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The sustainable development of fish nutrition in aquaculture will need to correspond with the challenges that aquaponics delivers with respect to the growing need for producing high-quality food. Manipulating the nitrogen, phosphorus and the mineral content of fish diets used in aquaponics is one way of influencing the rates of the accumulation of nutrients, thereby reducing the need for the artificial and external supplementation of nutrients. According to Rakocy et al. (2004), fish and feed waste provide most of the nutrients required by plants if the optimum ratio between daily fish feed input and plant growing areas is sustained. Solid fish waste called 'sludge' in aquaponic systems results in losing approximately half of the available input nutrients, especially phosphorus, that theoretically could be used for plant biomass production but information is still limited (Delaide et al. 2017; Goddek et al. 2018). Whilst the goal of sustainability in fish nutrition in aquaculture will in the future be achieved by using tailor-made diets, fish feed in aquaponics needs to fulfil the nutritional requirements both for fish and for plants. Increases in sustainability will in part derive from less dependence on fishmeal (FM) and fish oil (FO) and novel, high-energy, low-carbon footprint raw natural ingredients. To safeguard biodiversity and the sustainable use of natural resources, the use of wild fisheries-based FM and FO needs to be limited in aquafeeds (Tacon and Metian 2015). However, fish performance, health and final product quality may be altered when substituting dietary FM with alternative ingredients. Thus, fish nutrition research is focused on the efficient use and transformation of the dietary components to provide the necessary essential nutrients that will maximize growth performance and achieve sustainable and resilient aquaculture. Replacing FM, which is an excellent but costly protein source in fish diets, is not straightforward due to its unique amino acid profile, high nutrient digestibility, high palatability, adequate amounts of micronutrients, as well as having a general lack of anti-nutritional factors (Gatlin et al. 2007).
Many studies have shown that FM can be successfully replaced by soybean meal in aquafeeds, but soybean meal has anti-nutritional factors such as trypsin inhibitors, soybean agglutinin and saponin, which limit its use and high replacement percentages in farming carnivorous fish. High FM replacement by plant meals in fish diets can also reduce nutrient bioavailability in fish, which results in nutrient alterations in the final quality of the product (Gatlin et al. 2007). It can also cause undesirable disturbances to the aquatic environment (Hardy 2010) and reduce fish growth due to the reduced levels of essential amino acids (especially methionine and lysine), and reduced palatability (Krogdahl et al. 2010). Gerile and Pirhonen (2017) noted that a 100% FM replacement with corn gluten meal significantly reduced growth rate of rainbow trout but FM replacement did not affect oxygen consumption or swimming capacity.
High levels of plant material can also affect the physical quality of the pellets, and may complicate the manufacturing process during extrusion. Most of the alternative plant-derived nutrient sources for fish feeds contain a wide variety of anti-nutritional factors that interfere with fish protein metabolism by impairing digestion and utilization, therefore leading to increased N release in the environment which can affect fish health and welfare. In addition, diets including high levels of phytic acid altered phosphorus and protein digestion that lead to high N and P release into the surrounding environment. Feed intake and palatability, nutrient digestibility and retention may vary according to fish species' tolerance and levels and can change the quantity and composition of the fish waste. Taking into consideration these results, fish diet formulations in aquaponics should investigate 'the tolerance' dietary levels of anti-nutritional factors (i.e. phytate) for different feed ingredients and for each fish species used in aquaponics and also the effects of the addition of minerals such as Zn and phosphate in the diets. It also should be noted that even if plant material is regarded as an ecologically sound option to replace FM in aquafeeds, plants need irrigation, and thus may induce ecological impacts in the form of their water and ecological footprints (Pahlow et al. 2015) from nutrient run-off from the fields.
Terrestrial animal by-products such as non-ruminant processed animal proteins (PAPs) derived from monogastric farmed animals (e.g. poultry, pork) that are fit for human consumption at the point of slaughter (Category 3 materials, EC regulation 142/2011; ΕC regulation 56/2013) could also replace FM and support the circular economy. They have higher protein content, more favourable amino acid profiles and fewer carbohydrates compared to plant feed ingredients whilst also lacking antinutritional factors (Hertrampf and Piedad-Pascual 2000). It has been shown that meat and bone meals may serve as a good phosphorus source when it is included in the diet of Nile Tilapia (Ashraf et al. 2013), although it has been strictly banned in the feed of ruminant animals due to the danger of initiating bovine spongiform encephalopathy (mad cow disease). Certain insect species, such as black soldier fly (Hermetia illucens), could be used as an alternative protein source for sustainable fish feed diets. The major environmental advantages of insect farming are that (a) less land and water are required, (b) that greenhouse gas emissions are lower and that (c) insects have high feed conversion efficiencies (Henry et al. 2015). However, there is a continuing need for further research to provide evidence on quality and safety issues and screening for risks to fish, plants, people and the environment.
It is important to note that fish cannot synthesize several essential nutrients required for their metabolism and growth and depend on the feed for this supply. However, there are certain animal groups that can use nutrient-deficient diets, as they bear symbiotic microorganisms that can provide these compounds (Douglas 2010), and thus, fish can obtain maximal benefit when the microbial supply of their essential nutrients is scaled to demand. Undersupply limits fish growth, whilst oversupply can be harmful due to the need for the fish to neutralize toxicity caused by non-essential compounds. The extent to which the microbial function varies with the demands of different fish species and what are the underlying mechanisms are largely unknown. Importantly, an aquatic animal's gut microbiota can in theory play a critical role in providing the necessary nutrients and obtaining sustainability in fish farming (Kormas et al. 2014; Mente et al. 2016). Further research in this field will help facilitate the selection of ingredients to be used in fish feeds that promote gut microbiota diversity to improve fish growth and health.
Research into the utilization of alternative plant and animal protein sources and low trophic fish feed ingredients is ongoing. The substitution of marine sourced raw ingredients in fish feed, which could be used directly for human food purposes should decrease fishing pressure and contribute to preserving biodiversity. Low trophic-level organisms, such as black soldier fly, which may serve as aquafeed ingredients may be grown on by-products and waste of other agricultural industrial practices given different nutritional quality meals, thereby adding additional environmental benefits. However, efforts to succeed with the circular economy and the recycling of organic and inorganic nutrients should be handled with care since undesirable compounds in raw materials and seafood products could increase the risk to animal health, welfare, growth performance and safety of the final product for consumers. Research and continuous monitoring and reporting on contaminants of farmed aquatic animals in relation to the maximum limits in feed ingredients and diets are essential to inform revisions in and introductions of new regulations.