Time to rethink trophic levels in aquaculture policy

By: Richard S. Cottrell, Marc Metian, Halley E. Froehlich, Julia L. Blanchard, Nis Sand Jacobsen, Peter B. McIntyre, Kirsty L. Nash, David R. Williams, Lex Bouwman, Jessica A. Gephart, Caitlin D. Kuempel, Daniel D. Moran,

Max Troell and Benjamin S. Halpern *

In this review article developed by a group of specialists from 19 Research Centers and universities located in 9 different countries the premise that the complexity of designating trophic levels in aquaculture has unexamined implications for devising policy positions and Best Practices guidelines to enhance the sustainability of aquaculture is explored.

The aquaculture sector accounts for half of all fish and seafood produced globally, provides an important source of nutrition in some of the world’s most rapidly developing countries, and will be key for meeting future global fish demand. The critical role forage fish play in marine ecosystems has created concern over their extraction and tension over the food security implications of diverting these nutritious species away from human consumption.

At present, the high demand for these resources by the feed industry and favorable profit margins reduce incentives and innovation efforts for increasing direct consumption. Reducing the dependence of aquaculture feeds on wild-caught fish is widely recognized as an important strategy for the sustainable growth of aquaculture.

Environmental and supply chain concerns have led to widespread calls to refocus fish farming on low-trophic level species whose natural diets do not include fish. The inherent inefficiency of trophic transfers through food webs means that the higher the trophic level of an animal eaten by humans, the more ecosystem energy is embodied in its production.

Invoking labels from food web ecology assumes that the trophic level concept is readily applicable in an aquaculture setting. Generalizations about trophic transfer efficiency enable us to equate low-trophic levels with greater sustainability.

Yet ‘low-trophic level’ aquaculture production can take many forms – from unfed shellfish, seaweed, and finfish (such as some filter-feeding carp species) to fed species that primarily depend on plant products in their feeds. The premise of this study is that the complexity of designating trophic levels in aquaculture has unexamined implications for devising policy positions and Best Practices guidelines to enhance the sustainability of aquaculture.

“The inherent inefficiency of trophic transfers through food webs means that the higher the trophic level of an animal eaten by humans, the more ecosystem energy is embodied in its production.”

To evaluate the meaning of trophic level for farmed seafood, we used global aquaculture production, diet, and feed efficiency data to calculate the effective trophic level of fed aquaculture species from 1995 to 2015. Our results elucidate three broad reasons why focusing on the production of low-trophic level species may be unhelpful for increasing the sustainability of aquaculture.

Looking forward, we discuss how more precise dialog and policy could support the responsible and sustainable use of feed ingredients for aquaculture production as the sector continues to grow and becomes more important for food security globally.

Aquafeed advances blur trophic position and taxonomic distinction

During the early growth of the aquaculture industry in the 1980s and 1990s, fishmeal and oil were used heavily in aquafeeds as palatable, nutrient-dense, and cheap sources of protein and lipids that matched the requirements of farmed fish. For farmed carnivores, this meant feed composition closely resembled natural diets, dominated by fish-derived ingredients, but also included small amounts of plant–protein and oils. Conversely, feeds for naturally herbivorous species, such as carp and tilapia, were predominantly plant-based, including fishmeal improved growth rates and body condition.


Temporal evolution of the mean effective trophic level of fed aquaculture. Sensitivity analysis of the mean trophic level change for global fed aquaculture over time since 1995. FF inclusion = only the observed forage fish inclusion rates are changed through time. FF TL = only the observed shifts in trophic level of wild-caught forage fish composition used for feed are changed through time; Spp. comp = only observed changes in the composition of farmed species are included. For each of these combinations, the other two variables were held at 1995 values. All variables = forage fish inclusion, forage fish trophic levels and species composition change with observed values through time. Inset picture shows the temporal change in Atlantic salmon diets in Norway from 1990 to 2016 taken from Aas et al. (2019) as an example of feed composition shifts.

Stagnation in global catches of wild forage fish, competition from other economic sectors, and the enormous expansion of aquaculture production over the past 30 years have driven substantial shifts in the formulation of aquaculture feeds as the price gap between fishmeal/oil and other ingredients widens. Reduced dependence on marine ingredients has occurred with a greater shift towards crops such as soybean, canola, maize, wheat, and nuts to supply energy, protein, and oils for farmed taxa.

Shifts in the feeds provided to carnivorous species have been possible due to advances in aquaculture nutrition, such as a better understanding of the importance of supplementing diets with essential, conditionally essential, and non-essential amino acids and the effects of aquafeed processing on digestibility. For non-obligate carnivores, such as carps or tilapias, lower or no fishmeal inputs align with natural dietary habits and are typically well-tolerated. 

“Not only has the dietary profile of each fed aquatic species shifted through time, but also the overall species composition of farmed fish production has changed substantially at the same time that the actual trophic position of wild forage fish species used in feeds has varied dynamically. When only the observed changes in the trophic level of species assigned as forage fish (and subsequently used in feeds) are accounted for, there is a very slight increase in effective trophic level through time.”

The reduced dependence on fishmeal and oil in feeds across farmed taxa has overwhelmingly influenced the effective trophic level of fed aquaculture. However, when only observed changes in the amount of fishmeal and oil included in feeds are accounted for through time (as opposed to the trophic level of fish used in feed ingredients), the mean effective trophic level responses of the fed sector closely track those that occur when observed shifts in all variables are accounted for.

This shift in dietary composition means that most farmed taxa have been steadily diverging in effective trophic levels from their wild counterparts. The net effect of temporal changes in feed formulation and alteration to the natural diet of cultured species is that many farmed taxa are now converging on effective trophic levels between 2.0 and 2.5. Thus, interspecific distinctions are becoming increasingly blurred: herbivorous fish are fed animal protein and thus farmed as omnivores, and carnivores have become omnivores as they are fed proportionally more plant proteins.

Tanks used for raising tilapia on a fish farm in Brazil

This reality highlights the problem of characterizing any particular taxon as ‘unsustainable’ based only on its wild or historic cultured trophic level. Instead, we must recognize different and dynamic inputs into feeds, and the dynamic nature of practices and management used to grow them. 

Trophic levels mask feed and resource efficiency

Through a combination of feed technologies, nutrition, selective breeding, feed, and on-farm management practices, feed conversion ratios have, on average, improved (decreased) for all species globally. Carnivorous species, such as salmon, are more efficient than naturally herbivorous fish at converting feed into biomass when optimal ingredients are used.

As average estimates, it is important to reiterate that the efficiency of individual production units will depend on feed resource qualities, specific management practices, and environmental conditions. Feed conversion ratios do not consider protein or nutrient retention – important aspects that reflect the capacity for aquaculture to deliver nutritional benefits to consumers efficiently. As average estimates, it is important to reiterate that the efficiency of individual production units will depend on feed resource qualities, specific management practices, and environmental conditions. 

“‘Low-trophic level’ aquaculture production can take many forms – from unfed shellfish, seaweed, and finfish (such as some filter-feeding carp species) to fed species that primarily depend on plant products in their feeds.”

Emphasis on the trophic levels of farmed species also biases our understanding of the impacts of feeds in general. But there has been a widespread lack of consideration for the consequences of displacing the burden of sourcing future aquafeeds from marine to terrestrial environments given that aquafeed ingredients are now tied to multiple food sectors, expansion of reliance on overstressed terrestrial agroecosystems and potential trade-offs across sectors need closer examination.


Temporal trends in global average farmed trophic levels across taxa relative to average reference values from wild counterparts. Note that y-axes have different maxima to effectively illustrate temporal trends within groups. FW = freshwater. Upper and lower boxplot hinges represent 75th and 25th percentiles respectively, and whiskers represent these quantiles plus or minus 1.5 times the interquartile range. Numbers in parentheses represent the number of species used to represent wild trophic levels within a taxon. Note trophic levels for wild species are not specific to any year.

Beyond neglecting other feed components, trophic level indices for farmed species fail to account for details of quality and sourcing of feed ingredients (Fry et al. 2018). For example, while wild-caught forage fish still provide most fishmeal and oil used in fish and livestock feeds, a growing proportion is sourced from trimmings from farmed and wild-caught fish.

Closing loops within feed sourcing processes in this way represents a significant advance in resource efficiency. There could also be limitations if these waste streams represent lower quality ingredients or contamination vectors that influence farmed taxa’s growth rates or nutritional composition, leading to potential trade-offs from these seeming efficiency gains. These important sustainability considerations are not accounted for by trophic level classifications of aquaculture species. 

“Feed conversion ratios do not consider protein or nutrient retention important aspects that reflect the capacity for aquaculture to deliver nutritional benefits to consumers efficiently.”

Irrespective of how aquaculture develops, fishmeal and oil will almost certainly continue to be ingredients used for feed production in the short term. Increasing demand for these ingredients has driven up their price in globalized commodity markets, but potential lower demand for fishmeal and oil for aquafeeds could relax competition with other sectors, such as terrestrial livestock and fertilizer.

Seaweed ,used for industrial purposes,is grown at Kiwengwa Beach, Zanzibar.

In any case, aquaculture policy guidance should focus on the judicious use of forage fish as a limited resource rather than abstractions such as trophic levels of farmed seafood. A complete evaluation of sustainability implications also must account for alternative uses for small pelagic forage fish, such as supporting the food and nutrition security of vulnerable human communities and maintaining a sufficient prey base for marine ecosystems.

Growth in seafood demand will be accompanied by a species-specific preference

Critically, trophic level-oriented policies rarely address the tensions between the desire for improved environmental sustainability and growing global preferences for specific species. With high-value aquaculture dominated by private corporate entities, policies that focus on the trophic level of farmed species will be moot because they ignore the role of profit margins and demand growth in driving the trajectory of aquaculture under the current model of open-ended economic growth.

Towards clearer aquaculture policy

In many cases, unfed species, such as many bivalves and seaweeds, may provide considerably more environmental benefits with fewer environmental impacts than fed finfish. But these products serve different market sectors, so their value as a reference point is, at best, context-dependent. For a given production unit, a species that is farmed at a higher trophic level because of greater proportions of dietary fishmeal/oil may still have a lower forage fish demand than less fish-dependent species if breeding, farming practices, and feed manufacturing result in far superior feeding efficiency.

“A complete evaluation of sustainability implications must account for alternative uses for small pelagic forage fish, such as supporting the food and nutrition security of vulnerable human communities and maintaining a sufficient prey base for marine ecosystems.”

Furthermore, feed ingredients other than forage fish have their own sustainability concerns, such as crops grown using environmentally damaging agricultural practices. The aquaculture industry is highly motivated to adopt practices that improve the efficiency of energy assimilation and the stability of feed supply chains, and continued gains can be expected from continued experimentation with feed composition and the genetics of farmed species. These developments will further undercut the value of trophic levels as a measure of sustainability in aquaculture.

Trophic level indicators are attractive because of their simplicity and familiarity with wider use in other disciplines. Still, the information embedded in these indices is insufficient for assessing the multiple facets of feed sustainability. For the fed segment of aquaculture, continued changes in the formulation of compound feed and convergence of effective trophic levels across taxa will trivialize the trophic levels of wild counterparts as a useful indicator of resource intensiveness.

“Unfed species, such as many bivalves and seaweeds, may provide considerably more environmental benefits with fewer environmental impacts than fed finfish. But these products serve different market sectors, so their value as a reference point is, at best, context-dependent.”

Instead, greater support for feed source transparency policies and participation in voluntary certification schemes, such as Aquaculture Stewardship Council (ASC), Best Aquaculture Practices (BAP), and Safe Feed/Safe Food (SF/SF) Certification Program in the US, should be embraced and incentivized.

Workers on the oyster farm

The ASC has developed farm feed standards that are unique in including aquatic and terrestrial resources and aim to minimize perverse social and environmental outcomes. Rather than concentrating on simple sustainability metrics, these standards explore the nuance of supply chains, trade, and the factors that drive differences in social and ecological impacts of production. Importantly, feed traceability policies or certification programs equip governing bodies with the necessary tools for overseeing the growing aquaculture sector while also empowering consumers and markets with the information needed to favor seafood products produced through best practices.

“A key goal of aquaculture development should be to create species- diverse and nutrient-diverse food sources that remain accessible and appropriate to people across regions and economies.”

The dynamic nature of effective trophic level in fed aquaculture calls into question the use of trophic level as a trait of species grown and a reliable indicator of sustainability. Naturally carnivorous and herbivorous species are typically farmed as omnivores with converging effective trophic levels due to continued feeding practices and formulation changes. While naturally herbivorous species can effectively utilize low-grade plant material for feeds, some carnivorous species may more efficiently convert feed into nutrient-rich biomass.

But focusing on these different efficiencies does not necessarily result in a shift towards greater overall sustainability. A world focused solely on the efficiency of aquatic food – a world of ‘aquatic chicken’ – would favor globalized, vertically integrated seafood supply chains that would likely limit market access for marginalized communities and reduce the diversity of farmed products to a few key commodities. Thus, efficiency gains in one context may actually compromise the environmental and nutritional benefits of access to seafood for humanity as a whole. Instead, a key goal of aquaculture development should be to create species- diverse and nutrient-diverse food sources that remain accessible and appropriate to people across regions and economies.

Realizing the potential of aquaculture to promote environmental sustainability requires the integration of diverse goals, including food system stability, economic development, and global equity. We have shown that trophic level classifications of cultured species can do little to guide us towards such a future because they ignore key intrinsic features of aquaculture production and broader macroeconomic and consumer demand.

Methods

We collated published data on aquaculture production, feed composition, and trophic levels of wild fish species from various sources to investigate temporal trends in the effective trophic level of fed aquaculture between 1995 and 2015. We also used food supply data to understand spatial changes in apparent human consumption of fish and seafood globally. We extracted trophic level values for the wild equivalents of farmed species represented in our analyses using Fishbase and SeaLifebase repositories. To capture the range of species represented in the broad taxa groups we use for effective trophic level calculations, we extracted available trophic level values from each database for the top ten species by farmed biomass within each taxon (or more if this did not represent more than 90% global production of that taxon).

Effective trophic level calculations

Effective trophic level calculations were required for both feed ingredients derived from forage fish (fishmeal and oil) and the farmed fish taxa. The mean trophic level of the fishmeal and oil used in feed largely depends on changes in the annual composition of the forage fish harvested to produce them. We, therefore, calculated the catch-weighted mean trophic level of forage fish using FAO landings data for major forage fish species harvested by render fisheries.

“We recognize that at any given time, the trophic level of fishmeal and oil provided in the feed may be spatially variable as different forage fish species are randomly assigned for feed ingredients in different locations. But given the global nature of this analysis over 20 years, we assume an even contribution of forage fish species to a ‘pool’ of fishmeal and oil.”

Using the trophic values assigned to feed ingredients, we calculated the annual global trophic level of fed aquaculture across 11 farmed taxa within the fed sector (carps, catfish, tilapias, milkfish, other freshwater fish, freshwater crustaceans, anguillid eels, trouts, salmons, shrimps and marine fish) and for the entire fed sector as a whole (marine crustaceans were omitted due to lack of temporal data in feed composition).

We then explored the main drivers of the temporal trends in global effective trophic level among; the proportion of fishmeal and oil included in feeds, the change in species composition of fed aquaculture, or the change in trophic level of forage fish used as feed using a sensitivity analysis. To explore the role of each variable, we held the values for the other two constants at 1995 values through time while allowing the variable of interest to vary as observed and study the effect on temporal trends in mean effective trophic level.

This is a summarized version developed by the editorial team at Aquaculture Magazine of the review article “Time to rethink trophic levels in aquaculture policy” written by Richard S. Cottrell, Marc Metian, Halley E. Froehlich, Julia L. Blanchard, Nis Sand Jacobsen, Peter B. McIntyre, Kirsty L. Nash, David R. Williams, Lex Bouwman, Jessica A. Gephart, Caitlin D. Kuempel, Daniel D. Moran, Max Troell and Benjamin S. Halpern. The original version was published on January, 2021 trough de Reviews in Aquaculture Journal (1-11) in Research Gate. The full version can be accessed at doi: 10.1111/raq.12535

Correspondence author: 
Richard S. Cottrell, National Center for Ecological Analysis and Synthesis, University of California. Email: cottrell@nceas.ucsb.edu


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