Skip to main content
Log in

Dietary mixture of short-chain fatty acids, a phytogenic agent, and a permeabilizer improved growth, antioxidant enzymes, and immunocompetence in whiteleg shrimp juveniles (Penaeus vannamei)

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

An 8-week study was carried out to examine the influence of dietary Biotronic Top3 (BTT3), which is a blend of short-chain fatty acids (formate, propionate, and acetate), a phytogenic agent (cinnamaldehyde), and a permeabilizer complex (Biomin), in whiteleg shrimp (Penaeus vannamei) juveniles. Five isonitrogenous (∼38%) diets were formulated and supplemented with BTT3 at 0 (control), 0.3, 0.6, 0.9, or 1.2 g/kg. Shrimps (2.7 g) were allocated into 15 circular fiberglass tanks filled with 150 L seawater (20 shrimp per tank) and each dietary treatment was in triplicate. Shrimps were handfed thrice a day at the rate of 7% of their initial biomass for 8 weeks. At the end of the feeding trial, hemolymph and hepatopancreas (HP) were sampled to evaluate plasma biochemical factors, immune-related genes, and digestive enzymes, respectively. The growth rate in shrimps fed with a 0.3 g BTT3/kg diet was markedly higher (∼1.6 g) than in the control (P < 0.05), but higher dietary BTT3 levels did not improve growth and feed utilization. Protein deposition in the whole body of shrimps fed with 0.3 or 0.6 g BTT3/kg diets was significantly increased (∼1.5%) compared to the control. Total alkaline proteases activity in BTT3 groups was significantly higher than in the control. The activity of antioxidant enzymes, including catalase, superoxide dismutase, and glutathione peroxidase, was increased in HP of shrimps fed BTT3-supplemented diets; meanwhile, malondialdehyde level was significantly reduced by increasing dietary BTT3 level. Shrimps fed diets supplemented with 1.2 g BTT3/kg, and the control had the highest and lowest plasma phenoloxidase activity, respectively. The plasma alkaline phosphatase content in BTT3 groups was higher than in the control. The highest relative abundance of prophenoloxidase gene mRNA transcript was in HP of shrimps fed a 1.2-g BTT3/kg diet. The relative abundance of lysozyme and penaeidin-3α genes mRNA transcript in HP of shrimps fed 0.9 and 1.2 g BTT3/kg diets was higher than in the other groups. Based on the abovementioned findings, the inclusion of aquafeeds with 0.3 g BTT3/kg can increase growth performance in P. vannamei juvenile by promoting the antioxidant capacity and immune responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Data will be available on reasonable request.

References

  • Abbaszadeh A, Yavari V, Hoseini SJ, Nafisi M (2019) Mozanzadeh, M.T. Effects of different carbon sources and dietary protein levels in a biofloc system on growth performance, immune response against white spot syndrome virus infection and cathepsin L gene expression of Litopenaeus vannamei. Aqua Res 50:1162–1176

    CAS  Google Scholar 

  • Abdel-Tawwab M, Samir F, Abd El-Naby AS, Monier MN (2018) Antioxidative and immunostimulatory effect of dietary cinnamon nanoparticles on the performance of Nile tilapia, Oreochromis niloticus (L.) and its susceptibility to hypoxia stress and Aeromonas hydrophila infection. Fish Shellfish Immunol 74:19–25

    Article  CAS  PubMed  Google Scholar 

  • Abd El-Hamid MI, Ibrahim SM, Eldemery F, El-Mandrawy SAM, Metwally AS, Khalifa E, Elnahriry SS, Ibrahim D (2021) Dietary cinnamaldehyde nanoemulsion boosts growth and transcriptomes of antioxidant and immune related genes to fight Streptococcus agalactiae infection in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 113:96–105

    Article  CAS  PubMed  Google Scholar 

  • Alakomi HL (2007). Weakening of the Gram-negative bacterial outer membrane: A tool for increasing microbiological safety. Vtt Publications

  • Aalamifar H, Soltanian S, Vazirzadeh A, Akhlaghi M, Morshedi V, Gholamhosseini A, Mozanzadeh MT (2020) Dietary butyric acid improved growth, digestive enzyme activities and humoral immune parameters in Barramundi (Lates calcarifer). Aquac Nutr 26:156–114

    Article  CAS  Google Scholar 

  • Amer SA, Metwally AE, Ahmed SAA (2018) The influence of dietary supplementation of cinnamaldehyde and thymol on the growth performance, immunity and antioxidant status of monosex Nile tilapia fingerlings (Oreochromis niloticus). Egyptian J Aquat Res 44:251–256.

    Google Scholar 

  • Amparyup P, Charoensapsri W, Tassanakajon A (2013) Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish Shellfish Immunol 34:990–1001

  • AOAC (Association of Official Analytical Chemists), (2005) Official Methods of Analysis of AOAC International, 18th edn. Maryland, USA

    Google Scholar 

  • Awad E, Awaad A (2017) Role of medicinal plants on growth performance and immune status in fish. Fish Shellfish Immunol 67:40–54

    Article  CAS  PubMed  Google Scholar 

  • Baringou S, Rouault JD, Koken M, Hardivillier Y, Hurtado L, Leignel V (2016) Diversity of cytosolic HSP70 heat shock protein from decapods and their phylogenetic placement within Arthropoda. Gene 591(1):97–107

  • Bernfeld P (1951) Amylases α and β. In: Colowick P, Kaplan NO (eds) Methods in enzymology. Academic Press, New York, pp 149–157

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation methods. Methods Enzymol 52:302–310

    Article  CAS  PubMed  Google Scholar 

  • Cánovas M, Torroglosa T, Iborra JL (2005) Permeabilization of Escherichia coli cells in the biotransformation of trimethylammonium compounds into L-carnitine. Enzyme Microb Tech 37:300–308

    Article  Google Scholar 

  • Castillo S, Rosales M, Pohlenz C, Gatlin DM (2014) Effects of organic acids on growth performance and digestive enzyme activities of juvenile red drum Sciaenops ocellatus. Aquaculture 433:6–12

    Article  CAS  Google Scholar 

  • Ceccaldi HJ (1997) Anatomy and physiology of the digestive system. In: D’Abramo LR, Conklin DE, Akiyama DM (eds) Crustacean nutrition: advances in world aquaculture. World Aquaculture Society, Baton Rouge, LA, USA, pp 261–291

    Google Scholar 

  • Chen Z, Chang Z, Zhang L, Jiang Y, Ge H, Song X, Chen S, Zhao F, Li F (2019) Effects of water recirculation rate on the microbial community and water quality in relation to the growth and survival of white shrimp (Litopenaeus vannamei). BMC Microbiol 19:192

    Article  PubMed  PubMed Central  Google Scholar 

  • Chellapandi P (2021) Development of top-dressing automation technology for sustainable shrimp aquaculture in India. Discover Sustainability 2:26. https://doi.org/10.1007/s43621-021-00036-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Chowdhury MAK, Song H, Liu Y, Bunod J-D, Dong X-H (2021) Effects of microencapsulated organic acid and their salts on growth performance, immunity, and disease resistance of Pacific White Shrimp Litopenaeus vannamei. Sustainability 13:7791

    Article  CAS  Google Scholar 

  • Chuchird N, Rorkwiree P, Rairat T (2015) Effect of dietary formic acid and astaxanthin on the survival and growth of Pacific white shrimp (Litopenaeus vannamei) and their resistance to Vibrio parahaemolyticus. Springerplus 4:440

    Article  PubMed  PubMed Central  Google Scholar 

  • da Silva BC, Vieira FDN, Mourino JLP, Ferreira GS, Seiffert WQ (2013) Salts of organic acids selection by multiple characteristics for marine shrimp nutrition. Aquaculture 384–387:104–110

    Article  Google Scholar 

  • da Silva BC, Vieira FdN, Mourino JLP, Bolivar N, Seiffert WQ (2016) Butyrate and propionate improve the growth performance of Litopenaeus vannamei. Aqua Res 47:612–623

    Article  Google Scholar 

  • Dawood MAO, Koshio S, Esteban MÁ (2018) Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev Aqua 10:950–974

    Article  Google Scholar 

  • Destoumieux D, Muñoz M, Cosseau C, Rodriguez J, Bulet P, Comps M, Bachère E (2000) Penaeidins, antimicrobial peptides with chitin-binding activity, are produced and stored in shrimp granulocytes and released after microbial challenge. Jo Cell Sci 113:461–469

  • Duan YF, Zhang Y, Dong HB, Zheng XT, Wang Y, Li H, Liu Q, Zhang J (2017) Effect of dietary poly-β-hydroxybutyrate (PHB) on growth performance, intestinal health status and body composition of Pacific white shrimp Litopenaeus vannamei (Boone, 1931). Fish Shellfish Immunol 60:520–528

    Article  CAS  PubMed  Google Scholar 

  • Duan Y, Wang Y, Zhang J, Sun Y, Wang J (2018) Dietary effects of succinic acid on the growth, digestive enzymes, immune response and resistance to ammonia stress of Litopenaeus vannamei. Fish Shellfish Immunol 78:10–17

    Article  CAS  PubMed  Google Scholar 

  • Doyle AA, Krämer T, Kavanagh K, Stephens JC (2019) Cinnamaldehydes: synthesis, antibacterial evaluation, and the effect of molecular structure on antibacterial activity. Result Chem 1:100013

    Article  CAS  Google Scholar 

  • Emerenciano MGC, Rombenso AN, Vieira FDN, Martins MA, Coman GJ, Truong HH, Noble TH, Simon CG (2021) Intensification of Penaeid shrimp culture: an applied review of advances in production systems, nutrition and breeding. Animals 12:236

    Article  Google Scholar 

  • El-Sayed AFM (2021) Use of biofloc technology in shrimp aquaculture: a comprehensive review, with emphasis on the last decade. Rev Aqua 13:676–705

    Article  Google Scholar 

  • FAO (Food and Agriculture Organization) (2020) The state of world fisheries and aquaculture 2020. Sustainability in action, Rome. https://doi.org/10.4060/ca9229en

    Book  Google Scholar 

  • Friedman M (2017) Chemistry, antimicrobial mechanisms, and antibiotic activities of cinnamaldehyde against pathogenic bacteria in animal feeds and human foods. J Agric Food Chem 65:10406–10423

    Article  CAS  PubMed  Google Scholar 

  • Ghaffarizadeh A, Sotoudeh E, Mozanzadeh MT, Sanati AM, Ghasemi A (2022) Supplementing dietary selenium nano-particles increased growth, antioxidant capacity and immune-related genes transcription in Pacific whiteleg shrimp (Penaeus vannamei) juveniles. Aqua Rep 25:101215

    Article  Google Scholar 

  • Ghanei-Motlagh R, Mohammadian T, Gharibi D, Khosravi M, Mahmoudi E, Zarea M, El-Matbouli M, Menanteau-Ledouble S (2021) Quorum quenching probiotics modulated digestive enzymes activity, growth performance, gut microflora, haemato-biochemical parameters and resistance against Vibrio harveyi in Asian seabass (Lates calcarifer). Aquaculture 531:735874

    Article  CAS  Google Scholar 

  • Gowder SJ, Devaraj H (2006) Effect of the food flavour cinnamaldehyde on the antioxidant status of rat kidney. Basic Clin Pharmacol Toxicol 99:379–382

    Article  CAS  PubMed  Google Scholar 

  • Habiba MM, Hussein EE, Ashry AM, El-Zayat AM, Hassan AM, El-Shehawi AM, Sewilam H, Van Doan H, Dawood MAO (2021) Dietary cinnamon successfully enhanced the growth performance, growth hormone, antibacterial capacity, and immunity of European Sea Bass (Dicentrarchus labrax). Animals 11:2128. https://doi.org/10.3390/ani11072128

    Article  PubMed  PubMed Central  Google Scholar 

  • Han F, Xu C, Qi C, Lin Z, Li E, Wang C, Wang X, Qin JG, Chen L (2020) Sodium butyrate can improve intestinal integrity and immunity in juvenile Chinese mitten crab (Eriocheir sinensis) fed glycinin. Fish Shellfish Immunol 102:400–411

    Article  CAS  PubMed  Google Scholar 

  • Harada E, Kiriyama H, Kobayashi E, Tsuchita H (1988) Postnatal development of biliary and pancreatic exocrine secretion in piglets. Comp Biochem Physiol 36:843–856

    Google Scholar 

  • He W, Rahimnejad S, Wang L, Song S, Lu K, Zhang C (2017) Effects of organic acids and essential oils blend on growth, gut microbiota, immune response and disease resistance of Pacific white shrimp (Litopenaeus vannamei) against Vibrio parahaemolyticus. Fish Shellfish Immunol 70:164–173

    Article  CAS  PubMed  Google Scholar 

  • Hernández-López J, Gollas-Galván T, Vargas-Albores F (1996) Activation of the prophenoloxidase system of the brown shrimp (Penaeus californiensis Holmes). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 113:61–66

    Article  Google Scholar 

  • Hernandez-Contreras A, Hernandez MD (2020) Application of aromatic plants and their extracts in aquaculture. In: Florou-Paneri P, Christaki E, Giannenas I (eds) Feed additives. Academic Press, Cambridge, Massachusetts, US, pp 239–259

    Chapter  Google Scholar 

  • Hoseinifar SH, Sun YZ, Caipang CM (2017) Short chain fatty acids as feed supplements for sustainable aquaculture: an updated view. Aqua Res 48:1380–1391

    Article  CAS  Google Scholar 

  • Hoseinifar SH, Safari R, Dadar M (2017) Dietary sodium propionate affects mucosal immune parameters, growth and appetite related genes expression: insights from zebrafish model. General Comp Endocrinol 243:78–83

    Article  CAS  Google Scholar 

  • Hsieh TJ, Wang JC, Hu CY, Li CT, Kuo CM, Hsieh SL (2008) Effects of rutin from Toona sinensis on the immune and physiological responses of white shrimp (Litopenaeus vannamei) under Vibrio alginolyticus challenge. Fish Shellfish Immunol 25:581–588

    Article  CAS  PubMed  Google Scholar 

  • Hsieh SL, Wu CC, Liu CH, Lian JL (2013) Effects of the water extract of Gynura bicolor (Roxb. & Willd.) DC on physiological and immune responses to Vibrio alginolyticus infection in white shrimp (Litopenaeus vannamei). Fish Shellfish Immunol 35:18–25

    Article  PubMed  Google Scholar 

  • Iijima N, Tanaka S, Ota Y (1998) Purification and characterization of bile salt activated lipase from the hepatopancreas of red sea bream, Pagrus major. Fish Physiol Biochem 18:59–69

    Article  CAS  Google Scholar 

  • Keyshams P, Mousavi SM, Zakeri M, Kochanian P, Souri M (2021) Effects of different levels of commercial food supplement, Biotronic® Top3 on biochemical and immune parameters of Litopenaeus vannamei. IranVet J 17:33–45

    Google Scholar 

  • Langhout P (2000) New feed additives for broiler chickens. World Poult 16:22–27

    Google Scholar 

  • Liu T, Zhang G, Feng Y, Kong C, Ayisi CL, Huang X, Hua X (2019) Dietary soybean antigen impairs growth and health through stress-induced non-specific immune responses in Pacific white shrimp. Litopenaeus Vannamei Fish Shellfish Immunol 84:124–129

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Qu YK, Geng C, Wang AM, Zhang JH, Chen KJ, Liu B, Tian HY, Yang WP, Yu YB (2020) Effects of hesperidin on the growth performance, antioxidant capacity, immune responses and disease resistance of red swamp crayfish (Procambarus clarkii). Fish Shellfish Immunol 99:154–166

    Article  CAS  PubMed  Google Scholar 

  • Luckstadt C (2008) The use of acidifiers in fish nutrition. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 3:1–8

    Google Scholar 

  • Menanteau-Ledouble S, Krauss I, Goncalves RA, Weber B, El-Matbouli SCA, M, (2017) Antimicrobial effect of the Biotronic® Top3 supplement and efficacy in protecting rainbow trout (Oncorhynchus mykiss) from infection by Aeromonas salmonicida subsp. salmonicida. Res Vet Sci 114:95–100

    Article  CAS  PubMed  Google Scholar 

  • Miandare HK, Mirghaed AT, Hosseini M, Mazloumi N, Zargar A, Nazari S (2017) Dietary Immunogen® modulated digestive enzyme activity and immune gene expression in Litopenaeus vannameipost larvae. Fish Shellfish Immunol 70:621–627

    Article  CAS  PubMed  Google Scholar 

  • Muhlia-Almazan A, Sanchez-Paz A, Garcia-Carreno FL (2008) Invertebrate trypsins: a review. J Comp Physiol B 178:655–672

    Article  PubMed  Google Scholar 

  • Naylor RL, Hardy RW, Buschmann AH, Bush SR, Cao L, Klinger DH, Little DC, Lubchenco J, Shumway SE, Troell M (2021) A 20-year retrospective review of global aquaculture. Nature 591:551–563

    Article  CAS  PubMed  Google Scholar 

  • Ng WK, Koh CB (2017) The utilization and mode of action of organic acids in the feeds of cultured aquatic animals. Rev Aqua 9:342–368

    Article  Google Scholar 

  • Pan LQ, Xiao GQ, Zhang HX, Luan ZH (2005) Effects of different dietary protein content on growth and protease activity of Eriocheir sinensis larvae. Aquaculture 246:313–319

    Article  CAS  Google Scholar 

  • Pereira SA, Oliveira HM, Jesus GFA, Addam KGS, Silva BC, Yamashita MM, Lehmann NB, Martins ML, Mouriño JLP (2018) Can the minerals calcium and sodium, chelated to propionic acid, influence the health and zootechnical parameters of native silver catfish Rhamdia quelen? Aquaculture 496:88–95

    Article  CAS  Google Scholar 

  • Rao PV, Gan SH (2014) Cinnamon: a multifaceted medicinal plant. Evid based complement alternat med 2014:642942. https://doi.org/10.1155/2014/642942

  • Ravardshiri M, Bahram S, Javadian SR, Bahrekazemi M (2021) Cinnamon promotes growth performance, digestive enzyme, blood parameters, and antioxidant activity of rainbow trout (Oncorhynchus mykiss) in low-carbohydrate diets. Turk J Fish Aquat Sci 21:309–322

    Article  Google Scholar 

  • Reverter M, Tapissier‐Bontemps N, Sasal P, Saulnier D (2017) Use of medicinal plants in aquaculture. Diagnosis and control of diseases of fish and shellfish, John Wiley & Sons, Chichester, UK, pp 223–261

  • Reyshahri A, Mohammadiazarm H, Mohammadian T, Mozanzadeh MT (2019) Effects of sodium diformate on growth performance, gut microflora, digestive enzymes and innate immunological parameters of Asian sea bass (Lates calcarifer) juveniles. Aquac Nutr 25:1135–1144

    Article  Google Scholar 

  • Riemensperger AV, Bachinger D, Schaumberger S, Urbaityte R, Pasteiner S (2012) The effect of an organic acid blend, cinnamaldehyde and a permeabilising substance on the inhibition of bacterial growth in vitro and growth performance of weaning pigs. Vet Med Zootech 60:59–66

    Google Scholar 

  • Romano N, Koh CB, Ng WK (2015) Dietary microencapsulated organic acids blend enhances growth, phosphorus utilization, immune response, hepatopancreatic integrity and resistance against Vibrio harveyi in white shrimp, Litopenaeus vannamei. Aquaculture 435:228–236

    Article  CAS  Google Scholar 

  • Rombenso AN, Truong H, Simon C (2020) Dietary butyrate alone or in combination with succinate and fumarate improved survival, feed intake, growth and nutrient retention efficiency of juvenile Penaeus monodon. Aquaculture 528:735492

    Article  CAS  Google Scholar 

  • Romero J, Feijoó CG, Navarrete P (2012) Antibiotics in aquaculture–use, abuse and alternatives. Health and environment in aquaculture 159:159–198

  • Salehi, M., Bagheri, D., Sotoudeh, E. Ghasemi A, Mozanzadeh, MT (2022) The combined effects of propionic acid and a mixture of Bacillus spp. probiotic in a plant protein–rich diet on growth, digestive enzyme activities, antioxidant capacity, and immune-related genes mRNA transcript abundance in Lates calcarifer fry. Probiotic Antimicrob Prot. https://doi.org/10.1007/s12602-021-09902-4

  • Sangari M, Sotoudeh E, Bagheri D, Morammazi S, Mozanzadeh MT (2021) Growth, body composition, and hematology of yellowfin seabream (Acanthopagrus latus) given feeds supplemented with organic acid salts (sodium acetate and sodium propionate). Aqua Int 29:261–273

    Article  CAS  Google Scholar 

  • Saurabh S, Sahoo PK (2008) Lysozyme: an important defense molecule of fish innate immune system. Aqua Res 39:223–239

    Article  CAS  Google Scholar 

  • Schar D, Klein EY, Laxminarayan R, Gilbert M, Van Boeckel TP (2020) Global trends in antimicrobial use in aquaculture. Sci Rep 10:2018–2027

    Article  Google Scholar 

  • Setiawati M, Jusadi D, Laheng S, Suprayudi MA, Vinasyiam A (2016) The enhancement of growth performance and feed efficiency of Asian catfish, Pangasianodon hypophthalmus fed on Cinnamomum burmannii leaf powder and extract as nutritional supplementation. Aqua Conserv Legis 9:1301–1309

    Google Scholar 

  • Silva BC, Nolasco-Soria H, Magallón-Barajas F, Civera-Cerecedo R, Casillas-Hernández R, Seiffert W (2016b) Improved digestion and initial performance of whiteleg shrimp using organc salt supplements. Aqua Nutr 22:997–1005

    Article  CAS  Google Scholar 

  • Silva BC, Jesus GFA, Seiffert WQ, Vieira FN, Mouriño JLP, Jatobá A, Nolasco-Soria H (2016) The effects of dietary supplementation with butyrate and polyhydroxybutyrate on the digestive capacity and intestinal morphology of Pacific white shrimp (Litopenaeus vannamei). Marine Fresh Behav Physiol 49:447–458

    Article  CAS  Google Scholar 

  • Sotoudeh E, Sangari M, Bagheri D, Morammazi S, Mozanzadeh MT (2020) Dietary organic acid salts mitigate plant protein induced inflammatory response and improve humoral immunity, antioxidative status and digestive enzyme activities in yellowfin seabream, Acanthopagrus latus. Aqua Nutr 25:1669–1680

    Article  Google Scholar 

  • Su X, Li X, Leng X, Tan C, Liu B, Chai X, Guo T (2014) The improvement of growth, digestive enzyme activity and disease resistance of white shrimp by the dietary citric acid. Aqua Int 22:1823–1835

    Article  CAS  Google Scholar 

  • Thornber K, Verner-Jeffreys D, Hinchliffe S, Rahman MM, Bass D, Tyler CR (2020) Evaluating antimicrobial resistance in the global shrimp industry. Rev Aqua 12:966–986

    Article  Google Scholar 

  • Tran NT, Li Z, Wang S, Zheng H, Aweya JJ, Wen X, Li S (2018) Progress and perspectives of short-chain fatty acids in aquaculture. Rev Aqua 12:283–298

    Article  Google Scholar 

  • Tzuc TJ, Escalante DR, Herrera RR, Cortés GG, Ortiz MLA (2014) Microbiota from Litopenaeus vannamei: digestive tract microbial community of Pacific white shrimp (Litopenaeus vannamei). Springerplus 3:1–10

    Article  Google Scholar 

  • Vaara M (1992) Agents that increase the permeability of the outer membrane. Microb Rev 56:395–411

    Article  CAS  Google Scholar 

  • Wang W, Sun J, Liu C, Xue Z (2017) Application of immunostimulants in aquaculture: current knowledge and future perspectives. Aqua Res 48:1–23

    Article  Google Scholar 

  • Wang Y, Feng K, Yang H, Zhang Z, Yuan Y, Yue T (2018) Effect of cinnamaldehyde and citral combination on transcriptional profile, growth, oxidative damage and patulin biosynthesis of Penicillium expansum. Front Microbiol 9:597

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Jin J, Liu X, Wang Y, Liu Y, Zhao Y, Xing F (2018) Effect of cinnamaldehyde on morphological alterations of Aspergillus ochraceus and expression of key genes involved in ochratoxin A biosynthesis. Toxins 10:340

    Article  PubMed  PubMed Central  Google Scholar 

  • Wyban J (2019) Selective breeding of Penaeus vannamei: impact on world aquaculture and lessons for future. J Coast Res 86:1–5

    Article  Google Scholar 

  • Yang QO, Duan X, Li L, Tao N (2019) Cinnamaldehyde exerts its antifungal activity by disrupting the cell wall integrity of Geotrichum citri-aurantii. Front Microbiol 10:55

    Article  Google Scholar 

  • Yao W, Li X (2019) Chowdhury, M.A.K.; Wang, J.; Leng, X.-J. Dietary protease, carbohydrase and micro-encapsulated organic acid salts individually or in-combination improved growth, feed utilization and intestinal histology of Pacific white shrimp. Aquaculture 503:88–95

    Article  CAS  Google Scholar 

  • Zahizadeh A, Zakeri M, Mousavi SM, Kochanian P, Souri M (2020) Effect of different levels of dietary Biotronic Top3 on growth performance, feed utilization and body biochemical composition of the white leg shrimp (Litopenaeus vannamei). J Fish 73:515–527 ((In Persian with English abstract))

    Google Scholar 

  • Zhang H, Yi L, Sun R, Zhou H, Xu W, Zhang W, Mai K (2016) Effects of dietary citric acid on growth performance, mineral status and intestinal digestive enzyme activities of large yellow croaker Larimichthys crocea (Richardson, 1846) fed high plant protein diets. Aquaculture 453:147–153

    Article  CAS  Google Scholar 

  • Zhou Y, Jiang W-D, Zhang J-X, Feng L, Wu P, Liu Y, Jiang J, Kuang S-Y, Tang L, Peng Y, Zhou Z, Liu Y, He S, Shi P, Gao X, Yao B, Ringø E (2009) Effects of dietary potassium diformate (KDF) on growth performance, feed conversion and intestinal bacterial community of hybrid tilapia (Oreochromis niloticus × O. aureus). Aquaculture 291:89–94

    Article  CAS  Google Scholar 

  • Zhou X-Q (2020) Cinnamaldehyde improves the growth performance and digestion and absorption capacity in grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 46:1589–1601

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Wang X, Hou L, Jiang X, Li C, Zhang J, Pei C, Zhao X, Li L, Kong X (2021) The related immunity responses of red swamp crayfish (Procambarus clarkii) following infection with Aeromonas veronii. Aqua Rep 21:100849

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

FA: project administration and methodology. ES: conceptualization, methodology, project administration, and supervision. MTM: conceptualization, investigation, validation, interpretation of data, and writing—original draft. AG: project administration and methodology, and supervision.

Corresponding authors

Correspondence to Ebrahim Sotoudeh or Mansour Torfi Mozanzadeh.

Ethics declarations

Ethics approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Conflict of interest

The authors declare no competing interests.

Additional information

Handling editor: Elena Mente

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Afshari, F., Sotoudeh, E., Mozanzadeh, M.T. et al. Dietary mixture of short-chain fatty acids, a phytogenic agent, and a permeabilizer improved growth, antioxidant enzymes, and immunocompetence in whiteleg shrimp juveniles (Penaeus vannamei). Aquacult Int 31, 847–866 (2023). https://doi.org/10.1007/s10499-022-01003-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-022-01003-5

Keywords

Navigation