Fish and Shellfish Immunology 114 (2021) 263–281

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Fish and Shellfish Immunology

journal homepage: www.elsevier.com/locate/fsi

Overview of the latest developments in the role of probiotics, prebiotics and

synbiotics in shrimp aquaculture
Usman Dawood Butt a, Na Lin b, Najeeb Akhter c, Tooba Siddiqui d, Sihui Li a, Bin Wu a, *
a
Ocean College, Zhejiang University, Zhoushan, 316021, China
b
Lishui Hospital of Traditional Chinese Medicine, Lishui, 323000, China
c
Centre of Excellence in Marine Biology, University of Karachi, Karachi, 75270, Pakistan
d
Institute of Marine Science, University of Karachi, Karachi, 75270, Pakistan

A R T I C L E I N F O A B S T R A C T

Keywords: With the growing world population, the demand for food has increased, leading to excessive and intensive
Probiotics breeding and cultivation of fisheries, simultaneously exacerbating the risk of disease. Recently, shrimp producers
Prebiotics have faced major losses of stocks due to the prevalence of periodical diseases and inappropriate use of antibiotics
Synbiotics
for disease prevention and treatment, leading to bacterial resistance in shrimp, along with imposing health
Shrimp aquaculture
Litopenaeus vannamei
hazards on human consumers. Strict regulations have been placed to ban or reduce the use of prophylactic
antibiotics to lessen their detrimental effects on aquatic life. Dietary and water supplements have been used as
substitutes, among which probiotics, prebiotics, and synbiotics have been the most beneficial for controlling or
treating bacterial, viral, and parasitic diseases in shrimp. The present analysis addresses the issues and current
progress in the administration of pro-, pre-, and synbiotics as disease controlling agents in the field of shrimp
farming. Furthermore, the benefits of pro-, pre-, and synbiotics and their mechanism of action have been
identified such as; strengthening of immune responses, growth of antibacterial agents, alteration in gut micro­
flora, competition for nutrients and binding sites, and enzymes related activities. Overall, this study aims to
depict the antagonistic action of these supplements against a variety of pathogens and their mode of action to
counter diseases and benefit shrimp species.

1. Introduction human food consumption, and it is expected to reach 109 mt by 2030. A

It is believed that aquaculture initially started in China and has now
become one of the fastest-growing sectors of the animal-based food
supply in the world [1]. Due to the increased demand for food from
marine and freshwater resources, aquaculture has emerged as an alter­
native source of nourishment and nutrition. Its usage in raising marine
and freshwater crustaceans in a culturally and artificially controlled
environment, has not only helped to meet the demand for consumption
but also to compensate for the scarce resources. According to the United
Nations Food and Agricultural Organization (FAO), most of the
economically and commercially important fish (including shrimp)
stocks have been destroyed or overfished and as a result, are either
extinct or on the verge of collapse [2]. In contrast, the global production
of aquaculture reached around 82.1 mt in 2018, accounting for 46% of
the world’s overall fish (including shrimp) production and 52% of
rise of 32% is estimated, reaching to 26 mt over 2018 [3]. The increase
in shrimp aquaculture practices in the last few decades is due to the
rising demand and shrimp’s nutritional quality (see Table 1). According
to the latest survey by the Boston Consulting Group (BCG) in 2019,
global production of shrimp has tripled in less than two decades, and
cultivated shrimp is listed as one of the fastest-growing foods in the
world [4]. It is estimated that global farmed shrimp production reached
4.455 mt in 2019, rising to about 17% compared to 2018 [5]. However,
the latest pandemic, Coronavirus (COVID-19) has hindered global
development and prospects, which has led to a decreased demand for
shrimp, shortage of labour, and suspension of trade between countries;
increasing the likelihood that the economy will struggle in the near
future [5].
Since aquatic species interact closely with the surrounding envi­
ronment, aquaculture microbiomes have a direct impact on their health

* Corresponding author.
E-mail addresses: usman_butt@zju.edu.cn (U.D. Butt), 854954086@qq.com (N. Lin), na_memon@marinebiology.edu.pk (N. Akhter), toobasiddiqui202@gmail.
com (T. Siddiqui), 21934038@zju.edu.cn (S. Li), wubin@zju.edu.cn (B. Wu).

https://doi.org/10.1016/j.fsi.2021.05.003
Received 17 January 2021; Received in revised form 4 April 2021; Accepted 3 May 2021
Available online 8 May 2021
1050-4648/© 2021 Elsevier Ltd. All rights reserved.
U.D. Butt et al.
Table 1
Nutritional value of shrimp [213].
NUTRITIONAL VALUE
Amount Per 100g Serving
Total Calories 118 .8 (15.3 From Fat)
DV % *
Total Fat 1.6g 3%
Saturated Fat 0.5g 3%
Cholesterol 210.6 mg 70%
Sodium 947.2 mg 29%
Potassium 170.6 mg 5%
Total Carbohydrates 1.5g 1%
Proteins 22.4g
Vitamin A 6%
Calcium 9.1%
Iron 1.8%
* DV = Daily Value.
* Daily Values % is Based on 2000 Calorie Diet.
and development. Therefore, investigating the microbial fauna of
aquatic species and their surroundings is important [6]. As shrimp are
closely interdependent on their environment, any changes can lead to
various types of viral and bacterial diseases. Therefore centralized,
intensive, and rigorous management is needed to conserve shrimp
stocks. Due to their proven beneficial effect, the use of probiotics, pre­
biotics, and synbiotics in aquaculture has now become a popular prac­
tice [7–17]. Recently, various evaluations of professional pro-, pre-, and
synbiotics have been carried out in shrimp aquaculture, namely for the
activation of innate, humoral, and cell-mediated immunity, as dietary
and nutritional supplements, environmental capacity builder agents,
growth promoters, and prophylactic against infectious diseases. These
supplements also directly induce artificial immune responses, including
activating phagocytes, stimulating neutrophils, activating alternative
regeneration systems, and enhancing lysosomal activity.
However, some studies have raised concerns about the continuous
and inappropriate use of pro-, pre-, and synbiotics, as they may lead to
changes in the bacterial composition of the culture system and the
naturally protected flora of the cultured species. This increases the host
animal’s vulnerability to opportunistic pathogens and reduces the feed
conversion rate due to the disruption of the GIT microflora [13]. Thus,
developing an experimental test for identifying and checking strain
mechanisms, a clear understanding of the professional pro-, pre-, and
synbiotic-based products and studies about the efficiency of these
products to weigh their strengths or weaknesses is vital. By far, an
insufficient amount of studies has been conducted to examine the
effectiveness of pro, pre, and synbiotics in shrimp farming, rendering the
existing data inadequate for analysis. Thus, this review emphasizes the
importance of identifying the benefits and limitations of such in­
terventions. It also briefly summarizes the current evidence on the main
uses of pro-, pre-, and synbiotic in shrimp aquaculture. It describes and
focuses on the most significant characteristics that have been proven and
disclosed to date.
1.1. Probiotics
Probiotic is a Greek term, where pro means benefit, and bios means
life [18]. It is a bacteria-based product in which essential bacteria is used
to promote health, prevent multiple diseases and pathogenic growth in
aquaculture. The use of non-pathogenic bacteria can also improve di­
etary safety and environmental performance, which can control allergies
and improve the immune system by altering host-related microorgan­
isms [19–21]. Several gram-positive and gram-negative bacterial can­
didates such as Bacillus species [22–28], Vibrio species [29–31], lactic
acid bacteria [32], and some other bacterial species [13,33–35] have
been used as probiotics in shrimp aquaculture in recent times.
Probiotics are mainly focused on energy production, immune
response, and the production of inhibitory compounds which impairs
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Fish and Shellfish Immunology 114 (2021) 263–281
the action of cortical sensing in pathogens [36]. At present, there is
evidence that probiotics can not only enhance the absorption of nutri­
ents and increase stress resistance but also enhance the fertility of the
host species [37]. According to Llewellyn et al. [38] probiotics can also
be added to the culture system to improve water quality and to monitor
infectious diseases caused by bacteria (Fig. 1). For example, a variety of
bacteria, phages, microalgae, and yeast are conventionally used in
aquaculture or feed supplements. Probiotics can improve immunity and
survival rate, produce digestive enzymes and reduce disease occurrence
(Fig. 1) [39,40]. There are several prototypes commercially available in
mono or multi-stains [41]. However, the development phase of com­
mercial probiotic-based feed requires rigorous experiments, formation
of suitable observatory tools, and controlled manufacturing [25,42].
1.2. Prebiotics
The concept of prebiotics was first introduced by Gibson and
Roberfroid who defined it as “an indigestible fibre that can enhance the
growth and activity of health-promoting bacteria in the intestine and
beneficially affect the host” [43]. Similarly, Bindels et al. [44] described
prebiotics as “non-digestible food ingredients that are broken down into
simpler substances, enhancing the growth and activity of preferred mi­
croorganisms found in the gastrointestinal tract and benefiting the
health of the host”. Guerreiro et al. [45] presented them as “useful food
ingredients that have numerous favourable effects on the host”.
Recently, the application of antibiotics in aquaculture has been
widely criticized, due to the growth of antibiotic-resistant strains, the
emergence of antibiotic residues in the host, changes in the microbial
population of the gut and the culture system, and reduced immunity
[46–49]. Probiotics may not survive or grow during the production,
preserving and pelleting process of the probiotic-based feed. The feed, if
prepared under inappropriate and adverse conditions may reduce its
efficiency (Fig. 1) [50]. Thus, prebiotics have been recently adopted as
an alternative to antibiotics and probiotics. Several analyses and com­
ments have been published emphasizing the beneficial effect of pre­
biotics in aquaculture [45,51–54]. Inulin, fructooligosaccharides (FOS),
short-chain fructooligosaccharides (scFOS), mannan oligosaccharides
(MOS), galactooligosaccharides (GOS), xylooligosaccharides (XOS),
arabinoxylooligosaccharides (AXOS), isomaltooligosaccharides (IMO),
and GroBiotic-A, which are usually derived from plants and fibres, are
commonly recognized prebiotics in shrimp farming [55–57]. Some
carbohydrates are also classified as prebiotics on the degree of their
polymerization into monosaccharides, oligosaccharides, and poly­
saccharides [58].
Prebiotics possess the ability to be metabolized by beneficial bacte­
ria, Lactobacillus and Bifidobacterium, producing short-chain fatty acids
(SCFAs) and lactate [58]. SCFAs can be absorbed through the intestinal
tract to act as a source of energy while lactate acts as a stimulant for
gluconeogenesis [59]. The production of SCFAs helps to reduce the pH
of the colon, which prevents the proliferation of pathogens and enhances
the growth of Bifidobacterium and other lactic acid-type bacterial species
[17]. Similarly, the administration of prebiotics promotes the growth of
beneficial bacteria and reduces the number of pathogenic bacteria by
competing with glycoconjugates on the epithelial lining, resulting in
mucus production, increased SCFAs and cytokines [50,60]. They posi­
tively affect the growth parameters of the host, such as final weight,
weight gain, daily weight gain, specific growth rate, dietary conversion
ratio, feed efficiency ratio, and protein efficiency ratio [61–64].
A diet supplemented with prebiotics can also increase digestive
enzyme activity (Fig. 1) [62,65]. Increased levels of digestive enzymes
associated with weight gain and effective feed conversion efficiency
were reported [62], but consistent improvements were not observed as
some studies also reported ineffective behaviour of prebiotics [54,65,
66]. Prebiotics can further enhance immunity [61,66] by activating the
non-specific immune system and promoting beneficial bacterial health
[67]. The beneficial microbiota provides protection against harmful
U.D. Butt et al. Fish and Shellfish Immunology 114 (2021) 263–281

Fig. 1. Constraints and potentials of probiotics, prebiotics and synbiotics in shrimp aquaculture.

bacteria present in the colon, and improves the host’s immunity, and
also provides a clear balance between the gastrointestinal and immune
system’s microbiota [68]. Prebiotic candidates must fulfill the following
criteria by both in vivo and in vitro experiments to be considered as po­
tential prebiotics: (i) they must be resistant to gastric/abdominal acidity
(ii) initiate various enzymatic processes and effects (iii) enhance
gastrointestinal digestion (iv) support microbial fermentation (v) stim­
ulate the activity of desirable microbes that can confer health benefits
[44,69]. However, not all prebiotics have these specifications [50].
various shrimp species [15,80–82]. Their effectiveness in shrimp aqua­
culture is further demonstrated by increased stimulation of host species’
growth and survival [83]. This occurs via the secretion of pancreatic
enzymes which leads to improvement in enzymatic digestion, modula­
tion in intestinal microflora, reduced rate of mortality by changing the
potential immune responses, and antagonism to pathogenic species
(Fig. 1) [82,84–86].
2. Modes of application

1.3. Synbiotics Probiotics can be classified into several types depending on their
application;
The term synbiotic is a combination of two Greek words "συν" and
"βíoς", meaning “joint or together” and “life” respectively [70]. The term
synbiotics denotes a dietary supplement that includes both prebiotics
and probiotics in a synergistic relationship. A nutrient that helps pro­
mote the growth and survival of probiotics in the gastrointestinal tract of
the host species by altering the opportunistic bacterial community [71,
72]. The choice of prebiotics for the formulation of synbiotic is based on
their ability to indirectly promote the growth and survival of beneficial
bacteria within their target range. Probiotics are chosen based on their
specific beneficial effects on the host. However, the choice of prebiotics,
as per its synergistic effects, is based on their ability to enhance the
growth of probiotic bacteria as its primary function, while the choice of
probiotics as per its synergistic effects is based on their overall benefits
on the host correspondingly [70]. Most recent studies have focused and
emphasized solely on the synergistic effects of synbiotics [73–75].
The composition of synbiotics depends mainly on the mechanism of
action of prebiotics in the host species [76]. However, prebiotic with
low-degree-of-polymerization is better suited for the development of
synbiotics than the ones with higher-degree-of-polymerization [77], as
they hydrolyze the grown beneficial strains and produce primary and
secondary metabolites that may have beneficial effects on the host [76].
Additionally, the administration of synbiotics has been proven to be
more effective than the use of probiotics alone [78], as better survival of
probiotics has been observed when used in combination with prebiotics
and vice versa. Prebiotics, however, provide better resistance to signif­
icant changes in oxygen, temperature, and pH levels [79]. The following
studies have reported synbiotic effectiveness as a positive alternative to Fig. 2. Common viral diseases in shrimp.

265
U.D. Butt et al.
a) Probiotics that are collected from the gut and can be orally admin­
istered in combination with feed to improve the beneficial microflora
of the intestine [87].
b) Those that are administered as water additives and can grow in the
water medium by absorbing all the ingestible food thus, resulting in
starving of pathogenic bacteria due to malnutrition [88].
c) Which can be administered through micro-encapsulation, and have a
direct and positive impact on water quality, physical parameters, and
shrimp health [26].
d) In the form of living cells [30].
e) Those that can be administered via probiotic-rich Artemia or micro­
algae and can promote growth and survival during the nursing phase
[28].
However, prebiotics are a popular set of alternative disease man­
agement strategies that promote non-specific immune responses. There
are several varieties of prebiotics, depending on their application. For
example.
a) Supplementing an aquatic diet with prebiotics can increase glucose
uptake [89], and bioavailability of trace elements [90].
b) Prebiotics when used as a water additive for a specific time period,
stimulate immune responses and enhance resistance against diseases
[91].
c) Bio-encapsulation of Artemia species with prebiotics provided
appropriate size for consumption, high nutritional value, and pro­
moted larval growth [80].
Fig. 3. Expected pond condition with and without probiotic treatment.
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Fish and Shellfish Immunology 114 (2021) 263–281
d) Raw addition of prebiotic-rich Artemia nauplii increased shrimp
larval and post-larval survival [92].
Similarly, synbiotics also have several forms depending on their
applications;
a) The incorporation of synbiotics in the diet results in better growth
[93], strengthened immune responses, and resistance against disease
[74,94].
b) Bio-encapsulation of Artemia species with synbiotics not only pro­
mote growth but also provide optimal size and nutrients to growing
larvae of shrimp [80].
c) Micro-encapsulation of synbiotics can support the survival and
growth of probiotics bacteria [95] and promote the growth of in­
testinal microflora [96].
3. Mechanism of action
Shrimp are vulnerable to various viral and bacterial epizootics [97].
Several infections and diseases have dominated shrimp farming in
recent years (Fig. 2) [98–100]. The periodical damage may result in
widespread mortality and huge economic losses. It is estimated that
shrimp disease outbreaks result in global losses of approximately 3
billion US dollars [101]. The development of new techniques and
methods was inevitable. Thus, pro-, pre-, and synbiotics were produced
and effectively used in shrimp aquaculture.
Some mechanisms have been proposed as the mode of action of
U.D. Butt et al.
probiotics in recent years but the pathways of their activities in aqua­
culture are not well known. According to some hypotheses, stimulation
or regulation of immunity, enhancement of growth and tolerance,
antagonism against pathogens, and alteration in gut microflora are the
key mechanisms by which probiotics exert their effects. Several other
mechanisms of probiotics are also observed during in vitro and in vivo
experiments such as production of inhibitory compounds, competition
for adhesion sites, Iron (Fe) and nutrients (as well as nutrient source
themselves), increased enzymatic activities (such as contribution to
digestion), bioremediation of accumulated ammonia, nitrite and other
organic material from the culture system and pond bottom through
bacterial mediation (Fig. 3), and antiviral activities [23,26,87,102].
Recently, numerous articles and reviews on the use of prebiotics in
shrimp farming have been published [103–106]. Prebiotics’ mechanism
of action observed in various shrimp species includes increased sus­
tainability against disease [107,108], stimulation and modulation of
immunity [80,109,110], enhancement, modulation, and alteration of
intestinal microbiota [109,111,112], improvement in growth and sur­
vival of host species [113–115], antioxidant activity [61,115] and
beneficial changes in enzyme activity [114,115]. Moreover, the use of
prebiotics enhances the activity of amylase and hydrolysis of carbohy­
drates in shrimps [116]. It facilitates and promotes the growth of
beneficial bacteria such as Bifidobacterium and Lactobacillus species
[117].
During the past decades, the role of pro-, and prebiotics in shrimp
aquaculture have been studied separately, while the concept of syn­
biotics emerged recently. They flourished after their first use in 2009
[118]. Synbiotics have demonstrated several mechanisms of action since
their application on shrimps. According to Boonanuntanasarn et al.
[119], synbiotics can provide greater yields and better sustainability in
shrimp aquaculture. Litopenaeus vannamei when administered with
probiotic Bacillus OJ and isomalto-oligosaccharide as a feed additive,
resulted in significant effects on gastrointestinal microbes and antago­
nism against White Spot Syndrome Virus (WSSV) [120]. Synbiotics
improved the efficiency of growth-enhancing probiotic bacteria in
cultured shrimp [121]. They can also proliferate immune parameters
such as lysozyme activity, production of hemocytes, respiratory burst
activity, phenoloxidase activity, superoxide dismutase activity, and in­
crease competitiveness against bacterial and viral infections [122].
Moreover, better digestive enzyme activities in shrimp gut have been
observed which resulted in improved growth [123]. Recently, the syn­
biotics and probiotics in combination with plant products or yeast/β-­
glucan are used in aquaculture and demonstrated potential benefits on
gut microbiota and gut morphology, and mucosal immune responses
[124].
3.1. Immune modulation and disease resistance
Recently, several studies have illustrated the key functions and ef­
ficacy of probiotics as immunostimulants (see Table 2) [13,51,125,126].
The major mechanism of probiotics as an immunostimulant is to stim­
ulate phagocytosis, an inflammatory response before antibody produc­
tion and antibacterial activity in the host [127,128]. In particular,
probiotics can effectively modulate the growth of anti-inflammatory
cytokines such as IL-10 and Transforming Growth Factor b (TGF-b)
and pro-inflammatory cytokines such as interleukin-1 (IL-1), IL-6, IL-12,
and tumour necrosis factor-a (TNF-a) in several life forms [129]. Like­
wise, Kim and Austin [130] reported the impact of probiotic isolates
from rainbow trout on cytokine mRNA expression in head kidney leu­
cocytes and gut cells. These gut leukocyte isolates demonstrated
phagocytosis and secretion of bactericidal oxygen free radicals [131].
The same isolates from the head kidney when used as a feed supplement
demonstrated enhanced immune function, such as phagocytosis by
neutrophils and macrophages [132], as enhancement of host immunity
is one important benefit of probiotics when implied as dietary additives
[133].
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Fish and Shellfish Immunology 114 (2021) 263–281
Several Bacillus probiotic species are known for enhancing the host’s
innate and adaptive immunity by immunostimulatory effects and stim­
ulation of beneficial gut microflora [124,134]. Bacillus subtilis, Bacillus
licheniformis, Bacillus coagulans, Bacillus pumilus, Bacillus amyloliquefa­
ciens, Bacillus velezensis and Bacillus megaterium are the most used Ba­
cillus species in shrimp cultures [27,32,135]. The combination of Bacillus
and Vibrio spp. Enhanced the resistance of Litopenaeus vannamei to Vibrio
harveyi and WSSV [136]. Chiu et al. [127] recorded an increase in
transcription of peroxinectin (PE) and prophenoloxidase (proPO) mRNA
as immune profiling factors in white shrimp supplemented with Lacto­
bacillus plantarum. Besides, an increase in activities of superoxide dis­
mutase (SOD), phenoloxidase (PO), respiratory burst, and the removal
efficiency of Vibrio alginolyticus has also been observed.
These beneficial microbes can further enhance the immunity of
shrimp significantly by both in vivo and in vitro; for instance, 58%
average increase in the survival rate of shrimp Penaeus orientalis (Post
Larvae) in the pond, while 21% on average in control and remarkable
reduction in hazardous pathogens in shrimp ponds has been observed as
compared to the control [137,138]. Rengpipat et al. [139] mentioned
the use of three different approaches for the welfare of shrimp; a) by
using disease-resistant shrimp b) by vaccinating or immunostimulation
and, c) by using probiotic strains for immunity improvement and
exclusion of pathogenic bacteria. However, vaccination or immunosti­
mulation might not result in effective protection against disease-causing
bacterium [140] due to uncertain immune responses in shrimp [141].
The probiotic treatment has been proven to be broadly effective in
disease resistance by improving serological immunity and competitive
exclusion in the shrimp’s gut. The modulation of humoral immune re­
sponses and expression of immune-related genes in probiotic-treated
shrimps by stimulation of innate immunity was observed [40]. Dietary
supplementation of selected probiotics is also reported to enhance
cellular and humoral parameters [142], especially Bacillus species re­
flected as disease-resistant [135]. The use of Bacillus S11 strain
strengthens the immunity of tiger shrimp [139]. Serum immune stipu­
lations such as lysozyme, peroxidase, superoxide dismutase (SOD),
protease and antiprotease, catalase (CAT), and myeloperoxidase (MPO)
have shown vigorous antibacterial activity against infectious microbes
[133], and increased immune response in the host species [143]. As
compared to serum, few studies emphasized probiotic’s role as mucosal
immunomodulator [144]. Mucus plays an important role in protection
against infectious agents [145] and probiotics interact with
mucosa-associated lymphoid tissues to help strengthen the defence
against infections [68]. Several Bacillus species are also identified as
mucosal immunomodulators [144,146].
The ability of species to resist certain bacterial and viral loads de­
pends on their antagonism capacity triggered by genetic makeup as well
as certain immune parameters [147]. Shrimps normally possess
non-specific immune genes which exert defensive responses against
pathogenic strains [148] such as recognition, phagocytosis, melaniza­
tion, cytotoxicity, and cell to cell communication in hemocytes [149].
Several articles reported the efficiency of prebiotics as immunostimu­
lator/modulator in aquaculture (see Table 3) [53,54,150]. A diet sup­
plemented with Bio-Mos® and β-1,3-D-glucan, promoted growth and
survival of Penaeus latisulcatus and increased the efficiency of immune
parameters [151]. The use of xylooligosaccharides in shrimp, promotes
growth factors [152], the feed conversion ratio (FCR), protection against
disease and potential immune responses [153]. The immunostimulatory
function of prebiotics is to interact with pattern recognition (PR) mol­
ecules such as β-glucan and dectin-1 receptors present on macrophages
and to activate signalling molecules such as NF-kB, which enhances the
ability of immune cells [154,155]. The saccharides may also interact
with the Microbe-Associated Molecular Patterns (MAMPs) such as tei­
choic acid, peptidoglycan, glycosylated proteins, and bacterial capsule
polysaccharides to stimulate the immune response [156]. Growth
stimulation of anaerobic bacteria specifically Bifidobacterium, preven­
tion of opportunistic/pathogenic adhesion, reduction in pH of the colon
U.D. Butt et al. Fish and Shellfish Immunology 114 (2021) 263–281

Table 2
Probiotics evaluated for shrimp aquaculture applications.
Probiotic Strains Source Targeted Mode of Application Concentration and Responses References
Species Duration

a. Gram-Positive Bacteria
Arthrobacter XE-7 Isolated from the L. vannamei Feed Additive 1010 CFU g− 1
feed for 63 Modulates the intestinal [214]
culture water of (Pacific white days microflora, enhanced the
Pacific white shrimp) immune parameters,
Shrimp. significantly decreased
mortalities to
V. parahaemolyticus
Arthrobacter MCCB 104 Isolated from P. monodon Water Additive 106 CFU mL − 1
No Significant activity against [34]
seawater hatchery (Larvae) V. harveyi, enhanced SR as well
as functioned as probiotics
through immunostimulatory
and digestive enzyme-
supporting modes of action.
Probiotic B. thuringiensis Isolated from White Shrimp Water Additive (As a 109 CFU mL − 1 daily3–4 Effectively improves GR, SR, [26]
A BUU 001 P. monodon intestine (Post Larvae) freeze-dried Bacillus or nauplii per shrimp beneficial bacteria, water
B. megaterium microencapsulated 4 times daily quality parameters, especially
BUU 002 Bacillus)Fed with pH, ammonia and nitrite as
B. polymyxa probiotic enriched compared to controls.
BUU 003 Artemia
B. licheniformis
BUU 004
B. subtilis BUU
005
Probiotic B. subtilis BUU
B 006
B. polymyxa
BUU 007
B. megaterium
BUU 009
B. circulans BUU
010
B. pumilus BUU
012
Bacillus pumilus Obtained from the P. japonicas Added as alive cells Starting with 104 to 1010 94.9% Larval survival increase [30]
Bacillus Genetic (Larvae) cells g− 1 daily for 10 after 7 days
Stock Center days
(Columbus, Ohio)
(http://Bacillus.bi
osci.ohio-state.edu)
Bacillus PC465 Isolated from the Litopenaeus Feed Additive 107 CFU g − 1 Higher biomass of microbes as [22]
gut of vannamei 10% of body weight 3 compare to 109 CFU g − 1. DEA
Fenneropenaeus times daily for 30 days such as amylase, protease, and
chinensis lipase, in the mid-gut
significantly increased.
Protects against viral
infections.
109 CFU g − 1 Higher GR as compare to 107
10% of body weight 3 CFU g − 1. Improve SR,
times daily for 30 days digestion, nutrient absorption.
DEA such as amylase, protease,
and lipase, in the mid-gut
significantly increased. Protect
against viral infections.
B. subtilis Not Mentioned White Shrimp Included in diet Not Mentioned Increased SOD, GPX, LYZ & PO [23]
enzymes. Increased SR and GR.
(A) B. subtilisand (B) Not Mentioned White Shrimp Feed Additive 1.2 × 104 CFU/g (1 g/ (A) Very good GR, higher FCR [27]
B. megaterium (Both strains Kg) values, 100% SR and
administered separately) 3 times daily for 4 weeks haemolymph metabolites
positively affected.
(B) Good FCR values, 96.67%
SR and improved culture
oxygen concentration.
B. subtilis Isolated from White Shrimp Feed Additive 105 and 108 CFU g− 1
Improve GR, DEA, resistance to [102]
fermented pickles (juvenile) 8 weeks V. harveyi and upregulation of
immune gene expression.
Commercial Probiotic Belgium, www.inve. Litopenaeus Water Additive 2.5 × 104 CFU mL− 1 for Increased survival and growth [28]
NVE Sanolife® MIC, INVE be vannamei with microalgae Nauplius4-5 to Zoea2 and of zoea and mysis phases.
(B. subtilis, B. licheniformis, (Larvae & probiotic enriched 5.0 × 104 CFU mL− 1 for
B. pumilus) Post Larvae) Artemia Zoea3 to PL10 (in water
daily)
10.0 × 104 CFU mL− 1
(with microalgae daily)
(continued on next page)

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U.D. Butt et al. Fish and Shellfish Immunology 114 (2021) 263–281

Table 2 (continued )
Probiotic Strains Source Targeted Mode of Application Concentration and Responses References
Species Duration

20.0 × 104 CFU mL− 1

(via Artemia)
Bacillus DMS Series Supplied by Penaeids Water Additive 1 x 104 to 1 x 105 mL− 1
Reduce Vibrio and luminous [215]
Biomanagement for 160 days Vibrio in pond, low Vibrio
Systems, Darwin, numbers in sediments and no
Australia luminous Vibrio occurred.
Improved production.
Bacillus tequilensis YC5-2 Isolated from the Whiteleg Water Additive 1 × 105 CFU mL− 1
daily Improved survival and [25]
B. endophyticus C2-2 and guts of healthy wild shrimp showed remarkable
YC3-b adult shrimp (Larvae) antagonistic activity against
B. subtilis YC2-a Vibrio campbelli, V. vulnificus,
V. parahaemolyticus, and
V. alginolyticus.
Bacillus S11 (As wet or Isolated from black Penaeids Feed Additive ~1010 CFU g− 1 Lack of any success other than [216]
lyophilized cells, or as tiger shrimp 3 times daily for 100 better survival against
saline suspensions) habitats days V. harveyi.
Antagonistic Bacillus spp. Indigenously P. monodon Lab Experiment Average zone of Reduce the pathogenic effect of [24]
isolated Bacillus spp. (Juvenile) inhibition against virulent luminous V. harveyi.
luminescent V. harveyi
strains was 10 mm.
Bacillus S11 Isolated from black Black Tiger Feed Supplement ~1010 CFU g− 1 mixed Significantly larger growth and [217]
tiger shrimp Shrimp (P. with 3 kg of feed daily higher survival and
habitats monodon) for 100 days controlled V. harveyi
infections.
B. subtilis BT23 Isolated from Black Tiger Water Additive After 6 days of treatment Reduced growth of V. harveyi [218]
shrimp culture Shrimp (P. at 106–108 CFU mL− 1 at and
ponds monodon) 28◦ shrimp infected with reduced mortality.
103–104 CFU mL− 1 of
V. harveyi for 1 h then
again treated with the
same amount of BT23 for
1h
B. subtilis UTM 126 Isolated from Litopenaeus Feed Supplement 105 CFU g− 1 Reduced mortality against [172]
shrimp culture vannamei 28 days pathogenic V. harveyi.
ponds (White
shrimp)
B. subtilis E20 Isolated from Litopenaeus Water Additive 109 CFU L− 1 once every Improved larval SR, [219]
human health food vannamei 3 days during 14 days of development, stress resistance,
‘Natto’ (Larvae) a breeding experiment and immune status.
Bacillus OJ + IMO Isolated from the Litopenaeus Feed Additive 108 CFU/g of feed + Immunity improved, intestinal [120]
Pacific white shrimp vannamei 0.2% IMO microbes altered and
(Litopenaeus (White 28 days resistance to WSSV increased.
vannamei) shrimp)
Bacillus P64 Isolated from the L. vannamei By Inoculation 107 bacteria mL− 1
Showed inhibitory and [220]
hepatopancreas of (White 24 h immunomodulatory effect.
healthy wild shrimp shrimp)
Enterococcus faecium MC13 Isolated from Penaeus Feed Additive 200 mg/100 PL in feed Protects against V. harveyi and [35]
brackish water fish monodon Water Additive twice a day V. parahaemolyticus.
and shrimp intestine 107 CFU mL− 1 at the rate
of 200 μl/100 PL in
water twice a day
Streptococcus phocae P180 Feed Additive 200 mg/100 PL in feed Growth and protection against
Water Additive twice a day V. harveyi infection increased.
107 CFU mL− 1 at the rate
of 200 μl/100 PL in
water twice a day
Streptomyces spp. Isolated from P. monodon Feed Supplement 2.5, 5.0, 7.5, or 10.0 g Changes in physical [221]
sediment samples per kg feed twice a day parameters observed.
collected from on day 1, 10 and 20 Improved growth, survival and
Vellar estuary India disease resistance. Decreased
pathogenic Vibriosis
Streptomyces spp. Isolated from Black Tiger Feed Supplement Streptomyces cells at 1% Enhanced GR and survival [33]
marine sediment Shrimp (Post 15 days in 3 treatments against V. harveyi.
samples of shrimp Larvae)
farms at
Queensland,
Australia
Bacillus coagulans NJ105 Isolated from Penaeus Water Additive 1 × 107 CFU mL− 1
daily Beneficial in terms of [32]
shrimps and vannamei for 35 days increasing GR and enhancing
common carp ponds immune responses, such as PO
activity, SOD activity, POD
activity and antibacterial
activity.
b. Gram-Negative Bacteria
Pseudomonas 1-2 Shrimp [222]
(continued on next page)

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Table 2 (continued )
Probiotic Strains Source Targeted Mode of Application Concentration and Responses References
Species Duration

Pseudomonas MCCB 102 and
MCCB 103
Rhodopseudomonas palustris
GH642
Synechocystis MCCB 114 and
115
V. fluvialis
Vibrio fluvialis PM 17
Pseudomonas sp. PM 11
(Both strains administered
separately)
Vibrio gazogenes NCIMB 2250
Isolated from Lab ExperimentWater In well and disc diffusion Showed good inhibition in
estuarine water Additive assay diameter of the pathogenic Vibrio damsela,
sample collected zone of inhibition was 17 Vibrio harveyi, Vibrio fluvialis,
from Mangalore, and 9 mm respectively. Vibrio parahaemolyticus and
India In cross-streak method, Vibrio vulnificus.
inhibition was averaging Nonpathogenic as a water
41.4 mm in all five additive.
pathogens106 CFU mL − 1
Isolated from Penaeus Water Additive 106 CFU mL − 1 Proved to be resistant, [34]
seawater hatchery monodon antagonistic and inhibitory.
Higher survival against
V. harveyi MCCB 111 was
observed.
Isolated from Penaeus Water Additive 1 × 107 CFU mL− 1
daily Beneficial in terms of [32]
shrimps and vannamei for 35 days increasing GR and enhancing
common carp ponds immune responses, such as PO
activity, SOD activity, POD
activity and antibacterial
activity.
Isolated from Penaeus Feed Additive Daily for 20 days Exhibited antagonistic activity, [223]
surface seawater of monodon (Post higher survival against
Vypeen Island Larvae) V. harveyi, a substantial
reduction or total absence of
Vibrio spp.. Cultures were
found to contain high levels of
protein.
Isolated from Penaeus Added as alive cells Starting with 104 to 1010 94.9% Larval survival increase [30]
shrimp cultures japonicus cells g− 1 daily for 10 after 7 days.
days
Isolated from the Tiger Shrimp By inoculation in rearing 103 CFU mL− 1 every 3 No effectiveness observed. [29]
gut of farm-reared (Penaeus water days and 7 days intervals
sub-adult shrimp monodon) for 45 days
Isolated from the GI Pacific white Injection 3 x 107 or 3 x 105 Higher mortality observed. [31]
tract of marine shrimp bacteria per shrimp
invertebrates mL− 1
Dragon Feeds 3 x 107 live bacteria Reduced levels of Vibrios in the
Supreme™ + Chitin (V. gazogenes) per gram fore and hindgut. Improved
Powder (Sigma-Aldrich) of feed health & welfare.
+ Live V. gazogenes
culture

Abbreviations: CFU: colony-forming unit, DEA: digestive enzyme activity, FCR: feed conversion rate, GR: growth rate, GI: gastrointestinal, IMO: Iso­
maltooligosaccharide, LYZ: Lysozyme, PO: Phenoloxidase, POD: peroxidase, SOD: superoxide dismutase, SR: survival rate, WSSV: white spot syndrome virus.

by producing SCFAs, suppressing the space for toxin receptors, compe­
tition for nutrition, and up-regulation of immune responses against in­
fections are the immunomodulatory functions of prebiotics [17,157].
White shrimp larvae (Litopenaeus vannamei) when fed with MOS,
enhanced immunity by increasing total hemocyte count, phenoloxidase
and respiratory burst activity [80]. This increase can be noticed due to
recognition of foreign particles through pattern recognition receptors,
intracellular signalling cascade and nodular aggregations [158]. Innate
immunity of shrimp was also enhanced by triggering of immune-related
gene expressions [107] such as lipopolysaccharide, β-1,3-glucan-bind­
ing protein (LGBT) [159], serine protein and peroxinectin. Diet sup­
plemented with commercial prebiotics also stimulated the expressions of
immune-related genes in white shrimp such as prophenoloxidase,
penaeidin, crustin and lysozyme activity in shrimp’s gut [109,110].
Non-specific immune responses such as alkaline phosphate and acid
phosphate in serum also improved immune responses [114]. On some
occasions, the outcome of prebiotic administration may be
dose-dependent; for instance, appropriate doses of β-glucan can accel­
erate immune-related genes, expression of Toll-Like Receptors (TLRs),
myostatin and heat shock protein 70 [115]. Higher concentration of
MOS along with β-glucan supplemented with the diet resulted in cell
damage, suppressed immunity and reduced resistance against in­
fections. However, when used in appropriate quantities, it resulted in
increased immunity, humoral responses and respiratory burst activity
[160].
Various studies also presented prebiotics in shrimp aquaculture as
anti-disease agents (see Table 3). According to Sun et al. [108] the
sustainability of Pacific white shrimp against Vibrio alginolyticus
enhanced by the up-regulation of some defensive parameters such as
albumin, superoxide dismutase, lysozyme and phenoloxidase activity.
Dietary supplementation of MOS can stimulate the bactericidal activity
in plasma and enhance the resistance against Vibrio harveyi [161]. Sac­
charides are similar to the specific receptors of bacteria, toxic molecules
and viruses, so they prevent the adhesion of pathogens by acting as
competing receptors in intestinal epithelial cells and reduce the preva­
lence of specific viral species [160]. Prebiotics are also reported to
stimulate shrimp’s hemocyte activity to eliminate certain viruses and
increase the degree of resistance by activating phagocytosis and
expression of antimicrobial peptides [107]. Moreover, microbial surface
antigens such as peptidoglycans, lipopolysaccharides (LPS), and β-1,
3-glucans stimulate lysis in hemocytes which induces various humoral
defence factors including agglutinins, clotting proteins, lysosomal hy­
drolytic enzymes and antimicrobial glucan peptides [162,163]. Sabry
Neto and Nunes [164] observed that the dietary supplementation of β-1,
3/1, 6-glucan enhanced resistance genes (R-Genes) of shrimp without
altering their total hemocyte count (THC) and reduced mortality against
viruses; however, the reduction in THC may lead to stress in crustaceans
[165]. These hemocytes are also known to play a vital role in the acti­
vation of proPO cascade, cytotoxicity, and haemolymph clotting
mechanism [149,166].

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Table 3
Prebiotics evaluated for shrimp aquaculture applications.
Prebiotic Source Targeted Species Mode of Concentration and Responses References
Strains Application Duration

a) Oligosaccharides
1
FOS Sucrose, 1–3 fructose, Fish Litopenaeus Diet 1.0, 2.0, 4.0 g kg− feed Significant improvement in SGR, SOD, AKP, [114]
meal, Soybean meal, Fish vannamei Additive for 60 days ACP, [lipase and amylase activities (0.4%)],
oil, Soybean oil, and microbial diversity. GOT, GPT dropped
Cholesterol, Lecithin, with increasing supplementation of FOS
Starch diets.
1
ScFOS Barley & wheat Litopenaeus Feed 0, 0.4, 0.8, 1.2, 1.6 g kg− Remarkable Iincrease in the growth rate, feed [112]
vannamei Additive feed for 8 weeks intake and decreased FCR.
(Juvenile) ScFOS affected the gut microbial community.
0.17g
ScFOS Not Mentioned White Shrimp Feed 0.25, 0.5, 0.75, 1, 2, 4 & No effect on WG, FC, Survival. [111]
(L. vannamei) Additive 8 g kg− 1 feed for 6 weeks ScFOS affected the gut microbial community.
(75.4 ± 0.8g)
IMO Prepared from cornstarch Pacific White Feed 0.2% IMO in feed for 28 No significant effect on microbial population, [120]
Shrimp Additive days immune responses & resistance to WSSV.
(L. vannamei)
1
MOS Cell wall of yeast Tiger Shrimp Feed 0, 1.5, 3, 4.5 g kg− feed Increased growth, FC (3g kg− 1) and survival. [200]
(Penaeus Additives for 48 days No harmful effect on hepatopancreas tissue.
semisulcatus) Reduced protein content with increasing
MOS.
1
MOS Not Mentioned Pacific White Water 12mgL− Supplementation of MOS increased THC, PO, [80]
Shrimp (Larvae) Additive RB and Ssurvival of shrimp larvae.
(M3 – PL12)
MOS & Inulin MOS: Cell wall of yeast Pacific White Diet 2, 5, 4 & 10 mg/g for 4 Significant improvement in the TLC 1, 2, 3, [16]
Inulin: Not Mentioned Shrimp Additive weeks proPO, STAT, crustin, anti-
L. vannamei lipopolysaccharide factor (5 mg/g inulin and
MOS). Decreased mortality against WSSV and
Vibrio alginolyticus challenges.
1
XOS 35% XOS, 65% Defatted L. vannamei Feed 0, 1, 2, 4, 6 g kg− feed Final body weight and WGR not affected. [108]
rice bran (Juvenile) Additive for 60 days SR, VL & A were higher in diet supplemented
with XOS. Provide resistance against Vibrio
alginolyticus.
β-1,4 Coconut meal enzymatic Kuruma Shrimp Diet 0%, 0.02% & 2% MNB Stimulate PO, PA, SR, immune response, [107]
mannobiose hydrolysate (Marsupenaeus Additive for 12 days increase resistance against Vibrio
japonicus) parahaemolyticus.
b) Polysaccharides
Inulin Not Mentioned Fenneropenaeus Water (A) No significant changes in TL, CL, weight/CL [92]
indicus Additive 150 mgL− 1 Selco & SGR of larvae and post larvae.
Larvae (M1- M3) enriched Artemia nauplii, No significant differences between the
3–4 nauplii per larvae 4 survivals of individuals from M1 – M3.
times a day Survival of PL was remarkably higher in the
(B) control group & the group fed with inulin-
60 mgL− 1 Inulin enriched Artemia.
enriched Artemia nauplii,
3–4 nauplii per larvae 4
times a day
(C)
150 mgL− 1 Selco + 60
mgL− 1 Inulin
Post larvae (PL1 – (A)
PL8) 50 mgL− 1 Selco enriched
Artemia nauplii, 3–4
nauplii per larvae 5–6
times a tay
(B)
50 mgL− 1 Inulin
enriched Artemia nauplii,
3–4 nauplii per larvae
5–6 times a day
(C)
50 mgL− 1 Selco + 50
mgL− 1 Inulin
Inulin Blue agave (Agave White Leg Shrimp Feed 0, 1.25, 2.5, 5.0, 10 g Enhanced growth, remarkably increased the [160]
tequilana) (L. vannamei) Additive kg− 1 of feed for 62 days PO.
(1.1 ± 0.08g) Decreased the prevalence of WSSV, Survive
1
(1.09 ± 0.07g) 2.5 g kg− of feed for 73 rate has not increased.
days
c) Fungal Polysaccharides
β –glucan S. cerevisiae P. monodon (Post- Water 0.25, 0.5, 1.0, and 2.0 Significant improvement in WG, PO. Reduced [91]
larvae) Additive mg mL− 1 for 43 days mortality rate and resistance against
V. vulnificus.
1
β − 1, 3 – S. commune P. monodon (Post- Feed 2 g kg− feed for 11 days Significantly improve DR, SR and resistance [224]
glucan larvae) Additive against V. harveyi.
(continued on next page)

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Table 3 (continued )
Prebiotic Source Targeted Species Mode of Concentration and Responses References
Strains Application Duration

β − 1, 3 – S. commune P. monodon Feed 0.2–10 g kg− 1 feed for 20 Significant increase in resistance against [225]
glucan Additive days V. damsela
β − 1, 3 – S. commune P. monodon Feed 2 g kg− 1 feed for 20 days Showed enhancement in sustainability [226]
glucan (Juveniles) Additive against disease and reduced the rate of
− 1
P. monodon (Post- 2 g kg feed for 15 days mortality.
larvae)
β − 1, 3 – S. commune P. monodon Feed 2.0 g kg− 1 feed for 40 Stimulate SR, haemocyte PA, cell adhesion, [227]
glucan (Brooders) Additive days superoxide anion production.
β – glucan S. cerevisiae P. monodon Feed 2 g kg− 1 feed for 3 days Stimulate PO, THC, survival and resistance [228]
Additive against V. harveyi.
− 1
β – glucan S. cerevisiae P. monodon Feed 1–1.3 g kg feed for 75 Significantly increased WG, SGR, survival, [229]
Additive days DR against V. alginolyticus.
β – glucan Cell wall of marine yeast F. indicus (Post- Feed 0.05, 0.1, 0.2, 0.3,0.4 g/ Improved THC, PO, NBT, survival and [230]
larvae) Additive 100g Feed for 21 days resistance to WSSV.
β − 1, 3 – S. cerevisiae L. vannamei Feed 2 g kg− 1 feed for 40 days Stimulate DGC, PO, DGG, TAG, Hc. [231]
glucan (Juveniles) Additive
β − 1, 3 – S. commune L. vannamei Feed 0, 0.2%, 1% in feed for 7 Stimulate PO, SOD, PA, superoxide anion [232]
glucan Additive days production. No significant effect on proPO,
Hc, transglutaminase activity.
1
β – glucan S. cerevisiae L. vannamei Feed 2 g kg− feed for 42 days Stimulate SGR, THC, SOD, PO, superoxide [113]
(Juveniles) Additive anion production.
β – glucan S. cerevisiae L. vannamei Feed 1 or 2 g kg− 1 feed for 35 Significantly increase THC, PO, SOD, RB, [233]
(Juveniles) Additive days disease resistance and resistance to WSSV.
β-1, 3/1, 6- S. cerevisiae L. vannamei Feed 1.0 mg kg− 1 feed for 70 Improved SR. No effect on THC, PO and total [164]
glucan (Juveniles) Additive days protein. Resist against infectious myonecrosis
virus.
β-1, 3/1, 6- G. lucidum L. vannamei Feed 0, 1, 2, and 4 g/kg for 30 Stimulate PO, SOD, superoxide anion [234]
glucan Additive days production.
β – glucan Not Mentioned White Shrimp Diet 0.5 g kg− 1 for 90 days Stimulated the level of lipopolysaccharide [159]
Larvae Additive and β-1, 3- glucan binding protein.
No significant effect on peroxinectin, LYZ,
and THC.
β – glucan Extracted from yeast cell L. vannamei Diet 0, 0.01%, 0.02%, 0.04% Significant increase in WG, SOD, GP, SR, [115]
wall Additive dry diets for 8 weeks protease, amylase, glutathione (0.02% &
0.04%), mRNA expression of TLR, myostatin,
heat shock protein 70. Decreased mRNA
expression of tumour necrosis factor- α,
richness and diversity of IMC (0.04).
MOS & Cell wall of yeast L. vannamei Feed 0, 0.2%, 0.4%, 0.8% for 100% mortality when challenged with [235]
β-glucan (Juvenile) Additive 45 days Vibriosis (0.8%). Significant increase in THC,
RB, PO (0.4% & 0.2%). Immune responses
suppressed (0.8%).
d) Commercial Prebiotics
Immunogen Cell wall of yeast Pacific White Feed 0, 0.5, 1 & 1.5 g kg-1 for No remarkable effect on WG, FCR, SGR, [110]
(β-glucan & Shrimp Additive 60 days Amylase activity.
MOS) L. vannamei (Post Stimulate protease activity (1.5 g kg− 1),
larvae) lipase activity (1 & 1.5 g kg− 1), proPO,
crustin, g-type lysozyme (1.5 g kg− 1),
expression of penaeidin gene (1g kg− 1).
Previda 100% hemicellulose (83% Pacific White Feed 0, 0.2, 0.5, 1.0 & 1.6 g Increased HPC, hyaline cell counts, [109]
sugar, 5% ash, 12% Shrimp Additive kg− 1 feed for 35 days haemolymph glucose, haemolymph protein
hemicellulose extract) L. vannamei (1.6 g kg− 1).
Modification of microbial communities in the
shrimp gut. WG, SR, FCR were not affected by
supplementation of Previda in the diet.

Abbreviations: A: area, ACP: acid phosphate, AKP: alkaline phosphate, CL: carapace length, DGC: daily growth coefficient, DGG: digestive gland glycogen, DR: disease
resistance, FCR: feed conversion rate, FOS: fructooligosaccharide, GOT: glutamic-oxaloacetic transaminase, GPT: glutamic-pyruvic transaminase, GP: growth per­
formance, HPC: haemocyte phagocytic capacity, Hc: hemocyanin, IMO: isomaltooligosaccharide, LYZ: lysozyme, MOS: mannan oligosaccharide, NBT: nitroblue
tetrazolium activity, ProPO: prophenoloxidase activity, PO: phenoloxidase activity, PA: phagocytic activity, PL: post larvae, RB: respiratory burst, SR: survival rate,
SGR: specific growth rate, SOD: superoxide dismutase, STAT: signal transducer and activator of transcription, ScFOS: short-chain fructooligosaccharide, TL: total
length, THC: total haemocyte count, TLR: toll-like receptor, VL: villi length, WG: weight gain, WGR: weight gain rate, WSSV: white spot syndrome virus, XOS:
xylooligosaccharide.

Several studies have stressed the use of synbiotics as immunomod­
ulators (see Table 4). Synbiotics enhance immunity by facilitating the
growth of beneficial bacterial strains colonized on mucus lining and
prevent the pathogenic growth by competing for substrates and adhe­
sion sites [84]. The host’s mucosal immune system serves as the first line
of defence as it is exposed to the outside environment, while intestinal
epithelium acts as a natural barrier for the digestive tract by increasing
antagonism against pathogens (see Table 4) [84]. Synbiotic metabolites
also act as immunity boosters in aquaculture, for example, the role of
amino acids in activation of T lymphocytes, B lymphocytes, natural
killer cells, macrophages, as well as lymphocyte proliferation, and the
production of antibodies, cytokines, and other cytotoxic substances
[167,168]. They activate non-specific immune responses by enhancing
respiratory burst, phenoloxidase, nitric oxide synthetase, and serum
lysozyme activity [82]. Similarly, the dietary administration of
beta-glucan along with probiotic strains (B. subtilis and Pediococcus
acidilactici) enhanced the immunity of shrimp by stimulating superoxide
dismutase activity and also induced the gene expressions of serine

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Table 4
Synbiotics evaluated for shrimp aquaculture applications.
Probiotic Candidate Prebiotic Targeted Mode of Concentration and Duration Responses References
Candidate Species Application

B. licheniformis IMO Penaeus Feed Additive (A) Stimulated TBC, THC, PO, RB, LYZ, NOS, [82]
+ japonicus 108 CFU g− 1 B. licheniformis & SOD. Decreased Vibrio counts, cumulative
B. subtilis 0.2% IMO (T1) for 56 days mortality.
(B) Positive effects on bacterial flora &
108 CFU g− 1 B. subtilis & 0.2% activation of non-specific immunity.
IMO (T2) for 56 days
(C)
108 CFU g− 1 B. licheniformis +
B. subtilis & 0.2% IMO (T3) for 56
days
Bacillus sp. Mixture of White Shrimp Feed Additive 0, 1.5, 3 g kg− 1 or Powder of 109 Significantly increase WG, SGR, body [201]
Herbs L. vannamei CFU g− 1 (Bacillus) + 0, 1, 2 g lipid (1 g kg− 1), stimulated amylase and
(1.91 ± 0.03g) kg− 1 (Mixture of medical herbs) protease activities.
for 10 weeks
B. subtilis β – glucans White Feed Additive (1) Diet β-glucan + B. subtilis induced [159]
+ Shrimp Larvae 5 × 107 CFU kg− 1 (β-glucan + B. expression of serine protease and PO
Pediococcus (156 ± 39 mg) subtlis) for 90 days genes.
acidilactici (2) Diet β-glucan + P. acidilactici improved
0, 5 × 107 CFU kg− 1 (β-glucan + SOD & PO.
P. acidilactici) for 90 days
B. subtilis β – glucans L. vannamei Feed Additive 5 × 107 CFU kg− 1 (Probiotics) Remarkable increase in GP, BPC (β-glucan [119]
+ (PL 5) + & β-glucan + P. acidilactici), haemolymph
Pediococcus 0.35 g kg− 1 (β-glucans) for 90 glucose level, osmolarity (β-glu), the
acidilactici days height of intestinal villi (β-glucan +
P. acidilactici), intestinal LAB (β-glu +
B. subtilis). Decreased Vibrio species. No
remarkable changes in HLTG, cholesterol,
protein, haemolymph urea nitrogen or
chloride.
Bacillus OJ IMO White Shrimp Feed Additive 0, 108, 1010 CFU g− 1 (Bacillus) Significantly improved immune response, [120]
L. vannamei + AKP, PA, PO, RB, SR, disease resistance.
(1.75g) 0.2% IMO for 28 days Decreased TBC, Vibrio counts.
Mixture of Bacteria Inulin White Shrimp Feed Additive 0, 105 CFU g− 1 (Probiotics) Stimulated THC, ACP in haemocyte lysate [202]
(2LAB + 2Bacillus) L. vannamei + supernatant. Increased GP, SR, SGR,
(1.4 ± 0.31g) 0, 0.4, 0.8 g kg− 1 (Inulin) for 60 enzymatic activity of several enzymes in
days plasma.
Decreased prevalence of WSSV.
Pediococcus parvulus Mixture of White Shrimp Feed Additive 0, 2.1, 4.2, 8.4 mg kg− 1 Significantly increased PO, protein [236]
+ Echinacea L. vannamei (Probiotics) concentration of haemocyte lysate
Candida parapsilosis purpurea + (3.6 ± 0.58g) + supernatant.
(yeast) Uncaria 0, 1, 2, 4, g kg− 1 (Prebiotics) for Decreased prevalence of WSSV.
tomentosa 21 days
Pseudoalteromonas MOS Pacific White Through bio- 106 CFU mL− 1 (P. piscicida 1UB) Stimulated THC, PO, RB, SR, expression [80]
piscicida 1UB Shrimp encapsulation of + of immune-related genes, increased
(Larvae) Artemia 12 mg L− 1 (IMO) for 13 days disease resistance.
M3 – PL12
Lactobacillus GOS White Shrimp Feed Additive 108 CFU kg− 1 (L. plantarum 7–40) Improved colonization of Lactobacillus [86]
plantarum L. vannamei + plantarum and reduced prevalence of
0.4% GOS for 60 days Vibrio harveyi and Photobacterium
damselae in the intestines.
Lactobacillus GOS White Shrimp Feed Additive 108 CFU kg− 1 (L. plantarum 7–40) Significantly improved WG, LAB, [85]
plantarum L. vannamei + protease, leu-aminopeptidase and β
(Post-larvae) 0.4% GOS for 60 days -galactosidase activity. Reduced Vibrio
counts in the intestine, DEA.
Vibrio alginolyticus 1.115% inulin, Pacific White Feed Additive Diet P1 (daily), Diet P2 (twice a Significant increase in GP, enhanced SR, [15]
SKT-bR 1.015% FOS, Shrimp week), Diet P3 (once a week) for PO, RB in shrimp fed with diet (P1), THC.
1.488% GOS L. vannamei 30 days
(PL 15)
1
Bacillus sp. NP5 Ipomoea batatas White Shrimp Encapsulated diet 0.5%, 1%, 2% g kg− for 30 days Improved GP, FCR, THC, PO, differential [96]
L (sweet potato) L. vannamei haemocyte count, intestine bacteria.
Bacillus sp. NP5 Rf Ipomoea batatas White Shrimp Mirco- Group A (Once a week), Group B Improved GR & SR, stimulated immune [14]
L (sweet potato) L. vannamei encapsulated diet (Twice a week), Group C (Daily) responses in treatment C as compared to
for 40 days treatment A and B. Decreased FCR in
treatment C. Overall, Improvement in
intestinal bacterial count.
Probiotic SKT-b Ipomoea batatas White Shrimp Feed Additive 1% Probiotic +2% Prebiotic for Stimulated THC, PA activity, and PO [103]
L (sweet potato) L. vannamei 14 days activity.
Pseudoalteromonas MOS Pacific white Through Enriched 10 g/L (Pseudoalteromonas Promoted SGR & SR, stimulated THC, PO [81]
piscicida 1Ub shrimp larvae Artemia piscicida 1Ub) + & RB. It increased bacterial population
12 mg L− 1 (MOS) for 13 days and antagonism against disease.
Bacillus NP5 RfR MOS Pacific White Mirco- 0.5%, 1%, 2% for 30 days Stimulated THC, RB, and ProPO. [83]
Shrimp encapsulated Significant increase in growth & survival.
L. vannamei synbiotic Decreased FCR as compared to the control
group.

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Abbreviations: ACP: acid phosphate activity, AKP: alkaline phosphate activity, BPC: body protein content, CFU: colony-forming unit, DEA: digestive enzyme activity,
FCR: feed conversion rate, GP: growth performance, GOS: galactooligosaccharides, HLTG: haemolymph triglyceride, IMO: isomaltooligosaccharide, LYZ: lysozyme,
LAB: lactic acid bacteria, MOS: mannan oligosaccharide, NOS: nitric oxide synthetase, PO: phenoloxidase, PA: phagocytic activity, RB: respiratory burst, SR: survival
rate, SGR: specific growth rate, THC: total haemocyte count, TBC: total bacterial count, WG: weight gain, WSSV: white spot syndrome virus.
protease and phenoloxidase [159]. Synergistic effects of synbiotics may
also enhance immune parameters of shrimp such as phagocytosis, res­
piratory burst activity and alkaline phosphate activity and reduce Vibrio
counts [120]. These effects further protect shrimp against WSSV and
Vibrio harveyi [96,120]. Several other scholars also observed increased
immunity to various infections due to increased hemocyte count, phe­
noloxidase and respiratory burst activity [15,81,96] which resulted in
better protection against pathogens [14,103].
3.2. Competitiveness against pathogens
Probiotics are well known for their antagonism against pathogens in
the host species as well as in the culture system (see Table 2). Several
mechanisms are defined by which probiotic bacteria can induce bacte­
rial antagonism such as production of siderophore substances, but more
importantly, antimicrobial agents (antibiotics, antimicrobial peptides)
[169]. The application of probiotics can further induce a competitive
exclusion process, preventing pathogens from developing vital resis­
tance genes. This ecological process can be intentionally altered to
modify the microbial composition of pond water and soil. Numerous
Bacillus species having the ability to produce opportunistic antibiotics
and metabolites in response to pathogenic microbes are indicated in the
literature [170,171]. Sieved supernatant of B. subtilis UTM 126 has
shown significant inhibition against three different strains of Vibrio
harveyi. However, inhibitory activity against V. alginolyticus or
V. parahaemolyticus (the isolates from deceased shrimp) was insignifi­
cant. The observed diameter of the zone of inhibition of the
above-mentioned supernatant on the culture dish during in vitro was
about 10–15 mm. Overall, B. subtilis UTM 126 resulted in the suppres­
sion of pathogenic expansion both in vivo and in vitro [172]. Further­
more, probiotics are cheap, non-pathogenic and mostly non-toxic
sources of antibiotics, having the ability to synthesize a variety of me­
tabolites with antibacterial function, thus are worthwhile for commer­
cial production. They also have been experimentally used to control
microbial pathogenicity in fish [170,173].
3.4. Production of inhibitory compounds
The production of inhibitory biological compounds such as antibi­
otics, antibacterial substances, siderophores, bacteriolytic enzymes,
proteases and protease inhibitor, lactic acid and other organic com­
pounds like bacteriocins, hydrogen peroxide [181] and butyric acid
[182] are widely studied and well-documented functioning mechanism
of probiotics [183]. Probiotic microbes possess the potential to inhibit or
even eliminate some pathogenic bacteria. However, in vitro inhibition
may not be observed during in vivo experiments, due to incessantly
changing physicochemical environmental factors [184].
Several Bacillus spp. are known to compete with pathogenic micro­
organisms and produce antibiotic-inhibiting compounds [128,185]. The
production of bacteriocins [186], inhibition of virulence gene expres­
sion [187], and lytic enzymes such as β-1,3-glucanase that inhibit and
lyse the cell wall of the pathogens, protease, chitinase, and cellulose
have been widely observed [188]. Other antibacterial compounds such
as organic acid and hydrogen peroxide may also have an inhibitory ef­
fect due to the residual activity after catalase and acid treatment [189].
3.5. Competition for nutrients and adhesion sites
The potential probiotic bacterium is usually able to colonize and
adhere to the intestinal mucosa as it prevents the adhesion of pathogens
through inhibition of etiological agents. It also eradicates pathogens
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Fish and Shellfish Immunology 114 (2021) 263–281
from the infected GI tract [175] and prevents the disease occurrence by
interfering with the disease cycle. Several gram-positive, gram-negative,
and lactate-producing probiotics have superposed other bacteria in
adhesion capacity [40,190,191]. Probiotic Bacillus can replace Vibrio
through competitive exclusion for nutrients and adhesion sites [40],
thereby becoming a prepotent component of intestinal microflora (see
Table 2) [192]. Furthermore, in vitro and in vivo experiments suggested
that some potential strains are able to attach to the mucus by dislocating
pathogenic bacteria [190] to compete for essential nutrients and space.
The adhering mechanism of probiotics can be summarized in the
following steps; (a) it starts with attraction (b) binds to surface-secreting
gel and (c) ends with attachment to animal tissue cells [132]. However,
constant exposure to inadequate feeding ratios may lead to a reduction
in probiotic’s efficiency as well as intermittent production of organic
matter and nutrients (Fig. 4). Vine et al. [175] proposed the idea of
careful determination of dose-effect relationship to avoid such
conditions.
3.3. Alteration in gut microflora
The complex polymicrobial ecology of the alimentary canal of
shrimp is an interface between the external environment and the body
and has an important influence on health and disease. The intestine
performs multiple functions such as supporting digestion and absorption
of feed, maintaining osmotic balance, regulating endocrine and immu­
nity. The alimentary microbiota of adult penaeid shrimp (Penaeus chi­
nensis) may serve as an additional source of food, vitamins, necessary
amino acids and enhance microbial activity in the gastrointestinal tract
[174]. This microbiota can be favoured by many factors, for example,
increased population, density and types of microbes and the complex
interactions between them [37].
It has become a common practice to alter shrimp’s gut microbiota by
adding probiotics in feed or culture systems to improve digestion,
growth, and survival. Some microorganisms participate in the digestion
processes by producing extracellular enzymes, such as proteases and
lipases, and can provide necessary growth factors [175]. Similarly,
probiotics can consume carbohydrates from the intestine for self-growth
and produce various digestive enzymes such as amylase, protease,
lipase, increase growth rate, and pre-digestibility of secondary com­
pounds [176]. Ziaei-Nejad et al. [177] investigated Bacillus spp. For its
effects on Indian white shrimp (Fenneropenaeus indicus) at different
stages of its life cycle, and noted a significant increase in growth per­
formance as compared to control. Additionally, treated ponds
Fig. 4. Possible scenarios of organic matter and nutrient production in pond
water, related bacterial growth and its effects.
U.D. Butt et al.
manifested increased activity of amylase, protease, and lipase with
evidently higher digestibility of essential nutrients.
Several studies reported the potential mechanism by which pre­
biotics alter the intestinal microflora in aquaculture [51,69,112],
including Pacific white shrimp Litopenaeus vannamei [112,114]. Pre­
biotics regulate local cytokine and antibodies to increase intestinal
SCFAs production and improve the binding capability of SCFAs to
G-protein coupled receptors on leukocytes and carbohydrate receptors
on intestinal epithelial [178]. Supplementation of Previda (a commer­
cially produced prebiotic) modulated intestinal bacterial community
and stimulated immunity of shrimp [109]. Prebiotic administration
further stimulated nutrient absorption and improved homeostasis sta­
bility [179]. However, improper doses may result in proliferation of
intestinal microbiota.
Synbiotic administration can enhance, modulate and alter gut
microbiota (see Table 4). Gastrointestinal bacteria can produce physi­
ologically active substances such as enzymes, amino acids, and vitamins
through nutrient decomposition, which can provide increased utiliza­
tion and digestion of feed [94]. The probiotic component of synbiotics
can produce molecules such as bacteriocin to prohibit the growth of
pathogens on the intestinal wall and enhance the mucosal barrier [14,
180] whereas, the prebiotic component of synbiotics, serves as a sub­
strate for probiotics to grow [119]. The presence of sulfate-reducing and
nitrifying probiotic bacteria in the colon of Litopenaeus vannamei may
increase resistance against ambient sulfide, ammonia or nitrite [86,
121]. Synbiotics can further reduce mortality, regulate intestinal flora
and enhance the immune status of shrimp against Vibrio alginolyticus
[82,96,120].
3.6. Stimulation of growth and survival
Literature has proven that both dietary supplementation and oral
administration of probiotics enhanced the growth of the target species
by providing the necessary nutrients and improved feed utilization and
digestibility by increasing digestive enzymes (see Table 2) [78,193].
Several strains of Bacillus as probiotics have been tested in shrimp
aquaculture and proved to be effective (see Table 2). Bacillus generally
facilitates nutrient assimilation by using a variety of nutrients for their
own growth and simultaneously releasing necessary digestive enzymes
for the host, resulting in higher growth and survival [194]. Litopenaeus
vannamei and Fenneropenaeus indicus administered with Bacillus at the
rate of 50 g kg− 1 of feed resulted in increased growth [195].
B. megaterium BM1 at a concentration of 106 cells g− 1 diet of L. vannamei
during in vivo study resulted in better feed utilization and growth [196].
However, the application of microencapsulated and freeze-dried Bacillus
has shown no significant effect on shrimp larvae but increased the
growth and survival of Post Larvae (PL) remarkably [177]. This uncer­
tainty may be associated with shrimp’s exposure time to probiotics.
Giant tiger shrimp (Penaeus monodon) supplemented with Bacillus spp.
DDKRC1, induced exceptional growth, better protein ratio and lower
FCR [197]. Similar effects were observed in Litopenaeus vannamei (white
shrimp) [198].
A wide variety of prebiotics are administered as feed supplements to
attain better growth activity in treated shrimp [199]. Live feed has also
been reported to promote the growth of shrimp larvae, specifically
Artemia enriched feed due to its high nutritional value and digestibility
[80]; for instance, bioencapsulation of Artemia species with MOS,
improved survival of Litopenaeus vannamei while enhanced growth and
FCR when supplemented with diet [200]. Prebiotic application may also
enhance the survival rate by stimulating several immune parameters
such as phagocytic, bactericidal and phenoloxidase activities [107,115].
Synbiotics are proved to have beneficial effects on growth parame­
ters by increasing fat decomposition [201]. Dietary supplementation of
B. subtilis and Pediococcus acidilactici, along with beta-glucan have
improved growth performance [119]. Administration of a mixture of
bacteria (2LAB + 2Bacillus) and inulin in white shrimp improved its
275
Fish and Shellfish Immunology 114 (2021) 263–281
survival by reducing the prevalence of WSSV [202]. Synbiotics also
promote shrimp growth by increasing the efficiency of active feed intake
[121]. Improved growth of treated species may be correlated with
increased bacterial counts and improved intestinal morphology [203];
for instance, synbiotic application promoted growth by altering physi­
ological properties of GIT and morphology of epithelium [15].
3.7. Enzymatic activities
It is speculated that the application of probiotics in aquaculture can
help attain higher enzymatic activities and enhance feed utilization and
digestive capacity by modulating extracellular and antioxidant enzymes
(see Table 2) [180]. Glutathione peroxidase (GPx), superoxide dismut­
ase (SOD) and catalase (CAT) are commonly found antioxidant enzymes
in aquatic species [204]. SOD helps decompose harmful oxygen mole­
cules (O−2 ) into H2O2 [205] while CAT catalyzes the dismutation of H2O2
into H2O and O2 [206]. Antioxidant enzymes are also known to coun­
teract the damage caused by reactive oxygen species (ROS) [207] thus
protect the host against oxidative stress [173]. It is reported that the
secretion of digestive enzymes is another characteristic of Bacillus spe­
cies [208]. Usually, Bacillus species can modulate almost all major
digestive enzymes such as protease, amylase, trypsin, and lipase [9,
209]. In particular, B. coagulans have been reported to enhance digestive
enzyme activity of freshwater prawn [209]. Similarly, Bacillus PC465
improved feed absorption of Litopenaeus vannamei by increasing diges­
tive enzyme activity [22].
Administration of prebiotics has also been reported to make en­
hancements in enzymatic activities (see Table 3). Dietary supplemen­
tation of beta-glucan as prebiotic may result in significant enhancement
of protease and amylase activities, increased nutrients and feed assim­
ilation in the host, alteration in Bacillus and Geobacillus microbial com­
munities and a reduction in lipase levels through hypolipidemic activity
[210]. The combination of β-glucan (prebiotic) and Bacillus (probiotic)
can enhance digestive enzymes as Bacillus triggers extracellular enzymes
in the shrimp’s colon, such as protease and amylase [211]. Commer­
cially available prebiotic immunogen may also increase digestive en­
zymes in Pacific white shrimp Litopenaeus vannamei [110]. However,
excessive dosage of prebiotics may result in reduced enzymatic activities
such as glutamic-pyruvic transaminase (GPT) and glutamic-oxaloacetic
transaminase (GOT) [114].
Synbiotics are also known to produce necessary digestive enzymes
which improve digestion of the host and provide better FCR (see
Table 4). Yu et al. [201] observed stimulation in the level of digestive
enzymes by synbiotic supplementation. The use of probiotics for syn­
biotic preparation, resulted in biosynthesis and secretion of digestive
enzymes in shrimp’s gut [212]. Synbiotics stimulate the level of intes­
tinal proteases and leu-aminopeptidase, which play an important role in
protein digestibility [121]. Synbiotic supplementation may also increase
enzymes in plasma such as N-acetyl-β-glucosaminidase, β-galactosidase
and naphthol-AS-BI-phosphohydrolase, which is mainly due to probiotic
strains [202]. However, the effects of prebiotics as a synbiotic compo­
nent requires further investigations to understand their effects on
digestive enzyme activities.
4. Conclusion and future outlook
Shrimp aquaculture has been dominated by various pathogenic and
viral diseases over the past few decades. The use of antibiotics, to
counter these diseases, backfired as it equally threatened the health of
the host and the consuming bodies. Besides resisting the pathogens
inappropriate antibiotic application led to bacterial resistance in shrimp
and human consumers. Considering the gradual spike in the global de­
mand and preference for healthy and hygienic shrimp, there is a need for
natural alternatives such as pro-, pre-, and synbiotics as dietary sup­
plements to improve competitive exclusion of pathogens from the sys­
tem and to enhance the immune parameters of shrimp without affecting
U.D. Butt et al.
its health. However, to achieve optimal protection, a clear understand­
ing of these immunostimulants is necessary. As per the experiments
conducted in recent decades, pro-, pre-, and synbiotics could be
considered a better alternative, as compared to antibiotics and similar
products, for achieving protection while maintaining environmental
stability thereby increasing the shrimp yields. The experiments further
confirmed that the addition of these supplements in shrimp feed can
significantly decrease the occurrence of disease and increase enzymatic
activities, feed consumption, growth and survival of cultured shrimp.
Few studies also raised some concerns regarding the use of these sup­
plements in inappropriate quantities which can lead to excessive
nutrient production and disturbed microbial balance. In conclusion, a
methodical and comprehensive understanding of the utilities of pro-,
pre-, and synbiotics in the field of shrimp farming can be achieved
through profound knowledge of the genetic makeup and transcriptomic
and proteomic profiling of these products.
Furthermore, other alternatives, such as paraprobiotics (non-bio­
logical counterparts of the probiotic organisms), algae and plant extracts
with prebiotic properties are highly recommended, as the use of natural
products can yoke comparable advantageous effects and may reduce the
production cost. In summary, the present review reveals the higher
effectiveness of pro-, pre-, and synbiotics; however, immediate diagnosis
of the molecular pathways regulating the mechanisms of the pro-, pre-,
and synbiotics in shrimp metabolism is obligatory.
Declaration of competing interest
The authors declare that they have no competing financial interests
or personal relationships that seem to affect the work done in this paper.
Acknowledgements
This work was supported by the science fundation of Lishui Science
and Technology Bureau (2017ZDYF17) and the National Key Research
and Development (R&D) Program of China (No. 2017YFE0103102).
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