Probiotics in shellfish aquaculture

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Aquaculture and Fisheries

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aquaculture-and-fisheries

Review article

Probiotics in shellfish aquaculture

Einar Ringø

Norwegian College of Fishery Science, Faculty of Biosciences, Fisheries and Economics, UiT, The Arctic University of Norway, Tromsø 9037, Norway

A R T I C L E I N F O Keywords:

Probiotics Shellfish Aquaculture

A B S T R A C T

The shellfish aquaculture industry has dramatically developed during the last two decades. However, this de- velopment has, in some cases, resulted in environmental degradation, emergence of diseases and low pro- ductivity. The need for improving disease resistance, growth performance, feed efficiency, and safe aquatic production for human consumption has stimulated development and applications of probiotics in aquaculture.

Probiotics used in shellfish aquaculture include genera of Lactobacillus, Enterococcus, Bacillus, Aeromonas, Alteromonas, Arthrobacter, Bifidobacterium, Clostridium, Paenibacillus, Phaeobacter, Pseudoalteromonas, Pseudomonas,Rhodosporidium,Roseobacter,Streptomyces andVibrio. The beneficial effects of these probiotics include improved growth performance, enzymatic contribution to nutrition, inhibition of adherence and colo- nization of pathogenic bacteria in the digestive tract, modulation of the gut microbiota, and increase haema- tological parameters and immune response.

The present review addressed insight into the application of probiotics in shellfish aquaculture, methods of administration, mode of actions, and their enhancing effects, and discuss research gaps and issues that merit further investigations.

1. Introduction

In the 1970s and 1980s antibiotics were commonly used in disease control. However, the indiscriminate use of antibiotics used to treat infectious diseases led to selective pressure of antibiotic resistance, a property that may be transferred to other bacteria (Cabello, 2006;

Romero, Feijoó, & Navarrete, 2012). Moreover, it is generally accepted that antibiotics administration in finfish and shellfish modulate the gut microbiota (Ringø et al., 2016), which in turn exerts negative effects on humans (Greenless, 2013;Salyers, Gupta, & Wang, 2014). Based on this fact, the European Union in 2003 banned the use of antibiotics in production. The use of probiotics is one of the alternative approaches to immunoprophylactic control in aquaculture, and is considered as a supplementary strategy or alternative to vaccines and chemicals.

There is a long history of health claiming microorganisms.

According toBottazzi (1983), the Roman historian Plinius in 76 B.C.

recommended administration of fermented milk products for treating gastroenteritis. The wordprobioticstems from the Greek rootsproand bios, or “profile”(Schrezenmeir & de Vrese, 2001), and several defini- tions of probiotics have been put forward since the first definition was given by Lilly and Stillwell (1965), but the most widely used is the definition by World Health Organisation's (WHO);“live microorganisms that when administrated in adequate amounts, confer a health benefit to the host”. During the last decades, several reviews have addressed on

probiotics and their impacts in shellfish aquaculture as growth pro- moters, nutritional, environmental capacity, as immunostimulants and advantage as prophylactic against infectious diseases (Ayisi, Apraku, &

Afriyie, 2017; Cordero, Esteban, & Cuesta, 2014; Farzanfar, 2006;

Hoseinifar, Dadar, van Doan, & Harikrishnan, 2019;Hoseinifar, Sun, Wang, & Zhou, 2018;Kuebutornye, Abarike, & Lu, 2019;Kumar, Roy, Meena, & Sarkar, 2016;Li et al., 2018;Ninawe & Selvin, 2009;Shefat, 2018;Soltani et al., 2019;van Hai et al., 2009a;van Hai and Fotedar, 2010).

Even though information was presented in the above mention re- views, the present review address to present an update on probiotics in shellfish aquaculture, and on probiotics data not mention in the aforementioned reviews. In order to avoid overlaps, studies discussed in the aforementioned reviews are only briefly presented in the text and Tables.

In shellfish aquaculture, several probiotics species are used;

Lactobacillus, Enterococcus, Bacillus, Aeromonas, Alteromonas, Arthrobacter,Bifidobacterium,Clostridium,Microbacterium,Paenibacillus, Phaeobacter, Pseudoalteromonas, Pseudomonas, Rhodosporidium, Roseobacter,Streptomyces andVibrio. To my knowledge, the first studies on the use of probiotics in shellfish aquaculture was carried out by Maeda and Liao (1992, pp. 25–29)andNogami and Maeda (1992), using bacterial strain PM-4 originally isolated from a crustacean culture pond, but since then numerous studies have been carried out (Table 1–

https://doi.org/10.1016/j.aaf.2019.12.001

Received 10 September 2019; Received in revised form 1 December 2019; Accepted 2 December 2019 E-mail address:[email protected].

Aquaculture and Fisheries 5 (2020) 1–27

Available online 09 January 2020

2468-550X/ © 2019 Shanghai Ocean University. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).

Table1 Effectoflacticacidbacteria(LAB)ongrowthperformance,immuneresponseanddiseaseresistanceinshrimpculture. SpeciesIsolatedfromDoses/durationShellfishspeciesParametersinvestigatedReferences LABShrimpgut1.5×108CFUmL-1/60daysPacificwhiteshrimp (Litopenaeusvannamei)↑Survival,resistanceagainstV.harveyiVieiraetal.(2007)a LABstrainsNationalCollection,Pune, India5×106cellsg-1/ 4weeksPenaeusindicus↑ResistanceagainstV.parahaemolyticusAjithaetal.(2004)b LABstrainNS61Giantlion'spawscallop104CFUmL−-1/ 11daysCortezoyster(Crassostrea corteziensis)larvae↑Survival →GrowthCampa-Cordovaetal.(2011) Enterococcus E.faeciumNationalCollection,Pune, India5×106cellsg-1/ 4weeksPacificwhiteshrimp↑ResistanceagainstV.parahaemolyticusAjihaetal.(2004)b E.faeciumN/A107CFUg-1/ N/AaboutdurationGianttigerprawn(P. monodon)↑ResistanceagainstV.harveyiand V.parahaemolyticusSwainetal.(2009)b E.faeciumN/A106CFUg-1/ 4weeksPacificwhiteshrimp↑Survival,adhesiveactivity,expressionofimmuneanddigestion relatedgenesinthemidgutShaetal.(2016a,2016b) E.faeciumShrimpintestineN/AGianttigerprawn↑GrowthandresistanceagainstVibrioShefat(2018) Lactococcus Lac.garvieaeN/A107CFUg-1/ N/AaboutdurationGianttigerprawn↑ResistanceagainstV.harveyiSwainetal.(2009)b Lac.lactisShrimpintestine105CFUg-1/7daysM.japonicus↑Upregulationoflysozymegeneexpressioninintestineand hepatopancreas,andresistanceagainstV.penaeicida →anti-lipopolysaccharidefactor,superoxidedismutase, prophenoloxidaseandtoll-likereceptor

Maedaetal.(2014) Lac.lactisPacificwhiteshrimp intestine2–4×108cellsg-1/ 16daysPacificwhiteshrimp↑HaemolymphPOactivity,relativemRNAexpressionof LvproPO1,LvproPO2andresistanceagainstV.parahaemolyticusChomwongetal.(2018) Lac.lactissubsp.lactisIntestineof Pacificwhiteshrimp106,107,and108CFUg-1/ 8weeksPacificwhiteshrimp↑Growthperformance,digestiveenzymesactivities, LactobacillusandBacilluscounts, Vibriocountsandresistanceagainst V.anguillarum

Adeletal.(2017a)d Lactobacillus Lactobacillussp.Digestivetractofchicken~1010CFUg-1/ 100daysGianttigerprawn↑Growth,survivalandresistanceagainst V.harveyiPhianphaketal.(1999)c Lactobacillussp.AMET1506Curd106CFUg-1/30daysPacificwhiteshrimp↑ResistanceagainstV.harveyiKarthiketal.(2014) Lactobacillussp.AMET1506Curd105CFUg-1/30daysPacificwhiteshrimp↑TotalheterotrophicbacterialloadandLABcountsinintestine ReducedthebacterialloadofE.coli,Salmonellaspp.andShigella spp.inintestine

Karthiketal.(2015) Lactobacillussp.Intestineof Pacificwhiteshrimp107CFUg-1/27daysPacificwhiteshrimp↑Bodyweight,digestiveenzymeactivitiesandresistanceagainst WSSVZuoetal.(2019)d Lb.acidophilusHomemadecurd105CFUg-1/30daysGianttigerprawn↑ResistanceagainstV.alginolyticusSivakumaretal.(2012)b Lb.acidophilusHomemadecurd106cells·g-1/ onemonth

Macrobrachium rosenbergii

↑GrowthandresistanceagainstVibriospp.KhanandMahmud(2015) Lb.brevisMTCC4463CulturecollectionDoseN/A/90daysM.rosenbergii↑Growthperformance,digestiveenzymesandbodycomposition ProbioticadministrationmodulatethegutmicrobiotaKarthikandBhavan(2018) Lb.bulgaricusNationalCollection,Pune, India5×106cellsg-1/ 4weeksPenaeusindicus↑ResistanceagainstV.parahaemolyticusAjithaetal.(2004)b Lb.bulgaricusIntestineofPacificwhite shrimp107and109CFUg-1/30daysPacificwhiteshrimp↑ImmuneresponseanddiseaseresistanceRoomianietal.(2018)d Lb.pentosusN/A106CFUg-1/ 4weeksPacificwhiteshrimp↑Survival,adhesiveactivity,expressionofPEN-3α,proPO,trypsin andα-amylaseinthemidgut,andproPO,LGBP,IveLee,trypsin andα-amylaseinthehepatopancreas Shaetal.(2016a)b (continuedonnextpage

Table1(continued) SpeciesIsolatedfromDoses/durationShellfishspeciesParametersinvestigatedReferences Lb.pentosusIntestineofhealthy Acanthogobiushasta107CFUg-1/ 4weeksPacificwhiteshrimp↑AbundanceofintestinalActinobacteria →improvementsofintestinalhistologyShaetal.(2016c)b Lb.pentosusIntestinaltractofabalone103,105,and107CFUg-1/8weeksHaliotisdiscushannai↑SR,Foodintake,shelllength-specificgrowthrate,FCR, antioxidantcapacityandresistanceagainstV.parahaemolyticusGaoetal.(2018)d Lb.pentosusGutofBrandedgoby (Chaeturichthysstigmatias)5×108CFUgfeed-1/ 4weeksPacificwhiteshrimp↑Digestionrelatedenzymes,resistanceagainstV. parahaemolyticusandinducedstressresponsegenesexpressionDuetal.(2019)d Lb.plantarumShrimpisolate107and1010CFU kg-1/168hPacificwhiteshrimp↑immuneresponse,gutmicrobiota,resistanceagainstV. alginolyticusChiu,Guu,Liu,Pan,and Cheng(2007)a Lb.plantarumPacificwhiteshrimp2×1010CFU kg-1/8daysPacificwhiteshrimp→TotalbacterialandLABcountsinthedigestivetract ReducedVibriocountsinthedigestivetractVieiraetal.(2008) Lb.plantarumBroodstockshrimp1.5×108CFUg-1/ 60daysPacificwhiteshrimp↑TotalLABcountsandresistanceagainst V.harveyi DecreasedtotalbacterialcountsandtotalVibriocounts

Vieiraetal.(2010) Lb.plantarumN/A3.16×109CFUg-1/60daysGiantfreshwaterprawn (M.rosenbergii)↑Specificgrowthrate,weightgainandphenoloxidase →Survival,totalhaemocytecountsandrespiratoryburstRahimanetal.(2010) Lb.plantarumCommercial3.3×1011CFUg-1feed;0,0.001,0.01, 0.1and1g/30daysPacificwhiteshrimp↑Growthperformanceandstressresistanceat1ginclusion ↑Survivalat0.1ginclusion →proteaseactivity

Tungetal.(2010) Lb.plantarumPacificwhiteshrimp2–4×108CFUg-1feed/42daysPacificwhiteshrimp↑DiseaseresistanceagainstV.harveyiKongnumand Hongpattarakere(2012) Lb.plantarumGutoffemaleblue swimmingcrab106,5×106,and107CFUmL-1/14daysPortunuspelagicus↑Survival,protease–andamylaseactivities,totalbacterial-and Vibriocountsintankwater →NitrogencontentandpHofculturewater Talpuretal.(2013) Lb.plantarumCulturecollection107,108,and109CFUg-1diet/ 90days

Macrobrachium rosenbergii

↑WG,SGR,FCE,PER,FCR,carcassproteincontent,LABcountsin intestine,totalhemocytecount,phenoloxidase-andrespiratory burstactivitiesandresistanceagainstA.hydrophila ↓LABcountsafterswitchingbacktobasaldiet

Dashetal.(2014)d Lb.plantarumCulturecollection107,108,and109CFUL-1diet/ 90daysM.rosenbergii↑WG,SGR,FCE,PER,FCR,carcassproteincontent →WaterqualityDashetal.(2016)d Lb.plantarumPacificwhiteshrimp intestine107mL-1/4weeksPacificwhiteshrimp↑Phenoloxidaseactivity,intestinalLABandresistanceagainstV. alginolyticus →Growthperformance,totalheterotrophicbacteriainintestine andintestinalVibriocounts

Ramirezetal.(2017) Lb.plantarumCommercialprobiotic109CFUmL-1/ 45daysPacificwhiteshrimp↑Finalweight,WG,SGR,FCRandimprovedtheresistanceagainst thestressofacutelowsalinityZhengetal.(2017)d Lb.plantarumPacificwhiteshrimp intestine2–4×108cells·g-1/ 16daysPacificwhiteshrimp↑HaemolymphPOactivity,relativemRNAexpressionof LvproPO1,LvproPO2andresistanceagainstV.parahaemolyticusChomwongetal.(2018) Lb.plantarumShrimpintestine1.0×107CFUmL-1/ 35daysPacificwhiteshrimp→GrowthperformanceandwaterqualityCorreaetal.(2018)d Lb.plantarumT8HepatopancreasfromPacific whiteshrimpN/A/10weeks+2dayschallengePacificwhiteshrimp↑Growthandresistanceagainst V.parahaemolyticusNguyenetal.(2018) Lb.plantarumT13HepatopancreasfromPacific whiteshrimpN/A/10weeks+2dayschallengePacificwhiteshrimp↑ResistanceagainstV.parahaemolyticus →GrowthNguyenetal.(2018) Lb.plantarumCommercialprobiotic20×103cellsmL-1and1×108(CFU) mL-1/45daysPacificwhiteshrimp↑Improvewaterqualityinbioflocsystem ReduceshrimpdiseasesandenvironmentalimpactPacheco-Vegaetal.(2018)d Lb.plantarumWildshrimpintestineN/APacificwhiteshrimp↑ResistanceagainstV.harveyiShefat(2018) Lb.plantarumShrimpintestineN/APacificwhiteshrimp↑ResistanceagainstVibrioShefat(2018) (continuedonnextpage)

Table1(continued) SpeciesIsolatedfromDoses/durationShellfishspeciesParametersinvestigatedReferences Lb.plantarumCommercialprobiotic109CFUmL-1/15daysPacificwhiteshrimp↑Finalweight,WG,SGR,FCR,digestiveenzymeactivitiesand enterocytesheightZhengetal.(2018)d Lb.plantarumIntestineofrainbowtrout0,107(LB7),108(LB8),and109(LB9) CFUg-1diet/97daysCrayfish(Astacus leptodactylus)↑Totalhaemocytecount,semigranularcells,hyalinecellscount, totalplasmaproteinandphenoloxidasebyLB7andLB8 administrations ↑SuperoxidedismutaseandcatalasebyLB7administration ↑Protease-,amylase-andalkalinephosphatasebyLB8andLB9

administration →Autochthonousintestinalbacteriacounts Valipouretal.(2019) Lb.sporogenesCommercialprobiotic0%,1%,2%,3%and4%/90daysM.rosenbergii↑SR,WG,SGR,FCEandPER,FCR,totalprotein,totalfreeamino acid,totalcarbohydrate,andtotallipidcontent, feedingrate,absorptionrate,conversionrateandexcretoryrate

Seenivasanetal.(2014)d Pediococcus P.acidilacticiCommercialprobiotic107CFUg-1feed/ 1monthLitopenaeusstylirostris↑Antioxidantstatus,resistanceagainst V.nigripulchritudoCastexetal.(2010)b P.pentosaceusIntestineof Pacificwhiteshrimp0,106,107,and108CFUg-1diet/ 8weeksPacificwhiteshrimp↑Finalweight,finallength,WG,SR,WG, FCR,proteaseandamylaseactivities, Lactobacillussp.andBacillussp.intestinalcounts

Adel,Yeganeh,Dawood, Safari,andRadhakrishnan (2017b)d Streptococcus S.cremorisNationalCollection,Pune, India5×106cellsg-1/ 4weeksPenaeusindicus↑ResistanceagainstV.parahaemolyticusAjithaetal.(2004)b S.phocaeIntestineofP.indicusDoseN/A/15daysGianttigerprawn↑ResistanceagainstV.harveyiKanmanietal.(2010) S.phocaeN/A107CFUg-1/ N/AaboutdurationGianttigerprawn↑SpecificgrowthrateandresistanceagainstV.harveyiSwainetal.(2009) S.phocaeCommercial108CFUmL-1/30daysGianttigerprawn↑Totalhemocytecounts,phenoloxidase-,phagocyteactivities, respiratoryburstandresistanceagainstV.parahaemolyticusPattukumaretal.(2013) S.phocaeFishintestineN/AGianttigerprawn↑ResistanceagainstVibrioShefat(2018) MixtureofLAB Lb.acidophilus,Lb.bulgaricus,Lb. casei,Lb.caseisubsp.tolerans andLb.jensenii

GItractofchicken1010CFUg-1/100daysGianttigerprawn↑GrowthandresistanceagainstV.harveyiPhianphaketal.(1999) Lb.plantarum,Lb.salivariusand Lb.rhamnosusGutoffemale P.pelagicus106,5×106and107CFUmL-1/14daysP.pelagicus↑Growthanddigestiveenzyme(proteaseandamylase)activities bymultipleprobioticsTalpuretal.(2012) PrimaLac©(Lb.acidophilus,Lb. casei,E.faeciumandB. bifidium) N/A0.25,0,5and10g kg-1/60daysPacificwhiteshrimp↑Weightgain,specificgrowthrate,body,bodycrudeprotein,FCR, protease,amylase,lipaseandpenaeidingeneexpression ↓bodycrudelipidandbodymoisture Miandareetal.(2016) E.faeciumandLb.pentosusGutofFenneropenaeus chinensis)and Chaeturichthysstigmatias

1×107CFU-1gfeed/4weeksPacificwhiteshrimp↑ResistanceagainstV.parahaemolyticusShaetal.(2016b)d E.faecalisandE.faeciumIntestineofprawnand mulletDoseN/A/ DurationN/APacificwhiteshrimp↑ResistanceagainstA.hydrophilaandV.vulnificusCuietal.(2017) S.faecium, S.thermophilus, Lb.acidophilus, Lb.bulgaricus, Lb.johnsonii, Lb.plantarum, B.bifidium,Aspergillusourozai andCandidapentolopsy

Commercial2×109CFUg-1/28daysPacificwhiteshrimp↑Growthperformance →CountsofcoliformsandS.aureus ↓TotalbacterialcountsandC.perfringens

JavadiandKhatibi(2017) CombinationofLABandBacillus (continuedonnextpage

3).Shellfish aquaculture plays an important role in the world economy, and according toFAO (2016)brackish and marine shrimp production have increased from less than 10.000 metric tonnes in 1970 to more than 4.000.000 metric tonnes in 2014, and most of the aquaculture shrimp production come from Pacific white shrimp (Litopenaeus van- namei) which accounts for 80% of the production. However, as patho- genic bacteria cause enormous economic loss, an alternative to che- motherapies and antibiotics is probiotics. The present review highlight probiotics as a key factor in sustainable shellfish aquaculture, and present information on the use of probiotics by their stimulating effect on growth performance, innate immune response and improved re- sistance towards pathogenic microbial infection.

2. Methods of probiotic administration

To my knowledge, the first application of probiotics in aquaculture was carried out by Kozasa (1986), but since then the environment- friendly treatment has increased rapidly, and several comprehensive aquaculture reviews have been published (e.g. Gatesoupe, 1999;

Hoseinifar et al., 2018;Ringø et al., 2014;Ringø et al., 2018;van Hai, Buller, & Fotedar, 2010;Verschuere, Rombaut, Sorgeloos, & Verstraete, 2000). With regard to the use of probiotics, it is essential to investigate the best way of administration, optimal dose, and the technical solu- tions required; especially to keep the probiotics alive in dry pellets (Gatesoupe, 1999).

Probiotic administrations mainly depends on several factors i.e. the probionts, supplementation form, vector of administration, dosage level and duration of application, and several different administration modes have been used:

i) Oral administration via diet or water/bath. Supplementation to the diet is the most widely used administration method. Generally, probiotics and cell wall components (parabiotics) are applied in the feed, added to the entire tank or pond water to confer pro- tection against infection (Verschuere et al., 2000). In fish- and shellfish larvae, live food (e.g.Artemia) has proved to be an effi- cient carrier of probiotics (e.g.Giarma, Amanetidou, Toufexi, &

Touraki, 2017;van Hai et al., 2010).

ii) Administration of several probiotics in combination. In his pioneer review devoted to “Probiotics in man and animals,”Fuller (1989) wrote, “Probiotic preparations may consist of single strains or may contain any number up to eight strains.” However, since the early 1990s most probiotic studies in aquaculture used single adminis- tration, but during the last decade, supplementation of multiple probiotics in the diets to aquatic animals has gained interest (e.g.

Mohapatra et al., 2014;Allameh et al., 2016;Zorriehzahra et al., 2016; Kesselring, Gruber, Standen, & Wein, 2019; Mukherjee, Chandra & Ghosh, 2019). The advantage of multiple-strain pre- parations is; they are active against wider range of conditions and species.

iii) Inactivated bacteria. For example, oral administration of heat-in- activated Lactobacillus delbrueckii ssp.lactis andBacillus subtilis, individually or combined (Salinas et al., 2008).

iv) Spores, a structure produced by few bacteria genera is resistant to many environmental or induced factors that the bacteria may be subjected to. The spores help the bacteria to survive by being re- sistant to extreme changes in the bacteria's habitat including ex- treme temperatures, lack of moisture/drought, or being exposed to chemicals and radiation. Bacterial spores can also survive at low nutrient levels, and according to Elisashvili, Kachlishvili, and Chikindas (2019)spore-forming probiotic bacteria have received increased scientific and commercial interest. Several studies listed inTable 2, have used bacilli spores.

v) Culturing, storing and administration. Probiotics are usually added to feed as freeze-dried cultures, which are sometimes mixed with Table1(continued) SpeciesIsolatedfromDoses/durationShellfishspeciesParametersinvestigatedReferences Enterococcussp.,Lactobacillussp. andBacillussp.N/A6×103CFUmL-1/30 daysPinkshrimp

(Farfantepenaeus brasilliensis

)

↑Finalweight,specificgrowthrate Higherlevelsoftotalproteinandgranularhaemocyte LowerVibriocountsinwater

deSouzaetal.(2012) MolassesandLactobacillusand BacillusN/A253.5kgpond-1/2.2×108CFUg-1/16 weeksPacificwhiteshrimp→DissolvedO2,temperature,salinity,totalheterotrophicbacteria, FCR,finalweightandsurvivalMaia,Modesto,Brito,Galvez, andGesteira(2016) LactobacillusandBacillusN/A2.2×108CFUg-1/ 16weeksPacificwhiteshrimp↑Totalheterotrophicbacteriacountinthesediment,concentration ofPyrrophytaalgae,andinwaterandsedimentqualityDePaiva-Maiaetal.(2013) Lactobacillus, B.subtilisand B.licheniformis

N/A3×107CFUkg-1, 1.8×108CFUkg-1and 2×107CFUkg-1/8weeks Pacificwhiteshrimp↑Growthperformance,superoxidedismutase,catalase,alkaline phosphatase,lysozyme,lipaseandamylaseactivities,intestinal villiheightsandmicrobialgutdiversity

Xieetal.(2019) N/A:noinformationavailable. Generaabbreviations:E.–Enterococcus;Lac.–Lactococcus;Lb.–Lactobacillus;P.–Pediococcus;Str.–Streptococcus;W.–Weissella;V.–Vibrio. ↑-positiveeffect;↓-negativeeffect;→-noeffect. aStudiesdiscussedinthereviewofNinaweandSelvin(2009). bStudiesdiscussedinthereviewofHoseinifaretal.(2018). cStudiesdiscussedinthereviewofKumaretal.(2016). dStudiesdiscussedinthereviewofRingø,vanDoan,Lee,&Song(2019).

Table2 EffectofBacillusongrowthperformance,immuneresponseanddiseaseresistanceinshrimpculture. BacillusspeciesIsolatedfromDoses/durationShellfishspeciesParametersinvestigatedReferences Bacillussp.S11Intestineofgianttigershrimp~1010CFUg-1feed/100daysGianttigershrimp (P.monodon)↑MSW,diseaseresistanceagainst VibrioharveyiRengpipatetal.(1998a,b)a Bacillussp.S11Intestineofgianttigershrimp~1010CFUg-1feed/90daysGianttigershrimp↑MSW,phagocytosis,phenoloxidase,diseaseresistanceagainst V.harveyiRengpipatetal.(2000)a Bacillussp.S11Intestineofgianttigershrimp~1010CFUg-1/100daysGianttigershrimp↑ARG,diseaseresistanceagainst V.harveyiRengpipatetal.(2003)a Bacillussp.S11Intestineofgianttigershrimp~1010CFUg-1/90daysPacificwhiteshrimp (L.vannamei)↑Survival,totalhaemocyte,granularhaemocytecounts, phenoloxidaseanddiseaseresistanceagainstVibrioharveyiSapcharoenandRengpipat (2013) Bacillussp.Sediment1011/0.8hapondGianttigershrimp↑ARG,diseaseresistanceagainstVibriosp.Dalminetal.(2001)a BacillusOJIntestineofPacificwhite shrimp108and1010CFUg-1/28daysPacificwhiteshrimp↑Phenoloxidase,phagocytosis,respiratoryburst,acid phosphatase,resistanceagainstwhitespotdiseaseLietal.(2009)a BacillusNL110N/A4.73±2.87×109CFUg-1a/twiceadayfor 60daysGiantfreshwaterprawn (M.rosenbergii)↑SGR,WG,survival,ARG,totalhemocytecount, phenoloxidaseactivity,respiratoryburstRahimanetal.(2010) BacillusPC465IntestineofChinesewhite shrimp (F.chinensis) 108and109CFUg-1/ 30daysPacificwhiteshrimp↑Growthrate,amylase,protease,histology,transcriptionof penaeidin3a,peroxinectin,C-typelectin3,andthioredoxinin hemocytes,anddiseaseresistanceagainstwhitespotsyndrome virus

Chaietal.(2016) BacillusMJA1.1Mucusoftilapia(Oreochromis sp.)DoseN/A/30daysGianttigershrimp↑Survivalandsurvivalandresistanceofshrimpexposedto ammoniastress →Growth

Doroteo,Pedroso,Lopez,and Apines-Amar(2018) B.aquimarisIntestineofshrimp*>3×106CFUg-1/ 4weeksPacificwhiteshrimp↑GrowthandphenoloxidaseactivityNgoetal.(2016) B.aryabhattaiSedimentfromshrimpfarm108CFUg-1/6weeksPacificwhiteshrimpUpregulationofantioxidantenzymes(C-typelec,pen3a,hsp60, trxandfer) ↑Phenoloxidase,totalantioxidantactivityanddisease resistanceagainstV.harveyi →Totalhemocytecountandsuperoxidedismutaseinplasma andhepatopancreas

Tepaamorndechetal.(2019) B.cereusbiovartoyoiN/A105CFUmL-1/durationN/AGianttigershrimp↓SurvivalGuoetal.(2009) B.cereusGianttigershrimp0.1–0.4%per100feed/90daysGianttigershrimp↑SGR,FCE,AGR,FCR,phenoloxidase,lysozyme,respiratory burst,bactericidalactivityanddiseaseresistanceagainstV. harveyi

Chandranetal.(2014)a B.cereusIntestineofmudcrabNottestedinaninvivoexperimentMudcrab(Scylla paramamosain)Asthestrainshowedlessprobioticcharacteristicscomparedto B.pumilusandB.subtilisitwasnottestedinvivoWuetal.(2014) B.cereusPacificwhiteshrimp108CFUg-1/24daysPacificwhiteshrimp↑Weightgain →Diseaseresistanceagainst V.parahaemolyticus Vidaletal.(2018) B.cereusIntestineofadultfreshwater prawn(M.rosenbergii)104CFUg-1/28daysGiantfreshwaterprawn↑Growth,propionicacidlevel,superoxidedismutase →Aceticandbutyricacidlevel,anddiseaseresistanceagainst A.hydrophila

Wee,Mok,Romano,Ebrahimi, andNatrah(2018) B.coagulansIntestineofcommoncarp (Cyprinuscarpio)Threeconcen-trationsoflyophilized Rhodobactersphaeroidesand B.coagulans/28days

Pacificwhiteshrimp↑Growthperformanceanddigestiveenzyme(protease, amylaseandlipase)activitiesWang(2007) B.coagulansPondsedimentofshrimp105,5×105and106CFUmL-1/durationN/APacificwhiteshrimp↑SurvivalanddigestiveenzymeactivitiesZhouetal.(2009) B.coagulansCulturecollection107CFUg-1/50daysPacificwhiteshrimp↑Finalweight,dailyweightgain,survivalrate,andprotease-, amylase-andlipaseactivities →Musclecompositionofmoisture,crudeproteinandash

Wangetal.(2012) B.coagulansATCC7050Culturecollection106–108CFUg-1/56daysPacificwhiteshrimp↑Growthperformance,immune-andantioxidantresponse, digestiveenzymeactivitiesandintestinalmorphologyAmoahetal.(2019) B.flexusPondwater/sediment105CFUmL-1/21daysPacificwhiteshrimp↑Growthperformance,innateimmuneenzyme-anddigestive enzymeactivities,stresstoleranceanddiseaseresistance againstV.harveyi →Totalbacterialcountsinwater ↓Vibriocountsinwater

Caietal.(2019) (continuedonnextpage