Evaluation of Enzyme Additives on the Nutritional Use of Feeds with a High Content of Plant Ingredients for Mugil cephalus
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Ingredients and Experimental Feeds
4.2. Analytical Techniques Used
4.3. In Vitro Digestive Hydrolysis Assay
4.4. In Vivo Digestibility Test
4.5. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Tacon, A.G.J.; Metian, M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture 2008, 285, 146–158. [Google Scholar] [CrossRef]
- Naylor, R.L.; Hardy, R.W.; Bureau, D.P.; Chiu, A.; Elliott, M.; Farrell, A.P.; Forster, I.; Gatlin, D.M.; Goldburg, R.J.; Hua, K.; et al. Feeding aquaculture in an era of finite resources. Proc. Natl. Acad. Sci. USA 2009, 106, 15103–15110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abellan, E.; Arnal, I. Múgiles, mújoles o mugílidos. In Diversificación de Especies en la Piscicultura Marina Española; Ministerio de Agricultura, Alimentación y Medio Ambiente: Madrid, Spain, 2013; pp. 506–509. [Google Scholar]
- Brusle, J. Food and Feeding in Grey Mullet. In Aquaculture of Grey Mullet; Oren, O.H., Ed.; Cambridge University Press: Cambridge, UK, 1981; pp. 185–217. [Google Scholar]
- Oren, O.H. Aquaculture of Grey Mullets; Cambridge University Press: Cambridge, UK, 1981; p. 507. [Google Scholar]
- Biswas, G.; De, D.; Thirunavukkarasu, A.R.; Natarajan, M.; Sundaray, J.K.; Kailasam, M.; Kumar, P.; Ghoshal, T.K.; Ponniah, A.G.; Sarkar, A. Effects of stocking density, feeding, fertilization and combined fertilization-feeding on the performances of striped grey mullet (Mugil cephalus L.) fingerlings in brackish water pond rearing systems. Aquaculture 2012, 338, 284–292. [Google Scholar] [CrossRef]
- Gisbert, E.; Mozanzadeh, M.T.; Kotzamanis, Y.; Estévez, A. Weaning wild flathead grey mullet (Mugil cephalus) fry with diets with different levels of fish meal substitution. Aquaculture 2016, 462, 92–100. [Google Scholar] [CrossRef]
- Wassef, E.A.; El Masry, M.H.; Mikhail, F.R. Growth enhancement and muscle structure of striped mullet, Mugil cephalus L., fingerlings by feeding algal meal-based diets. Aquac. Res. 2001, 32 (Suppl. 1), 315–322. [Google Scholar] [CrossRef]
- Kalla, A.; Garg, S.K.; Kaushik, C.P.; Arasu, A.R.T.; Dinodia, G.S. Effect of replacement of fish meal with processed soybean on growth, digestibility and nutrient retention in Mugil cephalus (Linn.) fry. Indian J. Fish. 2003, 50, 509–518. [Google Scholar]
- Jana, N.S.; Sudesh Garg, S.K.; Sabhlok, V.P.; Bhatnagar, A. Nutritive Evaluation of Lysine- and Methionine-Supplemented Raw Vs Heat-Processed Soybean to Replace Fishmeal as a Dietary Protein Source for Grey Mullet, Mugil cephalus, and Milkfish, Chanos chanos. J. Appl. Aquac. 2012, 24, 69–80. [Google Scholar] [CrossRef]
- El-Dahhar, A.A.; Salama, M.A.; Moustafa, Y.T.; Elmorshedy, E.M. Effect of using equal mixture of seaweeds and marine algae in striped mullet (Mugil cephalus) larval diets on growth performance and feed utilization. J. Arab. Aquacult. Soc. 2014, 9, 145–158. [Google Scholar] [CrossRef]
- Gatlin, D.M.; Barrows, F.T.; Brown, P.; Dabrowski, K.; Gaylord, G.; Hardy, R.; Herman, E.; Hu, G.; Krogdahl, A.; Nelson, R.; et al. Expanding the utilization of sustainable plant products in aquafeeds: A review. Aquac. Res. 2007, 38, 551–579. [Google Scholar] [CrossRef]
- Norwegian Scientific Committee. Opinion of the Panel on Animal Feed of the Norwegian Scientific Committee for Food Safety Criteria for Safe Use of Plant Ingredients in Diets for Aquacultured Fish; VKM: Oslo, Norway, 2009. [Google Scholar]
- Navarro, D.M.D.L.; Abelilla, J.J.; Stein, H.H. Structures and characteristics of carbohydrates in diets fed to pigs: A review. J. Anim. Sci. Biotechnol. 2019, 10, 1–17. [Google Scholar] [CrossRef]
- Morales, G.A.; Moyano, F.J.; Marquez, L. In vitro assessment of the effects of phytate and phytase on nitrogen and phosphorus bioaccessibility within fish digestive tract. Anim. Feed Sci. Technol. 2011, 170, 209–221. [Google Scholar] [CrossRef]
- Humer, E.; Schwarz, C.; Schedle, K. Phytate in pig and poultry nutrition. J. Anim. Physiol. Anim. Nutr. 2015, 99, 605–625. [Google Scholar] [CrossRef] [PubMed]
- Castillo, S.; Gatlin, D.M. Dietary supplementation of exogenous carbohydrase enzymes in fish nutrition: A review. Aquaculture 2015, 435, 286–292. [Google Scholar] [CrossRef]
- Cao, L.; Wang, W.; Yang, C.; Yang, Y.; Diana, J.; Yakupitiyage, A.; Luo, Z.; Li, D. Application of microbial phytase in fish feed. Enzyme Microb. Technol. 2007, 40, 497–507. [Google Scholar] [CrossRef]
- Cain, K.D.; Garling, D.L. Pretreatment of Soybean Meal with Phytase for Salmonid Diets to Reduce Phosphorus Concentrations in Hatchery Effluents. Prog. Fish Cult. 1995, 57, 114–119. [Google Scholar] [CrossRef]
- Sugiura, S.H.; Gabaudan, J.; Dong, F.M.; Hardy, R.W. Dietary microbial phytase supplementation and the utilization of phosphorus, trace minerals and protein by rainbow trout (Oncorhynchus mykiss (Walbaum) fed soybean meal based diets. Aquac. Res. 2001, 32, 583–592. [Google Scholar] [CrossRef]
- Yigit, N.O.; Olmez, M. Effects of cellulase addition to canola meal in tilapia (Oreochromis niloticus L.) diets. Aquac. Nutr. 2011, 17, e494–e500. [Google Scholar] [CrossRef]
- Forster, I.; Higgs, D.A.; Dosanjh, B.S.; Rowshandeli, M.; Parr, J. Potential for dietary phytase to improve the nutritive value of canola protein concentrate and decrease phosphorus output in rainbow trout Oncorhynchus mykiss held in 11 °C fresh water. Aquaculture 1999, 179, 109–125. [Google Scholar] [CrossRef]
- Cheng, H.Z.; Liu, Z.H. Enzymatic hydrolysis of lignocellulosic biomass from low to high solids loading. Eng. Life Sci. 2016, 4, 1–11. [Google Scholar]
- Opazo, R.; Ortuzar, F.; Navarrete, P.; Espejo, R.; Romero, J. Reduction of Soybean Meal Non-Starch Polysaccharides and α-Galactosides by Solid-State Fermentation Using Cellulolytic Bacteria Obtained from Different Environments. PLoS ONE 2012, 7, e44783. [Google Scholar] [CrossRef]
- Moyano, F.J.; Saénz de Rodrigáñez, M.A.; Díaz, M.; Tacon, A.G. Application of in vitro digestibility methods in aquaculture: Constraints and perspectives. Rev. Aquac. 2015, 7, 223–242. [Google Scholar] [CrossRef]
- Dalsgaard, J.; Verlhac, V.; Hjermitslev, N.H.; Ekmann, K.S.; Fischer, M.; Klausen, M.; Pedersen, P.B. Effects of exogenous enzymes on apparent nutrient digestibility in rainbow trout (Oncorhynchus mykiss) fed diets with high inclusion of plant-based protein. Anim. Feed Sci. Technol. 2012, 171, 181–191. [Google Scholar] [CrossRef]
- Ai, Q.; Mai, K.; Zhang, W.; Xu, W.; Tan, B.; Zhang, C.; Li, H. Effects of exogenous enzymes (phytase, non-starch polysaccharide enzyme) in diets on growth, feed utilization, nitrogen and phosphorus excretion of Japanese seabass, Lateolabrax japonicus. Comp. Biochem. Physiol. Part A—Mol. Integr. Physiol. 2007, 147, 502–508. [Google Scholar] [CrossRef]
- Jiang, T.T.; Feng, L.; Liu, Y.; Jiang, W.D.; Jiang, J.; Li, S.H.; Tang, L.; Kuang, S.Y.; Zhou, X.Q. Effects of exogenous xylanase supplementation in plant protein-enriched diets on growth performance, intestinal enzyme activities and microflora of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac. Nutr. 2014, 20, 632–645. [Google Scholar] [CrossRef]
- Denstadli, V.; Hillestad, M.; Verlhac, V.; Klausen, M.; Øverland, M. Enzyme pretreatment of fibrous ingredients for carnivorous fish: Effects on nutrient utilisation and technical feed quality in rainbow trout (Oncurhynchus mykiss). Aquaculture 2011, 319, 391–397. [Google Scholar] [CrossRef]
- Knöpfel, T.; Himmerkus, N.; Günzel, D.; Bleich, M.; Hernando, N.; Wagner, C.A. Paracellular transport of phosphate along the intestine. Am. J. Physiol. Liver Physiol. 2019, 317, G233–G241. [Google Scholar] [CrossRef]
- Bakke, A.M.; Glover, C.; Krogdhal, A. Feeding, digestion and absorption of nutrients. In The multifunctional Gut of Fish—Fish Physiology; Groser, M., Farrel, A.P., Brauner, C.J., Eds.; Academic Press: Cambridge, MA, USA, 2011; Volume 30, pp. 57–119. [Google Scholar]
- Coloso, R.M.; King, K.; Fletcher, J.W.; Weis, P.; Werner, A.; Ferraris, R.P. Dietary P regulates phosphate transporter expression, phosphatase activity, and effluent P partitioning in trout culture. J. Comp. Physiol. Part B Biochem. Syst. Environ. Physiol. 2003, 173, 519–530. [Google Scholar] [CrossRef]
- Faulks, R.M.; Southon, S. Challenges to understanding and measuring carotenoid bioavailability. Biochim. Biophys. Acta–Mol. Basis Dis. 2005, 1740, 95–100. [Google Scholar] [CrossRef] [Green Version]
- Dimes, L.E.; Haard, N.F.; Dong, F.M.; Rasco, B.A.; Forster, I.P.; Fairgrieve, W.T.; Arndt, R.; Hardy, R.W.; Barrows, F.T.; Higgs, D.A. Estimation of protein digestibility-II. In vitro assay of protein in salmonid feeds. Comp. Biochem. Physiol. Part A Physiol. 1994, 108, 363–370. [Google Scholar] [CrossRef]
- Rungruangsak-Torrissen, K.; Rustad, A.; Sunde, J.; Eiane, S.A.; Jensen, H.B.; Opstvedt, J.; Nygård, E.; Samuelsen, T.A.; Mundheim, H.; Luzzana, U.; et al. In vitro digestibility based on fish crude enzyme extract for prediction of feed quality in growth trials. J. Sci. Food Agric. 2002, 82, 644–654. [Google Scholar] [CrossRef]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Miller, G.L. Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. 1959, 31, 426–428. [Google Scholar] [CrossRef]
- Douglas, S.G. A rapid method for the determination of pentosans in wheat flour. Food Chem. 1981, 7, 139–145. [Google Scholar] [CrossRef]
- AOAC. Official Methods of Analysis of AOAC International, 16th ed.; AOAC International: Arlington, VA, USA, 1995. [Google Scholar]
- Haug, W.; Lantzsch, H.J. Sensitive method for the rapid determination of phytate in cereals and cereal products. J. Sci. Food Agric. 1983, 34, 1423–1426. [Google Scholar] [CrossRef]
- Morales, G.A.; Moyano, F.J. Application of an in vitro gastrointestinal model to evaluate nitrogen and phosphorus bioaccessibility and bioavailability in fish feed ingredients. Aquaculture 2010, 306, 244–251. [Google Scholar] [CrossRef]
- Walter, H.E. Proteinases: Methods with haemoglobin, casein and azocoll as substrates. In Methods of Enzymatic Analysis; Bergmeyer, H.J., Ed.; Verlag Chemie: Weinheim, Germany, 1984; Volume V, pp. 270–277. [Google Scholar]
- Church, F.C.; Swaisgood, H.E.; Porter, D.H.; Catignani, G.L. Spectrophotometric Assay Using o-Phthaldialdehyde for Determination of Proteolysis in Milk and Isolated Milk Proteins. J. Dairy Sci. 1983, 66, 1219–1227. [Google Scholar] [CrossRef]
Ingredient (in g/100 g d.w.) | FEED 1 | FEED 2 |
---|---|---|
Fishmeal 67/10 | 15.0 | 10.0 |
Soybean meal 47 | 15.0 | 21.8 |
Rapeseed meal | 15.0 | - |
Defatted rice bran | - | 12.0 |
Soybean protein concentrate | 8.0 | 10.0 |
Corn gluten meal 60 | 16.0 | 15.0 |
Guar meal (Korma) | 15.0 | 20.0 |
Fish oil | 4.9 | 4.9 |
Sunflower oil | 3.9 | 3.9 |
Soy lecithin | 1.0 | 1.0 |
Vitamin/mineral premix | 0.1 | 0.1 |
Taurin | 0.5 | 0.5 |
Yeast | 0.7 | 0.8 |
Cr2O3 | 1.0 | 1.0 |
Starch | 4.4 | - |
Proximate Composition (in g/100 g) | ||
Crude protein | 45.00 | 45.01 |
Crude fat | 13.00 | 13.00 |
Digestible carbohydrates (starch + oligosaccharides) | 5.85 | 9.00 |
NSP | 23.90 | 25.17 |
Ash | 5.95 | 6.42 |
Phosphorus | 0.89 | 0.87 |
Phytate P | 0.28 | 0.33 |
Experimental Feed | Total Protein | Soluble Protein | Reducing Sugars | Pentoses | Phosphorus | Phytate |
---|---|---|---|---|---|---|
FEED 1 | 46.85 ± 1.18 | 6.19 ± 0.66 Aa | 0.67 ± 0.07 Aa | 0.24 ± 0.02 Aa | 1.33 ± 0.03 | 0.44 ± 0.04 Aa |
FEED 1 + enz | 46.85 ± 1.18 | 4.12 ± 0.24 b | 5.94 ± 0.34 b | 0.83 ± 0.04 b | 1.30 ± 0.01 | 0.21 ± 0.00 b |
FEED 2 | 46.96 ± 0.84 | 2.94 ± 0.44 Ba | 1.12 ± 0.04 Ba | 0.28 ± 0.01 Aa | 1.55 ± 0.20 | 0.96 ± 0.02 Ba |
FEED 2 + enz | 46.96 ± 0.84 | 4.82 ± 0.37 b | 5.61 ± 0.29 b | 0.82 ± 0.04 b | 1.41 ± 0.10 | 0.56 ± 0.02 b |
Experimental Feed | Amino Acids (mg) | Amino Acids (%) | Pentoses (mg) | Pentoses (%) | P (mg) | P (%) |
---|---|---|---|---|---|---|
FEED 1 | 110.65 ± 0.87 Aa | 39.36 ± 0.31 Aa | 1.32 ± 0.13 Aa | 0.99 ± 0.09 Aa | 4.63 ± 0.50 A | 58.0 ± 6.21 A |
FEED 1 + enz | 115.76 ± 1.02 b | 41.18 ± 0.36 b | 3.32 ± 0.34 b | 2.31 ± 0.27 b | 4.62 ± 0.07 | 59.2 ± 0.85 |
FEED 2 | 72.73 ± 0.19 Ba | 25.81 ± 0.07 Ba | 1.14± 0.11 Aa | 0.76 ± 0.08 Aa | 3.07 ± 0.02 B | 33.0 ± 0.26 B |
FEED 2 + enz | 85.91 ± 13.07 b | 30.49 ± 4.63 b | 3.48± 0.08 b | 2.31 ± 0.05 b | 2.51 ± 0.27 | 39.7 ± 3.15 |
Experimental Feed | Protein | Phosphorus | Phytate |
---|---|---|---|
FEED 1 | 89.6 ± 1.0 Aa | 47.9 ± 7.1 Aa | 55.2 ± 2.5 Aa |
FEED 1+ enz | 92.3 ± 0.4 b | 38.5 ± 3.9 a | 54.6 ± 5.0 a |
FEED 2 | 91.9 ± 0.1 Aa | 70.1 ± 3.0 Ba | 62.4 ± 1.5 Ba |
FEED 2 + enz | 91.9 ± 0.5 a | 61.0 ± 6.0 b | 52.9 ± 5.7 b |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Martínez, F.P.; Bermúdez, L.; Aznar, M.J.; Moyano, F.J. Evaluation of Enzyme Additives on the Nutritional Use of Feeds with a High Content of Plant Ingredients for Mugil cephalus. Fishes 2019, 4, 56. https://doi.org/10.3390/fishes4040056
Martínez FP, Bermúdez L, Aznar MJ, Moyano FJ. Evaluation of Enzyme Additives on the Nutritional Use of Feeds with a High Content of Plant Ingredients for Mugil cephalus. Fishes. 2019; 4(4):56. https://doi.org/10.3390/fishes4040056
Chicago/Turabian StyleMartínez, Francisca P., Laura Bermúdez, María J. Aznar, and Francisco J. Moyano. 2019. "Evaluation of Enzyme Additives on the Nutritional Use of Feeds with a High Content of Plant Ingredients for Mugil cephalus" Fishes 4, no. 4: 56. https://doi.org/10.3390/fishes4040056