Abstract
The ontogenesis of main pancreatic and intestinal enzymes was investigated in the recent promising Mediterranean candidate species of meagre, Argyrosomus regius, during larval development until 40 days after hatching (DAH). The green-water technique was carried out for larval rearing. Whole-body homogenates were used for enzymatic analysis in larvae younger than 15 DAH; after this date, older larvae were dissected into two segments as pancreatic and intestinal segment. Trypsin was detected as early as hatching and sharply increased concurrently with age and exogenous feeding 15 DAH, but constant decline was observed until the end of experiment. Amylase was determined at 2 DAH and sharply increased 10 DAH. Then, slight decreases were found between 10 and 15 DAH, and then slow alterations were continued until the end of the experiment. Lipase was firstly measured on day 3; then, sudden decline was observed between 20 and 25 DAH. After this date, slow fluctuations were maintained until the end of the experiment. Pepsin was firstly assayed 15 DAH related to gastric gland secretion and sharply increased 30 DAH. Then, it slowly varied until end of the experiment. Enzymes of brush border membranes, alkaline phosphatase and aminopeptidase N showed similar pattern on specific activities during the first 10 days. Thereafter, while specific activity of alkaline phosphatase slightly decreased 15 and fluctuated until 20 DAH, aminopeptidase N activity slowly increased 20 DAH. Then, activity of alkaline phosphatase and aminopeptidase N constantly increased 30 DAH, indicating maturation of the intestinal digestive process, and also, these activities continued to slowly increase until the end of the experiment. The specific activity of cytosolic peptidase, leucine–alanine peptidase, smoothly increased on day 8, then fluctuated until 15 DAH. After this date, in contrast to enzymes of brush border membranes, it sharply decreased 25 DAH and continued to gradually decline until the end of the experiment. These converse expressions were indicative of a maturation of enterocytes and the transition of an adult mode of digestion.
Similar content being viewed by others
References
Alpers DH, Zhang Y, Ahnen DJ (1995) Synthesis and parallel secretion of rat intestinal alkaline phosphatase and a surfactant–like particle protein. Am J Physiol 268:1205–1214
Alvarez-González CA, Cervantes-Trujano M, Tovar-Ramírez D, Conklin DE, Nolasco H, Gisbert E, Piedrahita R (2006) Development of digestive enzymes in California halibut, (Paralichthys californicus), larvae. Fish Physiol Biochem 31:83–93
Bessey OA, Lowry OH, Brock MJ (1946) Rapid coloric method for determination of alkaline phosphatase in five cubic millimeters of serum. J Biol Chem 164:321–329
Bradford MM (1976) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Cahu CL, Zambonino Infante JL (1994) Early weaning of sea bass (Dicentrarchus labrax) larvae with a compound diet: effect on digestive enzymes. Comp Biochem Physiol 109A:213–222
Cahu CL, Zambonino Infante JL (2001) Substitution of live food by formulated diets in marine fish larvae. Aquaculture 200:161–180
Cara JB, Moyano FJ, Cárdenas S, Fernández-Díaz C, Yúfera M (2003) Assessment of digestive enzyme activities during larval development of white bream. J Fish Biol 63:48–58
Chao LN (1986) Sciaenidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean, vol 2. UNESCO, Paris, pp 515–1007
Chatzifotis S, Panagiotudou M, Divanach P (2012) Effect of protein and lipid dietary levels on the growth of juvenile meagre (Argyrosomus regius). Aquacult Int 20:91–98
Chen BN, Qin JG, Kumar SM, Hutchinson WG, Clarke SM (2006) Ontogenetic development of digestive enzymes in yellowtail kingfish Seriola lalandi larvae. Aquaculture 260:264–271
Deguara S, Jauncey K, Agius C (2003) Enzyme activities and pH variations in the digestive tract of gilthead sea bream. J Fish Biol 62:1033–1043
Drossou A, Ueberschär B, Rosenthal H, Herzig K (2006) Ontogenetic development of the proteolytic digestion activities in larvae of Oreochromis niloticus fed with different diets. Aquaculture 256:479–488
El-Shebly AA, El-Kady MAH, Hussin AB, Hossain MY (2007) Preliminary observation on the pond culture of meagre, Argyrosomus regius (Asso, 1801) in Egypt. J Fish Aquac Sci 2:345–352
Griffiths MH, Heemstra PC (1995) A contribution to the taxonomy of the marine fish genus Argyrosomus (Perciformes: Sciaenidae), with description of two new species from Southern Africa. Ichth Bull 65:1–40
Kolkovski S (2001) Digestive enzymes in fish larvae and juveniles–implications and application to formulated diets. Aquaculture 200:181–201
Kurokawa T, Suzuki T (1996) Formation of the diffuse pancreas and the development of digestive enzyme synthesis in larvae of the Japanese flounder Paralichthys olivaceus. Aquaculture 141:267–276
Lagardère JP, Mariani A (2006) Spawning sounds in meagre Argyrosomus regius recorded in the Gironde estuary, France. J Fish Biol 69:1697
Lazo JP, Holt GJ, Arnold CR (2000) Ontogeny of pancreatic enzymes in larval red drum Sciaenops ocellatus. Aquac Nutr 6:183–192
Ma H, Cahu C, Zambonino Infante JL, Yu H, Duan Q, Le Gall M–M, Mai K (2005) Activities of selected digestive enzymes during larval development of large yellow croacker (Pseudosciaena crocea). Aquaculture 245:239–248
Martinez I, Moyano FJ, Fernández-Diaz C, Yufera M (1999) Digestive enzyme activity during larval development of the Senegal sole (Solea senegalensis). Fish Physiol Biochem 21:317–323
Mckellar RC, Cholette H (1986) Determination of the extracellular lipases of Pseudomonas fluorescens spp. in skim milk with the beta–naphthyl caprylate assay. J Dairy Res 53:301
Métais P, Bieth J (1968) Détermination de l’α-amylase par une microtechnique. Ann Biol Clin 26:133–142
Moutou KA, Panagiotaki P, Mamuris Z (2004) Effects of salinity on digestive protease activity in the euryhaline sparid Sparus aurata L.: a preliminary study. Aquac Res 35:912–914
Moyano FJ, Diaz M, Alarcon FJ, Sarasquete MC (1996) Characterisation of digestive enzyme activity during larval development of gilthead seabream (Sparus aurata). Fish Physiol Biochem 15:121–130
Moyano FJ, Barros AM, Prieto A, Cañavate JP, Cárdenas S (2005) Evaluación de la ontogenia de enzimas digestivas en larvas de hurta, Pagrus auriga (Pisces: Sparidae). Revista AquaTIC 22:39–47
Nicholson JA, Kim YS (1975) A one–step L-amino acid oxidase assay for intestinal peptide hydrolase activity. Anal Biochem 63:110–117
Pedersen BH, Andersen KP (1992) Induction of trypsinogen secretion in herring larvae (Clupea harengus). Mar Biol 112:559–565
Piccolo G, Bovera F, De Rui N, Marono S, Salati F, Cappuccinelli R, Moniello G (2008) Effect of two different protein/fat ratios of the diet on meagre (Argyrosomus regius) traits. Italy J Anim Sci 7:363–371
Poli BM, Parisi G, Zampaca Vallo G, Iurzan F, Mecatti M, Lupi P, Bonelli A (2003) Preliminary results on quality and quality changes in reared meagre (Argyrosomus regius): body and fillet traits and freshness changes in refrigerated commercial–size fish. Aquacult Int 11:301–311
Porteous JW, Clark B (1965) The isolation and characterization of subcellular components of the epithelial cells of rabbit small intestine. Biochem J 96:159–171
Quéro JC (1989) Sur la piste des maigres Argyrosomus regius (Pisces, Sciaenidae) du Golfe de Gascogne et de Mauritanie. In: Facteurs externes et internes du déterminisme des migrations: séminaire 15 et 22 décembre 1988. Oceanis Doc. Oceanograph 15(2): 161–170
Ribeiro L, Zambonino-Infante JL, Cahu C, Dinis MT (1999) Development of digestive enzymes in larvae of Solea senegalensis, Kaup 1858. Aquaculture 179:465–473
Ribeiro L, Couto A, Olmedo M, Álvarez-Blázquez B, Linares F, Valente LMP (2008) Digestive enzyme activity at different developmental stages of blackspot seabream, Pagellus bogaraveo (Brunnich 1768). Aquacult Res 39:339–346
Roo J, Hernández-Cruz CM, Borrero C, Schuchardt D, Fernández-Palacios H (2010) Effect of larval density and feeding sequence on meagre (Argyrosomus regius; Asso, 1801) larval rearing. Aquaculture 302:82–88
Suzer C, Fırat K, Saka Ş (2006a) Ontogenic development of the digestive enzymes in common pandora, Pagellus erythrinus, L. larvae. Aquacult Res 37:1565–1571
Suzer C, Saka Ş, Fırat K (2006b) Effects of illumination on early life development and digestive enzyme activities in common pandora Pagellus erythrinus L. larvae. Aquaculture 260:86–93
Suzer C, Aktülün S, Çoban D, Kamacı HO, Saka Ş, Fırat K, Alpbaz A (2007a) Digestive enzyme activities in sharpsnout seabream (Diplodus puntazzo) larvae. Comp Biochem Physiol 148A:470–477
Suzer C, Kamacı HO, Çoban D, Saka Ş, Fırat K, Ozkara B, Ozkara A (2007b) Digestive enzyme activity of the red porgy (Pagrus pagrus, L.) during larval development under culture conditions. Aquacult Res 38:1178–1785
Tengjaroenkul B, Smith BJ, Smith SA, Chatreewongsin U (2002) Ontogenic development of the intestinal enzymes of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 211:241–251
Tseng HC, Grendell JH, Rothman SS (1982) Food, duodenal extracts, and enzyme secretion by the pancreas. Am J Physiol 243:G304–G312
Ueberschär B (1995) The use of tryptic enzyme activity measurement as a nutritional condition index: laboratory calibration data and field application. ICES Mar Sci Symp 201:119–129
Versaw WK, Cuppett SL, Winters DD, Williams LE (1989) An improved colorimetric assay for bacterial lipase in nonfat dry milk. J Food Sci 54:1557–1558
Walford J, Lam TJ (1993) Development of the digestive tract and proteolytic enzyme activity in seabass (Lates calcarifer) larvae and juveniles. Aquaculture 109:187–205
Worthington TM (1982) Enzymes and related biochemicals. Biochemical Products Division. Worthington Diagnostic System, Freehold
Zambonino Infante JL, Cahu CL (1994) Development and response to a diet change of some digestive enzymes in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 12:399–408
Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol 130C:477–487
Zambonino Infante JL, Gisbert E, Sarasquete C, Navarro I, Gutiérrez J, Cahu CL (2008) Ontogeny and physiology of the digestive system of marine fish larvae. In: Cyrino JEP, Bureau D, Kapoor BG (eds) Feeding and digestive functions of fishes. Oxford&IBH Publishing Co. Pvt. Ltd., New Delhi, pp 281–348
Acknowledgments
The authors wish to thank the staff of the Kılıç Sea Products Inc., Güvercinlik R&D hatchery, Bodrum, Muğla, Turkey, where the experiments were conducted, for their most efficient technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Suzer, C., Kamacı, H.O., Çoban, D. et al. Functional changes in digestive enzyme activities of meagre (Argyrosomus regius; Asso, 1801) during early ontogeny. Fish Physiol Biochem 39, 967–977 (2013). https://doi.org/10.1007/s10695-012-9755-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-012-9755-5