Reviews in Aquaculture (2020) 12, 186–203 doi: 10.1111/raq.

12312

Innovative protein sources in shrimp (Litopenaeus vannamei)

feeding

Sa
Mar
ıa Jose
nchez-Muros1 , Patricio Renteria2, Antonio Vizcaino1 and Fernando G. Barroso1
1 Department of Biology and Geology, University of Almer
ıa, Almer
ıa, Spain
2 Faculty of Agricultural Sciences, Technical University of Machala, Machala, Ecuador

Correspondence Abstract
Mar
ıa Jos

e S

anchez-Muros Lozano, CITE 2B,
Universidad de Almeria, Carretera de Shrimps are one of the most important cultures in aquaculture with an estimated
~ada de San Urbano,
Sacramento s/n. La Can production of around 4.5 million MT, that is constantly growing. This fact entails
04120 Almeria, Spain. Email: mjmuros@ual.es the necessity to increase aquafeed production to meet demand. As in other aqua-
culture species, fishmeal (FM) is the main protein source used in shrimp feeding.
Received 18 May 2018; accepted 18 October
In this context, the current review summarises several innovative protein sources
2018.
for shrimp nutrition, focusing primarily on those sources that are less commer-
cialised including fishery by-products, terrestrial animal by-products, single-cell
proteins, grain legumes, plant protein concentrates and cereal by-products, with
emphasis placed on novel raw materials in experimental phase: algae, insect meal
or biofloc. Nutritive values, inclusion levels and constraints are discussed.
Key words: fishmeal, Litopenaeus vannamei, insects, algae, biofloc, growth.

aquaculture feeds and is the first consumer of FM (Tacon

Introduction
& Metian 2008; Gillett 2010). Nevertheless, the estimation
The nutritional requirements of fish and crustaceans for 2020 indicates a decrease in 37.7% of FM for shrimp
include a large amount of high quality protein. From a feed due of a decreasing market availability of fish meal,
nutritional point of view, the protein sources used for ani- increasing market cost and global use alternative protein
mal feed should meet some important requirements, such (Tacon & Metian 2008), so it is foreseeable that in the
as high protein content, an adequate amino acid profile, future the sustainability of aquaculture depends of terres-
high digestibility, good palatability, not containing anti- trial animal and vegetable proteins (FAO 2012).
nutritional factors, as well as secure supplied and affordable Dietary protein content in shrimp feed ranges from 250
costs (Barrows et al. 2008; Vizca
ıno et al. 2014). to 330 g kg 1 crude protein (Ayisi et al. 2017) with FM as
FAO estimates that fish supplies from aquaculture will the main protein source (minimum 12% : Su
arez et al.
have increased from 52,843 9 103 ton in 2008 to 2009). FM inclusion level depends of protein used, for
93,612 9 103 ton by 2030 (FAO 2013). Global aquaculture example for soy meal, the substitution reaches 37.42%
shrimp production has dramatically grown in the last two whereas for fermented soy raised 61.67% of substitution
decades (Cummins et al. 2017). The world’s shrimp pro- (Shiu et al. 2015). These high protein levels in diets imply a
duction, in both capture and aquaculture terms, is approxi- significant increase in feed prices, and feeding is considered
mately 6 million tons, of which about 60% enters the to represent around 50–70% of total production costs.
world market. In value terms, shrimp is today the most Indeed, a reduction in the percentage of FM inclusion in
important internationally traded fish product (Gillett 2010) shrimp feed would imply significant savings in FM globally,
and represents a significant percentage of feed destined for and also reduced production costs.
aquaculture. In 2008, 708 million tonnes of industrial com- Nowadays, fishmeal (FM) and soya meal are the most
pound feed were produced, of which 29.2 million tonnes commonly used protein sources in diets for aquatic organ-
corresponded to aquafeed (4.1% of total feed); 17.3% of isms given their good nutritional qualities. However, they
total aquafeed was destined to feed marine shrimp and are two sources that have a strong environmental impact
4.55% to freshwater crustaceans, which ranked second in such as deforestation, use of water, utilisation of GMO and
feed consumption of those destined to aquaculture, behind pesticides for soy (S
anchez-Muros et al. 2014), and over-
carp. In 2006–2007, the shrimp culture uses 27% of FM for fishing in the case of fishmeal. In consequence, currently,

186 © 2018 Wiley Publishing Asia Pty Ltd

 Innovative protein sources to shrimp feed

the sustainability of protein source must be a point to take potato flour concentrates of vegetable proteins regarding
account. Thus, aquaculture looks for new protein sources commercial protein source as different soya products, etc.
that allow a maximum percentage of replacement without The percentage of inclusion ranges from 16% for papaya
lowering either growth or quality that must be renewable. leaf meal (Penaflorida 1995) to 100% for lupine meal
Recently, several works have studied the potential use of (Molina-Poveda et al. 2013) corresponding to the commer-
different proteins from animals, plants and microorgan- cial sources, soy and lupino, the mayor percentages of
isms, including by-products that could contribute to diver- replacement.
sify the ingredient, decrease the dependence of fish and soy In general, the inclusion of commercial vegetable sources
meal in aquafeed and contribute to the development of sus- at high levels (over 50%) decreased the growth. For lupine,
tainability aquaculture. Molina-Poveda et al. (2013) found that the body weight
The present review presents further information about gain in shrimps gradually decreased with increasing con-
possible alternatives sources to FM for L. vannamei feed. centrations of lupine meal in diet, and displayed excellent
Nutritive values, quality, inclusion levels and constraints growth with 50% replacement of FM with de-fatted and
are discussed. dehulled lupine meal. At 75% levels and higher ones, signif-
icant drops in weight gain and in the specific growth rate
(SGR) were observed in shrimp kept under lab conditions
Traditional sources
and in clear water. Nevertheless, in green water, replace-
Vegetable sources ments of up to 100% were possible and have no negative
As an alternative to fishmeal, many authors have recom- effect on growth.
mended the plant protein sources mainly owing to the lower Liu et al. (2012) replaced FM with peanut meal at inclu-
price compared to fishmeal, the greater availability and sion levels of 0%, 7%, 14%, 21%, 28% and 35% of diet.
improved consistency of composition (Ayadi et al. 2012; Weight gain, feed utilisation, protein efficiency ratio, feed-
Daniel 2018). However, vegetable feedstuffs have several ing rate, survival, protease activity and physiological stress
unfavourable characteristics such as essential and non- resistance were lower in the shrimps fed at higher peanut
essential amino acids imbalances, deficiency of essential replacement levels compared with those fed a basal diet.
amino acid as in lysine, cysteine and methionine. Vegetables Their data suggested that 50% of replacement of FM by
also contain anti-nutritional factors, such as saponins, alka- peanut meal (diet with 14% of peanut meal) could be
loids and tannins low palatability and a high portion of fibre included in practical diets for L. vannamei.
and non-starch polysaccharides. All these unfavourable Percentages over to 50% of replacement were obtained
characteristics limit the percentage of their inclusion in diet. with canola (Su
arez et al. 2009) rice (Oujifard et al. 2012)
Soya meal offers high digestibility, high protein quality and and Cowpea (Aya et al. 2015) (Table 1) but did not reach
quantity and the best amino acid profile of the vegetable 100%. Amaya et al. (2007) and Molina-Poveda et al.
protein sources available, together with other nutritive ben- (2015a,b) obtained similar growth and productive perfor-
efits, provided that inclusion percentages do not exceed mance to a control diet in white shrimp fed a diet in which
40% (Lim & Dominy 1990) being the most used in fish feed- 100% FM was replaced with a combination of soya, milo
ing. However, soy has environmental problems discussed and corn gluten meals (Amaya et al. (2007) and lupino
above, so that the current crop is considered unsustainable. (Molina-Poveda et al. 2015a,b). Nevertheless, shrimps are
In addition, of soy there are other important locally pro- reared in semi-closed recirculating systems in which they
duced plant protein sources frequently used in aquaculture have access to natural food. In clear water, Su
arez et al.
that include ground nut cake, cottonseed meal, mustard/ (2009) obtained good results for growth and survival, and
rapeseed cake sunflower cake meal coconut cake, corn glu- confirmed that L. vannamei could be fed plant meals (70%
ten meal and rice gluten. However, these sources have weak soya bean/30% canola), which thereby reduced the quantity
points that limit their inclusion in aquafeed Hardy (2010) as of FM from 30 to 6 g/100 g dry weight (corresponding to a
the price that must be cheaper, lack of anti-nutritional fac- reduction in 80%).
tors, improve the digestibility is low, because low digestibil- Lower percentages of replacement were obtained with
ity provoke major contamination by faeces. Other problem uncommercial sources camote, papaya and amaranth leaves
is identified the nutrients in fishmeal such as taurine, anime (Table 1) probably due to the high percentage of crude
or other compound biologically actives that allow us to sup- fibre in the leaves regarding seed.
plement the diet and decrease fish meal inclusion. Neverthe- The reductions in growth observed in experiments in
less, there is a great variety of vegetables relatively which FM was replaced with vegetable protein sources were
understudied that could open new options in shrimp feed. attributed to the inadequate balance of amino acids (Lim &
Table 1 shows studies that include different protein Dominy 1990). The unbalanced amino acids profile of
sources, quinoa, canola meal papaya leaves and sweet some vegetable sources are completed by adding free amino

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M. J. S

anchez-Muros et al.

Table 1 Vegetable sources used as FM replacement. In the table are shown the effect on growth at maximum level of FM substitution that report
similar to superior growth or minimum level of FM substitution at growth decrease regarding FM based diet

Vegetable sources Weight Replacement PB diet FM % Growth Density/culture Authors

(g) % % diet effect system

Soy bean 0.172 <37.42 37.00 7.00 No effect 36/acuario 100 l Shiu et al. (2015)
(exp)
Fermented mixture (1:4 soybean meal: 0,22 80 37.00 20.00 No effect 30/27 m2 (exp) Chiu et al. (2016)
Eisenia fetida)
Soybean meal based protein blend 0.44 20 40.00 5.00 No effect 30/300 l (exp) Xie et al. (2016)
Lupino + squid meal 5.5 100 36.85 0.00 No effect 30/m2 (green Molina-Poveda et al.
water) (2013)
Lupino + squid meal 1.23 <50 36.85 16.46 No effect 44/m2exp) Molina-Poveda et al.
(2013)
Canola+squid meal+ soy 0.3 80 38.60 6.00 No effect 100/m2 (exp) Su
arez et al. (2009)
Milo+ corn gluten+ poultry by-product+ 0.03 100 36.60 0.00 No effect 35/m2 (green Amaya et al. (2007)
soy water)
Corn gluten meal +squid meal 1.23 >25 36.79 0.25 Decrease 44/m2 (exp) Molina-Poveda et al.
(2015a,b)
Corn, sorghum. wheat and soybean 4.1 ≤100 35.00 30 No effect 280/m3 Moreno-Arias et al.
(2018)
Rice+(protein concentrate+shrimp meal) 6.99 ≤50 36.60 22.85 No effect 8/m3 e(xp) Oujifard et al. (2012)
Amaranto+squid meal 1.3 <15 30.17 26.83 No effect 39/m2 (exp) Molina-Poveda et al.
(2015a,b)
Quinoa +squid meal 1.3 <45 30.22 17.36 No effect 39/m2 (exp) Molina-Poveda et al.
(2015a,b)
Cowpea (Vigna unguiculata L.) Meal* 0.03 45 37.00 16.65 No effect 15/m2 (exp) Aya et al. (2015)
Cowpea (Vigna unguiculata L.) Meal* 0.04 45 37.00 16.65 Increase 15/m2 (green Aya et al. (2015)
water)
Peanut 3.37 50 42.00 20.00 No effect 35/150 l (exp) Liu et al. (2012)
Camote leaf 0.05 17 37.80 22.00 Decrease 10/40 l (exp) Penaflorida (1995)
Papaya leaf 0.05 16 37.60 23.00 No effect 10/40 l (exp) Penaflorida (1995)
Jatropha curcas 4.46 50 0.35 24.60 Increased 60/45 l (exp) Harter et al. (2011)

*M. Rosenbergii.

acids or a high value protein source. Animal protein, which (Lim & Dominy 1990; Fox et al. 1995; Lim et al. 1997) as
offers high digestibility, and a good balance between essen- HUFAS deficiency. Moreover, replacing FM with plant
tial and non-essential amino acids (Webster et al. 1992, meal in shrimp diet could induce changes in the fatty acids
1995; Refstie et al. 1997, 1998) which, in turn, allows profile, which showed low levels of docosahexaenoic acid
increased inclusion levels of vegetable protein sources. In (DHA) and eicosapentaenoic acid (EPA), where HUFA
fact, most of the diet cited in Table 1 include squid meal or content was a quality and healthy factor for seafood. This
protein concentrate. The combination of different vegetable deficiency could be covered by very small amounts of fish
meals improves the amino acids profile and dilutes the oil, squid meal and liquid fish soluble, which not only
anti-nutritional compounds of each source by allowing improved palatability, but also acted as a full or superior
greater FM replacement if only one source is used. equivalent in shrimp production grow-out feed compared
The digestibility of vegetable sources is usually low. Ouji- to conventional FM-based diets (Browdy et al. 2006). On
fard et al. (2012) found that FM replacement with rice pro- the other hand, Moreno-Arias et al. (2018), evaluating four
tein concentrate by up to 50% resulted in an almost linear experimental diets (0%, 10%, 20% and 30% fishmeal) with
reduction in the apparent digestibility coefficients of nutri- the combination of different ingredients (soybean, corn,
ents. Similar result obtained by Yang et al., (2015) with soy sorghum and wheat), obtained that the essential fatty acids
meal. The anti-nutritional factor together with non-digestible and high quality proteins provided by the biofloc compen-
carbohydrates could be responsible for this decrease in sated the lower inclusion of fish meal in the diets, except
digestibility. for the experimental diet 0% FM.
Marine protein replacement is very complex because of The consulted bibliography shows that although vegeta-
the many interactions that take place at different levels bles can substitute high FM levels (50%), FM cannot be

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188 © 2018 Wiley Publishing Asia Pty Ltd
 Innovative protein sources to shrimp feed

totally replaced without including some animal marine nutritional qualities of animal protein sources have been
protein sources (Browdy et al. 2006). Most of the diets commonly used to supplement soya bean meal, which
cited in Table 1 include a low percentage of squid meal or allows higher FM replacement levels being poultry and fish
some other marine source to guarantee a minimum marine by-products flour those that allow a high level of replace-
protein input. Currently, the research is focused in the ment.
blended with different plants or treatments to decreased Poultry by-product meal has a similar nutrient profile to
anti-nutritional factor and/or use of varieties low content that of FM and may, therefore, serve as an acceptable ingre-
in antinutritional factors, or treatment to improve nitritive dient in shrimp diets (Cheng et al. 2002). This protein
value such as fermentation etc. . . .that allow us increased source has high crude protein content and a similar amino
the level of replacement of FM. acids profile to FM. Although this allows elevated levels of
FM replacement, low isoleucine, lysine, methionine and
tryptophan contents prevent total replacement (Cheng
Animal sources
et al. 2002), and those shrimps fed 33.3% or 66.7% FM
Nowadays, very few studies in shrimp have analysed replac- replacement diets grow faster than those fed 100% FM
ing FM with animal protein sources (Table 2). To replace replacement diets. Thus, 66.7% FM replacement with PBM
or minimise the inclusion of FM in commercial shrimp, not affecting shrimp growth is possible. In their experi-
studies have mostly focused on developing alternative for- ments, Davis and Arnold (2000) used a co-extruded/soya
mulations using plant proteins (Colvin & Brand 1977; Lim bean poultry by-product meal (CEPM) and flashed dried
& Dominy 1990; Piedad-Pascual et al. 1990; Lim et al. poultry by-product meal (FD-PBM) as FM replacements,
1998; Hardy 1999; Davis & Arnold 2000; Divakaran et al. which ranged from 0 to 30 g FM/100 g diet to 80%
2000; Tacon 2000; Mendoza et al. 2001; Dersjant-Li 2002; replacement (6 g FM/100 g diet) in diet with 17.7% soya
Conklin 2003; Fox et al. 2004; Gonz
alez-Rodr
ıguez & Abdo meal. No significant differences in either survival or feed
de la Parra 2004; Samocha et al. 2004) mainly due to the efficiency, but a significant increase in protein conversion
food security issues limit the use of animal protein sources, efficiency, were observed by replacing FM with either co-
most of which was forbidden from 2001 (CE 999/2001) to extruded/soya bean or flashed dried poultry by-product
2013 (CE 56/2013). Therefore, recently, the research into meal CEPM or FD-PBM. The meat and bone meal (MBM)
alternatives to FM has focused on vegetable sources. combination, poultry by-product meal (PBM), blood meal
Animal sources have better nutritive characteristics than (BM) and corn gluten meal (CGM) (Ye et al. 2011) with a
vegetable sources: better digestibility and an essential/non- fixed formulating proportion in practical diets for pacific
essential amino acids balance (aa/aaee), absence of anti- white shrimp at two dietary protein levels (330 or 380 g
nutritional factors and higher crude protein. The highest kg 1 protein diet) have shown that white shrimp can be fed

Table 2 Animal sources used as FM replacement. In the table are shown the effect on growth at maximum level of FM substitution that report simi-
lar to superior growth or minimum level of FM substitution at growth decrease regarding FM based diet

Animal sources Weight Replacement PB diet FM % Growth Density/culture Authors

(g) % % diet effect system

Poultry-by- product 0.17 <66.7 30.00 8.17 No effect 100/m2 (exp) Cheng et al.
(2002)
Poultry-by- product+bone and meat meal+ blood 5.7 10 32.19 18.00 No effect 133/m3 (exp) Ye et al. (2011)
meal+ corn gluten meal
Porcine meat 0.55 >26.18 34.3 21.1 Decrease 15/25l (exp) Hern
andez et al.
(2008)
Flashed dried poultry by-product meal 0.37 80 32 6 Increase 9/68l (exp) Davis & Arnold
(2000)
Fish -by -product (10 different by-products) 1 100 0.69 0.00 No effect 50/m2 (exp) Forster et al.
(2004)
Fishmeal with fish protein hydrolysate + biofloc 0.002 <20 42.00 32.00 No effect 59/m2 (exp) Valle et al.
flour (2015)
Fishmeal analog (blend of animal and plant protein 0.45 15 35 10 No effect 10/135l (exp) Qiu (2017)
+ encapsulated aaee
Hydrolisate 0.0002 27 38.74 51 Increase 1000/500l (exp) Niu et al. (2014)
Co-extruded soybean poultry by-product meal 0.37 80 32 6 Increase 8/68l (exp) Davis & Arnold
(2000)

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a diet with 350 or 510 g kg 1 FM replacement in a 330 or as acceptable substitutes for FM in diet for Pacific white
380 g kg 1 protein diet, respectively. Beyond protein levels, shrimp reaching similar final weights and feed conversion
a negative response occurs in terms of growth, digestibility ratios (FCR).
and body composition with an increased mixture in diet. The processing by-products are necessary to preserve
On the other hand, body composition can be an effect, and utilisation in feed, but it can change the nutritive value.
unless fish oil is added to defatted PBM diets. Heat treatment is frequent for meal production. In FM pro-
Including animal protein can influence diet digestibility. duction, the heat can enhance the double links in protein
A drop in apparent digestibility for dry matter, crude pro- structure and may affect their digestibility. However, the
tein, crude lipids and gross energy has been observed with high content of burned particles or high levels of histamine
the increasing inclusion of porcine meat meal in shrimp and total volatile nitrogen due to overcooking can lower
diet (Hern
andez et al. 2008), but it also affects the apparent nutritive values (Cruz-Su
arez et al. 1992).
digestibility of nutrients in diets by decreasing digestibility The silage is a conservation method that does not use
with increased protein in diet (Ye et al. 2011). On the other high temperature. Indeed a temperature at 35°C proved
hand, the apparent digestibility can be improved by adding adequate for silage production and did not alter pH values.
protein of a marine origin, such as squid meal or shrimp Espe and Lied (1999) have reported that pH does not
shell meal, to provide the balanced amino acid content change at different storage temperatures, but hydrolysis
required for shrimp (Williams et al. 1997). drops when the temperature goes above 50°C or below
Ingredients from terrestrial animals, such as bone meal, 4°C, or if waste material has been previously cooked.
poultry by-product meal and blood meal, have also been Studies on weight gain and digestibility have reported
successfully used in feeds for various crustacean species that protein silage can be an adequate substitute for FM in
(Davis & Arnold 2000; Forster et al. 2003; Samocha et al. diets for warm-water fish such as carp (Cirrhinus mrigala)
2004; Cruz-Su
arez et al. 2007; Hern
andez et al. 2008; (Ali et al. 1994; Singh et al. 2018) and tilapia (Oreochromis
Saoud et al. 2008 Hern
andez et al. 2016; Pranama et al., niloticus, O. aureus) (Fagbenro & Jauncey 1998; Goddard
2018). However, animal by-products may be deficient or et al. 2003 Soltan et al. 2017) owing to increased diet
excessive in one essential amino acid or more and the fatty digestibility and pre-hydrolysed protein regarding FM. One
acid profile differs of marine sources which often affects disadvantage is that lysine, tryptophan and methionine are
animal productivity (Fasakin et al. 2005) because a nutri- partly hydrolysed by acidic conditions and, hence, their
tional imbalance arises when marine animal meals are concentration in silage is low (Backhoff 1976; Jackson et al.
removed from formulations (Akiyama 1989; Akiyama et al. 1984; Fagbenro & Jauncey 1993; Shahidi et al. 1995). Con-
1991; Lim et al. 1998; Tacon & Barg 1998; Hertrampf & versely, however, another experiment has shown that the
Piedad-Pascual 2000; Fox et al. 2004), being the fish by- concentrations of non-essential and essential amino acids
product the source that allow higher percentages of substi- in fish waste are not affected by ensiling processes, except
tution (100%) (Table 2). for tryptophan, whose concentration lowered by 23.7%
The waste produced by fisheries and fish by-products is (Vidotti et al. 2003; Vizcarra-Maga~ na et al. 1999; Gallardo
another alternative source with the advantage that provides et al. 2012). Gallardo et al. (2012) have compared the
nutrients from marine origin and a similar composition to inclusion of waste fish silage with formic acid versus fish
FM as regards the amino acids proportion or fatty acids waste. Their results reveal how fish silage acid at a low pH
profile, but also presents quantitative differences regarding is beneficial to the white shrimp L. vannamei and it sus-
protein or lipids proportion. tains reasonable weight gain combined with soya bean meal
Fish waste includes heads, fins, skin, dark muscle meat in practical diets. A significantly lower weight gain has been
and viscera, which are rich in protein and fat (Hern
andez observed with shrimps fed fish waste silage. Hence, fish
et al. 2004). Such waste is currently converted into meal, waste silage cannot be used as a single protein source. The
which is a commercially available product, such as tuna by- authors’ explanation for these results is that fish waste diet
product meal. One problem with using these products is silage is 63% tryptophan-deficient compared to the shrimp
their variable quality as they are obtained from different profile. Supplementing silage with soya bean meal diet
fish parts and distinct species. Forster et al. (2004) studied improves its amino acid balance, mainly because soya bean
10 different by-products from Alaska fisheries with several diet enhances the tryptophan level of diet. Similar results
protein and quality levels. The experimental diets tested in have been reported in the silage obtained from a mixture of
this experiment were formulated with 50% FM replacement pre-cooked tuna waste and fresh viscera (4:1 ratio) (Viz-
with a fish by-product by taking into account the different carra-Maga~ na et al. 1999).
protein contents of each by-product so that all the experi- The protein hydrolysates could enhance the protein utili-
mental diets were isonitrogenous to isoenergetic. These sation. Litopenaeus vannamei and Homarus americanus fed
authors concluded that all the checked products could act with diets supplemented with fish protein hydrolysates

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 Innovative protein sources to shrimp feed

show increased growth (Anggawati et al. 1990; Hertrampf Besides their chemical composition, these sources offer the
& Piedad-Pascual 2000; Floreto et al. 2001; C
ordova-Mur- advantage of being used to recycle different waste forms
ueta & Garc
ıa-Carre~
no 2002; Quinto et al. 2018)). Hern
an- and being more sustainable sources. But most of them are
dez et al. (2011) have found that, via lactic acid in an experimental phase. There is a long way to go before
fermentation, tuna by-product protein hydrolysate (TBPH) these components are included in commercial feed.
improves the digestibility and amino acid profile of porcine
meal-based diets, and thus enhances the growth response of
Biofloc
L. vannamei.
Different authors’ results have shown the possibility of Shrimp rearing in green water systems are able to use natu-
replacing a high percentage of FM with another protein rally available foods where they are commonly cultured.
source of an animal origin but, in all cases, dependence has This means that shrimp growth in ponds is achieved by the
been observed for protein of a marine origin, which might simultaneous feed consumption and endogenously pro-
be due to protein properties, and may be related with other duced food organisms, such as microalgae and microbial–
protein source components, such as fatty acid composition. detrital aggregates (Moss & Pruder 1995; Moss et al. 2001;
Forster et al. 2002; Tacon et al. 2002) to complete diet with
marine feed. In fact the shrimp culture that uses a biofloc
Innovative sources
system reduces dietary costs and dietary protein (30.3%
Nowadays, new protein sources, such as biofloc, insect meal CP), whereas the highest final weight, the highest weight
or algae, are being proposed for aquaculture nutrition, but gain and the lowest cost are observed in the shrimps fed a
have barely been checked in shrimp feeding (Table 3). 32.9% protein diet in semi-intensive systems (Jatob
a et al.

Table 3 New sources used as FM replacement. In the table is shown the effect on growth at maximum level of FM substitution that report similar to
superior growth or minimum level of FM substitution at growth decrease regarding FM based diet

New sources Weight Replacement PB FM % Growth Density/ Authors

(g) % diet diet effect culture system
%

Soy bean fermented Bacillus subtilis E20 0.172 <61.67 37.00 7.00 No effect 35/100 l Shiu et al. (2015)
Dried fermented biomass 0.59 50 35 9.8 Slight 10/340 l (exp) Qiu (2017)
decrease
Yeast 7.5 100 40 0 No effect 50/m2 (exp) Zhao et al. (2015)
Candida utilis 0.59 60 39.7 19 Increase 12/60 l (exp) Gamboa-Delgado et al.
(2016)
Biofloc 3 20 38.80 9 No effect 50/m2 (exp) Kuhn et al. (2016)
Biofloc 0.0023 15 43.74 Increase 3/l (exp) Dantas et al. (2014)
Biofloc + soy concentrate +shrimp head 2.48 100 38.00 0 No effect 35/m2 (exp) Bauer et al. (2012)
Biofloc meal 7.76 15 43.14 40 No effect 222/m3 Shao et al. (2017)
Biofloc meal PL1 ≤100* ≤43.8 Increase 50/l Khatoon et al. (2016)
Haematococcus pluvialis (micro alga) 1 12 32.00 13 Increase 50/m2 (exp) Ju et al. (2012)
Haematococcus pluvialis (micro alga) 1 50 32.00 7 No effect 50/m3 (exp) Ju et al. (2012)
Hypnea cervicornis and Cryptonemia PL10 100 30.00 0 No effect 20/10 l (exp) da Silva & Barbosa
crenulata + soy*meat bone meal (2009)
Green water meal (microalgae) 1.73 10 41.52 43.14 Decrease 20/50 l (exp) Basri et al. (2015)
Ulva lactuca 1.1 10 34 22 Decrease 6/40 l (exp) Rodr
ıguez-Gonz
alez
et al. (2014a,b)
Gracilaria parvispora 1.1 15 34 21 No effect 6/40 l (exp) Rodr
ıguez-Gonz
alez
et al. (2014a,b)
Ulva sp+ soy+protein concentrate 0.26 7 36.52 8 No effect 10/135 l (exp) Qiu (2017)
Arthrospira platensis (spirulina) Egg albumina 1 75 33.4 10.00 No effect 50/m2 (exp) Mac
ıas-Sancho et al.
(2014)
Mealworm 4.42 100 38.50 0.00 No effect 30/400 l (exp) Panini et al. (2017a)
Hermetia illucens 1.24 <20 35.00 25.00 No effect 50/m2 (exp) Cummins et al. 2017
Trichocorixa sp 0.5 25 of 22 (ref Decrease 25/104 m2 Mart
ınez-Co
rdova
diet diet) (exp) et al. (2013)

*Commercial diet replacement.

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anchez-Muros et al.

2014). The reduction in protein diet is substantial when Substrates like acetate and glycerol might promote the
comparing the culture in clear water and the biofloc sys- bacteria involved in cellular growth to increase the protein
tem: from 35% CP in clear water to 25% in biofloc (Xu & content in biofloc, whereas wheat flour may promote the
Pan 2012) Xu et al. (2012) have suggested that the pro- bacteria that produce large amounts of exopolysaccharides
moted bioflocs can improve growth performance and feed (Anand et al. 2014). Chlorophyll-dominated biofloc have
utilisation of cultured shrimps, probably by providing a been found to contain higher crude protein content (42%)
supplemental food source and enhancing feed digestion than the flocs dominated by diatoms (26–34%) and bacte-
and utilisation. ria (38%) (Ju et al. 2008).
Roy et al. (2009) observed no differences in growth, sur- Lipid content also depends on biofloc composition, and
vival or feed conversion rate in L. vannamei in an experi- algae and zooplankton are richer source of lipids than bac-
mental biofloc culture in an experimental biofloc culture in teria (Zhukova & Kharlamenko 1999). Of the 20 fatty acids
which fishmeal was replaced by other animal and plant detected in biofloc, palmitic acid, cis-vaccenic acid, linoleic
ingredients. acid and oleic acid are the dominant ones, and omega 3
There are several experiments in which the nutrients fatty acids have been detected at trace levels (Crab et al.
from the biofloc have been used directly as ingredients in 2010; Anand et al. 2014). The lower PUFA level in biofloc
shrimps. For example, Shao et al. (2017) replaced fishmeal may be due to the dominance of heterotrophic bacteria
with biofloc meal at 15%, and they did not observe differ- compared to PUFA-rich microalgal communities (Meyers
ences with the control group with fishmeal and that such & Latscha 1997). Martins et al. (2016) pointed out that the
biofloc meal can be considered a sustainable feed for microalgae diatoms developed in the biofloc can provide
shrimp. Khatoon et al. (2016) to breed L. vannamei post- essential fatty acids (especially EPA and linoleic) to shrimp.
larvae used dried waste biofloc to replace commercial feed The percentage of ash found in biofloc is high, which can
in a proportion of 25%, 50%, 75% and 100%. These be explained by the high salt content in the water system
authors found that, although 75% was comparable, 50% where bioflocs are produced (Ju et al. 2008). Nevertheless,
substitution produced better results in survival and growth the increased sodium content in diet does not apparently
than the commercial diet. affect the homoeostasis of shrimp (Bauer et al. 2012).
Accordingly, an ingredient that can be potentially used Studies about feeding shrimps with biofloc, included at
in shrimp feed is microbial floc meal (Kuhn et al. 2009, the 4–8% proportion, report beneficial effects on growth
2010). This product can be obtained from the effluent of performance and digestive enzymes (Anand et al. 2014).
super-intensive shrimp farms that use Biofloc Technology The presence of Bacillus sp. and Lactobacillus sp. indicates
Systems (BFT), which have been successfully used in the that biofloc can be considered a source of potential probi-
shrimp industry. Bioflocs are composed of microbial com- otics (Anand et al. 2014; Kuhn et al. 2016) have reported
munity growth gram-negative bacteria and Vibrionaceae, similar growth rates to controls at 20% replacement rates.
Bacillus sp. and Lactobacillus sp., with aggregates of partic- If biofloc is supplemented with soya, replacement can reach
ulate organic matter, zooplankton communities like cili- 100% FM (Bauer et al. 2012).
ates, rotifers and a small amount of autotrophic
microalgae. Similarly, Ballester et al. (2010) have reported
Algae
that biofloc is composed of attached heterotrophic bacteria,
filamentous cyanobacteria, dinoflagellates, ciliates, flagel- Currently, seaweeds and microalgae have drawn research-
lates and rotifers. However, biofloc composition depends ers’ attention for their potentiality as ingredients for aqua-
on various factors, like salinity, light and culture system feed. Numerous studies have evaluated their potential as
type. For example, algal communities in outdoor shrimp dietary protein ingredients for aquafeed (G€ uroy et al. 2013;
culture units dominate over bacterial biomass, whereas the Tibaldi et al. 2015; Zhu et al. 2016; Peixoto et al. 2017; de
autotrophic community dominated less in this study, Cruz et al. 2018; Vizca
ıno et al. 2015, 2018) with positive
which might be due to the lack of direct sunlight in biofloc effects on growth, fish utilisation and digestion physiology.
outdoors (Ju et al. 2008) In general, shrimp diets are supplemented with microalgae
Biofloc nutritional composition varies with carbohydrate (Boonyaratpalin et al. 2001; Supamattaya et al. 2005; Ju
source type, the microbial community structure, culture et al. 2009, 2012; Pakravan et al. 2017), macroalgae (Yeh
condition, etc. For instance, Crab et al. (2010) have et al. 2006; Niu et al. 2018), probiotics (Ziaei-Nejad et al.
observed that the biofloc developed from glycerol and inoc- 2006; Wang 2007; Yang et al. 2010), prebiotics (Zhang
ulated with Bacillus contains higher protein (58% CP) than et al. 2012) and periphyton (Anand et al. 2013) to improve
that developed from glycerol, acetate (42–43% CP) and growth, the immune response and the activity of digestive
glucose (28% CP). enzymes, but not as FM replacements.

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 Innovative protein sources to shrimp feed

From a nutritional point of view, seaweeds chemical performance was obtained in shrimp fed with the diet of
composition varies with species, physiological status and 10–20% substitution. Guti
errez-Leyva (2006) has reported
environmental conditions. In general, macroalgae are rich an improved SGR in L. vannamei feed for a diet with 10%
in non-starch polysaccharides, vitamins and minerals inclusion of Macrocystis or Sargassum meals. FM replace-
(Mabeau & Fleurence1993; Wong & Cheung 2000) and ment with Hypnea cervicornis and Cryptonemia crenulata in
moderate protein content, with 3–15 g 100 g dry weight 1 shrimp diets at different percentages (39%, 26% and 13%)
in brown algae, and approximately 10–47 g 100 g dry has shown no significant differences between treatments
weight 1 in green or red algae (Arasaki & Arasaki 1983). and control diet in terms of final biomass, biomass gain
The amino acid profile has been frequently studied and and SGRs (da Silva & Barbosa 2009). Similarly, the FCR
compared to other widely used ingredients in aquaculture improves with higher algae content: the inclusion of Hyp-
nutrition, such as soya bean meal. Some authors have con- nea cervicornis and Cryptonemia crenulata meals at high
firmed that algal protein is relatively rich in alanine, gly- levels has exhibited better feed conversion than diets with
cine, methionine and valine, and poor in aspartic acid, lower contents (da Silva & Barbosa 2009). Regarding the
glutamic acid and serine (Van den Burg et al. 2012), while protein efficiency ratio (PER), positive results have been
others have defended that its amino acid profile is charac- found after including seaweed in white shrimp L. vannamei
terised by a marked aspartic and glutamic acid content (Cruz-Su
arez et al. 2000), which varies among species.
(Flourence 1999). The lipid content is generally low, sea- Shrimps fed a Ulva diet present a higher PER than those
weeds present around 0.3–7.2 g 100 g dry weight 1. How- fed diets containing Macrocystis and Ascophyllum meals
ever, the fatty acid composition varies greatly, both (Cruz-Su
arez et al. 2008). In contrast, other studies have
between and within the different phyla (Mæhre 2015). In concluded that supplementing Gracilaria bursa-pastoris,
general, seaweeds are good source of high polyunsaturated Ulva rigida, Gracilaria cornea and Ascophyllum in feed with
fatty acids (HUFA) as eicosapentaenoic acid (EPA, 20:5n- sea bass that does not modify the PER (Nakagawa 1997;
3), arachidonic acid (ARA, 20:4n-6), stearidonic acid Valente et al. 2006). It is difficult to draw conclusions
(8:4n-3) and a-linolenic acid (18:3n-3) (Miyashita et al. about digestibility because published results are unclear,
2013). In addition, seaweeds are rich in non-starch polysac- and different authors have reported that digestibility
charides, vitamins and minerals (Mabeau & Fleurence1993; increases or decreases depending on alga or shrimp weight
Wong & Cheung 2000). (Cruz-Su
arez et al. 2008). On the other hand, freeze-dried
Numerous works have reported that the inclusion of sea- biomass of several microalgae species also arise as an alter-
weeds meal improves growth, feed intake and protein effi- native ingredient of interest in aquaculture nutrition. A
ciency at low inclusion levels (<10%) (see the review by high protein with an adequate amino acid profile charac-
Cruz-Su
arez et al. 2008). A significant increase in the terises their chemical composition. Their protein content
growth rate in white shrimp (L. vannamei) juveniles has ranges from 30 to 55 g 100 g dry weight 1 (L
opez et al.
been observed in 2–4% diet content of Macrocystis pyrifera. 2010), with values around 70 g protein 100 g dry weight 1
Nevertheless, at higher inclusion levels of 4–8%, no signifi- in some species like Spirulina (Arthrospira) sp., Scenedesmus
cant increase in weight has been observed (Cruz-Su
arez sp. and Chlorella sp. (Venkataraman & Becker 1985).
et al. 2000). Qiu et al. (2018) reported that Ulva sp. can be Notwithstanding, very little information about the
included in the shrimp diet up to 6.35% to replace 2% fish- digestibility of macro- and microalgae protein for shrimp is
meal without negative effects on growth. However, the available (Tibbetts et al. 2017). In addition, their fatty acid
results with moderate and high inclusion levels of seaweed profile and, especially the large amount of essential polyun-
meals are somewhat inconsistent. Rodr
ıguez-Gonz
alez saturated fatty acids, such as EPA, ARA or DHA, also play a
et al. (2014a,b) evidenced that 10% and 15% dietary inclu- key role in the evaluation of their nutritional quality
sion level of U. lactuca meal significantly reduced the (Reitan et al. 1997).
weight gain of Pacific white shrimp, whereas shrimp fed In the last two decades, many studies have focused on
with diets containing similar levels of Gracilaria parvispora using microalgae in fish and also shrimps nutrition. Most
did not show growth depression. Yang et al. (2018) of them have revealed that the dietary inclusion of microal-
reported a decrease on growth and nutrient utilisation of gae has no negative effects on growth and development. Ju
juvenile Pacific white shrimp fed diet supplemented with et al. (2012) have observed that the shrimps fed a diet with
30% of five different seaweeds (Saccharina japonica, Por- 12.5% FM protein replaced with defatted Haematococcus
phyra dioica, Gracilariopsis lemaneiformis, Ulva lactuca and pluvialis show a significantly higher growth rate and a lower
Undaria pinnatifida). feed conversion ratio than those that received the control
Anh et al. (2018) suggested that green seaweed Clado- diet. Other authors like Pacheco-Vega et al. (2018) demon-
phora could replace up to 30% of fishmeal protein in the strate that low dietary inclusion levels of microalgal bio-
tiger shrimp postlarvae diet, however, the optimal mass (Schizochytrium sp. and Grammatophora sp.) in diets

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M. J. S

anchez-Muros et al.

for Penaeus vannamei elicit similar or higher growth rates levels than FM and no traces of DHA, except for Clistoro
than diets based on a fishmeal only and observed that that magnifica, which presents 34% of total lipids (Hanson et al.
microalgae actually contributed protein to tissue accretion. 1985). However, high levels of EPA, but not of DHA, have
Similarly, Pakravan et al. (2017) have demonstrated the been detected in aquatic insects (S
anchez-Muros et al.
effectiveness of microalgae Spirulina platensis (Arthorspira 2014). It is possible to enrich the fatty acids profile of Her-
platensis) as a reliable protein source for replacing fishmeal metia illucens with n-3 Hufas by rearing and using diets
in shrimp aquaculture. Their study shows no significant rich in these n-3 fatty acids (Barroso et al. 2017).
differences on growth parameters and proximate composi- Only a few experiments have been run to study the effect
tion with 100% FM replacement. Kohal et al. (2018) sug- of replacing FM with insect meal in L. vannamei diets. The
gested that dietary inclusion of S. platensis meal at a level of housefly has been checked by Cao et al. (2012a), which
8–10% can improve the growth, survival and, in particular, limits FM replacement with housefly meal by 40%, and the
reproductive performance of red cherry shrimp in com- maximum level should not exceed 60%. The SGR tends to
mercial aquaria during maturity only up to the sixth lower with housefly inclusion, with no changes found in
spawning event. In addition, a marked influence on average muscle nutritional composition or digestive enzyme activi-
survival rate by the inclusion levels of S. platensis was ties. However, pathological changes in the histological
observed, showing positive supplementary effects of the structure of the hepatopancreas have been observed with
diets formulated with microalgal biomass. In fact, earlier replacement levels over 60% (Cao et al. 2012b). In another
works found significant improvement in immunological experiment that included lower replacement proportions,
factors in Pacific white shrimp when fishmeal was replaced e.g., 5%, 10% and 15% of FM for housefly larva meal, Li
with S. platensis meal, indicating that microalgae may stim- et al. (2012) obtained no significant differences in growth
ulate and/or enhance the immune system of shrimp (Kohal performance between the control diet and the 5% and 10%
et al. 2018). replacing diets, but found very significant differences in
In addition, the microalgae culture is widespread and growth performance between the control and the 15%
performed to obtain pharmaceutical products like astaxan- replacing groups.
thin, b-carotene, lutein, carotenoid, omega-fatty acid and In a control diet (35% protein) containing 25% FM and
biodiesel. 23% soya bean meal, Cummins et al. (2017) have evaluated
the progressive replacement of protein from FM with black
soldier fly (Hermetia illucens) larvae meal at the 7%, 14%,
Insects
21%, 28% and 36% inclusion rates of diet. They conclude
In the last 10 years, several studies on feeding experiments that the maximum limit of inclusion of H. illucens in diet is
have been conducted in vivo with diets based on insect meal <25% to obtain no differences in shrimp final weight,
in different fish species (Achionye-Nzeh & Ngwudo 2003; weight gain, the SGR and food conversion with the control
Alegbeleye et al. 2012; Aniebo et al. 2011; Fasakin et al. diet. They consider that the main problem is essential
2003; Sealey et al. 2011; St-Hilaire et al. 2007; S
anchez- amino acids (EAA) deficiencies and EAA/nonessential
Muros et al. 2016; Ogunji et al. 2006; Kroeckel et al. 2012; amino acids (NEAA) imbalances. They also consider it nec-
among others). Although insects are rich in protein and essary for future strategies to increase its use in order to
lipids, the presence of chitin a priori indicates a negative estimate limiting amino acids in the insect and to supple-
characteristic because it affects digestibility (Barroso et al. ment them.
2014). Nonetheless, Ramos-Elorduy et al. (1981) have The performance of L. vannamei is not affected by
determined the digestibility of several edible insect species replacing 100% FM with mealworm meal in diet if meal-
from Mexico, and digestibility varied among species from worm meal is supplemented with methionine. Moreover,
77.9% to 98.9% for organic matter, and from 45% to when FM is replaced with mealworm meal, shrimp body
66.9% for proteins, which composes more than 60% for lipid levels rise with no significant changes in protein con-
most species. Insects’ protein content is generally lower tent (Panini et al. 2017b). Conversely, Mart
ınez-C
ordova
than that of FM and it is similar to soya bean meal, while et al. (2013) have reported a minor weight gain in shrimp
the profile of amino acids is related to the taxonomic feed with a 25% reference diet by live Trichocorixa sp.
group, with Diptera being the most similar to FM in essen- Weight gain lowers with an increase in the replacement of a
tial and limiting amino acids terms (Barroso et al. 2014). reference diet with live insects.
Development stage may also affect fat content. Larvae gen-
erally contain significantly more fat than adults (Barker
Yeast
et al. 1998), which seems to vary between stages, and usu-
ally ranges between 15% and 30% (Barroso et al. 2014). FM replacement with yeast has been proved in different fish
Regarding the fatty acids profile, insects have lower n-3 species with contradictory results (Oz

orio et al. 2012). In

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194 © 2018 Wiley Publishing Asia Pty Ltd
 Innovative protein sources to shrimp feed

shrimp, yeasts have been tested as an additive (probiotic) and nutritious foods, which should be tested in future
with very good results (Deng et al. 2013; Sarlin & Philip research. Algae consume much less fresh water than con-
2016). Jin et al. (2018) compared a control diet (without ventional feedstock-based biodiesel production (vegetable
yeast) with two experimental feeds, containing 1% hydrol- oil and animal fats), and microalgae can grow in seawater
ysed yeast and 1% brewer’s yeast, respectively. The findings or wastewater (Groom et al. 2008), and purify air sulphur
in this study clearly demonstrated that the experimental dioxide (NO2) and nitrogen monoxide (NO) (Brown
feeds (1% yeast hydrolysate or brewer’s yeast supplementa- 1996). Insects can be used to recycle waste, be reared by
tion) improved not only growth, but also innate immunity, employing fewer resources (food, water, space) than those
and ammonia nitrogen resistance of L. vannamei. of poultry, swine and beef, and emit low greenhouse gas
A few experiments have been run using yeasts to replace levels (Raubenheimer and Rothman 2012; van Huis, 2013).
FM, but reveal that the growth and survival rates are statis- Accordingly, we can argue that the ecological footprint of
tically similar in the shrimp fed on all mixed diets with tor- insect and algae production as food is fairly low (Blonk
ula yeast. This, therefore, indicates the suitability of this et al. 2008). Microalgae, insects and yeasts offer another
single cell protein as a dietary ingredient in diets containing excellent advantage as their nutritional value can be modi-
up to 60% of this yeast (Gamboa-Delgado et al. 2016). fied through the culture system, or even by genetic manipu-
lation (as in yeasts).
In short, it is perceived that these protein alternatives
New protein sources versus traditional sources
have an enormous potential, which will allow shrimp farm-
FM replacement with other protein sources is an important ing to grow with less pressure on FM. However, future
research field in the shrimp culture in particular, and in research is necessary to determine which insect or micro-
aquaculture in general, and has allowed to lower FM inclu- alga species are the most suitable, in what proportions they
sion in shrimp diet. Nevertheless, the use of these sources should be included in diets and how their nutritive value
entails nutritional, availability and ecological problems. increases.
In general, most new ingredients present lower digestibil-
ity than typical sources, an unbalanced amino acids profile
and HUFAS n-3 deficiency. In order to increase their nutri- Acknowledgements
tional value, these ingredients must be manipulated (added The authors thank Helen Warburton (HyA) for revising
enzymes or amino acids, submitted to hydrolysis, etc.), the English. This work was supported by the European
which implies a rise in prices at least. Regional Development Fund (FEDER), the Campus de
Availability is another problem with these alternative Excelencia Internacional Agroalimentaria (CEI3), the Cam-
ingredients because most are by-products and quantity is pus de Excelencia Internacional del Mar (CEImar) and the
determined by original product production. They are Secretar
ıa de Educaci

on Superior, Ciencia, Tecnolog
ıa e
mostly local products whose production and distribution Innovaci
on (SENESCYT), Programa Prometeo (Ecuador).
area are limited.
Products like soya pose major ecological problems, such
as deforestation of areas with a high biological value (Car- References
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