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* Animal Nutrition Group, Wageningen UR, P.O. Box 338, 6700 AH Wageningen, The Netherlands
Animal Sciences Group of Wageningen UR, P.O. Box 65, 8200 AB Lelystad, The Netherlands
Department of Food Technology and Nutritional Sciences, Wageningen UR, 6703 HD Wageningen, The Netherlands
2 Corresponding author: Bernardo.Suarez{at}wur.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Key Words: veal calf • concentrate feed composition • rumen fermentation • enzyme activity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Rumen development is triggered by the production of VFA resulting from fermentation of OM in the rumen (Flatt et al., 1958). Butyrate, and to a lesser extent propionate, stimulate the development of the rumen mucosa, mostly because of their use as energy sources by the rumen epithelium (Sander et al., 1959; Tamate et al., 1962). Since the early 1970s, extensive research has evaluated different protein and carbohydrate sources in calf starters. To date, only a few experiments have evaluated the effect of concentrate supplementation on performance and rumen development in veal calves. Concentrate feeds, as opposed to roughages, are provided to young calves to obtain high DMI and subsequent rapid VFA production, promoting fast papillae growth and rumen development. However, when compared with rearing calves, the DMI of concentrates in veal calves is hampered by high intakes of milk replacer. In addition, milk replacer intake may influence the fermentation process in the rumen. Consequently, the present study was conducted to evaluate the effects of intake of concentrates differing in their carbohydrate composition in addition to a milk replacer on the performance and rumen fermentation characteristics of veal calves. The effects of these diets on morphological rumen development are presented in a companion paper (Suárez et al., 2006).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Calves and Diet Transport and Slaughter Procedure
One hundred and sixty male Holstein Friesian x Dutch Friesian calves, averaging 44.9 kg of BW (SE = 2.8 kg) were purchased in 2 batches of 80 animals. On arrival, calves were weighed and, based on their BW, assigned to 1 of 8 blocks. Within blocks and batches, calves were randomly assigned to 1 of 5 dietary treatments and 1 of 2 slaughter ages. The dietary treatments included a milk-fed control and 4 treatments in which a concentrate, varying in carbohydrate composition, was fed in addition to the milk replacer: 1) milk replacer (control); 2) pectin-based concentrate; 3) NDF-based concentrate; 4) starch-based concentrate; or 5) mixed concentrate (equal amounts of the concentrates in treatments 2, 3, and 4). The detailed ingredient and nutrient compositions of the concentrates are presented in Table 1
. Animals were individually housed in open metal boxes (0.9 m2) with a wooden slatted floor, without bedding material. Boxes were located in 2 stables, where the environmental temperature was maintained at least at 15°C. In treatments 2 to 5, concentrates were provided as pellets, up to a maximum of 750 g/d of DM. Milk replacer and concentrates were supplied in separate buckets and meals were supplied in equal amounts twice daily (0730 and 1830 h). For the pelleting process, special care was taken to minimize particle size reduction of the ingredients. Therefore, corn was only broken and barley was rolled prior to inclusion; soybean hulls (beans dehulled after toasting) and corn grits were not further ground before pelleting. Sugar beet pulp (without molasses) was ground through a 2.75-mm screen on a hammer mill prior to pelleting. The average pellet size was 15 mm long and 6 mm in diameter.
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, and its nutrient and ingredient composition is presented in Table 3. For the control treatment, milk replacer was reconstituted in a ratio of 
130 g/L of water and provided in 2 equal meals at 39°C. For treatments with additional solid feed (treatments 2 to 5), the amount of milk replacer was reduced to stimulate the intake of solid feed (see Table 2) and reconstituted in the same volume of water as the control group. Calves were weighed every 4 wk, and once a week samples of milk replacer and concentrates were collected and pooled by month for further analysis.
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Analytical Procedures
Dry matter was determined by drying at 103°C to a constant weight (ISO 6496; ISO, 1983) and ash by combustion at 550°C (ISO 5984; ISO, 1978). Crude fat was determined by extraction with petroleum ether (boiling range 40 to 60°C). After extraction, samples were dried in a vacuum oven at 80°C to a constant weight, according to ISO 6492 (ISO, 1985). Nitrogen was determined with the Kjeldahl method with CuSO4 as the catalyst (ISO 5983; ISO, 1998). Total starch was analyzed by an enzymatic method according to Brunt (1993). Reducing sugars (RS) were extracted from the samples using 40% ethanol and subsequent hydrolysis in a weak acid environment. Protein was precipitated using a Carrez I and II solution. After the hydrolysis, copper(II) was reduced by oxidation of the monosaccharides to copper(I). Copper(I) forms a yellow complex with neocuproïne (2,9-dimethyl-1,10-fenantroline hydrochloride). This complex can be measured in a spectrophotometer at 460 nm.
The NDF analysis was based on the method of Van Soest et al. (1991) but included, after the neutral detergent treatment incubation, an enzyme cocktail containing termamyl (Novo Nordisk, Copenhagen, Denmark), amylase (Sigma 6814; Sigma-Aldrich, St. Louis, MO), and protease (Novo Nordisk) in phosphate buffer (pH 7.0) to remove starch and proteins from the residue. The ADF analysis involved 2 steps. First, the sample was treated according to the NDF method described. In the second step, the neutral detergent residue was treated with the acid detergents as described by Van Soest and McQueen (1973). The acid detergent lignin analysis was based on the treatment of the sample with acid detergent, followed by incubation with 72% sulfuric acid.
Volatile fatty acid concentrations and lactic acid were analyzed using HPLC with a Merck polyspher OA 51272 column as the stationary phase (Merck & Co., Inc., Whitehouse Station, NJ) and 0.0025 M sulfuric acid as the mobile phase (elution fluid). Detection was performed by using a refractive index detector. Calibration and quantification was done by using an external standard solution. Ammonia concentrations were estimated according to the method of Berthelot, modified by Schneider (1976).
Isolation of rumen enzymes and subsequent measurement of their activities were performed as follows. Whole rumen contents of 8 of the 16 calves per treatment, slaughtered at 12 wk of age, were used. The intra-and extracellular microbial enzymes and those enzymes attached to rumen particles were extracted from whole rumen contents. A combination of methods was applied to maximize the extraction of enzymes from the homogenized whole rumen contents, obtained at slaughter (i.e., freezing and thawing, sonication, and osmotic shock). After thawing, samples were kept on ice and sonified (Branson Sonifier 250; Branson Ultrasonics Corporation, Danbury, CT), using a flat tip (1/2-in. diameter), for 2 min (at 40% of the duty cycle) in a 50 mM sodium acetate (NaAc) buffer (pH 5) including 2 M NaCl and 0.01% NaN3. Subsequently, feed particles and lysed bacteria were removed (centrifugation at 20,000 x g, 22.5 min, 4°C) and the enzyme cocktail obtained was dialyzed (dialysis tubing: size 5 i.d.; 24/ 32-in.; 19.0 mm; 30 M; approximately 12,000 to 14,000 Da; Medicell International, Liverpool, UK) against a 50 mM NaAc buffer (pH 5.0, 18 h, 4°C) to remove dissolved sugars and NaCl. Changes in volume during dialysis were recorded. Enzyme activity was determined by the release of RS after 60 min of incubation of 0.5 mL of the enzyme cocktail with 0.5 mL of 120 mM NaAc buffer (pH 5.0) and 0.5 mL of each of 4 substrate suspensions in an Eppendorf mixer at 39°C. The reaction was stopped at 100°C after 5 min. The substrate suspensions (sugar beet pulp, sugar beet pectin, soybean hulls, and native cornstarch, 2% wt/vol) provided excess substrate for the incubations and were prepared in demineralized water containing 0.01% NaN3, and kept over-night at 39°C in a water bath before use. Incubates, substrate blanks, and enzyme extract blanks were analyzed for reducing sugar end-groups according to Somogyi (1952). Enzyme activity was expressed as millimoles of RS released per minute per gram of DM in the rumen.
Statistical Analysis
Data for DMI, average daily gain (ADG), and blood and rumen parameters were analyzed as a complete randomized block design, in a 5 x 2 factorial arrangement, with diets and length of the experimental period (i.e., 8 or 12 wk of age at slaughter) as main factors. Continuous data were subjected to ANOVA, according to Model 1:
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where y is the dependent variable; µ is the average experimental value; batchi is the effect of batch i; i is 1 of 2 (2 batches of 80 calves); dietj is the effect of dietary treatment j; j is the control, pectin, NDF, starch, or mixed diet; periodk is the effect of period (age at slaughter) k; k is 8 or 12 wk; (diet x period)jk is the effect of the interaction between diet and period; 
ijkl is an error term; and l is 1, . . ., 160.
The main effects and the interaction between diet and time of the experiment (age at slaughter) were evaluated using the F-test, followed by posthoc pairwise comparisons (Fisher LSD method) when the F-value showed significance (P < 0.05). Rumen parameters were also subjected to an analysis of covariance. The average DMI during the last week prior to slaughter, expressed for each calf as the deviation from the overall mean, was included as a covariable in Model 1. For calves in the control treatment, the covariable was equal to 0. The statistical analyses were carried out using Genstat (Genstat Committee, 2000). The rumen enzyme activities were analyzed as a split-plot design using the GLM procedure of SAS (SAS Institute, 2002) according to Model 2:
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where y is the dependent variable; µ is the average experimental value; dieti is the effect of dietary treatment i, i is the control, pectin, NDF, starch, or mixed diet; calfj is the effect of calf j, j is 1, 2, 3, . . ., 40; substratek is the effect of substrate k; k is soybean hulls, native cornstarch, sugar beet pectin, and sugar beet pulp; and ijkl is an error term.
Diet was considered as the main plot factor and substrate as the subplot. The term diet x calf was used as an error term to test the effect of the diet. Other effects were tested against the residual error term. The Tukey test was used to test for all pairwise comparisons among means when the F-value was significant (P < 0.05).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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shows the effects of experimental treatments on concentrate DMI and on ADG. The averaged DMI of the concentrate diets varied between 0.37 and 0.52 kg/d of DM. Calves receiving the starch diet showed the lowest DMI (0.37 kg/d of DM) throughout the trial. The DMI of the NDF diet was higher than that of the pectin diet (P < 0.05). A diet effect (P < 0.001) and diet x period interaction (P < 0.01) were observed in the last week of the experiment. First, for calves in the last week of the 8-wk period, the DMI of the starch diet was the lowest (0.40 kg/d of DM) among the concentrate treatments. Calves fed the pectin diet had a lower DMI (0.59 kg/d of DM) than those fed the mixed diet (0.71 kg/d of DM). Second, in the last week of the 12-wk period, the diet x period interaction was due to a common decrease on DMI for the concentrate diets but an increase for the starch diet.
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), a direct comparison of the feed conversion of those treatments with the milk fed-only calves cannot be done. An analysis of the growth performance is presented in the Discussion section.
Rumen Fermentation Characteristics
Table 5 shows the results of the analysis performed on the samples of rumen contents. The pH of the rumen liquid varied between 4.9 and 5.6 and was affected by diet and period (P < 0.001). An interaction between diet and period also was observed (P < 0.05). This interaction was caused by the rise in pH of the control treatment from 5.2 to 5.6 from wk 8 to 12, respectively, while remaining constant in the calves fed concentrates. An exception was the starch diet, which was 4.9 at the end of the 8-wk period and increased to 5.2 at the end of wk 12.
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The concentration of ammonia in the rumen liquid varied between 14 and 21 mmol/L, and no significant differences between the treatments were observed (P > 0.05). The concentration of ammonia in the rumen fluid was significantly (P < 0.001) higher at the end of the 12-wk period (23 mmol/L) than at the end of the 8-wk period (13 mmol/L).
The analysis of covariance revealed that the variation in DMI did not significantly explain the variation in total VFA or its molar proportions. For pH of the rumen fluid and for concentrations of lactate and NH3, the inclusion of DMI as a covariable appeared significant (estimates of regression coefficients ± SE for DMI: 0.4 ± 0.1, –13.3 ± 5.9, and –15.2 ± 6.3, respectively; P < 0.05). Following the analysis of covariance, differences in the rumen lactate concentrations between the control, the pectin, and the mixed diets remained as presented. However, the difference between the pectin and mixed diets was decreased (predicted means 10 vs. 6 mmol/L, P = 0.20) after the analysis of covariance. The effects on ammonia concentrations did not change. Likewise, for rumen pH, inclusion of the covariable increased the P-value for the interaction between diet and period (from P = 0.03 to P = 0.06).
Enzyme Activity in Whole Rumen Contents
Table 6 shows the effects of experimental treatments on the polysaccharide-degrading enzyme (PDE) activity extracted from the rumen contents. Diet and substrate effects and a diet x substrate interaction (P < 0.001) were observed. When averaged over substrates, PDE activities in the rumen content of calves fed concentrate diets varied between 3.9 and 6.0 mmol/min per g of DM. Calves fed the pectin diet showed higher PDE activity than those fed either the starch or the NDF diet (6.0 vs. 4.6 and 3.9 mmol/min per g of DM), respectively. In addition, the PDE activity of control-fed calves was small (<1 mmol/min per g of DM). When averaged over treatments, the PDE activity ranged from 3.4 to 4.8 mmol/min per g of DM, decreasing in the order of native cornstarch, sugar beet pectin, sugar beet pulp, and soybean hulls as substrates (4.8, 4.5, 3.7, and 3.4 mmol/min per g of DM, P < 0.05). Generally, the results in Table 6 illustrate an increased enzyme activity for substrates that were present in the diet [e.g., increased pectin- and sugar beet pulp-degrading (pectinase) activities on the pectin diet and increased starch-degrading (amylase) activity on the starch diet]. However, the NDF diet was an exception to this rule, because it showed higher pectin-degrading activity (pectinase) when compared with degradation of soybean hulls (SBHase; P < 0.05). In addition, the highest SBHase activity was observed in calves fed the pectin, not the NDF, diet. The mixed diet induced fairly high activities of all enzymes tested and exhibited the least variation among treatments.
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DISCUSSION |
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), and calves did not consume the whole concentrate portion fed (maximized at 0.75 kg/d of DM). The absence of increased DMI from concentrate with age was likely due to the increased supply of milk replacer at the end of the trial (Table 2). The increase of the starch diet with age was an exception (causing an interaction between treatment and period; Table 2). The low intake of the starch diet in the first period may have been related to the low ruminal pH observed, because acidosis generally depresses the DMI (Kellaway et al., 1977; Nocek, 1997; Owens et al., 1998).
Calves fed additional concentrates showed an ADG (700 to 780 g/d) close to the ADG of veal calves (Table 4). The higher intake of milk replacer in the control treatment, however, hampers a direct comparison of data performance (and efficiency) across treatments. To facilitate this comparison, growth rates on both levels of milk replacer intake were simulated using the veal calf growth model developed by Gerrits et al. (1997). Extra growth attributable to intake of concentrates could be calculated based on the simulated BW gain on the low intake of milk replacer (Table 7). The simulated daily gain values on the high-milk scheme were in line with the observed values (691 vs. 681 and 841 vs. 864 g/d at 8 and 12 wk, respectively). Extra daily gain per kilogram of concentrate ranged from 0.82 to 1.04 kg and from 0.56 to 0.62 kg at 8 and 12 wk of the trial period, respectively. At 8 wk, calves fed the starch diet showed the highest extra growth, whereas at 12 wk calves fed the starch and mixed diets showed the highest extra growth. Compared with the 8-wk period, at the 12-wk period the extra growth achieved by all the concentrate treatments may be related to the decline in growth rate and growth efficiency accompanying an increase in BW present in farm animals.
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Among the concentrates, calves fed the starch diet revealed a particularly low rumen pH (4.9) at 8 wk of age. At 12 wk of age, the rumen pH was slightly higher than at 8 wk, in particular for the starch diet. This rise in pH might indicate an increased absorption of VFA as a consequence of a more developed and mature rumen.
The VFA concentrations on the concentrate diets were close to the range normally observed in adult ruminants (120 to 160 mmol/L; Bergman, 1990). Similar results were obtained in rearing calves (Quigley et al., 1992a,b; Abdelgadir et al., 1996; Beharka et al., 1998; Lesmeister and Heinrichs, 2004). As expected, the rumen VFA concentrations observed in calves fed the concentrate diets were higher (100 to 121 mmol/L) than those observed in control-fed calves (36 mmol/L). The VFA concentration found in the rumen of control-fed calves suggests the presence of milk in the rumen.
In agreement with expectations (Van Soest, 1994), the NDF-based diet led to high molar proportions of acetate, the starch-based diet led to high molar proportions of propionate, and the pectin diet to high molar proportions of butyrate. At a low pH, microorganisms may shift fermentation pathways and increased proportions of propionate and lactate occur (see review by Dijkstra, 1994). Indeed, in the present experiment, pH values of the rumen fluid were low and molar proportions of propionate were high (>27%).
Hristov et al. (2001) and Ghorbani et al. (2002) reported that in feedlot cattle perceived to have subclinical acidosis, the lactate concentration in ruminal fluid rarely exceeded 10 mmol/L. Lactate concentrations observed in the present experiment (5 to 11 mmol/L) were higher than results reported in calves by Anderson et al. (1987a, b), Abdelgadir et al. (1996), and Beharka et al. (1998) but lower than those reported by Quigley et al. (1992c), ranging from 13 to 25 mmol/L [D(–) plus L(+) lactate]. Furthermore, the concentration of lactate present in the control-fed diet was the highest (>20 mmol/L). This information, together with the high values of ammonia in the rumen fluid (21 mmol/L), indicates fermentation of the milk replacer in the rumen. The occurrence of ruminal drinking has been well documented (Toullec and Guilloteau, 1989; Dos Santos et al., 1986) but has rarely been quantified in experiments in which concentrates are fed. Therefore, the extent to which ruminal drinking contributes to the fermentation processes observed in this experiment is unknown.
Branched-chain VFA are mainly end-products of protein fermentation and are considered a growth factor for fiber-degrading microorganisms in the rumen (Yang, 2002). Anderson et al. (1987a) showed that in rearing calves, the molar proportions of isobutyrate declined with age as feed intake increased, indicating an increased cellulolytic activity as calves aged. They also reported that the molar proportion of valerate increased until 12 wk of age, and then remained constant thereafter. In the present trial, for the concentrate-fed treatments, the molar proportions of isobutyrate (P < 0.001) and valerate (P < 0.05) decreased with age, but the ammonia concentration increased. Higher molar proportions of branched-chain VFA were expected in the milk diet, in line with the observed high ammonia concentrations.
Enzyme Activities and Soluble Sugars in Rumen Content
Assessing the PDE activity of the microorganisms present in the rumen is a useful approach to obtain quantitative estimates of substrate degradation in the rumen. Provided that representative samples of whole rumen contents are taken and that intra- and extracellular enzymes are completely extracted and their activity is well preserved, the relationship between substrate degradation in vitro and their degradation in vivo should be good. Silva et al. (1987) reported a high correlation (r = 0.98) for in sacco DM degradation and cellulolytic activity after 24 h of rumen incubation.
In contrast with other in vitro techniques regularly used to characterize substrate degradation in the rumen (e.g., Tilley and Terry, 1963; cumulative gas production technique) the enzyme assay does not have the disadvantage of isolating the microflora and its adaptation to the incubation medium and substrate. Nevertheless, interassay variation of the analysis of enzymes is large, and procedural standardization among research groups applying this technique is lacking. Furthermore, the selection of substrates, as well as their pretreatment (unpublished observations) is crucial when determining PDE activities. However, between-treatment variation remains estimable using this technique.
The results from the present experiment illustrate adaptation of the rumen microflora to the diet. The effects of diet on PDE activities (high amylase and low SBHase) are in line with those reported for high grain/ low roughage-based diets in dairy cattle (Huhtanen and Khalili, 1992; Martin and Michalet-Doreau, 1995; Hristov et al., 1999). However, the increased hydrolysis of soybean hulls of the calves on the pectin treatments, compared with the NDF treatment, is difficult to explain.
Most techniques studying substrate degradation (e.g., enzyme assay) or substrate disappearance (e.g., the in sacco technique) assume that the end-products of hydrolysis are rapidly utilized by the microbes (Dhanoa et al., 1999), resulting in concentrations of free RS in the rumen fluid close to or below the detection level. An exception to these low levels is the high levels observed in rumen fluid immediately after a meal rich in easily degradable carbohydrates, because the supply of sugars may temporarily exceed the microbial capacity to utilize these sugars (Dijkstra et al., 2002). However, the high concentrations of RS in rumen contents found in the present experiment suggest that the assumption of rapid utilization may not always be true.
In the present research, no big differences were observed in RS concentrations among treatments. Moreover, the concentration of RS varied between 45 and 61 g/kg of DM, whereas in dairy cows reported concentrations ranged from 0.02 to 2.57 mmol/L of rumen fluid (approximately 0.04 and 5.55 g/kg of DM, assuming an average of 120 g/kg of DM in the rumen contents; Hristov et al., 2000; Hristov et al., 2001; Hristov and Ropp, 2003). The relatively high concentration of RS is likely related to relatively low bacterial growth rates while high rates of substrate hydrolysis are maintained. A reduced growth rate of bacteria may be related to the low rumen pH observed in this experiment. A low pH is known to increase the energy expenditure of rumen bacteria to maintain their intracellular pH (Russell and Wilson, 1996) and decrease the uptake of soluble carbohydrates by ruminal microorganisms (see, e.g., Moore and Martin, 1991; Chow and Russell, 1992; Martin, 1996; Martin and Wani, 2000). Maintaining a high rate of substrate hydrolysis could be related to the (extracellular) enzymes maintaining their activity while present in the rumen. This effect may be enlarged by low rumen motility, often observed in ruminants with low ruminal pH (Dirksen, 1989, as cited in Nocek, 1997). Interestingly, it has been demonstrated that the PDE are still active far below the optimal pH at which the rumen bacteria produce them. For example, at pH 5.0, ruminal-extracted cellulases still retained 65% of their maximum activity (pH = 6; Morgavi et al., 2000), whereas the activity of cellulolytic bacteria decreases rapidly at a pH below pH 5.6 (Russell and Wilson, 1996).
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CONCLUSIONS |
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FOOTNOTES |
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Received for publication December 23, 2005. Accepted for publication June 20, 2006.
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