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Development of Digestive Enzymes in California Halibut Paralichthys californicus Larvae

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Abstract

California halibut Paralichthys californicus is an important commercial species with high aquaculture potential in Baja California Sur, México. To optimize the feeding process using live prey and/or inert diets, we evaluated alkaline proteases, pepsin, trypsin, chymotrypsin, leucine aminopeptidase, lipase, α-amylase, and acid and alkaline phosphatase activities on starved larvae and larvae fed live prey. Highest activities were observed for alkaline protease, trypsin, chymotrypsin, leucine aminopeptidase, and alkaline phosphatase in feeding larvae than starved larvae on day 4 after hatching. At day 5, a sizeable increase in all enzymatic activities was detected in feeding larvae. Alkaline protease, trypsin, chymotrypsin, and alkaline phosphatase decreases progressively from day 5 until day 18. At day 18, a slight pepsin activity was observed. This was considered an indicator of the start of digestive system maturation. We concluded that total enzymatic equipment for this species is complete between day 18 and 30 after hatching. Based on this evidence, early weaning from live prey to inert feed would be possible at this time.

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References

  • F.J. Alarcón (1997) Procesos digestivos en peces marinos: Caracterización y aplicaciones prácticas Universidad de Almería Spain

    Google Scholar 

  • M.L. Anson (1938) ArticleTitleThe estimation of pepsin, trypsin, papain and cathepsin with hemoglobin J. Gen. Physiol. 22 79–89 Occurrence Handle10.1085/jgp.22.1.79 Occurrence Handle1:CAS:528:DyaA1cXmsFCjtA%3D%3D Occurrence Handle19873094

    Article  CAS  PubMed  Google Scholar 

  • S.L. Applebaum G.J. Holt (2003) ArticleTitleThe digestive protease, chymotrypsin, as an indicator of nutritional condition in larval red drum (Sciaenops ocellatus) Mar. Biol. 142 1159–1167 Occurrence Handle1:CAS:528:DC%2BD3sXjvFCltrw%3D

    CAS  Google Scholar 

  • C. Beccaria J.P. Díaz R. Connes B. Chatain (1991) ArticleTitleOrganogenesis of the exocrine pancreas in the sea bass, Dicentrarchus labrax L., reared extensively and intensively Aquaculture 99 339–354 Occurrence Handle10.1016/0044-8486(91)90254-5

    Article  Google Scholar 

  • Bergmeyer, H.V. 1974. Methods of Enzymatic Analysis. Phosphatases. Vol. 2. Verlag Chemie. Academic Press. Inc.

  • M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein dye binding Anal. Biochem. 72 248–254 Occurrence Handle10.1016/0003-2697(76)90527-3 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051

    Article  CAS  PubMed  Google Scholar 

  • V. Buchet J.L. Zambonino-Infante C.L. Cahu (2000) ArticleTitleEffect of lipid level in a compound diet on the development of red drum Sciaenops ocellatus larvae Aquaculture 184 339–347 Occurrence Handle10.1016/S0044-8486(99)00325-7 Occurrence Handle1:CAS:528:DC%2BD3cXit1Wjtro%3D

    Article  CAS  Google Scholar 

  • V. Buchet J.L. Zambonino Infante C. Cahu (1997) Variation in activities of some digestive enzymes during larval development of Scianops ocellatus L. Creswell Y. Harache (Eds) Island Aquaculture and Tropical Aquaculture, 4–9 Mai 1997, Les Trois Ilets, Martinique European Aquaculture Society Oostende, Belgium 55–56

    Google Scholar 

  • B. Cara F.J. Moyano S. Cárdenas C. Fernández-Díaz M. Yúfera (2003) ArticleTitleAssesment of digestive enzyme activities during larval development of white bream J. Fish Biol. 63 48–58 Occurrence Handle10.1046/j.1095-8649.2003.00120.x Occurrence Handle1:CAS:528:DC%2BD3sXntVygt7Y%3D

    Article  CAS  Google Scholar 

  • J. Clark K.R. Murray J.R. Stark (1986) ArticleTitleProtease development in dover sole (Solea solea (L) Aquaculture 53 253–262 Occurrence Handle10.1016/0044-8486(86)90355-8 Occurrence Handle1:CAS:528:DyaL28XksFyhsb8%3D

    Article  CAS  Google Scholar 

  • D.E. Conklin R.H. Piedrahita G. Merino J.B. Muguet D. Bush E. Gisbert J. Rounds M. Cervantes-Trujano (2003) ArticleTitleDevelopment of California halibut, Paralichthys californicus, culture J. Appl. Aquacult. 14 143–154

    Google Scholar 

  • J.B.C. Cousin F. Baudin-Laurencin J. Gabaudan (1987) ArticleTitleOntogeny of enzymatic activities in fed and fasting turbot, Scophthalmus maximus L Fish Biol. 30 15–33 Occurrence Handle1:CAS:528:DyaL2sXhslehurw%3D

    CAS  Google Scholar 

  • A. Cuvier Péres P. Kestemont (2002) ArticleTitleDevelopment of some digestive enzymes in Eurasian perch larvae Perca fluviatilis Fish Physiol. Biochem. 24 279–285

    Google Scholar 

  • E.G. DelMar C. Largman J.W. Brodrick M.C. Geokas (1979) ArticleTitleA sensitive new substrate for chymotrypsin Anal. Biochem. 99 316–20 Occurrence Handle10.1016/S0003-2697(79)80013-5 Occurrence Handle1:CAS:528:DyaL3cXltlyrtg%3D%3D Occurrence Handle574722

    Article  CAS  PubMed  Google Scholar 

  • M. Díaz F.J. Moyano L.F. García-Carreño F.J. Alarcón M.C. Sarasquete (1997) ArticleTitleSubstrate-SDS-PAGE determination of protease activity through larval development in sea bream Aquacult. Int. 5 461–471

    Google Scholar 

  • B. Erlanger N. Kokowsky W. Cohen (1961) ArticleTitleThe preparation and properties of two new chromogenic substrates of trypsin Arch. Biochem. Biophys. 95 271–278 Occurrence Handle10.1016/0003-9861(61)90145-X Occurrence Handle1:CAS:528:DyaF38XkslOmtg%3D%3D Occurrence Handle13890599

    Article  CAS  PubMed  Google Scholar 

  • A. Gawlicka B. Parent M.H. Horn N. Ross I. Opstad O.J. Torrinsen (2000) ArticleTitleActivity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding Aquaculture 184 303–314 Occurrence Handle10.1016/S0044-8486(99)00322-1 Occurrence Handle1:CAS:528:DC%2BD3cXit1Wjtrw%3D

    Article  CAS  Google Scholar 

  • A. Gawlicka C.T. Leggiadro J.W. Gallart S.E. Douglas (2001) ArticleTitleCellular expression of the pepsinogen and gastric proton pump genes in the stomach of winter flounder as determined by in situ hybridization J. Fish Biol. 58 529–536 Occurrence Handle1:CAS:528:DC%2BD3MXht1aqsb4%3D

    CAS  Google Scholar 

  • E. Gisbert R.H. Piedrahita D.E. Conklin (2004a) ArticleTitleOntogenic development of the digestive system in California halibut (Paralichthys californicus) with notes in feeding practices Aquaculture 232 455–470 Occurrence Handle10.1016/S0044-8486(03)00457-5

    Article  Google Scholar 

  • E. Gisbert D.E. Conklin R.H. Piedrahita (2004b) ArticleTitleEffects of delayed first feeding on the nutritional condition and mortality of California halibut larvae J. Fish Biol. 64 116–132 Occurrence Handle10.1111/j.1095-8649.2004.00289.x

    Article  Google Scholar 

  • E. Gisbert J.B. Muguet D.E. Bush G.E. Merino R.H. Piedrahita D.E. Conklin (2005) ArticleTitleCalifornia halibut larviculture: a step toward the intensive culture of a promising species World Aquaculture 36 31–35

    Google Scholar 

  • S.Z. Herzka D.E. Conklin R. Piedrahita M. Drawbridge J. Fodrie J.P. Lazo (2003) ArticleTitleUS–Mexico cooperative efforts in California halibut research Bight Bull. 7 4–7

    Google Scholar 

  • G.J. Holt (1993) ArticleTitleFeeding larval red drum on microparticulate diets in a closed recirculating water system J. World Aquacult. Soc. 24 225–230

    Google Scholar 

  • M.S. Izquierdo R.J. Henderson (1998) ArticleTitleThe determination of lipase and phospholipase activities in gut contents of turbot (Scophthalmus maximus) by fluorescence-based assays Fish Physiol. Biochem. 19 153–162 Occurrence Handle10.1023/A:1007734425931 Occurrence Handle1:CAS:528:DyaK1MXjtVeiu7k%3D

    Article  CAS  Google Scholar 

  • M.S. Izquierdo J. Socorro L. Arantzamendi C.M. Hernández-Cruz (2000) ArticleTitleRecent advances in lipid nutrition in fish larvae Fish Physiol. Biochem. 22 97–107 Occurrence Handle10.1023/A:1007810506259 Occurrence Handle1:CAS:528:DC%2BD3cXjtVensro%3D

    Article  CAS  Google Scholar 

  • T. Kurokawa T. Suzuki (1996) ArticleTitleFormation of a diffuse pancreas and the development of digestive enzymes synthesis in larvae of Japanese flounder Paralichthys olivaceus Aquaculture 141 267–276 Occurrence Handle10.1016/0044-8486(95)01237-0 Occurrence Handle1:CAS:528:DyaK28XkslSiurw%3D

    Article  CAS  Google Scholar 

  • J.P. Lazo M.T. Dinis G.J. Holt C. Faulk C.R. Arnold (2000) ArticleTitleCo-feeding microparticulate diets with algae: toward eliminating the need of zooplankton at first feeding in larval red drum Sciaenops ocellatus Aquaculture 188 339–351 Occurrence Handle10.1016/S0044-8486(00)00339-2

    Article  Google Scholar 

  • P. Ma B. Sivaloganathan P.K. Reddy W.K. Chan T.J. Lam (2001) ArticleTitleOntogeny of a-amylase gene expression in sea bass larvae (Lates calcarifer) Mar. Biotechnol. 3 463–469 Occurrence Handle10.1007/s10126-001-0018-1 Occurrence Handle1:CAS:528:DC%2BD3MXpt1SgsL4%3D Occurrence Handle14961339

    Article  CAS  PubMed  Google Scholar 

  • S. Morais C. Cahu J. Zambonino-Infante J. Robin I. Rønnestad M.T. Dinis L.E.C. Conceiçao (2004) ArticleTitleDietary TAG source level affect performance and lipase expression in larval sea bass (Dicentrarchus labrax) Lipids 39 449–458 Occurrence Handle1:CAS:528:DC%2BD2cXnvFeitro%3D Occurrence Handle15506240

    CAS  PubMed  Google Scholar 

  • S. Maraux D. Louvard J. Baratti (1973) ArticleTitleThe aminopeptidase from hog-intestinal brush border Biochim. Biophys. Acta 321 282–295

    Google Scholar 

  • I. Martínez F.J. Moyano C. Fernández-Díaz M. Yúfera (1999) ArticleTitleDigestive enzyme activity during larval development of the Senegal sole (Solea senegalensis) Fish Physiol. Biochem. 21 317–323 Occurrence Handle10.1023/A:1007802708459

    Article  Google Scholar 

  • F.J. Moyano M. Díaz F.J. Alarcón M.C. Sarasquete (1996) ArticleTitleCharacterization of digestive enzyme activity during development of gilthead seabream (Sparus aurata) Fish Physiol. Biochem. 15 121–130 Occurrence Handle10.1007/BF01875591 Occurrence Handle1:CAS:528:DyaK28XkvVCqs7k%3D

    Article  CAS  Google Scholar 

  • J.R. Munilla-Morán R. Stark A. Barbour (1990) ArticleTitleThe role of exogenous enzymes in the digestion in culture of turbot larvae (Scophthalmus maximus L) Aquaculture 88 337–350

    Google Scholar 

  • S. Ozkizilcik F.-L.E. Chu A.R. Place (1996) ArticleTitleOntogenetic changes of lipolytic enzymes in Striped bass (Morone saxatilis) Comp. Biochem. Physiol. 113 631–637

    Google Scholar 

  • L. Ribeiro J.L. Zambonino-Infante C.L. Cahu M.T. Dinis (1999) ArticleTitleDevelopment of digestive enzymes in larvae of Solea senegalensis, Kaup 1858 Aquaculture 170 465–473

    Google Scholar 

  • L. Ribeiro J.L. Zambonino Infante C. Cahu M.T. Dinis (2002) ArticleTitleDigestive enzymes profile of Solea senegalensis post larvae fed Artemia and a compound diet Fish Physiol. Biochem. 27 61–69 Occurrence Handle10.1023/B:FISH.0000021817.98363.47 Occurrence Handle1:CAS:528:DC%2BD2cXisVyqtro%3D

    Article  CAS  Google Scholar 

  • C.R. Rojas-Garcia I. Rønnestad B. Ueberschär (2001) ArticleTitleCombined sensitive analytical methods for cholecystokinin levels and tryptic activity in individual fish larvae J. Exp. Mar. Biol. Ecol. 265 101–115 Occurrence Handle1:CAS:528:DC%2BD3MXotlyrs70%3D Occurrence Handle10.1016/S1095-6433(01)00305-1

    Article  CAS  Google Scholar 

  • M.C. Sarasquete A. Polo M.L. Conzález de Canales (1993) ArticleTitleA histochemical and immnohistochemical study of digestive enzymes and hormones during the larval development of Sparus aurata L Histochem. J. 24 337–344

    Google Scholar 

  • A.S. Srivastava T. Kurokawa T. Suzuki (2002) ArticleTitlemRNA expresión of pancreatic enzyme precursors and estimation of protein digestibility in first feeding larvae of Japanese flounder Paralichthys olivaceus Comp. Biochem. Physiol. 132 629–635

    Google Scholar 

  • Ueberschär, B. 1993. Measurement of proteolytic enzyme activity: significance and application in larval fish research. In: Physiological and Biochemical Aspects of Fish Development. Edited by B.T. Walther and H.J. Fuhn. University of Bergen, Norway.

  • F. Vega-Villasante H. Nolasco-Soria R. Civera-Cerecedo (1993) ArticleTitleThe digestive enzymes of the Pacific brown shrimp (Penaeus californiensis) I. Properties of amylase activity on digestive tract Comp. Biochem. Physiol. 112 123–129

    Google Scholar 

  • W.K. Versaw S.L. Cuppett D.D. Winters L.E. Williams (1989) ArticleTitleAn improved colorimetric assay for bacterial lipase in nonfat dry milk J. Food Sci. 54 1557–1558 Occurrence Handle1:CAS:528:DyaK3cXltlymtw%3D%3D

    CAS  Google Scholar 

  • T.T. Vu (1983) ArticleTitleEtude histoenzymologique des activities proteasiques dans le tube digestif des larves et des adultes de bar, Dicentrarchus labrax (L) Aquaculture 32 57–69

    Google Scholar 

  • J. Waldford T.J. Lam (1993) ArticleTitleDevelopment of digestive tract and proteolytic enzyme activity in seabass (Lates calcarifer) larvae and juveniles Aquaculture 109 187–205

    Google Scholar 

  • H.E. Walter (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates H.J. Bergmeyern (Eds) Methods of Enzymatic Analysis NumberInSeriesVol. 5 Verlag Chemie Weinham 270–277

    Google Scholar 

  • J.L. Zambonino-Infante C. Cahu (1994) ArticleTitleDevelopment and response to a diet of some digestive enzymes in sea bass (Dicentrarchus labrax) larvae Fish Physiol. Biochem. 12 399–408

    Google Scholar 

  • J.L. Zambonino-Infante C.L. Cahu (1999) ArticleTitleHigh dietary lipid levels enhance digestive tract maturation and improve Dicentrarchus labrax larval development J. Nutr. 129 1195–1200 Occurrence Handle1:CAS:528:DyaK1MXjsFGnt78%3D Occurrence Handle10356086

    CAS  PubMed  Google Scholar 

  • J.L. Zambonino-Infante C.L. Cahu (2001) ArticleTitleOntogeny of the gastrointestinal tract of marine fish larvae Comp. Biochem. Physiol. 130 477–487 Occurrence Handle1:STN:280:DC%2BD3MnptFCiug%3D%3D

    CAS  Google Scholar 

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Alvarez-González, C.A., Cervantes-Trujano, M., Tovar-Ramírez, D. et al. Development of Digestive Enzymes in California Halibut Paralichthys californicus Larvae. Fish Physiol Biochem 31, 83–93 (2005). https://doi.org/10.1007/s10695-006-0003-8

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