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Seafood arising from animals encompasses a vast array of invertebrate and vertebrate species captured from, and grown in, marine, fresh, brackish and indoor recirculating water systems. Combined production from fisheries and aquaculture amounted to over 180 million tonnes in 2017. Rapid growth in aquaculture has increased its contribution to total aquatic food production (now ~50%) and to overall global animal production, with over 400 different species being farmed (Supplementary Section 1.1 and Supplementary Fig. 1.1). In the next three decades, increased demand for aquatic protein as a component of human diets is predicted, requiring a doubling of output from global aquaculture as capture fisheries remain stable1. By 2050, at least 100 million tonnes of extra seafood, predominantly arising from aquaculture, will be placed on the market (Supplementary Section 1.2 and Supplementary Fig. 1.1). Differential projected growth in the four major subsectors of animal aquaculture—marine fish, freshwater fish, crustaceans and molluscs—is expected to consolidate freshwater fish as the dominant contributor to global seafood, with more modest but nonetheless substantial expansions in supply from the other three subsectors (Supplementary Section 1.2 and Supplementary Fig. 1.2). In this Analysis, we propose that pathogen and chemical hazards present in aquatic systems have the potential to severely limit production, or safe consumption, of seafood arising from aquaculture. The Seafood Risk Tool (SRT) described here allows detailed profiling of the uncontrolled and controlled impact of these diverse hazards at six key phases in the seafood supply chain. When applied to specific national or subnational aquaculture scenarios (for example, for production of a given species from a defined location, with products destined for designated markets and end uses), the SRT can perform a critical function for national governments by supporting conditions for high animal health status and conditions for trade and safe consumption—core components of the One Health approach to aquaculture2 and integral within strategies aiming to nourish nations with ‘blue foods’ (defined in ref. 3).

Hazards and seafood

Aquatic animals have a particularly intricate relationship with their environment—their physiology and life-history traits making them prone to exposure, accumulation and impact of diverse chemical and pathogen hazards present in water, sediments and their food. The SRT considers three broad hazard categories with the potential to interact with, and impact, the seafood supply chain from different aquaculture subsectors: (1) chemical hazards (CH) from natural or anthropogenic sources that may affect the health or survival of animals used for seafood, and humans consuming seafood products; (2) animal pathogen hazards (AH) that may affect the growth, performance, survival or product quality of animals destined for use as seafood; (3) human pathogen hazards (HH) associated with seafood that may affect the health and survival of human consumers. Analysis of the literature associated with hazard interaction with, and impact on, different seafood species groups (Supplementary Section 2.1), augmented with information on chemical and pathogen categories listed in international aquatic animal health and seafood safety guidelines4,5, proposed 14 hazard subcategories within CH, AH and HH. Further definition of hazards falling within these subcategories (for example, specific animal and human pathogen taxa, anthropogenic chemical species, natural biotoxins and allergens) then forms a customized hazard list relevant to specific aquaculture scenarios, taking account of farmed species, farm location and method, intended market and product end use. Hazard subcategories and empirical illustrations of interaction between specific hazards and aquatic animals used for seafood are presented in Table 1 and, for representative marine fish, freshwater fish, crustacean and mollusc seafood groups, in Supplementary Section 2.1.

Table 1 Hazard categories, types and examples of hazards (customized list) with the potential to interact with, and impact, the production, harvesting, processing, trade and safe consumption of animals destined for the seafood supply chain from aquaculture
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Pathogen and chemical hazards interact differentially with discrete phases of the supply chain, through early life (for example, hatchery production of larvae), grow-out (where juvenile and adult animals are grown in farm settings), harvesting, processing (to products), trading (nationally or internationally) and, eventually, consumption (in different forms). While the impacts of pathogen and chemical hazards on production phases are usually economic (for example, slow growth or mortality of stock, poor animal welfare and costs associated with therapies), those affecting processing, trade and consumption phases may be economic (where they may limit processing efficiency and restrict trade or the capacity to place products on the market) or health related (where intake of hazards via seafood consumption has public health consequences) (Supplementary Section 2.2 and Supplementary Fig. 2.1). Regardless of where in the supply chain hazards interact and impact, collectively they translate to a loss of supply of (safe and sustainable) food—a crucial consideration to be factored into future production aspirations at national, regional and global levels. Estimating the impact of specific hazards at given phases of supply also facilitates focus on those phases where interventions for control may have the greatest impact. The SRT may therefore be applied in three control states: (1) when assessing the potential uncontrolled impact of hazards acting upon supply from a specific aquaculture scenario; (2) when assessing benefit of applying discrete phase-specific control measures for limiting impact of hazards acting at that phase of supply; (3) when assessing multi-phase (cumulative or stepwise) control measures in limiting impact of hazards acting upon supply from a specific aquaculture scenario. Where hazard impact can be mitigated by intervention (for example, biosecurity control plans, active monitoring, post-harvest processing and so on), either at single or multiple phases in supply, the SRT provides a basis to target measures most efficiently and to calculate ensuing benefits of intervention compared with the uncontrolled state. In situations where application of controls is unable to adequately limit the impact of specific hazards, the SRT may guide go/no-go decisions relating to the feasibility of a stated aquaculture scenario to fulfil its proposed consequences (that is, production of seafood for an intended market and use). Here, amendment of the scenario (for example, alternative farmed species, site, intended market and product use) may lead to improved outcomes where seafood can be safely produced and consumed (Fig. 1).

Fig. 1: Application of the SRT to a specified aquaculture scenario.
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Stepwise progression requires a clear definition of the scenario to which the SRT is being applied (1) followed by the formation of a customized hazard list relating to the major CH, AH and HH hazard categories likely to interact with specific phases of supply (2 and 3). The SRT is initially applied to the uncontrolled state (4) where no mitigations are applied. By considering the role of phase-specific control options identified within the RMM (5), the SRT can be re-applied to this controlled state (6), repeating, if necessary, with different control combinations. The outturn is a biosecurity and seafood safety plan (7) that assists a decision to progress, amend or reject the aquaculture scenario in fulfilling its goal, as initially stated (8). CH1, heavy metals; CH2, persistent organic pollutants; CH3, radiological contaminants; CH4, natural biotoxins; CH5, veterinary, pharmaceutical and personal care chemicals; CH6, allergens; AH1, viral pathogens; AH2, bacterial pathogens; AH3, protistan pathogens; AH4, metazoan pathogens; AH5, syndromes; HH1, environmental pathogens; HH2, anthropogenically derived pathogens; HH3, zoonotic pathogens. See Table 1 for descriptions and examples of specific hazard types and their mode of interaction with seafood and Supplementary Section 2.1 for examples of hazard interaction with, and impact on, different seafood species groups. The spider diagram profiles represent the hypothetical risk profile when hazards are not controlled (red border) and when controls are applied (green border) throughout the supply chain for the scenario under consideration.

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The SRT

In lieu of a single method to efficiently capture the combined impacts of diverse chemical and pathogen hazards on discrete phases of seafood supply, the SRT uses a two-step semi-quantitative risk assessment schema to calculate impact as a multiple of scores for severity of harm caused and the likelihood of harm occurring (Supplementary Section 2.2 and Supplementary Table 2.1). Application of the SRT requires initial definition of the aquaculture scenario under investigation, including data on specific taxonomy, geography, seasonality, production method, product type, proposed market and intended end use. Further, a supply phase-specific customized hazard list (within the hazard definitions of CH, AH and HH) should be tailored to the scenario and used as the basis for generation of impact scores via the SRT schema. Outputs from the SRT include cumulative impact scores for specific hazard categories acting through the whole supply chain and scores for specific hazards interacting at discrete phases of supply. The SRT can be applied to both ‘uncontrolled’ (no hazard mitigations applied) and ‘controlled’ (hazard mitigations applied) states to inform a biosecurity and seafood safety plan appropriate to the aquaculture scenario under investigation (Fig. 1).

Here we demonstrate application of the SRT to a hypothetical aquaculture scenario intending to produce farmed bivalve molluscs in coastal waters of a non-European Union (EU) marine state for intended live export (and raw consumption) within nations of the EU. The scenario was chosen to represent one in which multiple CH, AH and HH hazards are likely to interact with different phases in supply, and where recognized control measures are potentially available at state and sub-state levels to mitigate hazard impact. The filter-feeding behaviour of bivalve molluscs and propensity for some species groups (for example, oysters) to be consumed raw also represent a particularly good example of the intricate relationship between certain seafood types, hazards present in their growing environments and risk to human consumers of certain end products arising from the sector (Table 1 and Supplementary Section 2.3). Environmental pathogens (HH2), natural biological toxins (CH4), anthropogenic pathogens (HH2), heavy metals (CH1) and bacterial diseases (AH2) represented the top five cumulative uncontrolled risks over the whole supply chain (Fig. 2a). The top-ranking risks within each of these categories over the whole supply chain were Vibrio parahaemolyticus (in HH2); amnesic, paralytic and lipophilic biological toxins (in CH4); hepatitis A virus and Salmonella (in HH1); cadmium, mercury and lead (in CH1); and diseases caused by various Vibrio spp. (in AH2) (Fig. 2a and Supplementary Section 2.3). When specific supply phases were considered, pronounced impacts of AH hazards were predicted for early-life and grow-out phases (for example, viral, bacterial and parasite-induced mortality of animals on farms), with further potential for impact during the international trading phase, where pathogens of concern (for example, Marteilia refringens) are listed in legislation (Fig. 2b and Supplementary Section 2.3). Human health hazards had a less pronounced impact on production phases but presented a higher risk of impacting harvest and processing (for example, hepatitis A virus and norovirus), trading (for example, Salmonella spp. or high levels of indicator bacteria indicative of faecal contamination) and, particularly, consumption phases. In the latter, contamination by faecal-borne human pathogens such as hepatitis A virus, norovirus and Vibrio cholerae non-01/139 may elicit significant public health consequences via consumption, if not controlled (Fig. 2b and Supplementary Section 2.3). Similarly, CH had less impact on early-life and grow-out phases but impacted harvest and processing (for example, where concentrations of natural biological toxins exceed safe limits), trading (for example, where presence of heavy metals exceeds safe limits) and consumption phases (for example, where contamination of bivalves by natural biotoxins directly impacts human health) (Fig. 2b and Supplementary Section 2.3).

Fig. 2: Application of the SRT to a bivalve mollusc aquaculture scenario in which live animals are destined for an export market for consumption in raw form.
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a, Cumulative SRT scores for uncontrolled impact of 14 hazard types across all phases in supply. The top five relative cumulative risks are associated with impact of HH2 (anthropogenically derived pathogens), CH4 (natural biotoxins), HH1 (environmental pathogens), CH1 (heavy metals) and AH2 (bacterial pathogens). b, Relative impact of hazards belonging to hazard categories CH, AH and HH at the six phases in supply; animal health hazards impact predominantly during production phases (and during trade) while human health and chemical hazards impact more greatly during harvest and post-harvest phases. c, Hazard-specific relative impact following application of control measures as detailed in the RMM for bivalve molluscs (Fig. 3). Control 1 (non-accrued scores) and control 2 (accrued scores) are compared with the uncontrolled state in which no phase-specific controls are applied. See Table 1 for descriptions and examples of specific hazard types and their mode of interaction with seafood and Supplementary Section 2.1 for examples of hazard interaction with, and impact on, different seafood species groups.

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Application of the SRT to the uncontrolled state can directly support decisions to progress or amend the aquaculture scenario plan (Fig. 1). The uncontrolled SRT also provides a baseline to which a Risk Mitigation Matrix (RMM) can be applied—a bespoke inventory of measures aimed at reducing risk associated with specific hazards impacting discrete phases of supply. Figure 3 shows the application of the RMM to the bivalve mollusc scenario and compares SRT scores for the uncontrolled state in which no controls are applied with those where either standalone/non-accrued control measures are applied at discrete phases of supply (control 1) or where the benefit of controls applied at one phase are accrued in subsequent phases of supply (control 2) (details provided in Supplementary Section 2.3). For anthropogenically derived CH and HH hazards, benefits of controlling hazards through the supply chain are enhanced by siting of farms where comprehensive environmental characterization has already been performed6,7. Subsequently, interventions during harvest include suspension of harvest, transfer of live animals to cleaner sites (‘relaying’) or otherwise informing onward processing requirements. Processing interventions include purification through re-immersion in clean water (for example, depuration) or other mechanical interventions (for example, irradiation for denaturing potential human pathogens in final products)8. Further, product monitoring during the processing phase may either occur at the official services level and/or by the food business operator informed by the application of Hazard Analysis Critical Control Point (HACCP) plans (including batch release measures)9. Labelling and traceability, good hygiene practices, general education of workers (such as cold chain breaches and contamination by staff with diarrhoea–vomiting symptoms) and avoidance of consumption of raw product by ‘at risk’ groups are critical measures for reducing risk during the consumption phase10. For AH hazards, interventions during the production phase may be essential, including initiatives such as the Progressive Management Pathway for Aquatic Biosecurity approach supported by appropriate national biosecurity tools11, on-farm biosecurity planning (determined by government biosecurity policy/practice) and application of best aquaculture practices (BAP) approaches from organizations such as the Global Aquaculture Alliance12. During the trading phase, application of the Office International des Epizooties (OIE) Code is relevant for listed pathogens, with generic chapters (surveillance and biosecurity) also contributing to de-risking of disease outbreaks from non-listed taxa. Most producer and trading countries are OIE members, with standards for international trade recognized by the World Trade Organization (WTO). More stringent national/regional controls can also be implemented if justified by risk assessment and meeting other criteria (equivalence) set out in the WTO SPS (sanitary and phytosanitary measures) agreement13. For the bivalve mollusc scenario, benefits of application of control measures are set out in Fig. 3 and summarized in Fig. 2c (detailed in Supplementary Sections 2.1 and 2.3). The most pronounced reductions in risk were observed where controls were applied in early phases, and accrued at subsequent phases, of supply. For some hazards (for example, CH6), the application of available controls did not materially reduce risk; for CH6 hazards, avoidance of a product by susceptible consumer groups was the most relevant measure to reduce risk (Supplementary Section 2.3). The SRT is widely applicable to other aquaculture scenarios, including for marine fish, freshwater fish and crustaceans, using the schema presented here—although in each scenario, the impacts of hazards associated with discrete CH, AH and HH hazards acting at specific phases in supply are expected to differ significantly (Supplementary Section 2.1).

Fig. 3: RMM applied to bivalve mollusc aquaculture scenario where live animals are destined for export market to be consumed raw.
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Control measures for specific hazards can be applied to given supply phases. The RMM informs re-application of the SRT to the uncontrolled scenario (no mitigations applied) for potential de-risking of supply using standalone/non-accrued benefits of applying controls at specific supply phases supply (control 1) or to cumulative/accrued benefits of applying controls at subsequent supply phases (control 2). Resultant scores are represented in red, yellow and grey columns (Fig. 2c). Data relating to calculation of the SRT for these control options are provided in Supplementary Section 2.3. aSite pre-selection (covering CH, AH and HH hazards) offers the best risk mitigation measure that may be accrued during all subsequent supply phases. bActions include suspension of harvest, ‘relaying’ animals at clean sites or otherwise informing onward processing requirements. cPurification through re-immersion of molluscs in clean water (for example, depuration and relay) or other mechanical interventions where criteria for efficacy of intervention are measurable (for example, irradiation). dProduct monitoring either by official services or food businesses informed by application of HACCP plans (including batch release measures). eGood hygiene practices and education of workers to avoid cold chain breach, contamination of seafood by staff and consumption by ‘at risk’ groups; labelling and traceability are critical. fApplication of Progressive Management Pathway, supported by appropriate national biosecurity tools, on-farm biosecurity plans, application of BAP or similar, application of measures in OIE Code for listed pathogens and generic chapters (surveillance and biosecurity) for other pathogens. gApplication of OIE standards for international trade as recognized by the WTO, including more stringent national/regional controls where justified by risk assessment, and meeting other criteria (equivalence) set out in the WTO SPS agreement. NA, not applicable.

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Policy implications and outlook

Diverse hazards interacting with seafood supply undermine sustainability via lost yield (food and profit) relative to the human, organism and environmental capital inputs required to create it2. Aquatic animal health and seafood safety are public goods, given that they cannot be easily purchased in the marketplace and thus require government intervention to ensure they are enacted9,14. Nationally, state-level responsible authorities designated to oversee aquaculture production and trade must be supported by official control laboratories able to apply quality-assured surveillance, analytical and diagnostic tools with respect to animal health (for example, OIE, the Progressive Management Pathway for Aquaculture Biosecurity (PMP-AB) and National Biosecurity Plan), anthropogenic and natural contaminants, and pathogens threatening seafood safety (for example, Codex Alimentarius codes of practice and standards). Known hazards (where regulatory requirements exist) can also be controlled by industry (for example, by farm-level best management practice and application of HACCPs to production and processing), supported by formal responsible authority monitoring, and surveillance activities and audit functions. Individual and societal preferences for, say, cooked seafood may confer additional protection against the impact of microbial hazards present within some seafoods, though they may have less effect at mitigating the risk of chemical threats. Where seafood is exported, regulations spanning primary production and final product are frequently in force with audit by importing countries or by trading blocs (for example, the EU) helping to mitigate risks of identified hazards in final products for consumers within those markets. The desire to trade often becomes a primary motive for deployment of hazard controls in producer nations. However, understanding hazards at each stage of the supply chain in the country or region of production, which may vary geographically, is considered vital irrespective of whether the product is destined for export or domestic markets. For all seafood production, quality and safety standards should be designed to control risks extant within that region and intended use of the product, with export regulatory requirements applied in addition.

Increased reliance on protein arising from aquaculture in global diets3 coupled with significant potential for blue foods to support development of a ‘low stressor’ global food system15 must now be placed in context with the impact of mass global human migrations to coastal zones16, substantial pressures on water supply and quality, and the widespread use of water systems to dispose of human, agricultural and industrial wastes containing diverse pollutants17. Special focus must be applied to low- and middle-income nations where >90% of current aquaculture production occurs, where the most future growth and altered blue food consumption is predicted3 and where the majority of wastewater from land-based sources is currently discharged without treatment17. While predominant scientific, policy and public discourse has focused on the potential impact of aquaculture on aquatic systems—outlined and discussed in ref. 2—much less consideration has been paid to the impact of land-based human activities on contamination of those aquatic habitats that will be increasingly relied upon to provide human dietary protein in the coming decades18. The SRT considers those hazards with potential for greatest impact on supply of seafood from different aquaculture sectors, and the transnational-, state-, farm- and societal-level interventions that may be required to mitigate them. It also provides a flexible framework to which novel emerging chemical and pathogen hazards may be added, potentially including those hazards (exemplified by severe acute respiratory syndrome coronavirus 2) that although not directly impacting aquatic animal health or seafood safety may nevertheless significantly impact supply chains19. For enactment, national strategies for aquaculture growth must therefore include (or interact with) comprehensive policies aimed at protecting aquatic habitats from diverse pollution sources, not least to protect the biodiversity upon which future aquaculture and its diversification will inevitably rely19. Initiatives such as the Global Burden of Animal Diseases approach aimed at identifying baseline metrics for supply chain losses (to disease) and justifying resource allocation for interventions may provide a logical methodology for extension to justify investment in the control of wider chemical and microbial hazards in food systems20. Further, proportional investment in state infrastructures that minimize the release of hazards to aquatic systems and increase the capability to detect known and emerging hazards where they occur and to apply appropriate controls to ensure the blue food revolution is a safe one should be considered a multi-faceted public good, where benefits extend beyond food and wealth to protection of biodiversity and climate change mitigation relative to food systems.

Methods

The SRT scores were generated for farmed bivalve molluscs in coastal waters of a non-EU marine state for live export (and raw consumption) within nations of the EU through small expert group elicitation (subgroups of authors of this paper) for each hazard category or subcategory, according to the framework provided in Fig. 1 (and detailed in Supplementary Sections 2.2 and 2.3). Impact and likelihood scores (with supporting evidence) for discrete hazard categories acting at specific phases in the supply chain for bivalve molluscs were provided by each subgroup to a coordinator (R.H.). The coordinator (an expert in the scenario under consideration), working with representatives of each subgroup, then agreed a final score for each hazard (at each phase) on the basis of evidence presented, using a probabilistic approach. Subgroups were asked to assess three states: (1) where there is uncontrolled impact of hazards on supply; (2) where application of phase-specific control measures is used to limit impact on supply; (3) where application of multi-phase (cumulative or stepwise) control measures is used to limit impact on supply. The evidence used was a mixture of peer review, grey literature and expert opinion generated within subgroups and was represented as the RMM provided in Fig. 3. The semi-quantitative process broadly followed the expert knowledge elicitation method, a structured approach to collate opinions from expert groups in a transparent manner focusing primarily on probabilistic methods to elicit expert judgement on quantitative parameters whilst minimizing bias21. Other formal expert elicitation processes (for example, the IDEA protocol)22 have previously been used to calculate impact of discrete aquatic animal diseases in aquaculture23 and may also be suitable to SRT application.