Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-18T20:42:28.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary probiotic supplementation improves growth and the intestinal morphology of Nile tilapia

Published online by Cambridge University Press:  12 January 2017

M. A. Ramos ,
S. Batista ,
M. A. Pires ,
A. P. Silva ,
L. F. Pereira ,
M. J. Saavedra ,
R. O. A. Ozório  and
P. Rema
M. A. Ramos
Affiliation:
Centro Interdisciplinar de Investigação Marinha e Ambiental (CIMAR/CIIMAR), Rua dos Bragas, 289, 4050-123 Porto, Portugal Instituto Politécnico de Coimbra (IPC), Escola Superior Agrária de Coimbra (ESAC), Bencanta, 3045-601 Coimbra, Portugal Centro de Ciência Animal e Veterinária (CECAV), Universidade de Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal
S. Batista
Affiliation:
Centro Interdisciplinar de Investigação Marinha e Ambiental (CIMAR/CIIMAR), Rua dos Bragas, 289, 4050-123 Porto, Portugal Instituto de Ciências Biomédicas de Abel Salazar (ICBAS), Universidade do Porto, Rua Jorge Viterbo Ferreira n° 228, 4050-313 Porto, Portugal
M. A. Pires
Affiliation:
Centro de Ciência Animal e Veterinária (CECAV), Universidade de Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal
A. P. Silva
Affiliation:
Instituto Politécnico de Coimbra (IPC), Escola Superior Agrária de Coimbra (ESAC), Bencanta, 3045-601 Coimbra, Portugal
L. F. Pereira
Affiliation:
Centro Interdisciplinar de Investigação Marinha e Ambiental (CIMAR/CIIMAR), Rua dos Bragas, 289, 4050-123 Porto, Portugal
M. J. Saavedra
Affiliation:
Centro Interdisciplinar de Investigação Marinha e Ambiental (CIMAR/CIIMAR), Rua dos Bragas, 289, 4050-123 Porto, Portugal Centro de Ciência Animal e Veterinária (CECAV), Universidade de Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal
R. O. A. Ozório
Affiliation:
Centro Interdisciplinar de Investigação Marinha e Ambiental (CIMAR/CIIMAR), Rua dos Bragas, 289, 4050-123 Porto, Portugal Instituto de Ciências Biomédicas de Abel Salazar (ICBAS), Universidade do Porto, Rua Jorge Viterbo Ferreira n° 228, 4050-313 Porto, Portugal
P. Rema*
Affiliation:
Centro de Ciência Animal e Veterinária (CECAV), Universidade de Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal
*
†E-mail: [email protected]
Get access

Abstract

Probiotic administration can be a nutritional strategy to improve the immune response and growth performance of fish. The current study aimed to evaluate the effects of a probiotic blend (Bacillus sp., Pediococcus sp., Enterococcus sp., Lactobacillus sp.) as a dietary supplement on growth performance, feed utilization, innate immune and oxidative stress responses and intestinal morphology in juvenile Nile tilapia (Oreochromis niloticus). The probiotic was incorporated into a basal diet at three concentrations: 0 g/kg (A0: control), 3 g/kg (A1: 1.0×106 colony forming unit (CFU)/g) and 6 g/kg (A2: 2.3×106 CFU/g diet). After 8 weeks of probiotic feeding, weight and specific growth rate where significantly higher in fish-fed A1 diet than in fish-fed A0. Alternative complement in plasma was significantly enhanced in fish-fed A2 when compared with A0. The hepatic antioxidant indicators were not affected by probiotic supplementation. Villi height and goblet cell counts increased significantly in the intestine of fish-fed A1 and A2 diets compared with A0. The dietary probiotic supplementation was maintained until 20 weeks of feeding. Then the selected immune parameters, digestive enzymes and apparent digestibility of diets were studied. No effect of probiotic feeding was observed after that longer period supplementation. The dietary supplementation of mixed species probiotic may constitute a valuable nutritional approach towards a sustainable tilapia aquaculture. The improvement of the immune responses and intestinal morphology play an important role in increasing growth performance, nutrient absorption and disease resistance in fish, important outcomes in such a competitive and developing aquaculture sector.

Keywords

probioticsNile tilapiagrowth rateinnate immune responsesintestinal morphology
Type
Research Article
Information
animal , Volume 11 , Issue 8 , August 2017 , pp. 1259 - 1269
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Balcazar, JL, De Blas, I, Ruiz-Zarzuela, I, Vendrell, D, Calvo, AC, Marquez, I, Girones, O and Muzquiz, JL 2007. Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). British Journal of Nutrition 97, 522–527.Google Scholar
Castex, M, Lemaire, P, Wabete, N and Chim, L 2009. Effect of dietary probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress status of shrimp Litopenaeus stylirostris . Aquaculture 294, 306–313.Google Scholar
Essa, MA, Serafy, SSE, El-Ezabi, MM, Daboor, SM, Esmael, NA and Lall, SP 2010. Effect of different dietary probiotics on growth, feed utilization and digestive enzymes activities of Nile tilapia, Oreochromis niloticus . Journal of the Arabian Aquaculture Society 5, 143–162.Google Scholar
Food and Agriculture Organization 2016. The state of world fisheries and aquaculture 2016: contributing to food security and nutrition for all. FAO of the United Nations, Rome, Italy.Google Scholar
Food and Agriculture Organization/World Health Organization 2002. Guidelines for the evaluation of probiotics in food (Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. London, ON, Canada.Google Scholar
Giannenas, I, Karamaligas, I, Margaroni, M, Pappas, I, Mayer, E, Encarnação, P and Karagouni, E 2015. Effect of dietary incorporation of a multi-strain probiotic on growth performance and health status in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry 41, 119–128.Google Scholar
Giatsis, C, Sipkema, D, Smidt, H, Heilig, H, Benvenuti, G, Verreth, J and Verdegem, M 2015. The impact of rearing environment on the development of gut microbiota in tilapia larvae. Scientific Reports 5, 18206.CrossRefGoogle ScholarPubMed
Gisbert, E, Castillo, M, Skalli, A, Andree, KB and Badiola, I 2013. Bacillus cereus var. toyoi promotes growth, affects the histological organization and microbiota of the intestinal mucosa in rainbow trout fingerlings. Journal of Animal Science 91, 2766–2774.CrossRefGoogle ScholarPubMed
Gravato, C, Teles, M, Oliveira, M and Santos, MA 2006. Oxidative stress, liver biotransformation and genotoxic effects induced by copper in Anguilla anguilla L. – the influence of pre-exposure to b-naphthoflavone. Chemosphere 65, 1821–1830.Google Scholar
Irianto, A and Austin, B 2002. Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25, 333–342.CrossRefGoogle Scholar
Lara-Flores, M, Olvera-Novoa, MA, Guzmán-Méndez, BE and López-Madrid, W 2003. Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216, 193–201.Google Scholar
Lazado, CC and Caipang, CMA 2014. Mucosal immunity and probiotics in fish. Fish & Shellfish Immunology 39, 78–89.Google Scholar
Li, XQ, Zhu, YH, Zhang, HF, Yue, Y, Cai, ZX, Lu, QP, Zhang, L, Weng, XG, Zhang, FJ, Zhou, D, Yang, JC and Wang, JF 2012. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS One 7, e40666.CrossRefGoogle Scholar
Lushchak, VI 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology 101, 13–30.CrossRefGoogle ScholarPubMed
Lutgendorff, F, Nijmeijer, RM, Sandström, PA, Trulsson, LM, Magnusson, K-E, Timmerman, HM, Minnen, LPv, Rijkers, GT, Gooszen, HG, Akkermans, LMA and Söderholm, JD 2009. Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis. PLoS One 4, e4512.Google Scholar
Madsen, K, Cornish, A, Soper, P, McKaigney, C, Jijon, H, Yachimec, C, Doyle, J, Jewell, L and De Simone, C 2001. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121, 580–591.CrossRefGoogle ScholarPubMed
McGuckin, MA, Lindén, SK, Sutton, P and Florin, TH 2011. Mucin dynamics and enteric pathogens. Nature Reviews Microbiology 9, 265–278.CrossRefGoogle ScholarPubMed
Merrifield, DL and Carnevali, O 2014. Probiotic modulation of the gut microbiota of fish. In Aquaculture nutrition: gut health, probiotics and prebiotics (ed. D Merrifield and E Ringø), pp. 185–222. John Wiley & Sons, Ltd, Chichester, UK.Google Scholar
Merrifield, DL and Ringø, E 2014. Aquaculture nutrition: gut health, probiotics and prebiotics. John Wiley & Sons, Ltd, Chichester, UK.Google Scholar
Merrifield, DL, Harper, GM, Dimitroglou, A, Ringø, E and Davies, SJ 2010. Possible influence of probiotic adhesion to intestinal mucosa on the activity and morphology of rainbow trout (Oncorhynchus mykiss) enterocytes. Aquaculture Research 41, 1268–1272.Google Scholar
Ozório, ROA, Kopecka-Pilarczyk, J, Peixoto, MJ, Lochmann, R, Santos, RJ, Santos, G, Weber, B, Calheiros, J, Ferraz-Arruda, L, Vaz-Pires, P and Gonçalves, JFM 2016. Dietary probiotic supplementation in juvenile rainbow trout (Oncorhynchus mykiss) reared under cage culture production: effects on growth, fish welfare, flesh quality and intestinal microbiota. Aquaculture Research 47, 2732–2747.CrossRefGoogle Scholar
Pirarat, N, Pinpimai, K, Endo, M, Katagiri, T, Ponpornpisit, A, Chansue, N and Maita, M 2011. Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Research in Veterinary Science 91, e92–e97.CrossRefGoogle ScholarPubMed
Ramos, MA, Gonçalves, JFM, Batista, S, Costas, B, Pires, MA, Rema, P and Ozório, ROA 2015. Growth, immune responses and intestinal morphology of rainbow trout (Oncorhynchus mykiss) supplemented with commercial probiotics. Fish & Shellfish Immunology 45, 19–26.CrossRefGoogle ScholarPubMed
Ray, AK, Ghosh, K and Ringø, E 2012. Enzyme-producing bacteria isolated from fish gut: a review. Aquaculture Nutrition 18, 465–492.CrossRefGoogle Scholar
Reyes-Becerril, M, Tovar-Ramírez, D, Ascencio-Valle, F, Civera-Cerecedo, R, Gracia-López, V, Barbosa-Solomieu, V and Esteban, MÁ 2011. Effects of dietary supplementation with probiotic live yeast Debaryomyces hansenii on the immune and antioxidant systems of leopard grouper Mycteroperca rosacea infected with Aeromonas hydrophila . Aquaculture Research 42, 1676–1686.CrossRefGoogle Scholar
Ringø, E, Olsen, RE, Mayhew, TM and Myklebust, R 2003. Electron microscopy of the intestinal microflora of fish. Aquaculture 227, 395–415.Google Scholar
Ringø, E, Salinas, I, Olsen, RE, Nyhaug, A, Myklebust, R and Mayhew, TM 2007. Histological changes in intestine of Atlantic salmon (Salmo salar L.) following in vitro exposure to pathogenic and probiotic bacterial strains. Cell & Tissue Research 328, 109–116.Google Scholar
Robertson, PAW, O’Dowd, C, Burrells, C, Williams, P and Austin, B 2000. Use of Carnobacterium sp. as a probiotic for Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss, Walbaum). Aquaculture 185, 235–243.Google Scholar
Standen, BT, Rodiles, A, Peggs, DL, Davies, SJ, Santos, GA and Merrifield, DL 2015. Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Applied Microbiology and Biotechnology 99, 8403–8417.Google Scholar
Standen, BT, Peggs, DL, Rawling, MD, Foey, A, Davies, SJ, Santos, GA and Merrifield, DL 2016. Dietary administration of a commercial mixed-species probiotic improves growth performance and modulates the intestinal immunity of tilapia, Oreochromis niloticus. Fish & Shellfish Immunology 49, 427–435.Google Scholar
Suzer, C, Çoban, D, Kamaci, HO, Saka, Ş, Firat, K, Otgucuoğlu, Ö and Küçüksari, H 2008. Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture 280, 140–145.CrossRefGoogle Scholar
Telli, GS, Ranzani-Paiva, MJT, Dias, DC, Sussel, FR, Ishikawa, CM and Tachibana, L 2014. Dietary administration of Bacillus subtilis on hematology and non-specific immunity of Nile tilapia Oreochromis niloticus raised at different stocking densities. Fish & Shellfish Immunology 39, 305–311.Google Scholar
Thongprajukaew, K, Kovitvadhi, U, Kovitvadhi, S, Somsueb, P and Rungruangsak-Torrissen, K 2011. Effects of different modified diets on growth, digestive enzyme activities and muscle compositions in juvenile Siamese fighting fish (Betta splendens Regan, 1910). Aquaculture 322–323, 1–9.Google Scholar
Verschuere, L, Rombaut, G, Sorgeloos, P and Verstraete, W 2000. Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews 64, 655–671.Google Scholar
Watanabe, WO, Losordo, TM, Fitzsimmons, K and Hanley, F 2002. Tilapia production systems in the Americas: technological advances, trends, and challenges. Reviews in Fisheries Science 10, 465–498.CrossRefGoogle Scholar