Enrichment of Artemia sp. with autochthonous probiotics at different levels in larviculture of piauçu Megaleporinus macrocephalus
Keywords:
Growth performance, Live food, Sanity, Microbiology, PathogenAbstract
The research investigated the effect of dietary supplementation with Artemia sp. enriched with the autochthonous probiotic Enterococcus faecium on growth performance, microbiota modulation, intestinal morphology, and resistance to pathogenic bacteria of Megaleporinus macrocephalus larvae. The study evaluated four treatments (C: without probiotics; T1:1 × 104; T2:1× 106; and T3:1 × 108 CFU·mL-1) in quadruplicates. The larvae (n=160; weight= 5.3 ± 2.3mg and length= 3.73±0.4mm) were distributed in 16 L containers at a density of 10 larvae·L-1 for 20 days. The productive performance, survival, gut microbiology, and histology were measured. The larvae were also submitted to acute challenge against the pathogenic bacterium Aeromonas hydrophila. The results showed that supplementation with 1 × 108 CFU·mL-1 promotes greater gain in length (13.78 ± 0.40 cm) and total weight (0.08 ± 0.002 g), higher counts of lactic acid bacteria and lower total heterotrophic in the intestines (7.11±0.30; 0.12 ± 0.09 log CFU·g-1, respectively) and larger villi (0.26 ± 0.03μm). Diets containing probiotics influenced the animals’ resistance to acute infection, with a lower accumulated mortality in T3 (33% ± 11.54%) and a higher one in C+ (93% ± 11.54%). Thus, probiotic supplementation with the autochthonous bacterium E. faecium (1×108CFU·mL-1) provides zootechnical improvement, villus increase and greater resistance to infections.
References
Abe, H.A.; Dias, J.A.R.; Cordeiro, C.A.M.; Ramos, F.M.; Fujimoto, R.Y. 2015. Pyrrhulina brevis (Steindachner, 1876) como uma nova opção para a piscicultura ornamental nacional: larvicultura. Boletim do Instituto de Pesca, 41(1):113-122.
Allameh, S.K.; Noaman, V.; Nahavandi, R. 2017. Effects of probiotic bacteria on fish performance. Advanced Techniques in Clinical Microbiology, 1(2): 11.
Angeletti, S. 2017. Matrix assisted laser desorption time of flight mass spectrometry (MALDI-TOF MS) in clinical microbiology. Journal of Microbiological Methods, 138:20-29. https://doi.org/10.1016/j.mimet.2016.09.003
Arrieta, M.C.; Stiemsma, L.T.; Amenyogbe, N.; Brown, E.M.; Finlay, B. 2014. The intestinal microbiome in early life: health and disease. Frontiers Immunology, 5: 427. https://doi.org/10.3389/fimmu.2014.00427
Avella, M.A.; Olivotto, I.; Silvi, S.; Place, A.R..; Carnevali, O. 2010. Effect of dietary probiotics on clownfish: a molecular approach to defne how lactic acid bacteria modulate development in a marine fish. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 298(2): R359-R371.https://doi.org/10.1152/ajpregu.00300.2009
Azevedo, R.V.; Fosse-Filho, J.C.; Pereira, S.L.; Andrade, D.R.; Júnior, V.M. 2016. Prebiótico, probiótico esimbiótico para larvas de Trichogaster leeri (Bleeker, 1852, Perciformes, Osphronemidae). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 68(3): 795-804. https://doi.org/10.1590/1678-4162-8580
Barros, F.A.L.; Silva, L.A.; Dias, J.A.R.; Abe, H.A.; Paixão, P.E.G.; Sousa, N.C.; Cordeiro, C.A.M.; Fujimoto, R.Y.2022.In vitro selection of autochthonous bacterium with probiotic potential for the neotropical fish piauçu Megaleporinus macrocephalus. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 74(2): 327-337. https://doi.org/10.1590/1678-4162-12404
Bhaheerathan, J.I.; Saravana, B.P.; Chinnasamy, D.; Thangaraj, M.; Ramasamy, K.; Thirunavukkarasu,M.; Madhayan,K.; Paramasivam, P. 2020. Growth and survival promotion of a probiotic bacteriumEnterococcus durans enriched Artemia nauplii on the prawn Macrobrachium rosenbergii. GSC Biological and Pharmaceutical Sciences, 12(1): 87-101. https://doi.org/10.30574/gscbps.2020.12.1.0201
Chauhan, A.; Singh, R. 2019. Probiotics in aquaculture: a promising emerging alternative approach. Symbiosis, 77: 99-113. https://doi.org/10.1007/s13199-018-0580-1
Chung, H.; Pamp, S.J.; Hill, J.A.; Surana, N.K.; Edelman, S.M.; Troy, E.B.; Reading, N.C.; Villablanca, E.J.; Wang, S.; Mora, J.R.; Umesaki, Y.; Mathis, D.; Benoist, C.; Relman, D.A.; Kasper, D.L. 2012. Gut Immune Maturation Depends on Colonization with a Host-Specific Microbiota. Cell, 149(7): 1578-1593. https://doi.org/10.1016/j.cell.2012.04.037
Comabella, Y.; Hernández Franyutti, A.; Hurtado, A.; Canabal, J.; García-Galano, T. 2013. Ontogenetic development of the digestive tract in Cuban gar (Atractosteus tristoechus) larvae. Reviews in Fish Biology and Fisheries, 23: 245-260. https://doi.org/10.1007/s11160-012-9289-z
Deng, Y.; Verdegem, M.C.; Eding, E.; Kokou, F. 2022. Effect of rearing systems and dietary probiotic supplementation on the growth and gut microbiota of Nile tilapia (Oreochromis niloticus) larvae. Aquaculture, 546: 737297. https://doi.org/10.1016/j.aquaculture.2021.737297
Dias, J.A.R.; Abe, H.A.; Sousa, N.C.; Couto, M.V.; Cordeiro, C.A.; Meneses, J.O.; Fujimoto, R.Y. 2018. Dietarysupplementation with autochthonous Bacillus cereus improves growth performance and survival in tambaqui Colossoma macropomum. Aquaculture Research, 49(9):3063-3070.https://doi.org/10.1111/are.13767
Dias, J.A.R.; Abe, H.A.; Sousa, N.C.; Silva, R.D.F.; Cordeiro, C.A.M.; Gomes, G.F.E.; Ready, J.S.; Mouriño, J.L.P.; Martins, M.L.; Carneiro, P.C.F.; Maria, N.A.; Fujimoto, R.Y. 2019. Enterococcus faecium as potential probiotic for ornamental neotropical cichlid fish, Pterophyllum scalare (Schultze, 1823). Aquaculture Inernational, 27: 463-474.https://doi.org/10.1007/s10499-019-00339-9
Dias, J.A.R.; Alves, L.L.; Barros, F.A.L.; Cordeiro, C.A.M.; Meneses, J.O.; Santos, T.B. R.; Santos, C.C-M.; Paixão, P.E.G.; Filho, R.M.N.; Martins, M.L.; Pereira, S.A.; Mouriño, J.L.P.; Diniz, L.E.C.; Maria, A.N.; Carneiro, P.C.F.; Fujimoto R.Y. 2022. Comparative effects of autochthonous single-strain and multi-strain probiotics on the productive performance and disease resistance in Colossoma macropomum (Cuvier,1818). Aquaculture Research, 53(11): 4141-4154. https://doi.org/10.1111/are.15916
Evans, A.S. 1976. Causation and disease: the Henle-Koch postulates revisited. The Yale Journal of Biology and Medicine, 49(2): 175-195.
Ghoname, R.M.; El-Sayed, H.S.; Ghozlan, H.A.; Sabry, S.A. 2020. Application of probiotic bacteria for the improvement of sea bream (Sparus aurata) larval production. Egyptian Journal of Aquatic Biology and Fisheries, 24(1): 371-398. https://doi.org/10.21608/EJABF.2020.70859
Ghorbani Vaghei, R.; Shenavar Masouleh, A.R.; Alipour, A.R.; Yeganeh, H. 2019. Effects of Artemia nauplii enrichment with a bacterial species (Weissiella koreensis) on growth performance and survival rate of stellate sturgeon larvae (Acipenser stellatus). Journal of Survey Fisheries Science, 5(2): 1-10. https://10.18331/SFS2019.5.2.1
Gonçalves Júnior, L.P.; Pereira, S.L.; Matielo, M.D.; Mendonça, P.P. 2013. Efeito da densidade de estocagem no desenvolvimento inicial do acará-bandeira (Pterophyllum scalare). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 65(4): 1176-1182. https://doi.org/10.1590/S0102-09352013000400033
He, S.; Ran, C.; Qin, C.; Li, S.; Zhang, H.; de Vos, W.M.; Ringo, E.; Zhou, Z. 2017. Anti-infective effect of adhesive probiotic Lactobacillus in fish is correlated with their spatial distribution in the intestinal tissue. Scientific Reports, 7: 13195. https://doi.org/10.1038/s41598-017-13466-1
Hoseinifar, S.H.; Sun, Y.Z.; Wang, A.; Zhou, Z. 2018. Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Frontiers in Microbiology, 9: 2429. https://doi.org/10.3389/fmicb.2018.02429
Hossain, M.K.; Ishak, S.D.; Iehata, S., Noordiyana, M.N.; Kader, M.A.; Abol-Munafi, A.B. 2022. Effect of intestinal autochthonous Enterococcus faecalis on the growth performance, gut morphology of Malaysian mahseer (Tor tambroides) and protection against Aeromonas hydrophila. International Aquatic Research, 14(1): 1-12 https://doi.org/10.22034/IAR.2022.1945276.1213
Ina-Salwany, M.Y.; Al-saari, N.; Mohamad, A.; Mursidi, F.A.; Mohd-Aris, A.; Amal, M.N.A.; Kasai, H.; Mino, S.; Sawabe. T.; Zamri-Saad, M. 2019. Vibriosis in fish: a review on disease development and prevention. Journal of Aquatic Animal Health, 31(1): 3-22. https://doi.org/10.1002/aah.10045
Jatobá, A.; Jesus, G.F. 2022. Autochthonous and allochthonous lactic acid bacteria: action on the hematological and intestinal microbiota for two species of Astyanax genus. Anais da Academia Brasileira de Ciências, 94(Suppl. 4): e20201611. https://doi.org/10.1590/0001-3765202220201611
Jatobá, A.; Pereira, M.O.; Rodhermel, J.C.B. 2020. Hematological profile of Astyanax bimaculatus underdifferent offer of Lactobacillus sp. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 72(3): 871-878. https://doi.org/10.1590/1678-4162-10832
Jatobá, A.; Vieira, F.D.N.; Neto, C.B.; Silva, B.C.; Mourino, J.L.P.; Jeronimo, G.T.; Dotta, G.; Martins, M.L. 2008. Lactic-acid bacteria isolated from the intestinal tract of Nile tilapia utilized as probiotic. Pesquisa Agropecuária Brasileira, 43(9): 1201-1207. https://doi.org/10.1590/S0100-204X2008000900015
Jomori, R.K.; Luz, R.K.; Takata, R.; Fabregat, T.E.H.P.; Portella, M.C. 2013. Água levemente salinizada aumenta a eficiência da larvicultura de peixes neotropicais. Pesquisa Agropecuária Brasileira, 48(8): 809-815. https://doi.org/10.1590/S0100-204X2013000800001
Khalkhali, S.; Mojgani, N. 2017. Enterococcus faecium; a suitable probiotic candidate for modulation of immune responses against pathogens. International Journal of Basic Science in Medicine, 2(2): 77-82. https://doi.org/10.15171/ijbsm.2017.15
Le Cren, E.D. 1951. The length–weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). Journal of Animal Ecology, 20(2): 201-219. https://doi.org/10.2307/1540
Li, X.; Ringø, E.; Hoseinifar, S.H.; Lauzon, H.L.; Birkbeck, H.; Yang, D. 2019. The adherence and colonization of microorganisms in fish gastrointestinal tract. Reviews in Aquaculture, 11(3): 603-618. https://doi.org/10.1111/raq.12248
Lima, K.S.; Santos Cipriano, F.; Oliveira Júnior, F.M.; Tonini, W.C.T.; Souza, R.H.B.; Simões, I.G.P.C.; Braga, L.G.T. 2015. Performance and hematological variables of piavuçu whose diets were supplemented with phytobiotic and probiotic additives. Semina: Ciências Agrárias, 36(4): 2881-2891. https://doi.org/10.5433/1679-0359.2015v36n4p2881
Lobo, C.; Martín, M.V.; Moreno-Ventas, X.; Tapia-Paniagua, S.T.; Rodríguez, C.; Moriñigo, M.A.; La Banda, I.G. 2018. Shewanella putrefaciens Pdp11 probiotic supplementation as enhancer of Artemia n-3 HUFA contents and growth performance in Senegalese sole larviculture. Aquaculture Nutrition, 24(1): 548-561. https://doi.org/10.1111/anu.12587
Masduki, F.; Zakaria, T.; Min, C.C.; Karim, M. 2020. Evaluation of Enterococcus hirae LAB3 as potential probiont against Vibrio harveyi in Artemia nauplii and Asian seabass larvae (Lates calcarifer) cultures. Journal Environmental Biology, 41(5): 1153-1159. https://doi.org/10.22438/jeb/41/5(SI)/MS_06
Moraes, A.V.; Pereira, M.; Moraes, K.N.; Rodrigues-Soares, J.P.; Jesus, G.F.A.; Jatobá, A. 2018. Autochthonous probiotic as growth promoter and immunomodulator for Astyanax bimaculatus cultured in water recirculation system. Aquaculture Research, 49(8): 2808-2814. https://doi.org/10.1111/are.13743
Mouriño, J.L.P.; Vieira, F.N.; Jatobá, A.; Silva, B.C.; Pereira, G.V.; Jesus, G.F.A.; Ushizima, T.T.; Seiffert, W.Q.;
Martins, M.L. 2017. Symbiotic supplementation on the hemato-immunological parameters and survivalof the hybrid surubim after challenge with Aeromonas hydrophila. Aquaculture Nutrition, 23(2): 276-284. https://doi.org/10.1111/anu.12390
Nikapitiya, C.; Dananjaya, S.H.S.; Silva, B.C.J.; Heo, G.J.; Oh, C.; Zoysa, M.; Lee, J. 2018. Chitosan nanoparticles: A positive immune response modulator as display in zebrafish larvae against Aeromonas hydrophila infection. Fish & Shellfish Immunology, 76: 240-246. https://doi.org/10.1016/j.fsi.2018.03.010
Oliveira, F.C.; Kasai, R.Y.D.; Fernandes, C.U.; Souza, W.S.; Campos, C.M. 2022. Probiotic, prebiotic and synbiotics supplementation on growth performance and intestinal histomorphometryPseudoplatystoma reticulatum larvae. Journal of Applied Aquaculture, 34(2): 279-293. https://doi.org/10.1080/10454438.2020.1841060
Pereira, T.S.B.; Boscolo, C.N.P.; Batlouni, S.R., 2020. Use of 17β-estradiol for Leporinus macrocephalus feminization. Boletim do Instituto de Pesca, 46(2): e547.https://doi.org/10.20950/16782305.2020.46.2.547
Poolsawat, L.; Li, X.; He, M.; Ji, D.; Leng, X. 2019. Clostridium butyricum as probiotic for promoting growth performance, feed utilization, gut health and microbiota community of tilapia (Oreochromis niloticus × O. aureus). Aquaculture Nutrition, 26(3): 657-670. https://doi.org/10.1111/anu.13025
Pramod, P.K.; Ramachandran, A.; Sajeevan, T.P.; Thampy, S.; Pai, S.S., 2010. Comparative efficacy of MS-222 and benzocaine as anaesthetics under simulated transport conditions of a tropical ornamental fish Puntius filamentosus (Valenciennes). Aquaculture Research, 41(2): 309-314.https://doi.org/10.1111/j.1365-2109.2009.02333.x
Ramirez, J.L.; Birindelli, J.L.O.; Galetti, P. 2017. A new genus of Anostomidae (Ostariophysi: Characiformes): Diversity, phylogeny and biogeography based on cytogenetic, molecular and morphological data. Molecular Phylogenetics and Evolution, 107: 308-323. https://doi.org/10.1016/j.ympev.2016.11.012
Ringø, E.; Van Doan, H.; Lee, S.H.; Soltani, M.; Hoseinifar, S.H.; Harikrishnan, R.; Song, S.K. 2020. Probiotics, lactic acid bacteria and bacilli: interesting supplementation for aquaculture. Journal of Applied Microbiology, 129(1):116-136. https://doi.org/10.1111/jam.14628
Samat, N.A.; Yusoff, F.M.; Rasdi, N.W.; Karim, M. 2021. The Efficacy of Moina micrura Enriched with Probiotic Bacillus pocheonensis in Enhancing Survival and Disease Resistance of Red Hybrid Tilapia (Oreochromis spp.) Larvae. Antibiotics, 10(8): 989. https://doi.org/10.3390/antibiotics10080989
Silva, D.M.; Valente, L.M.P.; Sousa-Pinto, I.; Pereira, R.; Pires, M.A.; Seixas, F.; Rema, P. 2015. Evaluation of IMTA- produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. Journal of Applied Phycology, 27: 1671-1680. https://doi.org/10.1007/s10811-014-0453-9
Soares Junior, M.S.; Caliari, M.; Pereira, D.E.P. 2013. Effect of soybean inclusion in extruded rations on performance of juvenile Piavuçu (Leporinus macrocephalus L.). Ciência Animal Brasileira, 14(4): 399-405. https://doi.org/10.5216/cab.v14I4.15834
Sousa, N.C.; Couto, M.V.S.; Abe, H.A.; Paixão, P.E.G.; Cordeiro, C.A.M.; Lopes, E.M.; Ready, J.R.; Jesus, G.F.A.; Martins, M.L.; Mouriño, J.L.P.; Carneiro, P.F.; Maria, A.N.; Fujimoto, R.Y. 2019. Effects of an Enterococcus faecium based probiotic on growth performance and health of Pirarucu, Arapaima gigas. Aquaculture Research, 50(12): 3720-3728. https://doi.org/10.1111/are.14332
Sousa, N.C.; Silva, J.A.; Lopes, E.M.; Santos, A.F.L.; Barros, F.A.B.; Cordeiro, C.A.M.; Paixão, P.E.G; Santos Medeiros, E.; Souza, J.C.N.; Couto, M.V.S. 2020. Enriched Artemia Nauplii with Commercial Probiotic in the Larviculture of Angelfish Pterophyllum scalare Lichtenstein (1823). Journal of Fisheries Science, 2(1): 17-21. https://doi.org/10.30564/jfsr.v2i1.1569
Stephens, W.Z.; Burns, A.R.; Stagaman, K.; Wong, S.; Rawls, J.F.; Guillemin, K.; Bohannan, B.J. 2016. The composition of the zebrafish intestinal microbial community varies across development. Journal ISME, 10: 644-654. https://doi.org/10.1038/ismej.2015.140
Standen, B.T.;Peggs, D.L.; Rawling, M.D.;Foey, A.; Davies, S.J.; Santos, G.A.; Merrifield, D.L. 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. https://doi. org/10.1016/j.fsi.2015.11.037
Sun, Y.Z.; Yang, H.L.; Huang, K.P.; Ye, J.D.; Zhang, C.X. 2013. Application of autochthonous Bacillus bioencapsulated in copepod to grouper Epinephelus coioides larvae. Aquaculture, 392-395: 44-50. https://doi.org/10.1016/j.aquaculture.2013.01.037
Suphoronski, S.A.; Souza, F.P.; Chideroli, R.T.; Mantovani Favero, L.; Ferrari, N.A.; Ziemniczak, H.M.; Gonçalves, D.D.; Lopera Barrero, N.M.; Pereira, U.P. 2021. Effect of Enterococcus faecium as a Water and/or Feed Additive on the Gut Microbiota, Hematologic and Immunological Parameters, and Resistance Against Francisellosis and Streptococcosis in Nile Tilapia (Oreochromis niloticus). Frontiers in Microbiology, 12: 743957. https://doi.org/10.3389/fmicb.2021.743957
Tataje, D.R.; Zaniboni-Filho, E. 2010. Cultivo de piapara, piauçu, piava e piau: gênero Leporinus. In: Baldisserotto. B.; Gomes, L.C. (Eds.). Espécies nativas para piscicultura no Brasil. Santa Maria, Editora UFSM, pp. 73-99.
Tavares-Dias, M.; Moraes, F.R.; Imoto, M.E. 2008. Hematological parameters in two neotropical freshwater teleost, Leporinus macrocephalus (Anostomidae) and Prochilodus lineatus (Prochilodontidae). Bioscience Journal, 24(3): 96-101. Urdaci, M.; Pinchuk I. 2004. Antimicrobial activity ofBacillus probiotics-bacterial spore formers. In: Ricca, E.; Henriques, A.O.; Cutting, S.M. (Eds.). Bacterial spore formers: Probiotics and emerging applications. Norfolk, Horizon Bioscience, pp. 171-182.
Vázquez-Silva, G.; Castro-Mejía, J.J.; Sánchez de la Concha, B.; González-Vázquez, R.; Mayorga-Reyes, L.; Azaola-Espinosa, A. 2016. Bioencapsulation of Bifidobacterium animalis and Lactobacillus johnsonii in Artemia franciscana as feed for charal (Chirostoma jordani) larvae. Revista Mexicana de Ingeniería Química, 15(3): 809-818.
Vieira, F.N.; Jatobá, A.; Mouriño, J.L.P.; Vieira, E.A.; Soares, M.; Silva, B.C.; Seiffert, W.Q.; Martins, M.L.; Vinatea, L.A. 2013. In vitro selection of bacteria with potential for use as probiotics in marine shrimp culture. Pesquisa Agropecuária Brasileira, 48(8): 998-1004. https://doi. org/10.1590/S0100204X2013000800027
Yamashita, M.M.; Ferrarezi, J.V.; Pereira, G.V.; Júnior, G.B.; Silva, B.C.; Pereira, S.A.; Martins, M.L.; Mouriño, J.L.P. 2020. Autochthonous vs allochthonous probiotic strains to Rhamdia quelen. Microbial Pathogenesis, 139: 103897. https://doi.org/10.1016/j.micpath.2019.103897
Yeganeh Rastekenari, H.; Kazami, R.; Shenavar Masouleh, A.; Banavreh, A.; Saltanat Lashgari, S.N.; Hassani, M.H.S.; Vaghei, R.G.; Roudposhti, M.A.; Hallajian, A. 2021. Lactococcus lactis and Weissella confusa in the diet of fingerlings great sturgeon, Huso huso: effects on growth performance, feed efficiency, haematological parameters, immune status and intestinal morphology. AquacultureResearch, 52(8): 3687-3695. https://doi.org/10.1111/are.15213
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Francisco Alex Lima Barros; Joel Artur Rodrigues Dias; Higo Andrade Abe, Keber Santos Costa Júnior, Natalino da Costa Sousa, Cordeiro, C.A.M., Rodrigo Yudi Fujimoto
This work is licensed under a Creative Commons Attribution 4.0 International License.
