Sustainable intensification of aquaculture through nutrient recycling and circular economies: More fish, less waste, Blue Growth 

Camilla Campanati1*, David Willer1, Jasmin Schubert2, David C. Aldridge1

1 Department of Zoology, University of Cambridge, The David Attenborough Building, Pembroke Street, Cambridge CB2 3QZ, UK



22

[footnoteRef:2] RethinkResource, Hohlstrasse 400, Zürich, Switzerland [2: 2 Current affiliation: BIO.NRW, Merowingerpl. 1, 40225 Düsseldorf, Germany ] 


*Corresponding author:
Department of Zoology, The University of Cambridge, UK
+44(0)7563417222, cc2011@cam.ac.uk

Co-authors e-mail:
David Willer: dw460@cam.ac.uk
Jasmin Schubert: jasminschubert@msn.com
David C. Aldridge: da113@cam.ac.uk



Running title: More fish, less waste, Blue Growth








Abstract 

Aquaculture has grown rapidly to play a crucial economic and social role and meet the increasing global demand for seafood. As aquaculture intensifies, there is increasing pressure to find more sustainable practices that save resources and reduce waste. Major wastes and by-products from aquaculture were quantified across a full range of farming types. Key opportunities for wastewater treatment and by-product recovery include nutrient recycling through a combination of biofilters, bioaccumulation and multitrophic systems. To support a sustainable intensification of aquaculture, improvements in by-product harvesting, accumulation and processing methods require further investigation. Likewise, energy generated from by-products can potentially support intensified production through land-based recirculating aquaculture systems (RAS). Future challenges faced by the reuse of side streams include control of food safety and gaining consumer acceptance. Combined with increases in resource use efficiency across the aquaculture sector, from feeding methodologies to product storage, nutrient recycling can enable aquaculture to contribute sustainably towards the nutritional requirements of billions of people over the next century. 

Key words: By-products; circular economy; nutrient recycling; sustainable aquaculture; wastewater 










1. Introduction

Aquaculture is predicted to play a critical role in supplying nutritious food to a growing human population (Miller et al. 2008; Troell et al. 2014; FAO 2018), which is expected to exceed 9 billion by 2050 (UN 2015). To meet increasing global demand for seafood and omega-3 fatty acids (particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA); Tur et al. 2012; Salem and Eggersdorfer 2015; Tocher et al. 2019), aquaculture, which today contributes to 47% of global seafood production (171 MT in 2016; FAO 2018), is expected to intensify practices (Klinger and Naylor 2012; Diana et al. 2013; Blanchard et al. 2017; Stevens et al. 2018). This raises significant concerns regarding limiting resources (e.g. water, space, feed) and the environmental impacts (e.g. wastewater, solid waste) that higher stocking densities and feed supplementation can cause (Arvanitoyannis and Kassaveti 2008; Klinger and Naylor 2012; Bao et al. 2018; Bohnes et al. 2018; Boyd et al. 2020). For example, mismanagement in the release of nutrients (e.g. N Nitrogen, P Phosphorous) and solid organic matter into the environment can drive algal blooms (Herath and Satoh 2015), eutrophication (Alonso-Rodrı́guez and Páez-Osuna 2003; Camargo and Alonso 2006), hypoxic events and water acidification (Sarà 2007; Cai et al. 2011). Organic material discharge can also increase concentrations of pathogenic bacteria and viruses in water systems (McAllister and Bebak 1997; Vezzulli et al. 2002, 2008). Furthermore, extensive antibiotic usage in farm systems can accelerate the spread of disease resistant pathogens in receiving waters (Boxall 2004; Sapkota et al. 2008; Zou et al. 2011; Hossain et al. 2012; Muziasari et al. 2016), with detrimental impacts on aquaculture production (Karunasagar 2015).
In order to sustainably intensify aquaculture and maintain a continuous seafood supply, without causing catastrophic ecosystem damage, there is a need to implement a more resource-efficient approach (Miller et al. 2008; Nichols et al. 2010; Tlusty and Thorsen 2017; Stevens et al. 2018) and minimise aquaculture waste (Hall et al. 2011; Castine, McKinnon, et al.  2013; Castine, Paul, et al. 2013; Newton et al. 2014; Dauda et al. 2019; Turchini et al. 2019). Consequently, there is growing global awareness and interest in the valorisation of available resources, specifically recycling of nutrients and by-products, to support a circular economy within aquaculture (Boyd et al. 2007; Arvanitoyannis and Kassaveti 2008; Alonso et al. 2010; Lopes et al. 2015; Stevens et al. 2018; de la Caba et al. 2019). In 2012, the European Commission promoted “Blue Growth”, a green economy applied to maritime and coastal sectors (EC 2012). There is potential for by-products and wastewater effluents to be diverted back into aquaculture systems and account for high percentages of aquaculture production (Newton et al. 2014; Mehta et al. 2015; FAO 2018; Smárason et al. 2019).
This paper reviews the major wastewater constituents from effluents of different aquaculture systems. The aim of this paper is to highlight potential areas for nutrient and by-product recycling, key challenges in the reuse of side streams and potential solutions to overcome these challenges, in order to provide sustainable aquaculture options for the future. For the purpose of this review, “by-products” and “side streams” are considered “co-products”, as parts of the farmed animals or discharged effluents, not directly used for human consumption, which have a nutritional value, and that could be a useful resource to reuse (Stevens et al. 2018). “Waste” is, instead, considered as a non-reusable material and thus to be disposed of (i.e. composted, burned or destroyed; Rustad et al. 2011). 

2. Major effluents and by-products in aquaculture

2.1. Seafood processing by-products
Seafood by-products are a large and highly valuable resource, already being recycled for other uses, and there is potential to increase this further to benefit the aquaculture industry. By-products include damaged fish, body parts not usually utilised for direct human consumption, and trimmings from fish processing and canning (Stevens et al. 2018). Today 11.5 % of total global seafood produced (19.7 MT) is not used for direct human consumption (FAO 2018). Over 4.7 MT of by-products are generated from fish processing (Ytrestøyl et al. 2015; FAO 2018; Stevens et al. 2018), and a further 0.5 MT from crustaceans and molluscs as carapaces, exoskeletons and shells (FAO 2018). At present, 30% of fish meal and fish oil production (up to 54% in Europe; Jackson and Newton 2016; FAO 2018) is derived from by-products (Rustad et al. 2011; Ghaly et al. 2013; Stevens et al. 2018). With the intensification of aquaculture, there is the potential and expectation that recycling of seafood by-products for feed and other uses will increase (Naylor et al. 2009; Klinger and Naylor 2012; Troell et al. 2014). 
There is a need to treat wastewaters and solids generated during seafood processing and fish meal and fish oil production and this also represents a recycling opportunity. In fact, the mechanical pressing of seafood during fish oil preparation produces effluents with a high organic content (e.g. Chemical Oxygen Demand, COD 80-120 g l-1; Afonso and Bórquez 2002; Arvanitoyannis and Kassaveti 2008; Gehring et al. 2011; Ghaly et al. 2013). Suspended solids in wastewaters from a fish processing industry in Portugal were reported to be in the range of 320-3150 mg l-1, with 90-2350 mg of dissolved organic carbon (DOC) l-1, 10-50 mg l-1 of total phosphorus (TP), 20-470 mg l-1 total nitrogen (TN), and 160-2800 mg l-1 of oil and grease (Cristóvão et al. 2014). The volumes of wastewater produced are also large; studies suggest 15 and 17 L of effluents are produced per kg of fish from skinning and canning respectively (Kim and Park 2007; Arvanitoyannis and Kassaveti 2008). Seafood-by products are a highly valuable resource and in such great demand, for example for producing omega-3 rich aquafeeds, that other sources such as microalgae and polychaetes are already needed to bridge the market demand-supply gap (Brown et al. 2011; Adarme-Vega et al. 2012; Chauton et al. 2015; Aasen et al. 2016; Tocher et al. 2019). There is little doubt that increased re-use of seafood by-products would have significant economic, environmental, and resource use efficiency benefits (Naylor et al. 2009; Alonso et al. 2010; Klinger and Naylor 2012; Olsen et al. 2014; Troell et al. 2014; Lopes et al. 2015; Stevens et al. 2018).

2.2. Dissolved and solid (i.e. suspended and settleable) effluent materials 
Aquaculture effluents are composed mainly of dissolved and settleable nutrients from unconsumed food and faeces of farmed species (Crab et al. 2007; van Rijn 2013). The amount and type of discarded material produced from aquaculture depends on factors including dietary supplementation, the metabolism and feeding habits of the farmed species, and consequently feed conversion efficiencies (i.e. FCR; Cho and Bureau 2001; Bureau and Hau 2010; Amirkolaie 2011). 
International standards for aquaculture wastewater loads do not exist but permits, concerning effluents’ nutrients and solids concentration and daily water load, are issued based on the specific recipient water bodies’ characteristics (Boyd 2003; Turcios and Papenbrock 2014). On broader scales aquaculture facilities are supposed to follow guidelines for best practices, such as those produced by the Environmental Protection Agency (EPA), Food and Agricultural Organization (FAO), Global Aquaculture Alliance (GAA) or Best Aquaculture Practice (BAP), in the management of effluent production (Boyd 2003; Tacon et al. 2009; van Rijn 2013; Dauda et al. 2019; Fig. 1). 
Recirculating aquaculture systems (RAS) and raceway systems can produce wastewaters with high concentrations of solids and nutrients (Fig. 1; Table 1) which can be useful resources if treated effectively (Fig. 2). To evaluate reuse options realistically discharge rates must be considered. For example, RAS systems, with low water exchange, produce effluents at 1000 times lower rates compared to raceways, and more concentrated compared to ponds and cages (Table 1; Fig. 1). The paucity of cage effluents studies urges a more careful and standardised method for monitoring compound concentration, to allow better comparison across systems (Table 1). In ponds and cages efficient management of solids can make use of significant quantities of reusable biomass (kg N, P. solids) (Fig. 1) and maximise production through in-situ nutrient upcycling with polycultures and multi-trophic systems (Fig. 2; Boyd et al. 2020). 

2.2.1. Wastewater solids
Solid waste is a key component of aquaculture wastewaters, generally holding 10-30 % of the total nitrogen (TN) and 30-80 % of the total phosphorus (TP) discarded in faeces or uneaten food (Cripps and Bergheim 2000; Dauda et al. 2019), and is usually retained from effluents in a primary treatment (Castine, McKinnon, et al. 2013; Bao et al. 2018; Fig. 2). Feed digestibility determines faeces consistency, quantity and form (suspended or settled) of solids in wastewaters (Cho and Bureau 2001; Bureau and Hua 2010; Amirkolaie 2011; Bao et al. 2018). Settleable solids (>100 m) sink to the bottom of the water column and are more-easily removed compared to suspended solids (30-100 m) (Armikolaie 2011). Dietary stabilizers and binders such as guar gum or alginate are often added to feeds to increase faeces particle size (Storebakken 1985; Brinker 2007; Turcios and Papenbrock 2014) and thus facilitate their sinking and removal processes (Brinker et al. 2005; Amirkolaie 2011). 
Due to difficulties in their removal process, suspended solids (i.e. TSS) are considered major pollutants within aquaculture wastewaters (Chen et al. 1997; Bao et al. 2018). Suspended solids, which can derive from different sources (e.g. feed, faeces, detached biofilm, sediments and system enclosures’ substrates; Davidson et al. 2009), are mostly organic particles and can drive bacterial proliferation, which can clog biofilters in the system (Andersson et al. 1994; Eding et al. 2006; Singh et al. 2018). Elevated levels of TSS also increase turbidity and reduce light penetration, limiting in-situ autotrophic remediation (e.g. Bulmer et al. 2018) and the visual inspection of farmed species health (Espinal and Matulić 2019). Elevated TSS can negatively impact farmed species (Kjelland et al. 2015; Bao et al. 2018), by impairing gill functioning (Chapman et al. 1987; Bilotta and Brazier 2008) and facilitating pathogen infections in aquaculture stock (Gonçalves and Gagnon 2011; Pedersen et al. 2017). Several species appear to tolerate TSS exposure up to 200-300 mg l-1 for 20-40 days (Gaona et al. 2015; Poli et al. 2015), whilst others tolerate TSS levels of 30 mg l-1 for 2 months (Eding et al. 2006; Becke et al. 2017). Regardless, careful monitoring of TSS levels is required to reduce the risk of bacterial proliferation from fine solids availability (Boyd and Gautier 2000; Barraza-Guardado et al. 2013; Espinal and Matulić 2019; Fig. 1). 
Other solid pollutants found in aquaculture effluents, including pharmaceuticals such as hormones, steroids, parasiticides and antibiotics are problematic. Mismanaged antibiotic use can give rise to antimicrobial resistance in pathogenic bacteria in receiving waters (Boxall 2004; Sapkota et al. 2008; Zou et al. 2011; Hossain et al. 2012; Muziasari et al. 2016; Watts et al. 2017) and can threaten the persistence of biofilms in bioreactors (Gonzalez-Martinez et al. 2018).
Sediments in ponds or beneath cages and pens act as major sinks for excreted N (~30% of output), P (~80%), organic matter (~60%) and solids (~90%; Briggs and Funge-Smith 1994; Primavera 2006; Martinez-Córdova and Ocaña 2007), and can contribute to a thick harvestable sludge which can negatively affect water quality and biodiversity (Primavera 2006; Martinez-Garcia et al. 2013). Effective sludge thickening methods can reduce effluent volume for practical storage, off-site transport and composting, and further concentrate nutrients for other applications (Fig. 2; Chen et al. 1997; Mirzoyan et al. 2010; Sharrer et al. 2010; Castine, Paul, et al. 2013).

2.2.2 Wastewater dissolved nutrients (nitrogen and phosphorus)
Nitrogen (N) is one of the most significant components of aquaculture wastewaters. Differently from freshwater ecosystems, which are usually P-limited, marine ecosystems are generally N-limited. Therefore, N has a primary role in the risk of producing eutrophic systems (Camargo and Alonso 2006). Most of the N released from aquaculture (60-90%) is in dissolved form, predominantly as ammonia (TAN: NH3 + NH4+; van Rijn 2013). Ammonia can be found in water in non-ionized form (NH3), which is toxic to many species at concentrations higher than 1.5 mg l-1 (Crab et al. 2007), with an average acute toxicity value of 2.79 mg NH3 l-1 for freshwater species (Randall and Tsui 2002). Depending on pH, temperature and salinity, ammonia can be hydrated and charged into its ionized form (NH4+), which is non-toxic to most species (Körner et al. 2001; Camargo and Alonso 2006). Released ammonia can also be further broken down into nitrite (NO2-) and nitrate (NO3-) by biological activities occurring in the water column (Piedrahita 2003; Dauda et al. 2019). NO2- interferes with oxygen transport and causes respiratory distress in farmed species (Kioussis et al. 2000), making it highly toxic even at very low concentrations. Aquaculture species can tolerate slightly higher levels of NO3- , likely due to lower permeability through the gills relative to NO2- (Fig. 1; Zweig et al. 1999; Verdegem 2013; Dauda et al. 2019; Espinal and Matulić 2019). Reducing the quantity of N excreted by target species is achieved in some systems through “protein-sparing” (Ackefors and Enell 1994; Watanabe 2002; Li et al. 2012). This involves replacing protein with a higher level of lipids in fish feeds, or more carbohydrates for crustacean feeds (Cho and Bureau 2001; Amirkolaie 2011; Wang et al. 2014). Nutrient seepage from feeds can be further reduced with specific feeding formulations such as in the form of microencapsulated diets (e.g. Willer and Aldridge 2017, 2019a).
Phosphorous (P) is a second major component of aquaculture wastewaters. Around 25-85% of P lost from feed in aquaculture is in solid form within faeces (Seawright et al. 1998; Schneider et al. 2005; van Rijn 2013). The high levels of P in fish oil and fish meal (Fry et al. 2016; Gasco et al. 2018; Turchini et al. 2019), are largely excreted by farmed species (Amirkolaie 2011). Vegetable-based meals and oils contain lower levels of P but are inadequate alternatives for 100 % fish meal or fish oil substitution, particularly for carnivore species (Hardy 2010; Amirkolaie 2011; Boissy et al. 2011; Davidson et al. 2016; Fry et al. 2016; Sánchez-Muros et al. 2018). Digestibility and bioavailability of P from vegetable-based feeds can be enhanced through additional phytase enzymes, feed pre-treatments (e.g. Dephytinization; Storebakken et al. 1998; Vielma et al. 2002; von Danwitz et al. 2016; Boyd et al. 2020) and organic acid supplementation in diets (Herath and Satoh 2015). Additionally, although still not widely implemented, breeding programmes exist to select carnivorous fish over generations for better growth and feeding efficiency on plant-based diets (Quinton et al. 2007; Overturf et al. 2013). Genetically modified (GM) farmed fish (e.g. GM tilapia with growth hormone gene segment from other fish or mammals) are also shown to have greater nutrient assimilation and nutrient loss in effluents can be 50-60% lower (Lu et al. 2009). Further optimisations in feed formulations and inclusion rates in the diet are suggested to reduce P losses further (Cho and Bureau 2001; Gasco et al. 2018; Turchini et al. 2019).

3. Key recycling opportunities in aquaculture

The application of both established and newly emerging recycling methods to aquaculture has great potential to make the industry more sustainable and to greatly increase production output. Retrieved solids, dissolved nutrients and seafood by-products can all be reused to benefit aquaculture itself, and also other industries including agriculture and nutraceuticals (Fig. 2, Fig. 3). As just one example, recycling of omega-3 fatty acids from seafood by-products and the use of bioremediating microalgae and filter-feeders (e.g. polychaetes, bivalves) can enable a large increase in the supply of omega-3 oils, with significant economic and human health benefits (Fig. 2, Fig. 3). Energy generated from sludge digestion, clean water retrieved from bioremediation, and upcycled nutrients through integrated aquaculture systems, could each help sustain intensive arable farming. The following recycling methodologies have the potential to play primary roles in establishing sustainable circular economies in aquaculture.

3.1. By-product recovery
Seafood by-products can be recovered for use in multiple high value industries including aquaculture, agriculture, the food and pharmaceutical industries (Arvanitoyannis and Kassaveti 2008; Rustad et al. 2011; Kandra et al. 2012; Leal et al. 2016; Morris et al. 2018; Stevens et al. 2018). The most common reutilization of seafood by-products remains integrating them back into food or feed ingredients for aquaculture (Olsen et al. 2014; Aasen et al. 2016; FAO 2018; Stevens et al. 2018). As valuable sources of high-quality proteins (20-70 %) and energy (19 % lipids), seafood by-products are widely used as animal and pet feed (Hammoumi et al. 1998; Esteban et al. 2007; Arvanitoyannis and Kassaveti 2008; Goddard et al. 2008; Stevens et al. 2018; Fig. 1, Fig. 2). There is potential to make more effective use of wastewater derived from trimmings and silage processing into fish meal and fish oil (Afonso and Bórquez 2002; Arvanitoyannis and Kassaveti 2008; Gehring et al. 2011; Ghaly et al. 2013). Wastewater from seafood by-products processing (e.g. 1300 m3 day-1 from 170 t tuna day-1) can be reused after solid filtration as a medium for algal growth (Queiroz et al. 2013; Fig. 2). Over 360 g day-1 of microalgal biomass (50 g lipid day-1) can be obtained from 1 m3 of fish processing wastewater (88 % organic matter, 6.5 % TN, 0.6 % TP) (Queiroz et al. 2013; Table 1). 
Shells discarded by bivalve aquaculture can be used for treatment of soil acidity, livestock calcium supplements, construction materials, natural substrates, alkalinity buffers for wild reefs and restoration programs (Powell and Klinck 2007; Morris et al. 2018). Oyster shells have also been considered as filter substrates to remove P (PO43-) from wastewaters (Roy 2017) and shell extracts used to enrich microalgae in biodiesel production (Choi et al. 2014). 
Extracted and isolated bioactive compounds and natural pigments such as carotenoids, collagen and protein hydrolysates from seafood by-products (Arvanitoyannis and Kassaveti 2008; Kim and Wijesekara 2010; Olsen et al. 2014; Rustad et al. 2011; Newton et al. 2014), are of interest for functional food, nutraceuticals and pharmaceutical use due to their antihypertensive, antioxidative, anticoagulant and antimicrobial properties (Ferraro et al. 2010; Kim and Wijesekara 2010). Currently these high-value components are retrieved in too small amounts for a cost-effective resource recycling process, but more effective extraction methods could change this (Gildberg and Stenberg 2001; Gehring et al. 2011; Kandra et al. 2012; Olsen et al. 2014).

3.2. Wastewater solids recycling
Land application is the most common recycling use of solids deriving from hatchery settling ponds, basins and RAS effluents (Bergheim et al. 1998; Chen et al. 2002; Amirkolaie 2011; Castine, McKinnon, et al. 2013; van Rijn 2013). Nutrient-rich aquaculture sludges are valuable bioresources for land plant fertilization, improving or maintaining soil structure (Cripps and Bergheim 2000; Piedrahita 2003; Panwar et al. 2012), while decreasing the environmental impacts caused by mining and artificial fertilizers (WHO 2006; Roy 2017). Generally, aquaculture sludge contains lower toxic and health-concerning components compared to sludges retrieved from industry and domestic treatments (van Rijn 2013). Composting of aquaculture wastewater (e.g. at 40C for few days), combined with sludge dewatering and C/N ratio alteration when needed, can reduce biosolid pathogens (Adler and Sikora 2004; van Rijn 2013). Sediments retrieved from ponds after each aquaculture production cycle (Briggs and Funge-Smith 1994; Martinez-Córdova and Ocaña 2007) could be dried and reused for fertilizing ponds (Boyd et al. 1994; Boyd, 1995; Das and Jana 2003), mangrove reforestation (Primavera 1998; Sidik et al. 2019), fertilization of soil and/or fodder grass (Muendo et al. 2014; Haque et al. 2016).
Solids retrieved from aquaculture could also be used as feedstock for vermicomposting (e.g. Eisenia fetida earthworm; Marsh et al. 2005). This approach has already been used for treating high-moisture-content organic material discarded from agricultural, industrial and municipal sources, with production rates of 0.30 kg vermicast kg-1 of worm day-1 (Ndegwa and Thompson 2001; Yadav et al. 2010; Roy 2017), which can in turn, be used as feeds. Marine polychaete worms could also be included in integrated recirculation systems and be fed on aquaculture effluents (Honda and Kikuchi 2002; García-Alonso et al. 2008; Bischoff et al. 2009; Brown et al. 2011; Gómez et al. 2019). Worms could be easily included in experimental food webs for wastewater bioremediation and fatty acid enrichment of farmed species (Fig. 2; Bischoff et al. 2009; Brown et al. 2011; Granada et al. 2016; Stabili et al. 2019). For example, more than 50% of solids derived from pond wastewaters can be removed using sand filters filled with polychaetes, which can produce 3-4 g l-1 yieldable biomass and 20 mg l-1omega-3 (Palmer 2010; Brown et al. 2011; Table 1). 
Polychaete worms have been shown to supply suitable nutritional balance for shrimp (Lytle et al. 1990; FIdalgo e Costa et al. 2000; Wouters et al. 2001; Hoa et al. 2009; Brown et al. 2011), and fish (Stabili et al. 2019) diets, proving their sustainable adequacy as omega-3 sources (FIdalgo e Costa et al. 2000; Klinger and Naylor 2012). 
Aquaculture sludge treated in anaerobic digesters can produce biogases useful for energy production. This includes methane (17-30% of organic carbon input; Green et al. 1995; Zhang et al. 2013) and carbon dioxide (Lanari and Franci 1998; Mirzoyan et al. 2010; Fig. 2). Combination of biological (anaerobic digestion) and thermochemical (gasification; Panwar et al. 2012) conversion of biomass have shown to be advantageous for energy recovery from municipal sludge (e.g. 675-1240 KW h-1; Gorgec et al. 2016). Partially due to the lower amount of solids retrieved, however, the concentration of biogases from anaerobic digestion of aquaculture sludge is currently lower than those produced from industrial or domestic sludge (Mirzoyan et al. 2008). For example, methane production was reported in the range of 0.02 -0.25 l g of COD added-1 (Mirzoyan et al. 2010). Nevertheless, several studies suggest that 5% of RAS energy demand could be met by biogas production from anaerobic digestion of sludge (Gebauer and Eikebrokk 2006; Tal et al. 2009). Further investment in anaerobic digestion and thermochemical systems (Rawat et al. 2011; Islam et al. 2017) could significantly increase this value and help build a circular economy in aquaculture regarding energy supply.

3.3. Wastewater nutrients recycling (Microalgal bioremediation, omega-3, biofuel)

Aquaculture wastewaters are nutrient enriched, with elevated concentrations of N, P, as well as trace elements K, Ca, Mg, Fe, Cu, and Mn and could be incorporated into bacterial and algal biomass for high value reuse (Hussenot 2003; Mehta et al. 2015; Milhazes-Cunha and Otero 2017; Han et al. 2019). Many studies have demonstrated that liquid side streams are valuable reusable sources of nutrients for cost-effective cultivation of autotrophic, heterotrophic and mixotrophic cyanobacteria, microalgae and seaweed (Castine, McKinnon, et al. 2013; Pires et al. 2013; Sahu et al. 2013; Khademi et al. 2014; Han et al. 2019; Lu et al. 2019; Cabanelas et al. 2013; Pires et al. 2013; Sahu et al. 2013; Gao et al. 2016; Khatoon et al. 2016; Ansari et al. 2017; Tossavainen et al. 2019). 
Nutrient removal and biomass production levels can be favourably high (Table 1). For example, 425 g N- NH4+ day-1 and 125 g P-PO43 day-1 can be removed in large-scale (104 l) wastewater remediation with photoautotrophic Scenedesmus obliquus (Ruiz-Marin et al. 2010). The alga Nannochloris maculata is able to produce more lipids in shrimp pond wastewaters than in traditional Conway medium (Khatoon et al. 2016). Heterotrophic Chlorella vulgaris and Tetraselmis chuii can grow on concentrated fish manure (Lowrey and Yildiz, 2014) and Aphanothece microscopica on fish processing wastewaters producing 0.025 g PUFAs (i.e. polyunsaturated fatty acids) l-1 day-1 (Queiroz et al. 2013). Wastewater phytoremediation with species such as Chlorella sp. can achieve 80 % NO3- removal with biomass yield of 160 mg l-1 day-1 (Ansari et al. 2017). Mixed cultivation of Euglena gracilis and Selenastrum sp. in pikeperch wastewaters amended with sludge addition, can achieve 1.5 g l-1 in algal biomass, of which 85 mg l-1 were lipids and 7.3 mg l-1 omega-3 fatty acids (EPA+DHA; Tossavainen et al. 2019).
Raceway ponds have particular potential as a means for nutrient removal and biomass production. Raceways ponds can produce algal biomass at 10-25 g m-2 day-1 from wastewater and have greater scalability and lower costs compared to tubular and flat panel photobioreactors (2.95 vs 3.85 USD l-1 algal oil extracted) (Oncel 2013; Chauton et al. 2015; Gutiérrez et al. 2015). In intensive land-based aquaculture systems, filamentous green tide algae have high bioremediation and upcycling potential, given their ability to retain 3.3 kg N ha-1 day-1 and yield 1-1.5 kg of fresh weight m-2 (de Paula Silva et al. 2008). “Microalgae-assisted aquacultures”, the smart combination of bacteria and algae in symbiotic co-culture, could also allow cost-effective bioremediation in ponds or enclosed farming systems. This would enable oxygenation of water, CO2 recycling, and further synthesis of value-added components such as lipids and protein with a 20% reduction in energy use compared to conventional methods (d’Orbcastel et al. 2009; Su et al. 2012; Hernández et al. 2013; Lananan et al. 2014; Van Den Hende et al. 2014; Bohutskyi et al. 2018; Han et al. 2019). 
Phycoremediation can also involve the use of immobilized cultures, for example in alginate or carrageenan, to facilitate the harvest of suspended microalgal cells (Lananan et al. 2014). Revolving algal biofilm (RAB) systems can produce biomass more efficiently than raceway pond systems (15-30 g m-2 day-1; Gutiérrez et al. 2015) although initial investment costs are higher (Han et al. 2019). Newly developed membrane photobioreactors (MPBR) allow cultivation of microalgae at high concentrations which can remove 100 % of NH3 day-1 in dilute wastewater (<0.002 mg l-1) and produce up to 43 mg l-1 day-1 of biomass (Gao et al. 2016). Electro-biochemical reactors (EBR) with microbial fuel or electrolysis cells can also produce energy or hydrogen, while removing 74 % of NO3- and 97 % of TAN (Mook et al. 2012; Oncel 2013).
As algae are at the base of the food web they also offer huge opportunities for nutrient upcycling in polycultures and multi-trophic aquaculture systems (Jones et al. 2002; Guedes and Malcata 2012) and to partly substitute commercial feeds (omega-3 oil; Erler et al. 2010; de Paula Silva et al. 2012; Adarme-Vega et al. 2014; Roy and Pal 2015; Bossier and Ekasari 2017; Tossavainen et al. 2019; Fig. 3). Omega-3 fatty acids could be accumulated in microalgae up to 10-60 % of their dry weight (Guedes et al. 2011), although this ability is species-specific (Huerlimann et al. 2010). Genetic and metabolic engineering are being developed to increase the biosynthesis of omega-3 and silence genes for competing pathways (Gong et al. 2011; Radakovits et al. 2012; Hamilton et al. 2014). Concentrating omega-3 into a smaller volume of culture would allow a more feasible and cost-effective production intensification (Hamilton et al. 2014; Willer and Aldridge 2017, 2019b). 
Besides its use for aquafeeds and CO2 sequestration (Adarme-Vega et al. 2012; Armenta and Valentine 2013; Boelen et al. 2013; Roy and Pal 2015; Zhou et al. 2017) harvested microalgal biomass can have several other applications, such as being used as natural fertilizer (Panwar et al. 2012; Castine, Paul, et al. 2013; Milhazes-Cunha and Otero 2017; Roy 2017). With subsequent further processing, microalgae can contribute to added value components for nutraceuticals and pharmaceuticals markets (Spolaore et al. 2006; Wells et al. 2017; Bohutskyi et al. 2018) and biofuel in biorefinery-based production systems (Fig. 2; Rawat et al. 2011; Mata et al. 2013). Metabolic engineering of microalgal pathways can optimize lipid production from these microorganisms and potentially maximise by-product valorisation (Mühlroth et al. 2013; Oncel 2013; Islam et al. 2017). The sustainable production of microalgal biofuel at large industrial scale is, however, still challenged by finding more economically viable methods of harvesting and lipid extraction (Greenwell et al. 2010; Mata et al. 2013). Energy requirements for producing microalgal biofuels are today still higher than the energy retrievable from the biofuel itself (Carneiro et al. 2017). Emerging techniques such as the hydrothermal liquefaction of wet biomass to crude oil or the supercritical fluid extraction and transesterification are showing significant promise with further optimisation (Oncel et al. 2013; Islam et al. 2017).

3.4. Upcycling nutrient systems (bioflocculation, IMTAs)

Bioflocculation technology (BFT) is an emerging and highly promising, cost-effective, environmentally friendly bioremediation option for land-based aquaculture systems (Chávez-Crooker and Obreque-Contreras 2010; Crab et al. 2012; Castine, Paul, et al. 2013; Bossier and Ekasari 2017). When wastewaters have a C/N ratio >10 (Mook et al. 2012), BFT can reduce ammonium concentration ~20% faster than nitrification (Hargreaves 2006; Rahman et al. 2008; Avnimelech 2009; Crab et al. 2012) and ~30% more economically than conventional biofilters (Van Den Hende et al. 2014; Ansari et al. 2017; Chatla et al. 2020). Bioflocculation has also great potential to be applied as a low-cost technology to upgrade nutrients and biomass through the food-web in integrated multi-trophic aquaculture (i.e. IMTA; Luo et al. 2017; Han et al. 2019; Table 1; Fig. 2). Containing essential fatty acids, free amino acids, carotenoids, chlorophylls, vitamins and trace minerals (Nunes et al. 2006; Ju et al. 2008; Crab et al. 2012; Dauda et al. 2019), biofloc is of appropriate nutritional value for the cultivation of zooplankton, shrimp, red Nile tilapia and mussels (Burford et al. 2004; Ekasari et al. 2014; Glencross et al. 2014; Luo et al. 2017) and could reduce feed costs (Browdy et al. 2001; Burford et al. 2004; Wasielesky et al. 2006). In intensive shrimp pond cultures biofloc use has led to a net productivity 8-43 % greater than conventional systems (Browdy et al. 2001; Kuhn et al. 2009, 2010; Emerenciano et al. 2012; Ekasari et al. 2014). Furthermore, it has also been demonstrated that inoculation of bioflocs with specific microorganisms could act as a probiotic against pathogen loads in shrimp cultures (Crab et al. 2012; Emerenciano et al. 2012; Anand et al. 2014; Ekasari et al. 2014) and fish particularly at their early-life stages (Ekasari et al. 2015; Poli et al. 2015; Bossier and Ekasari 2017). Microalgal-biofloc sludges can be obtained through solid-liquid separation or air floatation (Gutiérrez et al. 2015) and further upcycled through vermicomposting using polychaetes (Gómez et al. 2019; Fig. 2). Integrated polyculture systems have strong potential in valorising added-value by-products from farm effluents through nutrient upcycling and increasing of harvestable biomass (Shpigel et al. 1993; Hussenot 2003; Chopin et al. 2001, 2012; Fig. 2, Fig. 3). Several studies have shown positive effects of cultivating microalgae, oysters, mussels or seaweed in bioremediating polycultures, in wastewater effluents from fish and shrimp cultures (Jones et al. 2002; Martinez-Cordova and Martinez-Porchas 2006; Martinez-Porchas and Martinez-Cordova 2012; Lananan et al. 2014; Sirakov et al. 2015). For example, in a polyculture with shrimps, oysters and clams, earthen ponds in Mexico could produce a yield of 2.5-2.95 t of shrimps ha-1, 0.8-1.12 t of oysters ha-1, and 0.7 -0.9 t of clams ha-1 (Martinez-Cordova and Martinez-Porchas 2006). 
Suspended particulates and phytoplankton can be cleared from the water by bivalves and other filter feeders in raceway side-stream settling basins to upcycle nutrients into yieldable biomass (Hussenot et al. 1998; Lefebvre et al. 2000; Shpigel 2005; Martinez-Porchas and Martinez-Cordova 2012; Carboni et al. 2016; Fig. 1, Fig. 2). For example, 10,000 oysters can remove and hold 13.6 kg N and 1.4 kg P (Shpigel 2005). Omega-3 DHA and EPA levels retrievable from bivalve tissues (1.76 and 2.12 mg g-1; Tacon and Metian 2013) are comparable to fatty fish (2.61 and 2.27 mg g-1; Tacon and Metian 2013; Willer and Aldridge 2019a). Water bioremediated by the clam Chione fluctifraga and benthic alga Navicula sp., were shown to improve production (+556 kg ha-1) and survival (+14%) of shrimps (Litopenaeus vannamei) (Martínez-Córdova et al. 2011). Where large surface areas are available, seaweed biofiltration should be considered for upcycling nutrients (Table 1; Zhou et al. 2006; Mata et al. 2010; Buschmann et al. 2017). In integrated cultures with bivalves, complimentary biofiltration of seaweed can improve bioremediation efficiency (Chopin et al. 2001; Neori et al. 2004) and alleviate pressure from coastal eutrophication risk (e.g. Jiang et al. 2012). In multitrophic systems,  bivalve biodeposits can additionally be used as food for deposit feeders beneath cages, such as holothuroids, polychaetes and echinoids (Irisarri, 2014; Cubillo et al. 2016). These could bioturbate and oxygenate the sediments, and regenerate dissolved inorganic nitrogen (i.e. DIN), making it available for other extractive species (e.g. seaweed or microalgae; Chopin et al. 2001, 2012; Troell et al. 2003; Neori et al. 2004), while potentially yielding 5-15 kg m-2 per production cycle in IMTAs (Cubillo et al. 2016). Deposit feeders, together with ‘extractive’ species, such as bivalves and seaweed, could be directly harvested for human consumption or used to feed other cultured species (Lin et al. 1993; Alleway et al. 2019; Gentry et al. 2019; Olivier et al. 2020). 
Integrated multi-trophic aquaculture (IMTA) may represent the most feasible bioremediation strategy for discharges from sea cages, ponds and extensive systems, allowing higher yieldable biomass and value-added co-products through economic diversification (Neori et al. 2004; Troell et al. 2009; Chopin et al. 2012; Granada et al. 2016). Examples of these systems include the use of periphyton (Azim et al. 2005; Crab et al. 2007), constructed wetlands (e.g. Lin et al. 2002; Turcios and Papenbrock 2014), aquaponics (Tyson et al. 2011; Goddek et al. 2015; Wong et al. 2016; Lu et al. 2019) and integrated marine systems (Chopin et al. 2012). In inland production systems, aquaponics can be a highly efficient mechanism for culturing both animals and plants with low water and energy requirements (Turcios and Papenbrock 2014; Love et al. 2015). Wastewater N and P removal by plants can be optimised by knowing the excretion and uptake rates of co-cultured species (Tyson et al. 2011; Boxman et al. 2015; Waller et al. 2015). 
Integrated multi-trophic aquaculture systems could be implemented within freshwater aquaculture, functioning at a smaller scale than extensive mariculture systems (Chopin et al. 2012; Turcios and Papenbrock 2014; Goddek et al. 2015; Love et al. 2015; Wongkiew et al. 2017). In wetlands, saltwater plants can be used to remove and accumulate nutrients from aquaculture wastewaters (Table 1; Bunting and Shpigel 2009; Turcios and Papenbrock 2014; Gunning et al. 2016), with low energy requirements, investment and maintenance costs, though requiring large space (Lin et al. 2005). Genes for “x desaturases” enzymes, key for omega-3 production in bacteria and lower eukaryotes, have been found in many invertebrates, highlighting potential endogenous capabilities of de-novo synthesis of omega-3 PUFAs in various aquatic animal groups (e.g. Cnidaria, Rotifera, Mollusca, Anellida and Arthropoda; Kabeya et al. 2018). Further research should aim on improving de-novo synthesis of omega-3 PUFAs in invertebrates and upgrade them through the food webs.

4. Key hurdles and future challenges
The reutilization of wastewater and aquaculture by-products, coupled with improved feeding compositions and formulations (Casillas-Hernández et al. 2007; Willer and Aldridge 2017, 2019a, b), offer great potential to improve sustainability in the rapidly growing aquaculture industry (Turchini et al. 2019; Boyd et al. 2020). Some limitations, however, exist, and further research should address these challenges in order for the potential of sustainable aquaculture to be realised.
Feed production
Life Cycle Assessments (LCA) are useful tools for providing production chain transparency and accountability (Cao et al. 2013; Little et al. 2018) and are playing an increasingly important role in assessing the environmental impacts of aquaculture (Iribarren et al. 2012; Little et al. 2018). The production of raw material (especially fish meal, soybeans and wheat grains) dominates the impacts categories, contributing from 18 % to greenhouse gas emissions (i.e. global warming impact), to 88 % of eutrophication impact (Iribarren et al. 2012). Improvements in feed formulation, manufacturing methods and in-farm management, while enhancing feed digestibility and thus reducing waste production, have reduced the food conversion ratios (ratio between biomass of feed and biomass of fish produced) from 3:1 to 1.3:1 (FAO 2018). In order to tackle the problem of sourcing safe and more sustainable feed, significant effort and progress have also been made to suggest and test alternatives to fish meal and fish oil (Glencross et al. 2007; Tacon et al. 2009; Turchini et al. 2009; Hardy 2010; Olsen 2011; Klinger and Naylor 2012; Oliva-Teles 2012; Soller et al. 2017; Gasco et al. 2018; Sánchez-Muros et al. 2018). This has resulted in a decreased Fish In: Fish Out (FIFO) ratio, a proxy metric to assess the impact of aquaculture on wild stocks (FAO 2018; Kok et al. 2020). Further research advancement in the nutritional domain of aquafeeds is certainly a key element for achieving sustainability in the sector (Turchini et al. 2019). Feed ingredients should not only be evaluated based on the nutritional values for the farmed species, but also on availability from co-products and upon the environmental impacts of the feed manufacture (Little et al. 2018; Kok et al. 2020). Valenti et al. (2018) set out a useful set of indicators of environmental, economic and social sustainability, which can be applied at different levels (i.e. from farm to broader global scales), enabling assessment of the impacts of each component in the aquaculture production chain, identifying limitations in each system and permitting focused interventions towards more sustainable measures. These sustainability indicators can, additionally, be clearly communicated to stakeholders and consumers and can facilitate and improve the certification of organisations for labelling products. 

Resource reuse efficiency 
For efficient reuse of side streams, wastewater treatment methods must be tailored to the daily loads, location and characteristics of a given aquaculture facility (Fig. 1, Fig. 3; Table 1; Miller and Semmens 2002; van Rijn 2013; Badiola et al. 2018). The rates at which the effluents are discharged from different farms must be considered (Table 1; Bureau and Hua 2010; Martins et al. 2010; Amirkolaie 2011; van Rijn 2013). Wastewater nutrient recycling into microalgal biomass is a promising sustainable route for limiting aquaculture waste and increasing production. The harvesting and extraction processes of microalgal biomass and lipids, however, still require technological advances to reduce operating costs and make resource reutilization environmentally sustainable (Mata et al. 2013; Barros et al. 2015; Carneiro et al. 2017). Greater efficiencies are required in nutrient bioremediation and bioaccumulation in raceways (Table 1; Dauda et al. 2019), but metabolic engineering and strain selection could support an optimization of lipid production (Huerlimann et al. 2010; Adarme-Vega et al. 2012; Aravantinou et al. 2013; Oncel 2013). Thermochemical processing of microalgal sludge requires further improvements to make energy recycling within aquaculture economically feasible (Mirzoyan et al. 2010; Panwar et al. 2012; Islam et al. 2017). Further investigations on bacteria-algal sludge co-digestion pathways are needed to improve sludge thickening processes and efficient recovery of by-products at large scales (Mirzoyan et al. 2010; Rawat et al. 2011; Sahu et al. 2013; Fig. 2). Life-cycle assessments of aquaculture sludge by-products, processed via different biological and chemical transformation (Carneiro et al. 2017; Farmery et al. 2017; Henriksson et al. 2018), will add rigour to sustainable production prioritization and support the most sustainable by-product recovery path (Rawat et al. 2011; Oncel et al. 2013; Lopes et al. 2015; Islam et al. 2017; Badiola et al. 2018). Economic evaluations should also value water saving profits derived from the amount of clean water that can be retrieved after bioremediation (Queiroz et al. 2013). 
Polycultures and IMTA offer effective means to upcycle nutrients through the food web in a cost-efficient manner (Chopin et al. 2012). These types of farming, however, face various challenges. These include ensuring pathogen-free integrated systems, monitoring of nutrients and balanced co-culture of species, requiring trained personnel to ensure scalability and food safety (Elston and War 2003; Pruder 2004; Bischoff et al. 2009; Tyson et al. 2011; Chopin et al. 2012). Inclusion of probiotics (e.g. BFT-derived) in encapsulated diets could reduce antibiotics application and dispersal in the environment and improve product storage (Emerenciano et al. 2017; Willer and Aldridge 2019a). It would also be highly desirable to increase the number of studies that can demonstrate positive interactions between co-culture species that can serve as disease control (Skår and Mortensen 2007; Molloy et al. 2011). 

By-product processing and storage
Appropriate facilities for wastewater and seafood by-product processing, transportation, storage, and effluent management are required (Garcia-Sanda et al. 2003; Falch et al. 2007; Rustad et al. 2011; Ghaly et al. 2013). The processing of seafood by-products needs to be carefully regulated in order to avoid microbial spoilage, preserve high nutritional value (Jennings et al. 2016) and ensure a fresh product (Falch et al. 2007; Thorkelsson et al. 2009; Rustad et al. 2011; Olsen et al. 2014). Better control of oxidative stability and unfavourable odours dispersal, for example via fish oil refinement, would improve by-product recovery (Chakraborty and Joseph 2015; Šimat et al. 2019). 

Consumer acceptance
Finally and crucially, there is a need to consider economic factors and consumer behaviour. Aquafeed production cost will affect seafood price, which consumers then use to inform their purchasing choices (Wijesundera et al. 2011; EC 2017). For example, a survey involving >2500 Europeans demonstrated that consumer choice was more closely linked to seafood quality, price and origin, rather than on production system (EC 2017). Ecolabelling and knowledge transfer towards consumers about environmental impacts and farming production practices would help reduce misplaced or incorrect environmental and health concerns amongst the public regarding aquaculture (Salladarré et al. 2010; Dey et al. 2014; Uchida et al. 2014; Ziegler et al. 2016; Sprague et al. 2017; Tlusty and Thorsen 2017). The use of nutrients recycled from aquaculture wastewaters could generate negative perceptions amongst consumers and make them unwilling to purchase more sustainable products (Crab et al. 2012; Handå, Min, et al. 2012; Handå, Ranheim, et al. 2012; Lander et al. 2013). Education regarding the unchanged or improved quality and nutritional value of new sustainable aquaculture products, and the benefits of using side streams for feeds, could change perceptions and increase demand for these products (Chopin et al. 2001; Bunting and Shpigel 2009; Barrington et al. 2010; Roheim et al. 2012). There is a need for greater research, media, and marketing efforts to improve consumer awareness of sustainable seafood production and drive more sustainable consumption choices (Venegas-Calerón et al. 2010; SAPEA 2017). 

5. Conclusion
	Without careful management of limited resources and wastewaters, aquaculture as an industry will fail to thrive under the increasing pressures of population growth and climatic change (Troell et al. 2014; Boyd et al. 2020). Sustainable intensification of aquaculture echoes as an oxymoron and it is certainly not straightforward. Nevertheless, improved nutrient recycling practices, through technological advances in harvesting and processing wastewaters and by-products (Han et al. 2019; Lu et al. 2019), as well as optimization of feeding composition (Martins et al. 2010; Turchini et al. 2019) and formulations (e.g. Willer and Aldridge 2019b) can increase sustainable productive output to consumers and industry. 
Recirculating aquaculture systems have potential to intensify production (Martins et al. 2010) and, given that the highly concentrated effluents are produced at lower rates compared to other farming systems (Fig. 1; Table 1), recycling capacity may be greater. Further research should move towards sustainable improvements of these systems, particularly focusing on efficient methods for energy circularity. Raceways and pond systems require improved designs to sustain intensified production (e.g. eco-ponds; semi-recirculating; Liu et al. 2014; Boyd et al. 2020). Flow-through systems with high rates of daily water load, and RAS systems with elevated energy demand (Toner 2002), could utilise hydropower to reduce the carbon footprint (Badiola et al. 2018). Production in ponds and cages could be maximised through in-situ nutrient upcycling with polycultures and multi-trophic systems. With effective harvesting methods, nutrient recycling from wastewaters can allow upcycling of discarded material through the food web alongside cost-effective water bioremediation. Other lower-tech approaches can enable reduced costs for water treatment, feeds and antibiotics and maximise resource use efficiency. These include the use of probiotics, polyculture and multi-trophic systems. 
All players in the value chain, including production, processing, transportation, storage and retail have a role to play. For example, policy makers should facilitate different industries (e.g. aquaculture, agriculture, restoration, hospitality, tourism) to collaborate for more sustainable and resource-efficient cycles (Bostock et al. 2010). Retailers need to innovate to increase public awareness of resource-efficient aquaculture practices and drive more responsible and sustainable seafood choice (Barrington et al. 2010). Predictions estimate that in early 2020s global seafood production from aquaculture will leave a demand-supply gap of 28 MT fish, with a 9% industry growth needed to meet this gap (Cai and Leung 2017). Long-term predictions on whether aquaculture will meet this new global seafood demand are challenging (Jennings et al. 2016). There is significant uncertainty in several key variables including climate change, marine ecosystem stability, international markets, and consumer and stakeholder preferences (e.g. Brown et al. 2011; Chidmi et al. 2012; FAO 2018). Novel nutrient and by-product recycling in aquaculture will, though, certainly play a key role in increasing production output. The circular economy can enable aquaculture to grow and contribute to the sustainable nutrition of billions of people by 2050. 

Acknowledgments
This project was partly supported by EIT Food Grant MIDSA (Grant numbers 19167 and 20293). DFW was supported by a BBSRC Doctoral Training Programme. DCA was supported by a Dawson Lectureship at St. Catharine’s College, Cambridge.


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