Aquaculture is predicted to supply the majority of aquatic dietary protein by 2050. For aquaculture to deliver significantly enhanced volumes of food in a sustainable manner, appropriate account needs to be taken of its impacts on environmental integrity, farmed organism health and welfare, and human health. Here, we explore increased aquaculture production through the One Health lens and define a set of success metrics — underpinned by evidence, policy and legislation — that must be embedded into aquaculture sustainability. We provide a framework for defining, monitoring and averting potential negative impacts of enhanced production — and consider interactions with land-based food systems. These metrics will inform national and international science and policy strategies to support improved aquatic food system design.
Aquaculture is one of the fastest growing and highly traded food sectors globally — Asia accounts for 90% of production1 and volumes are predicted to double by 20501 (Supplementary Section 1). Enhanced sustainable production (ESP) in aquaculture features within the Rome Declaration of the Second International Conference on Nutrition (ICN2), the United Nations Framework Convention on Climate Change (COP21) and in the 2030 Agenda for Sustainable Development2. Achieving ESP is technically, socially and politically complex: the sector spans small homestead-scale production systems — underpinning food security in rural settings in low- and middle-income countries — to medium-sized farms that contribute to exports and high-technology industrial-scale production of globally traded products. More than 500 aquatic species are farmed in widely divergent social and legislative infrastructures — with different end goals. Thus, a holistic approach to the design and implementation of aquaculture systems is needed3 — framed within the broader context of sustainable food systems4.
The sector offers many positive aspects: poverty alleviation in some of the lowest-income regions5, production increases from technological advances and selected species lines6, the use of non-fed (for example, molluscs) and extractive (for example, seaweed)7 species with benefits of farms for proximate marine biodiversity8, comparatively lower environmental impact of some types of aquaculture9,10, and smaller spatial footprints compared with both capture fisheries11,12 and land-based agriculture13. However, numerous sustainability challenges must be addressed across the diverse range of aquaculture sectors. For example, economic gains in the global shrimp sector have been prioritized in spite of evidence of major mangrove forest degradation14, bonded labour and social inequities15, and potentially high carbon footprints16,17. The profitable Northern Hemisphere Atlantic salmon aquaculture industry farms native stocks, but claims of subsequent pathogen spillover18, loss of genetic integrity of native populations19 and wider environmental degradation of sensitive habitats20 persist. Similarly, antibiotic overuse in Southern Hemisphere Atlantic salmon production21 remains disproportionate to the economic benefits in otherwise deprived rural communities22. The principles of One Health — defined as the collaborative, multisectoral and transdisciplinary approach to achieving beneficial health and well-being outcomes for people, non-human organisms and their shared environment (Supplementary Section 2) — offer a practical framework to achieve aquaculture ESP. Governments, producers, wider industry, scientists and the public must engage to facilitate the design of food systems to decouple the human health benefits of consuming aquatic protein from negative environmental, organismal and societal impacts that may develop around a rapidly expanding, unregulated sector. Interaction and integration of independent accreditation schemes, such as the Best Aquaculture Practice standards (https://www.bapcertification.org/), with traditional governmental regulation could deliver greater positive impacts23.
Here, we propose a practical means to implement the One Health approach to aquaculture ESP within national and international policy, legislation, evidence provision and research (Fig. 1) that can be tailored to industry sub-sectors to address specific sustainability requirements.
Sustainability measures must be rigorously applied across all food sectors if aquaculture is to become part of regional and global sustainable food systems. Evidence-based success metrics indicate producers’, co-operatives’, sub-sectors’ or the regional industry’s compliance with the One Health principles (Table 1 and Fig. 2) and aid metric-specific policy and legislation development. Metrics that are fully achieved gain the highest score of 5, corresponding to policy and legislation being in place and consistently applied. The lowest score of 1 is given for unsuccessful metrics when no supporting research or evidence is in place to support policy and legislative design. This approach allows tailored sub-sector evaluation, highlighting specific areas for improvement and directing future research and evidence to support design of policy and legislation (Fig. 3).
Aquaculture can provide a range of public health, economic and social benefits. The One Health approach might result in a series of decisions on investment and health quality that make ‘optimization’ closer to a set of trade-offs between economic gain and productivity, animal welfare or system-wide health. Market preferences or social aspirations to sponsor or tolerate certain levels of health will become crucial in establishing practical health. In Bangladesh, for example, finfish consumption increased by 150% between 2000–2010, while adjusted prices for cultured catfish and tilapia fell by 40% — largely as a result of expanding freshwater pond production24 — with considerable impact on human health and well-being25. Simultaneously, rapidly urbanizing populations can suffer from the coexistence of food poverty and overconsumption of processed foods26 — aquaculture products could alleviate some of these issues. While producers may choose more profitable and sometimes less nutritious cash- and export-oriented crops, aquaculture as a component of polyculture traditions in many low- and middle-income countries can contribute to the local availability of nutritious products. An estimated 20 million people are directly employed in aquaculture worldwide, mostly in Asia, while supporting industries and services contribute to 100 million jobs globally. Trade, meaningful employment, gender equity, increasing rural production (which further benefits rural schooling), diet and infrastructure can be included in human success metrics. Early evaluation of public health risks is fundamental within the principles of One Health. For example, whilst the perceived increased gross domestic product (GDP) gains from international trade have driven rapid growth in bivalve mollusc production since the 1950s, a systemic absence of mature legal frameworks, robust data on origin, prevalence and levels of putative human pathogens in aquatic systems, and scarce expertise at the food business operator or official services level have underestimated hazards and severely impacted value chains, limiting exports for many low- and middle-income countries1.
Between 70 to 80% of production is undertaken by a “missing or squeezed middle” of commercial producers27 who “enjoy none of the benefits of investments in biosecurity or pathogen control characteristic of intensive systems nor, the low input/low risk/low output typical of extensive systems”28. These producers are adopting practices such as commercial feed use, water and livestock treatments, but are also loosely tied to value chains, subject to little or no veterinary oversight and are weakly regulated by buyer and/or state organizations. Disease is a persistent threat — constituting an estimated US$6 billion loss per annum in the global industry29 — meaning these producers will be key in improving health outcomes globally. Developing accreditation and consumer trust can be a challenge, particularly as production starts to shift from a bipolar South–North export model (with relatively well-developed buyer driver governance) to a trade pattern that is increasingly South–South with growing production for domestic markets30. Enhancing animal and environmental health requires a programme of engagement with producers to develop ownership of and compliance with ESP goals. The burden of risk and rewards is unevenly distributed within many aquaculture value chains, providing disincentives for innovative and sustainable practices — equitable value chains and rewards for sustainable production will be fundamental to achieve ESP. We outline five success metrics for the human health component of the One Health approach to aquaculture ESP in Table 1 and Fig. 2.
Production occurs within complex ecological systems physically embedded within an environment differing from the farmed species’ wild habitat. Farmed animals or plants interact with communities of viruses, bacteria, small eukaryotes, and other animals and plants within the aquaculture system. Microbes within the system include known and unknown pathogens with potential to cause infection and disease in farmed species. Crop-growing ponds are highly modified, ‘artificial’ ecosystems that can unintentionally create an environment for rapid pathogen propagation and epidemic disease outbreaks — and have been a source of many emergent diseases. For example, the incidentally discovered microsporidian Enterocytozoon hepatopenaei found at low levels in a pond in Thailand over 10 years ago is now one of the most widespread and impactful pathogens in shrimp aquaculture31. Thus, stock management must be considered in terms of health and disease manifestation, zoonoses, biosecurity, genetics, and treatments’ or interventions’ impact on the local environment.
Creating growing conditions conducive to high stock health and welfare is critical for aquaculture ESP — perhaps the most important barrier to development of the industry to 205029. Profiling microbial hazards, even in a preventative manner, utilizing emergent technologies such as high-throughput sequencing of water, sediment, feed and host tissues is increasingly an option32. These technologies can also identify broad biosecurity risks that aquaculture farms pose to the surrounding environment. Preventing pathogen spillover to the environment and wildlife, and vice versa, is a critical measure that must be built into aquaculture systems.
Aquaculture feeds alter the ecology of aquaculture systems and can introduce other compounds such as antimicrobial residues (AMR), which can potentially influence stock health and the physicochemical properties of the system. Feeds range from natural pond fertilizers to formulaic feeds for enhancing stock performance. Pharmaceuticals, liming or sterilization between cropping cycles, and biocides can create favourable conditions for disease development by eutrophication, leading to hypoxic stress, or by environmental dysbiosis, whereby disease agents may be preferentially selected and become pathogenic for resident hosts33. Chemical spillover into the surrounding environment, to other farmed stock, wildlife and humans via zoonotic diseases and AMR must be prevented in future One Health design of aquaculture systems. AMR genetic elements within aquaculture systems is of great concern largely due to the intensive and often inappropriate use of antibiotics to treat disease. While some aquaculture sub-sectors, such as Norwegian salmon, are exemplars of antibiotic use reduction, other sub-sectors require substantial improvement34.
The choice of farmed species can be determined by their capacity for their maintenance with minimal ecological modification to the farm environment and a low potential to impact the surrounding environment. While the benefits of sourcing seed stock from natural environments may encourage propensity for disease in captive settings29, conversely, the use of specific-pathogen-free stock may not always be an appropriate choice, particularly when animals are stocked into open systems in which a native microbial community may rapidly exploit microbiologically naive hosts35. Genetic structuring at farm population level must aim to reduce the likelihood of disease epidemics and create resilience to challenges encountered within and between cropping cycles. Mixed species or multitrophic culture systems can be considered for managing health of other stock, minimizing environmental impact and may be more ecologically stable and resilient than monocultures36. Introducing non-native, invasive species to the local environment should be avoided to prevent the risk of hybridization and genetic introgression with native species, and the introduction of pathogen spillover37.
Close attention to national and transboundary spread of hazards — particularly via trade — must extend beyond live animals and include the risk of distributing pathogens via end-products, even those destined directly for human consumption that would not normally interact further with the environment38. The organism health component of the One Health approach is outlined by five broad success metrics in Table 1 and Fig. 2.
Sixty-three per cent of aquaculture occurs in fresh waters, with 29% in marine and 8% in brackish habitats39 — relatively similar projections are expected in future production (Supplementary Section 1). Aquaculture ESP is constrained by the amount and quality of freshwater available. Inland aquaculture globally withdraws around 429 km3 freshwater per year, representing 3.6% of Earth’s surface flowing water40. Future freshwater demands must be balanced against other needs, including for land-based agriculture that currently uses 70% of the readily accessible supply40. The IPCC Special Report on the Ocean and Cryosphere in a Changing Climate indicated that climate change will result in warming seas and the expansions of hypoxic zones, affecting where marine aquaculture may operate and which species can be farmed41. Climate models indicate many tropical regions of the world — where most aquaculture takes place — will become hotter and drier, which is likely to limit available freshwater supply and influence which species can farmed in those environments42. In contrast, temperate regions may be expected to become warmer and wetter, potentially opening new aquaculture development opportunities. Up to 60% of water withdrawn for inland aquaculture could be re-used with adequate pollution control measures for purification of effluents, re-use of nutrients and control of percolation losses39. Highest production to 2030 and beyond will occur in freshwater systems in Asia1. Sustainable management of pollution and effluent discharge is essential; special attention must be given to sub-regions where little or no freshwater operational control measures exist. Freshwater ecosystems are especially vulnerable to biodiversity impacts — 35% of freshwater fish are classified as vulnerable or threatened43, which are vital for providing feed, broodstock, seed (eggs/larvae/fry) and genetic resources for many farmed species.
Although all aquaculture animals are ectotherms, some forms of aquaculture currently operate with a relatively high carbon footprint. For example, shrimp produced on land formerly occupied by mangroves has a carbon footprint of 1,603 kg CO2 per kg of shrimp produced — a figure similar to the production of beef (1,440 kg CO2; ref. 16). Feed inputs are a major environmental and economic cost for many species in aquaculture — an estimated 15.6 million tonnes of wild fish harvested globally is used in the production of fish meal and fish oils (FMFO), almost half of which is used in aquaculture feed44. Alternative feeds, including those based on insect, plant or algal proteins, show promise45, but are yet to offer consistent replacement of FMFO-based feeds. The comparative efficiency at converting protein and energy from feed sources and toleration of species such as carp and tilapia to challenging physicochemical environments have led to significant expansion in the global production of these species1, demonstrating their potential for future aquaculture ESP. Similarly, extractive, non-fed species such as filter‐feeding bivalves, algal grazers, detritivores and autotrophic plants (mainly macroalgae) are considered some of the lowest impact aquaculture organisms (Supplementary Section 1). Culture platforms for seaweeds and bivalves can simultaneously act as nurseries for native biodiversity and boost productivity of wild fisheries, while helping to control nutrient and microbial levels in the water column8. Alternatively, the contained nature of onshore recirculating aquaculture systems hold potential for greater environmental control, better biosecurity and a smaller environmental footprint in terms of land space and water use compared with open systems, particularly when aligned with terrestrial food and energy systems46.
Land-space allocation for future aquaculture must take into account the impacts on biodiversity and natural resource productivity. Globally, approximately 8.7 million hectares is used for freshwater aquaculture production and a further 2.3 million hectares for brackish water production39. Future inland aquaculture will likely compete for space with terrestrial agriculture, which occupies more than one-third — or 5 billion hectares — of the Earth’s surface47. Open oceans provide ample space but offshore systems present considerable operational challenges more suited to larger industry operations. Nevertheless, current US seafood consumption could be met by extending offshore marine aquaculture into less than 1% of exclusive economic zones belonging to coastal states48. Lessons must be learned from the detrimental environmental effects of mangrove removal for shrimp aquaculture — countries such as Bangladesh have destroyed nursery grounds for important commercial wild fisheries and rendered large tracks of land unsuitable for agriculture due to the resulting saltwater intrusion49. Finally, aquaculture ESP must consider areas of cultural and (inter)national heritage importance and must not impose on areas of outstanding natural beauty. The environment component of the One Health approach to aquaculture ESP is outlined in five metrics in Table 1 and Fig. 2.
Interactions between success metrics
The success metrics presented here comprise a research, evidence, policy and legislative package that can guide governing bodies’ aquatic food strategies. Importantly, aquaculture production must not be considered in isolation but rather as a food system with intricate linkages to wild-capture fisheries and terrestrial agriculture systems9. Individual metrics will benefit aquaculture ESP, but it is the interactions and dependencies between individual metrics that may have the greatest capacity to elicit positive change. Conversely, interactions may elicit unforeseen negative feedback loops, which must be guarded against. Such examples include the metrics organism SM2, organism SM3 and organism SM4 (Table 1 and Fig. 2): policy and legislation promoting farm biosecurity can reduce chemical, AMR and zoonotic hazards from entering the environment. The metrics environment SM3, environment SM5 and people SM4 (Table 1 and Fig. 2) interact where lowering the spatial footprint of aquaculture has positive impacts on protecting biodiversity, optimizing water quality and providing people with quality employment. However, if a metric is perceived as requiring excessive regulation, counterproductive actions may be taken by stakeholders to evade the metric, thereby negating its intended impact.
The One Health approach captures detailed aspects of the ecosystem aquaculture approach50 and broader targets from the United Nations Sustainable Development Goals51. The extension of the One Health approach beyond zoonotic diseases — to address grand societal challenges such as food security — was proposed in programmes such as the Network for Evaluation of One Health (Supplementary Section 2). Our approach enables national policies to collectively contribute to aquaculture ESP.
Data collection for monitoring success metrics will require interaction across government departments and a broad range of aquaculture stakeholders. Accountability must extend beyond national borders, particularly where high-income countries obtain food from medium- to low-income and/or less stable regions at the cost of those ecosystems and people52. Given seafood is one of the most traded commodities53, the unaccounted burdens of international, unsustainable socio-ecological practices require attention within the aquaculture sector — and seafood in general. Success metric achievement at national levels, coupled with international cooperation, forms the cornerstone of widespread One Health adoption.
Aquaculture can mitigate the negative consequences associated with land-based food production systems — particularly where land- and water-based systems are integrated — to protect terrestrial habitats from the impact associated with some current farming systems54,55. The One Health principles will facilitate increasing production of aquaculture species with efficient food production and sustainable environmental footprints — while supporting local socio-economic needs. If put into practice, the success metrics presented here will serve as an example for the design and assessment of not just aquaculture, but whole food systems.
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We acknowledge the Centre for Sustainable Aquaculture Futures (a collaboration between the Centre for Environment, Fisheries and Aquaculture Science and the University of Exeter) for funding under contract Cefas Seedcorn contract no. SP003 to host a workshop ‘Sustainable Aquaculture through the One Health Lens’ at the Department for Environment, Food and Rural Affairs (Defra) London, on 1 July 2019. The input to that workshop by colleagues from across Defra provided significant guidance for the material contained within this article.
The authors declare no competing interests
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Stentiford, G.D., Bateman, I.J., Hinchliffe, S.J. et al. Sustainable aquaculture through the One Health lens. Nat Food 1, 468–474 (2020). https://doi.org/10.1038/s43016-020-0127-5
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