Abstract
This study was conducted to investigate the effects of dietary supplementation of a mixture of the glycerol esters of short-chain fatty acids (SCFAs) and medium-chain fatty acids (MCFAs) (short and medium chain fatty acid mixture, SMCFAM) on the growth performance, feed utilization efficiency, innate immunity, diet digestibility, and disease resistance of Pacific white shrimp, Litopenaeus vannamei. A basal diet was prepared (Con) and four other diets were prepared supplementing graded levels of SMCFAM at 0.35, 0.55, 0.70, and 1.10 g kg−1. Quadruplicate groups of shrimp were fed one of the diets for 53 days and then challenged with Vibrio harveyi. Growth performance was significantly improved by SMCFAM supplementation. Innate immunity and antioxidant capacity of shrimp were significantly increased by dietary SMCFAM. Diet digestibility was significantly improved in 0.35 and 0.70 groups than in Con and 1.10 groups. During the challenge test, shrimp fed SMCFAM supplemented diets had higher disease resistance to Vibrio harveyi compared to shrimp fed Con diet. Therefore, these results indicate that dietary supplementation of SMCFAM at low doses less than 1 g kg−1 can improve growth performance, innate immunity, antioxidant capacity, diet digestibility, and disease resistance of shrimp against V. harveyi.
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All datasets analyzed in this study are available from the corresponding author upon reasonable request.
References
Abdelrhman AM, Ashour M, Al-Zahaby MA, Sharawy ZZ, Nazmi H, Zaki MA, Ahmed NH, Ahmed SR, El-Haroun EE, Doan HV, Goda AM (2022) Effect of polysaccharides derived from brown macroalgae Sargassum dentifolium on growth performance, serum biochemical, digestive histology and enzyme activity of hybrid red tilapia. Aquac Rep 25:101212. https://doi.org/10.1016/j.aqrep.2022.101212
Anuta JD, Buentello A, Patnaik S, Lawrence AL, Mustafa A, Hume ME, Gatlin DM III, Kemp MC (2011) Effect of dietary supplementation of acidic calcium sulfate (Vitoxal) on growth, survival, immune response and gut microbiota of the Pacific white shrimp, Litopenaeus vannamei. J World Aquac Soc 42:834–844. https://doi.org/10.1111/j.1749-7345.2011.00519.x
AOAC (1995) Official methods of analysis of AOAC International. AOAC Arling, VA
Baltić B, Starčević M, Dordević J, Mrdović B, Marković R (2017) Importance of medium chain fatty acids in animal nutrition. IOP Conf Ser Earth Environ Sci 85:012048. https://doi.org/10.1088/1755-1315/85/1/012048
Baruah K, Sahu NP, Pal AK, Debnath D, Yengkokpam S, Mukherjee SC (2007) Interactions of dietary microbial phytase, citric acid and crude protein level on mineral utilization by rohu, Labeo rohita (Hamilton), juveniles. J World Aquac Soc 38:238–249. https://doi.org/10.1111/j.1749-7345.2007.00092.x
Beuchat LR (1980) Comparison of anti-Vibrio activities of potassium sorbate, sodium benzoate, and glycerol and sucrose esters of fatty acids. Appl Environ Microbiol 39:1178–1182. https://doi.org/10.1128/aem.39.6.1178-1182.1980
Bui HTD, Khosravi S, Lee C, Kim MG, Lim SJ, Shin CH, Yoo BW, Choi SI, Lee KJ (2017) Supplemental effects of AAMC, an anionic alkali mineral complex, in diets for Pacific white shrimp (Litopenaeus vannamei). Isr J Aquac 69:1–8
Chen WW, Romano N, Ebrahimi M, Natrah I (2017) The effects of dietary fructooligosaccharide on growth, intestinal short chain fatty acids level and hepatopancreatic condition of the giant freshwater prawn (Macrobrachium rosenbergii) post-larvae. Aquac 469:95–101. https://doi.org/10.1016/j.aquaculture.2016.11.034
Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol B Comp Biochem 73:25–41. https://doi.org/10.1016/0305-0491(82)90198-5
Chowdhury MAK, Song H, Liu Y, Bunod JD, Dong XH (2021) Effects of microencapsulated organic acid and their salts on growth performance, immunity, and disease resistance of Pacific white shrimp Litopenaeus vannamei. Sustain 13:7791. https://doi.org/10.3390/su13147791
Defoirdt T, Halet D, Sorgeloos P, Bossier P, Verstraete W (2006) Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. Aquac 261:804–808. https://doi.org/10.1016/j.aquaculture.2006.06.038
Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54:2325–2340. https://doi.org/10.1194/jlr.R036012
Duan Y, Zhang Y, Dong H, Zheng X, 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. https://doi.org/10.1016/j.fsi.2016.11.020
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. https://doi.org/10.1016/j.fsi.2018.04.008
Ellis AE (1990) Serum antiproteases in fish. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, Fair Haven, NJ, pp 95–99
FAO (2020) The state of world fisheries and aquaculture. Sustainability in action, Food and Agriculture Organization of the United Nations
Freitag M (2007) Organic acids and salts promote performance and health in animal husbandry. Acidifiers Anim Nutr 31:131–139
Gunathilaka BE, Veille A, Tharaka K, Shin J, Shin J, Jeong JB, Meallet V, Lee KJ (2021) Evaluation of marine algal (Ulva spp./Solieria spp.) extracts combined with organic acids in diets for olive flounder (Paralichthys olivaceus). Aquac Res 52:3270–3279. https://doi.org/10.1111/are.15172
Han JE, Choi SK, Han SH, Lee SC, Jeon HJ, Lee C, Kim KY, Lee YS, Park SC, Rhee G, Park SY, Kim J, Park S, Kim JH, Lee KJ (2020) Genomic and histopathological characteristics of Vibrio parahaemolyticus isolated from an acute hepatopancreatic necrosis disease outbreak in Pacific white shrimp (Penaeus vannamei) cultured in Korea. Aquac 524:735284. https://doi.org/10.1016/j.aquaculture.2020.735284
Hao YT, Wu SG, Jakovlić I, Zou H, Li WX, Wang GT (2017) Impacts of diet on hindgut microbiota and short-chain fatty acids in grass carp (Ctenopharyngodon idellus). Aquac Res 48:5595–5605. https://doi.org/10.1111/are.13381
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. https://doi.org/10.1016/0742-8413(95)02033-0
Hirazawa N, Oshima SI, Hara T, Mitsuboshi T, Hata K (2001) Antiparasitic effect of medium-chain fatty acids against the ciliate Cryptocaryon irritans infestation in the red sea bream Pagrus major. Aquac 198:219–228. https://doi.org/10.1016/S0044-8486(01)00503-8
Hong SM, Hwang JH, Kim IH (2012) Effect of medium-chain triglyceride (MCT) on growth performance, nutrient digestibility, blood characteristics in weanling pigs. Asian-Australasian J Anim Sci 25:1003. https://doi.org/10.5713/ajas.2011.11402
Hoseinifar SH, Sun YZ, Caipang CM (2017) Short-chain fatty acids as feed supplements for sustainable aquaculture: an updated view. Aquac Res 48:1380–1391. https://doi.org/10.1111/are.13239
Khajepour F, Hosseini SA (2012) Calcium and phosphorus status in juvenile beluga (Huso huso) fed citric acid-supplemented diets. Aquac Res 43:407–411. https://doi.org/10.1111/j.1365-2109.2011.02843.x
Lee C, Shin J, Feyaerts J, Shin J, Kim MG, Gunathilaka BE, Ko D, Jo S, Eom G, Ji S, Jeong J, Lee KJ (2021) Effects of dietary supplementation of monobutyrin and tributyrin on growth, feed efficiency, innate immunity, digestibility and disease resistance of Pacific white shrimp (Litopenaeus vannamei) against Vibrio harveyi. Aquac Nutr 27:771–781. https://doi.org/10.1111/anu.13222
Lückstädt C (2008) The use of acidifiers in fish nutrition. Perspect Agri, Vet Sci, Nutr Nat Resour 3:1–8. https://doi.org/10.1079/PAVSNNR20083044
Lückstädt C, Schulz C (2008) The dietary effects of potassium diformate on the protein and fat digestibility of Atlantic salmon (Salmo salar) reared in sea water. Aquac Europe, Krakow, Poland, pp 391–392
Magouz FI, Essa M, Mansour M, Paray BA, Van Doan H, Dawood MA (2020) Supplementation of AQUAGEST® as a source of medium-chain fatty acids and taurine improved the growth performance, intestinal histomorphology, and immune response of common carp (Cyprinus carpio) fed low fish meal diets. Ann Anim Sci 20:1453–1469. https://doi.org/10.2478/aoas-2020-0016
Mine S, Boopathy R (2011) Effect of organic acids on shrimp pathogen, Vibrio harveyi. Curr Microbiol 63:1–7. https://doi.org/10.1007/s00284-011-9932-2
Moquet PCA, Salami SA, Onrust L, Hendriks WH, Kwakkel RP (2018) Butyrate presence in distinct gastrointestinal tract segments modifies differentially digestive processes and amino acid bioavailability in young broiler chickens. Poult Sci 97:167–176. https://doi.org/10.3382/ps/pex279
Muñoz M, Cedeno R, Rodrı́guez J, Knaap van der WP, Mialhe E, Bachere E (2000) Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquac 191:89–107. https://doi.org/10.1016/S0044-8486(00)00420-8
Ng WK, Koh CB, Teoh CY, Romano N (2015) Farm-raised tiger shrimp, Penaeus monodon, fed commercial feeds with added organic acids showed enhanced nutrient utilization, immune response and resistance to Vibrio harveyi challenge. Aquac 449:69–77. https://doi.org/10.1016/j.aquaculture.2015.02.006
Nordrum S, Krogdahl Å, Røsjø C, Olli JJ, Holm H (2000) Effects of methionine, cysteine and medium chain triglycerides on nutrient digestibility, absorption of amino acids along the intestinal tract and nutrient retention in Atlantic salmon (Salmo salar L.) under pair-feeding regime. Aquac 186:341–360. https://doi.org/10.1016/S0044-8486(99)00385-3
Odle J (1997) New insights into the utilization of medium-chain triglycerides by the neonate: observations from a piglet model. J Nutr 127:1061–1067. https://doi.org/10.1093/jn/127.6.1061
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Pourmozaffar S, Hajimoradloo A, Miandare HK (2017) Dietary effect of apple cider vinegar and propionic acid on immune related transcriptional responses and growth performance in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 60:65–71. https://doi.org/10.1016/j.fsi.2016.11.030
Rahimnejad S, Guardiola FA, Leclercq E, Esteban MÁ, Castex M, Sotoudeh E, Lee SM (2018) Effects of dietary supplementation with Pediococcus acidilactici MA18/5M, galactooligosaccharide and their synbiotic on growth, innate immunity and disease resistance of rockfish (Sebastes schlegeli). Aquac 482:36–44. https://doi.org/10.1016/j.aquaculture.2017.09.020
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. Aquac 435:228–236. https://doi.org/10.1016/j.aquaculture.2014.09.037
Sandamalika WG, Priyathilaka TT, Liyanage DS, Lee S, Lim HK, Lee J (2018) Molecular characterization of kappa class glutathione S-transferase from the disk abalone (Haliotis discus discus) and changes in expression following immune and stress challenges. Fish Shellfish Immunol 77:252–263. https://doi.org/10.1016/j.fsi.2018.03.058
Sarker MSA, Satoh S, Kamata K, Haga Y, Yamamoto Y (2012) Partial replacement of fish meal with plant protein sources using organic acids to practical diets for juvenile yellowtail, Seriola quinqueradiata. Aquac Nutr 18:81–89. https://doi.org/10.1111/j.1365-2095.2011.00880.x
Schönfeld P, Wojtczak L (2016) Short-and medium-chain fatty acids in energy metabolism: the cellular perspective. J Lipid Res 57:943–954. https://doi.org/10.1194/jlr.R067629
Shah SZH, Afzal M, Khan SY, Hussain SM, Habib RZ (2015) Prospects of using citric acid as fish feed supplement. Int J Agric Biol 17:1–8
Silva BC, Vieira FDN, Mouriño JLP, Ferreira GS, Seiffert WQ (2013) Salts of organic acids selection by multiple characteristics for marine shrimp nutrition. Aquac 384:104–110. https://doi.org/10.1016/j.aquaculture.2012.12.017
Silva BC, Jesus GFA, Seiffert WQ, Vieira FN, Mouriño JLP, Jatobá A, Nolasco-Soria H (2016a) The effects of dietary supplementation with butyrate and polyhydroxybutyrate on the digestive capacity and intestinal morphology of Pacific white shrimp (Litopenaeus vannamei). Marine Freshw Behav Physiol 49:447–458. https://doi.org/10.1080/10236244.2016.1257759
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 organic salt supplements. Aquac Nutr 22:997–1005. https://doi.org/10.1111/anu.12315
Silva BC, Vieira FDN, Mouriño JLP, Bolivar N, Seiffert WQ (2016c) Butyrate and propionate improve the growth performance of Litopenaeus vannamei. Aquac Res 47:612–623. https://doi.org/10.1111/are.12520
Sotira S, Dell’Anno M, Caprarulo V, Hejna M, Pirrone F, Callegari ML, Tucci TV, Rossi L (2020) Effects of tributyrin supplementation on growth performance, insulin, blood metabolites and gut microbiota in weaned piglets. Animals 10:726. https://doi.org/10.3390/ani10040726
Sotoudeh E, Sangari M, Bagheri D, Morammazi S, TorfiMozanzadeh M (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. Aquac Nutr 26:1669–1680. https://doi.org/10.1111/anu.13112
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. Aquac Int 22:1823–1835. https://doi.org/10.1007/s10499-014-9785-3
Tacon AGJ, Cody JJ, Conquest LD, Divakaran S, Forster IP, Decamp OE (2002) Effect of culture system on the nutrition and growth performance of Pacific white shrimp Litopenaeus vannamei (Boone) fed different diets. Aquac Nutr 8:121–137. https://doi.org/10.1046/j.1365-2095.2002.00199.x
Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L (2014) The role of short-chain fatty acids in health and disease. Adv Immunol 121:91–119. https://doi.org/10.1016/B978-0-12-800100-4.00003-9
Tran NT, Li Z, Wang S, Zheng H, Aweya JJ, Wen X, Li S (2020) Progress and perspectives of short-chain fatty acids in aquaculture. Rev Aquac 12:283–298. https://doi.org/10.1111/raq.12317
Tumbokon BLM, Serrano AE Jr (2020) Effects of vinegars on the growth performance of black tiger post larvae shrimp, Penaeus monodon. Isr J Aquac Bamid 72:1–8. https://doi.org/10.46989/001c.18993
Ullah S, Zhang J, Xu B, Tegomo AF, Sagada G, Zheng L, Wang L, Shao Q (2022) Effect of dietary supplementation of lauric acid on growth performance, antioxidative capacity, intestinal development and gut microbiota on black sea bream (Acanthopagrus schlegelii). PLoS ONE 17:e0262427. https://doi.org/10.1371/journal.pone.0262427
Vinolo MAR, Rodrigues HG, Nachbar RT, Curi R (2011) Regulation of Inflammation by short chain fatty acids. Nutr 3:858–876. https://doi.org/10.3390/nu3100858
Wang CC, Jiang GZ, Cao XF, Dai YJ, Huang YY, Li XF, Liu WB (2020) Effects of dietary docosahexaenoic acid on growth performance, fatty acid profile and lipogenesis of blunt snout bream (Megalobrama amblycephala). Aquac Nutr 26:502–515. https://doi.org/10.1111/anu.13012
Wang Y, Zhong H, Wang J, Feng F (2021) Dietary glycerol monolaurate improved the growth, activity of digestive enzymes and gut microbiota in zebrafish (Danio rerio). Aquac Rep 20:100670. https://doi.org/10.1016/j.aqrep.2021.100670
Wong JM, De Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clinical Gastroenterol 40:235–243
Yin B, Liu H, Tan B, Dong X, Chi S, Yang Q, Zhang S (2021) Supplementing tributyrin to cottonseed protein concentrate-based diets can improve growth performance, lipid metabolism and distal intestinal immunity in hybrid grouper (Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂). Aquac Nutr 27:2378–2391. https://doi.org/10.1111/anu.13370
Yoon BK, Jackman JA, Valle-González ER, Cho NJ (2018) Antibacterial free fatty acids and monoglycerides: biological activities, experimental testing, and therapeutic applications. Int J Mol Sci 19:1114. https://doi.org/10.3390/ijms19041114
Zentek J, Buchheit-Renko S, Männer K, Pieper R, Vahjen W (2012) Intestinal concentrations of free and encapsulated dietary medium-chain fatty acids and effects on gastric microbial ecology and bacterial metabolic products in the digestive tract of piglets. Archives Anim Nutr 66:14–26. https://doi.org/10.1080/1745039X.2011.644916
Zheng K, Liang M, Yao H, Wang J, Chang Q (2012) Effect of dietary fish protein hydrolysate on growth, feed utilization and IGF-I levels of Japanese flounder (Paralichthys olivaceus). Aquac Nutr 18:297–303. https://doi.org/10.1111/j.1365-2095.2011.00896.x
Zhu D, Yang L, Huang J, Zhou F, Yang Q, Jiang S, Jiang S (2018) The comprehensive expression analysis of the G protein-coupled receptor from Penaeus monodon indicating it participates in innate immunity and anti-ammonia nitrogen stress. Fish Shellfish Immunol 75:17–26. https://doi.org/10.1016/j.fsi.2018.01.019
Funding
This study was supported by Proviron Industries NV, Belgium and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553) and the Korea government (MSIR) (2021R1A2C2008384).
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Jaebeom Shin participated in the feeding trial, sampling, analyses, and manuscript preparation. Julie Feyaerts designed the experiment, reviewed and edited the manuscript, and provided ingredients. Mirasha Hasanthi and Chorong Lee mainly edited the manuscript and analyzed the parameters. Danbi Shin, Yeonji Lee, Jongho Lim, and Han-Se Kim were involved in feeding and sampling the shrimp. Kyeong-Jun Lee organized and supervised the whole study and completed the manuscript.
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The feeding trial protocols were evaluated and approved by the Institutional Animal Care and Use Committee of Jeju National University.
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Shin, J., Feyaerts, J., Hasanthi, M. et al. Evaluation of a mixture of short-chain and medium-chain fatty acid glycerides as a dietary supplement in diets for Pacific white shrimp (Litopenaeus vannamei). Aquacult Int 31, 1483–1498 (2023). https://doi.org/10.1007/s10499-022-01037-9
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DOI: https://doi.org/10.1007/s10499-022-01037-9