Abstract
Probiotic supplementation in fish aquaculture has significantly increased in the last decade due to its beneficial effect on fish performance. Probiotic use at early stages of fish development may contribute to better face metamorphosis and weaning stress. In the present work, we studied the influence of Shewanella putrefaciens Pdp11 supplementation on growth, body composition and gut microbiota in Senegalese sole (Solea senegalensis) during larval and weaning development. S. putrefaciens Pdp11 was incorporated using Artemia as live vector (2.5 × 107 cfu mL−1) and supplied to sole specimens in a co-feeding regime (10–86 DAH) by triplicate. Probiotic addition promoted early metamorphosis and a significantly higher growth in length at 24 DAH larvae. S. putrefaciens Pdp11 also modulated gut microbiota and significantly increased protein content and DHA/EPA ratios in sole fry (90 DAH). This nutritional enhancement is considered especially important after weaning, where significantly higher growth in length and weight was observed in probiotic fish. Moreover, a less heterogeneous fish size in length was detected since metamorphosis till the end of weaning, being of interest for sole aquaculture production. After weaning, fish showed significantly higher growth (length and weight) and less variable lengths in fish when supplemented with probiotics. Both the enhancement of nutritional condition and the decrease in size variability associated with probiotic addition are highly interesting for sole aquaculture production.
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Abelli L, Randelli E, Carnevali O, Picchietti S (2009) Stimulation of gut immune system by early administration of probiotic strains in Dicentrarchus labrax and Sparus aurata. Ann N Y Acad Sci 1163:340–342
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Alves TT, Cerqueira VR, Brown JA (2006) Early weaning of fat snook (Centropomus parallelus, Poey 1864) larvae. Aquaculture 253:334–342
Alves-Martins D, Engrola S, Morais S, Bandarra N, Coutinho J, Yúfera M, Conceicao LEC (2011) Cortisol response to air exposure in Solea senegalensis post-larvae is affected by dietary arachidonic acid to eicosapentaenoic acid ratio. Fish Physiol Biochem 37(4):733–743
Andersen NG, Alsted NS (1993) Growth and body composition of turbot (Scophthalmus maximus (L.)) in relation to different lipid/protein ratios in the diet. In: Kaushik SJ, Luquet P (eds) Fish nutrition in practice. INRA Editions, Paris
Avella MA, Olivotto I, Silvi S, Place AR, Carnevali O (2010a) Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol 298(2):359–371
Avella MA, Gioacchini G, Decamp O, Makridis P, Bracciatelli C, Carnevali O (2010b) Application of multi-species of Bacillus in sea bream larviculture. Aquaculture 305:12–19
Avella MA, Olivotto I, Silvi S, Ribecco C, Cresci A, Palermo F, Polzonetti A, Carnevali O (2011) Use of Enterococcus faecium to improve common sole (Solea solea) larviculture. Aquaculture 315:384–393
Baskerville-Bridges B, Kling LJ (2000) Early weaning of Atlantic cod (Gadus morhua) larvae onto a microparticulate diet. Aquaculture 189:109–117
Bell JG, McEvoy LA, Estévez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Physiol Pharm 37:911–917
Borges P, Oliveira B, Casal S, Dias J, Conceicao LEC, Valente LMP (2009) Dietary lipid level affects growth performance and nutrient utilization of Senegalese sole (Solea senegalensis) juveniles. Brit J Nutr 102:1007–1010
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
Bromley PJ (1980) The effect of dietary water content and feeding rate on the growth and food conversion efficiency of turbot (Scophthalmus maximus L.). Aquaculture 20:91–99
Brunvold L, Sandaa RA, Mikkelsen H, Welde E, Bleie H, Bergh O (2007) Characterization of bacterial communities associated with early stages of intensively reared cod (Gadus morhua) using denaturing gradient gel electrophoresis (DGGE). Aquaculture 272:319–327
Campbell AC, Buswell JA (1983) The intestinal microflora of farmed Dover sole (Solea solea) at different stages of fish development. J Appl Microbiol 55:215–223
Cañavate JP, Fernández-Díaz C (1999) Influence of co-feeding larvae with live and inert diets on weaning the sole Solea senegalensis onto commercial dry feeds. Aquaculture 174:255–263
Carnevali O, Zamponi MC, Sulpizio R, Rollo A, Nardi M, Orpianesi C, Silvi S, Caggiano M, Polzonetti AM, Cresci A (2004) Administration of probiotic strain to improve sea bream wellness during development. Aquacult Int 12:377–386
Carnevali O, de Vivo L, Sulpizio R, Gioacchini G, Olivotto I, Silvi S, Cresci A (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax, L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture 258:430–438
Carter CG, Purser GJ, Houlihan DF, Thomas P (1996) The effect of decreased ration on feeding hierarchies in groups of greenback flounder (Rhombosolea tapirina: teleostei). J Mar Biol Assoc UK 76:505–516
Castell JD, Bell JG, Tocher DR, Sargent KJR (1994) Effects of purified diets containing different combinations of arachidonic and docosahexaenoic acid on survival growth and fatty acid composition of juvenile turbot (Scophthalmus maximus). Aquaculture 128:315–333
Castro-Cunha MC, Rodrigues P, Soares F, Makridis P, Skjermo J, Dinis MT (2003) Development of the immune system and use of immunostimulants in Senegalese sole (Solea senegalensis). The big fish bang. In: Proceedings of 26th annual larval fish conference, pp 189–192
Chabrillón M, Rico RM, Arijo S, Diaz-Rosales P, Balebona MC, Moriñigo MA (2005a) Interactions of microorganisms isolated from gilthead sea bream, Sparus aurata L., on Vibrio harveyi, a pathogen of farmed Senegalese sole, Solea senegalensis (Kaup). J Fish Dis 28:531–537
Chabrillón M, Rico RM, Balebona MC, Moriñigo MA (2005b) Adhesion to sole, Solea senegalensis Kaup, mucus of microorganisms isolated from farmed fish, and their interaction with Photobacterium damselae subsp. piscicida. J Fish Dis 28:229–237
Conceicao LEC, Van der Meeren T, Verreth JAJ, Evjen MS, Houlihan DF, Fyhn HJ (1997) Amino acid metabolism and protein turnover in larval turbot (Scophthalmus maximus) fed natural zooplankton or Artemia. Mar Biol 129:255–265
Conceicao LEC, Ribeiro L, Engrola S, Aragao C, Morais S, Lacuisse M, Soares F, Dinis MT (2007) Nutritional physiology during development of Senegalese sole (Solea senegalensis). Aquaculture 268:64–81
Conceicao LEC, Yúfera M, Morais S, Dinis MT (2010) Live feeds for early stages of fish rearing. Aquacult Res 41:613–640
D’Agostino A (1980) The vital requirements of Artemia: physiology and nutrition. In: Persoone G, Sorgeloos P, Roels I, Jaspers E (eds) The brine shrimp Artemia ecology, culture, use in aquaculture. Universa Press, Wetteren
Dámaso-Rodrígues ML, Pousao-Ferreira P, Ribeiro L, Coutinho J, Bandarra NM, Gavaia N, Morais S (2010) Lack of essential fatty acids in live feed during larval and post-larval rearing: effect on the performance of juvenile Solea senegalensis. Aquacult Int 18:741–757
Decamp O, Makridis P, Qi Z, Xin N, Moriarty DJW, Sorgeloos P, Lavens P (2006) Performance of selected Bacillus probiotics in marine fish culture. Internat Aquafeed Sept–Oct:16–18
Díaz-Rosales P, Arijo S, Chabrillón M, Alarcón FJ, Tapia-Paniagua ST, Martínez-Manzanares E, Balebona MC, Moriñigo MA (2009) Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Solea senegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 293:16–21
Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Güroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production—a Mediterranean perspective. Fish Shellfish Inmun 30:1–16
Dinis MT, Reis J, Arrobas I (1996) Evaluation of the farming potential of Solea senegalensis Kaup, 1858, a new species for aquaculture in the Mediterranean area. Abstracts world aquaculture 1996, Bangkok (Thailand): 107–109
Douillet P (1987) Effect of bacteria on the nutrition of the brine shrimp Artemia fed on dried diets. In: Sorgeloos P, Bengtson DA, Decleir W, Jaspers E (eds) Artemia research and applications—ecology, culturing, use in aquaculture. Universa Press, Wetteren
El-Haroun ER, Goda AMAS, Kabir Chowdhury MA (2006) Effect of dietary probiotic Biogen supplementation as a growth promoter on growth performance and feed utilization of Nile tilapia Oreochromis niloticus (L.). Aquacult Res 37:1473–1480
Engrola S (2008) Improving growth performance of Senegalese sole postlarvae. PhD thesis, Algarve University, Faro, Portugal, 167 pp
Engrola S, Conceicao LEC, Gavaia PJ, Cancela ML, Dinis MT (2005) Effects of pre-weaning feeding frequency on growth, survival and deformation of senegalese sole, Solea senegalensis (Kaup, 1858). Isr J Aquac Bamidgeh 57(1):10–18
Engrola S, Conceicao LEC, Dias L, Pereira R, Ribeiro L, Dinis MT (2007) Improving weaning strategies for Senegalese sole: effects of body weight and digestive capacity. Aquacult Res 38:696–707
Engrola S, Figueira L, Conceicao LEC, Gavaia PJ, Ribeiro L, Dinis MT (2009) Co-feeding in Senegalese sole larvae with inert diet from mouth opening promotes growth at weaning. Aquaculture 288:264–272
Faramarzi M, Jafayran H, Farahi A, Boloki ML, Iranshahi F (2011) The effects on growth and survival of probiotic Bacillus spp. fed to persian sturgeon (Acipenser persicus) larvae. Aquac Aquar Conserv Legislat 4(1):10–14
Fernández-Díaz C, Yúfera M, Cañavate JP, Moyano FJ, Alarcón FJ, Díaz M (2001) Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J Fish Biol 58:1086–1097
Fernández-Reiriz MJ, Pérez-Camacho A, Ferreiro MJ, Blanco J, Planas M, Campos MJ, Labarta U (1989) Biomass production and variation in the biochemical profile (total protein, carbohydrates, RNA, lipids and fatty acids) of seven species of marine microalgae. Aquaculture 83:17–37
Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGGE) fingerprinting patterns. Environ Microbiol 4:634–643
Gamboa-Delgado J, Cañavate JP, Zerolo R, Vay LL (2008) Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis). Aquaculture 280:190–197
García de la Banda I, Chereguini O, Rasines I (1992) Influence of lactic bacterial additives on turbot (Scophthalmus maximus L.) larvae culture. Bol Inst Esp Oceanogr 8:247–254
García de la Banda I, Lobo C, Leon-Rubio JM, Tapia-Paniagua S, Balebona MC, Moriñigo MA, Moreno-Ventas X, Lucas LM, Linares F, Arce F, Arijo S (2010) Influence of two closely related probiotics on juvenile Senegalese sole (Solea senegalensis, Kaup 1858) performance and protection against Photobacterium damselae subsp. piscicida. Aquaculture 306:281–288
García de la Banda I, Lobo C, Chabrillón M, León-Rubio JM, Arijo S, Pazos G, Lucas LM, Moriñigo MA (2012) Influence of dietary administration of a probiotic on Senegalese sole (Solea senegalensis, Kaup, 1858) on growth, body composition and resistance to Photobacterium damselae subsp. piscicida. Aquacult Res 43(5):662–669
Garrido D, Suau A, Pochart P, Cruchet S, Gotteland M (2005) Modulation of the fecal microbiota by the intake of a Lactobacillus johnsonii La1-containing product in human volunteers. FEMS Microbiol Lett 248:249–256
Gatesoupe FJ (1991) The effect of three strains of lactic bacteria on the production rate of rotifers, Brachionus plicatilis, and their dietary value for larval turbot, Scophthalmus maximus. Aquaculture 96:335–342
Gatesoupe FJ, Arakawa T, Watanabe T (1989) The effect of bacterial additives on the production rate and dietary value of rotifers as food for Japanese flounder, Paralichthys olivaceus. Aquaculture 83:39–44
Gavlik S, Albino M, Specker JL (2002) Metamorphosis in summer flounder: manipulation of thyroid status to synchronize settling behavior, growth and development. Aquaculture 203:359–373
Ghosh S, Sinha A, Sahu C (2007) Dietary probiotic supplementation in growth and health live-bearing ornamental fishes. Aquacult Nutr 14:289–299
Gómez-Gil B, Roque A, Turnbull JF (2000) The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture 191:259–270
Gorospe J, Nakamura K (1996) Associated bacterial microflora in Artemia-rice bran culture. Isr J Aquac Bamidgeh 48(2):99–107
Grisez L, Reyners J, Verdonck L, Swings J, Ollevier F (1997) Dominant intestinal microflora of sea bream and sea bass larvae, from two hatcheries, during larval development. Aquaculture 155(1–4):387–399
Hjelm M, Bergh O, Riaza A, Nielsen J, Melchiorsen J, Jensen S, Duncan H, Ahrens P, Birbeck H, Gram L (2004) Selection and identification of autochthonous potential probiotic bacteria from turbot larvae (Scophthalmus maximus) rearing units. Syst Appl Microbiol 27:360–371
Huys L, Dhert P, Robles R, Ollevier F, Sorgeloos P, Swings J (2001) Search for beneficial bacterial strains for turbot (Scophthalmus maximus L.) larviculture. Aquaculture 193:25–37
Imsland AK, Foss A, Conceicao LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fisher 13:379–408
Izquierdo MS (1999) Essential fatty acid requirements of cultured marine fish larvae. Aquacult Nutr 2:183–191
Jobling M (1983) Effect of feeding frequency on food intake and growth of Artic charr, Salvelinus alpinus L. J Fish Biol 23:177–185
Jobling M, Wandsvik A (1983) Effect of social interactions on growth rates and conversion efficiency of Artic charr, Salvelinus alpinus L. J Fish Biol 22:577–584
Kim D-H, Austin B (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Inmun 21:513–524
Klaren PHM, Wunderink Y, Yúfera M, Mancera KM, Flik G (2008) The thyroid gland and thyroid hormones in Senegalese sole (Solea senegalensis) during early development and metamorphosis. Gen Comp Endocr 155:686–694
Kostantinov SR, Zhu W-Y, Williams BA, Tamminga S, de Vos WM, Akkermans ADL (2003) Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiol Ecol 43:225–235
Koven WM, Henderson RJ, Sargent JR (1994) Lipid digestion in turbot (Scophthalmus maximus) I: lipid class and fatty acid composition of digesta from different segments of the digestive tract. Fish Physiol Biochem 13:69–79
Lauzon HL, Gudmundsdottir S, Steinarsson A, Oddgeirsson M, Petursdottir SK, Reynisson E, Bjornsdottir R, Gudmundsdottir BK (2010) Effects of bacterial treatment at early stages of Atlantic cod (Gadus morhua, L.) on larval survival and development. J Appl Microbiol 108:624–632
Lee SM, Cho SH, Kim DJ (2000) Effects of feeding frequency and dietary energy level on growth and body composition of juvenile flounder, Paralichthys olivaceus (Temminck & Schlegel). Aquacult Res 31:917–921
Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 27:114–120
Lund I, Steenfeldt SJ, Hansen BW (2007) Effect of dietary arachidonic acid, eicosapentaenoic acid and docosahexaenoic acid on survival, growth and pigmentation in larvae of common sole (Solea solea L.). Aquaculture 273:532–544
Lund I, Steenfeldt SJ, Banta G, Hansen BW (2008) The influence of dietary concentrations of arachidonic acid and eicosapentaenoic acid at various stages of larval ontogeny on eye migration, pigmentation and prostaglandin content of common sole larvae (Solea solea L.). Aquaculture 276:143–153
Mahmood S, Paton GI, Prosser JJ (2005) Cultivation-independent in situ molecular analysis of bacteria involved in degradation of pentachlorophenol in soil. Environm Microbiol 7:1349–1360
Mai MG, Engrola S, Morais S, Portella MC, Verani JR, Dinis MT, Conceicao LEC (2009) Co-feeding of live feed and inert diet from first-feeding affects Artemia lipid digestibility and retention in Senegalese sole (Solea senegalensis) larvae. Aquaculture 296:284–291
Makridis P, Martins S, Reis J, Dinis MT (2008) Use of probiotic bacteria in the rearing of Senegalese sole (Solea senegalensis) larvae. Aquacult Res 39:627–634
Mandiki SNM, Milla S, Wang N, Blanchard G, Djonkack T, Tanascaux S, Kestemont P (2011) Effects of probiotic bacteria on growth parameters and immune defence in Eurasian perch Perca fluviatilis L. larvae under intensive culture conditions. Aquacult Res 42:693–703
Martín-Antonio B, Manchado M, Infante C, Zerolo R, Labella A, Alonso C, Borrego JJ (2007) Intestinal microbiota variation in Senegalese sole (Solea senegalensis) under different feeding regimes. Aquacult Res 38:1213–1222
Martínez G, Shaw EM, Carrillo M, Zanuy S (1998) Protein salting-out method applied to genomic DNA isolation from fish whole blood Biotechniques Protein salting-out method applied to genomic DNA isolation from fish whole blood. Biotechniques 24:238–239
McIntosh D, Baijing J, Forward BS, Puvanendran V, Boyce D, Ritchie R (2008) Culture-independent characterization of the bacterial populations associated with cod (Gadus morhua L.) and live feed at an experimental hatchery facility using denaturing gradient gel electrophoresis. Aquaculture 275:42–50
Merrifield DL, Burnard D, Bradley G, Davies SJ, Baker RTM (2009) Microbial community diversity associated with the intestinal mucosa of farmed rainbow trout (Oncorynchus mykiss Walbaum). Aquacult Res 40:1064–1072
Morais S, Narciso L, Dores E, Pousao-Ferreira P (2004) Lipid enrichment for Senegalese sole (Solea senegalensis) larvae: effect on larval growth, survival and fatty acid profile. Aquacult Int 12:281–298
Morais S, Koven W, Ronnestad I, Dinis MT, Conceicao LEC (2005) Dietary protein/lipid ratio affects growth and amino acid and fatty acid absorption and metabolism in Senegalese sole (Solea senegalensis Kaup, 1858) larvae. Aquaculture 246:347–357
Muyzer G, Waal ECD, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Nubel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16s rRNAs in Paenibacillus polymixa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643
Overton JL, Steenfeldt SJ, Pedersen PB (2010) The effects of grading on the growth and survival of juvenile Dover sole (Solea solea L.). Aquacult Res 42:31–39
Parra G, Yúfera M (1999) Tolerance response to ammonia and nitrite exposure in larvae of two marine fish species (gilthead seabream Sparus aurata L. and Senegal sole Solea senegalensis Kaup). Aquacult Res 30:857–863
Parra G, Yúfera M (2002) Tolerance response to water pH in larvae of two marine fish species, gilthead seabream, Sparus aurata (L.) and Senegal sole, Solea senegalensis (Kaup), during development. Aquacult Res 33:747–752
Planas M, Pérez-Lorenzo M, Hjelm M, Gram L, Fiksdal IU, Bergh O, Pintado J (2006) Probiotic effect in vivo of Roseobacter strain 27-4 against Vibrio (Listonella) anguillarum infections in turbot (Scophthalmus maximus L.) larvae. Aquaculture 255:323–333
Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. P Natl Acad Sci USA 101:4596–4601
Reitan KI, Rainuzzo JR, Olsen Y (1994) Influence of lipid composition of live feed on growth, survival and pigmentation of turbot larvae. Aquacult Int 2:33–48
Ribeiro L, Zambonino-Infante JL, Cahu C, Dinis MT (2002) Digestive enzymes profile of Solea senegalensis post larvae fed Artemia and a compound diet. Fish Physiol Biochem 27:61–69
Ribeiro L, Engrola S, Dinis MT (2005) Weaning of Senegalese sole (Solea senegalensis) postlarvae to an inert diet with a co-feeding regime. Cienc Marin 31(2):327–337
Ringo E, Birkbeck TH (1999) Intestinal microflora in fish larvae and fry. Aquacult Res 30:73–93
Ringo E, Sinclair PD, Birkbeck H, Barbour A (1992) Production of eicosapentaenoic Acid (20:5n-3) by Vibrio pelagius isolated from turbot (Scophthalmus maximus (L.)) Larvae. Appl Environ Microbiol 58:3777–3778
Rodiles A, Hachero-Cruzado I, Herrera M, Cañavate JP, Alarcón FJ (2008) Studies on the utilization of dietary protein and energy in juvenile Senegalese sole. Abstracts IV Internat Sole Workshop, Faro, pp 22–23
Rodríguez C, Pérez JA, James-Henderson R (2002) The esterification and modification of n-3 and n-6 polyunsaturated fatty acids by hepatocytes and liver microsomes of turbot (Scophthalmus maximus). Comp Biochem Phys B 132:559–570
Rodríguez C, Lorenzo A, Martín V (2009) Nutrición lipídica, in OESA, CSIC, MARM (Eds). La nutrición y la alimentación en piscicultura, Madrid
Rosenlund G, Stoss J, Talbot C (1997) Co-feeding marine fish larvae with inert and live diets. Aquaculture 155:183–191
Rueda-Jasso RA, Conceicao LEC, Coen WD, Rees JF, Sorgeloos P (2005) Diet and weaning age affect the growth and condition of Dover sole (Solea solea L.). Cienc Marin 31(3):477–489
Sáenz de Rodrigáñez MA, Díaz-Rosales P, Chabrillón M, Smidt H, Arijo S, Rubio JML, Alarcón FJ, Balebona MC, Moriñigo MA, Cara JB, Moyano FJ (2009) Effect of dietary administration of probiotics on growth and intestine functionality of juvenile Senegalese sole (Solea senegalensis, Kaup 1858). Aquacult Nutr 15:177–185
Salinas I, Díaz-Rosales P, Cuesta A, Meseguer J, Chabrillón M, Moriñigo MA, Esteban MA (2006) Effect of heat-inactivated fish and non-fish derived probiotics on the innate immune parameters of a teleost fish (Sparus aurata L.). Vet Immunol 111:279–286
Sambrook J, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Sanguinetti CJ, Neto ED, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914–921
Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press New York, New York, pp 181–257
Segner H, Rosch R, Verreth J, Witt U (1993) Larval nutritional physiology: studies with Clarias gariepinus, Coregonus lavaretus and Scophthalmus maximus. J World Aquacult Soc 24:121–134
Sokal R, Rohlf J (1981) Biometry, 2nd edn. WH Freeman and Company, New York (USA)
Stottrup JG, McEvoy LA (2003) Live feeds in marine aquaculture. Blackwell Science, Oxford
Sun YZ, Yang HL, Huang KP, Ye JD, Zhang CX (2013) Application of autochthonous Bacillus bioencapsulated in copepod Epinephelus coioides larvae. Aquaculture 392–395:44–50
Suzer C, Coban D, Kamaci HO, Saka S, Firat K, Otgucuoglu O, Kucuksari 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
Tannock GW, Munro K, Bibiloni R, Simon MA, Hargreaves P, Gopal P, Harmsen H, Welling G (2004) Impact of consumption of oligosaccharide-containing biscuits on the fecal microbiota in humans. Appl Environm Microbiol 70:2129–2136
Tapia-Paniagua ST, Díaz-Rosales P, León-Rubio JM, García de la Banda I, Lobo C, Alarcón FJ, Chabrillón M, Rosas-Ledesma P, Varela JL, Ruíz-Jarabo I, Mancera JM (1858) Use of the probiotic S. putrefaciens Pdp11 on the culture of Senegalese sole (Solea senegalensis, Kaup and gilthead seabream (Sparus aurata, L.). Aquacult Int 20(6):1025–1039
Tapia-Paniagua S, Chabrillon M, Rosales PD, García de la Banda I, Lobo C, Balebona MC, Moriñigo MA (2010) Intestinal microbiota diversity of the flat fish Solea senegalensis (Kaup, 1858) following probiotic administration. FEMS Microbiol Ecol 60:310–319
Tapia-Paniagua S, Lobo C, García de la Banda I, Balebona MC, Moriñigo MA (2011) Impact of the intestinal microbiota species of Senegalese sole larvae and fries fed with Shewanella putrefaciens Pdp11 probiotic bioencapsulated in Artemia, effect of one or two intervals of application. In CD: Abstracts Aquaculture Europe2011. Rhodes, Greece, pp 622–623
Tinh NTN, Dierckens K, Sorgeloos P, Bossier P (2008) A review of the functionality of probiotics in the larviculture. Food Chain Mar Biotechnol 10(1):1–12
Tocher DR (2003) Metabolism and functions of lipids and Fatty acids in teleost. Rev Fish Sci 11:107–184
Tourna M, Freitag TE, Prosser JI (2010) Stable isotope probing analysis of interactions between ammonia oxidizers. Appl Environm Microbiol 76:2468–2477
Vadstein O (1997) The use of immunostimulation in marine larviculture: possibilities and challenges. Aquaculture 155:401–417
Varela JL, Ruíz-Jarabo I, Vargas-Chacoff L, Arijo S, León-Rubio JM, García-Millán I, Martín del Río MP, Moriñigo MA, Mancera JM (2010) Dietary administration of probiotic Pdp11 promotes growth and improves stress tolerance to high stocking density in gilthead seabream Sparus auratus. Aquaculture 309:265–271
Villalta M (2007) Requerimientos nutricionales en ácidos grasos esenciales y organogénesis de la larva del lenguado senegalés, Solea senegalensis (Kaup, 1858). PhD thesis, Barcelona Autónoma University, Barcelona, Spain, 317 pp
Vine NG, Leukes WD, Kaiser H (2006) Probiotics in marine larviculture. FEMS Microbiol Rev 30:404–427
Vizcaíno-Ochoa V, Lazo JP, Barón-Sevilla B, Drawbridge MA (2010) The effect of dietary docosahexaenoic acid (DHA) on growth, survival and pigmentation of California halibut Paralichthys californicus larvae (Ayres, 1810). Aquaculture 302:228–234
Watanabe T, Kiron V (1994) Prospects in larval fish dietetics. Aquaculture 124:223–251
Zacarías-Soto M, Lazo JP, Viana MT (2011) Effect of three probiotics administered through live feed on digestive enzyme activity in California halibut, Paralichthys californicus, larvae. J World Aquacult Soc 42:321–331
Zarza C, Padrós F (2008) An overview of diseases of farmed sole. Abstracts IV Internat Sole Workshop, Faro, Portugal, 15pp
Zarza C, Padrós F, Estévez A, Crespo S, Furones MD (2003). New fish species for aquaculture, old pathological problems: the case of Solea sp. In: Proceedings of 11th European association of fish pathologists, Saint Julians, Malta
Acknowledgments
This study was funded by Spanish National Development Plan for Sole farming (JACUMAR) and the Ministry of Science and Technology (AGL2008-05119-C02-02 and AGL 2011-30381-C03-02). The authors wish to acknowledge the assistance of the Spanish Oceanography Institute staff and especially that of Cristina Rodríguez. We are also grateful to the EULEN/FERROSER employees and especially to Javier Revilla for their assistance. Covadonga Rodríguez belongs to the Institute of Biomedical Technologies (ITB) of the Canary Islands.
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Lobo, C., Moreno-Ventas, X., Tapia-Paniagua, S. et al. Dietary probiotic supplementation (Shewanella putrefaciens Pdp11) modulates gut microbiota and promotes growth and condition in Senegalese sole larviculture. Fish Physiol Biochem 40, 295–309 (2014). https://doi.org/10.1007/s10695-013-9844-0
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DOI: https://doi.org/10.1007/s10695-013-9844-0