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Partial replacement of fishmeal by brewers yeast (Saccaromyces cerevisae) in diets for sea bass (Dicentrarchus labrax) juveniles
Aquaculture 202 Ž2001. 269–278 www.elsevier.comrlocateraqua-online
Partial replacement of fishmeal by brewers yeast žSaccaromyces cereÕisae / in diets for sea bass žDicentrarchus labrax / juveniles Aires Oliva-Teles ) , Paula Gonc¸alves Departamento de Zoologia e Antropologia e CIIMAR (Centro de InÕestigac¸ao ˜ Marinha e Ambiental), Faculdade de Ciencias da UniÕersidade do Porto, 4099-002 Porto, Portugal ˆ
Abstract A trial was conducted to test the effect of partial replacement of fishmeal ŽDanish LT fishmeal —the only protein source in the control diet. by brewers yeast, in isonitrogenous Ž48% CP. and isoenergetic Ž22 MJ kgy1 . diets for sea bass juveniles with an initial average weight of 12 g. Diets were formulated to include 0%, 10%, 20%, 30% or 50% of dietary N from yeast Ždiets D0, D10, D20, D30, D50, respectively.; another diet supplemented with methionine Ždiet D50M. was also prepared. Each diet was distributed by hand to satiation to duplicate groups of 25 fish and the growth trial lasted 12 weeks. During the trial, feed intake Žg kgy1 dayy1 . was identical in all groups. At the end of the trial growth rate was not significantly different among groups, except for the D50M diet, which was significantly lower than diet D30. Feed conversion was better for diets D10, D20 and D30, containing yeast than for the control diet. N retention Ž% N intake. was significantly higher in fish fed diets containing yeast Žexcept for the D50M diet. than in those fed the control diet. There were no significant differences among groups in energy retention Ž% E intake.. The protein content of the fish was significantly higher in fish fed diets containing yeast Žexcept for the D50M diet. than in those fed the control diet. Apparent digestibility of the diets was determined in a separate trial with fish weighing 62 g. Feces collection was performed according to the Guelph system. Apparent digestibility coefficients of dry matter and energy significantly decreased with the increase of dietary yeast level. ADC of protein was significantly lower for the D50 diet than for the other diets. Results of this trial indicate that brewers yeast can replace 50% of fishmeal protein with no negative effects in fish performance. Moreover, the inclusion of up to 30% brewers yeast in the
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Corresponding author. Tel.: q351-22-3401507; fax: q351-22-3401511. E-mail address: [email protected] ŽA. Oliva-Teles..
0044-8486r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 0 1 . 0 0 7 7 7 - 3
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diet improved feed efficiency. There was no beneficial effect of supplementing the brewers yeast diets with methionine. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Sea bass; Fishmeal replacement; Brewers yeast; Growth
1. Introduction Fishmeal is a limited feed resource, and serious concern exists on the future availability of this feedstuff for incorporation in fish diets ŽHardy, 1996; Sargent and Tacon, 1999.. Nonetheless, fishmeal is still the main or even the only protein source used in carnivorous fish diets, namely in marine fishes like sea bass. This is because fishmeal has the most adequate amino acid profile, is a very good source of essential fatty acids and minerals and is highly palatable. The evaluation of alternative protein sources to fishmeal is therefore a research priority. Among these, plant feedstuffs have received most attention in recent years; however, due to amino acid unbalances, presence of anti-nutritional factors and low palatability, a high level of replacement of fish meal with plant feedstuffs is generally not well accepted. Single cell proteins ŽSCP. include micro algae, bacteria and yeast, and are alternative non-conventional protein sources that are frequently used as feed ingredients for fish, due to the nutritional value of their nutrients such as proteins, B-vitamins, pigments and complex carbohydrates, such as glucans ŽSanderson and Jolly, 1994; Tacon, 1994.. Among SCP, yeasts have been the most used within aquafeeds ŽTacon, 1994.. Some yeast, like Candida sp. and Saccharomyces cereÕisae, are also believed to have immunostimulatory properties by virtue of their complex carbohydrate components and nucleic acid content ŽAnderson et al., 1995.. Compared to fishmeal, the majority of the SCP are either deficient in one or more amino acids or they suffer from an amino acid imbalance ŽTacon and Jackson, 1985; Kiessling and Askbrandt, 1993.. The supplementation of yeast-based diets with the deficient amino acids was shown to have beneficial effects on fish growth ŽNose, 1974; Bergstrom, 1979; Spinelli et al., 1979; Mahnken et al., 1980; Murray and Marchant, 1986.. Another concern with SCP is their high concentration in nucleic acids, ranging from 5% to 12% in yeast and 8% to 16% in bacteria ŽSchulz and Oslage, 1976.. In brewers yeast, nucleic acid nitrogen is present mostly in the form of RNA and represents about 20% to 25% of the nitrogen ŽRumsey et al., 1991a.. In humans and most monogastric animals, an excess of dietary nucleic acids supply is toxic, as the capacity of excretion of the uric acid formed is limited, leading to deposits of uric acid in the body and to possible disorders of metabolism ŽSchulz and Oslage, 1976; Tuse, ´ 1984.. However, no such an effect was found in fish due to their very active liver uricase ŽDe la Huiguera et al., 1981; Rumsey et al., 1991a.. In rainbow trout, Tiews et al. Ž1979. succeeded to obtain with yeast-based diets supplemented with methionine growth rates equivalent to that of the control diet. However, other attempts of using yeasts as the sole or the main dietary protein source
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resulted in reductions of fish performances ŽBeck et al., 1979; Mahnken et al., 1980; Rumsey et al, 1991a.. In practice, yeasts have been incorporated in rations at levels of 15–30%, resulting in a 25–50% replacement of the fishmeal content ŽTacon and Jackson, 1985; Tacon, 1994.. In sea bass, different yeasts were already evaluated as partial substitutes of fishmeal protein with different results ŽAlliott et al., 1979; Metailler and Huelvan, 1993.. The aim of this work is to compare the effect of replacing fishmeal with brewers yeast at levels between 10% and 50% of the dietary protein on the performance of sea bass juveniles.
2. Material and methods This study was performed at the Marine Zoology Station, at Porto, with sea bass Ž Dicentrarchus labrax . juveniles obtained from a commercial fish farm, and consisted of a growth trial and a digestibility trial. The growth trial was carried out in a water recirculation system equipped with a battery of 12 cylindrical fiberglass tanks of 80-l water capacity. Each tank was stocked with 25 fish with an average weight of 12 g. To duplicate groups of these fish was distributed one of the experimental diets whose composition is presented in Table 1. The fish were fed by hand to apparent visual satiety twice a day, except the day before weighing. The trial lasted 12 weeks and during this period the fish were bulk weighed every 2 weeks. During the trial, water temperature averaged 22 8C and salinity ranged from 32‰ to 34‰. Ten fish from the initial stock population and five fish from each tank at the end of the trial were collected and frozen for subsequent body composition analysis. Diets were formulated to be isonitrogenous and isoenergetic and were prepared as dry pellets in an experimental pellet mill ŽCPM.. In the control diet ŽD0. fishmeal was the only protein source and in the other diets brewers yeast Ž S. cereÕisae . was incorporated to replace 10%, 20%, 30% or 50% of the fishmeal protein Ždiets D10, D20, D30 and D50, respectively.. Another diet was formulated similar to diet D50 but supplemented with methionine ŽD50M.. The digestibility trial was performed in a thermoregulated recirculating water system equipped with a battery of six fiberglass tanks of 55-l water capacity, designed according to Cho et al. Ž1982., and covered with a transparent floating lid. A feces settling column was connected to the outlet of each tank. Each tank contained 25 fish with an average individual weight of 62 g, which were fed by hand, two times a day, to apparent visual satiety. Water temperature during the trial was maintained at 22 8C and salinity ranged from 32‰ to 34‰. The experimental protocol consisted of three periods of 17 days each. In each period, the fish of each tank received a different diet; the fish were accustomed to the diets during 3 days and feces were collected during the next 14 days. Then, diets were randomly changed between tanks and the same procedure was repeated. Feces from each tank in each period were pooled and frozen until analysis, giving a total of three samples for each diet. Chromic oxide was included to the diets as an external marker.
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Table 1 Composition of the experimental diets Diet:
D0
D10
D20
D30
D50
D50M
Ingredients (% DM) Fish meal a Brewers yeast b Cod liver oil Yellow dextrin L-methionine Vitamin premix c Mineral premix d Choline chloride Ž50%. Lignin sulphonate Chromic oxide
59.6 0 7.6 28.8 0 0.5 1.0 0.5 1.5 0.5
53.7 11.0 8.0 23.3 0 0.5 1.0 0.5 1.5 0.5
47.7 21.9 8.4 18.0 0 0.5 1.0 0.5 1.5 0.5
41.7 32.9 8.8 12.6 0 0.5 1.0 0.5 1.5 0.5
29.8 54.8 9.6 1.8 0 0.5 1.0 0.5 1.5 0.5
29.8 54.8 9.6 1.8 0.56 0.5 1.0 0.5 1.5 0.5
Proximate analysis (% DM) Dry matter Protein ŽN=6.25. Lipids Ash Chromic oxide Gross energy ŽkJ gy1 .
87.2 49.0 15.6 8.8 0.43 21.7
86.9 49.0 15.2 9.0 0.44 22.2
87.5 48.7 15.6 9.3 0.42 22.1
86.9 48.6 15.4 9.4 0.40 22.3
87.1 49.1 16.3 9.8 0.41 22.7
87.6 48.2 15.4 9.8 0.45 22.7
a
Danish LT fish meal ŽP: 80.5%; L: 12.6%.. Gist Brocades ŽP: 43.8%; L: 10.5%.. c Vitamins Žmg kgy1 diet.: retinol, 15000 ŽIU kgy1 diet.; calciferol, 1667 ŽIU kgy1 diet.; alpha tocopherol, 83.3; menadion sodio bis., 16.6; thiamin, 12.5; riboflavin, 12.5; Ca pantothenate, 33.3; nicotinic acid, 116.7; pyridoxine, 8.3; folic acid, 4.2; cyanocobalamin, 0.04; biotin, 0.5; ascorbic acid Žstay C., 83.3; inositol, 250. d Minerals Žmg kgy1 diet.: cobalt sulphate, 1.91; copper sulphate, 19.6; iron sulphate, 200; sodium fluoride, 2.21; potassium iodide, 0.78; magnesium oxide, 830; manganese oxide, 26; sodium selenite, 0.66; zinc oxide, 37.5; dicalcium phosphate, 8.02 Žg kgy1 diet.; potassium chloride, 1.15 Žg kgy1 diet.; sodium chloride, 0.44 Žg kgy1 diet.. b
Apparent digestibility coefficients ŽADC. of the diets was determined as follows: ADC Ž % . s 1 y Ž Ž %IF = % NFs . r Ž % IFs = % NF . . = 100 where IF is the % of indicator in the feed, NF is the % of nutrient or energy in the feed, IFs is the % of indicator in the feces and NFs is the % of nutrient or energy in the feces. ADC of protein ŽADCp. of brewers yeast was estimated as follows: ADCps ADCp experimental diet y Ž ADCp control diet = Ž 1 y a . . ra where a s Ž% protein from brewers yeast in the dietr% protein in the diet.. Chemical analyses of the diets, whole fish and feces were carried out as follows: dry matter after drying in an oven at 105 8C until constant weight; ash by incineration in a muffle furnace at 450 8C for 16 h; protein ŽN = 6.25. by the Kjeldahl method after acid digestion, using Kjeltec digestion and distillation units; lipids by petroleum ether extraction in a Soxtec HT System apparatus; energy by direct combustion in an adiabatic bomb calorimeter ŽPARR model 1261.; chromic oxide of diets and feces by acid
Diet:
D0
D10
D20
D30
D50
D50M
Initial weight Žg. Final weight Žg. Feed intake Žg kgy1 dayy1 . Specific growth rate Ž%. Feed intake: weight gain Weight gain: protein intake Protein retention Ž% protein intake. Žg kgy1 weight gain. Energy retention Ž% energy intake. ŽMJ kgy1 weight gain.
12.0 40.7"1.0ab 37.9"4.8 1.46"0.03ab 1.48"0.01a 1.38"0.01a 20.8"0.6a 150.7"2.8a 26.0"1.9 8.3"0.4
11.9 42.8"0.4ab 41.5"0.2 1.52"0.01ab 1.35"0.01bc 1.52"0.02bc 25.6"0.6bc 168.9"2.5c 29.8"0.9 8.9"0.1
11.9 42.9"0.8ab 44.4"1.3 1.53"0.02ab 1.38"0.02b 1.44"0.0ab 24.0"0.2bc 167.2"0.7bc 27.1"1.6 8.6"0.3
11.9 45.6"0.9b 42.9"0.4 1.60"0.02b 1.28"0.02c 1.61"0.03c 26.5"0.6c 164.5"0.9bc 30.7"2.3 8.7"0.3
12.0 40.9"1.8ab 39.5"2.2 1.46"0.05ab 1.42"0.0ab 1.49"0.03ab 24.7"0.8bc 165.8"1.4bc 27.6"0.4 8.6"0.1
11.9 39.2"0.8a 38.9"1.0 1.42"0.02a 1.43"0.01ab 1.45"0.01ab 22.8"0.2ab 157.6"2.4ab 25.8"1.2 8.4"0.3
Values are means"s.d. For each row, values followed by different letters are significantly different Ž P - 0.05..
A. OliÕa-Teles, P. Gonc¸alÕes r Aquaculture 202 (2001) 269–278
Table 2 Growth and feed utilization of sea bass juveniles fed the experimental diets
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274
Table 3 Body composition of sea bass juveniles fed the experimental diets Žfresh weight basis. Diet:
Initial Final
Water content Ž%. Protein Ž%. Lipids Ž%. Ash Ž%. Energy ŽkJ gy1 . Hepatosomatic index Ž%. Visceral index Ž%.
73.7 14.8 6.5 5.0 5.8
D0
D10
D20
D30
D50
D50M
69.9"1.4 15.0"0.2a 12.1"0.8 3.8"0.3 7.6"0.4 2.1"0.0 13.1"1.8
69.0"0.1 16.3"0.2c 11.8"0.6 3.6"0.1 8.0"0.1 2.3"0.1 12.5"1.2
69.5"0.6 16.2"0.1bc 10.9"0.4 3.9"0.0 7.8"0.3 2.1"0.2 15.8"5.1
69.3"0.2 16.0"0.1bc 11.6"0.6 3.8"0.1 8.0"0.3 2.2"0.4 13.4"1.9
69.2"0.1 16.0"0.1bc 11.2"0.3 4.1"0.2 7.8"0.0 2.2"0.2 14.2"3.2
70.0"0.9 15.4"0.2ab 11.1"0.1 3.9"0.2 7.6"0.3 2.5"0.2 10.8"1.0
Values are means"s.d. For each row, values followed by different letters are significantly different Ž P - 0.05..
digestion according to Furukawa and Tsukahara Ž1966.. Fish and feces were homogenized and dried before analyses. Statistical analysis consisted of one-way ANOVA, using the probability level of 0.05 for rejection of the null hypothesis. After ANOVA, significant differences among means were determined by Tukey’s multiple range test. All statistical analyses were performed using a Statgraphics Plus version 4 for Windows software package.
3. Results Inclusion of brewers yeast to the diets did not affect growth rate nor feed intake but feed conversion significantly improved until a fishmeal protein replacement level of 30% ŽTable 2.. Protein efficiency ratio Žweight gain: protein intake. was significantly higher in fish fed diets D10 and D30 than in those fed the control diet ŽTable 2.. Protein retention, both per unit of weight gain and as percentage of protein intake was significantly higher in fish fed the brewers yeast-containing diets than the control diet ŽTable 2.. There were no significant differences in energy retention among experimental groups. The inclusion of a methionine supplement to diet D50M did not improve results. Indeed, fish fed the supplemented diet performed slightly worse than those fed diet D50 that had the same composition, except for the amino acid supplement ŽTable 2..
Table 4 Apparent digestibility coefficients of the experimental diets Diet:
D0
D10
D20
D30
D50
D50M
Dry matter Ž%. Protein Ž%. Energy Ž%.
86.8"0.3a 92.8"0.2a 95.3"0.2a
84.3"0.3ab 92.5"0.3a 93.2"0.2ab
82.2"0.1bc 92.0"0.3ab 90.8"0.3bc
79.1"0.8c 91.2"0.6ab 88.9"0.5c
71.0"0.6d 86.7"0.5c 82.3"1.1d
72.3"0.6d 90.3"0.6b 82.5"1.1d
Values are means"s.d. For each row values followed by different letters are significantly different Ž P - 0.05..
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At the end of the trial there were no significant differences in whole body composition among experimental groups, except for the protein content which was significantly higher in fish fed the brewers yeast containing diets than the control diet ŽTable 3.. Apparent digestibility coefficients ŽADC. of dry matter and energy significantly decreased with the increase of brewers yeast to the diets ŽTable 4.. ADC of protein of diets D50 and D50M were significantly lower than in the other diets. ADC of brewers yeast protein was lower Ž88.3%. than that of fishmeal protein Ž92.8%..
4. Discussion Feed conversion of sea bass improved with the inclusion of up to 30% dietary protein from brewers yeast. There were no significant differences in growth performance with the replacement of 50% of fishmeal protein by brewer’s yeast, the maximum level tested in this study Žrepresenting an incorporation of 55% brewers yeast in the diet, on a dry weight basis.. Also in sea bass, Metailler and Huelvan Ž1993. tested the inclusion of 10%, 20% and 30% of lactic yeast, bakers yeast and brewers yeast in isoproteic fishmeal-based diets. The authors found no differences in growth and feed utilization among groups, except for fish fed diets including brewers yeast. In this case, and contrary to our results, fish fed diets with more than 10% brewers yeast performed worse than those fed the control diet. As in our study, Alliot et al. Ž1979. found no negative effect on growth performance of sea bass fed diets with 50% dietary fishmeal protein replaced by an alkane yeast protein. The inclusion of 5% to 15% yeast in the diets was even beneficial, improving feed efficiency. In other species, a beneficial effect on fish performance was also noticed at moderate dietary inclusion levels of yeast ŽOhmae et al., 1979; Rumsey et al., 1991a.. Although fish seem to be prepared to cope with the high nucleic acids content of SCP, due to their very active liver uricase ŽDe la Huiguera et al., 1981; Rumsey et al., 1991a., some authors consider that high levels of nucleic acids may have a deleterious effect ŽTacon and Cooke, 1980; Davies and Wareham, 1988.. Indeed, RNA and purine basis were implicated as potent depressors of feed intake in farm animals ŽRumsey et al., 1992.. In fish, Tacon and Cooke Ž1980. found that a nucleic acid extract of bacterial origin depressed feed intake of rainbow trout when incorporated in the diet at a level equivalent to a bacterial SCP intake of 50%. Rumsey et al. Ž1991a. observed a feed intake depression in rainbow trout due to reduced acceptability of diets including more than 25% of brewers yeast, and Atack and Matty Ž1979. observed a reduction of feed intake in rainbow trout fed a brewers yeast diet comparatively to an herring meal based diet. On the contrary, when rainbow trout was fed a diet including a yeast nucleic acid extract corresponding to a dietary level of 50% brewers yeast, no negative effect on feed intake was observed ŽRumsey et al., 1992.. Also in the present trial feed intake of sea bass was not affected among groups, suggesting that, within the levels tested, brewers yeast does not affect diet palatability or depresses feed intake.
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In this trial, N-utilization of fish fed the brewers yeast diets was significantly higher than in the control diet. On the contrary, in rainbow trout the replacement of casein by a mixed SCP biomass Žincluding predominantly yeasts. in semi-purified diets, although not affecting growth negatively affected N utilization ŽMurray and Marchant, 1986.. However, as in the present study, Rumsey et al. Ž1992. also observed an increase of N retention in rainbow trout fed with increasing levels of yeast extract. From this the authors conclude that some of the non-protein nitrogen was used as source of non-essential amino acids. Yeast protein is deficient in sulphur amino acids and several studies showed that supplementation of the diets with methionine improved fish growth ŽSpinelli et al., 1979; Mahnken et al., 1980; Murray and Marchant, 1986.. In this study, however, the supplementation of diet D50 with methionine did not improve sea bass performance. Kaushik and Luquet Ž1980. also did not find any positive influence of sulphur amino acid supplementation of a bacterial SCP on the growth performances of rainbow trout. On the contrary, supplementation with sulphur amino acids depressed rainbow trout growth to varying degrees. According to Rumsey et al. Ž1990. the lower performance of fish fed diets containing high levels of brewers yeast may be caused by intact yeast cells, as probably not all intracellular ingredients become available to the fish. Indeed, Rumsey et al. Ž1991b. found that digestibility of intact brewers yeast in rainbow trout is significantly lower than that of disrupted cells. In accordance to this finding, Rumsey et al. Ž1990. observed that brewers yeast could replace 50% of total nitrogen in the diet of lake trout when the yeast cell walls were disrupted but a growth depression occurred when intact yeasts were used. In this study, the ADC of the diets were high, although the ADC of dry matter and energy decreased with the inclusion level of brewers yeast to the diets, indicating a lower digestible energy value of brewers yeast than the feedstuffs it replaced in the diets. The estimated ADC of fishmeal protein is within the expected ADC values for high quality fishmeal in sea bass ŽGomes da Silva and Oliva-Teles, 1998.. The ADC of brewers yeast protein was also high Ž88.3%. but lower than that of fishmeal Ž92.8%.. This value is considerably higher than that estimated by Metailler and Huelvan Ž1993. for brewers yeast in sea bass, but is similar to that obtained for an alkane grown yeast by Alliot et al. Ž1979.. In rainbow trout, both true and apparent digestibility coefficients of brewers yeast protein were estimated to be lower than in sea bass ŽAtack and Matty, 1979; Rumsey et al., 1991b.. In conclusion, results of this trial indicate that brewers yeast can replace 50% of fishmeal protein, with no negative effects in sea bass juvenile performance. Moreover, the inclusion of up to 30% brewers yeast in the diet improved feed efficiency and protein utilization. Acknowledgements This work was partially sponsored by PRAXIS XXI and FEDER Žproject PRAXIS 3r3.2rAQr2009r95.. We would like to thank DSM Portugal Žformerly Gist-Brocades. for kindly providing the brewers yeast used in this trial.
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Rumsey, G.L., Winfree, R.A., Hughes, S.G., 1992. Nutritional value of dietary nucleic acids and purine bases to rainbow trout Ž Oncorhynchus mykiss .. Aquaculture 108, 97–110. Sanderson, G.W., Jolly, S.O., 1994. The value of Phaffia yeast as a feed ingredient for salmonid fish. Aquaculture 124, 193–200. Sargent, J.R., Tacon, A.G.J., 1999. Development of farmed fish: a nutritionally necessary alternative to meat. Proc. Nutr. Soc. 58, 377–383. Schulz, E., Oslage, H.J., 1976. Composition and nutritive value of single-cell protein ŽSCP.. Anim. Feed Sci. Technol. 1, 9–24. Spinelli, J., Mahnken, C., Steinberg, M., 1979. Alternate sources of proteins for fish meal in salmonid diets. In: Halver, J.E., Tiews, K. ŽEds.., 1979. Finfish Nutrition and Fishfeed Technology, vol. II. Heenemann, Berlin, pp. 131–142. Tacon, A.G.J., 1994. Feed ingredients for carnivorous fish species: alternatives to fishmeal and other dietary resources. FAO Fish. Circ. 881, 35 pp. Tacon, A.G.J., Cooke, D.J., 1980. Nutritional value of dietary nucleic acids to trout. Nutr. Reports Int. 22, 631–640. Tacon, A.G.J., Jackson, A.J., 1985. Utilisation of conventional and unconventional protein sources in practical fish feeds. In: Cowey, C.B., Mackie, A.M., Bell, J.G. ŽEds.., Nutrition and Feeding in Fish. Academic Press, London, pp. 119–145. Tiews, K., Koops, H., Gropp, J., Beck, H., 1979. Compilation of fish meal-free diets obtained in rainbow trout Ž Salmo gairdneri . feeding experiments at Hamburg Ž1970–1977r78.. In: Halver, J.E., Tiews, K. ŽEds.., 1979. Finfish Nutrition and Fishfeed Technology, vol. II. Heenemann, Berlin, pp. 219–228. Tuse, ´ D., 1984. Single-cell protein: current status and future prospects. CRC Crit. Rev. Food Sci. Nutr. 19, 273–325.
Partial replacement of fishmeal by brewers yeast žSaccaromyces cereÕisae / in diets for sea bass žDicentrarchus labrax / juveniles Aires Oliva-Teles ) , Paula Gonc¸alves Departamento de Zoologia e Antropologia e CIIMAR (Centro de InÕestigac¸ao ˜ Marinha e Ambiental), Faculdade de Ciencias da UniÕersidade do Porto, 4099-002 Porto, Portugal ˆ
Abstract A trial was conducted to test the effect of partial replacement of fishmeal ŽDanish LT fishmeal —the only protein source in the control diet. by brewers yeast, in isonitrogenous Ž48% CP. and isoenergetic Ž22 MJ kgy1 . diets for sea bass juveniles with an initial average weight of 12 g. Diets were formulated to include 0%, 10%, 20%, 30% or 50% of dietary N from yeast Ždiets D0, D10, D20, D30, D50, respectively.; another diet supplemented with methionine Ždiet D50M. was also prepared. Each diet was distributed by hand to satiation to duplicate groups of 25 fish and the growth trial lasted 12 weeks. During the trial, feed intake Žg kgy1 dayy1 . was identical in all groups. At the end of the trial growth rate was not significantly different among groups, except for the D50M diet, which was significantly lower than diet D30. Feed conversion was better for diets D10, D20 and D30, containing yeast than for the control diet. N retention Ž% N intake. was significantly higher in fish fed diets containing yeast Žexcept for the D50M diet. than in those fed the control diet. There were no significant differences among groups in energy retention Ž% E intake.. The protein content of the fish was significantly higher in fish fed diets containing yeast Žexcept for the D50M diet. than in those fed the control diet. Apparent digestibility of the diets was determined in a separate trial with fish weighing 62 g. Feces collection was performed according to the Guelph system. Apparent digestibility coefficients of dry matter and energy significantly decreased with the increase of dietary yeast level. ADC of protein was significantly lower for the D50 diet than for the other diets. Results of this trial indicate that brewers yeast can replace 50% of fishmeal protein with no negative effects in fish performance. Moreover, the inclusion of up to 30% brewers yeast in the
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Corresponding author. Tel.: q351-22-3401507; fax: q351-22-3401511. E-mail address: [email protected] ŽA. Oliva-Teles..
0044-8486r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 0 1 . 0 0 7 7 7 - 3
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diet improved feed efficiency. There was no beneficial effect of supplementing the brewers yeast diets with methionine. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Sea bass; Fishmeal replacement; Brewers yeast; Growth
1. Introduction Fishmeal is a limited feed resource, and serious concern exists on the future availability of this feedstuff for incorporation in fish diets ŽHardy, 1996; Sargent and Tacon, 1999.. Nonetheless, fishmeal is still the main or even the only protein source used in carnivorous fish diets, namely in marine fishes like sea bass. This is because fishmeal has the most adequate amino acid profile, is a very good source of essential fatty acids and minerals and is highly palatable. The evaluation of alternative protein sources to fishmeal is therefore a research priority. Among these, plant feedstuffs have received most attention in recent years; however, due to amino acid unbalances, presence of anti-nutritional factors and low palatability, a high level of replacement of fish meal with plant feedstuffs is generally not well accepted. Single cell proteins ŽSCP. include micro algae, bacteria and yeast, and are alternative non-conventional protein sources that are frequently used as feed ingredients for fish, due to the nutritional value of their nutrients such as proteins, B-vitamins, pigments and complex carbohydrates, such as glucans ŽSanderson and Jolly, 1994; Tacon, 1994.. Among SCP, yeasts have been the most used within aquafeeds ŽTacon, 1994.. Some yeast, like Candida sp. and Saccharomyces cereÕisae, are also believed to have immunostimulatory properties by virtue of their complex carbohydrate components and nucleic acid content ŽAnderson et al., 1995.. Compared to fishmeal, the majority of the SCP are either deficient in one or more amino acids or they suffer from an amino acid imbalance ŽTacon and Jackson, 1985; Kiessling and Askbrandt, 1993.. The supplementation of yeast-based diets with the deficient amino acids was shown to have beneficial effects on fish growth ŽNose, 1974; Bergstrom, 1979; Spinelli et al., 1979; Mahnken et al., 1980; Murray and Marchant, 1986.. Another concern with SCP is their high concentration in nucleic acids, ranging from 5% to 12% in yeast and 8% to 16% in bacteria ŽSchulz and Oslage, 1976.. In brewers yeast, nucleic acid nitrogen is present mostly in the form of RNA and represents about 20% to 25% of the nitrogen ŽRumsey et al., 1991a.. In humans and most monogastric animals, an excess of dietary nucleic acids supply is toxic, as the capacity of excretion of the uric acid formed is limited, leading to deposits of uric acid in the body and to possible disorders of metabolism ŽSchulz and Oslage, 1976; Tuse, ´ 1984.. However, no such an effect was found in fish due to their very active liver uricase ŽDe la Huiguera et al., 1981; Rumsey et al., 1991a.. In rainbow trout, Tiews et al. Ž1979. succeeded to obtain with yeast-based diets supplemented with methionine growth rates equivalent to that of the control diet. However, other attempts of using yeasts as the sole or the main dietary protein source
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resulted in reductions of fish performances ŽBeck et al., 1979; Mahnken et al., 1980; Rumsey et al, 1991a.. In practice, yeasts have been incorporated in rations at levels of 15–30%, resulting in a 25–50% replacement of the fishmeal content ŽTacon and Jackson, 1985; Tacon, 1994.. In sea bass, different yeasts were already evaluated as partial substitutes of fishmeal protein with different results ŽAlliott et al., 1979; Metailler and Huelvan, 1993.. The aim of this work is to compare the effect of replacing fishmeal with brewers yeast at levels between 10% and 50% of the dietary protein on the performance of sea bass juveniles.
2. Material and methods This study was performed at the Marine Zoology Station, at Porto, with sea bass Ž Dicentrarchus labrax . juveniles obtained from a commercial fish farm, and consisted of a growth trial and a digestibility trial. The growth trial was carried out in a water recirculation system equipped with a battery of 12 cylindrical fiberglass tanks of 80-l water capacity. Each tank was stocked with 25 fish with an average weight of 12 g. To duplicate groups of these fish was distributed one of the experimental diets whose composition is presented in Table 1. The fish were fed by hand to apparent visual satiety twice a day, except the day before weighing. The trial lasted 12 weeks and during this period the fish were bulk weighed every 2 weeks. During the trial, water temperature averaged 22 8C and salinity ranged from 32‰ to 34‰. Ten fish from the initial stock population and five fish from each tank at the end of the trial were collected and frozen for subsequent body composition analysis. Diets were formulated to be isonitrogenous and isoenergetic and were prepared as dry pellets in an experimental pellet mill ŽCPM.. In the control diet ŽD0. fishmeal was the only protein source and in the other diets brewers yeast Ž S. cereÕisae . was incorporated to replace 10%, 20%, 30% or 50% of the fishmeal protein Ždiets D10, D20, D30 and D50, respectively.. Another diet was formulated similar to diet D50 but supplemented with methionine ŽD50M.. The digestibility trial was performed in a thermoregulated recirculating water system equipped with a battery of six fiberglass tanks of 55-l water capacity, designed according to Cho et al. Ž1982., and covered with a transparent floating lid. A feces settling column was connected to the outlet of each tank. Each tank contained 25 fish with an average individual weight of 62 g, which were fed by hand, two times a day, to apparent visual satiety. Water temperature during the trial was maintained at 22 8C and salinity ranged from 32‰ to 34‰. The experimental protocol consisted of three periods of 17 days each. In each period, the fish of each tank received a different diet; the fish were accustomed to the diets during 3 days and feces were collected during the next 14 days. Then, diets were randomly changed between tanks and the same procedure was repeated. Feces from each tank in each period were pooled and frozen until analysis, giving a total of three samples for each diet. Chromic oxide was included to the diets as an external marker.
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Table 1 Composition of the experimental diets Diet:
D0
D10
D20
D30
D50
D50M
Ingredients (% DM) Fish meal a Brewers yeast b Cod liver oil Yellow dextrin L-methionine Vitamin premix c Mineral premix d Choline chloride Ž50%. Lignin sulphonate Chromic oxide
59.6 0 7.6 28.8 0 0.5 1.0 0.5 1.5 0.5
53.7 11.0 8.0 23.3 0 0.5 1.0 0.5 1.5 0.5
47.7 21.9 8.4 18.0 0 0.5 1.0 0.5 1.5 0.5
41.7 32.9 8.8 12.6 0 0.5 1.0 0.5 1.5 0.5
29.8 54.8 9.6 1.8 0 0.5 1.0 0.5 1.5 0.5
29.8 54.8 9.6 1.8 0.56 0.5 1.0 0.5 1.5 0.5
Proximate analysis (% DM) Dry matter Protein ŽN=6.25. Lipids Ash Chromic oxide Gross energy ŽkJ gy1 .
87.2 49.0 15.6 8.8 0.43 21.7
86.9 49.0 15.2 9.0 0.44 22.2
87.5 48.7 15.6 9.3 0.42 22.1
86.9 48.6 15.4 9.4 0.40 22.3
87.1 49.1 16.3 9.8 0.41 22.7
87.6 48.2 15.4 9.8 0.45 22.7
a
Danish LT fish meal ŽP: 80.5%; L: 12.6%.. Gist Brocades ŽP: 43.8%; L: 10.5%.. c Vitamins Žmg kgy1 diet.: retinol, 15000 ŽIU kgy1 diet.; calciferol, 1667 ŽIU kgy1 diet.; alpha tocopherol, 83.3; menadion sodio bis., 16.6; thiamin, 12.5; riboflavin, 12.5; Ca pantothenate, 33.3; nicotinic acid, 116.7; pyridoxine, 8.3; folic acid, 4.2; cyanocobalamin, 0.04; biotin, 0.5; ascorbic acid Žstay C., 83.3; inositol, 250. d Minerals Žmg kgy1 diet.: cobalt sulphate, 1.91; copper sulphate, 19.6; iron sulphate, 200; sodium fluoride, 2.21; potassium iodide, 0.78; magnesium oxide, 830; manganese oxide, 26; sodium selenite, 0.66; zinc oxide, 37.5; dicalcium phosphate, 8.02 Žg kgy1 diet.; potassium chloride, 1.15 Žg kgy1 diet.; sodium chloride, 0.44 Žg kgy1 diet.. b
Apparent digestibility coefficients ŽADC. of the diets was determined as follows: ADC Ž % . s 1 y Ž Ž %IF = % NFs . r Ž % IFs = % NF . . = 100 where IF is the % of indicator in the feed, NF is the % of nutrient or energy in the feed, IFs is the % of indicator in the feces and NFs is the % of nutrient or energy in the feces. ADC of protein ŽADCp. of brewers yeast was estimated as follows: ADCps ADCp experimental diet y Ž ADCp control diet = Ž 1 y a . . ra where a s Ž% protein from brewers yeast in the dietr% protein in the diet.. Chemical analyses of the diets, whole fish and feces were carried out as follows: dry matter after drying in an oven at 105 8C until constant weight; ash by incineration in a muffle furnace at 450 8C for 16 h; protein ŽN = 6.25. by the Kjeldahl method after acid digestion, using Kjeltec digestion and distillation units; lipids by petroleum ether extraction in a Soxtec HT System apparatus; energy by direct combustion in an adiabatic bomb calorimeter ŽPARR model 1261.; chromic oxide of diets and feces by acid
Diet:
D0
D10
D20
D30
D50
D50M
Initial weight Žg. Final weight Žg. Feed intake Žg kgy1 dayy1 . Specific growth rate Ž%. Feed intake: weight gain Weight gain: protein intake Protein retention Ž% protein intake. Žg kgy1 weight gain. Energy retention Ž% energy intake. ŽMJ kgy1 weight gain.
12.0 40.7"1.0ab 37.9"4.8 1.46"0.03ab 1.48"0.01a 1.38"0.01a 20.8"0.6a 150.7"2.8a 26.0"1.9 8.3"0.4
11.9 42.8"0.4ab 41.5"0.2 1.52"0.01ab 1.35"0.01bc 1.52"0.02bc 25.6"0.6bc 168.9"2.5c 29.8"0.9 8.9"0.1
11.9 42.9"0.8ab 44.4"1.3 1.53"0.02ab 1.38"0.02b 1.44"0.0ab 24.0"0.2bc 167.2"0.7bc 27.1"1.6 8.6"0.3
11.9 45.6"0.9b 42.9"0.4 1.60"0.02b 1.28"0.02c 1.61"0.03c 26.5"0.6c 164.5"0.9bc 30.7"2.3 8.7"0.3
12.0 40.9"1.8ab 39.5"2.2 1.46"0.05ab 1.42"0.0ab 1.49"0.03ab 24.7"0.8bc 165.8"1.4bc 27.6"0.4 8.6"0.1
11.9 39.2"0.8a 38.9"1.0 1.42"0.02a 1.43"0.01ab 1.45"0.01ab 22.8"0.2ab 157.6"2.4ab 25.8"1.2 8.4"0.3
Values are means"s.d. For each row, values followed by different letters are significantly different Ž P - 0.05..
A. OliÕa-Teles, P. Gonc¸alÕes r Aquaculture 202 (2001) 269–278
Table 2 Growth and feed utilization of sea bass juveniles fed the experimental diets
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Table 3 Body composition of sea bass juveniles fed the experimental diets Žfresh weight basis. Diet:
Initial Final
Water content Ž%. Protein Ž%. Lipids Ž%. Ash Ž%. Energy ŽkJ gy1 . Hepatosomatic index Ž%. Visceral index Ž%.
73.7 14.8 6.5 5.0 5.8
D0
D10
D20
D30
D50
D50M
69.9"1.4 15.0"0.2a 12.1"0.8 3.8"0.3 7.6"0.4 2.1"0.0 13.1"1.8
69.0"0.1 16.3"0.2c 11.8"0.6 3.6"0.1 8.0"0.1 2.3"0.1 12.5"1.2
69.5"0.6 16.2"0.1bc 10.9"0.4 3.9"0.0 7.8"0.3 2.1"0.2 15.8"5.1
69.3"0.2 16.0"0.1bc 11.6"0.6 3.8"0.1 8.0"0.3 2.2"0.4 13.4"1.9
69.2"0.1 16.0"0.1bc 11.2"0.3 4.1"0.2 7.8"0.0 2.2"0.2 14.2"3.2
70.0"0.9 15.4"0.2ab 11.1"0.1 3.9"0.2 7.6"0.3 2.5"0.2 10.8"1.0
Values are means"s.d. For each row, values followed by different letters are significantly different Ž P - 0.05..
digestion according to Furukawa and Tsukahara Ž1966.. Fish and feces were homogenized and dried before analyses. Statistical analysis consisted of one-way ANOVA, using the probability level of 0.05 for rejection of the null hypothesis. After ANOVA, significant differences among means were determined by Tukey’s multiple range test. All statistical analyses were performed using a Statgraphics Plus version 4 for Windows software package.
3. Results Inclusion of brewers yeast to the diets did not affect growth rate nor feed intake but feed conversion significantly improved until a fishmeal protein replacement level of 30% ŽTable 2.. Protein efficiency ratio Žweight gain: protein intake. was significantly higher in fish fed diets D10 and D30 than in those fed the control diet ŽTable 2.. Protein retention, both per unit of weight gain and as percentage of protein intake was significantly higher in fish fed the brewers yeast-containing diets than the control diet ŽTable 2.. There were no significant differences in energy retention among experimental groups. The inclusion of a methionine supplement to diet D50M did not improve results. Indeed, fish fed the supplemented diet performed slightly worse than those fed diet D50 that had the same composition, except for the amino acid supplement ŽTable 2..
Table 4 Apparent digestibility coefficients of the experimental diets Diet:
D0
D10
D20
D30
D50
D50M
Dry matter Ž%. Protein Ž%. Energy Ž%.
86.8"0.3a 92.8"0.2a 95.3"0.2a
84.3"0.3ab 92.5"0.3a 93.2"0.2ab
82.2"0.1bc 92.0"0.3ab 90.8"0.3bc
79.1"0.8c 91.2"0.6ab 88.9"0.5c
71.0"0.6d 86.7"0.5c 82.3"1.1d
72.3"0.6d 90.3"0.6b 82.5"1.1d
Values are means"s.d. For each row values followed by different letters are significantly different Ž P - 0.05..
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At the end of the trial there were no significant differences in whole body composition among experimental groups, except for the protein content which was significantly higher in fish fed the brewers yeast containing diets than the control diet ŽTable 3.. Apparent digestibility coefficients ŽADC. of dry matter and energy significantly decreased with the increase of brewers yeast to the diets ŽTable 4.. ADC of protein of diets D50 and D50M were significantly lower than in the other diets. ADC of brewers yeast protein was lower Ž88.3%. than that of fishmeal protein Ž92.8%..
4. Discussion Feed conversion of sea bass improved with the inclusion of up to 30% dietary protein from brewers yeast. There were no significant differences in growth performance with the replacement of 50% of fishmeal protein by brewer’s yeast, the maximum level tested in this study Žrepresenting an incorporation of 55% brewers yeast in the diet, on a dry weight basis.. Also in sea bass, Metailler and Huelvan Ž1993. tested the inclusion of 10%, 20% and 30% of lactic yeast, bakers yeast and brewers yeast in isoproteic fishmeal-based diets. The authors found no differences in growth and feed utilization among groups, except for fish fed diets including brewers yeast. In this case, and contrary to our results, fish fed diets with more than 10% brewers yeast performed worse than those fed the control diet. As in our study, Alliot et al. Ž1979. found no negative effect on growth performance of sea bass fed diets with 50% dietary fishmeal protein replaced by an alkane yeast protein. The inclusion of 5% to 15% yeast in the diets was even beneficial, improving feed efficiency. In other species, a beneficial effect on fish performance was also noticed at moderate dietary inclusion levels of yeast ŽOhmae et al., 1979; Rumsey et al., 1991a.. Although fish seem to be prepared to cope with the high nucleic acids content of SCP, due to their very active liver uricase ŽDe la Huiguera et al., 1981; Rumsey et al., 1991a., some authors consider that high levels of nucleic acids may have a deleterious effect ŽTacon and Cooke, 1980; Davies and Wareham, 1988.. Indeed, RNA and purine basis were implicated as potent depressors of feed intake in farm animals ŽRumsey et al., 1992.. In fish, Tacon and Cooke Ž1980. found that a nucleic acid extract of bacterial origin depressed feed intake of rainbow trout when incorporated in the diet at a level equivalent to a bacterial SCP intake of 50%. Rumsey et al. Ž1991a. observed a feed intake depression in rainbow trout due to reduced acceptability of diets including more than 25% of brewers yeast, and Atack and Matty Ž1979. observed a reduction of feed intake in rainbow trout fed a brewers yeast diet comparatively to an herring meal based diet. On the contrary, when rainbow trout was fed a diet including a yeast nucleic acid extract corresponding to a dietary level of 50% brewers yeast, no negative effect on feed intake was observed ŽRumsey et al., 1992.. Also in the present trial feed intake of sea bass was not affected among groups, suggesting that, within the levels tested, brewers yeast does not affect diet palatability or depresses feed intake.
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In this trial, N-utilization of fish fed the brewers yeast diets was significantly higher than in the control diet. On the contrary, in rainbow trout the replacement of casein by a mixed SCP biomass Žincluding predominantly yeasts. in semi-purified diets, although not affecting growth negatively affected N utilization ŽMurray and Marchant, 1986.. However, as in the present study, Rumsey et al. Ž1992. also observed an increase of N retention in rainbow trout fed with increasing levels of yeast extract. From this the authors conclude that some of the non-protein nitrogen was used as source of non-essential amino acids. Yeast protein is deficient in sulphur amino acids and several studies showed that supplementation of the diets with methionine improved fish growth ŽSpinelli et al., 1979; Mahnken et al., 1980; Murray and Marchant, 1986.. In this study, however, the supplementation of diet D50 with methionine did not improve sea bass performance. Kaushik and Luquet Ž1980. also did not find any positive influence of sulphur amino acid supplementation of a bacterial SCP on the growth performances of rainbow trout. On the contrary, supplementation with sulphur amino acids depressed rainbow trout growth to varying degrees. According to Rumsey et al. Ž1990. the lower performance of fish fed diets containing high levels of brewers yeast may be caused by intact yeast cells, as probably not all intracellular ingredients become available to the fish. Indeed, Rumsey et al. Ž1991b. found that digestibility of intact brewers yeast in rainbow trout is significantly lower than that of disrupted cells. In accordance to this finding, Rumsey et al. Ž1990. observed that brewers yeast could replace 50% of total nitrogen in the diet of lake trout when the yeast cell walls were disrupted but a growth depression occurred when intact yeasts were used. In this study, the ADC of the diets were high, although the ADC of dry matter and energy decreased with the inclusion level of brewers yeast to the diets, indicating a lower digestible energy value of brewers yeast than the feedstuffs it replaced in the diets. The estimated ADC of fishmeal protein is within the expected ADC values for high quality fishmeal in sea bass ŽGomes da Silva and Oliva-Teles, 1998.. The ADC of brewers yeast protein was also high Ž88.3%. but lower than that of fishmeal Ž92.8%.. This value is considerably higher than that estimated by Metailler and Huelvan Ž1993. for brewers yeast in sea bass, but is similar to that obtained for an alkane grown yeast by Alliot et al. Ž1979.. In rainbow trout, both true and apparent digestibility coefficients of brewers yeast protein were estimated to be lower than in sea bass ŽAtack and Matty, 1979; Rumsey et al., 1991b.. In conclusion, results of this trial indicate that brewers yeast can replace 50% of fishmeal protein, with no negative effects in sea bass juvenile performance. Moreover, the inclusion of up to 30% brewers yeast in the diet improved feed efficiency and protein utilization. Acknowledgements This work was partially sponsored by PRAXIS XXI and FEDER Žproject PRAXIS 3r3.2rAQr2009r95.. We would like to thank DSM Portugal Žformerly Gist-Brocades. for kindly providing the brewers yeast used in this trial.
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