The role of seafood in sustainable diets

As global human populations grow and become wealthier, demand rises on terrestrial and ocean environments as sources of foods and providers of other ecosystem services (Springmann et al 2018). Continued growth and development also places additional strain on our climate, and the resulting climatic changes will in turn influence regional food productivity (Godfray et al 2010). Our food systems primarily rely on land-based production of plants and animals, but wild capture fisheries and, increasingly, inland and marine aquaculture—the farming of fish shellfish and aquatic plants—are an important source of micronutrient rich foods (Seto and Fiorella 2017). Nevertheless, aquatic contributors to the global food system are often seen as peripheral, despite global fish production ranked between poultry and beef (Troell et al 2014, Edwards et al 2019). A recent review finds that seafood is often excluded from food security and food systems research, and when included, seafood consumption is viewed as a tradeoff between positive health outcomes and overfishing concerns (Farmery et al 2017). When included in global assessments, all seafood—both wild capture and aquaculture—is often included as a single commodity despite the widely varying nutrient compositions (Hicks et al 2019) and environmental impacts of catching or rearing different seafood species and bringing them to market (Hilborn et al 2018). This is, in part, due to the fact that the research and policy agenda for fishery policy and food, nutrition and health policy run 'on independent tracks, with only loose and superficial links between them' (Hall et al 2013, p 8398). To bring a more complete understanding of the potential role of seafood in healthy, sustainable diets, here we compare nutrient content and greenhouse gas (GHG) emissions—as a key indicator of environmental impacts—of major seafood species and production methods with land-based food production systems.

While most research and policy debate on the nutritional benefits of fish and shellfish has centered on protein and omega-3 fatty acids, many fish and shellfish may play a critical role in addressing deficiencies in other micronutrients such as vitamin A, calcium, vitamin B12, iron and zinc (Kawarazuka 2010, Golden et al 2016). These nutrients are often found in more bioavailable forms in fish and shellfish than they are in many vegetables, fortified staples, and food supplements (Bogard et al 2015, Thilsted et al 2016). For many countries facing nutrient deficiencies, finfish catches alone could provide all dietary micronutrient requirements for all people living within 100 km of the coast in those countries (Hicks et al 2019). Potential nutritional benefits of fish and other aquatic animals are not limited to coastal communities: inland capture fisheries production has increased each year, with most recent data indicating a 11.6 million metric tons (mmt) in 2018, and inland aquaculture is much larger that either marine aquaculture (30.8 mmt) or freshwater capture fisheries (12 mmt), producing 51.3 mmt in the same year (FAO 2020).

Given growing interest in the environmental sustainability of food production, and the known nutrient richness of seafood, a key question is then whether seafood provides an environmentally efficient way to supply essential micronutrients: does it have a place in 'planetary health diets' (Willett et al 2019)? This question can be addressed using life cycle assessments (LCAs), which provide a means to track inputs and outputs associated with different food commodities and production systems to compare the environmental cost, in this case, of supplying micronutrients to human diets (Garnett 2013). A 2017 meta-analysis of 369 published LCA studies across plant and animal-source foods (ASFs) found that plant-based foods had the lowest impact whereas ruminant meat had the highest, and seafood species ranged from moderately low (e.g. herring) to high (e.g. lobster) (Clune et al 2017). In 2018, Poore and Nemecek used existing LCA data to create a model to predict multiple environmental impacts at each node in the food supply chain, relying on thousands of datapoints from farms, processors, packaging firms, and retailers; it also found plant-based foods have impacts lower than the lowest impacts among ASFs (Poore and Nemecek 2018). A recent commission by the Lancet found a 'planetary health' diet consisting of raw plant-source foods a low to moderate amount of seafood and poultry, and no or a low quantity of red meat, processed foods, and starchy vegetables is needed to achieve nutrition requirements and minimize a range of environmental impacts including GHG emissions, land use, and acidification (Willett et al 2019). Similar to Poore and Nemecek (2018) and unlike the more species-specific study by Clune et al (2017)—the Lancet Commission chose to report 'fish' and 'crustaceans' as broad categories. These three studies analyzed environmental impact in terms of overall volume (e.g. kg of food produced), and not in terms of specific nutrients. While aggregation may be necessary at a high level, results from seafood-specific LCAs suggest much information is lost by such grouping. Aggregation is also problematic given that seafoods are diverse in terms of production and in terms of micronutrient richness (Thilsted et al 2016, Golden et al 2021b). A meta-analysis of animal proteins finds wild-capture small pelagic fisheries performed best while industrial beef and catfish aquaculture performed worse (Hilborn et al 2018).

This research extends the work of Hilborn et al (2018) and Hallstrom et al (2019) to include products from land and marine ASFs as well as a selection of plants that have yet to be compared with the ASF literature. This work establishes a connection between nutrient content and environmental footprints to determine which animal-source protein most efficiently supply nutrients relative to their GHG emissions (mentioned throughout as 'environmental impacts'). This work evaluates environmental tradeoffs in the production of macro- and micro-nutrients to improve decision-making toward more nutrient-dense food outputs that minimize environmental impact.

2.1. Summary of datasets

2.2. Environmental impact standardization

2.3. Estimating nutrient production using a nutrient richness index

A nutrient richness index was used to capture nutrient concentrations across a diversity of critical nutrients. This builds upon environmental impact research focusing on impacts related to single nutrients (e.g. Hilborn et al 2018), by recognizing that the value of many foods is in their portfolio of multiple nutrients (e.g. FAO et al 2020). The nutrient richness index for a food product was calculated as the proportion of daily requirements for a nutrient met by a 100 g serving (Drewnowski 2009). We modified Drewnowski's method of calculating the nutrient richness index in two ways. The first was to add a combined value of DHA and EPA Omega-3 fatty acids—marine-based and often discussed as important contributors to maternal and childhood health—to the 'NR15' nutrient group calculated by Drewnowski (2009) using 15 nutrients. Nutrient composition profiles were downloaded from the USDA Food Composition database, including information on 43 nutrients across 213 food products (United States Department of Agriculture and Agricultural Research Service 2019). The only nutrient data that was not sourced from USDA was for pangasius catfish because it is not in the USDA database. This data was sourced from the Aquatic Food Composition Database (Golden et al 2021a). The second was to make these calculations focus exclusively on the nutrients 'to encourage' in Drewnowski et al (2009) and not the nutrients 'to limit': saturated fats, sodium or added sugar. In total, 12 beneficial nutrients were used (table A4). To calculate the nutrient richness index, we determined the individual richness of each nutrient in terms of 100 g servings (equation (1))

$$\begin{equation}{N_{p,n}} = \frac{{{C_{p,n}}}}{{{D_n}}}{\text{ }}\end{equation} \tag{ 1 }$$

where nutrient richness N_p,n is the proportion of the daily requirement of a given nutrient n per 100 g of edible product p met by that product's concentration of a given nutrient per 100 g. C is the concentration of a given nutrient n per 100 g of edible product p, and D is the daily requirement required by adults for each nutrient n.

Once the nutrient richness scores were calculated for each individual nutrient, the scores were averaged across all 12 nutrients to create the nutrient richness composite index R_p for each individual food product (equation (2))

$$\begin{equation}{R_p} = \frac{{\sum\nolimits_{i = 1}^{12} {{N_{p,n}}} }}{{12}}.\end{equation} \tag{ 2 }$$

2.4. Methods to relate environmental impacts to nutrient production

Calculating the environmental impacts of nutrient production required the construction of a ratio of impacts to nutrient concentrations for each food. Environment-nutrition ratios were calculated as both impacts per nutrient richness composite index (equation (3)) and per individual nutrients (equation (4))

$$\begin{equation}{G_p} = \frac{{{I_p}}}{{{R_p}}}.\end{equation} \tag{ 3 }$$

${G_p}$ is the composite nutrient index for each product p, which is calculated by the impact of each product p divided by the composite nutrient richness index for that product. One environment-nutrition ratio was calculated for each combination of environmental impact and nutrient concentration for each product (e.g. three observations of GHG impacts per nutrient for corn meant three environment-nutrition ratios). Because the composite nutrient richness is an average of the 12 nutrient values, this ratio can be thought of as the environmental impacts required to meet the average daily recommendation across all included nutrients.

Environment-nutrition ratios were also calculated for specific nutrients where there are remaining concerns from the public health community regarding their deficiencies in diets around the world, namely zinc, iron, folate and vitamin A (Bailey et al 2015). We calculated individual environment-nutrition ratios for these nutrients and the others making up the composite index using equation (4).

$$\begin{equation}{S_{p,n}} = \frac{{{I_p}}}{{{N_{p,n}}}}.\end{equation} \tag{ 4 }$$

S_p,n is the environment-nutrition ratio for each product ${I_p}$ and each product's individual nutrient richness value ${N_{p,n}}$, calculated as the ratio of impact per 100 g of edible product to nutrient richness value.

2.5. Optimization of foods that minimize GHGs and meet dietary requirements

3.1. Nutrient richness across foods

The nutrient richness index (equation (1)) reveals a considerable difference across food production groups. Among the most nutrient rich food product groups, salmon and small pelagic fish (e.g. anchovy, herring, pilchards) rated highest, along with bivalves (e.g. mussels) and cephalopods (e.g. octopus). Some plant products—particularly nuts, rice and grain—were also nutrient-rich (figure 1). Beef, lamb and fowl (e.g. chicken) were the most nutrient-rich of the land-based ASFs. The lowest nutrient richness were prawns, catfish (pangasius), whitefishes, tilapia, plant flowers, bulbs, pork, dairy products, corn, stems tubers and fruits.

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3.2. GHG emissions relative to nutrient richness

Plant-based foods had generally lower GHG footprint (i.e. GHG emissions needed to meet average nutrient requirements) compared to most ASFs (figure 2). But there were significant exceptions. Small pelagic fish (sardines, anchovies, herrings, mackerels) are the most abundant type of fish in global wild fish catches (FAO 2020) and are the most nutrient rich across all food groups. When considering GHG emissions associated with their production, only the median level of emissions for select plants (i.e. roots, grain, wheat, soy, nuts) is lower than for small pelagic fish.

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Small pelagic fish, bivalves and carps all had GHG footprints much lower than land-based ASFs, where dairy and fowl had the lowest GHG footprint and pork, lamb and beef had the highest. Other than dairy and fowl, land-based ASFs had much higher median GHG footprints than most marine and aquatic ASFs. The GHG footprints of wild-capture small pelagic fish was 60-fold less than beef and 130-fold less than wild capture prawns, which had the highest environment-nutrition ratio. While prawn production generally had very high GHG footprints, it varied depending on production sector: prawn capture fisheries had lower GHG footprints compared to prawn aquaculture.

Higher environment-nutrition ratios were driven either by high environmental impacts, low nutrient richness scores or a combination of the two. For example, dairy and pangasius catfish had lower average nutrient richness than many other ASFs. However, the environment-nutrition ratio for pangasius catfish is much higher because the food group's GHG emissions to produce 100 g of product is comparatively higher than dairy.

3.3. Environmental impacts of meeting dietary requirements of individual nutrients

When considering the GHG footprint across individual nutrients for a selection of two of the terrestrial and aquatic food groups with environment-nutrition ratios that were the lowest (i.e. roots, small pelagics), and highest (i.e. beef, prawns), we see the importance of specific environment-nutrition ratios that drive the nutrient richness indicator (Figure 3). For some nutrients, the lowest and the highest have equal impacts to meet the daily requirement for some nutrients (e.g. Magnesium), but for others, there are considerable differences (e.g. Vitamin A RAE is approximately 150× higher for small pelagics than for roots). In still other cases, nutrients are not available for some food groups (e.g. dietary fiber is only found in plants and Omega 3 s DHA + EPA originate in marine sources, either in the wild or as part of feed formulations).

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3.4. Portfolio of foods that meet dietary needs while minimizing GHG emissions

Planning for our future requires a food system that produces enough to address malnutrition for growing populations while minimizing its global and regional environmental impacts. Decisions made on how food is produced, processed and distributed creates environmental impacts with consequences that range from exacerbating global climate change and its effects to finer-scale impacts on the surrounding environment like eutrophication. The results make clear that not all seafood is equal with respect to their environmental impacts and nutrient richness. Diversity with respect to species groups and production systems should be further recognized in future research and decision-making on the selection of food production systems that minimize environmental impacts and maximize contributions to food security and nutrition outcomes.

Across the development spectrum, nutrient-rich foods play an important role in addressing diet-based diseases and health risks caused by a transition to calorie-rich nutrient poor foods, a concern voiced in FAO's most recent State of Food Security and Nutrition in the World report (FAO et al 2020). A recent global study on environmentally sustainable diets found that vegetable availability is insufficient to meet recommended consumption levels and this gap is only expected to widen (Mason-D'Croz et al 2019). As food production systems continue to reconcile their contributions to global environmental change, they also need to recognize the impact that these changes have throughout supply chains from decreasing nutritional quality of crops to increasing the need for additional cold storage infrastructure (Fanzo et al 2018). If regional supply solutions are not found, sustainable food systems in these areas will have to find alternative sources of comparably low environmental impact foods. Our results indicate that alongside some nutrient rich aquatic and marine foods—with much higher nutrient richness than many land-based ASF production systems—can help to meet this shortfall where production and/or supply is feasible. Any proposal to increase the supply of such healthful and low environmental impact seafood requires careful consideration for the governance and value chains of seafood provisioning. While there are substantial gains to be made by improved management (Hilborn and Costello 2018), wild fishery stocks will not alone meet growing, global demand for seafood. While farm-raised bivalves have high potential to contribute nutrient rich food at lower environmental impact than many other animals, but their production depends on regional growth potential and strong governance that guides financial and regulatory backing to support development (Davies et al 2019). Regulation can become an obstacle, as is the case for US aquaculture where environmental concerns can delay or stop permitting approval at federal, state or local levels (Knapp and Rubino 2016).

Our results also suggest that small pelagic capture fisheries hold promise as a component of 'planetary health diets'. One challenge limiting availability of small pelagic fish in the food system is the focus on conserving small pelagic fish for their predators; there is unclear evidence whether reductions in directed fishing of small pelagic fish has such benefit because of the variability in their abundance—even without fishing (Knapp and Rubino 2016). There are opportunities to direct more of the existing harvest of small fish towards human consumption; a large portion of the global harvest of small pelagic fish is converted into fishmeal and fish oil for use in aquaculture (Cashion et al 2017). Technical changes in aquaculture feeds such as insects, agricultural waste, and algae indicate that in the future more small pelagic fishes may be used directly as human foods (Costello et al 2019). A combination of supply chain interventions and marketing to increase consumer awareness and demand are likely required.

There were some limitations to this research that require discussion. While the environment-nutrition ratio approach is useful for comparison, it must be stated that these ratios will change as more LCAs are published and as more nutrition information on species becomes available. The composite nutrient richness index, rather than the individual nutrient concentrations, is a useful summary metric when thinking of overall healthfulness of each food. However, from a public health nutrition standpoint an important consideration might be to find low impact foods that meet deficiencies in specific nutrients for a specific context. Here the preferred metric might be to focus on an individual nutrient exemplified in figure 3. Averaging across the 12 nutrients can hide low concentrations of nutrients within each food. For example, if dietary fiber is the concern, ASFs with high nutrient richness indices still will not be useful in meeting this need as fiber is found in plants. Relatedly, the focus of this research was on beneficial nutrients, and did not cover food safety concerns that exist among land and aquatic animal source foods. For example, toxins like methylmercury concentrate at higher trophic levels and in particular aquatic environments with adverse health outcomes particularly for pregnant women (Beckers and Rinklebe 2017). GHG emissions were the sole environmental impact in focus for this study, and it is important to note that these results may be cast in different light if other impacts are considered. For terrestrial systems, land use impacts may be similarly high for beef (Poore and Nemecek 2018). However, some plant-based foods that performed well in our analysis may have much higher impacts under metrics associated with land use. For example, land use for soy production may not only have high land use but has led to further biodiversity and deforestation impacts in Brasil (Garrett and Rausch 2016). This work was limited to impacts at the farm-gate or dock-side. Subsequent research should also consider impacts as these products move through the food chain, where we know that changes to processing, packaging, transport and food waste mitigation may have varied additional impacts (Poore and Nemecek 2018), but also present an opportunity for innovation. More research is required to extend the evaluation to these foods with respect to different types of environmental impacts, their use across the supply chain and whether scaling their production would provide a sustainable contribution to a more healthful food system.

Defining sustainable diets has received increased attention from the research and policy communities. The food combinations this analysis finds to deliver the lowest environmental cost per unit nutrient richness do not suggest a diet, but they do suggest a constellation of foods that contribute towards the creation of scenarios that may help shift consumers towards higher quality, nutritious plant-based food systems that can maintain a safe operating space across a suite of environmental impacts for aquatic and terrestrial foods. The environment-nutrition ratios for terrestrial foods largely uphold existing research by Poore and Nemacek (2018), namely that plant-based foods have among the lowest GHG footprints across all foods. This work builds on those conclusions: with the exception of a few aquatic foods, plant-based foods perform better than ASFs when considering their impact relative to nutrient richness as well. This result also affirms the general conclusion that dietary guidelines recommending diets focused on plant-based foods and some fish are among the most healthful and sustainable (Springmann et al 2020), but takes a different approach that focuses more on malnutrition than on diet-based disease. Our results also support the general conclusions of EAT-Lancet Commission (Willett et al 2019); a majority of plant-based foods tend to have some of the lowest environmental impacts given their nutrient richness. Results of this research build upon the EAT-Lancet report by taking a finer resolution look at the fishery and aquaculture sector relative to livestock and plant-based agriculture. While the EAT-Lancet report does recommend fish generally, our more detailed analysis indicates that some capture fisheries and farmed shellfish have environmental impacts at least as low as many plants, and lower than most animal-source proteins. The optimization results further affirm this, and also reveal that theoretical optima will sometimes be challenging or impossible to apply in practice. True diet-based solutions must be affordable, diverse and culturally acceptable (Tuomisto 2019). It is our hope that wider recognition of the contribution of fish and shellfish to the food system will help drive fishery reform where overexploitation remains a concern in some parts of the world. In doing so, fisheries and aquaculture products that are nutrient rich and low in environmental impact can further contribute to food system planning that meets the objectives of the planetary health agenda.

Food production varies in terms of its environmental impact and its capacity to meet nutritional needs; this research combines these two factors, comparing products across plants and ASFs from terrestrial, capture fishery and aquaculture production systems, to identify foods and production system that provide nutrition at lower environmental impact. Foods sourced from plants as well as bivalve and carp aquaculture and small pelagic fisheries tended to have the lowest environmental impact given their nutrient richness to meet dietary requirements across a diversity of nutrients. In contrast, beef, pork, crustaceans, prawns and pangasius catfish had the highest environmental impacts given their nutrient richness. The contribution of plant-based foods discussed here supports the existing literature, but the potential role that certain species of fish can play in meeting dietary guidelines provides a novel insight to identify nutrient-rich sources that not only combat malnutrition but also reduce environmental impacts of the entire food system.

This work formed part of JZK's PhD at the University of Washington's School of Aquatic and Fishery Sciences, which was supported NSF IGERT Program on Ocean Change (Grant Number 1068839). JZK and RH received additional funding from the Seafood Industry Research Fund. EHA and CDG were supported by the National Socio-Environmental Synthesis Center (SESYNC) under funding received from the National Science Foundation DBI-1639145. EHA was supported by WorldFish and the Nippon Foundation Ocean Nexus Programme. WorldFish is supported by contributors to the CGIAR Trust Fund. Special thanks to Jessica Gephart of American University for her thoughtful comments on an earlier version of this work.

All data that support the findings of this study are included within the article (and any supplementary files).