Agriculture can help aquaculture become greener

Aquaculture, the farming of fish and seafood, is recognized as a highly efficient system for producing protein for human consumption. In contrast, many terrestrial animal protein production systems are inefficient, impacting land use and exacerbating climate change. Humankind needs to adopt a more plant-centric diet, the only exception being fish consumed as both a source of protein and essential dietary nutrients such as omega-3 fatty acids. Here we consider the implications of such a transition, and the challenges that aquaculture must overcome to increase productivity within planetary boundaries. We consider how agriculture, specifically crops, can provide solutions for aquaculture, especially the sectors that are dependent on marine ingredients. For example, agriculture can provide experience with managing monocultures and new technologies such as genetically modified crops tailored specifically for use in aquaculture. We propose that a closer connection between agriculture and aquaculture will create a resilient food system capable of meeting increasing dietary and nutritional demands without exhausting planetary resources. Aquaculture must develop within planetary boundaries. Experience from agriculture, such as in managing monocultures and using genetically modified crops, can inform sustainable solutions for aquaculture.


A future for fish on the planetary plate
The EAT-Lancet Commission and the recommended Planetary Health Plate 1 proposed fish as the only form of animal protein recommended for increased production and consumption, but it made no distinction between wild capture and aquaculture, nor marine and freshwater species. Distinction between the latter two is critical in terms of the presence/absence of the nutritionally important omega-3 long-chain polyunsaturated fatty acids (LC-PUFAs)-lipids that play a vital role in neonatal and infant development as well as cardiovascular health and metabolic pathologies such as type-2 diabetes 3 , but that humans have a very low capacity to synthesize 4 .
Demand for aquatic species as a key source of protein for human consumption and omega-3 LC-PUFAs has continued to grow 5 . Since 2015, the majority (52% at present) of all fish and seafood consumed is produced by aquaculture 5 . The two production systems are quite different in terms of impact on the environment as deduced from life-cycle analysis 6 -only aquaculture has the potential to meet the needs of 10 billion people in 2050 while remaining within planetary boundaries. However, achieving that will require a significant reconfiguration of current aquaculture food systems ( Fig. 1) and, to some extent, the path will need to be similar to that proposed for humans-a predominantly plant-based diet 1,6 .
Still, the paradigm of aquaculture overcoming the limited supply of fish and seafood from our oceans is problematic, as aquaculture feeds, especially for salmonids and marine fish, are based on fishmeal and fish oil, both extracted from wild capture marine fisheries 4 . Dating back to the 1970s, this was a logical practice for the farming of carnivorous fish species as fishmeal and fish oil reflected their natural diets, providing balanced nutrients that were readily available and cheap. However, the subsequent global expansion of aquaculture, growing at an annual rate averaging around 10% in the 1980s and 1990s, and almost 6% over the last 20 years, has meant that this practice has become unsustainable worldwide 5 . Although aquaculture production of fish and seafood has increased from around 10 Mt in 1990 to 81 Mt in 2016, global reduction (feed-grade) fisheries have been static over this period with catches plateauing around ~20-25 Mt, producing around 5-6 Mt of fishmeal and 0.8-1.2 Mt of fish oil annually 7 . Thus, despite demand from aquaculture increasing, supply has remained relatively constant, and so other protein and oil sources were required to replace fishmeal and fish oil in feed formulations 8,9 . Terrestrial animal by-products such as poultry meals, blood meal and tallow have been used in some parts of the world, but the predominant alternative ingredients have been derived from plant seed meals and vegetable oils 10 . Thus, it was hoped that plant-based products could deliver the needs of aquaculture using a small percentage of global agricultural acreage to satiate the oil and protein requirements of aquafeed diets.

The impact of evolving fish feed formulations
The change in feed formulations from a traditionally marine-derived to a terrestrial-agriculture-derived raw material base has been successful in supporting the growth of aquaculture. In addition, aquaculture feeds and feeding strategies are now significantly more sustainable than in the past 11 . Fishmeal and fish oil are not inherently unsustainable products, as they are often portrayed. The reduction Agriculture can help aquaculture become greener Johnathan A. Napier 1 ✉ , Richard P. Haslam 1 , Rolf-Erik Olsen 2 , Douglas R. Tocher 3 and Mónica B. Betancor 3 Aquaculture, the farming of fish and seafood, is recognized as a highly efficient system for producing protein for human consumption. In contrast, many terrestrial animal protein production systems are inefficient, impacting land use and exacerbating climate change. Humankind needs to adopt a more plant-centric diet, the only exception being fish consumed as both a source of protein and essential dietary nutrients such as omega-3 fatty acids. Here we consider the implications of such a transition, and the challenges that aquaculture must overcome to increase productivity within planetary boundaries. We consider how agriculture, specifically crops, can provide solutions for aquaculture, especially the sectors that are dependent on marine ingredients. For example, agriculture can provide experience with managing monocultures and new technologies such as genetically modified crops tailored specifically for use in aquaculture. We propose that a closer connection between agriculture and aquaculture will create a resilient food system capable of meeting increasing dietary and nutritional demands without exhausting planetary resources.
fisheries from which fishmeal and fish oil are derived are no different to all other fisheries on the planet in that they must be properly managed and regulated to ensure catches are sustainable 4 . In addition, although a significant proportion of fishmeal and, to a lesser extent, fish oil is produced from recycling the by-products of food (capture) fisheries and aquaculture 4 , the fundamental issue with marine ingredients is that they are finite on an annual basis, and thus limiting as demand increases from direct human consumption and aquaculture 7,12 . Thus, formulating feeds with large proportions of marine ingredients became unsustainable 13 . Consequently, as demand for fishmeal (and especially fish oil) increased, availability declined and prices rose, feed manufacturers chose to increasingly replace fishmeal and fish oil with plant seed protein meals and vegetable oils that were readily available and cheaper. The finite amount of fishmeal and fish oil, constrained by the planetary boundary of what the oceans could produce, was spread thinner across the ever-increasing volume of demands 14 .
The changing raw material base of aquaculture feed also has consequences for human nutrition, as the nutrient composition of the farmed fish is altered 12 . This includes potential reductions in minerals (for example, iodine and selenium) and vitamins (such as vitamin D) that are traditionally associated with fish and seafood. Lower levels of essential nutrients in raw material feed ingredients have consequently impacted their levels in farmed fish. However, the most important impact has been on the fatty acid composition of farmed fish. In oily species such as salmon and trout, fish produced on predominantly vegetarian feeds have significantly reduced levels of the omega-3 LC-PUFA EPA (eicosapentaenoic acid) and DHA (docosahexaenoic acid) 12 . In 1990, around 90% of the feed formulation for salmon was fishmeal and fish oil, whereas by 2016, marine ingredients had reduced to around 25%, with 75% coming from terrestrial plant sources 11 . Consequently, the large-scale adoption of this vegetarian replacement strategy lowered EPA and DHA levels in salmon feeds, resulting in 2016 in a decline of omega-3 LC-PUFA in farmed salmon to around 50% of those farmed a decade earlier 15 . Sprague et al. 15,16 also indicated that this replacement strategy-substituting marine fishmeal and fish oil with terrestrial plant-derived ingredients devoid of omega-3 LC-PUFA-had reached a point whereby further substitution would seriously impact the quality of salmon and farmed fish in general. In addition, omega-3 LC-PUFA have the same essential roles in fish as they do in humans 17,18 : they are equally important for the health of fish. This could be compromised in farmed animals by further reductions in the levels of EPA and DHA in feeds 19,20 .
Expanding the production capacity of aquaculture while increasing sustainability is only possible through the extensive use of plant meals and vegetable oils. Agriculture therefore has a vital role to play in helping to further transform aquaculture. Some of this is already underway, with the application of data-driven approaches to many aspects of industrial-scale aquaculture. Equally, selective breeding approaches established for terrestrial animals and plants, such as genomic selection and genome wide association studies, are now also used routinely in genetic improvement for some commercial fish species 21 . However, it is the unrivalled potential of agriculture to expand that has the greatest potential to help aquaculture-twinning the continued growth of the latter with the former can help aquaculture to become greener and create a truly sustainable solution.
Crop-based agriculture plays a central role in global nutrition and food security. The global production of vegetable oils has increased from 148 Mt in 2010 to 198 Mt in 2017. Thus, the total outputs of the reduction fisheries look fairly insignificant, which indicates that crop-based agriculture has the capacity to contribute to the relief of current bottlenecks in the aquaculture sector. In the long term, significantly less land will be needed to produce feed ingredients for terrestrial animal protein production 2,22 .

Increasing the synergy between agriculture and aquaculture
One approach to increasing this synergy would be to use crops to produce some of the specialized feed ingredients that aquaculture is dependent on, namely omega-3 LC-PUFA and high-quality protein 23 . There is also strong demand for antioxidant pigments such as astaxanthin for skin and flesh colouration in many farmed species. Such new contributions would be in addition to the already significant contribution plant products make to aquafeeds, but (in some cases) provide a better-tailored composition (in terms of nutrition) or provide a de novo, scalable source of a previously rate-limiting component-examples are listed below.

Plant-derived omega-3 LC-PUFA replacements.
Although this concept has been mooted for well over a decade 24 , major progress has been made in the last few years with the development of different crop species capable of accumulating EPA and/or DHA. We have recently reviewed the different emerging alternative sources of omega-3 LC-PUFA (plants, algae) as sustainable solutions to the current supply gap 25 , but will briefly focus here on the role of transgenic plants. Progress has been achieved by genetic modification, introducing genes from marine microalgae to the oilseed crops Brassica napus (Canola) and Camelina sativa (Camelina). Both have now been brought to an advanced stage of technology readiness. The recently granted deregulated status of Canola 26 in the United States means that the crop is approved for commercial cultivation and can be grown at any scale. Concomitant to the progress in Canola, a platform for the synthesis of both EPA and DHA in transgenic Camelina has also been developed. The accumulation of The pristine environment and clean waters around the Shetland Islands make it a desirable location for aquaculture. However, such activities come with a responsibility to not only maintain the beautiful surroundings, but also conserve the natural capital. Such farms also face logistical challenges, operating in remote locations with extended supply chains. The challenge is to provide an economic return for the business, be excellent stewards of the environment and deliver safe and healthy fish for ever-increasing human consumption.
EPA and DHA in Camelina seed oil has been established as a viable prototype 27,28 , subject to approved experimental environmental release in the United Kingdom, United States and Canada, providing significant data on the stability of this trait 28 , as well as providing sufficient oil for the evaluation of the material as a drop-in replacement for fish oil. All previous studies confirm the promise of using genetically modified plants to provide a terrestrial source of fish oil, in both aquaculture 27,29,30 and direct human nutrition 31 .

Plant-based sources of astaxanthin and other ketocarotenoids.
Compared with omega-3 LC-PUFA, the requirement of aquaculture for the pigment astaxanthin, a ketocarotenoid that gives the flesh of salmonids its distinctive pinkish hue, is relatively modest (~500 tonnes per year). At present, most astaxanthin in aquafeed formulation is produced by chemical synthesis or via fermentation of microorganisms that accumulate ketocarotenoids, although both processes have a significant environmental footprint and a lack of flexibility 32 . Several recent attempts to use transgenic plants to produce ketocarotenoids and validate their bioequivalence to other industrial sources have proved successful. For example, it was shown that ketocarotenoids made in transgenic maize were efficiently taken up by trout and improved the pigmentation of the flesh 33 . Similar studies in trout and longfin yellowtail demonstrated the efficacy of astaxanthin produced in transgenic soybean 34 . More recently, transgenic tomato fruit was used to accumulate astaxanthin for evaluation in aquafeed trials of trout 35 . On the basis of these studies, it was estimated that 1 ha of transgenic tomatoes could produce 34 kg of ketocarotenoids 35 , meaning that the total current requirements of aquaculture could be produced in less than 15,000 ha of greenhouses.
Improved protein composition and designer crops tailored for aquafeeds. Many marine carnivorous species do not perform well on diets lacking fishmeal, and possible reasons may include: (1) a suboptimal amino acid balance for fish, specifically a relative deficiency of methionine, lysine, cysteine and the non-protein amino acid L-taurine 34 ; (2) the presence of antinutritional factors such as plant-specific secondary metabolites; and (3) an abundance of oligosaccharide species that are nutritionally inadequate and/or impede digestibility. When these are combined with a general lack of palatability, fish very often do not thrive on diets rich in plant protein, despite the latter's environmental credentials. Therefore, efforts are underway to tailor the composition of plant seeds for aquaculture, including the reduction of seed glucosinolates that can act as feeding deterrents to the fish. A more speculative advance would be the transgenic coproduction of vaccines to some of the diseases that are problematic in aquaculture 36 .

Learning from agriculture
One of aquaculture's main advantages is that it produces fish over a three-dimensional space and can thus deliver exceptionally high yields over a relatively small surface area. For example, a sea-pen holding 200,000 Atlantic salmon (1 million kg of slaughter-ready biomass) has a surface diameter of only ~50 m. Given the relentless pressure on land for terrestrial meat production, it is not surprising that there has been a global drive towards aquaculture production, even before the constraints of operating within planetary boundaries was fully articulated. For example, in Norway (a major aquaculture-intensive country), the government has set a goal to increase salmon production fivefold to over 5 Mt by 2050.
Increased growth in production volumes, however, produces similar problems to those encountered by agriculture during the mid-twentieth-century expansion. First, large concentrations of animals are a breeding ground for many pathogens. In open sea-pens for Atlantic salmon there has been a massive increase in sea lice infestations. These parasitic copepods attach to the skin and, as they mature, produce wounds that can eventually kill the fish. The short life cycle of sea lice ensures a relatively fast evolution of resistance to chemical treatments and, in that respect, this is a similar problem that industrialized agriculture has faced since the 1960s-that is, reliance on artificial pesticides in a monoculture 37 . Similar to agroecological methods used in some agricultural systems, other management measures can be adopted to reduce this pressure including the use of 'cleaner fish' (such as ballan wrasse and lumpfish) that prey on salmon lice 38 . However, although the use of cleaner fish has expanded over the past decade, high mortality rates and inherent disease still cause major fish welfare issues 38 . It is possible that, in general, aquaculture practices may also be stressful for the fish, making them susceptible to many other opportunistic diseases. This may be mitigated via functional feeds with ingredients such as omega-3 LC-PUFAs, which are known to be precursors of anti-inflammatory and stress-modulating compounds.

Sourcing and developing improved nutrition
In view of the predicted increase in aquaculture production volumes, it is expected that dietary macronutrients such as proteins and lipids in aquaculture feeds will come from a wide variety of sources. These could include processed meals and oils from poultry, swine and cattle, by-products from capture and farmed fish, and fishery discards. It is likely that lower trophic levels from the marine environment including algae, krill and mesopelagic fish will increasingly be incorporated, particularly as omega-3 LC-PUFA sources. Single-cell proteins 39 such as yeast, microalgae or bacteria, as well as insects 40 are also being increasingly positioned as new protein sources for animal feeds due to their generally high protein contents and favourable amino acid profiles.
These variations in nutrient sources will have a major impact on the gastrointestinal microbiota of farmed fish 41 , which is a potentially major health and welfare issue in fish. To maintain optimum fish health and welfare in intensive monoculture systems, future aquaculture might depend on a stable and controlled gut microbiota to prevent pathogen entry and eliminate establishment of harmful bacteria. This balance can, to some extent, be controlled by a probiotic approach 42 , common in Asian aquaculture. Most of these bacteria, however, will not establish themselves in the intestines, and need fibre or other 'prebiotic' components to stabilize. Alternatively, both can be fed simultaneously to the fish, in a 'synbiotic' approach 41,43 . Many of these components are of plant origin and it is expected that agriculture will have a key role in optimizing these products specifically for aquaculture in the future. In addition to fibre, other plant-derived components-such as terpenoid oils, which have been reported as antimicrobial, antioxidant, immune-stimulating and stress-reducing agents-will contribute significantly to the improved health and welfare of farmed fish 44 .

Conclusions and future prospects
Aquaculture already plays a central role in feeding us, but with the shifts in multiple factors described above, that role will expand and become more critical. Aquaculture has previously been portrayed by some in a negative light, with a focus on the environmental impact of fish farms and examples of poor animal health. However, further growth in the industry will come with increased public awareness, so aquaculture needs to adopt a new approach to scrutiny. In that respect, they can learn from the lessons of the plant biotechnology industry 45 . Much benefit can be derived from establishing public dialogues between industry and the consumer, helping to develop a more cooperative model of food production within the aquaculture sector. It is also important to recognize that aquaculture is a highly innovative industry, being adaptive and welcoming to new technologies and approaches. Ultimately, the two systems-aquaculture and agriculture-need to work in tandem to meet the challenges of operating resiliently within planetary boundaries and delivering optimal nutrition for a growing population. It is our hope that the ideas outlined in this Perspective are just the starting point for a more integrated approach to sustainable aquaculture, one in which the major role of agriculture is fully incorporated.