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Nutritional attributes, substitutability, scalability, and environmental intensity of an illustrative subset of current and future protein sources for aquaculture feeds: Joint consideration of potential synergies and trade-offs Nathan L. Pelletier, Dane H Klinger, Neil A Sims, Janice-Renee Yoshioka, and John N Kittinger Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05468 • Publication Date (Web): 10 Apr 2018 Downloaded from http://pubs.acs.org on April 11, 2018

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Environmental Science & Technology

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Nutritional attributes, substitutability, scalability, and environmental

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intensity of an illustrative subset of current and future protein sources for

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aquaculture feeds: Joint consideration of potential synergies and trade-offs

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Nathan Pelletier1*, Dane H. Klinger2, Neil A. Sims3, Janice-Renee Yoshioka4, John N.

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Kittinger4,5

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1

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Columbia, Kelowna, BC, V1V1V7. [email protected]

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2

Center on Food Security and the Environment, Stanford University, Stanford, CA, USA 94305

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3

Kampachi Farms LLC, Kailua-Kona, Hawaii, USA 96740

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4

Conservation International, Center for Oceans, Honolulu, Hawaiʻi USA 96825

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5

Arizona State University, Center for Biodiversity Outcomes, Julie Ann Wrigley Global Institute

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of Sustainability, Tempe, AZ USA 85281

* 340 Fipke Centre for Innovative Research, 3247 University Way, University of British

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Table of Contents/Abstract art

1 ACS Paragon Plus Environment


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Abstract:

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Aquaculture is anticipated to play an increasingly important role in global food security, as it may

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represent one of the best opportunities to increase the availability of healthy animal protein in the context

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of resource and environmental constraints. However, the growth and sustainability of the aquaculture

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industry faces important bottlenecks with respect to feed resources, which may be derived from diverse

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sources. Here, using a small but representative subset of potential aquafeed inputs (which we selected in

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order to highlight a range of relevant attributes), we review a core suite of considerations that need to be

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accommodated in concert in order to overcome key bottlenecks to continued development and expansion

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of the aquaculture industry. Specifically, we evaluate each input’s nutritional attributes, substitutability,

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scalability, and resource/environmental intensity. On this basis, we illustrate a range of potential synergies

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and trade-offs within and across attributes that are characteristic of ingredient types. We posit that

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recognition and management of such synergies and trade-offs is imperative to satisfying the multi-

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objective decision-making associated with sustainable increases in future aquaculture production.

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Introduction

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Global food production may need to double in the next 30 years to meet the demands of a

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growing and increasingly affluent population.1 However, the inputs required to sustain production in

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traditional agricultural sectors are already limited, and competition for these resources from other sectors

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is intensifying. For example, agriculture accounts for 70% of freshwater demand, and crop and

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pastureland occupy 30% of land surface area.2 Moreover, expansion of agricultural activities is a major

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contributor to a range of critical environmental problems, including climate change, biodiversity loss,

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water pollution, and perturbation of the global nitrogen cycle.3 This is particularly true of terrestrial

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livestock production, which plays a dominant role in food-related resource and environmental impacts.4

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In the ocean, fisheries production has stagnated, and there is similarly limited potential for expansion.5-7

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Aquaculture potentially presents one of the best opportunities for increasing global animal protein

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production while minimizing resource demands and environmental impacts. Compared to conventional

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terrestrial animal production, cold-blooded organisms reared in aquatic environments typically have

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superior feed conversion efficiencies.8 Global aquaculture production, excluding aquatic plants, increased

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by 1,567% between 1980 and 2014,9 and the sector is expected to grow by an additional 78% over the

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next 15 years.10 However, the growth potential of aquaculture production is dependent on numerous

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factors, including the method of farming, the species farmed and, for fed aquaculture, the specific kinds

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and amounts of feed inputs required.11 Feed price and availability remains one of the critical bottlenecks

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to expanding aquaculture globally. Demand for aquaculture feed is expected to rise from 30 million MT

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in 2008 to around 71 million MT in 2020, as more farms rely on commercial feeds and total aquaculture

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production increases.12

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Feeds used in intensive aquaculture are typically formulated from multiple ingredients to meet the

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nutritional requirements of the culture organism at least cost. While the nutritional profile and suitability

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of feed inputs are clearly essential considerations for the aquaculture sector, so too is the scalability of



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existing and emerging sources – which presents a second critical bottleneck for the expansion of

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aquaculture. Specifically, growth of the aquaculture sector may be limited by: (1) the extent to which the

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availability of feed materials can expand commensurate with increasing demand; (2) the costs of

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production inputs, which is often a function of alternative uses for each ingredient; and (3) the capacity of

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the sector to increase production and sales, while maintaining or increasing profitability and efficiency.

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These issues constitute core challenges for the sector and for global food security.

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As with terrestrial animal production, the resource use and emissions levels characteristic of fed

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aquaculture will depend on species type, production technology and, importantly, the environmental

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performance profile of specific inputs to aquaculture feeds. As of 2014, 69% of all farmed aquatic

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animals were raised with feeds (i.e. not filter feeders or autotrophs).8 Production of marine and

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diadromous finfish, which generally require higher levels of proteins and lipids in feeds, increased by

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169% between 2005 and 2014, to 7.3 million tons. Production of freshwater finfish, which generally

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require fewer protein and lipids, increased by 179% to 42.4 million tons.9 A variety of studies have

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described the importance of aquafeed production in the overall life cycle environmental impacts of fed

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aquaculture.13-20 For example, a study of global salmon aquaculture production found that feed inputs

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account for, on average, 90% of the cradle-to-farm gate impacts of producing farmed salmon.13 At the

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same time, the environmental performance profiles of potential aquafeed inputs – whether of fisheries,

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livestock, or agricultural origin – vary widely.13, 17 In light of the increasing attention being paid to the

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role of food systems, and of animal production in particular, with respect to resource demands and

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environmental change, considerations of the embedded environmental costs of aquaculture feeds will

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likely assume an important role in determining the trajectory of the aquaculture sector globally and may

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hence be considered a third important bottleneck.

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The nutrient profiles of feeds are often described in terms of four main components: energy,

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protein, lipid, and carbohydrate.21 Protein often makes up the largest fraction of aquaculture feeds, and

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increased usage of existing and novel protein sources is critically important in determining future

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increases in global aquaculture production. However, expanded use of protein inputs to aquaculture feeds


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may ultimately be constrained by these bottlenecks, specifically: (1) their substitutability (i.e., how their

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particular nutritional profiles limit the extent to which they might substitute for competing protein inputs);

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(2) their scalability (i.e. the extent to which production of protein inputs can feasibly be increased over

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time to match rising demand; and (3) the resource and environmental implications of their production.

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Moreover, these factors may potentially interact, creating a range of possible synergies or trade-offs.

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Understanding such potential synergies and trade-offs is imperative to inform decision-making in support

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of continued aquaculture development and efficient utilization of feed ingredients across multiple animal

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production sectors.

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Like terrestrial livestock production, aquaculture may source feed inputs from a wide range of

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production systems, including marine fisheries, terrestrial crop and animal agriculture, and others.

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Moreover, feed inputs may be “virgin materials”, co-products of food for human consumption, or

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recycled biomass. Looking forward, the latter may include substantial but currently underutilized sources

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– such as fish processing trimmings that are currently, in some cases, slurried and discharged to local

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waterways.22.

Here, we review a representative subset of important current and emerging protein

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sources for aquaculture feeds in order to illustrate such potential synergies and trade-offs. First, we

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consider soy (a relatively low-input leguminous crop) produced in two major production regions (the US

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and Brazil) that are characterized by differing production conditions and environmental implications. Soy

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is processed into either soybean meal (a low-energy process producing a feed input whose use may be

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constrained by anti-nutritional factors) or soy protein concentrate (an energy-intensive process resulting in

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an output of superior nutritional value). Second, we consider three types of marine protein: (1) Peruvian

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anchoveta meal, which is derived from a large-scale, energy efficient reduction fishery; (2) herring by-

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product meal, derived from a smaller-scale, less energy efficient fishery for human consumption (in this

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case, herring roe); and (3) Antarctic krill meal, which has unique nutritional properties but is derived from

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a comparatively energy-intensive fishery and low-yielding rendering process. We also consider two

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potential protein feed inputs derived from livestock processing materials. These are poultry by-product

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meal, which has high nutritional value, and feather meal, which has comparatively lower nutritional



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value. For both, raw material provision is characterized by non-trivial resource demands and emissions

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due to the inefficiencies inherent to biological feed conversion. The former is also produced via an

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energy-intensive rendering process relative to the latter. Finally, we also consider insect meal – an

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emerging protein source that is oft-touted as a sustainable alternative to animal proteins. For each, we

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evaluate aspects of their nutritional attributes, substitutability and scalability. We also employ Life Cycle

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Assessment (LCA) models (that we created on a methodologically consistent basis from previously

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reported, peer-reviewed studies in order to ensure comparability) to quantitatively assess and describe

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some of the resource utilization and environmental impacts characteristic of the life cycle of each feed

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input considered. On this basis, we discuss how these attributes of each protein source may both interact

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and influence their immediate and future utility as a protein source for aquaculture feeds. We recognize

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that protein provides a somewhat crude (albeit preferable to mass) basis for making comparisons among

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feed inputs, since proteins can differ in nutritional value and be of varying nutritional utility depending on

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what species and at what life stage they are fed. However, in the absence of more refined metrics such as

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Protein Digestibility Corrected Amino Acid Scores or Dietary Indispensable Amino Acid Scores that are

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generalizable across species, we nonetheless believe this provides a reasonable first-order basis for our

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analysis.

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The balance of the manuscript is hence organized into three sections. The first compares and

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contrasts each feed input in terms of its nutritional profile, potential substitutability, and scalability. The

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second describes the varied resource and environmental considerations that may be attributable to the

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different ingredient types, highlighting generalizable insights and underscoring where context-specific

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factors may be determining. The third section, which synthesizes and concludes, provides summary

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recommendations for decision support for feeding future aquaculture production.

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Nutritional Profiles, Substitutability and Scalability

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Protein is required in fish and crustacean diets as a source of amino acids for protein synthesis

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and for gluconeogenesis and metabolic energy.23,

24

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crustaceans is often described as a single value, but the value represents the variety and ratio of up to 22

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different amino acids, ten of which cannot be synthesized by fish and crustaceans and must be acquired

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through dietary sources (for reviews of amino acids and nutrition, see

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protein in an organism’s diet can change as a result of the size of the organism, the profile of amino acids

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in the protein, the bioavailability of amino acids in the protein, and the level of dietary energy in the

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feed.29, 30 There has been an extensive body of research focused on determining the optimal protein and

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amino acid levels for fish growth under common culture conditions.31 Generally, an ideal feed will

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contain similar amino acids as the proteins in the cultured animal.32

The specific requirement for protein in fish and

25-28

). The total requirement for

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Protein sources vary widely in both the amount of crude protein and the type and ratio of amino

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acids they provide.33, 34 Amino acid deficiencies can result in reduced growth and feed utilization.24 Diets

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deficient in specific amino acids have been associated with reduced immune function and increased

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overall susceptibility to disease.29, 30 Deficiencies in individual amino acids can also lead to erosion of the

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dorsal fin (lysine deficiency), spinal deformities (tryptophan, leucine, lysine, arginine or histidine

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deficiencies), or cataracts (methionine, tryptophan, or histidine deficiencies) (as reviewed in

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addition, many plant-based protein sources contain anti-nutritional factors which can interfere with

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utilization of nutrients in a feed and negatively impact the health and growth of an organism.36, 37. In some

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cases, processing of protein ingredients can help increase digestibility, but at added cost.38

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24, 35

). In

Protein ingredients are often among the most expensive components in aquaculture feeds, and farmers have a strong incentive to source the cheapest proteins that satisfy their animal’s nutritional



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needs.35, 39 Traditionally, fishmeal has provided an inexpensive, reliable, and nutritious source of protein

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for aquaculture feeds, but growing demand from aquaculture, other sectors, and human consumption,

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coupled with stagnating or decreasing supply from capture fisheries, has increased fishmeal prices to

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historically high levels.40-42 Many sectors in the aquaculture industry now diversify feed formulations to

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include large amounts of non-fishmeal protein ingredients.33, 43

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For a protein source to be viable for feed use in a range of aquaculture species, it must have

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adequate protein content (48-80%), a suitable amino acid profile, high digestibility, and acceptable

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palatability.44 Additionally, it must have low levels of fiber, starch, non-soluble carbohydrates, and anti-

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nutritional factors that might impair performance.44 A protein source should ideally also be scalable, to

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meet the growing demand from the aquaculture sector.

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The concept of scalability has multiple definitions across sectors and disciplines.45 A quantitative

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analysis of scalability to meet demand from aquaculture feeds would require extensive economic

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modeling, and is outside the scope of this review. Instead, we review and compare key factors that will

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likely influence scalability, including the availability of inputs to production, and the market price of

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protein meals.46 Specifically, we evaluate major inputs to production that could increase production costs

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through either supply or demand dynamics, such as supply constraints, or use in other sectors. The market

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price of each protein source is also considered, including discussion of historical price volatility,

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innovations in production technology, and demand for the protein from other sectors. Given the inherent

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difficult of forecasting future global production frontiers, factors are qualitatively determined to be

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favorable, uncertain, or unfavorable for scalability.

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Fishmeal

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Historically, fishmeal has been the primary protein source in aquaculture feeds. It has a high

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protein content (e.g. 65–72% crude protein), suitable amino acid profile, and numerous trace elements


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that are beneficial for the health of fish and crustaceans. The specific protein content of fishmeal varies

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depending on the species of fish used, and the season and location in which they were caught.47 Fishmeal

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is also highly digestible and palatable, and lacks anti-nutrients that can be toxic or impede growth.44, 48

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Fishmeal is produced by cooking, pressing, drying and milling raw fish or fish parts to produce a

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brown powder.49 Global fishmeal production increased from 1961 to 1985 and has since leveled out, with

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substantial annual and multi-year fluctuations. The primary input to fishmeal is whole fish or fish parts.

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On average, producing one kilogram of fishmeal requires 4.4 – 4.6 kilograms of whole fish.49 There is

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limited capacity to increase fishmeal production, due to limited access to additional fish as raw

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ingredients. Most fisheries for the small, pelagic fish used in fishmeal production (e.g. anchoveta and

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sardines) are either at maximum capacity, or are currently overharvesting.50 Additionally, many small

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pelagic fisheries are prone to dramatic fluctuations in abundance due to cyclical climatic variations every

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2 to 7 years, complicating management.51 Expanding fishmeal production by using additional fish species

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or populations would result in a net loss of available seafood for human consumption52 and would also

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provide only limited additional production, as most fisheries are near, at, or beyond long-term production

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capacity.5 There is some capacity to increase fishmeal production by utilizing fish that are currently

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discarded as bycatch, although doing so may not be economically attractive and can lead to additional

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incentives to overfish.53,

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processing by-products will likely continue to increase in the near-term,55 although the total production

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level is constrained by the total amount of fishery landings and aquaculture production.12

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Additionally, the amount of fishmeal production derived from seafood

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Fishmeal prices increased substantially in the mid-2000’s, and have remained higher than

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terrestrial protein meals.42, 56 Aquaculture used 73% of global fishmeal production in 2010 (competing

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uses included swine, 20%; poultry, 5%; and other sectors, 2%), and use in aquaculture is expected to

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remain constant or increase.49, 57 Due to the limited supply of fish and the increasing demand, fishmeal

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prices are expected to increase through 2025 and beyond, and high prices will continue to incentivize

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many aquaculture enterprises to substitute other types of protein for fishmeal.8 The inputs to production

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and the market price of fishmeal are therefore unfavorable for scalability of fishmeal use in aquaculture.



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We summarize below key attributes of each alternative protein source considered in terms of nutritional

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value, potential substitutability for fishmeal, and scalability.

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Soybean Meal

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Soybean meal, the co-product of oil extraction from soya beans, is the most frequently used non-

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fishmeal protein source in aquaculture, due to its high digestibility, suitable amino acid profile, and low

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price.47 Its performance with carnivorous aquatic species is diminished, relative to fishmeal, due to its

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lower protein content (47% crude protein), and low concentrations of two essential amino acids,

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methionine and lysine.34, 58, 59 Some species of fish also find soybean meal unpalatable without addition of

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other protein meals or attractants.60 In addition, soybean meal contains anti-nutritional factors (e.g.

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protease inhibitors, lectins, phytic acid, saponins, phytoestrogens, antivitamins, and allergens) that can

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lead to reduced gut health and may ultimately be toxic.36, 48, 61 While extensive (>30%) use of soybean

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meal is common in omnivorous species, use in carnivorous species is currently limited (

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