Abstract
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.
Similar content being viewed by others
References
AOAC (2005) Official methods of analysis. Association of Official Analytical Chemists. Arlington, Virginia
Applebaum SL, Holt GJ (2003) The digestive protease, chymotrypsin, as an indicator of nutritional condition in larval red drum (Sciaenops ocellatus). Mar Biol 142:1159–1167
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
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 354:132–143
Bureau DP, Harris AM, Cho CY (1999) Apparent digestibility of rendered animal protein ingredients for rainbow trout (Oncorhyncus mykiss). Aquac 180:345–358
Campbell TW, Ellis CK (2007) Avian and exotic animal hematology and cytology. Blackwell, Ames
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 305:102–108
Congleton JL, Wagner T (2006) Blood -chemistry indicators of nutritional status in juvenile salmonids. Fish Biol 69:473–490
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 146:107–114
De Silva SS, Anderson TA (1995) Fish nutrition in aquaculture. Chapman and Hall, London
Evans GO, Watterson CL (2009) General enzymology. In: Animal clinical chemistry, a practical guide for toxicologists and biochemical researchers, 2nd edn. CRC Press, New York
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 13:415–422
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 262:1–12
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 32:502–506
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 38:551–579
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 184:303–314
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 269:514–524
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 43:399–405
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 31:310–317
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 241:173–183
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 20:623–631
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 8:310–316
Hummel BCW (1959) A modified spectrophotometric determination of chymotrypsin, trypsin and thrombin. Can J Biochem Physiol 37:1393–1399
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 6:61–68
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 62:266–272
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 67:259–266
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 20:293–303
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 51:1667–1674
McClatchey KD (2002) Clinical laboratory medicine. Williams and Wilkins, Philadelphia
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 11:239–246
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 302:1–1
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 8:47–51
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 595
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 451:232–240
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 23:181–191
Navarro I, Gutierrez J (1995) Fasting and starvation. Elsevier, Amsterdam
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 106:15103–15110
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 179:13–23
NRC (2011) Nutrient requirements of fish. National Academy Press, Washington, DC
Nya EJ, Austin B (2011) Dietary modulation of digestive enzymes by the administration of feed additives to rainbow trout, Oncorhynchus mykiss Walbaum. Aquac Nutr 17:459–466
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 203–233
Pavlidis MA, Mylonas CC (2011) Sparidae biology and aquaculture of gilthead seabream and other species. Blackwell Publishing Ltd., UK
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 73:591–603
Peres H, Santos S, Oliva-Teles A (2013) Selected plasma biochemistry parameters in gilthead seabream (Sparus aurata) juveniles. J Appl Ichthyol 29:630–636
Peres H, Santos S, Oliva-Teles A (2014) Blood chemistry profile as indicator of nutritional status in European seabass (Dicentrarchus labrax). Fish Physiol Biochem 40:1339–1347
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 259:377–389
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 145–153
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 282:68–74
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 273:118–126
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):233–237
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 66:428–438
Tietz NW, Shuey DF (1993) Lipase in serum- the elusive enzyme: an overview. Clin Chem 39:746–756
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 46:874–883
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 25:1588–1594
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 464:50–59
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 37:40–48
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 322-323:122–127
Acknowledgments
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
This study was financed by Khorramshahr University of Marine Science and Technology, Iran and South Iranian Aquaculture Research Center, Ahwaz, Iran.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hekmatpour, F., Kochanian, P., Marammazi, J.G. et al. 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. Fish Physiol Biochem 45, 599–611 (2019). https://doi.org/10.1007/s10695-019-00619-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-019-00619-4