Reviews in Aquaculture, 1–16 doi: 10.1111/raq.

12368

Application of fermentation strategy in aquafeed for

sustainable aquaculture
Mahmoud A.O. Dawood1 and Shunsuke Koshio2
1 Department of Animal Production, Faculty of Agriculture, Kafrelsheikh University, Kafrelsheikh, Egypt
2 Laboratory of Aquatic Animal Nutrition, Faculty of Fisheries, Kagoshima University, Kagoshima, Japan

Correspondence
Mahmoud A.O. Dawood, Department of
Animal Production, Faculty of Agriculture,
Kafrelsheikh University, 33516 Kafrelsheikh,
Egypt. Email: Mahmouddawood55@
gmail.com
Received 4 April 2019; In Revised form 10 June
2019; accepted 17 June 2019.
Abstract
Because of its high nutritional value, palatability and increased digestibility, fishy
meal is widely used as an animal protein source in the aquafeed industry. How-
ever, the resource shortages and rising prices seriously restrict the use of fish meal
(FM) in aquaculture. In this light, much efforts have been conducted to seek the
sustainable supplies of protein sources to substitute FM. Due to their relatively
low protein content and palatability, the presence of anti-nutritional factors
(ANFs) and unbalanced amino acid profiles, the plant protein sources have been
limited in aquafeed, whereas the animal protein sources can replace FM in aqua-
feed due to their high protein content, total digestible dry matter and lack of
ANFs. The fermentation process was recognized for its role in improving the
nutritional quality of animal and plant protein sources. The protein sources can
be treated with appropriate microorganisms to preserve its nutrients and finally
incorporated into aquafeed, which would reduce feed costs and environmental
pollution. Fermented meals showed better nutrient efficiency and could improve
the nutritional value of aquafeed. This review was intended to present more
updated information about the application of fermented ingredients in aquafeed
industry. Based on the data collected, this review will contribute to further
research into the production of fermented feed as a functional feed for sustainable
aquaculture.
Key words: aquafeed, fermentation, fish meal, plant proteins, sustainable aquaculture, uncon-
ventional ingredients.

several of the ANFs are heat stable. Previous studies showed

Introduction
Cost of feeding is contributed with approximately 70% of
the total running expenses in aquaculture (Dossou et al.
2018a,2018b). The prices of aquafeed are increasing dra-
matically nowadays which will result in raising the total
cost required to produce aquatic animals (El Basuini et al.
2016, 2017; Hossain et al. 2016). Alternative strategies were
applied to replace the traditional feed ingredients with
unconventional ingredients (Yan et al. 2017a). Unconven-
tional ingredients are relatively available with low prices
but limited to include in aquafeed in its pure form due to
the high fibre and antinutritional factors (ANFs) contents
which decreased the digestibility of feed (Wu & Muir 2008;
Bu et al. 2018). Techniques including heat treatment and
microbial fermentation have been used to eliminate or
reduce ANFs (Peres et al. 2003; Liang et al. 2008). However,
that fermentation increased the content of crude protein
and decreased the content of crude fibre, ANFs and toxic
contents in feed ingredients (Drew et al. 2007; Imorou
Toko et al. 2008; Jakobsen et al. 2015).
In livestock and poultry nutrition, fermentation process
was successfully applied (Chiang et al. 2009). Fermentation
is based on using of microorganisms that can exhibit its
beneficial role if reared under specific conditions (Siddik
et al. 2018; Sugiharto & Ranjitkar 2019). Prior to feeding
the microorganisms can decrease the risk of aflatoxins in
feed ingredients (Mohamed et al. 2017; Mwihia et al. 2018).
In addition to their role as probiotics, beneficial microor-
ganisms can synergistically benefit the gastrointestinal tract
(GIT) organisms, which help to increase the digestibility of
feed in aquatic animals (Niba et al. 2009; Dawood et al.
2015a; Xie et al. 2016). Aquatic animals can therefore

© 2019 Wiley Publishing Asia Pty Ltd 1

M. A. O. Dawood and S. Koshio
exhibit increased feed efficiency, growth performance,
immunity and tolerance to various farming stressors
(Moniruzzaman et al. 2018; Jannathulla et al. 2019).
Unconventional fermented feedstuffs can partially or totally
replace fish meal (FM) to further reduce the cost of produc-
tion (Van Vo et al. 2015; Ilham & Fotedar 2017; Siddik et al.
2018). Unconventional feedstuffs are credited for being cheap
to purchase, by-products or waste products from agriculture,
farm made feeds and processing industries and can serve as a
form of waste management in enhancing good sanitation.
These include all types of feedstuffs from animal (silkworm,
maggot, termite, grub, earthworm, snail, tadpoles, etc.), plant
wastes (jack bean, cottonseed meal, soybean meal, cajanus,
chaya, duckweed, maize bran, rice bran, palm kernel cake,
groundnut cake, brewers waste, etc.) and wastes from animal
sources and processing of food for human consumption such
as animal dung, offal, visceral, feathers, fish silage, bone, blood
(Abowei & Ekubo 2011). The major limitation factors of
using unconventional dietary feed ingredients are the high
fibre content and low protein content (Jannathulla et al.
2017a,2017b). Fermentation is helping in improved availabil-
ity of vitamins and protein solubility and amino acid patterns
as well as increasing the feedstuff palatability (del Carmen
Flores-Miranda et al. 2015; Zhang et al. 2017; Dawood &
Koshio 2018). Fermentation can also increase the digestibility
of organic matter, nitrogen, amino acids, fibres and calcium
(Sun et al. 2015; Hassaan et al. 2018). Various types of
microorganisms, including bacterial (Bacillus Sp.; Enterococcus
Sp. and Lactobacillus Sp.) cells, yeasts (Saccharomyces) and
fungal cells (Aspergillus Sp.) have been used during fermenta-
tion (Mukherjee et al. 2016). The potential substitute for FM
is to use cheap, available and alternative fermented protein
sources that improve resistance to diseases in aquatic animals
by enhancing growth, innate defence mechanisms and well-
being for the continued expansion of the global aquaculture
industry (Ha et al. 2019; Jannathulla et al. 2019; Siddik et al.
2019). Unlike poultry and livestock, the available literature on
aquatic animal fermented feed is still rather limited.
This review aims at gathering most of the recommenda-
tions that applied the fermentation process in the prepara-
tion of feed ingredients to improve the quality of aquafeed.
The results of these studies will be of interest for the nutri-
tionists and farmers in order to sustain the aquaculture
industry. The results of this review will also provide a stan-
dard feed-processing protocol and identify research gaps in
aquafeed fermentation at the laboratory and field levels.
Methods of fermentation
Solid-state fermentation (SSF) and submerged fermenta-
tion (SmF) are the two major methods used for fermenta-
tion (Subramaniyam & Vimala 2012). The SSF method
depends on the inclusion of grains, rice, rice bran and
2 © 2019 Wiley Publishing Asia Pty Ltd
wheat bran without free-flowing liquid to produce fer-
mented dry ingredients that can be added to the formula-
tion whether as a whole grain or as a powder form.
Aspergillus spp., Rhizopus spp., some Lactobacillus spp. are
the major microorganisms that can be used in the SSF
method (Subramaniyam & Vimala 2012). SSF fermentation
method by Lactobacillus fermentum, Saccharomyces cere-
visiae and Bacillus subtilis mixture resulted in increased
counts of lactic acid bacteria and reduced enterobacteria in
the fermented feed (Hu et al. 2008).
SmF method on the other hand is based on the growth
of microorganisms in an aqueous medium (Shim et al.
2010). The SmF method is the reasonable method that can
be used for probiotics preparations (Shim et al. 2010),
whereas the SSF method is used for enzymes, organic acids
and bio-pesticides production (Lu et al. 1998; Battan et al.
2006).
Fermentation requirements
Microorganisms
Different forms of microorganisms have been used in fer-
mentation including, bacterial cells (Bacillus sp., Enterococ-
cus sp. and Lactobacillus sp.), yeasts (Saccharomyces) and
fungi (Aspergillus sp.) (Mukherjee et al. 2016) (See Tables 1
and 2).
Microorganisms used in the fermentation process have
different species that have produced various products, ‘for
example Lactic acid, ethanol or acetic acid’ since separate
microorganisms may respond to each substrate differently
(Niba et al. 2009). Following this hypothesis Lactobacillus
can produce lactic acid, citric acid, whereas yeasts produce
ethanol and CO2 (Subramaniyam & Vimala 2012).
Substrates
The type and nature of substrates can affect the final pro-
duct of fermentation (Subramaniyam & Vimala 2012). As
mentioned above that the SmF method requires free-flow-
ing liquid substrates ‘for example broth media, molasses,
whey and wet distillers’ grains’, whereas SSF method free-
flowing liquid (Sugiharto & Ranjitkar 2019). Generally, fer-
mented liquid feed can be produced by mixing feed stuffs
with water or liquid by-products.
Environmental conditions
The basic function of a fermenter is to provide a suitable
environment in which an organism can efficiently act its
role in fermentation. Microbes bring about fermentation
by secreting certain enzymes which have an optimum tem-
perature (Sugiharto & Ranjitkar 2019). Initial pH of the
fermentation medium must be very well optimized depend-
ing on the microbe substrate, organism and production
technique. The quality of fermentation is depending on
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 Fermentation process and aquafeed

Table 1 Fermented plant protein sources for aquafeed

Aquatic animal Plant protein Results Microorganism Reference

Atlantic salmon Soybean white Lactic acid fermentation improved the nutritional Lactobacillus brevis Refstie et al.
(Salmo salar) flakes value of soybean white flakes (2005)
Rainbow trout Soybean meal Fermented soybean meal is a promising ingredient as Bacillus spp. Yamamoto et al.
(Oncorhynchus the main protein source in a non-FM diet for (2010)
mykiss) rainbow trout
Turbot (Scophthalmus Soybean meal The results of this study indicate that fermented Lactobacillus plantarum P8 Wang et al. (2016)
maximus L.) soybean meal could replace up to 45% of FM
protein in juvenile turbot diet
Penaeus vannamei Soybean meal Fermented ingredients could be used as potential Aspergillus niger Jannathulla et al.
and sunflower protein sources rather than untreated materials in (2018)
oil cake the diet of P. vannamei
Penaeus vannamei Guar meal Fermented ingredients could be used as potential Aspergillus niger Jannathulla et al.
protein sources rather than untreated materials in (2017a)
the diet of P. vannamei
Penaeus vannamei Plant protein Fermented ingredients could be used as potential Aspergillus niger Jannathulla et al.
sources protein sources rather than untreated materials in (2017b)
the diet of P. vannamei
Indian prawn shrimp Soybean meal Fermented ingredients are an acceptable alternative Saccharomyces cerevisiae Sharawy et al.
(Fenneropenaeus plant protein source that can replace up to 50% of (2016)
indicus) dietary FM protein in diets of Indian white shrimps
White shrimp Soybean meal The maximal replacement levels of FM in shrimp diet Bacillus subtilis E20 Shiu et al. (2015)
(Litopenaeus with soybean meal and fermented soybean meal
vannamei) were 37.42% and 61.67% respectively
Pacific white shrimp Cottonseed Up to 50% of FM can be replaced by fermented Bacillus subtilis BJ-1 Sun et al. (2016)
(Litopenaeus meal cottonseed meal without adverse effects on growth
vannamei) and feed utilization of L. vannamei
Red sea bream (Pagrus Rapeseed meal Fermented rapeseed meal can successfully substitute Saccharomyces cerevisiae Dossou et al.
major) up to 56.25% of FM protein without negative (2018a)
effects on growth, nutrient utilization, innate
immune response or oxidative stress of juvenile red
sea bream
Parrot fish Soybean meal The fermentation process of soybean meal could Aspergillus oryzae Kim et al. (2009)
(Oplegnathus enhance the absorption of phosphorus and non-
fasciatus) specific immune responses in juvenile parrot fish
Olive flounder Soybean meal Microbial fermentation of soybean, which also can Aspergillus oryzae Kim et al. (2010)
(Paralichthys be simply adapted for soybean meal, is a promising
olivaceus) method for increasing phosphorus availability in
soybean meal, antioxidant activities in diets and
nonspecific immune response of olive flounder
Rockfish (Sebastes Soybean meal 10% of FM can be replaced by fermented soybean Bacillus subtilis Lee et al. (2016)
schlegeli) meal without negatively affecting juvenile rockfish
performance
Asian sea bass (Lates Canola meal 50% of FM in the diet of Asian sea bass could be Saccharomyces cerevisiae Plaipetch and
calcarifer) (Bloch, replaced by yeast-fermented canola meal without Yakupitiyage
1790) overall impact on growth (2012)
Nile tilapia Canola meal Fermented canola meal can replace dietary soybean Saccharomyces cerevisiae Plaipetch and
(Oreochromis meal for Nile tilapia without any reduction in Yakupitiyage
niloticus) (Linnaeus growth, survival rate, feed intake and feed (2014)
1758) conversion ratio
Nile tilapia Soybean meal Up to 37.4% FM in diets could be replaced by Saccharomyces cerevisiae Hassaan et al.
(Oreochromis fermented soybean meal without any adverse (2015)
niloticus) effect on growth performance, nutrient digestibility
and physiological condition
Black sea bream Soybean meal Up to 40% FM in the diets of juvenile black sea Bacillus subtilis Azarm and Lee
(Acanthopagrus bream could be replaced by fermented soybean (2014)
schlegeli) meal

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M. A. O. Dawood and S. Koshio

Table 1 (continued)

Aquatic animal Plant protein Results Microorganism Reference

Macrobrachium Soybean meal M. nipponense growth performance was not Mixture of microorganism Ding et al. (2015)
nipponense affected by including a high proportion of (Pediococcus acidilactic,
fermented soybean meal in the diet Enterococcus aecalis,
Saccharomyces cerevisiae,
Candida utilis, Bacillus
subtilis, Bacillus
licheniformis,
Rhodopseudomonas
palustri).
Black sea bream Soybean meal Up to 20% of dietary FM protein could be replaced Candida utilis Zhou et al. (2011)
(Acanthopagrus by fermented soybean meal protein in the diets of
schlegelii) juvenile black sea bream
Pacific white shrimp Duckweed FM can be replaced with up to 35 % fermented Bacillus pumilus and del Carmen Flores-
(Litopenaeus (Lemna sp.) duckweed without adversely affecting the survival Pediococcus pentosaceus Miranda et al.
vannamei) and growth performance of cultured shrimp (2015)
Red sea bream (Pagrus Rapeseed meal At a moderate level (25% and 50%), substitution of Aspergillus oryzae Dossou et al.
major) FM by the fermented rapeseed meal promoted (2018b)
growth, nutrient utilization and exerted immune
responses and anti-oxidative effects in red sea
bream
Japanese flounder Soybean meal Fermented ingredients can replace 36% FM protein Bacillus spp. Abdul Kader et al.
(Paralichthys and squid by- in the diet of Japanese flounder (2012)
olivaceus) product
White shrimp Soybean meal Replacing 25% FM protein with fermented soybean Lactobacillus spp. Lin and Mui
(Litopenaeus meal significantly reduces non-specific immune (2017)
vannamei) responses and induces oxidative stress in white
shrimps
Barramundi (Lates Lupin (Lupinus the fermentation by Lactobacilli improved the lupin’s Lactobacillus spp. Van Vo et al.
calcarifer) angustifolius) nutritional quality, allowing higher inclusion level in Lactobacillus acidophilus, (2015)
barramundi diets L. aporogenes, and
L. kefiri
Barramundi (Lates Lupin meal Fermented lupin meal has an obvious potential to Saccharomyces cerevisiae Ilham and Fotedar
calcarifer) substantially replace 75% FM protein in the diets of (2017)
barramundi
Rainbow trout Soybean meal Solid-state fermented protein concentrates could Bacillus subtilis U304 Moniruzzaman
(Oncorhynchus replace up to 30% of high FM protein in the diet of et al. (2018)
mykiss) rainbow trout without compromising the growth
and health status of fish
Penaeus monodon Soybean meal, It could be concluded that the fungal fermented Aspergillus niger Jannathulla et al.
and Penaeus indicus groundnut oil plant proteins are highly suitable for the (2019)
cake, rapeseed formulation of diets and could be considered as
meal and very good protein sources for both P. monodon
sunflower oil and P. indicus
cake
Nile tilapia Jatropha curcas Up 50% of FM can be replaced by Jatropha curcas Bacillus licheniformis and Hassaan et al.
(Oreochromis seed meal seed meal in Nile tilapia diets Bacillus pumilus (2017)
niloticus)
Nile tilapia Sunflower meal It is possible to replace animal protein in tilapia Saccharomyces cerevisiae Soltan et al.
(Oreochromis fingerlings diets with fermented sunflower seed (2015)
niloticus) meal, with optimum growth response at a 25%
substitution level
Nile tilapia Sunflower meal Replaced FM by fermented sunflower meal up to Saccharomyces cerevisiae Hassaan et al.
(Oreochromis 50% not affected the growth and physiological and Bacillus subtilis (2018)
niloticus) indices

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 Fermentation process and aquafeed

Table 1 (continued)

Aquatic animal Plant protein Results Microorganism Reference

Nile tilapia Cottonseed The findings suggest that microbial fermentation of Aspergillus oryzae Lim and Lee
(Oreochromis meal cottonseed meal with Aspergillus oryzae can (2011)
niloticus) enhance antioxidant activities in diets and fish, and
effectively reduce or degrade the toxicity of
gossypol present in cottonseed meal. A microbial
fermentation could make plant protein sources
more useful and functional in feeds for fish
Olive flounder Cottonseed The fermentation of cottonseed meal by Aspergillus Aspergillus oryzae Lim et al. (2010)
(Paralichthys meal oryzae could increase antioxidant activities in feed
olivaceus) and fish and effectively degrade toxic gossypol in
cottonseed meal
Black sea bream Cottonseed Up to 16% fermented cottonseed meal can be used Bacillus subtilis BJ-1 Sun et al. (2015)
(Acanthopagrus meal to replace FM in diets for black sea bream with the
schlegelii) optimal dietary level restricted to 3.11%
Crucian carp Mushroom bran 64%-80% proportion of dietary FM with fermented Ganodermalucidum and Zhang et al.
(Carassius auratus hydrolysate mushroom bran hydrolysate could improve the Saccharomyces cerevisiae (2017)
gibelio) growth, digestive enzyme activity and antioxidant
capacity of crucian carp

Where FM means fish meal.

several conditions ‘for example temperature, pH, the nat-
ure and composition of the medium, dissolved O2 and
CO2, operational systems, addition of precursors, mixing
(cycling through varying environments) and fermenter
shear rates and the length of the fermentation process’.
Fermented plant protein sources
With the expansion of the aquaculture activity, alternative
protein sources are required in order to decrease the usage
of FM as the main protein source in aquafeed. The cost of
feeding is another main challenge that needs to be consid-
ered during the preparation of formulations to feed aquatic
animals (Moss et al. 2019; Wang et al. 2019). Soybean
meals and rapeseed/cottonseed meals are among the main
plant protein sources that can be used due to their avail-
ability, rich amino acid profiles, low prices and sustainable
nature (Hardy 2010; Dossou et al. 2019). The presence of
ANFs, high fibre content and toxic compounds are affect-
ing the palatability of these ingredients in its pure form by
aquatic animals (Makkar 1993; Yamamoto et al. 2010).
Anti-nutritional factors have been defined as ‘substances
which by themselves, or through their metabolic products
arising in living systems, interfere with feed utilisation and
affect the health and production of animals’ (Makkar
1993). ANFs have been classified into: (i) factors affecting
protein utilisation and digestion (protease inhibitors, tan-
nins and lectins), (ii) factors affecting mineral utilisation
(include phytates, gossypol pigments, oxalates and glucosi-
nolates), (iii) antivitamins, (iv) miscellaneous substances
(mycotoxins, mimosine, cyanogens, nitrate, alkaloids, pho-
tosensitizing agents, phytooestrogens and saponins)
(Francis et al. 2001). Most ANFs do not lead to mortality,
but can generate negative physiological impacts, reduced
growth and health condition. Reduced feed utilization,
hypoglycaemia, pancreatic hypertrophy, liver damage and
other pathological lesions are observed (Hajra et al. 2013).
However, the severity of any of these aspects relies on the
amount of ingested ANFs, the animal species, their age, size
and other physiological condition.
To solve this problem, fermentation by microorganisms
are suggested to increase the acceptability of aquatic ani-
mals to fermented plant protein sources as following:
Fermented soybean meal
Fermentation of soybean meal (SBM) can increase the
nutritional value, nutrient availability ‘for example, small-
sized peptide, calcium and vitamin A’ (Kim 1999). The fer-
mentation process can also reduce the level of trypsin inhi-
bitor content which affecting its availability and
digestibility in the GIT of aquatic animals (Hong et al.
2004; Refstie et al. 2005).
SBM can be fermented by a fungus or a bacterial strain
(Table 1). The fermentation process can be done by SSF or
SmF methods depending on its state ‘that is crude without
any alteration of moisture content or texture of SBM’.
Much like SmF fermentation, the process related to SSF fer-
mentation has been reported to enhance the nutritional
quality of SBM that can be used in aqua-feed and animal
feed industries (Lena et al. 1997). Fermentation then can
increase the peptides content, fibrinolytic enzyme activity,
in vitro trypsin digestibility and nitrogen solubility and
reduce ANFs which resulted in increased feed efficiency in
aquatic animals (Mukherjee et al. 2016; Sharawy et al. 2016;

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M. A. O. Dawood and S. Koshio

Table 2 Fermented animal protein sources for aquafeed

Aquatic animal Animal protein Results Microorganism Reference

Labeo rohita Slaughter house 21.11% replacement of FM by the fermented blend Lactobacillus acidophilus Samaddar
blood and fish was ideal for optimum growth of L. rohita (NCIM 2903) et al. (2015)
offal blend
Catfish (Mystus Fish-offal meal Fish-offal meal could be effectively used to partially Lactobacillus sp., Samaddar
vittatus) (Bloch) replace FM in the diet of M. vittatus Rhodopseudomonas sp., et al. (2011)
Azotobacter sp. and
Saccharomyces sp.
Major carp (Labeo Mulberry leaf and The fermented mixture that could successfully Lactobacillus sp., Kaviraj et al.
rohita) fish offal replace up to 80 % of FM in the diet formulation Rhodopseudomonas sp., (2013)
Azotobacter sp. and
Saccharomyces sp.
Catfish Fish-offal meal Fish-offal meal could be included up to a 30% level The microbial suspension Mondal et al.
(Heteropneustes as a partial (50%) replacement of FM in the (EMTM) (2008)
fossilis) formulation of diet for H. fossilis
Indian major carp, Fish-offal meal 50% replacement of FM is possible when 30% is The microbial suspension Mondal et al.
rohu (Labeo rohita) fermented along with is used as ingredient in the (EMTM) (2007)
[Hamilton] formulated diet
Catla catla (Hamilton) Poultry feather 30 % poultry feather meal and 10 % FM, replacing Bacillus cereus Mondal (2014)
meal 75% of FM if hydrolysed poultry feather meal was
processed appropriately through fermentation
Barramundi (Lates Tuna hydrolysate PBM bioprocessed by Saccharomyces cerevisiae and Saccharomyces cereviceae Siddik et al.
calcarifer) supplementation Lactobacillus casei simultaneously supplemented and Lactobacillus casei (2019)
in poultry by- with 10% tuna hydrolysate can promote growth
product meal performance by improving feed intake and
intestinal mucosal morphology of fish
Barramundi (Lates Tuna hydrolysate The replacement of the FM protein with tuna Saccharomyces cereviceae Siddik et al.
calcarifer) hydrolysate at 50% and 75% inclusion levels and Lactobacillus casei (2018)
negatively affected the growth performance, feed
utilization and digestibility in juvenile barramundi

Where FM means fish meal; PBM means poultry by-products meal.

Wang et al. 2016; Jannathulla et al. 2018). The fungal or
bacterial fermentation also decreases the protein size due to
the secreted enzymes to be more digestible in the organism
GIT (Hong et al. 2004). Fermented SBM has approximately
10% more crude protein than SBM without changing the
essential AA profile (Hong et al. 2004). The efficiency of
fermentation in improving the nutritional value and reduc-
ing ANFs were ascertained in several aquatic animals as
described in Table 1.
Several microorganisms have been used to ferment SBM
as individual strain like L. brevis (Refstie et al. 2005), Bacil-
lus spp. (Yamamoto et al. 2010), L. plantarum P8 (Wang
et al. 2016), Aspergillus niger (Jannathulla et al. 2018),
A. oryzae (Kim et al. 2009; Kim et al.2010), S. cerevisiae
(Hassaan et al. 2015; Sharawy et al. 2016), B. subtilis E20
(Shiu et al. 2015) and Candida utilis (Zhou et al. 2011) or
as a mixture of several microorganisms like the bacterial
mixture ‘Pediococcus acidilactic, Enterococcus faecalis,
S. cerevisiae, C. utilis, B. subtilis, B. licheniformis,
Rhodopseudomonas palustri’ which used to ferment SBM in
Macrobrachium nipponense diet.
Fermented rapeseed/canola meal
Rapeseed and canola meal (RM) are considered the second
feedstuff most widely traded protein ingredient after SBM
(USDA, 2017). Due to an excellent balance of amino acids,
availability and reasonable cost, RM can be used as a pro-
tein-rich feed ingredient for aquafeed (Alashi et al. 2014;
Woyengo et al. 2015). But the major limiting factors that
affecting RM availability for aquafeed are its high content
of ANFs and fibre levels as well as the sinigrin and phenolic
compounds which has a negative impact on the aquatic
animal oxidative status and immunity (Wu & Muir 2008;
Bu et al. 2018). Furthermore, decreased palatability, feed
intake and feed efficiency were observed in fish fed RM
(Enami 2011).
Thus, fermentation process is encouraged to improve the
quality and availability of RM for aquafeed (Drew et al.
2007; Jakobsen et al. 2015). Bacteria and yeast used in RM
fermentation can reduce ANFs and phytic acid levels and
increase the relative levels of crude protein and minerals
(Greiner & Konietzny 2006). Fermentation of RM by
S. cerevisiae or A. oryzae successfully substituted FM

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protein partially or totally without negative effects on
growth, nutrient utilization, innate immune response or
oxidative stress of red sea bream (Pagrus major) (Dossou
et al. 2018a,2018b) (Table 1). Previous research also has
examined the addition of canola meal to aquafeeds and its
effects on growth and nutrient utilization of a variety of fish
species (Plaipetch & Yakupitiyage 2014, 2012). Dossou
et al. (2018a) concluded that, fermented RM can success-
fully substitute up to 56.25% of FM without negative effects
on growth, nutrient utilization, innate immune response or
oxidative stress of red sea bream.
Fermented cottonseed meal
Cotton seed meal (CSM) was used in aquatic animals as a
source of protein due to its high protein content, relatively
low price and availability (Sun et al. 2015). CSM substi-
tuted FM in several fish species including: crucian carp
(Carassius auratus gibelio) (Gui et al. 2010), Nile tilapia
(Oreochromis niloticus) (Yue & Zhou 2008), parrot fish
(Oplegnathus fasciatus) (Lim & Lee 2009) and rainbow
trout (Oncorhynchus mykiss) (Cheng & Hardy 2002). How-
ever, CSM was used in small amounts due to the presence
of free gossypol, fibre, phytic acid and ANFs (Imorou Toko
et al. 2008).
Fermented CSM is produced using beneficial microor-
ganisms to decrease the concentration of free gossypol and
fibre and increasing the protein fractions which can be sep-
arated into small-size peptides by enzymes secreted by the
microorganisms (Zhang et al. 2007). Furthermore, fermen-
tation can improve the digestibility of essential amino acids
and secreted enzymes (Zhang et al. 2006, 2007). Recently,
beneficial effects of fermented CSM were observed on the
performances of Nile tilapia (O. niloticus) (Lim & Lee
2011), olive flounder (Paralichthys olivaceus) (Lim et al.
2010), black sea bream (Acanthopagrus schlegelii) (Sun et al.
2015) and Pacific white shrimp (Litopenaeus vannamei)
(Sun et al. 2015) (Table 1). The authors suggested that
these improvements were due to enhanced enzyme activi-
ties, resulting in improved diet digestibility; including pro-
teins, starches and lipid.
Unconventional plant protein sources
The high fibre content and low protein content restrict the
use of unconventional dietary feed ingredients. The fer-
mentation approach is one possible strategy for improving
the quality of these feedstuffs. Fermentation can improve
feed utilization by reducing the fibre content, increasing
crude protein and lipid contents, improving the availability
of vitamins and improving protein solubility and amino
acid patterns as well as increasing the feedstuff palatability
(del Carmen Flores-Miranda et al., 2015; Zhang et al. 2017;
Jannathulla et al. 2017a,2017b). Fermentation can also
increase the digestibility of organic matter, nitrogen, amino
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Fermentation process and aquafeed
acids, fibres and calcium (Sun et al. 2015; Hassaan et al.
2018).
Another important aspect to consider when using novel
feed ingredients for aquatic animal diets is the presence of
ANFs ‘for example lectins and trypsin inhibitors in SBM,
glucosinolates in RM, tannins, haemagglutinins and proso-
pine in prosopis seed meal and phytate in maize’ that can
affect digestibility and feed nutritional value (del Carmen
Flores-Miranda et al. 2015; Zhang et al. 2017). Fermenta-
tion thus appears to be a practical choice to increase the
nutritional values of unconventional feed ingredients for
aquatic animals by reducing ANFs. Phytase enzymes pro-
duced by microorganisms during fermentation may
degrade the phytate resulting in reduced phytate and sub-
strate ANFs levels (del Carmen Flores-Miranda et al. 2015).
Fermentation can detoxify the toxic compounds ‘cyano-
genic glycoside compounds, phorbolesters, isothiocyanates,
etc.’ (Kobawila et al. 2005). With regards to the phor-
bolester content of Jatropha curcas and isothiocyanate con-
tent in RM decreased clearly after fermentation (Chiang
et al. 2009; Hassaan et al. 2017; Dossou et al. 2018a,2018b).
FM can be replaced with up to 35 % fermented duck-
weed without adversely affecting the survival and growth
performance of Pacific white shrimp (L. vannamei) (del
Carmen Flores-Miranda et al. 2015). The fermentation by
Lactobacilli improved the lupin (Lupinus angustifolius)
nutritional quality, allowing higher inclusion level (Van Vo
et al. 2015), whereas fermentation with S. cerevisiae has an
obvious potential to substantially replace 75% of FM in
barramundi (Lates calcarifer) diets (Ilham & Fotedar 2017).
Up to 50% of FM can be replaced by J. curcas seed meal in
Nile tilapia diets (Hassaan et al. 2017). Also, FM can be
replaced by S. cerevisiae and B. subtilis fermented sunflower
meal up to 50% without negative effects on the growth and
physiological indices in Nile tilapia diets (Soltan et al. 2015;
Hassaan et al. 2018). Up to 50% of FM can be replaced by
fermented CSM without adverse effects on growth and feed
utilization of Pacific white shrimp (L. vannamei) (Sun
et al. 2016). Jannathulla et al. (2017a) reported that fer-
mented guar meal could be used as potential protein
sources rather than untreated materials in the diet of
Penaeus vannamei.
In crucian carp (C. auratus gibelio), 64%-80% propor-
tion of dietary FM substituted with fermented mushroom
bran hydrolysate improved the growth, digestive enzyme
activity and antioxidant capacity (Zhang et al. 2017).
Fermented animal protein sources
The animal protein sources can replace FM in aquafeed due
to their high protein content, total digestible dry matter
and lack of ANFs (Oliva-Teles et al. 2015). The fermenta-
tion process was recognized for its role in improving the
7
M. A. O. Dawood and S. Koshio
nutritional quality of animal by-products (Mondal
et al.2011; Kaviraj et al. 2013). Aquaculture nutritionists
focused mainly on finding suitable alternatives to FM
through innovative approaches such as fermentation and
advanced nutritional enrichment bioprocessing (Bertsch &
Coello 2005; Adel et al. 2016, 2017a; Yan et al. 2017b). Sev-
eral studies have reported that fermentation, as an environ-
mentally friendly and cost-effective method, improves the
digestibility and amino acid profile of animal by-products
and thus enhances their suitability for inclusion in aquafeed
(Table 2). Fermentation also can break up carbohydrates
into compounds of lower molecular weight that potentially
boost innate energy and mineral absorption (Ilham & Fote-
dar 2017). Also, fermented products tend to have higher
water stability which can help the fish to ingest feed com-
pletely in enough period (Fagbenro et al. 1994).
Animal waste products have high humidity, indigestible
particles and microbial contaminants that can be resolved
through fermentation (Mondal et al. 2008; Samaddar et al.
2015). Poultry by-product meal (PBM) can be treated with
appropriate microorganisms to preserve its nutrients and
finally incorporated into the fish diet, which would reduce
feed costs and environmental pollution (Siddik et al. 2019).
Fermented animal by product meals showed better nutrient
efficiency and could improve nutritional value of aquafeed
(Mondal 2014; Samaddar et al. 2015). Fermented slaughter-
house blood and fish offal mixture, poultry feather meal,
tuna hydrolysate supplemented in PBM replaced FM as a
protein source in fish diets without reducing growth per-
formance and health status (Mondal 2014; Samaddar et al.
2015; Siddik et al. 2019) (Table 2). The results showed that,
21.11% replacement of FM by the fermented slaughter-
house blood and fish offal blend using L. acidophilus
(NCIM 2903) was ideal for optimum growth of L. rohita
(Samaddar et al. 2015). PBM bioprocessed by S. cerevisiae
and L. casei simultaneously supplemented with 10% tuna
hydrolysate can promote growth performance by improv-
ing feed intake and intestinal mucosal morphology of fish
(Siddik et al. 2019). Using B. cereus, 30 % poultry feather
meal and 10 % FM replaced 75% of FM if hydrolysed poul-
try feather meal was processed appropriately through fer-
mentation in Catla catla diets (Mondal 2014).
Poultry by-product meal is a good source of protein but
is limiting in some of the essential amino acids (Rawles
et al. 2006). PBM successfully replaced FM in Nile tilapia
(O. niloticus) (El-Sayed 1998), gibel carp (C. auratus)
(Yang et al. 2006), African catfish (Clarias gariepinus)
(Abdel-Warith et al. 2001), rainbow trout (O. mykiss)
(Steffens 1994), gilthead sea bream (Sparus aurata) (Nengas
et al. 1999), red sea bream (P. major) (Takagi et al. 2000)
and red drum (Sciaenops ocellatus) (Kureshy et al. 2000).
PBM quality can be improved by fermenting and supple-
menting with a fish protein hydrolysate (FPH) to minimize
8 © 2019 Wiley Publishing Asia Pty Ltd
the loss of amino acids and improve the quality of the final
meal (Siddik et al. 2019). FPH is a highly beneficial attrac-
tant made from whole fish or by-products of fish and used
in aquafeed as an immunostimulant (Kousoulaki et al.
2013; Ho et al. 2014; Khosravi et al. 2015). FPH contains
high amount of of low molecular weight bioactive peptides
which acts has immunomodulating and antibacterial effects
(Kotzamanis et al. 2007; Ha et al. 2019). Several studies
reported enhanced immune responses and accordingly
increased disease resistance in aquatic animals by FPH
(Murray et al. 2003; Liang et al. 2006; Kotzamanis et al.
2007). Krill, shrimp and tilapia hydrolysate resulted in
improved immunity and resistance against Edwardsiella
tarda challenge in red sea bream (P. major) (Khosravi et al.
2015).
Fermentation with probiotic effect
Beneficial bacteria, yeast and fungi are normally used to fer-
ment the plant and animal protein sources as clearly men-
tioned above which is reflexing the action of probiotics
(Dossou et al. 2019). The benefits of probiotics include
improved growth performance, feed value, enzymatic con-
tribution to digestion, inhibit adherence and colonization
of pathogenic microorganisms in the GIT, increase haema-
tological parameters and immune response (Van Doan
et al. 2017, 2019; Elsabagh et al. 2018; Dawood et al.,
2018a,2018b). Several probiotics species are used in aqua-
culture; for example Bacillus sp., Lactobacillus sp., Entero-
coccus sp., Streptomyces, Carnobacterium sp. and yeast (Adel
et al. 2017b; Zaineldin et al. 2018; Dawood et al.
2019a,2019b). Tables 1 and 2 summarize the results of pre-
vious studies, focusing on the effects of probiotics as
growth promoters and immunostimulants in fermenting
animal and plant protein sources for better aquafeed. Pro-
biotics can improve the host’s appetite and feed digestion
by breaking down indigestible components, increase pro-
duction of digestive enzymes, vitamins and detoxify com-
pounds in the diet (Giraffa et al. 2010; Dawood et al.
2016a,2016b,2016c,2016d). Importantly, probiotics have
characteristics such as colonization potential in the intes-
tine, interactions with the gut microbial population,
increased adhesion and pathogen exclusion and inhibition
of pathogen growth and activity (Dawood & Koshio 2016).
The host-associated Lactobacilli have gained much atten-
tion in aquaculture (Dawood 2016). The chemical compo-
sition of microorganisms includes different polysaccharides
that may have potential prebiotics in the host’s intestine
(Ringø et al. 2010). Both Bifidobacteria and Lactobacilli can
utilize these oligosaccharides and increase the number of
beneficial bacteria in host’s gut. Further benefits of dietary
supplemented oligosaccharides; include improved feed effi-
ciency, enhanced growth and increased digestive enzyme
Reviews in Aquaculture, 1–16

activities. Furthermore, they seem able to modulate
immune responses and preserve the integrity of the intesti-
nal wall (Dimitroglou et al. 2010).
Another critical feature of probiotics is their presence
inside the host, in which they are potentially colonizing
and replicating, which further serves to improve the host’s
GIT health (Dawood et al. 2015b,2015c,2015d). The colo-
nization ability of probiotics within the GIT of animals
provides a necessary competition to indigenous microbiota
(Hill 1993; Dawood et al. 2019c,2019d). The ability to
attach the gut surface is an important aspect of probiotics,
which in turn is associated with mucous formation of the
bacteria. These abilities are useful for protection against
pathogen or immune stimulation (Hill 1993).
Genus Bacillus is the most studied host-associated probi-
otic, among a wide variety of aquatic animals (Elsabagh
et al. 2018). Bacillus sp. supplementation diets significantly
improved growth performance, survival rate and feed con-
version ratio; as well as protease and lipase activities in
common carp (Cyprinus carpio) (Yanbo & Zirong 2006).
The authors suggested that these improvements were due
to enhanced enzyme activities, resulting in improved diet
digestibility; including proteins, starches and lipid (Yanbo
& Zirong 2006). The significant improvement in growth
performance within these findings may be due to the ability
of Bacillus spp. to adhere to the intestinal mucosa of the
host, allowing them to secrete a wide range of digestive
enzymes; such as amylase, lipase and protease; all of which
facilitate feed utilization (Latorre et al. 2016). Moreover,
Bacillus spp. has been reported to detoxify potentially
harmful food components and produce many essential
vitamins in the B-complex group (particular vitamin B12
and biotin), which results in higher feed utilization and
digestibility of feed components (El-Haroun et al. 2006).
More recently, a Bacillus spp. revealing exoenzymes
activities has been reported to improve the host’s growth
performance, including weight gain and feed efficiency (Liu
et al. 2017). Bacillus exoenzymes are very efficient at metab-
olizing a large variety of carbohydrates, lipids, and proteins
and dietary supplementation of Bacilli may improve diges-
tive enzyme activities (Han et al. 2015). It is widely
accepted, that the level of digestive enzyme activity is a use-
ful comparative indicator of the host’s feed utilization rate,
digestive capacity and growth performance (Suzer et al.
2008; Dawood et al. 2014; Dawood et al. 2019e).
Saccharomyces cerevisiae is among the well-known
microorganisms and its efficacy is rely on the functional
components such as ‘b-glucans, nucleic acids, mannan
oligosaccharides and chitin’ (Peppler 1982; Dawood et al.
2017a,2017b,2017c). Yeast also produces different metabo-
lites like, ‘enzymes, oligosaccharides, amino acids, peptides,
organic acids, vitamins and other soluble factors’ (Peppler
1982). S. cerevisiae can have a positive impact on the
Reviews in Aquaculture, 1–16
© 2019 Wiley Publishing Asia Pty Ltd
Fermentation process and aquafeed
growth performance, immune responses and disease resis-
tance of various cultivated fish species (Li & Gatlin 2004;
El-Boshy et al. 2010).
Fermentation of SBM with probiotics professionally
removes the ANFs and increased the nutrient value by pro-
ducing hydrolysis enzymes (Hong et al. 2004). Lactobacillus
species can produce lactic acid and remove trypsin inhibi-
tor contents during fermentation, thus increasing protein
hydrolysis and liberating free amino acids (Amadou et al.,
2010a,2010b).
Conclusion and future remarks
Fermented feed ingredients have more amino acids and
other biomolecules that plays a vital role in improving
aquatic animal performances than the non-fermented
nutrients. Several peer-reviewed publications have given an
insight on the numerous roles of fermented aquafeed in
maintaining the growth performance, feed utilization, sur-
vival, disease resistance, inhibition of bacterial quorum
sensing, immunity, stress tolerance, gut microbiota and
aquatic bioremediation.
Fermentation is an important tool for enhancing the
nutritional value of conventional and non-conventional
aquafeed feed ingredients. It is obvious that fermented feed
has beneficial effects on GIT ecosystems and morphology,
growth performance and feed utilization of aquatic animal.
Fermented feeds could also be used as a natural strategic
tool to minimize colonization of GIT pathogens in aquatic
animals due to the beneficial microorganisms’ competitive
effect. The inclusion of fermented feed stuff in aquafeed
resulted in improved immune response, oxidative status,
resistance against environmental stressors and infectious
diseases which reflex the well-being of aquatic animals.
Using local fermented feed ingredients could reduce feed
costs, particularly in developing countries, ensuring prof-
itable aquaculture activity. The fermentation strategy for
preparing aquafeed need more efforts and future studies
are required to reveal how fermented feed components
affect the microbiota of the aquatic animals GIT. Under-
standing the effects of fermented ingredient on the intesti-
nal immunity and gut microbiome of fish using novel
perspectives, involving high-throughput experimental
approaches would give an interesting insight into various
roles of fermented ingredient on health and nutrition of
aquatic animals. Recently, aquafeed sector is a remarkably
increasing due to the increased demand for fish feed. The
industry is faced with increasing demand of producing a
high-quality aquafeed that could meet the physiological
requirements of aquatic animals. Therefore, the next gener-
ation aquafeed should be of better quality to ensure a supe-
rior growth and improved health. Thus, in-depth research
to explore the wider roles and untapped functions of
9
M. A. O. Dawood and S. Koshio
fermented aquafeed in aquatic animal health and feed is
needed.
Conflict of interest
The author declares that the research was conducted in the
absence of any commercial or financial relationships that
could be construed as a potential conflict of interest.
Author contribution
The authors were responsible for data collection, data anal-
ysis, interpretation and writing the manuscript.
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