Fish Physiology and Biochemistry

, Volume 45, Issue 2, pp 599–611 | Cite as

Changes in serum biochemical parameters and digestive enzyme activity of juvenile sobaity sea bream (Sparidentex hasta) in response to partial replacement of dietary fish meal with poultry by-product meal

  • Fatemeh Hekmatpour
  • Preeta KochanianEmail author
  • Jasem G. Marammazi
  • Mohammad Zakeri
  • Seyed-Mohammad Mousavi


A 60-day experiment was conducted to evaluate the effect of dietary fish meal (FM) replacement with poultry by-product meal (PBM) on digestive enzymes, non-specific serum enzyme activity, and serum biochemical parameters of juvenile sobaity sea bream, Sparidentex hasta, weighing 29.27 ± 0.06 g. PBM replaced 0, 15, 25, 35, 45, and 55% of dietary FM in the isoproteic (50%) and isocaloric (21 kJ g−1) experimental diets. The final body weight, percentage weight gain, specific growth rate, and protein efficiency ratio were higher in PBM15, 25, and 35 than in control, PBM45, and 55. Digestive lipase and amylase activity did not differ significantly between the dietary treatments. Significantly lower trypsin and higher chymotrypsin activity were observed at PBM55 and 45, respectively. Digestive alkaline phosphatase (ALP) increased, whereas protein apparent digestibility coefficients (ADC) decreased significantly with increasing levels of PBM above 35%. Hematocrit, hemoglobin, mean corpuscular hemoglobin concentration, serum albumin, globulin, total protein, glucose, urea, uric acid, and aspartate aminotransferase did not show any significant differences between the treatments. Serum ALP, cholesterol, and calcium were higher in PBM diets than in the control diet, whereas an inverse trend was observed in triglyceride. Protein digestibility and trypsin activity and serum biochemical indices suggest that fish meal protein could be reduced up to 45% by the inclusion PBM in the formulated diets for S. hasta juveniles without any adverse effect on its overall performance.


Apparent digestibility Dietary substitution Digestive enzymes Poultry by-product meal Sobaity sea bream 



Authors are thankful to Dr. Morteza Yaghoubi and Mr. Esmail Paghe for their technical help throughout the experiment. We are grateful to the Director and staff of the Mariculture Research Station, Sarbandar, Iran, for providing the necessary facilities for the experiment.

Funding information

This study was financed by Khorramshahr University of Marine Science and Technology, Iran and South Iranian Aquaculture Research Center, Ahwaz, Iran.


  1. AOAC (2005) Official methods of analysis. Association of Official Analytical Chemists. Arlington, VirginiaGoogle Scholar
  2. Applebaum SL, Holt GJ (2003) The digestive protease, chymotrypsin, as an indicator of nutritional condition in larval red drum (Sciaenops ocellatus). Mar Biol 142:1159–1167CrossRefGoogle Scholar
  3. 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 72:248–254CrossRefGoogle Scholar
  4. Brill RW, Bushnell P, Schroff R, Seifert R, Galvin M (2008) Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of the sandbar shark (Carcharhinus plumbeus, Nardo). J Exp Mar Biol Ecol 354:132–143CrossRefGoogle Scholar
  5. Bureau DP, Harris AM, Cho CY (1999) Apparent digestibility of rendered animal protein ingredients for rainbow trout (Oncorhyncus mykiss). Aquac 180:345–358CrossRefGoogle Scholar
  6. Campbell TW, Ellis CK (2007) Avian and exotic animal hematology and cytology. Blackwell, AmesGoogle Scholar
  7. Cheng Z, Ai Q, Mai K, Xu W, Ma H, Li Y, Zhang J (2010) Effects of dietary canola meal on growth performance, digestion and metabolism of Japanese seabass, Lateolabrax japonicus. Aquac 305:102–108CrossRefGoogle Scholar
  8. Congleton JL, Wagner T (2006) Blood -chemistry indicators of nutritional status in juvenile salmonids. Fish Biol 69:473–490CrossRefGoogle Scholar
  9. Debnath D, Pal AK, Sahu NP, Yengkokpam S, Baruah 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, Part B 146:107–114Google Scholar
  10. De Silva SS, Anderson TA (1995) Fish nutrition in aquaculture. Chapman and Hall, LondonGoogle Scholar
  11. Evans GO, Watterson CL (2009) General enzymology. In: Animal clinical chemistry, a practical guide for toxicologists and biochemical researchers, 2nd edn. CRC Press, New YorkGoogle Scholar
  12. Fazio F, Marafioti S, Filiciotto F, Buscaino G, Panzera M, Faggio C (2013) Blood Hemogram profiles of farmed onshore and offshore Gilthead Sea bream (Sparus aurata) from Sicily, Italy. Turk J Fish Aquat Sci 13:415–422CrossRefGoogle Scholar
  13. Fernandez I, Moyano F, Dıaz M, Martınez T (2001) Characterization of α-amylase activity in five species of Mediterranean sparid fishes (Sparidae, Teleostei). J Exp Mar Biol Ecol 262:1–12CrossRefGoogle Scholar
  14. Furukawa A, Tsukahara H (1966) On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bull Jpn Soc Sci Fish 32:502–506CrossRefGoogle Scholar
  15. Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, 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 38:551–579CrossRefGoogle Scholar
  16. Gawlicka A, Parent B, Horn MH, Ross N, Opstad I, Torrissen OJ (2000) Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquac 184:303–314CrossRefGoogle Scholar
  17. Gaylord TG, Barrows FT, Teague AM, Johansen KA (2007) Supplementation of taurine and methionine to all- plant protein diets for rainbow trout (Oncorhynchus mykiss). Aquac 269:514–524CrossRefGoogle Scholar
  18. Gunben EM, Senoo S, Yong A, Shapawi R (2014) High potential of poultry by-product meal as a Main protein source in the formulated feeds for a commonly cultured grouper in Malaysia (Epinephelus fuscoguttatus). Sains Malaysiana 43:399–405Google Scholar
  19. Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011) Probiotics and herbal mixtures enhance the growth, blood constituents, and nonspecific immune response in Paralichthys olivaceus against Streptococcus parauberis. Fish Shellfish Immunol 31:310–317CrossRefPubMedGoogle Scholar
  20. Hekmatpour F, Preeta Kochanian P, Marammazi JG, Zakeri M, Mohammad Mousavi SM (2018) Inclusion of poultry by-product meal in the diet of Sparidentex hasta: effects on production performance, digestibility and nutrient retention. Anim Feed Sci Technol 241:173–183CrossRefGoogle Scholar
  21. Hernandez C, Sanchez-Gutierrez Y, Hardy RW, Benitez- Hernandez A, Dominguez- Jimenez P, Gonzalez-Rodriguez B, Bosuna-Osuna L, Tortoledo O (2014) The potential of pet-grade poultry by-product meal to replace fish meal in the diet of the juvenile spoted rose snapper Lutjanus guttatus (Steindachner, 1869). Aquac Nutr 20:623–631CrossRefGoogle Scholar
  22. Hossain M, Al-Abdul-Elah K, El-Dakour S (2014) Evaluation of different commercial feeds for culture of juvenile sobaity (Sparidentex hasta, Valenciennes) in Kuwait. APCBEE Proc 8:310–316CrossRefGoogle Scholar
  23. Hummel BCW (1959) A modified spectrophotometric determination of chymotrypsin, trypsin and thrombin. Can J Biochem Physiol 37:1393–1399CrossRefGoogle Scholar
  24. Jalili R, Noori F, Agh N (2012) Effects of dietary protein source on growth performance, feed utilization and digestive enzyme activity in rainbow trout (Oncorhynchus Mykiss). J Appl Biol Sci 6:61–68Google Scholar
  25. Kureshy ND, Davis A, Arnold CR (2000) Partial replacement of fish meal with meat and bone meal, flash- dried poultry by- product meal, and enzyme- digested poultry by-product meal in practical diets for juvenile red drum. N Am J Aquac 62:266–272CrossRefGoogle Scholar
  26. Lazzari R, Neto JR, de Araújo Pedron F, Loro VL, Pretto A, Gioda CR (2010) Protein sources and digestive enzyme activities in jundiá (Rhamdia quelen). Sci Agric 67:259–266CrossRefGoogle Scholar
  27. Lemieux H, Blier P, Dutil JD (1999) Do digestive enzymes set a physiological limit on growth rate and food conversion efficiency in the Atlantic cod (Gadus morhua)? Fish Physiol Biochem 20:293–303CrossRefGoogle Scholar
  28. Lindroth P, Mopper K (1979) High performance liquid chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivatization with o-phthaldialdehyde. Anal Chem 51:1667–1674CrossRefGoogle Scholar
  29. McClatchey KD (2002) Clinical laboratory medicine. Williams and Wilkins, PhiladelphiaGoogle Scholar
  30. Me’ dale F, Boujard T, Valle ´e F, Blanc D, Mambrini M, Roem A, Kaushik SJ (1998) Voluntary feed intake, nitrogen and phosphorus losses in rainbow trout (Oncorhyncus mykiss) fed increasing dietary levels of soy protein concentrate. Aquat Living Resour 11:239–246CrossRefGoogle Scholar
  31. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquac 302:1–1Google Scholar
  32. Moraes G, Bidinotto PM (2000) Induced changes in the amylohydrolytic profile of the gut of Piaractus mesopotamicus (Holmberg, 1885) fed different levels of soluble carbohydrate: its correlation with metabolic aspects. Rev Ictiol 8:47–51Google Scholar
  33. Mozanzadeh MT, Yaghoibi M, Yavari V, Agh N, Marammazi JG, Topic-Popovic N (2015) Reference intervals for haematological and plasma biochemical parameters in sobaity seabream juveniles (Sparidentex hasta, Valenciennes 1830). Comp Clin Pathol 595Google Scholar
  34. Mozanzadeh MT, Agh N, Yavari V, Marammazi JG, Mohammadian T, Gisbert E (2016) Partial or total replacement of dietary fish oil with alternative lipid sources in silvery-black porgy (Sparidentex hasta). Aquaculture 451:232–240CrossRefGoogle Scholar
  35. Mozanzadeh M, Marammazi J, Yaghoubi M, Yavari V, Agh N, Gisbert E (2017) Somatic and physiological responses to cyclic fasting and re-feeding periods in sobaity sea bream (Sparidentex hasta, Valenciennes 1830). Aquac Nutr 23:181–191CrossRefGoogle Scholar
  36. Navarro I, Gutierrez J (1995) Fasting and starvation. Elsevier, AmsterdamGoogle Scholar
  37. Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K (2009) Feeding aquaculture in an era of finite resources. PNAS 106:15103–15110CrossRefPubMedGoogle Scholar
  38. Nengas I, Alexis MN, Davies SJ (1999) High inclusion levels of poultry meals and related by products in diets for gilthead seabream Sparus aurata L. Aquac 179:13–23CrossRefGoogle Scholar
  39. NRC (2011) Nutrient requirements of fish. National Academy Press, Washington, DCGoogle Scholar
  40. Nya EJ, Austin B (2011) Dietary modulation of digestive enzymes by the administration of feed additives to rainbow trout, Oncorhynchus mykiss Walbaum. Aquac Nutr 17:459–466CrossRefGoogle Scholar
  41. OlivaTeles A, Enes P, Peres H (2015) Replacing fishmeal and fish oil in industrial aquafeeds for carnivorous fish. In: Davis AD (ed) Feed and Feeding Practices in Aquaculture. Elsevier, Cambridge, pp 203–233CrossRefGoogle Scholar
  42. Pavlidis MA, Mylonas CC (2011) Sparidae biology and aquaculture of gilthead seabream and other species. Blackwell Publishing Ltd., UKGoogle Scholar
  43. Perera WMK, Carter CG, Houlihan DF (1995) Feed consumption, growth and growth efficiency of rainbow trout, Oncorhynchus mykiss Walbaum fed diets containing bacterial single cell protein. Br J Nutr 73:591–603CrossRefPubMedGoogle Scholar
  44. Peres H, Santos S, Oliva-Teles A (2013) Selected plasma biochemistry parameters in gilthead seabream (Sparus aurata) juveniles. J Appl Ichthyol 29:630–636CrossRefGoogle Scholar
  45. Peres H, Santos S, Oliva-Teles A (2014) Blood chemistry profile as indicator of nutritional status in European seabass (Dicentrarchus labrax). Fish Physiol Biochem 40:1339–1347CrossRefPubMedGoogle Scholar
  46. Rawles SD, Riche M, Gaylord TG, Webb J, Freeman DW, Davis M (2006) Evaluation of poultry by-product meal in commercial diets for hybrid striped bass (Morone chrysops ♀×M. saxatilis ♂) in recirculated tank production. Aquac 259:377–389CrossRefGoogle Scholar
  47. Roosta H, Javadi T, Nazari F (2011) Isolation and characterization of trypsin inhibitors (Kunitz soybean trypsin inhibitor, Bowman-birk inhibitor) in soybean. Adv Environ Biol 145–153Google Scholar
  48. Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fishmeal replacement by plant protein sources. Aquac 282:68–74CrossRefGoogle Scholar
  49. Shapawi R, Ng W-K, Mustafa S (2007) Replacement of fish meal with poultry by-product meal in diets formulated for the humpback grouper, Cromileptes altivelis. Aquaculture 273:118–126CrossRefGoogle Scholar
  50. Silva FCP, Nicoli JR, Zambonino-Infante JL, Le Gall MM, Kaushik S, Gatesoupe FJ (2010) Influence of partial substitution of dietary fish meal on the activity of digestive enzymes in the intestinal brush border membrane of gilthead sea bream, Sparus aurata and goldfish, Carassius auratus. Aquac 306(1–4):233–237CrossRefGoogle Scholar
  51. Takagi S, Hosokawa H, Shimeno S, Ukawa M (2000) Utilization of poultry by-product meal in a diet for red sea bream Pagrus major. Nippon Suisan Gakkaishi 66:428–438Google Scholar
  52. Tietz NW, Shuey DF (1993) Lipase in serum- the elusive enzyme: an overview. Clin Chem 39:746–756PubMedGoogle Scholar
  53. Wang Y, Wang F, Ji WX, Han H, Li P (2015) Optimizing dietary protein sources for Japanese sea bass (Lateolabrax japonicus) with an emphasis on using poultry by-product meal to substitute fish meal. Aquac Res 46:874–883CrossRefGoogle Scholar
  54. Xu QY, Wang CA, Zhao ZG, Luo L (2012) Effects of replacement of fish meal by soy protein isolate on the growth, digestive enzyme activity and serum biochemical parameters for juvenile Amur sturgeon (Acipenser schrenckii). Asian Australas J Anim Sci 25:1588–1594CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yaghoubi M, T. Mozanzadeh M, Gh. Marammazi J, Safari. O, Gisber E (2016) Dietary replacement of fish meal by soy products (soybean meal and isolated soy protein) in silvery-black porgy juveniles (Sparidentex hasta). Aquac 464:50–59Google Scholar
  56. Yang Y, Xie SQ, Cui YB, Zhu XM, Lei W, Yang YX (2006) Partial and total replacement of fish meal with poultry by-product meal in diets for gibel carp, Carassius auratus gibelio Bloch. Aquac Res 37:40–48CrossRefGoogle Scholar
  57. Zhou QC, Zhao J, Li P, Wang HL, Wang LG (2011) Evaluation of poultry by-product meal in commercial diets for juvenile cobia (Rachycentron canadum). Aquaculture 322-323:122–127CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Fatemeh Hekmatpour
    • 1
  • Preeta Kochanian
    • 1
    Email author
  • Jasem G. Marammazi
    • 2
  • Mohammad Zakeri
    • 1
  • Seyed-Mohammad Mousavi
    • 1
  1. 1.Department of FisheriesKhorramshahr University of Marine Science and TechnologyKhorramshahrIran
  2. 2.South Iranian Aquaculture Research CenterAhwazIran

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