Effect of dietary protein level and source on digestive proteolytic enzyme activity in juvenile Senegalese sole, Solea senegalensis Kaup 1850

Aquaculture International

Volumn 20, Issue 6, 2012, Pages 1053-1070

  Rodiles, Ana ^a   Santigosa, Ester ^b   Herrera, Marcelino ^a   Hachero Cruzado, Ismael ^a   Cordero, María Luisa ^a   Martínez Llorens, Silvia ^c   Lall, Santosh P ^d   Alarcón, Francisco Javier ^b  

^a IFAPA CENTRO EL TORUÑO   (Spain)

^b UNIVERSITY OF ALMERÍA   (Spain)

^c UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Dietary protein; Digestive proteases; Plant protein sources; Protease inhibitor; Replacement; Senegalese sole; Zymogram

Indexed keywords

DIET; ENZYME ACTIVITY; FLATFISH; FOOD SUPPLEMENTATION; GROWTH RESPONSE; HYDROLYSIS; INHIBITOR; JUVENILE; PHYSIOLOGY; PROTEIN; SOYBEAN;

ANIMALIA; GLYCINE MAX; PISUM SATIVUM; SOLEA SENEGALENSIS; SOLEIDAE; TRITICUM AESTIVUM;

EID: 84870625198     PISSN: 09676120     EISSN: 1573143X     Source Type: Journal    
DOI: 10.1007/s10499-012-9508-6     Document Type: Article

References (63)

1. Alarcón FJ, Díaz M, Moyano FJ, Abellán E (1998) Characterization and functional properties of digestive proteases in two sparids; gilthead sea bream (Sparus aurata) and common dentex (Dentex dentex). Fish Physiol Biochem 19: 257-267.
2. Alarcón FJ, García-Carreño FL, Navarrete del Toro MA (2001) Effect of plant protease inhibitors on digestive proteases in two fish species, Lutjanus argentiventris and L. novemfasciatus. Fish Physiol Biochem 24: 179-181.
3. Alarcón FJ, Díaz M, Moyano FJ (2002) Evaluation of different protein sources for aquafeeds by an optimised pH-stat system. J Sci Food Agric 82: 697-704.
4. Aragão C, Conceição LEC, Dias J, Marques AC, Gomes E, Dinis MT (2003) Soy protein concentrate as a protein source for Senegalese sole (Solea senegalensis, Kaup 1858) diets: effects on growth and amino acid metabolism of postlarvae. Aquac Res 34: 1443-1452.
5. Arndt RE, Hardy RW, Sugiura SH, Dong FM (1999) Effects of heat treatment and substitution level on palatability and nutritional value of soy defatted £our in feeds for Coho salmon (Oncorhynchus kisutch). Aquaculture 180: 129-145.
6. Association of Official Analytical Chemists (1990) Official methods of analysis, 15th edn. Association of official analytical chemists, Arlington, USA, 1298.
7. Bazaz MM, Keshavanath P (1993) Effect of feeding different levels of sardine oil on growth, muscle composition and digestive enzyme activities of mahseer, Tor khudree. Aquaculture 115: 111-119.
8. Bonaldo A, Roem AJ, Pecchini A, Grilli E, Gatta PP (2006) Influence of dietary soybean meal levels on growth, feed utilization, gut histology of Egyptian sole (Solea aegyptiaca) juveniles. Aquaculture 261: 580-586.
9. Bureau DP, Harris AM, Cho CY (1998) The effects of purified alcohol extracts from soy products on feed intake and growth of Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss). Aquaculture 161: 27-43.
10. 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 A 109: 213-222.
11. Chong ASC, Hashim R, Ali AB (2002) Assessment of dry matter and protein digestibility of selected raw ingredients by discus fish (Symphysodon aequifasciata) using in vivo and in vitro methods. Aquac Nutr 8: 229-238.
12. Debnath D, Pal AK, Sahu NP, Yengkokapm S, Barauh K, Choudhury D, Venkateshwarlu G (2007) Digestive enzymes and metabolic profile of Labeo rohita fingerlings fed diets with different crude protein levels. Comp Biochem Physiol B 146: 107-114.
13. Dias J, Rueda-Jasso R, Panserat S, Conceição LEC, Gomes EF, Dinis MT (2004) Effect of dietary carbohydrate-to-lipid ratios on growth, lipid deposition and metabolic hepatic enzymes in juveniles Senegalese sole (Solea senegalensis, Kaup). Aquac Res 35: 1122-1130.
14. Dias J, Yúfera M, Valente LMP, Rema P (2010) Feed transit and apparent protein, phosphorus and energy digestibility of practical feed ingredients by Senegalese sole (Solea senegalensis). Aquaculture 302: 94-99.
15. Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review of the cultivation potential of Solea senegalensis in Spain and in Portugal. Aquaculture 176: 27-38.
16. Einarsson S, Davies PS, Talbot C (1997) Effect of exogenous cholecystokinin on the discharge of the gallbladder and the secretion of trypsin and chymotrypsin from the pancreas of the Atlantic salmon, Salmo salar L. Comp Biochem Physiol C 117: 63-67.
17. El-Saidy DMSD, Dabrowski K, Bai SC (2000) Nutritional effects of protein source in starter diets for channel catfish (Ictalurus punctatus Rafinesque) in suboptimal water temperature. Aquac Res 31: 885-892.
18. Escaffe A, Kaushik S, Mambrini M (2007) Morphometric evaluation of changes in the digestive tract of rainbow trout replacement with soy protein concentrate. Aquaculture 273: 127-138.
19. Eusebio PS, Coloso RM (2002) Proteolytic enzyme activity of juvenile Asian sea bass, Lates calcifer (Bloch), is increased with protein intake. Aquac Res 33: 569-574.
20. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199: 197-227.
21. Garcia-Carreño FL, Dimes LE, Haard NF (1993) Substrate gel-electrophoresis for composition and molecular-weight of proteinases of proteinaceous proteinase-inhibitors. Anal Biochem 214: 65-69.
22. Gatlin DBIII, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38: 551-579.
23. Gatta PP, Parma L, Guarniero I, Mandrioli L, Sirri R, Fontanillas R, Bonaldo A (2010). Growth, feed utilization and liver histology of juvenile common sole (Solea solea L.) fed isoenergetic diets with increasing protein levels. Aquac Res 42: 313-321.
24. González-Félix ML, Castillo-Yañez FJ, Ocaño-Higuera VM, Perez-Velazquez M, Cota-Moreno V, Lozano-Taylor J (2010) Effect of dietary protein source and time on alkaline proteolytic activity of Nile tilapia (Oreochromis niloticus). Fish Physiol Biochem 36: 779-785.
25. Gouveia A, Davies SJ (1998) Preliminary nutritional evaluation of pea seed meal (Pisum satium) for juvenile European Sea bass (Dicentrarchus labrax). Aquaculture 166: 311-320.
26. Gouveia A, Davies SJ (2000) Inclusion of an extruded dehulled pea seed meal in diets for juvenile European Sea bass (Dicentrarchus labrax). Aquaculture 182: 183-193.
27. Guillaume J, Choubert G (2001) Digestive physiology and nutrient digestibility in fishes. In: Guillaume J, Kaushik S, Bergot P, Métailler R (eds) Nutrition and feeding of fish and crustaceans. Springer, Chichester, pp 27-58.
28. Haard NF, Dimes LE, Arndt RE, Dong FM (1996) Estimation of protein digestibility. IV. Digestive proteinases from pyloric caeca of Coho salmon (Oncorhynchus kisutch) fed diets containing soybean meal. Comp Biochem Physiol B 115: 533-540.
29. Hidalgo MC, Urea E, Sanz A (1999) Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture 170: 267-283.
30. Howell B, Conceiçao L, Prickett R, Cañavate P, Mañanos E (2009) Sole farming: nearly there but not quite? Aquac Eur 34: 24-27.
31. Imsland AK, Foss A, Conceição 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 Fish 13: 379-407.
32. Johnson LR (2001) Gastric secretion. In: Johnson LR, Gerwin TA (eds) Gastrointestinal physiology, 6th edn. Mosby, St. Louis, pp 75-94.
33. Kohla U, Saint-Paul U, Friebe J, Wernicke D, Hilge V, Braum E (1992) Growth, digestive enzyme activities and hepatic glycogen levels in juvenile Colossoma macropomum Cuvier from South America during feeding, starvation and refeeding. Aquac Fish Man 23: 189-208.
34. Krogdahl A, Lea TB, Olli JL (1994) Soybean proteinase-inhibitors affect intestinal trypsin activities and amino-acid digestibilities in rainbow-trout (Oncorhynchus mykiss). Comp Biochem Physiol A 107: 215-219.
35. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227: 680-688.
36. Lopez-Lopez S, Nolasco H, Villareal-Colmenares H, Civera-Cerecedo R (2005) Digestive enzyme response to supplemental ingredients in practical diets for juvenile freshwater crayfish Cherax quadricarinatus. Aquac Nutr 11: 79-85.
37. Mohanta KN, Mohanty SN, Jena JK, Sahu NP (2008) Protein requirement of silver barb, Puntius gonionotus fingerlings. Aquac Nutr 14: 143-152.
38. Moyano FJ, Martínez I, Díaz M, Alarcón FJ (1999) Inhibition of digestive proteases by vegetable meals in three fish species; seabream (Sparus aurata), tilapia (Oreochromis niloticus) and African sole (Solea senegalensis). Comp Biochem Physiol B 122: 327-332.
39. Olli JJ, Hjelmeland K, Krogdahl Á (1994) Soybean trypsin inhibitors in diets for Atlantic salmon (Salmo salar, L.): effects on nutrient digestibilities and trypsin in pyloric caeca homogenate and intestinal content. Comp Biochem Physiol A 109: 923-928.
40. Olsson C, Holmgren S (2001) The control of gut motility. Comp Biochem Physiol A 128: 481-503.
41. Olsson C, Aldman G, Larsson A, Holmgren S (1999) Cholecystokinin affects gastric emptying and stomach motility in the rainbow trout Oncorhynchus mykiss. J Exp Biol 202: 161-170.
42. Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M (2005) Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245: 273-286.
43. Øverland M, Sørensen M, Storebakken T, Penn M, Krogdahl Å, Skrede A (2009) Pea protein concentrate substituting fish meal or soybean meal in diets for Atlantic salmon (Salmo salar)-effect on growth performance, nutrient digestibility, carcass composition, gut health, and physical feed quality. Aquaculture 288: 305-311.
44. Penn MH, Bendiksen EÅ, Campbell P, Krogdahl Å (2011) High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture 310: 267-273.
45. Rema P, Conceição LEC, Evers F, Castro-Cunha M, Dinis MT, Dias J (2008) Optimal dietary protein levels in juvenile Senegalese sole (Solea senegalensis). Aquac Nutr 14: 263-269.
46. Rodiles A, Hachero I, Herrera M, Navas JI, Alarcón FJ (2007) Protein requirement of juvenile Senegal sole (Solea senegalensis Kaup 1858) in intensive culture. In: Proceedings form of the 1st international symposium of marine science (ISMS), University of Valencia, Spain, 28-31 March 2007.
47. Rojas-García CR, Rønnestad I (2002) Cholecystokinin and tryptic activity in the gut and body of developing Atlantic halibut larvae: evidence for participation in the regulation of protein digestion. J Fish Biol 61: 973-986.
48. Romarheim OH, Skrede A, Penn M, Mydlanda LT, Krogdahl Å, Storebakken T (2007) Lipid digestibility, bile drainage and development of morphological intestinal changes in rainbow trout (Oncorhynchus mykiss) fed diets containing defatted soybean meal. Aquaculture 274: 329-338.
49. Rubio VC, Navarro DB, Madrid FJ, Sánchez-Vázquez FJ (2009) Macronutrient self-selection in Solea senegalensis fed macronutrient and challenged with dietary protein dilutions. Aquaculture 291: 95-100.
50. Sáenz de Rodrigáñez M, Alarcón FJ, Martínez MI, Ruiz F, Díaz M, Moyano FJ (2005) Caracterización de las proteasas digestivas del lenguado senegalés Solea senegalensis Kaup, 1858. Bol Inst Esp Oceanog 21: 95-104.
51. Sáenz de Rodrigáñez MA, Medina E, Moyano FJ, Alarcón FJ (2011) Evaluation of protein hydrolysis in raw sources by digestive proteases of Senegalese sole (Solea senegalensis, Kaup 1858) using a combination of an in vitro assay and sodium dodecyl sulphate polyacrylamide gel electrophoresis analysis of products. Aquac Res 42: 1639-1652.
52. Santigosa E, Sánchez J, Médale F, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Onchorynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 252: 68-74.
53. Santigosa E, Sáez de Rodigrañez MA, Rodiles A, García Barroso F, Alarcón FJ (2010) Effect of diets containing a purified soybean trypsin inhibitor on growth performance, digestive proteases and intestinal histology in juvenile sea bream (Sparus aurata L.). Aquac Res 41: 187-198.
54. Sharara AI, Bouras EP, Misukonis MA, Liddle RA (1993) Evidence for indirect dietary regulation of cholecystokinin release in rats. Am J Physiol 265: G107-G112.
55. Silva JMG, Espe M, Conceição LEC, Dias J, Costas B, Valente LMP (2010) Feed intake and growth performance of Senegalese sole (Solea senegalensis Kaup, 1858) fed diets with partial replacement of fish meal with plant proteins. Aquac Res 41: e20-e30.
56. Smith LS (1980) Digestion in teleost fish. In: Smith LS (ed) Fish feed technology lectures ACDP. FAO/UNDP, Rome, pp 4-187.
57. Suárez MD, Hidalgo MC, García Galego M, Sanz A, De la Higuera M (1995) Influence of the relative proportions of the energy yielding nutrients on the liver intermediary metabolisms of the European eel. Comp Biochem Physiol A 111: 421-428.
58. Sveier H, Kuamme BO, Raae AJ (2001) Growth and protein utilization in Atlantic salmon (Salmo salar L.) given a protease inhibitor in diet. Aquaculture 7: 255-264.
59. Takii K, Seoka M, Nagaoka T, Kawamura K, Nakamura M, Yoshizawa H, Kumai Y (2001) Inhibitory modes of Kunitz and Bowman-Birk soybean trypsin inhibitors to tryptic and chymotryptic proteinases of tiger puffer and yellowtail. Fish Sci 67: 52-57.
60. Temler RS, Dormond CA, Simon E, Morel B (1985) The effect of feeding soya bean trypsin inhibitor and repeated injections of cholecystokinin on rat pancreas. Plant Foods Hum Nutr 35: 315-321.
61. Tibbetts SM, Lall SP, Milley JE (2004) Apparent digestibility of common feed ingredients by juvenile haddock, Melanogrammus aeglefinus L. Aquac Res 35: 643-651.
62. Watanabe T (2002) Strategies for further development of aquatic feeds. Fish Sci 68: 242-252.
63. Yúfera M, Darías MJ (2007) Changes in the gastrointestinal pH from larvae to adult in Senegal sole (Solea senegalensis). Aquaculture 267: 94-99.