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One Earth
Review
The Future of Aquatic Protein: Implications
for Protein Sources in Aquaculture Diets
Katheline Hua,
1,2
Jennifer M. Cobcroft,
2
Andrew Cole,
2,3
Kelly Condon,
2
Dean R. Jerry,
1,2,4
Arnold Mangott,
2
Christina Praeger,
2,3
Matthew J. Vucko,
2,3
Chaoshu Zeng,
2
Kyall Zenger,
2,4
and Jan M. Strugnell
2,5,
*
1
Tropical Futures Institute, James Cook University, Singapore, Singapore
2
Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, QLD 4810, Australia
3
MACRO – Centre for Macroalgal Resources and Biotechnology, James Cook University, Townsville, QLD 4810, Australia
4
ARC Research Hub for Advanced Prawn Breeding, Townsville, QLD 4810, Australia
5
Twitter: @janstrugnell
*Correspondence: jan.strugnell@jcu.edu.au
https://doi.org/10.1016/j.oneear.2019.10.018
Approximately 70% of the aquatic-based production of animals is fed aquaculture, whereby animals are pro-
vided with high-protein aquafeeds. Currently, aquafeeds are reliant on fish meal and fish oil sourced from
wild-captured forage fish. However, increasing use of forage fish is unsustainable and, because an additional
37.4 million tons of aquafeeds will be required by 2025, alternative protein sources are needed. Beyond plant-
based ingredients, fishery and aquaculture byproducts and insect meals have the greatest potential to sup-
ply the protein required by aquafeeds over the next 10–20 years. Food waste also has potential through the
biotransformation and/or bioconversion of raw waste materials, whereas microbial and macroalgal biomass
have limitations regarding their scalability and protein content, respectively. In this review, we describe the
considerable scope for improved efficiency in fed aquaculture and discuss the development and optimiza-
tion of alternative protein sources for aquafeeds to ensure a socially and environmentally sustainable future
for the aquaculture industry.
Introduction
The growth of the human population leading into the middle of
the 21st century poses significant challenges to the supply of
high-quality, nutrient-rich food whereby a population of 9.7
billion by 2050
1
will require an increase in the supply of food by
25%–70%.
2
This is all in the face of a deteriorating natural
resource base and competing interests for agriculturally based
input commodities.
3
Concurrent with population growth is the
‘‘rise of the middle class,’’ whereby increased affluence (mainly
in China and southeast Asia) comes with a shift to diets that
incorporate an increasing proportion of protein from animal sour-
ces.
4–6
Although livestock food sectors are intensifying produc-
tion in an attempt to meet demand, this comes with significant
challenges including overgrazing, water shortages, and loss of
natural biodiversity.
3,7,8
It is now recognized that the farming of
aquatic species (i.e., aquaculture) will provide an increasingly
significant component of the global animal-derived protein
budget. In fact, aquaculture has been the fastest growing food
production sector by annual growth rate over the last three de-
cades, with annualized growth rates of 10% in the 1990s and
5.8% yearly between 2000 and 2016.
9
On an edible animal-
source food basis, sector growth is second only to poultry.
10
Aquaculture production can be classified as ‘‘unfed’’ or ‘‘fed.’’
Unfed aquaculture relies on supplying animals (e.g., filter-feeders
such as silver carp, grass carp, and bivalves) with food from the
production ecosystem itself.
11
Fed aquaculture is the largest
and fastest growing component of the sector (excluding sea-
weeds) and usually involves supplying animals with formulated
aquafeeds or whole or processed fish. The diets of fed species
have historically relied on high concentrations of fish meal (protein
source) and fish oil (lipid source, typically rich in long-chain poly-
unsaturated fatty acids of the omega-3 series) derived from the
capture of small pelagic fish, known as forage fish (Box 1). Unfor-
tunately, the rapid rise of aquaculture has placed a significant
amount of pressure on forage fish stocks,
12
whereby a peak in
the wild fisheries production volume was reached in 1995 fol-
lowed by a consistent decline.
13
At the same time, global fish con-
sumption is increasing at a rate of 1.5% per year on a per capita
basis and wild fisheries currently are static.
9
This raises concerns
regarding the disruption of aquatic food webs andthe sustainabil-
ity of supply of this global commodity, whereby about 10% of fish
biomass caught from wild-capture fisheries is used to feed high-
value, and often carnivorous, species.
9
High-value product is
commonly exported to affluent countries, reflected in the value
of seafood trade between global regions (Figure 1). However,
the estimated domestic consumption of aquaculture production
volume in 2011 was 85%–89% among the top ten aquaculture-
producing countries (representing 87% of global aquaculture pro-
duction, 51% of the total population, and 52% of the undernour-
ished population),
14
highlighting the importance of aquaculture
(unfed and fed) for the provision of protein for human consump-
tion (Figure 1). As such, the future expansion of the aquaculture
industry is critical for sustained human nutrition, and a balance
between the expanding production of resource-intensive carniv-
orous species and the continued production of high-yielding,
low-value species (e.g., herbivores or detritivores) that support
local communities is required
15
(Figures 1 and 2).
Although the production of fish meal and fish oil from forage
fish has been steadily decreasing over the last 20 years and
the proportion of these ingredients within aquafeeds is demon-
strating a downward trend, they are still important feed compo-
nents for many carnivorous fishes and crustaceans.
26
The total
316 One Earth 1, November 22, 2019 ª2019 The Author(s). Published by Elsevier Inc.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
annual production of fish meal was 4.5 million tons, and the to-
tal annual production of fish oil s 0.9 million tons in 2016, of
which 69% and 75%, respectively, are used in aquafeeds.
20
An additional 23% and 5% of this fish meal is used in pig and
chicken feeds.
20
Notably, the total production of aquafeeds for
all aquaculture species is predicted to increase by 75% from
49.7 million tons in 2015 to 87.1 million tons in 2025
11
(Figure 2).
The volume of wild-caught forage fish required for this increase is
unattainable based on current feed formulations, while uncer-
tainty of future access to this resource is a key issue. The avail-
ability of sustainably fished small pelagics for fish meal and oil
has not increased in 24 years,
13
and their inclusion levels in
aquafeeds must be decreased at a greater rate for aquaculture
to provide an increasingly large proportion of healthy seafood
to an expanding global population. A variety of plant protein in-
gredients (e.g., soybean meal, corn gluten meal, rapeseed
meal) and animal byproducts (e.g., meat and bone meal, poultry
meal) are being used as alternative protein sources to fish meal in
aquafeeds. While these terrestrial, plant-based proteins (e.g.,
soy concentrate) will continue to be important components of
aquafeeds, they have significant limitations, often containing
anti-nutritional elements, and the industry itself has limited po-
tential to expand production without putting additional stress
on land, water, and phosphorous resources.
27
As such, to
meet the demand of the additional 37.4 million tons of aquafeeds
required by 2025, finding alternative, cost-effective sources of
protein is critical. In this review we consider emerging, alternative
feed ingredients to replace the protein provided by forage fish
and highlight the opportunities and challenges to their imple-
mentation. We also suggest areas for improved efficiencies in
aquaculture through breeding and disease resistance and sug-
gest future directions to support the rapid and sustainable
growth of the aquaculture industry.
Fishery and Aquaculture Byproducts
Fishery and aquaculture byproducts are the raw materials that
remain after the industrial-scale processing of fish for human
consumption. After processing, between 50% and 70% of the
byproducts are considered ‘‘inedible’’ and typically consist of
trimmings (i.e., viscera, heads, skin, bones, and blood).
28
This
inedible portion is increasingly being considered as a practical
option to replace the use of fish meal from reduction fisheries
(i.e., wild-catch specifically caught for producing fish meal) in
aquafeeds.
28–30
Currently, around 20% of the global production
of fish meal is supplied through the use of fishery byprod-
ucts.
9,31,32
Conversely, about 10% of the global production of
fish meal is supplied through the use of aquaculture byprod-
ucts.
9,31,32
The continual growth and intensification of the aqua-
culture industry therefore provides an opportunity to develop the
processing capacity of aquaculture to intercept additional by-
products and increase the proportion used for fish meal. This
would also result in additional advantages including increasing
perceived environmental sustainability of the industry, providing
economic and social benefits through the valorization of waste
products and creating downstream processing jobs, which will
ultimately contribute to the long-term sustainability of fed aqua-
culture.
28
The nutrient content of fish meal depends on the type of raw
materials and manufacturing processes used in its production.
In general, high-quality fish meal produced using whole fish con-
tains 66%–74% crude protein, 8%–11% crude lipids, and <12%
ash.
33
In contrast, fish meal produced from byproducts contains
52%–67% crude protein, 7%–14% crude lipids, and 12%–23%
ash. For example, white fish meal produced from byproducts
contains 60%–67% crude protein, 7%–11% crude lipids, and
21%–23% ash,
18,34
and tuna fish meal produced from byprod-
ucts contains 57%–60% crude protein, 8%–14% fat, and
12%–21% ash.
35–38
The lower protein content and higher ash
content in byproduct fish meals are not unexpected, as the
nutrient composition differs between whole fish, fillets, and other
parts of the body (viscera, heads, skin, bones, and blood). The
different proportions of various byproducts that are used to pro-
duce fish meal will therefore also contribute to the nutrient vari-
ability of the fish meal made from byproducts.
Box 1. Components of Aquafeeds beyond Dietary Protein
Fish are valuable sources of nutrients and micronutrients, and play an important role in human nutrition and the global food
supply.
9,16,17
In addition to being a rich source of high-quality protein and essential amino acids, fish are a dietary source of
health-promoting omega-3 or n-3 long-chain polyunsaturated fatty acids (LC-PUFA), eicosapentaenoic acid (EPA) and docosa-
hexaenoic acid (DHA), essential minerals (calcium, phosphorus, zinc, iron, selenium, and iodine), and vitamins (A, B, and D).
9
Even with increased prevalence of alternative ingredients in aquafeeds, fish products from aquaculture must continue to maintain
the levels of these fatty acids and micronutrients for healthy and nutritious human diets.
9,18
Modern aquafeeds are a sophisticated, engineered mix of ingredients (raw materials) that provide the nutritional requirements that
facilitate the intensive and efficient production of aquaculture species. These raw ingredients include commodity meals, oils, vi-
tamins, pigments, minerals, and concentrates, which, when combined, satisfy an organism’s demand for macronutrients and mi-
cronutrients. In addition, these ingredients ensure rapid rates of growth, support animal health, and, importantly, result in a product
with sensory and quality properties that meet consumer demands.
Traditionally, forage fish have been the foundation ingredient of aquafeeds, as they contain high-quality protein, micronutrients,
and lipids, and are an important source of LC-PUFA. In addition to finding alternative sources of protein to alleviate the pressure
on forage fish, we recognize that alternative sources of micronutrients and lipids will be essential.
18,19
Fish-oil use in aquaculture is
projected to increase by 14% due to the growing demand in the marine finfish and crustacean aquaculture sectors as they
expand.
9,20,21
As such, global fish-oil supply is one of the limiting factors for the aquaculture feed industry.
18,19,22
Alternative lipid
sources to fish oil include vegetable oils, animal fats, single-cell oils, algae oils, transgenic oils, and fish byproduct oil.
18,22
How-
ever, discussions of alternative lipid and micronutrient sources are beyond the scope of this review.
One Earth 1, November 22, 2019 317
One Earth
Review
Despite this, fish meal derived from fishery and aquaculture
byproducts has been successfully used in aquafeeds, and its
use is common practice in some countries.
9,12,31,32
Research
on the nutritive values of byproduct fish meals has demonstrated
their good potential as alternative raw materials. Fish meal from
tuna byproducts can substitute 25%–30% of the protein from
premium-grade fish meal without affecting the growth perfor-
mance of spotted rose snapper (Lutjanus guttatus) when
included at a rate of 15.8%–21.4%.
37
For olive flounder (Para-
lichthys olivaceus), 30% of fish meal could be substituted by
tuna byproduct meal at a dietary inclusion rate of 21%.
38
For
Korean rockfish (Sebastes schlegeli), 75% of fish meal could
be substituted by tuna byproduct meal at a dietary inclusion
rate of 58.1%, without compromising growth and feed utiliza-
tion.
39
The less than ideal nutritional profile of byproduct fish
meals presents challenges in the complete replacement of
high-quality fish meal. Nevertheless, byproduct fish meal is still
a viable alternative to conventional fish meal, and, more impor-
tantly, is a more economical and sustainable protein source.
39
The industrial-scale production of fish meal and fish oil in-
volves considerable capital investment and running costs,
19
while prolonged economic efficiency requires a constant supply
of raw materials in large volumes. These factors present signifi-
cant challenges when it comes to byproducts,
32,40
and it can
be economically unjustifiable when raw materials need to be
collected from fish-processing plants located in remote areas
or when only small daily quantities are produced.
28,30,40
As
such, fully benefiting from the use of byproducts will require a co-
ordinated strategy to ensure that suitable facility infrastructures
are available, that economies of scale can be achieved, and
that transport networks are available—three factors that
currently limit the use of aquaculture byproducts in some coun-
tries.
28
Regardless, the rising prices of fish meal and fish oil com-
bined with positive consumer perception of byproducts will in-
crease their viability. At present 7.5 million tons of byproducts
are processed for the production of fish meal and fish oil, and
it is estimated that an additional 11.7 million tons of byproducts
are wasted.
32
Since capture fisheries production and aquacul-
ture production are projected to reach 91 and 109 million tons
in 2030,
9
respectively, there is enormous potential to increase
the production volume of fish meal and fish oil from byproducts.
Food Waste
Food loss and food waste is estimated to be 1.3 billion tons per
annum globally, accounting for 30% of all food produced.
41
Ac-
cording to the Food and Agriculture Organization of the United
Nations (FAO),
41
food loss is defined as any food lost in the sup-
ply chain and food waste is defined as discarded food items fit
for human consumption. The share of food waste in municipal
solid wastes can be >50% in some larger cities.
42
Since food wastes can be generated from various sources,
their nutrient composition also varies considerably. The main nu-
trients in food wastes are proteins from fishmongers, carbohy-
drates from greengrocers, and fats from butchers, whereas the
AMERICAS
AFRICA
OCEANIA
CHINA
ASIA
(exc. China)
EUROPE
LEGEND
Total value
0-10%
11-20%
21-30%
> 31% 3.5 4.5 5.5 6.5 7.5 8.5 9.5
% fish / total protein
wild-capture production
aquaculture production
pie chart scaled to
total production
Figure 1. Aquaculture and Wild-Capture Fishery Production in Global Regions and Value of Seafood Flows
Production volume from global regions (pie charts) demonstrating the value of export flows (l ines with arrows represent the percentage of the total value exported
from each region), and the contribution of fish to human protein consumption (percentage of fish in total protein represented by each region’s color). Data
sources: aquaculture and wild-capture fishery production;
9,23
export flows;
23
and human consumption of protein from fish.
23,24
318 One Earth 1, November 22, 2019
One Earth
Review
nutrients in household and restaurant wastes are mixed.
43
The
crude fat and carbohydrate content in mixed food wastes can
vary between 7%–12% and 52%–68%, respectively.
44
While
the crude protein level can vary from 3% to 38% depending on
the type of food waste, it is possible to reduce this variation to
20%–26% by industrial processing.
44
Food wastes have been used by some countries (e.g., China)
in freshwater polyculture systems, but are not widely used within
aquaculture feed pellets.
42
The growth performance of the fish is
highly dependent on the species being cultured and the type of
food waste being used. Pellets containing 70% sorted food
waste can support adequate growth of low-trophic-level fish,
including grass carp (Ctenopharyngodon idella), bighead carp
(Hypophthalmichthys nobilis), and mud carp (Cirrhinus molitor-
ella),
45,46
but have also resulted in reduced growth performance
in grass carp.
47
Similarly, pellets with 36.5% and 73%
kitchen wastes result in significantly lower weight gain in tilapia
(Oreochromis niloticus 3Oreochromis aurea) and giant grouper
(Epinephelus lanceolatus), respectively, compared with fish meal
controls.
48
The inclusion of kitchen waste at rates of %20% in
the feed of orange-spotted grouper (Epinephelus coioides) can
support adequate growth compared with a fish meal control
diet, whereas inclusion rates of 30% or 40% results in reduced
growth.
48
There are a number of challenges when using food wastes in
aquaculture feeds. Food wastes are high in moisture and are
perishable, and microorganisms or pathogens may be present,
which can be a health and safety concern.
42,49
Plant-based
wastes can also contain anti-nutritional elements.
42
Initial waste
separation can also be difficult, in terms of not only separating
different types of food wastes but also separating from wastes
other than food wastes, which results in high variability in nutrient
composition as well as contamination. These problems can be
mitigated through the sterilization of pathogens,
42,49
by using
feed additives (e.g., enzymes) to enhance nutritive values, or
even by improving the collection infrastructure of food waste to
Millions of tonnes
2015
2025
% fish meal of diet
marine shrimps
(820)
marine fishes
(672)
salmons
(635)
fed carp
(135)
freshwater
crustaceans
(265)
trouts
(230)
catfishes
(165)
tilapia
(184)
eels
(133)
milkfish
(32) 12% 18%
16% 1%
16%
3%
2%
38%
3%
other freshwater
and diadromous fishes
(232)
0
5
10
15
20
12%
12%
Figure 2. Projected Demand for Fish Meal in
Fed-Aquaculture Diets
The estimated aquafeed volume demand (millions
of tons) of the major fed-aquaculture species
groups in 2015 and 2025, and the use of fish meal in
the diet of each group in 2015 (represented by the
blue portion of each animal). The values (percent-
age) inside each species group symbol are the
estimated fish meal inclusion in 2015. The values in
brackets beside each species group symbol are the
estimated volume of fish meal included in the diets
in 2015 (thousands of tons). Data sources: fish meal
proportion in diets in 2015;
25
estimated aquafeed
volume demand.
11
increase separation and traceability. Alter-
natively, instead of using food wastes
directly, there are additional options
including bioconversion and biotransfor-
mation. Bioconversion uses the food
waste as a nutrient source for insects
and/or algae, which can subsequently be
used as a feed resource;
42,46
while
biotransformation uses food waste as a
nutrient source for microorganisms through solid-state fermen-
tation
42
with the same objective (see Insects and Microbial
Biomass below).
The use of food wastes in animal feed is well accepted and
regulated in many Asian countries, but elsewhere there exists
negative stereotypes of using waste as a feed source.
49
Regula-
tory barriers also exist in some countries (e.g., the European
Union), and food losses rather than food wastes may be more
acceptable as feed ingredients.
42,50
Although further economic
analyses are required to determine the feasibility of using food
losses in animal feed, it may prove suitable for lower-trophic-
level freshwater fish due to their low requirements of protein
and the low protein content in food wastes.
Insects
Production of insects as a protein feed input to aquafeeds does
not compete with human food sources or human food produc-
tion. Insects have short life cycles and can grow on a wide range
of substrates with high productivity and high feed conversion
factors.
51,52
Combined with relatively good nutritional profiles,
the potential of insect meal as a suitable aquafeed ingredient is
receiving increasing attention in many countries. The European
Union approved processed animal protein from insects (i.e., in-
sect meals) to be used in aquafeed in Regulation (EU) 2017/
893 from July 2017. There are seven approved insect species,
which must be raised with feed-grade substrates. Although all
of these species are considered non-pathogenic, non-vectors
of pathogens, and non-invasive,
53
research has mostly focused
on the black soldier fly (Hermetia illucens), the common housefly
(Musca domestica), and the yellow mealworm (Tenebrio molitor).
The crude protein level in most insects ranges from 40% to 63%;
however, defatted insect meal can contain up to 83% crude pro-
tein.
54
The amino acid profiles are taxon dependent and vary
with species, with the Diptera group (true flies) demonstrating
similar profiles to that of fish meal.
55–57
The crude lipid content
of insects ranges from 8.5% to 36%, while the fatty acids profiles
One Earth 1, November 22, 2019 319
One Earth
Review
are variable and dependent on developmental stage and the
substrates used as a nutrient source.
55,57
Insects contain negli-
gible amounts of eicosapentaenoic acid (EPA) and docosahexa-
enoic acid (DHA), lower levels of omega-3, and higher levels of
omega-6 fatty acids compared with fish meal. Lipid quality can
be manipulated by the substrates used to raise the insects,
and it is possible to enrich the EPA and DHA content by feeding
insects with fish offal;
58
however, this might be economically less
advantageous than feeding fish byproducts directly to fish.
57
Vitamin and mineral content are also highly dependent on sub-
strate type.
57
Insects are low in carbohydrates (<20%), which
are mostly in the form of chitin, a polymer of glucosamine
55–57
generally considered as anti-nutritional, that fish cannot digest.
59
However, there has been research demonstrating that low levels
of chitin could act as an immunostimulant.
57
Most studies that replace fish meal with insect meal recom-
mended partial replacement (reviewed by Tran et al.
56
and Henry
et al.
57
). However, an increasing number of recent studies are re-
porting that a 100% replacement of fish meal can be successful,
even for carnivorous fish. For example, in Atlantic salmon (Salmo
salar), insect meal produced using black soldier fly larvae re-
placed 100% of the fish meal at a dietary inclusion rate of
14.75%.
60
Insect meal produced using yellow mealworm at
graded levels from 5% to 25% improved the growth perfor-
mance of rainbow trout (Oncorhynchus mykiss) and achieved a
100% replacement of fish meal
61
(Figure 3A). Similar observa-
tions were made with red sea bream (Pagrus major) using insect
meal produced using defatted yellow mealworm larvae, whereby
inclusion rates of 25%–65% improved growth performance and
disease resistance.
62
Conflicting results exist regarding the ef-
fects of insect meal on sensory attributes of fish fillets in the liter-
ature. Insect meal was reported to affect sensory profile of the
fillets of Atlantic salmon
60
and rainbow trout,
63
but other studies
did not observe any sensory differences in Atlantic salmon,
64
rainbow trout,
58
or common carp.
65
Challenges of incorporating insect meal into aquaculture feeds
include the variable and sometimes less ideal nutritional pro-
files.
55,56
Moreover, insect meal is currently not a price-compet-
itive raw material for aquafeeds.
52
Economic analysis with the
case of European sea bass (Dicentrarchus labrax) demonstrated
fish oil
11.5%
other marine 8%
other 4.6% other marine 8%
other 7%
fish oil 5.6% fish oil 4.5%
other 5.4% other 6%
other marine 5% other marine 5%
fish meal 4.3%
fish oil
1.4%
fish oil 2.1% animal byproducts 5%
animal byproducts 5%
other 9.6% other 10.3%
Animal by−products
Fish meal
Fish oil
Novel ingredient
Other ingredients
Other marine ingredients
Plant ingredients
Rainbow trout
(Oncorhynchus mykiss)
White shrimp
(Litopenaeus vannamei)
European sea bass
(Dicentrarchus labrax)
Control Diet replacement
27.5% 15% 18% 51.5%56.5%
13%
71% 58.2%20%
25% 25%11% 51% 48.5%
A
B
C
Figure 3. Case Studies of Fish Meal Replacement in the Diets for Fed-Aquaculture Species
The complete or partial replacement of fish meal using alternative protein sources demonstrated equivalent or higher growth in the animals than the control fish
meal diets. Shading represents the proportion of dietary ingredients.
(A) Rainbow trout (Oncorhynchus mykiss) were fed a control diet with 25% fish meal or an experimental diet with 25% yellow mealworm protein meal.
61
(B) Pacific white shrimp (Litopenaeus vannamei) were fed a control diet with 13% fish meal or an experimental diet with 20% microbial biomass and 4.3% fish
meal.
66
(C) European sea bass (Dicentrarchus labrax) were fed a control diet with 27.5% fish meal or an experimental diet with 18% freeze-dried microalgae and 15% fish
meal.
67
320 One Earth 1, November 22, 2019
One Earth
Review
that the incorporation of yellow mealworm into aquafeeds re-
sulted in increased feeding costs.
68
Furthermore, production
levels of insect meal are currently insufficient for constant sup-
ply,
52,68
although global production is increasing. For example,
production of black soldier fly increased from 7,000 to 8,000
tons in 2014–2015 to 14,000 tons in 2016
69
and, if this continues,
the price of insect meal is forecast to be competitive with that of
fish meal by 2023.
69
While it will be important to scale up produc-
tion to improve price competitiveness and production stability,
52
marketing strategies to brand the fish that are fed insect meals as
socially and environmentally responsible could also help boost
the use of insects in aquafeeds.
68
The nutritive value of insects can be enhanced by combining
insect meals with complementary nutritional profiles or by
manipulating the substrate used as a nutrient source to improve
fatty acid content, digestibility, and even palatability.
57
Defatting
the insect source can also increase protein levels in the final in-
sect meal produced.
57
In addition, improved resource efficiency
can be achieved by using food waste as a substrate for insects
and converting those waste streams into feed protein for aqua-
culture in countries where legislation does not prohibit such sub-
strates. While technological improvements are required to pro-
duce a consistently high-quality product, the use of insect
meal in aquafeeds has long-term potential if the price is compet-
itive and supply can be maintained.
Microbial Biomass
The microbial biomass produced from various microorganisms,
also known as ‘‘microbial protein’’ or ‘‘single-cell protein,’’ is a
promising substitute for animal- or plant-derived ingredients for
aquafeeds
19,70–74
(Figure 3B). Among the highly diversified
group of microorganisms, bacteria, yeasts, and microalgae are
generally regarded as having the highest potential for aqua-
feeds.
70–73
To achieve this potential there should be a focus on
improving the scale of production, which will ensure the process
chain is environmentally sustainable and reduce the cost of pro-
duction.
70–72
Bacteria and yeasts have a relatively high protein content
(50%–65% and 45%–55%, respectively), with amino acid pro-
files that are comparable with fish meal
70,72,73
and can poten-
tially be used as either functional feed additives or as alternative
raw materials.
70,72–77
The nutritional profile of bacteria and
yeasts can also be manipulated or enhanced by modifying the
culture media, growth conditions, and post-harvest treat-
ments.
70,72
The resulting microbial biomass produced can pro-
vide excellent nutritional characteristics for aquatic ani-
mals.
70,72–77
For example, yeasts derived from hydrolyzed
lignocellulosic biomass through fermentation are a suitable
source of protein for the diets of fishes, including carnivorous
species such as Atlantic salmon and rainbow trout, with the
caveat that additional synthetic methionine would have to be
supplemented in the feed.
72
There is also a range of commercial
products available in the marketplace
70,72,74
, including Novacq,
a potent microbial bioactive that can reduce the quantity of fish
meal required in the feed of the black tiger prawn (Penaeus
monodon) while maintaining growth rates.
75
However, even
though bacteria and yeasts have high potential as an alternative
source of protein for aquafeeds, their use is still limited due to the
high cost of production.
73
Their suitability and inclusion rates will
also need to be evaluated at the species level, with a focus on
their digestibility and the bioavailability of nutrients contained
within the microbial biomass.
70,72,73,75,76
Microalgae are cultivated and used as a feed resource in the
aquaculture industry and are invaluable during the larval rearing
stage of many aquaculture species.
77
The nutritional quality of
microalgae is high, with a crude protein content of up to 71%
and a lipid content of up to 40%, which are comparable with
that of terrestrial plant and animal sources.
78–80
Microalgae
have the potential to replace fish meal and fish oil in aqua-
feeds
71,77,81
and many studies have demonstrated the success-
ful use of microalgal biomass as a feed additive or fish meal
replacement for a range of aquaculture species, generally with
positive effects on growth and quality
70,81–87
(Figure 3C). The
biological capacity of microalgae, underpinned with positive
research findings on the replacement efficacy in aquafeeds
across many aquaculture species, suggests that there is high
potential for the use of microalgae as a protein source. However,
this potential is diminished by the technical, biological, and eco-
nomic difficulties regarding the continuous production of high-
quality microalgal biomass, and its downstream processing, at
scale.
40,79,88–90
The current world production of microalgae
(auto- and heterotrophic) is estimated to be approximately
40,000 tons per year,
90
only 0.7% of what would actually be
needed to replace the protein from fish meal in aquaculture. In
addition, the current price of microalgae is between US$10
and $30 per kg, several magnitudes higher than soybean meal
($0.30 per kg), hence global production is limited to high-value
niches in the human supplement and nutraceutical mar-
kets.
19,90–92
Although attempts have been made to model the
cost and production of microalgae to satisfy the protein demand
of aquaculture,
93–95
such efforts can only be considered as aca-
demic exercises as they do not take into account the difficulties
of upscaling production from medium scale (<1 hectare) to large
scale (>10,000 hectare). Therefore, due to the current low vol-
umes, high production costs, and cultivation challenges, it is
highly unlikely that microalgae will become a viable alternative
source of protein for aquafeeds in the next decade.
Macroalgae
The production of marine macroalgae (also termed seaweeds) is
an established industry that accounts for nearly 30% of global
aquaculture production, with an output volume of 30 million
tons per year that is worth more than $6 billion.
96
Nearly 90%
of all cultivated seaweeds are produced in China and
Indonesia.
9,96
The main species of seaweed, which account for
95% of the total production, are Eucheuma spp., Laminaria
japonica (Japanese kelp), Gracilaria spp., Undaria pinnatifida
(Japanese wakame), Kappaphycus alvarezii, and Porphyra spp.
(Japanese nori),
9,96,97
the majority of which are produced almost
exclusively for human consumption.
9,96,98
In addition to targeting
high-value applications, recent developments have demon-
strated the bioremediation capacity of both seaweeds and fresh-
water macroalgae, and their integration into existing sources of
nutrient-rich waste water from agriculture, aquaculture, munic-
ipal wastewater treatment, and power generation.
99–104
The
key to this concept is that, as these macroalgae grow they
assimilate dissolved nutrients (particularly inorganic nitrogen
and phosphorous), which would otherwise be wasted, from the
One Earth 1, November 22, 2019 321
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Review
water column and convert them into biomass and, consequently,
a source of protein. This provides a unique opportunity to
recover waste nutrients, allowing these industries to expand
and intensify production while minimizing their environmental
impact. The potential scale of this resource is impressive, with
a demonstrated biomass production rate of 45–70 tons of dry
weight hectare
1
per year and an average crude protein content
of 22%.
103,105
The proportion of crude protein in macroalgae, particularly
when harvested from the wild, is highly variable, ranging from
<1% to 48% of the biomass dry weight,
99,106–109
and depends
on both species and environmental conditions. It should be
noted that many of the crude protein values reported in the liter-
ature are overestimated,
110
and the true crude protein content,
representing a more realistic range, is 10%–30% when grown
under non-limiting nutrient conditions.
111–113
Despite this, mac-
roalgae are considered to be a high-quality source of protein,
with the majority of species having equivalent, or higher, total
essential amino acids as a proportion of total amino acids than
traditional agricultural crops and fish meal.
99,113–115
For
example, one of the first limiting amino acids in plant-based diets
of fish and crustaceans is methionine,
116
which makes up a
higher proportion of the total amino acids in macroalgae
compared with soybean meal and can be up to twice as
high.
99,110,114
In contrast, the absolute concentration of essential
amino acids on a whole biomass basis is substantially lower in
macroalgae (5.5% dry weight) than in soybean meal (22.3%
dry weight) and fish meal (31.2% dry weight),
113
due to high con-
centrations of complex polysaccharides (up to 76% dry
weight),
117
also known as dietary fiber. Dietary fiber limits the di-
gestibility of the algal protein fractions and affects the overall
nutritional value when incorporated into aquafeeds.
118–120
Accordingly, inclusion levels of macroalgae at rates >10%
generally have negative effects on growth and feed conversion
of commercial fish species.
121–124
However, macroalgae is still
suitable when incorporated as a functional feed ingredient at
low levels and, when included at rates <10%, there are often
positive effects on the animals being cultivated.
122,125,126
The
bioactive compounds found in macroalgae are associated with
health-promoting effects including improved stress resistance
and enhanced immune function.
127–131
In addition, macroalgae
enhance the flavor of farmed fish
132,133
and act as a feeding stim-
ulant, which indirectly boosts protein intake.
127,134,135
As such,
using whole macroalgal biomass as a functional feed additive
for aquatic animals is a promising application.
Using whole macroalgal biomass as an alternative protein
source has been successful in conjunction with herbivorous
aquatic animal species.
136–140
This has been particularly suc-
cessful for abalone, whereby seaweeds are cultivated in the
discharge water and then used as feed.
100
There is also potential
for its use with omnivorous species,
141
as these animals have
lower protein requirements compared with carnivorous fish.
142
Currently, the opportunity and value of using macroalgae in
aquafeed for carnivorous fish lies more in its application as a
functional feed ingredient to improve the health and welfare of
these animals rather than as a viable large-scale alternative pro-
tein source. If macroalgae are to replace fish meal in aquafeeds,
processing of the biomass is required to deliver a more concen-
trated form of the protein. This can be achieved either through
the direct extraction and isolation of protein or by removing
non-protein components, such as ash and soluble carbohy-
drates, thus increasing the relative proportion of protein in the re-
sidual macroalgal biomass.
105,143–146
However, these processes
are still being developed and while not yet commercialized,
145
they have been successfully applied to Ulva ohnoi, a commer-
cially grown bioremediation species, to increase its protein con-
tent from 22% to 45% on a dry-weight basis.
105
Importantly, the
quality of the concentrated protein in that study was comparable
with that of soybean meal and white fish meal, suggesting that it
would be a suitable protein replacement option, with the caveat
that it still must be tested in vivo.
105
Although this process is
currently in its infancy, the development of macroalgae as a
source of protein will provide a net increase to the supply of pro-
tein for the world. Macroalgae cultivated through bioremediation
represents an environmentally friendly alternative to many tradi-
tional sources of protein and will help to alleviate some of the
competition for protein resources between aquaculture and
terrestrial livestock production.
Improvements in Efficiency
Improving animal performance and animal health is a key to not
only reducing aquaculture production costs but also reducing
environmental impacts including decreasing carbon foot-
prints.
147,148
Traditionally, in aquaculture to date, this has been
implemented through the optimization of feed formulations to
achieve the most efficient feed conversion ratios (FCRs), which
represent the quantity of feed consumed to produce one unit
of animal biomass gain. The optimization of FCRs is based on
maximizing animal survival and growth traits.
148
However, for
species that require relatively large quantities of fish meal and
fish oil in their diets, this can be environmentally and economi-
cally unsustainable given the limited fishery resources.
149,150
A
sustainable solution would be for farmed animals to be fed
renewable plant-sourced and emerging alternative protein and
oil products, while at the same time improving FCRs and other
production traits through husbandry, species-specific feed
formulation, functional feed additives, and selective breeding
practices and their interaction (i.e., genotype 3diet interac-
tion).
148,151
Consequently, there is considerable scope for
improved efficiency in fed-aquaculture production.
The transition toward plant-based diets has been challenging,
and the effects of plant ingredients on animal growth and health
have been widely studied.
152–154
Plant-based diets typically
contain carbohydrates that have low digestibility in carnivorous
animals as well as anti-nutritional elements that affect feed
intake, feed efficiency, metabolism, and health.
155,156
While
many aquaculture species are carnivorous (e.g., salmon and
tuna), others are omnivorous or herbivorous (e.g., shrimp, tilapia,
catfish, and carp species); therefore, different species vary in
their capacity to effectively use different kinds of animal or plant
feed ingredients. Recently, feed formulations have improved, al-
lowing complete substitution of animal-based diets with plant-
based ones in some species.
157
However, these results are spe-
cies specific, and total substitution with plant-based ingredients
can still negatively affect survival and growth rates in other spe-
cies.
158
Based on modern advances in feed ingredient process-
ing and gene technology, there is now the capability to process
and/or engineer plant crops as feed ingredients that specifically
322 One Earth 1, November 22, 2019
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Review
address the challenges of incorporating plant-based products
into aquafeeds.
159,160
At present, soybean meal is a primary source of vegetable pro-
tein in aquafeeds.
156
In an attempt to negate the negative effects
of soybean inclusion, biotechnology (i.e., gene expression
and silencing) is being used to suppress anti-nutritional elements
or to alter seed protein composition for increased digestibil-
ity.
159–161
In addition, biotechnology can be used to value-add
by genetically modifying soybean to produce unique products
for specific animal requirements. For example, soybean with
higher proportions of omega-3 fatty acids can be used for
enhanced animal growth and human health benefits,
89,162
and
soybean with carotenoid gene enhancements can be used to
enhance the flesh pigment of salmon.
161,163
There is also
research demonstrating the use of prototype vaccines engi-
neered by plant biotechnology for inclusion in plant-based aqua-
feeds for species requiring mass oral immunization.
161,164
In addition to the modification of soybean, there has been an
emergence of functional feed additives in aquaculture di-
ets.
75,165–167
Functional feed additives can indirectly act as
growth promoters by improving immune function, reducing
oxidative stress, and enhancing disease resistance, rather than
directly providing extra nutrients essential to growth. There is
an array of products sold under commercial trademarks (e.g.,
Novacq, ALIMET, and Sanocare) that report improved survival
and growth,
168–171
and while the active ingredients of these
can include bioactives obtained from plant-derived purifications,
the majority appear to be from microbial biomass-derived sour-
ces. In the absence of recombinant engineering of microbes,
most of the processes used to produce functional feed additives
are discoveries of biological action and lack the enforceable pro-
tections of a patent (e.g., US H2218H). Consequently, there is a
high level of commercial secrecy around their production and
mode of action. After reviewing a number of patents that exist
relating to microbial biomass products, it is apparent that their
mode of action is through immune stimulation, gut microbial/mi-
crobiome modulation, or improved expressers of nutrient ele-
ments including selenium (Patent EP1602716A1), glucosamine
(Patent US H2218H), and essential fatty acids (Patents
JP599652B2 and US6255505B1). Considering that the majority
of functional feeds promote immune response and growth, it is
perhaps misleading to consider them ‘‘optional additives’’ within
the context of aquafeed preparation. Rather, they could be
considered as additives that ameliorate deficiencies in current
diet formulations. Recognizing that aquafeeds must supply the
full spectrum of nutritional factors to support the action of multi-
ple biological pathways within an animal (including immune
competence under typical culture conditions) will facilitate a
more logical and systematic approach toward the replacement
of fish meal.
Many studies have sought to improve diet formulations,
whereas others have focused on improving the performance of
the animals fed a variety of diets through genetic improvement
programs.
147,151
Several studies have demonstrated the exis-
tence of genetic variability in different wild stocks as well as
domesticated animals fed different proportions of fish meal
and, therefore, protein. For example, divergent wild stocks
(i.e., discrete genetic pools) of the freshwater prawn (Macro-
brachium rosenbergii),
172
alternative genetic strains of tilapia
(Oreochromis spp.),
173
and selected groups of black tiger shrimp
(Penaeus monodon)
174
have different capacities to use different
animal proteins. Furthermore, the mean heritability (h
2
) estimates
for feed efficiency traits (FCR and reduced residual feed intake
[RFI]) in farmed fish range from 0.07 to 0.47, providing support
for genetic improvement through selective breeding pro-
grams.
148,175
In these studies, rainbow trout (Oncorhynchus
mykiss;h
2
FCR 0.12; h
2
RFI 0.13–0.23)
175,176
, sea bass (h
2
FCR 0.23 pedigree and 0.47 genomic),
177
European whitefish
(Coregonus lavaretus;h
2
FCR 0.07),
178
and Nile tilapia (Oreo-
chromis niloticus;h
2
FCR 0.32)
179
had moderate heritability esti-
mates sometimes comparable with terrestrial animals (h
2
range
of 0.12–0.67).
179–181
While heritability estimates for feed efficiency are starting to
emerge for farmed fish species, the lack of comprehensive her-
itability measurements among other aquatic animals is partly
due to the difficulty in obtaining accurate trait measurements.
182
Although the concept of measuring aquaculture feed efficiency
for selective breeding is long-standing, it lags behind terrestrial
animal production, as recording feed intake routinely in individ-
ual animals in commercial aquatic systems is a considerable
challenge.
176,182
Therefore, feed efficiency improvement using
phenotypic trait selection in aquaculture can be difficult. The
development of genomic approaches such as ‘‘genomic selec-
tion’’ can increase the precision of estimated breeding values
for feed efficiency traits, which can then be used in selective
breeding programs.
183
In this approach, large numbers of
genome-wide genetic markers aid in animal selection. Here,
most quantitative trait loci (QTL) regulating feed efficiency will
be in strong linkage disequilibrium with at least one genomic
marker. As such, genomic selection methodology simulta-
neously estimates the combined genetic effects of all relevant
QTL and provides accurate predictions of genetic merit for an
animal.
184
Of particular interest is the selective breeding of aquaculture
animals that can effectively use plant-based ingredients without
negative side effects. For example, there is significant genetic
variability around growth traits of rainbow trout (Oncorhynchus
mykiss) when provided a plant-based diet (including high herita-
bility estimates for body weight; e.g., 0.43–0.69),
185
suggesting
that genetic progress is achievable.
185–187
Furthermore, addi-
tional studies have demonstrated genetic improvement in
growth traits by selectively breeding animals on a plant-based
diet (e.g., rainbow trout
157
and salmon
188
). However, when tran-
sitioning production animals from conventional feed ingredients
to plant-based diets, the interaction of genetics and diet (i.e., re-
ranking of family performance on specific diets) needs to be
considered, particularly in established breeding programs.
Significant genotype (animal performance) by diet (plant-based
diets) interactions have been observed in fish whereby some an-
imals can more effectively accept and use the diets than
others.
189,190
It is apparent that animals that performed well on
traditional animal-based diets may not necessarily perform
equally well on a plant-based or modified diet. However,
exposing fish to plant-based diets early in life improves later-
life fish performance when fed the same diet again.
191,192
Regardless, to ensure optimum genetic gain and productivity,
the aquaculture industry needs to develop selective breeding
programs specific to plant-based diets from first feeding.
One Earth 1, November 22, 2019 323
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Future Directions
Feeds for lower-trophic-level freshwater fish species (e.g., cat-
fish, tilapia, and herbivorous carp) contain considerably lower
levels of fish meal compared with those for carnivorous species
(e.g., salmon, other marine fishes, diadromous fishes, eels, and
marine shrimps; Figure 2). Therefore, consumer awareness, la-
beling, and interest in seafood sustainability may help increase
consumption rates of farmed freshwater fish at the expense of
species with greater protein demands. As a caveat, to date there
is limited evidence for an increase in consumer demand for sus-
tainable seafood as a result of sustainable seafood labeling.
193
Although the percentage inclusion level of fish meal in feeds is
low for farmed freshwater fish in comparison with marine fish and
Protein
content
Fishery and aqua-
culture by-products
Insect meals
Bacteria and dry
bio-floc
Yeast
Microalgae
Macroalgae
Food wastes
Environmental
sustainability
Consumer
acceptance Feasibility
Microbial biomass
Figure 4. Qualitative Feasibility Assessment
of Alternative Protein Sources for Fed-
Aquaculture Diets
The broad-level qualitative assessments of alter-
native protein sources were based on a combina-
tion of the current-day realities and the future po-
tential (10–20 years) of each protein source.
Positive (+) represents a protein source with high
potential to meet demand, while negative () rep-
resents a protein source that has obstacles that will
need to be overcome before development. The
assessments were subjective and based on a
relative comparison with fish meal from wild-cap-
ture fisheries (for proximate composition see
Figure S1). The assessment for ‘‘feasibility’’ was
determined by considering the economics of
commercial-scale production, the relative limit of
the resource, the likelihood of meeting consistent
supply, the short-term prediction of commodity
price, and the legal ease of implementation.
crustaceans, the global production of
these fed carp, catfish, and tilapia is very
high
11
(Figure 2). Therefore, the inclusion
of even low levels of fish meal results in
substantial quantities of fish meal overall.
Given the projected increase in production
of these species and associated aquafeed
demand (Figure 2), substituting fish meal
by alternative protein sources in these di-
ets will result in a considerable reduction
in the total quantity of fish meal used. Sim-
ulations by Froehlich et al.
12
suggest that
this sector has the highest potential to
mitigate the use of forage fish by mid-
century.
Significant gains in aquaculture produc-
tion to supply additional protein, espe-
cially for freshwater fish, may also be
made by combining unfed aquaculture
with fed aquaculture or through the devel-
opment, promotion, and expansion of pol-
yculture-based systems, resulting in the
simultaneous culture of multiple fed spe-
cies in a single system.
194
In the related in-
tegrated multi-trophic aquaculture sys-
tems, which combine fed aquaculture
with extractive aquaculture, a higher yield
of protein is achieved through the production of several prod-
ucts.
100,101,195
While detailed knowledge is required to balance
multiple species,
196
these systems have the added benefits of
nutrient bioremediation and positive consumer perception.
The greatest challenges to alternative protein sources in aqua-
feeds include variable protein content (see Figure S1) and the
feasibility of increasing production, which is a function of avail-
able processing technologies, cost, and scalability (Figure 4 in-
cludes a subjective assessment of ingredient potential). Con-
sumer acceptance also varies among these raw materials.
Given these challenges, there is enormous potential for techno-
logical improvements to consistently produce high-quality alter-
native protein products with enhanced nutritional profiles, while
324 One Earth 1, November 22, 2019
One Earth
Review
economies of scale can result in improved price competitive-
ness. Some protein sources, such as fish byproducts and insect
meals, are viable and promising alternatives to conventional fish
meal, whereas some raw materials such as food waste may still
need to overcome a number of obstacles before becoming a sta-
ple in formulated aquafeeds (Figure 4) and may find greater use
in bioconversion/biotransformation.
It is important to bear in mind that aquaculture feeds are
formulated using a multitude of ingredients and it is unlikely,
nor necessary, that a single protein source will meet the require-
ments of the cultured species or fully replace fish meal. Multiple
protein sources can also be used in combination to benefit from
their complementary nutritional profiles. Feed supplements can
also be used to balance the nutrient composition of the feeds
and functional ingredients can be used to facilitate the replace-
ment of fish meal with alternative ingredients. Furthermore, using
multiple protein sources allows flexibility in feed formulations
when ingredient prices fluctuate,
192
as feed manufacturers often
use cost as a determinant in selecting ingredients.
There has been a 4-fold increase in fed-aquaculture produc-
tion from 12.2 million tons to 50.7 million tons from 1995 to
2015.
197
In parallel, the increase in aquafeed production was
6-fold, from 7.6 million tons to 47.7 million tons from 1995 to
2015.
25,197
Even though aquafeeds only account for a small pro-
portion (less than 4%) of total global animal feed production, the
ingredients used are also used in terrestrial livestock feed, pet
food, and human food.
11,25,192
Therefore, developing and opti-
mizing alternative sources of protein for aquafeeds will play an
important role in ensuring a socially and environmentally sustain-
able future for the aquaculture industry.
SUPPLEMENTAL INFORMATION
Supplemental Information can be found online at https://doi.org/10.1016/j.
oneear.2019.10.018.
ACKNOWLEDGMENTS
The figures for this article were created by Hillary Smith.
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