Reviews in Aquaculture, 1–18 doi: 10.1111/raq.

12272

Probiotic application for sustainable aquaculture

Mahmoud A.O. Dawood1 , Shunsuke Koshio2, Mohamed M. Abdel-Daim3 and Hien Van Doan4
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
3 Pharmacology Department, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt
4 Department of Animal and Aquatic Sciences, Faculty of Agriculture, Chiang Mai University, Chiang Mai, Thailand

Correspondence
Mahmoud A.O. Dawood, Department of
Animal Production, Faculty of Agriculture,
Kafrelsheikh University, 33516 Kafrelsheikh,
Egypt. Email:
Mahmouddawood55@gmail.com
Received 10 March 2018; accepted 18 June
2018.
Abstract
Aquaculture, which constitutes one of the largest food production sectors in the
world, is preferably practiced with natural organic products rather than with syn-
thetic chemicals or antibiotics. In addition to the daunting challenge of providing
food and livelihood to the exponentially increasing world population, the aqua-
culture industry is key to ensuring that development is based on environmentally
sustainable practices, specifically in the production of aquafeeds. Terrestrial
microorganisms that act as natural defence systems of cultured species have been
identified as the main producer for the beneficial bacterial candidates. Probiotics
have recently gained popularity as beneficial microbes candidates in cultured
organisms to maintain the health condition and well-being of different aquatic
animals. This review aimed to understand the necessity of using probiotics as a
sustainable alternative to regulate the growth performance, feed utilisation and
general health condition for sustainable aquaculture. Also, explanatory discussion
about the host microbiota and its ability to produce different probiotic strains
and the probiotic functionality to ameliorate the host immunity to provide the
interactive effects on the host-derived probiotics. By presenting the results
obtained from the previous studies about the ability of probiotics to sustain the
aquatic animal’s performances, this study condensed the current knowledge and
information for future research and development of the probiotic application in
aquaculture.
Key words: functional feed, growth promoters, immunostimulants, mode of action, probiotic,
sustainable aquaculture.

(Hern
andez-Serrano 2005; Shamsuzzaman & Biswas 2012;

Introduction
Aquaculture plays a vital role in providing sustainable
livelihood opportunities and food security for the ever-
increasing world population (Fazio et al. 2013; Faggio et al.
2014; Dawood et al. 2016a; El Basuini et al. 2016, 2017;
Wang et al. 2018). Therefore, intensification of aquaculture
practices has been applied to maintain high levels of pro-
duction, resulting in increased aquatic animal and environ-
mental stress (Tal et al. 2009; Dossou et al. 2018a,b). As a
direct result, disease outbreaks increased to weaken the
production and threaten the sustainability of aquaculture.
To control the diseases of aquatic organisms, a plethora of
chemical compounds and antibiotics has been applied
including oxytetracycline, chlortetracycline, amoxicillin,
co-trimoxazole, sulphadiazine and sulphamethoxazole
Carbone & Faggio 2016; Guardiola et al. 2016; Aliko et al.
2018). However, the application of these compounds
caused many problems and their risk could affect human’s
health indirectly. Thus, the development of natural friendly
alternatives and growth promoters has become important
and urgent for healthier aquatic animals.
The host terrestrial microorganisms play a vital role in
the health maintenance of the aquatic animals by stimulat-
ing the immune system, aiding in nutrient digestion and
increasing the resistance against opportunistic pathogens
(Llewellyn et al. 2014; Yan et al. 2017a). The functionality
of intestinal microbiota depends on the ability of microor-
ganisms to interact with the digestive tract, which can bene-
fit the host by the influence on the biological functions
(Ram
ırez & Romero 2017). Terrestrial microorganisms can

© 2018 Wiley Publishing Asia Pty Ltd 1

M. A. O. Dawood et al.
activate the digestion processes by providing digestive
enzymes and vitamins as well as the ability of nutrients to
compete the adhesion sites to enhance the feed utilisation
(Chabrill
on et al. 2005; Hovda et al. 2007). Further, the
antimicrobial substances produced by intestinal microor-
ganisms can enhance the immune response and decrease
the pathogenic bacteria (Verschuere et al. 2000; Ringø
et al. 2006). These microbial communities reside in differ-
ent places in the host; therefore, it was divided into ‘al-
lochthonous microbiota’, which passes through the lumen
with digested feed and ‘autochthonous microbiota’, which
exist in the host tissues (Gajardo et al. 2016; Tarnecki et al.
2017). In some cases, the indigenous bacteria showed more
beneficial effects when compared with other bacterial
sources due to the specificity of colonisation by the bacteria
(Ying et al. 2007; Nayak 2010; Mills et al. 2011).
The use of probiotics is important to maintain healthy
environment for aquatic animals and to increase its perfor-
mances without any negative impacts on the consumers
(Dawood et al. 2017a). Research on the use of probiotics
for aquatic animals is increasing as the demand for envi-
ronmentally sustainable aquaculture increases. Probiotics
have been defined as ‘live microbial feed supplements that
improve the health of humans and terrestrial livestock’
(Gatesoupe 1999). The application of probiotics in aquatic
animal diets can positively influence growth performance,
feed utilisation and physiological conditions (Irianto &
Austin 2003; Dawood 2016; Elsabagh et al. 2018; Zaineldin
et al. 2018). Dietary uptake of probiotics can optimise cell
proliferation to promote the immunological response, par-
ticularly under stressful conditions, and additional probi-
otics are required in some cases for further immune cell
stimulation (Merrifield et al. 2010a; Van Hai 2015).
From time to time, it is necessary to identify the latest
information that has a relationship with the aquatic animal
terrestrial microorganisms and the ability to produce bene-
ficial bacteria with probiotic characteristics. Furthermore,
probiotics mode of action and their effects on the intestinal
microbiota, immunological and physiological responses as
well as the growth performance of aquatic animals, must be
deeply identified. Thus, this review offers updated informa-
tion to assess whether supplementation of probiotics
induced changes in the intestinal mucus proteome, gut
autochthonous microbiota and disease susceptibility and
whether these changes could be reversed by the addition of
probiotics to the diets.
Terrestrial microorganisms and microbiota
Terrestrial microorganisms play a critical role in the normal
growth of aquatic animals and are considered an essential
tool for sustainable aquaculture. Indigenous microbiota has
been reported to enhance digestion and nutrient
2 © 2018 Wiley Publishing Asia Pty Ltd
metabolism in several cultured species (Llewellyn et al.
2014). Furthermore, intestinal microbiota improved the
health status of aquatic animals via the immunomodula-
tion and outcompeting of opportunistic pathogens (G
omez
& Balc
azar 2008).
Microorganisms exist in multiple ecological environ-
ments are an important component of the diverse ecosys-
tems (Lazado et al. 2015). The microorganism
communities which live symbiotically with the hosts are
known as microbiota, microflora or normal flora (Lazado
et al. 2015). The microbial interactions could happen due
to the existence of both pathogenic and beneficial microor-
ganisms in the same environment, resulted in increasing
the ability of beneficial microorganisms to eliminate patho-
genic microorganisms (Huttenhower et al. 2012). Most of
the pathogenic bacteria in marine fish are opportunistic
pathogens present as part of the normal seawater microor-
ganisms, and a few of them are obligate pathogens whose
propagation depends on a living host (Hansen & Olafsen
1999). The intestinal microbiota is highly influenced by the
host ecology and its environment (Wong & Rawls 2012).
The aquatic animal-associated microorganisms are par-
ticularly important due to the capability of microorganisms
to colonise in the intestinal gut of the host to perform
important and vital functions that cannot be performed by
the host itself (Hooper et al. 2001; Huttenhower et al.
2012). Furthermore, their important role in the host devel-
opment, homeostasis and protection, particularly in
the gut, earning them the recognition as ‘an extra organ’ of
the host (O’Hara & Shanahan 2006). The mucosal layer in
the gut of aquatic animals provides a niche for the adher-
ence, colonisation and proliferation of many beneficial
microbial species that affect various physiological functions
of the host (G
omez & Balc
azar 2008). The gut is also one of
few organs with defined and multiple functions, including
immunological, metabolic and respiratory functions (Gro-
sell et al. 2011). In addition to the gut, microorganisms
reside in other organs of the aquatic animals, most promi-
nently on mucosal surfaces such as the skin (approximately
102 to 104 cm
2) and gills (up to 106 bacteria 170 g
1 of
organ) (Austin 2006).
Probiotics for sustainable aquaculture
Aquaculture is emerging as one of the fastest growing and
most promising industries for providing animal protein
and food security to the world population (De et al. 2014).
The intensification of aquaculture practices has given rise
to stressful conditions for both the aquatic animals and the
environment (Dawood et al. 2016a,b; Hossain et al. 2016).
As a result, disease outbreaks are being increasingly recog-
nised as one of the most important risks to the aquaculture
industry. To control infectious disease in aquaculture,
Reviews in Aquaculture, 1–18

chemical compounds and antibiotics are typically used
(Adel et al. 2016; Dawood et al. 2017b,c). However, the use
of antibiotics can negatively impact the host and environ-
ment. Therefore, to expand in the aquaculture industry, it
is necessary to find safe and effective alternatives to antibi-
otics (Abdelkhalek et al. 2017; Yan et al. 2017b). The use of
probiotics is one of the most important developments for
sustainable aquaculture as a safe and nonconventional
alternative with the ability to improve growth, nutritional
efficiency and general health status in farmed fish and shell-
fish (Dawood et al. 2016a,b; Van Doan et al. 2017). The
use of probiotics has received special attention because of
its importance and ease of use so it was necessary to draw
attention to the mechanisms of action, both at the in vivo
and in vitro levels and particularly the intestinal ecosystem.
To improve the feed utilisation and health status of
hosts, various strategies have been investigated in animals
to modulate the gut microbiota, which is responsible about
the quality of food digestion (Burr et al. 2007). Probiotics
representing ideal interest and have become quite impor-
tant as growth supplements for promotion of functional
diets in several cultured and aquatic animal species (Ouwe-
hand et al. 2002; Dawood & Koshio 2016a). The definition
of probiotics was introduced by several specialists since it
was founded by Parker (1974), as ‘organisms and sub-
stances that contribute to intestinal microbial balance’.
Probiotics redefined as ‘a live microbial feed supplement
which beneficially affects the host animal by improving its
intestinal microbial balance’ (Fuller 1989). More recently,
the probiotics are defined as ‘live microorganisms that
when administered in adequate amounts confer a health
benefit on the host’ (FAO/WHO, 2001). It has been sug-
gested that the supplied probiotic bacterial cells in the
aquatic environment could influence the composition of
the terrestrial microorganisms as it shares the same ecologi-
cal system (Verschuere et al. 2000). As a result, the admin-
istration of probiotics should be applied for the larval stage
of fish and shellfish species as the larval forms, mostly
released into the aquatic environment at an early ontoge-
netic stage (Kapareiko et al. 2011; Arıg et al. 2013). Tem-
perature changes, density and the intensity of stress
management can exert immunosuppressive effects and
physiological responses, whereas feed additives with
immunomodulation properties can enhance the efficiency
of an organism’s response to stress (Magnadottir 2010).
Probiotics can act as a microbial dietary remedy that bene-
fits the host health condition by modulating mucosal and
systemic immunity and improving the physiological and
nutritional activities as well as the microbial balance in the
intestinal tract (Villamil et al. 2002). Probiotics introduced
for aquaculture have several forms including bacterial cells
(Bacillus sp., Lactococcus sp., Micrococcus sp., Carnobac-
terium sp., Enterococcus sp., Lactobacillus sp., Streptococcus
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd
Probiotics for sustainable aquaculture
sp. and Weissella sp.), microalgae (Tetraselmis) and yeasts
(Debaryomyces, Phaffia and Saccharomyces) (Gatesoupe
1999; He et al. 2011).
Probiotic mode of action
Bacterial probiotics do not have a specific mode of action
but do play a key role both in the immune responses of the
host animal and in the interaction between these responses
and intestinal bacterial communities (Dawood & Koshio
2016a). Common modes of action for probiotic supple-
mentation have been reported. Firstly, the enhancement of
feed utilisation and weight gain in aquatic animals (Al-
Dohail et al. 2009; Saenz de Rodriguez et al. 2009). Using
probiotics can also stimulate the host appetite and feed
palatability by breaking down of indigestible components
and the production of vitamins and detoxification of com-
pounds in the diet (Giorgio et al. 2010). Secondly, preven-
tion of pathogens via competitive exclusion for adhesion
sites (Chabrill

on et al. 2005); the production of peroxide,
bacteriocin, siderophore and lysozyme enzymes (Yan et al.
2002); and physiological and immunological effects (Telli
et al. 2014; Ramesh et al. 2015). Furthermore, probiotics
could modulate the growth and selectivity of the intestinal
microbiota by suppressing the effect of harmful bacteria
and reinforce the body’s natural defence mechanisms via
the production of inhibitory substances (Giorgio et al.
2010). The adherence of certain probiotics to the mucosal
layer of the intestine suggested to inhibit infection patho-
gens through the blocking of the common route used by
the pathogenic bacteria (Gatesoupe 1999; Ringo et al.
2010). Thirdly, increasing the resistance of aquatic animals
against stress caused by several environmental hazards
during the aquaculture activity (Rahiman et al. 2010;
Firouzbakhsh et al. 2011; Nimrat et al. 2012). The above-
mentioned mode of actions presented initial information
to interpret the beneficial effects in the aquatic animals.
However, future research on the interaction between
probiotic and the host should involve transcriptomic and
proteomic analyses for further understanding of the
probiotic activity.
Probiotic effects to improve the feed utilisation
Diets supplemented with probiotics are digested and
absorbed more efficiently due to the ability of probiotics to
produce digestive enzymes (amylases, proteases, and
lipases, etc.) and provide nutrients (vitamins, fatty acids
and amino acids), which may contribute to the digestive
processes and feed utilisation as well as on the assimilation
of diet components resulted in improved general health
condition and growth performance of aquatic animals
(Irianto & Austin 2002; Bolasina et al. 2006; Shan et al.
3
M. A. O. Dawood et al.

2008; Ray et al. 2012). Many studies have recently investi-
gated altered enzyme patterns due to the intake of probi-
otics in aquaculture (Table 1). Amylase, trypsin, protease
and lipase secretion have been elevated in sea bass (Dicen-
trarchus labrax) and rohu (Labeo rohita) after those ani-
mals were fed live mixture of probiotics (Tovar-Ramirez
et al. 2002; Mohapatra et al. 2012). The observed enhance-
ments in nutrient digestibility and health condition possi-
bly because of the increased availability of nutrients
produced by probiotics incorporation in aquafeeds (Lara-
Flores & Aguirre-Guzman 2009; Mohapatra et al. 2012).
Several fish species fed diets supplemented with beneficial
bacterial cells (B. cereus, B. subtilis, B. licheniformis and
E. faecium) showed enhanced feed utilisation and growth
performance accordingly (Hidalgo et al. 2006; Merrifield
et al. 2010b). Incorporation of Bacillus sp. in fish diets
resulted in improved digestion activities due to the ability
of Bacillus to produce exoenzymes (Arıg et al. 2013; Pur-
wandari & Chen 2013). Similarly, the digestion of dry mat-
ter, crude protein and phosphorus enhanced in white
shrimp species Litopenaeus vannamei and Fennerope-
naeus indicus fed diets supplemented with Bacillus sp.
(Ziaei-Nejad et al. 2006; Zokaeifar et al. 2012).
The probiotic yeast (Saccharomyces cerevisiae) affected
European sea bass larvae (D. labrax) growth performance
and digestive enzymes activities as well as the expression of
key antioxidant enzymes and gene expression patterns in
fish fed yeast supplemented diets (Tovar-Ramirez et al.

Table 1 Digestive enzyme activities altered by probiotic supplementation in aquatic animals

Species Probiotic Enzymes References

Sea bass (Dicentrarchus labrax)
Rohu (Labeo rohita)
Cichlid (Etroplus suratensis) and
Tilapia
(Oreochromis mossambicus)
Penaeus vannamei
Nile tilapia
(Oreochromis niloticus)
Portunus pelagicus (Linnaeus,
1758)
Rainbow trout
(Onchorhynchus mykiss)
Sea cucumber
(Apostichopus japonicus)
Common carp (Cyprinus carpio)
Indian white shrimp
(Fenneropenaeus indicus)
White shrimp
(Litopenaeus vannamei)
White Pacific shrimp
(Litopenaeus vannamei)
Gilthead sea bream
(Sparus aurata, L.)
Amberjack (Seriola dumerili)
Red sea bream (Pagrus major)
Gilthead sea bream
(Sparus aurata, L.)
Debaryomyces hansenii HF1 Amylase and trypsin Tovar-Ramirez et al. (2002)
Saccharomyces cerevisiae X2180
Bacillus subtilis, Lactococcus lactis Protease and lipase Mohapatra et al. (2012)
and Saccharomyces cerevisiae
Micrococcus MCCB 104 and Bacillus Amylase, total alkaline protease, Sankar et al. (2017)
MCCB 101 lipase and alpha-amylase
Bacillus sp. Protease and amylase Wang (2007)
Bacillus coagulans SC8168 Protease, amylase and lipase Zhou et al. (2009)
Bacillus subtilis NIOFSD017, Amylase, protease and lipase Essa et al. (2010)
Lactobacillus plantarum NIOFSD018
and Saccharomyces cerevisiae
NIOFSD019
Lactobacillus rhamnosus Protease and amylase Talpur et al. (2013)
Saccharomyces cerevisiae Alkaline phosphatase, c-glutamyl Wach
e et al. (2006)
transpeptidase and leucine
aminopeptidase
N
Rhodotorula benthica D30 Amylase activity, cellulase activity and Wang et al. (2015)
alginase activity
Bacillus sp. Protease, amylase and lipase Yanbo and Zirong (2006)
Bacillus sp. Amylase, total protease and lipase Ziaei-Nejad et al. (2006)
Bacillus subtilis Protease and amylase Zokaeifar et al. (2012)
Pediococcus pentosaceus Amylase, protease and lipase Adel et al. (2017a,b)
Bacillus subtilis E20 Protease Liu et al. (2009)
Bacillus spp. Protease and amylase Go
mez et al. (2008)
Bacillus sp. Alkaline protease Arıg et al. (2013)
Lactobacillus plantarum Protease Dawood et al. (2015c)
Lactobacillus rhamnosus and Protease Dawood et al. (2016a)
Lactococcus lactis
Lactobacillus spp. Amylase, trypsin, lipase, alkaline Suzer et al. (2008)
phosphatase and leucine leucine-
alanine peptidase

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4 © 2018 Wiley Publishing Asia Pty Ltd

2010). Zhou et al. (2009) reported about the importance of
probiotics supplementation during all the larval stages of
shrimp to affect the production of digestive enzymes. Orna-
mental fish also revealed improved specific activities of
digestive enzymes upon the probiotic supplementation
(Avella et al. 2012; Gioacchini et al. 2012).
Probiotics as effective growth promoters
Beneficial probiotic bacteria are vital tools to maintain the
normal growth and functions of the aquatic animals by
working as a source of nutrients, vitamins and digestive
enzymes, which have a positive effect on the feed utilisation,
absorption of nutrients and growth performance (Dawood
et al. 2014; Lauriano et al. 2016; Aragona et al. 2017; Nath
et al. 2018). Probiotic supplementation has been hypothe-
sised to increase the appetite or improve the digestibility of
organisms (Irianto & Austin 2002). Probiotics can enhance
aquatic animal feed efficiency by stimulating digestive
enzymes and maintaining the balance of intestinal microbes,
resulted in improved nutrient absorption and utilisation
and, ultimately, the survival and growth of those animals
(Irianto & Austin 2002; Dawood & Koshio 2016a). Further,
the addition of probiotics was examined in phytoplankton,
which forms the basis of aquatic food chains because of
their nutrient-producing photosynthetic mechanisms (Bon-
net et al. 2010; Paiva-Maia et al., 2013). Studies on diets
containing probiotics revealed the possible involvement of
these probiotics on the improvement of intestinal micro-
flora balance and the production of extracellular enzymes to
elevate the feed efficiency and growth of cultured species as
growth promoters (Kar & Ghosh 2008; Ringo et al. 2010;
Giri et al. 2013).
Probiotic as functional immunostimulants
The incorporation of probiotics in aquatic animal diets
resulted in improved immune response by the interaction
between bacterial cells and intestinal epithelial cells in the
host gut, which controls the physical and immunological
barrier properties of the intestine (Thomas & Versalovic
2010; Liu et al. 2013). Further, probiotics produce sig-
nalling molecules that can stimulate the immune system
against infectious diseases (Cerezuela et al. 2013). The oral
administration of beneficial bacterial cells modulated the
immune system of aquatic animals for both cellular and
humoural components (Rengpipat et al. 2000; Gullian
et al. 2004; Panigrahi et al. 2004; Song et al. 2006; Pais
et al. 2008; Biswas et al. 2013a,b). The most activated
immune components are lysozyme, peroxidase and bacteri-
cidal activities as well as the increased levels of lymphocytes
and granulocytes (Pirarat et al. 2011; Sorroza et al. 2012;
Sharma et al. 2013).
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Probiotics for sustainable aquaculture
Probiotics can affect the intestinal microbiota to produce
short-chain fatty acids, increase sodium and water absorp-
tion, decrease colonic motility and support host health;
these processes provide protection against infections by
stimulating the immune system, alleviating lactose intoler-
ance and reducing blood cholesterol levels (Lara-Flores &
Aguirre-Guzman 2009; Ringo et al. 2010).
Probiotics and disease resistance
Probiotics have received attention for disease prevention in
aquaculture (Newaj-Fyzul et al. 2014). For many years,
chemotherapeutics has been used to treat infectious dis-
eases in aquaculture; however, negative side effects, such as
the development of antibiotic-resistant bacteria, limit the
usefulness of antibiotics (Dawood & Koshio 2016b; Adel
et al. 2017a,b). Alternatively, as functional feed additives,
probiotics, prebiotics, medicinal herbs and immunostimu-
lants have recently gained attention in aquaculture (Adel
et al. 2016; Dawood et al. 2017d). Probiotics can interact
with or antagonise other enteric bacteria by resisting
colonisation or by directly inhibiting and reducing the inci-
dence of opportunistic pathogens. Probiotics can also
enhance host health via physiological or immune modula-
tion (Dawood et al. 2016c,d; Adel et al. 2017a).
Probiotics can produce effective molecules that have bac-
tericidal activity on intestinal pathogenic bacteria of the
host, providing a barrier against the proliferation of oppor-
tunistic pathogens (Mart
ınez Cruz et al. 2012). The func-
tional molecules produced during the bactericidal activity
are antibiotics, bacteriocins, siderophores, enzymes (lyso-
zymes, proteases) and/or hydrogen peroxide as well as the
alteration of the intestinal pH due to the generation of
organic acids (Verschuere et al. 2000). The inhibition of
intestinal related diseases has been reported in several cul-
tured species by probiotic incorporation in aquafeeds
(Vijayabaskar & Somasundaram 2008; Dahiya et al. 2012;
Sihag & Sharma 2012).
Thus, it can be confirmed that the ability of aquatic ani-
mals to avoid the infectious diseases mainly depends on the
immunomodulatory effect that happened due to the
administration of beneficial bacterial cells. Famous cultured
species were reported to increase their resistance against
infections such as Nile tilapia (Oreochromis niloticus),
Atlantic salmon (Salmo salar L.) and rainbow trout
(Oncorhynchus mykiss) fed diets supplemented with probi-
otics showed enhanced immune responses via the enhance-
ment of neutrophil migration, lysozyme and bactericidal
activities; as a result, the resistance against bacterial patho-
gens (Edwardsiella sp., Aeromonas sp., Flavobacterium sp.,
Photobacterium sp. and Vibrio spp., respectively) increased
(Robertson et al. 2000; Taoka et al. 2006a). Evidence also
exists on the effect of dead probiotic cultures consisting of
5
M. A. O. Dawood et al.
a mixture of Vibrio fluvialis A3-47S, A. hydrophila A3-51
and Carnobacterium BA211 on the control of furunculosis
in rainbow trout. In this case, more leucocytes were present
in the dead probiotic cells than in the live cells. The
obtained results showed that the addition of dead bacterial
cells could enhance the cellular immunity compared with
humoural factors (Irianto & Austin 2003). In shrimp aqua-
culture, probiotics strains (B. cereus, Paenibacil-
lus polymyxa and Pseudomonas sp.) enhanced the tolerance
of shrimps against the infection with pathogenic Vibrio spe-
cies (Vijayan et al. 2006; Ravi et al. 2007). Similar results
were obtained in L. vannamei and Penaeus japonicus fed
diets supplemented with Pediococcus pentosaceus, L. plan-
tarum or Biifidobacterium thermophilium, respectively
(Chiu et al. 2007; Adel et al. 2017a).
Probiotic effects on rearing water quality
The major disadvantage of using antibiotics to improve the
quality of rearing water is the growth of antibiotic-resistant
pathogenic bacteria (Akinbowale et al. 2006). The culture
environment helping to provide more beneficial microbial
organisms than the probiotics incorporated in diets (Fuller
1989). Interactive effects between aquaculture environment
and aquatic species have been confirmed for sustainable
aquaculture (Verschuere et al. 2000). Using of probiotics as
a bioremediation tool by the modulation of the microor-
ganism community and the inhibition of pathogenic bacte-
ria in the aquaculture environment resulted in improved
health status and performances of aquatic animals (Venka-
teswara 2007). Therefore, increased growth performance
and decreased diseases are interdependent and are linked to
microbial capacity in the aquaculture system. Water biore-
mediation effects of probiotics enhanced in case of using
Table 2 The application of probiotics in rearing water for sustainable aquaculture (modified from De et al. (2004))
Probiotic
Bacillus sp., Saccharomyces sp.
Bacillus sp., S. cerevisiae, Nitrosomonas sp.
Streptomyces sp.
B. subtilis and B. megaterium
Bacillus sp. and Lactobacillus
Bacillus circulans and B. licheniformis
Lactic acid bacteria
Arthrobacter XE-7
Bacillus strains (Bacillus subtilis, Bacillus licheniformis and
Bacillus pumilus)
Bacillus sp.
Mixed Bacillus
Enterococcus faecium ZJ4
Bacillus pumilus, B. licheniformis and B. Subtilis
Bacillus subtilis, Bacillus cereus and Bacillus licheniformis
6 © 2018 Wiley Publishing Asia Pty Ltd
multiple strains of bacteria and yeast (Kolndadacha et al.
2011). Several reports have highlighted that probiotics,
including bacteria and yeast, provide a more favourable
environment for fish through reducing the proliferation of
pathogenic bacteria and harmful phytoplankton as well as
via the bioremediation of organic wastes in rearing water
(Zorriehzahra et al. 2016; Banerjee & Ray 2017; Elsabagh
et al. 2018). For this purpose, probiotics have been pro-
duced commercially in several reasonable and specific
preparations for fish, shrimp and mollusc farming opera-
tions (Wang et al. 2005). The addition of live probiotic
cells to the aquaculture water environment improved the
rearing water quality resulting in the improvement of aqua-
tic animal health due to expulsion of pathogenic reasons
(Moriarty 1998). Therefore, probiotics used in aquaculture
are presented in several forms, whether as feed supplements
or water additives. The application of probiotics to rearing
water has been studied several times, as shown in Table 2.
Probiotic effects against stressful conditions
Environmental stressors normally weaken the immune sys-
tem of aquatic animals and increase their susceptibility to
infectious diseases (Dawood et al. 2017a,b). Stress is
defined as ‘physical or chemical factors that cause bodily
reactions that may contribute to disease or death’ (Rott-
mann et al. 1992). Besides the physical and chemical stres-
sors, the biological stress was defined as a ‘nonspecific
response of the body to any challenge’ (Selye 1985). Based
on the above-mentioned definitions, aquatic animals nor-
mally suffer from different stressors such as (transporta-
tion, malnutrition, stocking density, rearing temperature,
anoxia, hypoxia, hyperoxia, chemicals, pesticides and water
salinity; Das et al. 2005; Turnbull et al. 2005; North et al.
Dose References
108 + 105 CFU mL
1 Matias et al. (2002)
104–109 CFU mL
1 Wang et al. (2005)
2–10 g per kg feed Das et al. (2005)
1.2 9 104 CFU g
1 Olmos et al. (2011)
5.749  0.67 9 104 CFU g
1 Paiva-Maia et al. (2013)
1 9 106 CFU mL
1 Sahandi et al. (2012)
107 and 2 9 107 CFU mL
1 Gatesoupe (1994)
106 CFU mL
1 Li et al. (2006)
1.0 9 1010 CFU g
1 Elsabagh et al. (2018)
– Dalmin et al. (2001)
– Nimrat et al. (2012)
– Wang et al. (2008)
– Devaraja et al. (2013)
– Lalloo et al. (2007)
Reviews in Aquaculture, 1–18

2006; Raj et al. 2008; DeMicco et al. 2010; Lupatsch et al.
2010; Akhtar et al. 2011, 2012; Goncalves et al. 2011;
LeBlanc et al. 2011; Logan & Somero 2011; Prusty et al.
2011; Dawood et al. 2015a,b).
Apart from pathogen pressure, aquatic animals are nor-
mally subjected to environmental perturbations that can
severely affect their physiological state and increase the
oxidative stress in the animal (Lesser 2006; Zenteno-Sav
ın
et al. 2006; Wabete et al. 2008). Hence, to ameliorate the
effect of these oxidative stress factors, probiotics are fed to
the aquatic animals. It can therefore be assumed that the
probiotic-supplemented diet may increase the antioxidant
status by improving the diet utilisation and contribute to
increase the assimilation of dietary antioxidants from the
feed (Castex et al. 2009). Castex et al. (2009) hypothesised
that the antioxidative properties of a Lactobacillus fermen-
tum strain may serve as a defensive mechanism in the
intestinal microbial ecosystem and therefore help overcome
exogenous and endogenous oxidative stress (ess). L. fruc-
tivorans and L. plantarum, when administered to sea
bream, Sparus auratus, caused a significantly lower cortisol
level and higher heat-shock protein (HSP70) gene expres-
sion, and also resulted in significantly lower cumulative
mortality in probiotic-treated fish, subjected to an acute
pH stress (from 8.6 to 6.3) (Liu et al. 2010). It has been
reported that the protective mechanism of the aquatic ani-
mals is influenced by normal intestinal microflora com-
monly taken as probiotics, by increasing the immunity
especially the putative protective HSP under stress condi-
tions (Koninkx & Malago 2008). Taoka et al. (2006a) con-
cluded that a mixture of Bacillus subtilis, L. acidophilus,
Clostridium butyricum and Saccharomyces cerevisiae is help-
ful in increasing the stress tolerance in Paralichthys oli-
vaceus. In sea bream (S. auratus), cortisol level is increased
when subjected to acute stress condition by L. fructivorans
and L. plantarum supplementation (Varela et al. 2010).
Varela et al. (2010) also reported that the administration of
the probiotic strain, Pdp11, in the diet of S. auratus, helps
in promoting the growth as well as improves the stress tol-
erance to high stocking density, thus suggesting its benefi-
cial role in aquaculture industry.
Table 3 The application of probiotics to avoid the effects of different stress factors (modified from De et al. (2004))
Species Probiotic
Gilthead sea bream (Sparus auratus) Alteromonas sp. strain Pdp 11
Paralichthys olivaceus B. subtilis, L. acidophilus,
S. cerevisiae
Litopenaeus stylirostris Pediococcus acidilactici
Oyster larvae (Crassostrea virginica) Vibrio sp. strain OY15
Cultured fish and shrimp species Variety of probiotic preparations
Red sea bream (Pagrus major) Lactobacillus rhamnosus
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Probiotics for sustainable aquaculture
Supplementation of immunostimulants, vaccines and
probiotic bacteria in diets or the addition via rearing water
has been recommended to reduce the harmful effects of dif-
ferent stressors happened during the culture of aquatic ani-
mals (Akhtar et al. 2011, 2012; Rio-Zaragoza et al. 2011).
Probiotics viability has increased their efficiency in the
aquaculture ponds by mitigating the risks of high stocking
densities of cultured animals (Gatesoupe 1999; Gomez-Gil
et al. 2000). These probiotic bacteria can reduce biochemi-
cal stress levels when mixed with vitamins and nutrients
(Verschuere et al. 2000). The supplementation of Lacto-
bacillus delbrueckii in the diet of European sea bass
(D. labrax) resulted in lower cortisol levels (Carnevali et al.
2006). In line with the previous study, decreased cortisol
levels resulted in diminishing the stress happened during
transportation and handling of cardinal tetra
(Paracheirodon axelrodi) fed diets supplemented with Bacil-
lus spp. (Gomes et al. 2009). Table 3 presents the applica-
tion of probiotics in aquaculture to avoid the negative
effects that result from different stressors.
Inactivated or dead bacterial cells as probiotics
Probiotics defined also as ‘microbial cell preparations or
components of microbial cells that have a beneficial effect
on the health and well-being of the host’ (Salminen et al.
1999). This definition implies that probiotics definition
includes both viable and nonviable beneficial bacterial cells
(Ouwehand & Salminen 1998). The definition also clarified
that beneficial cells with probiotic characteristics do not
restrict that probiotics must be whole microbial cells, but
also portions of cells have been reported to improve host
health. The introduction of live bacterial cells to the aquatic
animals resulted in unaccepted outcomes to the aquacul-
ture environment (Salinas et al. 2008). Therefore, the use
of dead bacterial cells that could no longer interact with the
aquatic environment was considered (Salinas et al. 2008).
Inactivated or dead bacterial cells as probiotics are also
called as ‘postbiotic’ which described the effect of inacti-
vated bacteria or components of these bacteria. Postbiotics
are ‘non-viable bacterial products or metabolic byproducts
Stress References
High stocking density Varela et al. (2010)
Heat stress and pathogen Taoka et al. (2006a)
Vibrio anguillarum
Antioxidant status Castex et al. (2009)
Pathogenic stressors Kapareiko et al. (2011)
Pathogenic stressors Reviewed by Mohapatra
et al. (2013)
Low salinity stress Dawood et al. (2017c)
7
M. A. O. Dawood et al.
from probiotic microorganisms that have biologic activity
in the host’ (Fig. 1) (Patel & Denning 2013). Perhaps this
and other small molecule products of the normal flora are
at least partially responsible for the beneficial effects of the
normal flora (and exogenous probiotics and prebiotics).
Heat-killed probiotics also function, in the broad sense, as
postbiotics (Dawood et al. 2015a,b). Heat-killed microor-
ganisms retain important bacterial structures that may
exert biologic activity in the host. Dietary supplementation
of dead beneficial cells exhibited positive results regarding
the growth performance, immunity and disease resistance
of several aquatic animals (Irianto & Austin 2003; Diaz-
Rosales et al. 2006; Salinas et al. 2006; Choi & Yoon 2008;
Pan et al. 2008; Panigrahi et al. 2010; Rodriguez-Estrada
et al. 2013; Dawood et al. 2015a,b,c). Therefore, it can be
reasonably hypothesised that dead or inactivated bacterial
cells might constitute an effective alternative to live bacte-
rial supplementation in aquatic animal diets (Table 4).
Increasing the efficacy of probiotic
supplementation
Mostly, probiotics have been applied in a single form of
bacteria with one or more doses; however, using of differ-
ent strains of bacteria might be more beneficial to enhance
the performances of aquatic animals (Salinas et al. 2008).
Multispecies probiotic may be more effective than mono-
species supplementation due to the higher probability that
a microorganism consortium will survive in a changing
environment such as the gastrointestinal tract (GIT) and
dominate the associated microbiota (Verschuere et al.
2000; Timmerman et al. 2004; Nayak 2010). Few data are
available on the use of two or more strains as a probiotic
mixture and their effects on the aquatic animal perfor-
mance (Geng et al. 2012; Beck et al. 2015). Taken into
account, the diverse immune stimulation properties of
strain-specific properties and the great variety of
Figure 1 Mode of action of probiotics and postbiotics in the host.
8 © 2018 Wiley Publishing Asia Pty Ltd
antimicrobial properties associated with mixed formula-
tions, potential stimulation of the immune system could
prevent pathogen colonisation and improve the beneficial
microbial community in the GIT (Salinas et al. 2005; Pani-
grahi et al. 2007).
The combined application of probiotics and prebiotics,
known as ‘synbiotics’, is based on the principle of providing
a probiont with a competitive advantage over endogenous
populations; this advantage could improve the survival and
implantation of the live microbial dietary supplement in
the GIT of a host (Song et al. 2014). Synbiotic supplemen-
tation provided more benefits for aquatic animals when
compared with the single addition of only probiotics or
prebiotics (Merrifield et al. 2010a). The significance of
using synbiotic mixture is that prebiotic helps the live bac-
terial cells to show its positive effect in the intestinal tract
of cultured species, where the synbiotic preparations will be
relatively highly intolerant of oxygen, low pH and tempera-
ture (Song et al. 2014).
Synbiotics positively affect rainbow trout (O. mykiss) by
improving the survival and implantation of live microbial
dietary supplements in the GIT by selectively stimulating
the growth and activating the metabolism of a limited
number of health-promoting bacteria (Alak & Hisar 2012).
The potential effects of a synbiotic preparation containing
Enterococcus faecalis and two prebiotics (mannan oligosac-
charide (MOS) and poly-b-hydroxybutyrate (PHB))
increased the growth performance and feed utilisation of
rainbow trout (O. mykiss) (Rodriguez-Estrada et al. 2009).
Geng et al. (2012) reported that supplementation of synbi-
otic (B. subtilis and chitosan) in cobia (Rachycen-
tron canadum) diet showed improved growth performance.
Partida-Arangure et al. (2013) reported that supplementa-
tion of synbiotic (probiotic + inulin) improved the
immune response of white shrimp L. vannamei. In terms of
digestive enzymes activity, supplementation of synbiotic
(fructooligosaccharide (FOS) and MOS + B. clausii or/and
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Table 4 The application of inactivated probiotic bacteria in aquaculture
Species Probiotics
Rainbow trout Heat-killed Gordonia bronchialis
(Oncorhynchus mykiss)
Heat-inactivated Vibrionaceae 51M6 and
Pdp11
Heat-killed Lactobacillus rhamnosus
Inactivated Enterococcus faecalis
Atlantic cod (Gadus morhua) Heat-inactivated Pseudomonas sp. (GP21)
and Psychrobacter sp. (GP12)
Japanese pufferfish Heat-killed Lactobacillus paracasei spp.
(Takifugu rubripes) paracasei (strain 06TCa22) and
L. plantarum (strain 06CC2)
Heat-killed Lactobacillus paracasei spp.
paracasei (06TCa22)
Gilthead seabream Heat-inactivated Lactobacillus delbru¨eckii
(Sparus aurata L.) subsp. lactis and Bacillus subtilis
Heat-inactivated Bacillus subtilis
Nile tilapia Dead Bacillus subtilis,
(Oreochromis niloticus) Lactobacillus acidophilus,
Clostridium butyricum and
Saccharomyces cerevisiae
Dead Bacillus subtilis,
Lactobacillus acidophilus,
Clostridium butyricum and
Saccharomyces cerevisiae
Chinese drum (Miichthys miiuy) Heat-inactivated Clostridium butyrium
Sea bass (Dicentrarchus labrax) Heat-inactivated Lactobacillus farciminis
CNCM MA27/6R and
Lactobacillus rhamnosus CNCM MA27/6B
Atlantic cod (Gadus morhua) Heat-inactivated Pseudomonas sp. (GP21)
and Psychrobacter sp.
Red sea bream (Pagrus major) Heat-killed Lactobacillus plantarum
Heat-inactivated Pediococcus pentosaceus
Heat-killed Lactobacillus plantarum
Amberjack (Seriola dumerili) Heat-killed Lactobacillus plantarum
B. clausii) in grouper (Epinephelus coioides) diet resulted in
improved protease activity (Ye et al. 2011). Moreover,
Mehrabi et al. (2011) evaluated the dietary inclusion of dif-
ferent levels of synbiotic preparation composed of E. fae-
cium and FOS in rainbow trout diets; compared with the
control, the synbiotic supplementation resulted in
improved body weight gains. On the other hand, no signifi-
cant synergetic effects between B. subtilis and FOS were
observed on the growth performance, survival or feed utili-
sation of yellow croaker (Larimichthys crocea) (Ai et al.
2011).
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Probiotics for sustainable aquaculture
Effects References
Growth performance, intestinal Shabanzadeh et al. (2016)
histology and biochemical
parameters
Immune responses Choi and Yoon (2008)
Blood profiles Panigrahi et al. (2010)
Growth, immunity and disease Rodriguez-Estrada
protection et al. (2013)
Immune response and oxidative Lazado et al. (2010)
stress
Cytokine responses Biswas et al. (2013a)
Disease resistance Biswas et al. (2013b)
Cellular innate immune responses Salinas et al. (2006)
Immune response Cerezuela et al. (2012)
Immune response and disease Taoka et al. (2006b)
resistance
Digestive enzymes Taoka et al. (2007)
Immune response and disease Pan et al. (2008)
resistance
Digestive enzymes Frou€el et al. (2008)
Immune response Lazado and Caipang (2014)
Growth performance, Dawood et al. (2015a,b,d)
digestibility, immune response
and disease resistance
Growth performance, feed Dawood et al. (2016c)
utilisation and blood
characteristics
Immune responses and stress Dawood et al. (2016d)
resistance
Growth performance, digestibility Dawood et al. (2015c)
and immune response
Conclusion and the future of probiotic applications
in aquaculture
The above reviewed studies demonstrate that probiotics
can play a vital role for sustainable aquaculture, though it is
not clear whether probiotic or the terrestrial microorgan-
isms are the responsible about the enhanced production.
However, probiotic supplementation via feed is a better
method for ensuring the efficiency of probiotic bacteria in
the GIT of aquatic animals without adverse effects on the
surrounding environment. Therefore, in-depth knowledge
9
M. A. O. Dawood et al.
of the mode of action of probiotics is essential. Although
the effects of probiotics on the growth, feed efficiency, gut
microbiota and disease susceptibility as well as the innate
immune parameters, mucosal barriers and cell damage/
morphology of most aquatic animals have been investi-
gated thoroughly, their detailed mechanisms of action
remain unknown. Moreover, the species/strain/stage speci-
ficity of probiotics is a key concern that must be addressed
thoroughly and promptly.
The terrestrial microorganisms of aquatic animals are
considerably understudied compared to that of humans
and mammals, and its knowledge has been limited by the
fact that many species are not cultivable. However, the
advent of next-generation sequencing (NGS) technologies
has allowed for studying complex microbial ecosystems and
the growing appreciation of the importance of the indige-
nous microbiota of aquatic animals. In this regard, it is
noteworthy that the gut microbiota of aquatic animals is in
general more fluidic than that of terrestrial vertebrates, and
is highly sensitive to dietary changes, being also modulated
by life cycle variations, health status, farming conditions
and environmental and ecological factors.
Future research on the interaction between probiotic and
the terrestrial microorganisms should involve transcrip-
tomic and proteomic analyses. In addition, the transcrip-
tomic and proteomic profiling of gut microbiota should be
thoroughly documented to elucidate the various modes of
action of different probiotic organisms. Studies on probi-
otics should therefore be given high priority, and molecular
analysis should be included as standard procedure to assess
the effects of probiotics on fish health and nutrition.
Conflict of interest statement
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.
References
Abdelkhalek NK, Eissa IA, Ahmed E, Kilany OE, El-Adl M,
Dawood MAO et al. (2017) Protective role of dietary Spir-
ulina platensis against diazinon-induced Oxidative damage in
Nile tilapia; Oreochromis niloticus. Environmental Toxicology
and Pharmacology 54: 99–104.
Adel M, Yeganeh S, Dadar M, Sakai M, Dawood MAO (2016)
Effects of dietary Spirulina platensis on growth performance,
humoral and mucosal immune responses and disease
10
resistance in juvenile great sturgeon (Huso huso Linnaeus,
1754). Fish & Shellfish Immunology 56: 436–444.
Adel M, Yeganeh S, Dawood MAO, Safari R, Radhakrishnan S
(2017a) Effects of Pediococcus pentosaceus supplementation on
growth performance, intestinal microflora and disease resis-
tance of white shrimp, Litopenaeus vannamei. Aquaculture
Nutrition 23: 1401–1409.
Adel M, Caipang CMA, Dawood MAO (2017b) Immunological
responses and disease resistance of rainbow trout (Oncor-
hynchus mykiss) juveniles following dietary administration of
stinging nettle (Urtica dioica). Fish & Shellfish Immunology 7:
230–238.
Ai Q, Xu H, Mai K, Xu W, Wang J (2011) Effects of dietary sup-
plementation of Bacillus subtilis and fructooligosaccharide on
growth performance, survival, non-specific immune response
and disease resistance of juvenile large yellow croaker, Larim-
ichthys crocea. Aquaculture 317: 155–161.
Akhtar MS, Pal AK, Sahu NP, Alexander C, Meena DK (2011)
Dietary pyridoxine enhances thermal tolerance of Labeo rohita
(Hamilton) fingerlings reared under endosulfan stress. Journal
of Thermal Biology 36: 84–88.
Akhtar MS, Pal AK, Sahu NP, Ciji A, Meena DK, Das P (2012)
Physiological responses of dietary tryptophan fed Labeo rohita
to temperature and salinity stress. Journal of Animal Physi-
ololgy & Animal Nutrition 97: 1075–1083.
Akinbowale OL, Peng H, Barton MD (2006) Antimicrobial resis-
tance in bacteria isolated from aquaculture sources in Aus-
tralia. Journal of Applied Microbiology 100: 1103–1113.
Alak G, Hisar SA (2012) The effects of probiotics and prebiotics
on rainbow trout (Oncorhynchus mykiss) intestinal flora.
International Journal of Aquaculture 2(3): 11–14.
Al-Dohail MA, Hashim R, Aliyu-Paiko M (2009) Effects of the
probiotic, Lactobacillus acidophilus, on the growth perfor-
mance, haematology parameters and immunoglobulin con-
centration in African catfish (Clarias gariepinus, Burchell
1822) fingerling. Aquaculture Research 40: 1642–1652.
Aliko V, Qirjo M, Sula E, Morina V, Faggio C (2018) Antioxi-
dant defense system, immune response and erythron profile
modulation in Gold fish, Carassius auratus, after acute man-
ganese treatment”. Fish & Shellfish Immunology 76: 101–109.
Aragona M, Lauriano ER, Pergolizzi S, Faggio C (2017) Opuntia
ficus-indica (L.) Miller as a source of bioactivity compounds
for health and nutrition. Natural Product Research 14: 1–13.
https://doi.org/10.1080/14786419.2017.1365073.
Arıg N, Suzer C, Gokvardar A, Basaran F, Coban D, Yldırım S
et al. (2013) Effects of probiotic (Bacillus sp.) supplementa-
tion during larval development of Gilthead sea bream (Sparus
aurata, L.). Turkish Journal of Fisheries and Aquatic Sciences
13: 407–414.
Austin B (2006) The bacterial microflora of fish, revised. Scien-
tific World Journal 6: 931–945.
Avella MA, Place A, Du SJ, Williams E, Silvi S (2012) Lactobacil-
lus rhamnosus accelerates Zebrafish backbone calcification
and gonadal differentiation through effects on the GnRH and
IGF systems. PLoS ONE 7(9): 45572.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd

Banerjee G, Ray AK (2017) The advancement of probiotics
research and its application in fish farming industries.
Research in Veterinary Science 115: 66–77.
Beck BR, Kim D, Jeon J, Lee SM, Kim HK, Kim OJ et al. (2015)
The effects of combined dietary probiotics Lactococcus lactis
BFE920 and Lactobacillus plantarum FGL0001 on innate
immunity and disease resistance in olive flounder (Par-
alichthys olivaceus). Fish & Shellfish Immunology 42(1): 177–
183.
Biswas G, Korenaga H, Nagamine R, Takayama H, Kawahara S,
Takeda S et al. (2013a) Cytokine responses in the Japanese
pufferfish (Takifugu rubripes) head kidney cells induced with
heat-killed probiotics isolated from the Mongolian dairy
products. Fish & Shellfish Immunology 34: 1170–1177.
Biswas G, Korenaga H, Nagamine R, Kawahara S, Takeda S,
Kikuchi Y et al. (2013b) Elevated cytokine responses to Vibrio
harveyi infection in the Japanese pufferfish (Takifugu rubripes)
treated with Lactobacillus paracasei spp. paracasei (06TCa22)
isolated from the Mongolian dairy product. Fish & Shellfish
Immunology 35: 756–765.
Bolasina S, Perez A, Yamashita Y (2006) Digestive enzymes
activity during ontogenetic development and effect of starva-
tion in Japanese flounder (Paralichthys olivaceus). Aquaculture
252: 503–515.
Bonnet S, Webb A, Panzeca C, Karl DM, Capone DG, Sanudo-
Wilhelmy SA (2010) Vitamin B12 excretion by cultures of the
marine cyanobacteria Crocosphaera and Synechococcus. Lim-
nology and Oceanography 55: 1959–1964.
Burr G, Gatlin D, Ricke S (2007) Microbial ecology of the gas-
trointestinal tract of fish and the potential application of pre-
biotics and probiotics in fin fish aquaculture. Journal of the
World Aquaculture Society 36: 425–436.
Carbone D, Faggio C (2016) Importance of prebiotics in aqua-
culture as immunostimulants. Effects on immune system of
Sparus aurata and Dicentrarchus labrax. Fish & Shellfish
Immunology 54: 172–178.
Carnevali O, de Vivo L, Sulpizio R (2006) Growth improvement
by probiotic in European sea bass juveniles (Dicentrarchus
labrax, L), with particular attention to IGF-1, myostatin and
cortisol gene expression. Aquaculture 258: 430–438.
Castex M, Lemaire P, Wabete N, Chim L (2009) Effect of dietary
probiotic Pediococcus acidilactici on antioxidant defences and
oxidative stress status of shrimp, Litopenaeus stylirostris.
Aquaculture 294: 306–313.
Cerezuela R, Cuesta A, Meseguer J, Esteban M (2012) Effects of
dietary inulin and heat-inactivated Bacillus subtilis on gilthead
seabream (Sparus aurata L.) innate immune parameters. Ben-
eficial Microbes 3 (1): 77–81.
Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Mor-
i~
nigo MA,
Esteban MA
(2013) Changes in intestinal morphol-
ogy and microbiota caused by dietary administration of
inulin and Bacillus subtilis in gilthead sea bream (Sparus aur-
ata). Fish & Shellfish Immunology 34: 1063–1070.
Chabrill
on M, Rico R, Arijo S, Diaz-Rosales P, Balebona M,
Morinigo M (2005) Interactions of microorganisms isolated
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd
Probiotics for sustainable aquaculture
from gilthead sea bream, Sparus aurata L., on Vibrio harveyi, a
pathogen of farmed Senegalese sole, Solea senegalensis (Kaup).
Journal of Fish Diseases 28: 531–537.
Chiu CH, Guu YK, Liu CH, Pan TM, Cheng W (2007) Immune
responses and gene expression in white shrimp, Litopenaeus
vannamei, induced by Lactobacillus plantarum. Fish & Shellfish
Immunology 23: 364–377.
Choi SH, Yoon TJ (2008) Non-specific immune response of
rainbow trout (Oncorhynchus Mykiss) by dietary heat-inacti-
vated potential probiotics. Immune Network 8(3): 67–74.
Dahiya T, Sihag RC, Gahlawat SK (2012) Effect of probiotics on
the haematological parameters of Indian magur (Clarius
batrachus L). Journal of Fisheries and Aquatic Science 7: 279–
290.
Dalmin G, Kathiresan K, Purushothaman A (2001) Effect of
probiotics on bacterial population and health status of shrimp
in culture pond ecosystem. Indian Journal of Experimental
Biology 39: 939–942.
Das T, Pal AK, Chakraborty SK, Manush SM, Sahu NP, Mukher-
jee SC (2005) Thermal tolerance, growth and oxygen con-
sumption of Labeo rohita fry (Hamilton, 1822) acclimated to
four temperatures. Journal of Thermal Biology 30: 378–383.
Dawood MAO (2016) Effect of various feed additives on the per-
formance of aquatic animals (Doctoral dissertation, 鹿児島大
学). The United Graduate School of Agricultural Sciences,
Kagoshima University, Kagoshima, Japan.
Dawood MAO, Koshio S (2016a) Recent advances in the role of
probiotics and prebiotics in carp aquaculture: a review. Aqua-
culture 454: 243–251.
Dawood MAO, Koshio S (2016b) Vitamin C supplementation
to optimize growth, health and stress resistance in aquatic
animals. Reviews in Aquaculture 10: 334–350.
Dawood MAO, El-Dakar A, Mohsen M, Abdelraouf E, Koshio S,
Ishikawa M et al. (2014) Effects of using exogenous digestive
enzymes or natural enhancer mixture on growth, feed utiliza-
tion, and body composition of rabbitfish, Siganus rivulatus.
Journal of Agricultural Science and Technology. B, 4 (3B): 180–
187.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2015a)
Effects of partial substitution of fish meal by soybean
meal with or without heat-killed Lactobacillus plantarum
(LP20) on growth performance, digestibility, and immune
response of amberjack, Seriola dumerili juveniles. BioMed
Research International 2015. http://dx.doi.org/10.1155/2015/
514196.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2015b)
Effects of heat killed Lactobacillus plantarum (LP20) supple-
mental diets on growth performance, stress resistance and
immune response of red sea bream, Pagrus major. Aquaculture
442: 29–36.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2015c)
Interaction effects of dietary supplementation of heat-killed
Lactobacillus plantarum and b-glucan on growth performance,
digestibility and immune response of juvenile red sea bream,
Pagrus major. Fish & Shellfish Immunology 45(1): 33–42.
11
M. A. O. Dawood et al.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2015d) Effi-
ciency of Heat-killed Lactobacillus plantarum supplemental
diets on red sea bream, Pagrus major. World Aquaculture
2015 Jeju. Korea (한국수산과학회 양식분과 학술대회),
112. Jeju. Korea: World Aquaculture Society.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini
MF, Hossain MS et al. (2016a) Effects of dietary supplemen-
tation of Lactobacillus rhamnosus or/and Lactococcus lactis on
the growth, gut microbiota and immune responses of red sea
bream, Pagrus major. Fish & Shellfish Immunology 49: 275–
285.
Dawood MAO, Koshio S, Ishikawa M, El-Sabagh M, Esteban
MA, Zaineldin AI (2016b) Probiotics as an environment-
friendly approach to enhance red sea bream, Pagrus major
growth, immune response and oxidative status. Fish & Shell-
fish Immunology 57: 170–178.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2016c)
Effects of dietary inactivated Pediococcus pentosaceus on
growth performance, feed utilization and blood characteristics
of red sea bream, Pagrus major juvenile. Aquaculture Nutrition
22: 923–932.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2016d)
Immune responses and stress resistance in red sea bream,
Pagrus major, after oral administration of heat-killed Lacto-
bacillus plantarum and vitamin C. Fish & Shellfish Immunology
54: 266–275.
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini
MF, Hossain MS et al. (2017a) Dietary supplementation of b-
glucan improves growth performance, the innate immune
response and stress resistance of red sea bream, Pagrus major.
Aquaculture Nutrition 23(1): 148–159.
Dawood MAO, Koshio S, El-Sabagh M, Billah MM, Zaineldin
AI, Zayed MM et al. (2017b) Changes in the growth, humoral
and mucosal immune responses following b-glucan and vita-
min C administration in red sea bream, Pagrus major. Aqua-
culture 470: 214–222.
Dawood MAO, Koshio S, Ishikawa M, El-Sabagh M, Yokoyama
S, Wang WL et al. (2017c) Physiological response, blood
chemistry profile and mucus secretion of red sea bream
(Pagrus major) fed diets supplemented with Lactobacillus
rhamnosus under low salinity stress. Fish Physiology and Bio-
chemistry 43(1): 179–192.
Dawood MAO, Koshio S, Esteban MA
(2017d) Beneficial roles
of feed additives as immunostimulants in aquaculture: a
review. Reviews in Aquaculture. https://doi.org/10.1111/raq.
12209.
De BC, Meena DK, Behera BK, Das P, Mohapatra PD, Sharma
AP (2014) Probiotics in fish and shellfish culture:
immunomodulatory and ecophysiological responses. Fish
Physiology and Biochemistry 40(3): 921–971.
DeMicco A, Cooper KR, Richardson JR, White LA (2010) Devel-
opmental neurotoxicity of pyrethroid insecticides in Zebra
fish embryos. Toxicological Sciences 113: 177–186.
Devaraja T, Banerjee S, Sariff YM, Khatoon H (2013) A holistic
approach for selection of Bacillus sp. as a bioremediator for
12
shrimp post larvae culture. Turkish Journal of Biology 37: 92–
100.
Diaz-Rosales P, Salinas I, Rodr0 ıguez A, Cuesta A, Chabrill0 on
M, Balebona MC et al. (2006) Gilthead Sea bream (Sparus
aurata L.) innate immune response after dietary administra-
tion of heat-inactivated potential probiotics. Fish & Shellfish
Immunology 20: 482–492.
Dossou S, Koshio S, Ishikawa M, Yokoyama S, Dawood MAO,
El Basuini MF et al. (2018a) Growth performance, blood
health, antioxidant status and immune response in red sea
bream (Pagrus major) fed Aspergillus oryzae fermented rape-
seed meal (RM-Koji). Fish & Shellfish Immunology 75: 253–
262.
Dossou S, Koshio S, Ishikawa M, Yokoyama S, Dawood MAO,
El Basuini MF et al. (2018b) Effect of partial replacement of
fish meal by fermented rapeseed meal on growth, immune
response and oxidative condition of red sea bream juvenile,
Pagrus major. Aquaculture 490: 228–235.
El Basuini MF, El-Hais AM, Dawood MAO, Abou-Zeid AES,
EL-Damrawy SZ, Khalafalla MMES et al. (2016) Effect of dif-
ferent levels of dietary copper nanoparticles and copper sul-
fate on growth performance, blood biochemical profiles,
antioxidant status and immune response of red sea bream
(Pagrus major). Aquaculture 455: 32–40.
El Basuini MF, El-Hais AM, Dawood MAO, Abou-Zeid AS, EL-
Damrawy SZ, Khalafalla MS et al. (2017) Effects of dietary
copper nanoparticles and vitamin C supplementations on
growth performance, immune response and stress resistance
of red sea bream, Pagrus major. Aquaculture Nutrition 23 (6):
1329–1340.
Elsabagh M, Mohamed R, Moustafa EM, Hamza A, Farrag F,
Decamp O et al. (2018) Assessing the impact of Bacillus
strains mixture probiotic on water quality, growth perfor-
mance, blood profile and intestinal morphology of Nile tila-
pia, Oreochromis niloticus. Aquaculture Nutrition. https://doi.
org/10.1111/anu.12797.
Essa MA, El-Serafy SS, El-Ezabi MM, Daboor SM, Esmael NA,
Lall SP (2010) Effect of different dietary probiotics on growth,
feed utilization and digestive enzymes activities of Nile tilapia,
Oreochromis niloticus. Journal of the Arabian Aquaculture Soci-
ety 5(2): 143–162.
Faggio C, Piccione G, Marafioti S, Arfuso F, Trischitta F, Fortino
G et al. (2014) Monthly variations of haematological parame-
ters of Sparus aurata and Dicentrarchus labrax reared in
Mediterranean land off-shore tanks. Cahiers de Biologie Mar-
ine 55: 437–443.
FAO/WHO, (2001) Report of a Joint FAO/WHO Expert Consul-
tation on Evaluation of Health and Nutritional Properties of
Probiotics in Food Including Powder Milk with Live Lactic Acid
Bacteria. C
ordoba, Argentina. http://www.fao.org/3/a-a0512e.
pdf.
Fazio F, Marafioti S, Torre A, Sanfilippo M, Panzera M, Faggio
C (2013) Haematological and serum protein profiles of Mugil
cephalus: effect of two different habitat. Ichthyological Research
60(1): 36–42.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd

Firouzbakhsh F, Noori F, Khalesi MK, Jani-Khalili K (2011)
Effects of a probiotic, protexin, on the growth performance
and hematological parameters in the Oscar (Astronotus
ocellatus) fingerlings. Fish Physiology and Biochemistry 37:
833–842.
Frou€el S, Le Bihan E, Serpentini A, Lebel JM, Koueta N, Nicolas
JL (2008) Preliminary study of the effects of commercial lac-
tobacilli preparations on digestive metabolism of juvenile sea
bass (Dicentrarchus labrax). Journal of Molecular Microbiology
and Biotechnology 14(1–3): 100–106.
Fuller R (1989) Probiotics in man and animals: a review. Journal
of Applied Bacteriology 68: 365–378.
Gajardo K, Rodiles A, Kortner TM, Krogdahl  A, Bakke AM,
Merrifield DL et al. (2016) A high-resolution map of the gut
microbiota in Atlantic salmon (Salmio salar): a basis for com-
parative gut microbial research. Scientific Reports 6: 30893.
Gatesoupe FJ (1994) Lactic acid bacteria increase the resistance
of turbot larvae, Scophthalmus maximus, against pathogenic
vibrio. Aquatic Living Resources 7: 277–282.
Gatesoupe FJ (1999) The use of probiotic in aquaculture. Aqua-
culture 180: 147–165.
Geng X, Dong X-H, Tan B-P, Yang Q-H, Chi S-Y, Liu H-Y et al.
(2012) Effects of dietary probiotic on the growth perfor-
mance, non-specific immunity and disease resistance of cobia,
Rachycentron canadum. Aquaculture Nutrition 18: 46–55.
Gioacchini G, Giorgini E, Merrifield DL, Hardiman G, Borini A
(2012) Probiotics can induce follicle maturational compe-
tence: the Danio rerio case. Biology of Reproduction 86: 65.
Giorgio G, Nina C, Yantyati W (2010) Importance of Lacto-
bacilli in food and feed biotechnology. Research in Microbiol-
ogy 161: 480–487.
Giri SS, Sukumaran V, Oviya M (2013) Potential probiotic Lac-
tobacillus plantarum VSG3 improves the growth, immunity,
and disease resistance of tropical freshwater fish, Labeo rohita.
Fish & Shellfish Immunology 34: 660–666.
Gomes LC, Brinn RP, Marcon JL, Dantas LA, Brandao FR, Sam-
paio de Abreu J et al. (2009) Benefits of using the probiotic
Efinol L during transportation of cardinal tetra (Paracheiro-
don axelrodi) in the Amazon. Aquaculture Research 40: 157–
165.
G
omez GD, Balc
azar JL (2008) A review on the interactions
between gut microbiota and innate immunity of fish. FEMS
Immunology and Medical Microbiology 52: 145–154.
Gómez R, Geovanny D, Shen MA (2008) Influence of probiotics
on the growth and digestive enzyme activity of white Pacific
shrimp (Litopenaeus vannamei). Oceanic and Coastal Sea
Research 7: 215–218.
Gomez-Gil B, Roque A, Turnbull JF (2000) The use and selec-
tion of probiotic bacteria for use in the culture of larval aqua-
tic organisms. Aquaculture 191: 259–270.
Goncalves AT, Maita M, Futami K, Endo M, Katagiri T (2011)
Effects of a probiotic bacterial Lactobacillus rhamnosus dietary
supplement on the crowding stress response of juvenile
Nile tilapia (Oreochromis niloticus). Fisheries Science 77: 633–
642.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd
Probiotics for sustainable aquaculture
Grosell M, Farrel AP, Brauner CJ (2011) The Multifunctional
Gut of Fish: Fish Physiology. vol 30, pp. 165–212. Academic
Press, London, UK.
Guardiola FA, Porcino C, Cerezuela R, Cuesta A, Faggio C, Este-
ban MA (2016) Impact of date palm fruits extracts and probi-
otic enriched diet on antioxidant status, innate immune
response and immune-related gene expression of European
seabass (Dicentrarchus labrax). Fish & Shellfish Immunology
52: 298–308.
Gullian M, Thompson F, Rodriguez J (2004) Selection of probi-
otic bacteria and study of their immunostimulatory effect in
Penaeus vannamei. Aquaculture 233: 1–14.
Hansen GH, Olafsen JA (1999) Bacterial interactions in early life
stages of marine cold water fish. Microbial Ecology 38: 1–26.
He S, Liu W, Zhou Z, Mao W, Ren P (2011) Evaluation of pro-
biotic strain Bacillus subtilis C-3102 as a feed supplement for
koi carp (Cyprinus carpio). Journal of Aquaculture Research &
Development 3 (Suppl): S1–S005.
Hern
andez-Serrano P (2005) Responsible use of antibiotics in
aquaculture. FAO Fisheries Technical Paper 469, Food and
Agriculture Organization of the United Nations, Rome, 97
pp.
Hidalgo MC, Skalli A, Abell
an E, Arizcun M, Cardenete G
(2006) Dietary intake of probiotics and maslinic acid in juve-
nile dentex (Dentex dentex L.): effects on growth performance,
survival and liver proteolytic activities. Aquaculture Nutrition
12: 256–266.
Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon
JI (2001) Molecular analysis of commensal host-microbial
relationships in the intestine. Science 291: 881–884.
Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM,
Dawood MA et al. (2016) Efficacy of nucleotide related prod-
ucts on growth, blood chemistry, oxidative stress and growth
factor gene expression of juvenile red sea bream, Pagrus
major. Aquaculture 464: 8–16.
Hovda M, Lunestad B, Fontanillas R, Rosnes J (2007) Molecular
characterization of the intestinal microbiota of farmed Atlan-
tic salmon (Salmo salar L.). Aquaculture 272: 581–588.
Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH,
Chinwalla AT et al. (2012) Structure, function and diversity
of the healthy human microbiome. Nature 486: 207–214.
Irianto A, Austin B (2002) Probiotic in aquaculture. Journal of
Fish Diseases 25: 633–642.
Irianto A, Austin B (2003) Use of dead probiotic cells to control
furunculosis in rainbow trout, Oncorhynchus mykiss (Wal-
baum). Journal of Fish Diseases 26: 59–62.
Kapareiko D, Hyun JL, Eric JS, Ammar H, Gary HW (2011) Iso-
lation and evaluation of new probiotic bacteria for use in
shellfish hatcheries: II. Effects of a Vibrio sp. probiotic candi-
date upon survival of oyster larvae (Crassostrea Virginica) in
pilot-scale trials. Journal of Shellfish Research 30: 617–625.
Kar N, Ghosh K (2008) Enzyme producing bacteria in the gas-
trointestinal tracts of Labeo rohita (Hamilton) and channa
punctatus (Bloch). Turkish Journal of Fisheries and Aquatic
Sciences 8: 115–120.
13
M. A. O. Dawood et al.
Kolndadacha OD, Adikwu IA, Okaeme AN, Atiribom RY,
Mohammed A, Musa YM (2011) The role of probiotics in
aquaculture in Nigeria (a review). Continental Journal of Fish-
eries and Aquatic Science 5(1): 8–15.
Koninkx JFJG, Malago JJ (2008) The protective potency of pro-
biotic bacteria and their microbial products against enteric
infections-review. Folia Microbiologica 53: 189–194.
Lalloo R, Ramchuran S, Ramduth D, G€ orgens J, Gardiner N
(2007) Isolation and selection of Bacillus spp. as potential bio-
logical agents for enhancement of water quality in culture of
ornamental fish. Journal of Applied Microbiology 103: 1471–
1479.
Lara-Flores M, Aguirre-Guzman G (2009) The use of probiotic
in fish and shrimp aquaculture (a review). In: Perez-Guerra
N, Pastrana-Castro L (eds) Probiotics: Production, Evaluation
and Uses in Animal Feed, pp. 75–89. Research Signpost, Ker-
ala.
Lauriano ER, Pergolizzi S, Capillo G, Kuciel M, Alesci A, Faggio
C (2016) Immunohistochemical characterization of Toll-like
receptor 2 in gut epithelial cells and macrophages of goldfish
Carassius auratus fed with a high-cholesterol diet. Fish &
Shellfish Immunology 59: 250–255.
Lazado CC, Caipang CMA (2014) Bacterial viability differen-
tially influences the immunomodulatory capabilities of poten-
tial host-derived probiotics in the intestinal epithelial cells of
Atlantic cod Gadus morhua. Journal of Applied Microbiology
116: 990–998.
Lazado CC, Caipang CMA, Gallage S, Brinchmann MF, Kiron V
(2010) Expression profiles of genes associated with immune
response and oxidative stress in Atlantic cod, Gadus morhua
head kidney leukocytes modulated by live and heat-inacti-
vated intestinal bacteria. Comparative Biochemistry and Physi-
ology Part B: Biochemistry and Molecular Biology 155: 249–
255.
Lazado CC, Caipang CMA, Estante EG (2015) Prospects of host-
associated microorganisms in fish and penaeids as probiotics
with immunomodulatory functions. Fish & Shellfish
Immunology 45(1): 2–12.
LeBlanc S, Middleton S, Gilmour KM, Currie S (2011) Chronic
social stress impairs thermal tolerance in the rainbow trout
(Oncorhynchus mykiss). Journal of Experimental Biology 214:
1721–1731.
Lesser MP (2006) Oxidative stress in marine environments: bio-
chemistry and physiological ecology. Annual Review of Physi-
ology 68: 253–278.
Li J, Tan B, Mai K, Ai Q, Zhang W, Xu W et al. (2006) Compar-
ative study between probiotic bacterium Arthrobacter XE-7
and chloramphenicol on protection of Penaeus chinensis post-
larvae from pathogenic vibrios. Aquaculture 253(1): 140–147.
Liu CH, Chiu CS, Ho PL, Wang SW (2009) Improvement in the
growth performance of white shrimp, Litopenaeus vannamei,
by a protease-producing probiotic, Bacillus subtilis E20, from
natto. Journal of Applied Microbiology 107: 1031–1041.
Liu KF, Chiu CH, Shiu YL, Cheng W, Liu CH (2010) Effects of
the probiotic, Bacillus subtilisE20, on the survival,
14
development, stress tolerance, and immune status of white
shrimp, Litopenaeus vannamei larvae. Fish and Shellfish
Immunology 28: 837–844.
Liu W, Ren P, He S, Xu L, Yang Y, Gu Z et al. (2013) Compar-
ison of adhesive gut bacteria composition, immunity, and dis-
ease resistance in juvenile hybrid tilapia fed two different
Lactobacillus strains. Fish & Shellfish Immunology 35: 54–62.
Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Tele-
ost microbiomes: the state of the art in their characterization,
manipulation and importance in aquaculture and fisheries.
Frontiers in Microbiology 5: 207.
Logan CA, Somero GN (2011) Effects of thermal acclimation on
transcriptional responses to acute heat stress in the euryther-
mal fish Gillichthys mirabilis (Cooper). American Journal of
Physiology: Regulatory, Integrative and Comparative Physiology
300: 1373–1383.
Lupatsch GA, Santos JW, Schrama JA, Verreth J (2010) Effect of
stocking density and feeding level on energy expenditure and
stress responsiveness in European sea bass (Dicentrarchus lab-
rax). Aquaculture 298: 245–250.
Magnadottir B (2010) Immunological control of fish diseases.
Journal of Marine Biotechnology 12: 36–379.
Matias HB, Yusoff FM, Shariff M, Azhari O (2002) Effects
of commercial microbial products on water quality in
tropical shrimp culture ponds. Asian Fisheries Science 15:
239–248.
Mart
ınez Cruz P, Ib
an~ez AL, Monroy Hermosillo OA, Ram
ırez
Saad HC (2012) Use of probiotics in aquaculture. ISRN
Microbiology 2012. http://dx.doi.org/10.5402/2012/916845
Mehrabi Z, Firouzbakhsh F, Jafarpour A (2011) Effects of dietary
supplementation of synbiotic on growth performance, serum
biochemical parameters and carcass composition in rainbow
trout (Oncorhynchus mykiss) fingerlings. Journal of Animal
Physiololgy & Animal Nutrition 24: 0396–1439.
Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RT,
Bøgwald J et al. (2010a) The current status and future focus
of probiotic and prebiotic applications for salmonids. Aqua-
culture 302(1): 1–18.
Merrifield DL, Bradley G, Baker RTM, Davies SJ (2010b) Probi-
otic applications for rainbow trout (Oncorhyncus mykiss Wal-
baum) II. Effects on growth performance, feed utilization,
intestinal microbiota and related health criteria post antibiotic
treatment. Aquaculture Nutrition 16: 496–503.
Mohapatra S, Chakraborty T, Prusty AK, Das P, Prasad PK,
Mohanta KN (2012) Use of different microbial probiotics
in the diet of rohu (Labeo rohita) fingerlings: effect on
growth, nutrient digestibility and retention, digestive
enzyme activities and intestinal microflora. Aquaculture
Nutrition 18: 1–11.
Mohapatra S, Chakraborty T, Kumar V, DeBoeck G, Mohanta
KN (2013) Aquaculture and stress management: a review of
probiotic intervention. Journal of Animal Physiololgy & Ani-
mal Nutrition 97(3): 405–430.
Moriarty DJW (1998) Control of luminous Vibrio sp. in penaeid
aquaculture ponds. Aquaculture 164: 351–358.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd

Nath S, Matozzo V, Bhandari D, Faggio C (2018) Growth and
liver histology of Channa punctatus exposed to a common
biofertilizer. Natural Product Research 28: 1–8.
Nayak S (2010) Probiotics and immunity: a fish perspective. Fish
& Shellfish Immunology 29: 2–14.
Newaj-Fyzul A, Al-Harbi AH, Austin B (2014) Developments in
the use of probiotics for disease control in aquaculture. Aqua-
culture 431: 1–11.
Nimrat S, Suksawat S, Boonthai T, Vuthiphandchai V (2012)
Potential Bacillus probiotics enhance bacterial numbers, water
quality and growth during early development of white shrimp
(Litopenaeus vannamei). Veterinary Microbiology 159: 443–
450.
North BP, Turnbull JF, Ellis T, Porter MJ, Migaud H, Bron J et al.
(2006) The impact of stocking density on the welfare of
rainbow trout (Oncorhynchus mykiss). Aquaculture 255: 466–
479.
O’Hara A, Shanahan F (2006) The gut flora as a forgotten organ.
EMBO Reports. 7: 688–693.
Olmos J, Ochoa L, Paniagua-Michel J, Contreras R (2011) Func-
tional feed assessment on Litopenaeus vannamei using 100%
fish meal replacement by soybean meal, high levels of complex
carbohydrates and Bacillus probiotic strains. Marine Drugs 9:
1119–1132.
Ouwehand AC, Salminen SJ (1998) The health effects of cul-
tured milk products with viable and non-viable bacteria.
International Dairy Journal 8: 749–756.
Ouwehand AC, Salminen S, Isolauri E (2002) Probiotics: an
overview of beneficial effects. Antoine Van Leewenhoek 82:
279–289.
Pais R, Khushiramani R, Karunasagar I, Karunasagar I (2008)
Effect of immunostimulants on the haemolymph haemagglu-
tinins of tiger shrimp (Penaeus monodon). Aquaculture
Research 39: 1339–1345.
Pan X, Wu T, Song Z, Tang H, Zhao Z (2008) Immune
responses and enhanced disease resistance in Chinese Drum,
Miichthys miiuy (Basilewsky), after oral administration of live
or dead cells of Clostridium butyrium CB2. Journal of Fish Dis-
eases 31: 679–686.
de Paiva-Maia E, Alves-Modesto G, Otavio-Brito L, Olivera A,
Vasconcelos-Gesteira TC (2013) Effect of a commercial probi-
otic on bacterial and phytoplankton concentration in inten-
sive shrimp farming (Litopenaeus vannamei) recirculation
systems. Latin American Journal of Aquatic Research [online]
41: 126–137.
Panigrahi A, Kiron V, Kobayashi T, Puangkaew J, Satoh S,
Sugita H (2004) Immune responses in rainbow trout (Oncor-
hynchus mykiss) induced by a potential probiotic bacteria Lac-
tobacillus rhamnosus JCM 1136. Veterinary Immunology and
Immunopathology 102: 379–388.
Panigrahi A, Kiron V, Satoh S, Hirono I, Kobayashi T, Sugita H
et al. (2007) Immune modulation and expression of cytokine
genes in rainbow trout Oncorhynchus mykiss upon probiotic
feeding. Developmental and Comparative Immunology 31:
372–382.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd
Probiotics for sustainable aquaculture
Panigrahi A, Kiron V, Satoh S, Watanabe T (2010) Probiotic
bacteria Lactobacillus rhamnosus influences the blood profile
in rainbow trout, Oncorhynchus mykiss (Walbaum). Fish Phys-
iology and Biochemistry 36: 969–977.
Parker RB (1974) Probiotics, the other half of the antibiotic
story. Animal Nutrition & Health 29: 4–8.
Partida-Arangure BO, Luna-Gonz
alez A, Fierro-Coronado JA,
del Carmen Flores-Miranda M, Gonz
alez-Ocampo HA (2013)
Effect of inulin and probiotic bacteria on growth, survival,
immune response, and prevalence of white spot syndrome
virus (WSSV) in Litopenaeus vannamei cultured under labora-
tory conditions. African Journal of Biotechnology 12: 3366–
3375.
Patel RM, Denning PW (2013) Therapeutic use of prebiotics,
probiotics, and postbiotics to prevent necrotizing enterocoli-
tis: what is the current evidence? Clinics in Perinatology 40(1):
11–25.
Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A,
Chansue N et al. (2011) Modulation of intestinal morphology
and immunity in Nile tilapia (Oreochromis niloticus) by Lacto-
bacillus rhamnosus GG. Research in Veterinary Science 91: 92–
97.
Prusty AK, Kohli MPS, Sahu NP, Pal AK, Saharan N, Mohapatra
S et al. (2011) Effect of short term exposure of fenvalerate on
biochemical and haematological responses in Labeo rohita
(Hamilton) fingerlings. Pesticide Biochemistry and Physiology
100: 124–129.
Purwandari AR, Chen HY (2013) Effects of probiotic Bacillus
subtilis on intestinal microbial diversity and immunity of
Orange spotted grouper Epinephelus coioides. Journal of
Applied Biotechnology 1(1): 25–36.
Rahiman KMM, Jesmi Y, Thomas AP, Hatha AAM (2010) Pro-
biotic effect of Bacillus NL110 and Vibrio NE17 on the sur-
vival, growth performance and immune response of
Macrobrachium rosenbergii (de Man). Aquaculture Research 41
(9): 120–134.
Raj AJA, Suresh AV, Marimuthu K, Appelbaum S (2008) Probi-
otic performance on fish fry during packing, transportation
stress and post-transportation condition. Journal of Fisheries
and Aquatic Science 3: 152–157.
Ramesh D, Vinothkanna A, Rai AK, Vignesh VS (2015) Isolation
of potential probiotic Bacillus spp. and assessment of their
subcellular components to induce immune responses
in Labeo rohita against Aeromonas hydrophila. Fish & Shellfish
Immunology 45: 268–276.
Ram
ırez C, Romero J (2017) The microbiome of Seriola lalandi
of wild and aquaculture origin reveals differences in composi-
tion and potential function. Frontiers in Microbiology 8: 1844.
Ravi V, Musthafa KS, Jegathammbal G, Kathiresan K, Pandian
SK (2007) Screening and evaluation of probiotics as a biocon-
trol agent against pathogenic Vibrios in marine aquaculture.
Letters in Applied Microbiology 45: 219–223.
Ray AK, Ghosh K, Ringo E (2012) Enzyme-producing bacteria
isolated from fish gut: a review. Aquaculture Nutrition 18:
465–492.
15
M. A. O. Dawood et al.
Rengpipat S, Rukpratanporn S, Piyatiratitivorakul S, Menasaveta
P (2000) Immunity enhancement in black tiger shrimp
(Penaeus monodon) by a probiont bacterium, Bacillus s11.
Aquaculture 191: 271–288.
Ringo E, Lovmo L, Kristiansen M, Bakken Y, Salinas I, Mykle-
bust R et al. (2010) Lactic acid bacteria vs. pathogens in the
gastro-intestine of fish (a review). Aquaculture Research 41:
451–467.
Ringø E, Sperstad S, Myklebust R, Refstie S, Krogdahl  A (2006)
Characterisation of the microbiota associated with intestine of
Atlantic cod (Gadus morhua L.): the effect of fish meal, stan-
dard soybean meal and a bioprocessed soybean meal. Aqua-
culture 261: 829–841.
Rio-Zaragoza OBD, Fajer-Avila EJ, Almazan-Rueda P (2011)
Influence of b-glucan on innate immunity and resistance of
Lutjanus guttatus to an experimental infection of dactylogyrid
monogeneans. Parasite Immunology 33: 483–494.
Robertson PAW, O’Dowd C, Burrells C, Williams P, Austin B
(2000) Use of Carnobacterium sp. as a probiotic for Atlantic
salmon (Salmo salar L.) and rainbow trout (Oncorhynchus
mykiss, Walbaum). Aquaculture 185: 235–243.
Rodriguez-Estrada U, Satoh S, Haga Y, Fushimi H, Sweetman J
(2009) Effects of single and combined supplementation of
Enterococcus faecalis, mannan oligosaccharide and polyhy-
drobutyrate acid on growth performance and immune
response of rainbow trout (Oncorhynchus mykiss). Aquacul-
ture Science 57: 609–617.
Rodriguez-Estrada U, Satoh S, Haga Y, Fushimi H, Sweetman J
(2013) Effects of inactivated Enterococcus faecalis and mannan
oligosaccharide and their combination on growth, immunity,
and disease protection in rainbow trout. North American Jour-
nal of Aquaculture 75: 416–428.
Rottmann RW, Francis-Floyd R, Durborow R (1992) The role of
stress in fish disease. SRAC Publication Number 474.
Saenz de Rodriguez MA, Diaz-Rosales P, Chabrillon M, Smidt
H, Arijo S, Leon-Rubio JM (2009) Effect of dietary adminis-
tration of probiotics on growth and intestine functionally of
juvenile Senegalese sole (Solea senegalensis, Kaup 1858).
Aquaculture Nutrition 15: 177–185.
Sahandi J, Jafaryan H, Roozbehfar R, Babaei S, Dehestani M
(2012) The use of two enrichment forms (Brachionus plicatilis
enrichment and rearing water enrichment) with probiotic
bacilli spore on growth and survival of Silver carp (Hypoph-
thalmichthys molitrix). Iranian Journal of Veterinary Research
13: 289–295.
Salinas I, Cuesta A, Esteban MA,
Meseguer J (2005) Dietary
administration of Lactobacillus delbr€ ueckii and Bacillus subtilis,
single or combined, on gilthead seabream cellular innate
immune responses. Fish & Shellfish Immunology 19(1): 67–77.
Salinas I, D
ıaz-Rosales P, Cuesta A, Meseguer J, Chabrill
on M,
Mori~ nigo MA
et al. (2006) Effect of heat-inactivated fish and
nonfish derived probiotics on the innate immune parameters
of a teleost fish (Sparus aurata L.). Veterinary Immunology
and Immunopathology 111: 279–286.
16
Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D
et al. (2008) Monospecies and multispecies probiotic formu-
lations produce different systemic and local immunostimula-
tory effects in the gilthead seabream (Sparus aurata L.). Fish
& Shellfish Immunology 25: 114–123.
Salminen S, Ouwehand A, Benno Y, Lee YK (1999) Probiotics:
how should they be defined? Trends in Food Science & Tech-
nology 10: 107–110.
Sankar H, Philip B, Philip R, Singh ISB (2017) Effect of probi-
otics on digestive enzyme activities and growth of cichlids,
Etroplus suratensis (Pearl spot) and Oreochromis mossambicus
(Tilapia). Aquaculture Nutrition 23: 852–864.
Selye H (1985) Stress: eustress, distress and human perspectives.
In: Day S (ed) Life Stress, Vol III. Van Nostrand Reinhold,
Cincinnati, OH.
Shabanzadeh S, Shapoori M, Sheikhzadeh N, Nofouzi K, Oush-
ani AK, Enferadi MHN et al. (2016) Growth performance,
intestinal histology, and biochemical parameters of rainbow
trout (Oncorhynchus mykiss) in response to dietary inclusion
of heat-killed Gordonia bronchialis. Fish Physiology and Bio-
chemistry 42(1): 65–71.
Shamsuzzaman MM, Biswas TK (2012) Aqua chemicals in
shrimp farm: a study from south-west coast of Bangladesh.
The Egyptian Journal of Aquatic Research 38: 275–285.
Shan S, Xiao Z, Huang W, Dou S (2008) Effect of photoperiod
on growth, mortality and digestive enzymes in miiuy croaker
larvae and juveniles. Aquaculture 281: 70–76.
Sharma P, Ram C, Sihag CR, Gahlawat SK (2013) Relative effi-
cacy of two probiotics in controlling the Epizootic Ulcerative
Syndrome disease in Mrigal (Cirrhinus mrigala Ham). Journal
of Fisheries and Aquatic Science 8: 305–322.
Sihag RC, Sharma P (2012) Probiotics: the new ecofriendly alter-
native measures of disease control for sustainable aquaculture.
Journal of Fisheries and Aquatic Science 7: 72–103.
Song Z, Wu T, Cai L, Zhang L, Zheng X (2006) Effects of dietary
supplementation with Clostridium butyricum on the growth
performance and humoral immune response in Miichtys
miiuy. Journal of Zhejiang University Science B 7: 596–602.
Song SK, Beck BR, Kim D, Park J, Kim J, Kim HD et al. (2014)
Prebiotics as immunostimulants in aquaculture: a review. Fish
& Shellfish Immunology 40(1): 40–48.
Sorroza L, Padilla D, Acosta F, Roman L, Grasso V, Vega J et al.
(2012) Characterization of the probiotic strain Vagococcus flu-
vialis in the protection of European sea bass (Dicentrarchus
labrax) against vibriosis by Vibrio anguillarum. Veterinary
Microbiology 155: 369–373.
Suzer C, C ß oban D, Kamaci HO, Saka Sß, Firat K, Otgucuoglu O €
et al. (2008) Lactobacillus spp. bacteria as probiotics in gilt-
head sea bream (Sparus aurata, L.) larvae: effects on growth
performance and digestive enzyme activities. Aquaculture 280
(1): 140–145.
Tal Y, Schreier HJ, Sowers KR, Stubblefield JD, Place AR, Zohar
Y (2009) Environmentally sustainable land-based marine
aquaculture. Aquaculture 286(1): 28–35.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd

Talpur AD, Memon AJ, Khan MI, Ikhwanuddin M, Abdullah
MDD, Bolong AMA (2013) Gut Lactobacillus sp. bacteria as
probiotics for Portunus pelagicus (Linnaeus, 1758) larvicul-
ture: effects on survival, digestive enzyme activities and water
quality. Invertebrate Reproduction & Development 57: 173–
184.
Taoka Y, Maeda H, Jo JY, Jeon M-J, Bai SC, Lee WJ et al. (2006a)
Growth, stress tolerance and non-specific immune response of
Japanese flounder Paralichthys olivaceus to probiotics in a
closed recirculating system. Fisheries Science 72: 310–321.
Taoka Y, Maeda H, Jo JY, Kim SM, Park SI, Yoshikawa T et al.
(2006b) Use of live and dead probiotic cells in tilapia Ore-
ochromis niloticus. Fisheries Science, 72: 755–766.
Taoka Y, Maeda H, Jo JY, Sakata T (2007) Influence of commer-
cial probiotics on the digestive enzyme activities of Tilapia,
Oreochromis niloticus. Aquaculture Science, 55: 183–189.
Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intesti-
nal microbiome: diversity and symbiosis unravelled by
metagenomics. Journal of Applied Microbiology 123: 2–17.
Telli GS, Ranzani-Paiva MJT, De Carla Dias D, Sussel FR, Ishi-
kawa CM, Tachibana L (2014) Dietary administration of
Bacillus subtilis on hematology and non-specific immunity of
Nile tilapia Oreochromis niloticus raised at different stocking
densities. Fish & Shellfish Immunology 39: 305–311.
Thomas C, Versalovic J (2010) Probiotics-host communication:
modulation of signaling pathways in the intestine. Gut
Microbes 1(3): 1–16.
Timmerman HM, Koning CJM, Mulder L, Rombouts FM, Bey-
nen AC (2004) Monostrain, multistrain and multispecies pro-
biotics—a comparison of functionality and efficacy.
International Journal of Food Microbiology 96: 219–233.
Tovar-Ramirez D, Zambonino J, Cahu C, Gatesoupe FJ, Vaz-
quez-Juarez R, Lesel R (2002) Effect of live yeast incorpora-
tion in compound diet on digestive enzyme activity in
sea bass (Dicentrarchus labrax) larvae. Aquaculture 204: 113–
123.
Tovar-Ramirez D, Mazurais D, Gatesoupe JF, Quazuguel P,
Cahu CL, Zambonino-Infante JL (2010) Dietary probiotic live
yeast modulates antioxidant enzyme activities and gene
expression of sea bass (Dicentrarchus labrax) larvae. Aquacul-
ture 300(1–4): 142–147.
Turnbull J, Bell A, Adams C, Bron J, Huntingford F (2005)
Stocking density and welfare of cage farmed Atlantic salmon:
application of a multivariate analysis. Aquaculture 243: 121–
132.
Van Doan H, Hoseinifar SH, Dawood MA, Chitmanat C, Tayya-
math K (2017) Effects of Cordyceps militaris spent mushroom
substrate and Lactobacillus plantarum on mucosal, serum
immunology and growth performance of Nile tilapia (Ore-
ochromis niloticus). Fish & Shellfish Immunology 70: 87–94.
Van Hai N (2015) Research findings from the use of probiotics
in tilapia aquaculture: a review. Fish & Shellfish Immunology
45(2): 592–597.
Varela JL, Ruiz-Jarabo I, Vargas-Chacoff L, Arijo S, Leon-Rubio
JM, Garcia-Millan I et al. (2010) Dietary administration of
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd
Probiotics for sustainable aquaculture
probiotic of probiotic Pdp 11 promotes growth and improves
stress tolerance to high stocking density in gilthead
seabream Sparus auratus. Aquaculture 309: 265–271.
Venkateswara AR (2007) Bioremediation to restore the health of
aquaculture. Pond Ecosystem Hyderabad 500 082, India, pp.
1–12.
Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000)
Probiotic bacteria as biological control agents in aquaculture.
Microbiology and Molecular Biology Reviews 64: 651–671.
Vijayabaskar P, Somasundaram ST (2008) Isolation of bacteri-
ocin producing lactic acid bacteria from fish gut and probiotic
activity against common fresh water fish pathogen Aeromonas
hydrophila. Biotechnology 7: 124–128.
Vijayan KK, Bright Singh IS, Jayaprakash NS, Alavandi SV, Som-
nath Pai S, Preetha R et al. (2006) A brackishwater isolate of
Pseudomonas PS-102, a potential antagonistic bacterium
against pathogenic Vibrios in penaeid and non-penaeid rear-
ing systems. Aquaculture 251: 192–200.
Villamil L, Tafalla C, Figueras A, Novoa B (2002) Evaluation of
immunomodulatory effects of lactic acid bacteria in turbot
(Scophhalmus Maximus). Journal of Clinical and Diagnostic
Laboratory Immunology 9: 1318–1323.
Wabete N, Chim L, Lemaire P, Massabuau JC (2008) Life on the
edge: physiological problems in penaeid prawns Litopenaeus
stylirostris, living on the low side of their thermopreferendum.
Marine Biology 154: 403–412.
Wach
e Y, Auffray F, Gatesoupe FJ, Zambonino J, Gayet V,
Labb
e L et al. (2006) Cross effects of the strain of dietary
Saccharomyces cerevisiae and rearing conditions on the
onset of intestinal microbiota and digestive enzymes in rain-
bow trout, Onchorhynchus mykiss, fry. Aquaculture 258(1):
470–478.
Wang YB (2007) Effect of probiotics on growth performance
and digestive enzyme activity of the shrimp Penaeus van-
namei. Aquaculture 269(1): 259–264.
Wang YB, Xu ZR, Xia MS (2005) The effectiveness of commer-
cial probiotics in northern white shrimp (Penaeus vannamei)
ponds. Fisheries Science 71: 1036–1041.
Wang YB, Tian ZQ, Yao JT, Li WF (2008) Effect of probiotics,
Enteroccus faecium, on tilapia (Oreochromis niloticus)
growth performance and immune response. Aquaculture 277:
203–207.
Wang JH, Zhao LQ, Liu JF, Wang H, Xiao S (2015) Effect of
potential probiotic Rhodotorula benthica D30 on the growth
performance, digestive enzyme activity and immunity in juve-
nile sea cucumber Apostichopus japonicus. Fish & Shellfish
Immunology 43: 330–336.
Wang W, Ishikawa M, Koshio S, Yokoyama S, Dawood MAO,
Zhang Y (2018) Effects of dietary astaxanthin supplementa-
tion on survival, growth and stress resistance in larval and
post-larval kuruma shrimp, Marsupenaeus japonicus. Aquacul-
ture Research 49: 2225–2232.
Wong S, Rawls JF (2012) Intestinal microbiota composition in
fishes is influenced by host ecology and environment. Molecu-
lar Ecology. 21: 3100–3102.
17
M. A. O. Dawood et al.
Yan I, Boyd KG, Burgess JG (2002) Surface attachment induced
production of antimicrobial compounds by marine epiphytic
bacteria using modified roller bottle cultivation. Marine
Biotechnology 4: 356–366.
Yan J, Li Y, Liang X, Zhang Y, Dawood MA, Matuli’c D et al.
(2017a) Effects of dietary protein and lipid levels on growth
performance, fatty acid composition and antioxidant-related
gene expressions in juvenile loach Misgurnus anguillicaudatus.
Aquaculture Research, 48: 5385–5393.
Yan J, Guo C, Dawood MAO, Gao J (2017b) Effects of dietary
chitosan on growth, lipid metabolism, immune response and
antioxidant-related gene expression in Misgurnus anguillicau-
datus. Beneficial Microbes 8: 439–449.
Yanbo W, Zirong X (2006) Effect of probiotics for common carp
(Cyprinus carpio) based on growth performance and digestive
enzyme activities. Animal Feed Science and Technology 127:
283–292.
Ye JD, Wang K, Li FD, Sun YZ (2011) Single or combined effects
of fructo- and mannan oligosaccharide supplements and
Bacillus clausii on the growth, feed utilization, body composi-
tion, digestive enzyme activity, innate immune response and
lipid metabolism of the Japanese flounder (Paralichthys oli-
vaceus). Aquaculture Nutrition 17: 902–911.
Ying C, Lei W, Jiazhong L, Zhantao S, Liguo A (2007)
Identification and purification of a novel adhesion-asso-
ciated protein in a new strain of Lactobacillus, L15, from
flounder Paralichthys olivaceus. Veterinary Microbiology
122: 116–122.
18
Zaineldin AI, Hegazi S, Koshio S, Ishikawa M, Bakr A, El-Keredy
AM et al. (2018) Bacillus subtilis as probiotic candidate for red
sea bream: growth performance, oxidative status, and immune
response traits. Fish & Shellfish Immunology 79: 303–312.
Zenteno-Sav
ın T, Saldierna R, Ahuejote-Sandoval M (2006)
Superoxide radical production in response to environmental
hypoxia in cultured shrimp. Comparative Biochemistry and
Physiology Part C: Toxicology & Pharmacology 142: 301–308.
Zhou XX, Wang YB, Li WF (2009) Effect of probiotic on larvae
shrimp (Penaeus vannamei) based on water quality, survival
rate and digestive enzyme activities. Aquaculture 287: 349–
353.
Ziaei-Nejad S, Rezaei MH, Takami GA, Lovett DL, Mirvaghefi
AR, Shakouri M (2006) The effect of Bacillus spp. bacteria
used as probiotics on digestive enzyme activity, survival and
growth in the Indian white shrimp Fenneropenaeus indicus.
Aquaculture 252: 516–524.
Zokaeifar H, Balc
azar JL, Saad CR, Kamarudin MS, Sijam K,
Arshad A et al. (2012) Effects of Bacillus subtilis on the growth
performance, digestive enzymes, immune gene expression and
disease resistance of white shrimp, Litopenaeus vannamei. Fish
& Shellfish Immunology 33: 683–689.
Zorriehzahra MJ, Delshad ST, Adel M, Tiwari R, Karthik K,
Dhama K et al. (2016) Probiotics as beneficial microbes in
aquaculture: an update on their multiple modes of action: a
review. Veterinary Quarterly 36: 228–241.
Reviews in Aquaculture, 1–18
© 2018 Wiley Publishing Asia Pty Ltd