Expanding the utilization of sustainable plant products in aquafeeds: a review

TL;DR: This document reviews various plant feedstuis, which currently are or potentially may be incorporated into aquafeeds to support the sustainable production of various ¢sh species in aquaculture and strategies and techniques to optimize the nutritional composition and limit potentially adverse eiects of bioactive compounds are described.

Abstract: Continued growth and intensi¢cation of aquaculture production depends upon the development of sustainable protein sources to replace ¢sh meal in aquafeeds. This document reviews various plant feedstuis, which currently are or potentially may be incorporated into aquafeeds to support the sustainable production of various ¢sh species in aquaculture. The plant feedstuis considered include oilseeds, legumes and cereal grains, which traditionally have been used as protein or energy concentrates as well as novel products developed through various processing technologies. The nutritional composition of these various feedstuis are considered along with the presence of any bioactive compounds that may positively or negatively aiect the target organism. Lipid composition of these feedstuis is not speci¢cally considered although it is recognized that incorporating lipid supplements in aquafeeds to achieve proper fatty acid pro¢les to meet the metabolic requirements of ¢sh and maximize human health bene¢ts are important aspects. Speci¢c strategies and techniques to optimize the nutritional composition of plant feedstuis and limit potentially adverse eiects of bioactive compounds are also described. Such information will provide a foundation for developing strategic research plans for increasing the use of plant feedstuis in aquaculture to reduce dependence of animal feedstuis and thereby enhance the sustainability of aquaculture.

Summary

Introduction

• Continued growth and intensi¢cation of aquaculture production depends upon the development of sustainable protein sources to replace ¢sh meal in aquafeeds.
• This document reviews various plant feedstu¡s, which currently are or potentially may be incorporated into aquafeeds to support the sustainable production of various ¢sh species in aquaculture.
• The nutritional composition of these various feedstu¡s are considered along with the presence of any bioactive compounds that may positively or negatively a¡ect the target organism.
• As the aquaculture industry continues to expand on a global scale, access to key feedstu¡s, such as ¢sh meal and oil, will become increasingly limited because of a ¢nite wild-harvest resource.
• This programme has increased demand for soybean meal (SBM) for farm-raised ¢sh from almost 0 to an estimated 5 million metric tonnes (mmt) in 2005.

Soybean

• Soybean, Glycinemax Linnaeus, is the leading oilseed crop produced globally and its projected production for 2004^2005 is expected to exceed 200mmt.
• Concentrations of these EAA increase with processing of soy £akes to SPC and SPI and approach or exceed those found in ¢sh meal.
• Due to the processing costs involved, these products are not yet economical for large-scale use in aquafeeds.
• The fatty acids provided by alternative protein feedstu¡s vary considerably and lipid supplements will be the primary source of fatty acids.
• An added concern is the low availability of phosphorus and cationic minerals that are largely unavailable due to their being bound in or by phytic acid.

Barley

• The inclusion of barley in aquafeeds has been limited by several factors.
• Low protein, high ¢bre, b-glucan and phytate contents are important considerations for barley.
• These factors can be accommodated by speci¢c formulations or through use of improved cultivars or products.

Corn

• Production of corn, Zea may Linnaeus, is higher than any other grain or oilseed in the United States, but in contrast to other grains, only a small percentage of annual production is consumed directly by humans.
• Corn oil is the primary food product of corn production and although most corn grown in the United States is fed to livestock as an energy source, an ever increasing amount is going to ethanol production.
• The gluten protein is concentrated, ¢ltered and dried to form corn gluten meal.
• A higher crude protein corn gluten meal would be a more suitable product for use in aquafeeds although the price would be higher than commercially traded corn gluten meal.
• Conventional DDGS contains 28^32% crude protein and is relatively high in ¢bre content, which limits its use in aquafeeds.

Peas/lupins

• Both products are produced in signi¢cant quantities throughout the world.
• The nutrient pro¢le of peas and lupin indicate that that theyhave the potential to replace signi¢cant proportions of ¢sh meal protein in aquafeeds.
• Carbohydrates are the primary component of peas and lupin (Table 3).
• In general, ¢sh do not have the capacity to metabolize NSPs of plant origin (Stickney & Shumway1974; Kuz’mina1996).
• Glencross, Curnow et al. (2003) reported protein ADC values of495% for a range of lupinvarieties by the red sea bream, Pagrus auratus Forster.

Wheat

• Wheat (Triticum aestivum Linnaeus. and T. diccoides, var. durum) is widely produced in the United States and unlike other cereals has at least six large r 2007 TheAuthors 556 Journal Compilationr 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^579 subdivisions of cultivars that are based on end-use properties of the grain.
• Traditional preparations of wheat for diets have utilized £aking (roll milling) of whole grains or pelleting of mill feed and grains.
• Phy- tic acid mutants in wheat can signi¢cantly reduce phytic acid concentration and enhance inorganic phosphorus levels that are nutritionally more readily available in the diet (Guttieri et al. 2004).
• Protein quality in wheat is similar to other cereals with glutamic acid accounting for 30% of total protein weight (FAO1970).
• The remaining mill feed is high in crude ¢bre ( 10%,Martin et al.1976) of limited digestibility for monogastric animals and has a more concentrated phytic acid composition that reaches nearly 0.5% of total weight (Guttieri et al. 2004).

Carbohydrate fractions

• Soybeans are characterized by a high content of NSPs and negligible starch.
• Elevated faecal water content has been reported in salmonids when fed diets with SBM (Olli, Hjelmeland & Krogdahl1994; Refstie, Storebakken & Roem 1998; Storebakken, Kvien, Shearer, Grisdale-Helland, Helland & Berge1998), which probably in part is related to the NSPs content of SBM.
• Soybean meal contains oligosaccharide levels of up to 15% (Russett 2002).
• Most bioactive proteins are easily inactivated by heat treatment that is part of feed production.
• Lectins bind avidly with intestinal glycoproteins on the epithelial surface and interfere with nutrient absorption.

Oestrogenic compounds

• Oestrogenic activity of soybean in ¢shwas suspected based on vitellogenin appearance in male sturgeon fed commercial (animal/plant-based) diets; however, Pelissero, LeMenn and Kaushick (1991) can be credited for the ¢rst direct evidence.
• Pelissero, Bennetau, Babin, LeMenn and Dunogues (1991) extended those ¢ndings by directly examining oestrogenic activity (vitellogenin secretion in juvenile sturgeon) of iso£avones and cumestans by intraperitoneal injections of genistein, daidzein, equol and coumestrol and comparing with oestradiol.
• Iso£avonoids also may a¡ect steroidogenesis regulation and the amounts of circulating hormones by in£uencing sex steroid-binding proteins in plasma.
• Thus, further research is needed to directly compare dietary sources of genistein glycosides and aglycones with respect to hydrolysis, deposition and hepatic metabolism in ¢sh.

Phytic acid

• Asmentioned above, phytic acid is the storage formof phosphorus in all seeds, including grains and oilseeds fromwhich products used in livestock and ¢sh feeds are produced.
• Levels in canola meal average 4.0%, similar to that found in SBM.
• Total phosphorus in canola meal is 11g kg 1, and phytate phosphorus accounts for about 8.3 g kg 1, or about 75% of the total phosphorus in canola meal.
• Treatment with phytase increases total phosphorus digestibilityof canola meal to rainbow trout from 12% to 42% (Cheng & Hardy 2002).

Amino acid limitations

• Soybean protein is well known to be limiting in total sulphur amino acids (TSAA; methionine plus cysteine) when utilized in animal feeds.
• Soybean meal and SPC each contain TSAA at approximately 2.95% of protein.
• DL-methionine supplementation did have a positive e¡ect.
• Supplementation of multiple amino acids to diets containing over 42% extruded SBM also has been demonstrated to alleviate growth retardation in rainbow trout (Yamamoto, Shima, Furuita & Suzuki 2002), whileTakagi, Shimeno, Hosokawa and Ukawa (2001) found that growth retardation in red seabream could be partially overcome when a high level of SPC (52%) was included in the diet.
• Current research also has indicated that taurine may be limiting in all-plant protein diets, even for rainbow trout, which have some capacity to synthesize taurine from cysteine.

Nutrient composition

• The protein content of barley ranges from 9% to15% depending on variety, and also can vary due to environmental conditions.
• For rainbow trout, this level will yield a de¢cit of approximately 0.35% lysine in the diet, which can be overcome by blending protein sources with high lysine contents or adding supplemental lysine.
• Fibre is indigestible to coldwater ¢sh and only increases faecal output.
• Several approaches may improve digestibility of nutrients from barley.
• Kaiser, Bowman, Surber, Blake and Borowski (2004) also noted cultivar di¡erences in digestibility of dry matter, starch and aciddetergent ¢bre utilizing rats as an experimental model.

Erucic acid

• 1, n-9) is a normal constituent of rapeseed oil, and levels in oil from standard varieties of rapeseed range from 20% to 55% of the oil, also known as Erucic acid (C22.
• Erucic acid is valuable for production of industrial lubricants from rapeseed oil, but deleterious in oils used for livestock and ¢sh diets.
• Erucic acid is cardiotoxic, causing cardiac lesions in rats, evenat low levels of1^ 2% of the lipid fraction.
• Varieties of rapeseed have been developed that contain reduced levels of erucic acid, and solvent extraction of rapeseed/canola following mechanical pressing of the seeds reduces the residual amount of erucic acid in canola meal to levels below that required to have pathological e¡ects in ¢sh.

Pigments

• Corn products contain xanthophylls, a group of yellow carotenoid pigments, and pigment levels are concentrated in corn gluten meal compared with the xanthophyll content of ground corn.
• Rainbow trout fed diets containing corn gluten meal deposit xanthophyll pigments in the muscle tissue, resulting in a yellow colour in ¢llets.
• For trout receiving diets lacking supplemental astaxanthin or canthaxanthin, corn gluten meal cannot be used, but in trout fed diets supplemented with these carotenoid pigments to produce red ¢llets, the presence of corn gluten meal in the diet does not a¡ect ¢llet colour.

Lysine limitation

• Lysine is the most limiting indispensable amino acid in wheat for various aquatic species.
• The more complex pre-processing method of air classi¢cationuses air pressure and particle density to separate dense protein particles from the lighter carbohydrate fractions and results in a product with higher nutrient levels (Thiessen, Campbell & Tyler 2003;Thiessen, Campbell & Adelizi 2003).
• Other methods to increase nutrient and decrease antinutrients are also being developed and evaluated (Kim, Flores, Chung & Bechtel 2003).
• In the last decade, genetic manipulations have changed, as have the potential to further improve several speci¢c nutrients in seeds.

Low phytic acid mutations

• Phytic acid is the major form of phosphorus, representing 60^80% of the total phosphorus in mature seeds and is not usable by monogastric animals.
• Low phytic acid (up to 75% reduction in seed) but high free-phosphorus genetic materials have been identi¢ed in barley, maize, wheat, rice and soybean through mutations (Dorsch, Cook,Young, Anderson, Bauman,Volkmann, Murthy & Raboy 2003).
• High lysine genetic materials Lysine is an EAA for animals that is often limiting in plant feedstu¡s.
• More recent studies have found the modi¢er genes of the well-known opaque-2 phenotype in maize.
• Both low and high b-glucan lines may satisfy the needs of direct use and industry processing by-products for aquafeed production.

High-oil cereal crops

• Quantitative trait loci controlling oil content have been identi¢ed in cereal maize in which oil content could approach 20% by selection (Laurie, Chasalow, LeDeaux, McCarroll, Bush, Hauge, Lai, Clark, Rocheford & Dudley 2004).
• Quantitative trait loci identi¢ed in maize may help oil improvement in other cereal crops as well.

Starch-structure manipulation

• The level of di¡erent starch structures such as amylose and amylopectin can be changed according to the requirement of aquafeeds through better understanding of the genes in£uencing starch biosynthetic pathways (Morell & Myers 2005).
• In wheat grain, modi¢cation of starch to lower amylose content to produce amylose-free wheat starch (sometimes called ‘waxy’) is genetically possible through accumulationof threemutant forms of the granule-bound starch synthase gene.
• The ¢rst germplasm lines with amylase-free starch are widely available (Graybosch, Souza & Berzonsky 2003) and the ¢rst commercial amylose-free starch cultivars are now reaching the marketplace.
• Cultivar development in this area is less advanced than the development of cultivars with amylose-free starch.
• Modi¢cations of starch can alter the functional properties and the digestibility of the starch.

Increased micronutrient content

• Genes regulating micronutrients such as antioxidative compounds (like vitamin E) have been identi¢ed in Arabidopsis (Capell & Christou 2004).
• Enhancing utilization by genetic selection of ¢sh Evaluation of genotype by diet interactions in aquaculture species for speci¢c dietary components has only recently begun on a limited basis.
• In other animal systems, the e¡ects of dietary changes on speci¢c physiological parameters have been studied.
• Of greater interest is the determination of whether carnivorous ¢sh that have been evolutionary selected to utilize protein as their main energy source can be selected for improved utilization of plant material.
• With the recent impetus of genomics, and the increasing amount of sequence information available, an improved understanding of cellular signalling, and the role of genes and proteins in pathways, now several research groups are beginning to characterize what is occurring in the animal not only physiologically but also at the cellular and genomic levels.

Optimizing bioactive compounds

• Several plant feedstu¡s contain bioactive compounds that may have positive or negative e¡ects on aquatic animals and thus their concentrations in aquafeeds must be adjusted accordingly.
• Some other reports, r 2007 TheAuthors Journal Compilationr 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^579 569 however, claimed high toxicity of quercetin to the reproductive system of ¢sh upon external exposure (Weber, Kiparissis, Hwang, Niimi, Janz & Metcalfe 2002).
• E¡ects of probiotics, de¢ned as live microbial-feed supplements, on gastrointestinal microbiota have been studied in some ¢sh, but the primary application of microbial manipulations in aquaculture has been to alter the composition of the aquatic medium.
• An overwhelming majority of the studies, particularly those that have included the use of sensory methods to evaluate quality, have focused on salmonids, primarily rainbow trout and Atlantic salmon.
• While numerous studies have evaluated the e¡ects of various alternative plant proteins on ¢sh growth and feed e⁄ciency, relatively few have monitored the dietary in£uence on ¢sh quality.

Enhancing palatability of plant feedstu¡s

• Fish show distinct taste preferences in basic studies of taste and smell.
• Taste preferences in ¢sh show low plasticity (in relation to the diet), appear to be determined genetically and seem to be patroclinous.
• Fish-feeding motivation and various environmental factors like water temperature and pollutants such as heavy metals and low pH water may shift ¢sh taste preferences.
• The fact that palatability is the sum of many dietary characteristics and that there is a strong interaction between taste and nutritional quality should be re£ected in the experimental designs.
• Such interactions have not gained much attention in research so far, either in ¢sh nutrition or in the nutrition of other animals.

Metabolomics

• Metabolomics is the studyof themetabolic pro¢le of a given cell, tissue, £uid, organ or organism at a given point in time.
• The metabolome represents the end products of gene expression.
• The component may well be among the unidenti¢ed compounds.
• Developments in instrumentation and chemical approaches over the last few years have greatly improved.
• This approach can be used interactively to evaluate the composition of these feedstu¡s and fractions with di¡erential levels of antinutrients and to identify speci¢c antinutrients.

Conclusions and recommendations

• On the basis of the information reviewed in this document, speci¢c strategies and a variety of techniques have been identi¢ed to optimize the nutritional composition of plant feedstu¡s and limit potentially adverse e¡ects of bioactive compounds.
• A coordinated research e¡ort needs to be developed through strategic planning to further evaluate and re¢ne various means of improving the nutritional value of plant feedstu¡s for increasing their use in aquaculture.
• Such e¡orts will result in reducing the dependence on animal feedstu¡s and increasing the sustainability of aquaculture.

Figures

Table 2 Grain and oilseed production in the United States

Table 3 Typical composition (as-fed basis) of ¢sh meal and various plant feedstu¡s

Full text

Expanding the utilization of sustainable plant products
in aquafeeds: a review
Delbert M Gatlin III
1
, Frederic T Barrows
2
, Paul Brown
3
, Konrad Dabrowski
4
,T Gibson Gaylord
1
,
Ronald W Hardy
5
,EliotHerman
6
,GongsheHu
7
, —shild Krogdahl
8
,RichardNelson
9
,
Kenneth Overturf
1
, Michael Rust
10
,Wendy Sealey
5
, Denise Skonberg
11
,EdwardJSouza
7
,
David Stone
5
, RichWilson
9
& Eve Wurtele
12
1
Texas A&M University System, College Station,TX, USA
2
USDA/ARS Hagerman Fish Culture Experiment Station, Hagerman, ID, USA
3
Purdue University,West Lafayette, IN, USA
4
The Ohio State University, Columbus, OH, USA
5
Hagerman Fish Culture Experiment Station, Hagerman, ID, USA
6
USDA/ARS ^ Donald Danforth Plant Science Center, St Louis, MO, USA
7
USDA/ARS,Washington, DC, USA
8
Aquaculture Protein Centre, —s, Norway
9
Nelson & Sons, Murray, UT, USA
10
NOAA Northwest Fisheries Science Center, Seattle,WA, USA
11
University of Maine, Orono, ME, USA
12
Iowa State University, Ames, IA, USA
Correspondence: D M Gatl in III, Department of Wildlife and Fisheries Sciences, 2258 TAMUS, College Station, TX 77843-2258, USA.
E-mail: d-gatlin@tamu.edu
Gatlin and Barrows are Chair and Vice-chair, respectively, of the Plant Product s in AquafeedsWorking Group, and coordinated the devel-
opment of this document; al l other authors are listed in alphabetical order.
Abstract
Continued growth and intensi¢cation of aquacult ure
production depends upon the development of sus-
tainable protein sources to replace ¢sh meal in
aquafeeds. This document reviews various plant
feedstu¡s, which currently are or potentially may be
incorporated into aquafeeds to supp ort the sus tain-
able production of various ¢s h species in aquacul-
ture. The plant feedstu¡s considered include
oilseeds, legumes and cereal grains, which tradition-
ally have been used as protein or energy concentrates
as well as novel products developed through various
processing technologies.The nutritional composition
of these various feedstu¡s are considered along with
the presence of any bioactive compounds that may
positively or negatively a¡ect the target organism. Li-
pid composition of t hese feedstu¡s is not speci ¢cally
considered although it is recognized that incorporat-
ing lipid supplements in aquafeeds to achieve proper
fatty acid pro¢ les to meet the metabolic requirements
of ¢sh and maximize human health bene¢ts are im-
portant aspects. Speci¢c strategies and techniques to
optimize the nutritional composition of plant feed-
stu¡s and limit potentially adverse e¡ects of bioactive
compounds are also described. Such information will
provide a foundation for developing strategic re-
search plans for increasing the use of plant feedstu¡s
in aquacu lture to reduce dependence of animal
feedstu¡s and thereby enhance the sustainability of
aquaculture.
Keywords: alternative proteins, susta inable aqua-
feeds, plant protei ns
Introduction/justification for increased
use of plant products in aquaculture
According to the UN Foo d and Agriculture Organiza-
tion, aquaculture is growing more rapidly than all
other animal fo od-production sectors (FAO. State of
world aquaculture 2006). Its contribution to global
supplies of ¢sh, crustaceans and mollusc s increased
from 3.9% of total production by weight in 1970
to 33% in 2005. This growth is at an average
Aquaculture Research, 2007, 38, 551 ^ 579 d oi : 10.1111/ j.1365 -210 9.20 07.01704. x
r 2007 The Authors
Journal Co mpilation r 2007 Blackwell Publishing Ltd
551

compounded rate of 9.2% per year s ince 1970, c om-
pared with only 1.4% for capture ¢sheries and 2.8%
for terrestrial farmed-meat production systems. It i s
remarkable t hat one out of every three ¢sh consumed
in the world is now farm raised.
The expansion of aquaculture production has
been accompanied by rapid growth of aquafeed
production.The challenge facing the aquaculture in-
dustry is to identif y economica lly viable and environ-
mentally friendly alternatives to ¢sh meal and ¢ sh oil
on which many present aquafeeds are largely based.
While the supply of ¢sh meal a nd oil is arguably sus-
tainable, the a nticipated growth in demand interna-
tionally for use in aquafeeds is expected to exceed the
supply in the next decade. Thus, the aquafeeds indus-
try has recognized for many years that viable utiliza-
tion of plant feedstu ¡s formulated in aquafeeds for
the production of cold, cool and war mwater aquatic
species is an esse ntial requireme nt for future devel-
opment of aquaculture. Such plant feedstu¡s must
provide nutritious diets that will e¡ectively grow
aquatic species wit h minimal environme ntal impact
and produce high-qualit y ¢sh £esh to confer human
health bene¢ts in a cost-e¡ective manner. As the
aquaculture industry conti nues to expand on a glo-
bal scale, access to key feedstu¡s, such as ¢sh meal
and oil, will become increasingly limited because of
a ¢nite wild-harvest resource. In addition to con-
cerns about the sustainability o f ¢sheries resources,
other issues including the potential presence of or-
ganic a nd inorganic contaminants in ¢sh meal and
the net e¡ect of dema nd-and-supply economics in
the global market require enhanced e¡orts to thor-
oughly evaluate reasonable alternatives such as var-
ious plant feedstu¡s.
The US soybean industry has identi¢ed the poten-
tial demand for plant protein in aquafeeds as an op-
portunity to increase the use of US soybeans. Since
1995, the United Soybean Board (USB) has funded
market-development activities, primarily in China.
This programme has increased demand for soybean
meal (SBM) for farm-raised ¢sh from almost 0 to an
estimated 5 million metric tonnes (mmt) in 2005. In
2002, USB created a Managed Aquaculture Pro-
gramme, the Soy-in Aquaculture-Initiative (SIA), with
the joint objectives of expanding its marketing initia-
tive and c onducting research on the factors in SBM
that limit its use in salmonids. Nevertheless, there are
still unidenti¢ed biologically active compounds that
limit the amount of SBM and other plant feedstu¡s in
diets of carnivorous species, including most marine
species of commercial importance (existing or poten-
tial) as well as salmonids. For reasons that are not
clear, carnivorous species have limited tolerance to
SBM that ranges from none in juvenile chinook sal-
mon (Oncorhynchus tshawytschaWalbaum) to possibly
somewhat higher in diets for rainbow trout, O. mykiss
Walbaum (Olli & Krogdahl 1994), and Atlantic sal-
mon, Salmo salar L. (Olli, Krogdahl , van dan Ingh &
Bratts 1994; Bverfjord & K rogdahl 1996; K rogdahl,
Bakke-McKellep & Baeverfjord 2003). The salmon
aquaculture industry is clamoring for a stable source
of protein in terms of cost and supply, and such a
supply would bene¢t other established and emerging
sectors of the aquaculture industry as well.
Targeted nutritional and non-nutritional
characteristics (including cost) of plant-
derived feedstuffs for inclusion in
aquafeeds
Fish meal has been the protein source of choice in
aquafeeds for many reasons, including its high pro-
tein content, excellent amino acid pro¢le, high nutr i-
ent digestibility, general lack of antinutrients, relative
low price (until recently) and its wide availability.
Plant-der ived feedstu¡s all have some characterist ics
that place them at a disadvantage to ¢sh meal in
terms of their suitability for use in aquafeeds. How-
ever, demand for protein ingredients is expected to
exceed the annual world supply of ¢sh meal in the
next decade, and this increa sed demand will change
the economic and nutritional paradigms that up to
now have resulted in high use levels of ¢sh meal in
aquafeeds. The plant feedstu¡s considered in this
document include oilseeds, legumes and cereal
grains, which traditionally have been used as protein
or energy concentrates a s well as novel products de-
veloped through various processing technologies. Li-
pid composition of t hese feedstu¡s is not speci ¢cally
considered although it is recognized that incorporat-
ing lipid supplements in aquafeeds to achieve proper
fatty acid pro¢ les to meet the metabolic requirements
of ¢sh and maximize human health bene¢ts are
important aspects.
To be a viable alternative feedstu¡ to ¢sh meal
in aquafeeds, a candidate ingredie nt must possess
certain characteristics, i ncluding wide availability,
competitive price, plus ea se o f handling, shipping,
storage and use in feed production. Furthermore, it
must possess certain nutritional characteristics,
such as low levels of ¢bre, starch, especially non-
soluble carbohydrates and antinutrients, plus have a
Utilization of plant products in aquafeeds D M Gatlin III et al. Aquaculture Research, 2007, 38, 551^ 579
r 2007 The Authors
552 Journal Co mpilation r 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^579

relatively high protein content, favourable am ino acid
pro¢le, high nutrient digestibility and reasonable pa-
latabil ity. Alt hough some plant-derived ingredients,
such as soy protein concentrate (SPC) or wheat glu-
ten, possess most of t hese characteristics, they have
been too expensive relative to the price of ¢sh meal
to be used in most aquafeed s. It is likely that a combi-
nation of plant-derived feed ingredients will be re-
quired to replace ¢ sh meal, and that supplements,
such as amino acids, £avourings and possibly exo-
genous enzymes, will b e needed to produc e aqua-
feeds without ¢sh meal that support growth rates
nec essary for the economic production of farmed
¢sh. Table 1 summarizes the nutrients found in ¢sh
meal (expresse d on an as-fed basis), and the range
of nutrient concentrations that alternative ingredi-
ents should have to be viable alternative s to ¢sh meal.
Various grain and oilseed crops a re grown in the
United States, and their recent production is sum-
marized in Table 2. The gross nutr ient composition
of these and other plant feedstu¡s are presented in
Table 3.
Candidate plant products for increased
use in aquafeeds
Soybean
Soybean, Glycine max Linnaeus, is the leading oils eed
crop produced globally and its projected production
for 2004^2005 is expected to exceed 200 mmt. A
large part of this production is used in the extraction
of oil yielding a cake of high protein quality. This is
processed to yield a wide a rray of soybean products,
such as soy £our, SBM, SPC and soy protein isolate
(SPI) that have been evaluated in ¢sh. Full-fat SBM
(heat-treated whole soybeans) also has been evalu-
ated in ¢sh. Soybean meal has been the predominant
form of soybean used and is available eit her as de-
hulled ( 48% crude protein) or w ith hulls added
( 44% crude protein) (NRC1993).
Soy products are regarded as economical and
nutritious feedstu¡s with high crude protein content
and a reasonably balanced amino acid pro¢le. How-
ever, certain nutritional characteristics and the
presence of several antinutrit ional factors mer it dis-
cussion. Conce ntrations of the 10 essential amino
acids (EAA) and tyrosine are generally lower in SBM
than in ¢sh meal with the exce ption of cystine, which
is present at higher concentrations in SBM. The EAA
of concern a re lysine, methionine a nd threonine that
may be limiting in soy-based diets fed to aquatic ani-
mals. Concentrations of these E AA increase with
processing of soy £akes to SPC and SPI a nd approach
or exceed those found in ¢sh meal. However, due to
the processing costs involved, these products are not
yet economical for large-scale use in aquafeeds.
Crude fat and ash concentrations of solvent-
extracted SBM and other soy products tend to be
lower than those in ¢sh meal, but carbohydrate
concentrations tend to be higher. Lower ash and fat
Table 1 Proximate and nutrient content (as-fed basis) of
¢sh mea l, and targeted ranges in alternative i ngredients
derived from grains and oilsee ds
Category/nutrient
Fish
meal
(menhaden)
Target range
for alternative
ingredients
Crude protein (%) 65–72 48–80
Crude lipid (%) 5–8 2–20
Fibre (%) o2 o6
Ash (%) 7–15 4–8
NFE (%) o1 o20
Starch (%) o1 o20
Non-soluble CHO (%) None o8
Arginine (%) 3.75 43.0
Lysine (%) 4.72 43.5
Methionine (%) 1.75 41.5
Threonine (%) 2.5 42.2
o-3 fatty acids  2%


The fatty acids provided by alternative protein feedstu¡s vary
considerably and lipid supplements will be the primary source
of fatty acids.
Table 2 Grain and oilseed production in the United States
Grai n or
oilseed
Acres
planted
Production
(100 0 bushels)

Metric
tonnes
Barley 3 875000 352 445 7 689 709
Canolaw
Corn 81 759000 9 761 085 248 463 980
Cottonseed 14 195400 7 711 980
Oat 4 246000 114 878 1 667 450
Peanut
Peas/lupinsw 1 657000 4 821 250 2 186 880
Rice 3 384000 223 235 10 125 770
Soybeans 72 375000 2 756 794 75 185 291
Sunflower 2 709000 4 018 355 1 822 700
Wheat 65 871000 2 550 383 69 555 900

A bushel of barley, corn, soybeans and wheat weighs 48, 56, 60
and 60 pounds respect ively.
wProduction of canola, peas and lupins in the United States is
negligible.
Source: USDA Agricultural Statistic s (2005), http://www.nass.
usda.gov.
Aquaculture Research, 2007, 38, 551^579 Utilization of plant products in aquafeeds D M Gatlin III et al.
r 2007 The Authors
Journal Co mpilation r 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^ 579
553

concentrations in soy products can be overcome by
appropriate supple mentation with mineral prem ixes
and lipids, but high concentrations of carbohydrates
remain an area of concern. Carbohydrates in soy-
beans are largely present as oligosaccharides such
as sucrose, ra⁄nose and stachyose. Sucrose is gener-
ally available to aquatic animals, but ra⁄nose and
stachyose are not digestible due to a lack of a-galacto-
sidases that are necessary to metabolize these com-
plex sugars. An added concern is the low availability
of phosphorus and cationic minerals that are largely
unavailable due to t heir being bound in or by phytic
acid.The addition of the enzyme phytase to feeds has
been shown to improve phosphorus and cationic
mineral availability. There are di¡erences in concen-
trations of vitamins between soy products and ¢sh
meal.Vitamin availability data in ¢sh are scarce and
feed s are generally fo rti¢ed with vitamins assuming
minimal availability from feedstu¡s (NRC 1993).
Barley
Barle y, Hordeum vulgare Linnaeus, is grown for multi-
ple purposes including animal feeds, human food,
malting for the production of alcoholic beverages or
inclusion in extracts a nd syrups for adding £avour,
sweetness and colour to a variety of prepared foods.
Barle y is a short-season, early-maturing crop grown
on both irrigated and dry land product ion areas in
the United States, primarily in the Northern Plains
states and in the Paci¢c Northwest. The United States
is the seventh-largest barley-producing country in
the world, but is in the top ¢ve of exporting countries.
Feed barley is included in rations for many animal
sp ecies, but has not been widely used in aquafeeds.
Several factors have limited its use, but improve-
ments in crop ge netics and processing technology
are improving the value of this ingredient for aqua-
feeds. New varieties are available including hull-
less (lower ¢bre) and low phytic acid varieties
(Bregitzer 2005), both of which will help the aquacul-
ture industry decrease nutrients and solids in e¥uent.
Waxy type varieties also are available in which
the ratio of a mylose to amylopectin has been altered.
This may have a positive e¡ect on energy availability,
but also a¡ects the ease of manufacturing. The waxy
barley provides considerable binding capabilities
for feeds produced by cooking extrusion. This is
bene¢cial for the production of high protein and
ene rgy diets, because less carbohydrate is needed for
pel let production (Barrows & Hardy 2001).
While barley contains a good nutrient pro¢le in its
native state, the co-products resulting from the devel-
opment of other products willallow such barleyco-pro -
ducts to be included in higher amounts in aquafeeds.
For example, although corn has been the traditional
source of feed-stock for ethanol production, barley also
shows considerable promise (Hicks, Taylor, Kohout,
Kurantz,Thomas, O Brien, Johnston, Flores, Moreau &
Hoot 2004). In the Northern Plains and Paci¢c North-
west, barley may be the most economical source of
fermentable carbohydrates for ethanol production.
Methods are being developed to concentrate the protein
from barley before fermentation for ethanol production
(Flores, Eustace & Hicks 2004). Owing to the amino
acid pattern and protein content, this protein concen-
trate will be of high value to the aquaculture industry.
Table 3 Typical composition (as-fed basis) of ¢sh meal a nd various plant feedstu¡s
Ingredient
Internatio na l
feed number
Dry matter
(%)
Protein
(%)
Lipid
(%)
Ash
(%)
Lysine
(%)
Methionine
(%)
Cystine
(%)
Fish meal, herring

5-02-000 92.0 72.0 8.4 10.4 5.57 2.08 0.74
Barleyw 4-00-552 88.0 14.9 2.1 2.9 0.44 0.16 0.24
Canola

5-06-145 93.0 38.0 3.8 6.8 2.27 0.70 0.47
Corn

4-02-935 88.0 8.5 3.6 1.3 0.25 0.17 0.22
Corn gluten meal

5-28-242 91.0 60.4 1.8 2.1 1.11 1.63 1.20
Cottonseed meal

5-01-619 92.0 41.7 1.8 6.4 1.89 0.50 0.45
Lupin Lupinus angustifoliusz (whole) 5-27-717 89.0 39.2 10.3 2.8 1.40 0.27 0.51
Field peasz (whole) 5-03-600 89.0 25.6 1.3 3.4 1.50 0.21 0.31
Soybean meal, de-hulled

5-04-612 90.0 48.5 0.9 5.8 3.08 0.68 0.75
Soy protein concentratew 90.0 64.0 3.0 1.5 4.20 0.90 1.00
Wheat

4-05-268 88.0 12.9 1.7 1.6 0.36 0.21 0.27

Data f rom NRC (1993).
wData from NRC (1998).
zData from Allan et al. (2000).
Utilization of plant products in aquafeeds D M Gatlin III et al. Aquaculture Research, 2007, 38, 551^ 579
r 2007 The Authors
554 Journal Co mpilation r 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^579

Barle y also contains high levels of b-glucans,
which have been shown to have strong health
bene¢ts (Lupton, Robinson & Morin 1994; Jenkins,
Kendall, Vu ksan, Vidgen, Parker, Faulkner, Mehling,
Garsetti,Testolin, Cunnane, Ryan & Corey 2002). Ba r-
ley can be consumed directly to obtain these bene¢ts,
but b-glucans are being e xtracte d, puri¢ed and man-
ufactured into pill s for the nutritional-supplement
industry. This process, like ethanol produc tion, will
result in a protein concentrate as a co-product with
high nutritional value.
Canola
Canola, Brassica rapa Linnaeus, is produced from cul-
tivars of rapeseed that have been bred to contain low
levels of erucic acid and g lucosinolates, a g roup of
antinutrients that interfere with normal thyroid
function. Canola seed is an oilseed, and canola oil is
the primary product o f its cultivation. After oil is ex-
tracted and the solvent removed, the resulting meal
(10% moisture) c ontains about 3.5% residual oil,
35% c rude protein, 6% ash and 12% crude ¢bre on
an ‘as-is’ bas is. It also contains about 4% phytic acid
and15 mmol of glucosinolates g
1
. The price of cano-
la meal is l inked to that of SBM, and re£ects the pro-
tein content of the meal. Canola meal is not widely
used in aquafeeds in the United States as it is not
widelyavailable, but is used in Canadian aquafeeds.
Canola meal can be further processed to produce a
protein isolate, called canola protein concentrate
(CPC). Canola protei n concentrate has be en widely
tes ted as a protein source for salmonids and other
carnivorous sp ecies of farmed ¢sh. As the primary
protein source in aquafeeds for salmon and trout,
CPC supports growth rates similar to those of ¢sh
fed ¢sh meal-based diets, as long as amino acid sup-
plements are used to overcome l imiting amino acid
levels and providing feeding stimulants, such as be-
taine, are added to the diet to overcome reduced in-
take. Canola protein concentrate has a prote in
content similar to high-quality ¢sh meal. At present,
CPC is not widely available for use in aquafeeds, and
market price s have not bee n established.
Corn
Production of corn, Zeamay Linnaeus, is higher than
any other grain or oilseed in the United States, but in
contrast to other grai ns, only a small percentage of
annual production is consumed directly by humans.
Corn oil is the primary food product of corn produc-
tion and although most corn grown in the United
States is fed to livestock as an energy source, an ever
increasing amount is going to ethanol production.
Corn starch is used to produce over 400 products,
including ethanol, paper coatings and corn sy rup,
a widely used sweetener in foods and beverages.
In the wet-milling process, the corn kernel is sepa-
rated into its main components, bran/¢bre, germ, glu-
ten and starch. The oil is separated from the germ and
the remaining corn germ meal is used as an ingredi-
ent or added to corn gluten feed.The gluten protein is
concentrated, ¢ltered and d ried to form corn g luten
meal.The commonly traded corn gluten meal is guar-
anteed to contain a minimum of 60% protei n on an
‘as-is’ basis. Re¢ned and puri¢ed corn gluten protein
can have a crude protein content of 70^73% crude
protein, but there are limits i n the commercial pro-
duction proce ss so these levels cannot always be met.
A higher crude protein corn gluten meal would be a
more suitable product for use in aquafeeds although
the price would be higher than commercially traded
corn gluten meal. Economic and marketing analysis
is required to determine if the production of a high-
protein corn gluten meal is warranted.
Corn gluten meal is currently widely used in aqua-
feeds for salmon and several marine species such a s
European sea bass, Dicentrarchus labrax Linnaeus
and gilthead sea bream, Sparus aurata Linnaeus.
Corn gluten meal protein is highly digestible, but de-
¢cient in the EAA lysine. This characteristic and its
cr ude protein content result in upper inclusion limits
of 20^25% of diet for corn gluten meal in aquafeeds
for salmon and marine ¢sh. Generally, use levels are
in the10^ 15% range.
Corn distille rs dried grains with solubles (DDGS) is
the ending co-product of ethanol production. Con-
ventional DDGS contains 28^32% crude protein and
is relatively high in ¢bre content, which limits its
use in aquafeeds. Ethanol production is expected to
increase substantially in the United States, and
research is underway to explore the possibility of
removing protein and ¢bre from starch before using
the starch to produce ethanol. If this approach
becomes widespread, co rn protein concentrate may
become more readily available for us e in aquafeeds.
Cottonseed
Cottons eed, Gossypium hirsute Linnaeus, is the third
leading legume seed by weight (afte r soybean and
rapeseed) used worldwide. Ow ing to its high protein
Aquaculture Research, 2007, 38, 551^579 Utilization of plant products in aquafeeds D M Gatlin III et al.
r 2007 The Authors
Journal Co mpilation r 2007 Blackwell Publishing Ltd, Aquaculture Research, 38, 551^ 579
555

Frequently asked questions

Q1. What are the contributions in "Expanding the utilization of sustainable plant products in aquafeeds: a review" ?

This document reviews various plant feedstu¡s, which currently are or potentially may be incorporated into aquafeeds to support the sustainable production of various ¢sh species in aquaculture. Speci¢c strategies and techniques to optimize the nutritional composition of plant feedstu¡s and limit potentiallyadverse e¡ects of bioactive compounds are also described. 

Q2. What is the role of lectins in the nutrient availability of soybeans?

Lectins possess the ability to bind reversibly and speci¢cally to carbohydrates and glycoconjugates, which is responsible for their numerous physiological e¡ects. 

Q3. What is the common type of corn starch?

Corn starch is used to produce over 400 products, including ethanol, paper coatings and corn syrup, awidely used sweetener in foods and beverages. 

Q4. What species of fish will be used in future work?

Future work requiring genomic information will focus on the current most highly characterized species such as Atlantic salmon, channel cat¢sh and rainbow trout and may incorporate information gained from other highly developed research species such as zebra¢sh, Brachydanio rerio, fugu ¢sh,Takifugu £avidus and medaka. 

Q5. What is the common method of separating wheat from other seed components?

A rapidly increasing use of wheat in Europe and North America is cereal fractionation, the separation of vital wheat gluten from other seed components and further decomposition into starch, soluble ¢bre and oil. 

Q6. What is the main reason why soy is regarded as a nutritious feed?

Soy products are regarded as economical and nutritious feedstu¡s with high crude protein content and a reasonably balanced amino acid pro¢le. 

Q7. How many mg of quercetin was measured in three different cottonseed preparations?

a common £avonoid in plants, was measured at concentrations from 1320 to 1560mg kg 1 in three di¡erent cottonseed preparations (Lee et al. 2002). 

Q8. What are the expensive products for aquafeeds?

Pro-tein concentrates and isolates from wheat, soy and canola are commercially available, but are currently relatively expensive for use in aquafeeds. 

Q9. What is the potential for the availability of wheat fractions?

The availability of wheat fractions could increase the £exibilityof formulations for aquaculture, particularly for feed mills and aquaculture areas proximal to grain fractionation facilities. 

Q10. What could be done to determine the composition of the antifeedant fractions?

Antifeedant fractions could be further fractionated and the resultant fractions tested for antinutrient activity and metabolic composition. 

Q11. What is the way to evaluate the health benets of ino-3 ?

Given that consumers are becoming more interested in the health bene¢ts of these fatty acids, future research should include evaluating the e¡ects of ¢nishing diets rich ino-3 fattyacids on fattyacid pro¢le and sensory quality of the ¢llets. 

Q12. How much less ecacious is oestradiol in st?

when evaluated as relative a⁄nity to oestrogen receptors, i.e. displacing 50% of radiolabelled oestradiol, oestradiol glucuronide was 103 less e⁄cacious in case of rainbow trout hepatic nuclear extract, and 1.5 103 less e⁄cacious in case of sturgeon preparations (Latonnelle, Fostier, LeMenn & BennetauPelissero 2002). 

Q13. What is the reason for the lower nutrient availability of standard SBM?

It is likely that the remaining inhibitors in concert with the indigestible heat-damaged protein are signi¢cant factors for explaining the generally lower nutrient availability of standard SBM and increased requirements for sulphur-containing amino acids often recognized in animals fed SBM (Drackley 2000).