aquaculture sector of developed
resources with alternative uses, such as fishing, agriculture, and countries, their successful widespread application needs further
tourism. Marine Spatial Planning must consider the zoning of economic and political incentives as well as widespread
aquaculture (to define suitable areas for fish farming or mixed sharing of information (Badiola et al., 2012). Unlike offshore
activities) and identifying the most appropriate places for the cultures, RAS facilities also compete for land space with
specific location of farms (site selection) (Chen et al., 2007). other industries.
Environmental impacts of a single farm may not be significant Land-based marine fish farms are economically limited by the
when considered individually but may be relevant if other farms, pumping of water inside the facilities (elevation from sea) and
fishing grounds, or activities are located in the same area. need to be located at exposed coasts with high dispersive capacity
Environmentally sound selections of the site, away from habitats (Carballeira et al., 2012). Facilities may be ordered (from the
of ecological interest, together with adequate management, are highest to the lowest) according to the level of site requirements
the best tools to prevent or minimize the negative environmental as follows: Net cages, marine IMTA, land-based, offshore, IMTA
effects of farming (Porporato et al., 2020). Therefore, aquaculture land-based, RAS.
operators must act as environmental managers to ensure Site selection must also integrate multiple use marine spatial
a pollution-free environment in which to culture healthy plans to consider economic and social objectives from all affected
organisms. Impacts on the benthos and water column may sectors and achieve successful management. Wind farming and
happen because of an improper site selection, administrative energy production from micro and macroalgae are compatible

candidates, being the best ones that are based on nutrient removal (Whitmarsh et al., 2006). Their culture is, however, not a panacea
(Stelzenmüller et al., 2017). as particle absorption is restricted to appropriate size ranges
(Wang et al., 2012) and the benefits of bivalve culture
sometimes fail to be achieved at all (Navarrete-Mier et al., 2010).
Moreover, bivalves also produce particulate waste in the form of
DEVELOPMENT OF SUSTAINABLE
pseudofeces, creating a need for further remediation of impacted
METHODS sediment (Cubillo et al., 2016).
Particulate waste of fed species or shellfish cultivation can
Integrated Multi-Trophic Aquaculture be used as a source of feed for detritivorous animals such as
(IMTA) polychaetes and sea cucumbers. Some sea cucumber species have
An important step towards sustainable aquaculture is to consider been found to thrive on the debris of fish farms (Ahlgren, 1998;
excess food and fecal matter not as a waste product, but as a Slater et al., 2011; Hannah et al., 2013). They can constitute an
resource that contains high amounts of nutrients and essential additional crop and have beneficial effects on sediments by re-
fatty acids that should be recycled and not discarded (Bischoff working upper sediment layers and influencing the development
et al., 2009). Based on this idea the concept of IMTA was created, of microbial communities (Moriarty and Pollard, 1982; Moriarty
which applies a simplified food web structure to a farming et al., 1985; Uthicke, 1999; MacTavish et al., 2012). In closed
system of fed-species, such as fish and shrimp, together with aquaculture systems, such bioturbating detritivores can also be
extractive organisms, such as molluscs and seaweed that take integrated into sand filters where oxic and anoxic conditions in
up particles and nutrients from the environment (Neori et al., the sediment become the site of nitrogen conversion and removal
2004). Integrated aquaculture also produces higher yields than (Palmer, 2010; Robinson et al., 2015).
mono-species systems in addition to satisfying rising consumer In the case of land-based farms in the littoral zone, IMTA can
demands for environmental standards (Neori et al., 2004). The be arranged inside (indoor) or outside (outdoor) of the facilities
practice of IMTA aims to perfect this principle by combining (Figure 5). Outdoor systems require the aquatic installation of
species at different trophic levels for a balanced-ecosystem devices close to the source of pollution and in the direction
approach (Chopin et al., 2007). Reducing the load of nutrients of the prevailing current. This is a complex management
and organic matter released by IMTA systems, preserves the option and may be limited by physiological requirements of
quality of the receiving ecosystem, a secondary economic benefit the extractive species to specific seasons or hydrodynamic
is obtained and the social image of aquaculture is improved conditions. The strong energy of the sea in exposed coasts can
(Barrington et al., 2009). endanger the structures or detach organisms, e.g., Saccharina
Macroalgae are a popular component of IMTA setups and is able to withstand strong waves but can only be grown in
have a number of advantages over conventional mechanical winter (Guerrero and Cremades, 2012; Freitas, 2015). On the
or microbial filtration systems. Common nitrifications filters contrary, indoor systems with their controlled conditions are
use up dissolved oxygen and require additional equipment and more easily managed and are theoretically the most respectful
monitoring (Chopin et al., 2001). Contrary to this, integrating option for the environment (Guerrero and Cremades, 2012), but
algae into an aquaculture system counterbalances nutrients, CO2 compete for land space.
levels, acidity, and increases dissolved oxygen while producing
valuable biomass (Chopin et al., 2001; Neori et al., 2003). Lagooning/Artificial Wetlands
Macroalgae are fast and easy to grow, highly productive, with a Wastewater lagooning is a highly effective, low-cost solution
higher yield of cultivation than land plants, no need of pesticides (initial installation and maintenance) for purifying wastewater
and with great potential for various economic applications (Gao from land-based farms (Porrello et al., 2003). The treatment
and McKinley, 1994; Ditchburn and Carballeira, 2019). An of wastewater consists of a series of physical, chemical, and
example of ideal seaweed for a biofilter is Ulva lactuca, which biological processes to remove contaminants and separate clean
is fast-growing, has high filtration performance, thrives under or at least reusable water and solid waste, which can be used for
high nutrient conditions, tolerates a wide range of water quality, a number of industrial or agricultural purposes. Such types of
and has a high market value (Neori et al., 2003, 2004). Sales artificial wetlands are already widely used for the treatment of
of seaweed grown in biofilters can cover the additional costs of municipal waste and are especially effective at removing excess
implementation (Neori et al., 2004; Ditchburn and Carballeira, nitrogen and storing excess phosphorus in the soil (Vymazal,
2019), but economic validity is not always ensured and the area 2010; De Lange et al., 2013; Almuktar et al., 2018). This type
required can be extremely large (Kang et al., 2003; Shpigel et al., of phytotreatment has already been tested with wastewater
2013). from fish ponds as means of algal ponds and wetlands and
Rearing shellfish may have positive effects on the environment has shown to be an efficient system by reducing nutrient
and promote biodiversity (Ozbay et al., 2014). Oysters and contents and modifying physico-chemical parameters of water
mussels cultivated close to fish farms benefit from the suspended (Porrello et al., 2003; Adeoye et al., 2009; Omitoyin et al.,
organic matter, show improved growth and reduce organic 2017).
nutrient load in the water (Sarà et al., 2009; Troell et al., However, lagooning systems require large surface areas, thus,
2009; Reid et al., 2010) and integrating mussel longline competing for land space with other sectors. The installation
cultivation to existing operations should be economically viable of aeration systems makes artificial wetlands more efficient by

FIGURE 5 | Example of integrated multi-trophic aquaculture outside (OUT) and inside (IN) of a facility.
enhancing the oxidation rate of pollutants and allows reducing (Singh et al., 2014). While still a niche market, they are gaining
the space needed (El-Kamah et al., 2011; Almuktar et al., popularity as a delicacy vegetable (Custódio et al., 2017).
2018). Using the area for additional production makes this Maintaining the integrity and function of ecosystems is
method more profitable. Various halophytes in different types of vital for the sustainable spread of aquaculture operations. An
natural and constructed wetlands are already successfully used example is the practice of Silvofishery or Integrated Mangrove
as down-stream filters of municipal, industrial, or agricultural Aquaculture, which maintains a certain degree of tree cover in
wastewater (Verhoeven and Meuleman, 1999; Vymazal, 2010). and around aquaculture ponds constructed in mangrove areas
Their use can have great economic benefits when compared to (Budihastuti et al., 2012; Bosma et al., 2016). Mangroves are
conventional water treatment and they are being investigated important tropical ecosystems that provide a habitat and nursery
as possible extractive species in integrated aquaculture as they to many species, prevent sedimentation of reefs and seagrass
are able to utilize high levels of ammonia, which can be toxic meadows, protect coasts from storm surges and flooding, and
to other plants (Glenn et al., 1991; Cardoch et al., 2000; Kudo store atmospheric carbon dioxide (Nagelkerken et al., 2000,
and Fujiyama, 2010). Different species of halophytes have been 2008). Many mangrove areas globally have already been lost
successfully cultivated in the effluents of European sea bass to the conversion of coastal habitats, including for aquaculture
(Dicentrarchus labrax) in RAS (Waller et al., 2015) and can production (Valiela et al., 2001; Alongi, 2002). Constructing
be integrated in artificial wetlands or cultivated hydroponically aquaculture ponds while maintaining a level of tree cover in

and around the ponds is a strategy how to combine food can in turn be cultivated as a feed source, increasing their
production with mangrove protection (Yunus et al., 2015). practical value. The macroalgae Ulva lactuca, which has low
Sustainable aquaculture is seen as an important way to protect economic value when sold directly, provides high quality feed
these ecosystems, preserve their biodiversity and secure their for abalone or sea urchins (Neori et al., 2000) and microalgae
continued contribution to climate protection (Primavera, 2005; serve as feed for mussels (Shpigel et al., 1993). Thus, algae
Ahmed et al., 2016). Such an approach to integrated cultivation production can be considered as a more sustainable industry
is especially important in the context of tropical developing than continuing to harvest fish for fishmeal. It is estimated
countries where the importance of aquaculture goes beyond that if microalgae were used as fishmeal replacement, the effect
intensive production of high-value species and includes its vital would be to remove 30% of the fishing pressure thereby helping
contribution to food production and livelihoods in rural areas to conserve marine ecosystems (Beal et al., 2018). Algae may
(Harrison, 1996; Edwards, 2000). Especially in Asia, low-input, substitute fish oil, be viable and even improve growth of farmed
integrated fish farming systems have a long tradition (Chen et al., fish so it should be considered to reduce harvesting fish for
2019). Large, government driven projects have small success rates fishmeal (Sarker et al., 2020).
if they create dependencies and have low adaptation rates by Effluents can be directly valorised by growing primary
stakeholders (White et al., 2005). Community-based projects put producers (Milhazes-Cunha and Otero, 2017; Wei et al., 2017;
local actors in the focus and aim to improve livelihoods through Li et al., 2019). Sludges and effluents from aquaculture activities
capacity building, diversification and business development may also be bioremediated by decomposers, detritivores, and
(Pomeroy, 2012; Yuerlita et al., 2013). Extensive, co-managed biofilms, whose biomass in turn presents a useful resource for
aquaculture operations require low input and technologies while feed production (Martinez-Porchas et al., 2014; Barnharst et al.,
still being vital sources of income (Partelow et al., 2018; Senff 2018; Gómez et al., 2019; Robinson et al., 2019). Solid wastes are
et al., 2018). an appropriate feed for polychaetes, which provide protein and
important fatty acids as feed for fish, shrimp, or crab production,
Sustainable Feed Management reducing or eliminating the need for manufactured feed based on
Sourcing of aquaculture feed is one of the sustainability core farmed crops or fish meal (Brown et al., 2011; Alava et al., 2017;
challenges of marine finfish aquaculture (Klinger and Naylor, Pajand et al., 2017). Fish feed can also be supplemented or even
2012). Intensified production and the cultivation of high value replaced through the application of biofloc technology. In this
carnivorous fish largely depends upon the use of fish meal and approach, microbial growth in the water column of fish tanks
fish oil as the main feed ingredients, making it a consumer of or ponds is stimulated through the addition of carbohydrates
capture fisheries products, especially of nontargeted fisheries and in the form of sugar, starch, or cellulose (Avnimelech, 2012).
small forage fish (Cao et al., 2015). This has caused environmental Heterotrophic bacteria, using these as a substrate to build
as well as economic concerns, with feed costs being a large part of proteins for growth, require nitrogen, which they take from
total production expenses, and important progress has been made the surrounding water. Dissolved nitrogen species in the water
towards sustainability by improving feed efficiency (Verdal et al., are, thus, transformed into bacterial biomass, aggregating into
2017), turning fish offal into useful silage (Cunha et al., 2019; bioflocs that can be consumed by shrimp or fish (Avnimelech,
Gonçalves et al., 2019) or designing plant-based, polychaete- 2012). Biofloc technology in tilapia ponds can provide 50%
based, and insect-based protein feeds (Boyd, 2015; Pahlow et al., of the protein consumed by the fish (Avnimelech, 2007) and
2015; Rhodes et al., 2016; Gómez et al., 2019; Llagostera et al., when used as a protein source in shrimp feed, microbial floc
2019). The challenge has been to replace fish oil with other meal showed the same results or even outperformed soybean
alternatives and ensure the high content of highly unsaturated or fishmeal ingredients (Kuhn et al., 2009, Kuhn et al., 2010;
fatty acids within the feed to maintain the nutritional quality of Bauer et al., 2012). Biofloc systems have been mainly used in
the fish for human consumption (Little et al., 2016). While the freshwater ecosystem and for herbivorous organisms but recent
use of land-based feed may reduce the pressure on fisheries, it studies included mullets and pacific shrimp (Legarda et al.,
can significantly increase the pressure on freshwater resources 2019). The successful application of biofloc technology, however,
(water footprint), due to water consumption and pollution in requires knowledge of the system, close monitoring to maintain
crop production (Pahlow et al., 2015). appropriate C:N ratios and microbial densities and upscaling
However, recently new approaches have been developed to from laboratory to economic application (Kuhn et al., 2010;
reduce excess feed used and loss of food. In intensive fish farming Hende et al., 2014).
where feeding is taking place by an automatic system, it is
important to monitor the feeding activity of the fish and adjust Sustainable Use of Chemicals
the amount of feed to the feeding behavior. Such monitoring can There is an increasing tendency to develop methods with
be done by using, for example, an underwater camera technology the aim of reducing extensive chemical substance use,
or other similar methods that detect uneaten feed and stopping and, therefore, minimizing environmental pollution. Such
the feeding process (Zhou et al., 2017). alternative methods can have other positive effects on production
More sustainable feed management can be achieved through such as cost minimization for the producer and increased
IMTA in a number of ways. Dissolved nitrogen in wastewater consumer acceptance.
used to promote the growth of micro- or macroalgae replaces Methods that have been used vary between several factors
the need for fertilizer or growth media. These extractive species such as the fish species and disease in question as well as the

FIGURE 6 | Example of precision fish farming system including (a) surface camera, (b) underwater camera with multiparameter water probe, (c) sonar, (d) acoustic
telemetry system with hydrophone, and (e) smart trap (based on Føre et al., 2018).
production methods used and characteristics of the area where prebiotics, synbiotics, acidifiers, plant extracts, nucleotides, and
the facility is located. They can be divided as precautionary such immunostimulants as β-glucan and lactoferrin (Dawood
methods (e.g., limiting fish density), methods concerning disease et al., 2018). Chinese herbal medicines can be used as an
prevention (e.g., immunostimulant feeds and herbal medicine alternative in disease prevention in aquaculture because of
additives), co-culturing of different marine species which both antibacterial, antiviral, immunostimulant, and growth promoting
benefits from such a production model, different physical substances (He et al., 2016).
techniques used such as so called “lice skirts,” plankton nets Co-culturing of different fish species can be used to limit
around the fish cage, to avoid parasite infestations (Stien et al., pathogens during production. An example of this could be the use
2018) as well as other varying from above mentioned aspects (He of cleaner fishes, which can limit the spread of ectoparasites such
et al., 2016; Haugland et al., 2017; Dawood et al., 2018; Jahangiri as salmon lice (Lepeophtheirus salmonis) because of predation by
and Esteban, 2018; Escobar-Dodero et al., 2019). those fish species towards these small crustaceans. However, this
The largest aquaculture producing countries have been using implies that appropriate health and welfare conditions must be
regulations to report disease occurrence and to limit the fish provided for both species, as farming together different species
density according to those measures because high density of would also generate a risk of common disease spread, e.g.,
fish or cages highly increase the risk of disease transmission, amoebic gill disease when lumpfish (Cyclopterus lumpus) are
e.g., infectious salmon anemia or infectious pancreatic necrosis farmed together with Atlantic salmon (Haugland et al., 2017).
(Escobar-Dodero et al., 2019). Genetic improvement through selective breeding has been
Other methods that have been used include functional feed used in aquaculture mostly to improve growth performance of
additives, which can be administered via feed (He et al., 2016). fish. In Europe, around 80% of aquaculture originates from
They are non-nutritive ingredients that affect fish performance selective breeding mainly because of this reason. However, it is
concerning, for example, feed utilization, survival, and growth possible to select fish for other traits such as disease susceptibility
rate (Jahangiri and Esteban, 2018). These additives promote (Yáñez et al., 2014). Also, vaccines are being used to minimize
fish growth and can replace antibiotics in those countries the need for antibiotic treatments. However, the method can
where it is still used as preventing and growth promotional be associated with some negative effects such as stress caused
measures, and thereby avoiding associated negative effects (Done to fish during the treatment when handling of fish is involved
et al., 2015). Most widely researched options include probiotics, (Miccoli et al., 2019).

FIGURE 7 | Summary of main sustainability issues of marine mariculture and respective methodological (black boxes) and infrastructure based (gray boxes) solutions.
Lytic bacteriophages can be used as therapeutic agents against et al., 2013). However, the open sea is considerably rougher
marine bacterial diseases such as those associated with vibrios. than coastal waters and strong waves can break structures or
However, more research is still needed to apply these viruses detach organisms, worldwide distribution of species is uncertain,
under field conditions and to avoid dispersal of unwanted and there are political, technical, and cost-distance limitations
genes and effects on fish microbiota (Kalatzis et al., 2018; (Troell et al., 2009; Forster, 2013). Free-floating and propelled
Plaza et al., 2018). installations may be too expensive and improvements on
mooring systems are required to expand farms at deeper areas.
Offshore Some finfish farms are already located at open sea, most of
Generally, mariculture facilities are located close to human them are round and submersible net cages to dissipate water
settlements, in protected coasts or inland, with shallow waters currents and to avoid waves (Benetti et al., 2010). Seaweed and
and low hydrodynamic energy. Recently, more aquaculture bivalve become profitable more quickly because they do not need
facilities are being placed in semi-exposed areas with a potential to be fed and operational costs are lower. Several farms including
of offshore aquaculture development. To have a regular supply IMTA have been developed, mainly in Asian countries, but all
of oxygen and temperature, and to avoid diseases, parasites, at shallow waters and close to the coast (Buck et al., 2018).
algal blooms, and user conflicts, the aquaculture industry has Moreover, it is still difficult to avoid the detachment of seaweed
been developing new technologies for offshore facilities. Offshore and mussels with traditional longline systems (Troell et al., 2009).
systems are not environmentally sustainable in the long term Wind-powered water pumps and solar-powered water heating
(there is no reduction on contaminant outputs) but are a systems are proposed to be integrated with offshore systems
more respectful alternative with the environment since the load because will reduce long-term operating costs and environmental
capacity increases with the depth and the higher dispersion implications and increase competitiveness and profitability.
of the waste (Kapetsky and Aguilar Manjarez, 2013; Lovatelli For aquaculture to expand, greater social acceptance, adapted
et al., 2013; Gentry et al., 2016). From a spatial perspective, regulations and long-term sustainability are necessary (Kapetsky
offshore production has a lot of potential; it may be expanded and Aguilar Manjarez, 2013; Lovatelli et al., 2013). However,
to many countries, move away from sensitive marine biocenosis offshore production development is sometimes limited because
areas, be combined with wind, oyster, and mussel farms, few countries have regulations that explicitly mentions offshore
increase biodiversity by creating an artificial reef, etc. (Lovatelli or open-ocean aquaculture, and fewer still have codified

definitions of this type of culture (Davies et al., 2019). Sometimes CONCLUSION

governance of offshore industries is ambiguous or undefined,
presenting obstacles to allow their activities (e.g., United States The key to affordable and sustainable aquaculture practices
and Australia) (Davies et al., 2019). lies in the independence from natural resources through
recycling or remediation of fish production wastes. However,
Copper Net Cages sustainability and the reduction of ecological impacts depend
Biofouling development reduces the water flow inside the fish on the governance of infrastructure and environmental
cage forcing farmers to clean and change polymer nets frequently, agencies must improve legislation and regulations worldwide.
or use antifouling coatings, thus, increasing operational costs Many countries with important aquaculture production have
(Berillis et al., 2017). Antifouling coatings are discarded every some environmental regulations but lack clear frameworks
year producing toxic effects because of the release of their for emerging technologies such as offshore farming. Every
main active ingredients to the environment (copper oxide, farmer may develop sustainable principles, methodologies, or
cadmium, and zinc) (Kalantzi et al., 2016). Organisms grown practices. Therefore, it is recommended to promote certifications
inside and outside of trials using copper nets were safe for human of good practices.
consumption and no accumulation of copper was detected Environmental monitoring costs may be too expensive
in sediment, but assessment and environmental monitoring and onerous, hindering its application or interpretation and
is needed because copper alloy released more copper to the make sustainable development more difficult. So that, just
surrounding environment and affect the biota more compared to representative, non-redundant, reliable, cost-effective, and
the conventional net (Kalantzi et al., 2016). significant measures should be included within environmental
monitoring plans to harmonize production with the ECC of
Precision Fish Farming (PFF) the selected site.
There is a recent sustainable framework of fish farming called Different methods are being used to reduce the environmental
Precision Fish Farming (PFF), which developed from the impact of aquaculture practices, but further research is still
concept of Precision Livestock Farming (PLF) (Norton and needed. For example, the use of selective breeding to reduce
Berckmans, 2018) to pisciculture. PLF and PFF use hardware the use of chemicals for disease treatment may diminish the
(e.g., sensors), observers, and intelligent software to improve population genetic difference and possibly increase the virulence
animal health and welfare while increasing productivity, yield, of the pathogenic organisms that may specialize in particular
and environmental sustainability (Figure 6). In contrast to organisms. Also, the use of vaccines represents a sustainable
livestock production, intensive fish farming methods are more method but can cause significant stress for the fish during the
recent, crop is largely determined by environmental conditions vaccination which itself can increase the disease risk.
and monitoring methods are more expensive and complex at Land-based IMTA aquaculture with recirculation systems
aquatic ecosystems (Føre et al., 2018). seems to be the best alternative option in terms of wastewater
The majority of components proposed to be included in reduction and exploitation, prevention of disease outbreaks,
PFF systems are already developed (e.g., hydrophones, sonars, escapees, monitoring costs and efficiency. However, there is a
acoustic telemetry systems, cameras) but in many cases they competition for land space that can be complemented by well-
need to be adapted for mariculture activities. For example, managed offshore polyculture facilities integrated with solar and
smart sediment traps will greatly improve knowledge on wind farms. Despite those, numerous other sustainable measures
particle settling flux data, oceanic nutrient cycles, food efficiency were proposed (Figure 7).
through online monitoring and detection of temporal changes of Aquaculture sustainability is an on-going process that requires
sedimentation rates (Jurg, 1996). Studies of smart traps include integration of all stakeholders. Government, farmers, ecologists,
autonomous neutrally buoyant sediment traps (Sherman et al., and consumers should drive aquaculture practices under a risk
2011) and sedimentation accumulation sensors with a wiper arm assessment approach to reduce wastes, disease outbreaks, and
connected to a logger and a transmitter/receiver (Thomas and operational costs enhancing sustainability potential.
Ridd, 2005; Whinney et al., 2017).
Fish farming monitoring knowledge is required to understand
the complex interactions between growing methods and farmed
fish with the aquatic environment. An increase on the knowledge AUTHOR CONTRIBUTIONS
of behavioral and physiological responses may help reach
All authors contributed to conception and design of the study,
sustainability (by reducing feed loose, disease and parasitic
wrote sections of the manuscript, prepared the figures, and
outbreaks, enhance animal vital development, etc.) but it
revised, read, and approved the submitted version.
seems that the general aim is to improve intensive fish
farming conditions from a production perspective instead of
an environmental approach (carrying capacity, feed alternative,
etc.). To apply a more sustainable concept of PFF, predictive FUNDING
models should include the information supplied by the
application of technological advances to monitor other ecosystem CC is a postdoctoral researcher supported by the FONDECYT
parameters potentially affected by crops. Postdoctoral Programme (3170795).

ACKNOWLEDGMENTS our manuscript significantly. We thank Dr. Simon Jungblut,

Christina Hörterer, Stacy Ballyram, Arley Muth, and Francine
We are grateful for all the valuable comments from the Beaujot whose insightful comments and suggestions have helped
academic editor and reviewer, who we believe have strengthened to improve this review.
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published: 21 April 2021

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definitions of this type of culture (Davies et al., 2019). Sometimes CONCLUSION

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ACKNOWLEDGMENTS our manuscript significantly. We thank Dr. Simon Jungblut,

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