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The Digestibility of Cell-Wall Polysaccharides from Wheat (Bran or Whole Grain), Soybean Meal, and White Lupin Meal in Cockerels, Muscovy Ducks, and Rats
The Digestibility of Cell-Wall Polysaccharides from Wheat (Bran or Whole Grain), Soybean Meal, and White Lupin Meal in Cockerels, Muscovy Ducks, and Rats B. CARRE, L. DEROUET, and B. LECLERCQ Institut National de la Recherche Agronomique, Station de Recherches Avicoles, Nouzilly, 37380 Monnaie, France (Received for publication February 14, 1989) ABSTRACT The digestibility of nonstarch polysaccharides (NSP) were measured in cockerels, Muscovy ducks, and rats by using four diets where the only sources of NSP were wheat bran (Diet B), whole wheat grain (Diet W), soybean meal (Diet S), or white lupin meal (Diet L). The four diets contained similar amounts of crude protein (24.4%), lipids (5.2%), and NSP (6.9%). The proportions of water-soluble NSP in total NSP were 11.1% (Diet B), 19.7% (Diet W), 8% (Diet S), and 11.5% (Diet L). The NSP contents of feed and excreta were determined by measuring their individual sugars, using gasliquid chromatography of alditol acetate derivatives. The digestibility values of NSP ranged from 21.9% (Diet W) to 13% (Diet L) for cockerels, from 18.7% (Diet W) to 7.9% (Diet L) for ducks, and from 85.7% (Diet L) to 44.1% (Diet B) for rats. These results suggest that cockerels and ducks were only able to digest the watersoluble fraction of the nonstarch polysaccharides. The pectic polymers, which were major components in water-insoluble NSP of Diets S and L, were digested to a high extent by the rats. The digestible-energy (DE) values, calculated for the birds from the apparent metabolizable-energy values corrected for nitrogen retention (AME,,), were very similar when cockerels and ducks were compared; the differences between bird species did not exceed .23 MJ l per kg of dry matter. In all cases, the DE values were higher for rats than for birds. These results suggested that the main factor responsible for the differences in DE values between rats and birds was the ability to digest NSP, which was higher for the rats than for the birds. (Key words: cockerels, Muscovy ducks, rats, nonstarch polysaccharides, digestibility) 1990 Poultry Science 69:623-633 INTRODUCTION
The cell walls of plants represent the leastdigested components of diets in chickens. This explains why cell-wall related parameters are efficient predictors of the energy value in the diets for chickens (Sibbald et al., 1980; Carre et al., 1984; Janssen and Carre, 1985). Previous research (Carre" et al., 1984; Carre" and Leclercq, 1985) suggested that the waterinsoluble, cell-wall procedure probably is the most-convenient method of fiber determination in order to predict the energy value of diets for chickens. This suggestion was based mainly on the studies investigating cell walls from white lupin cotyledons, showing no digestion of this cell-wall material in cockerels (Carre and Leclercq, 1985; Carr6 et al., 1985). In the present study, this aspect was re-examined by measuring the digestibility of cell-wall components from other sources. For the current experiment, digestibility was measured in cockerels and also in Muscovy
' l MJ = 239 kcal.
ducks. Previous data on the ability of palmipeds to digest cell-wall fractions were somewhat confusing. In a review, Cowan (1980) concluded that cell-wall fractions are poorly digested by geese. Nehring and Knabe (1961) and Schubert et al. (1982) reported digestibility values for crude fiber ranging from 0 to 36% in ducks. Siregar and Farrell (1980) and Mohamed et al. (1984) did not find great differences between the energy values in the diets for chickens and ducks, suggesting that the digestibility values for cell-wall fractions probably are similar for chickens and ducks. By contrast, Muztar et al. (1977), who used fresh plants, observed great differences in the energy values between ducks and chickens. Previously, cell-wall digestibility for ducks was estimated by using a measurement of crude fiber. Further studies are needed, however, in order to obtain information about the digestibility of the whole cell-wall fraction in ducks, since crude fiber represents only a small part of the whole cell-wall (Asp and Johansson, 1984).
623
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CARRE ET AL.
Because the colon of birds is much shorter than that of mammals, differences would be expected between birds and mammals with regard to cell-wall digestion (Fonnesbeck et al., 1974). Yet, studies dealing with a direct comparison between birds and mammals are very scarce in the literature. In the present study, cockerels, Muscovy ducks, and rats received diets in which the only source of cell walls was wheat bran, whole-wheat grain, soybean meal, or white lupin meal. The digestibility values for nonstarch polysaccharides (the main components of cell walls) and the energy values of diets were measured in the three animal species. MATERIALS AND METHODS
Diets Four diets containing similar amounts of protein (27.4% of the dry matter), lipids (5.9% of the dry matter), and total nonstarch polysaccharides (NSP, 7.8% of the dry matter) were tested (Tables 1 to 3). In each diet, cell walls were provided by a single source: wheat bran (Diet B), whole-wheat grain (Diet W), defatted and dehulled soybean meal (Diet S), or defatted and dehulled white-lupin meal (Diet L).
The feed mixtures were as follows (percentage of water in the mixture): Diet B, 59.3; Diet W, 58.3; Diet S, 54.5; Diet L, 54.5. About 40 g of dry matter were given with one force-feeding. The balance experiment was conducted using the following periods successively: 24 h of adaptation, including two force-feedings; 24 h of starvation, plus a 54-h balance period, including 30 h of feeding (four force-feedings); and 24 h of final starvation. The cockerels had free access to water throughout the experiment; but the ducks had access to water only twice daily for 30 min, 2 h after force-feeding. This procedure was used with the ducks in order to avoid any regurgitation of the feed during drinking and to reduce the amount of spilled water. The ducks had free access to water during fasting. Excreta were collected twice daily during the balance period, stored immediately at -20 C, freeze-dried, equilibrated at the ambient temperature, weighed, and finely ground. Rats
A balance experiment was conducted on male Wistar rats3 using the experimental diets given to the cockerels and ducks. The rats were 46 days of age and weighed 184 g (SD equals 10 g) at the start of the experiment. Each of the four diets was given as mash to seven replicates. A replicate was represented by one animal placed Cockerels and Ducks in an individual metal cage. The cages were provided with drinking water and with special A balance experiment was conducted using feeders designed to avoid spillage. A plastic tray cockerels and Muscovy ducks. The cockerels, covered with blotting-paper designed to absorb from a commercial broiler strain (Hubbard), urine was put under each cage for feces were 73 days of age and weighed 2,602 g (SD collection. Feed for ad libitum intake was equals 264 g) at the beginning of the balance available to the rats for 3 days (Day 1 to Day 3). experiment. The Muscovy ducks, from a com- Then, the rats were restricted to 20 g of feed per mercial strain,2 had a similar weight (2,770 g; day for 7 days (Day 4 to Day 10). The actual feed SD = 279 g) and were slightly younger (60 intake was measured from Day 5 to Day 9. Feces days). Each of the four diets was given to seven were collected twice daily, from Day 6 to Day replicates from each of the two species of bird. A 10. The feces were stored immediately at -20 C replicate constituted 1 bird placed in an individ- after collection; then freeze-dried, equilibrated ual, metal cage. The cages were provided with at the ambient temperature, weighed, and finely drinking water and plastic trays for excreta ground. collection. The sides of the duck cages were covered with plastic plates in order to recover the excreta ejected horizontally by these birds. Analyses The birds were force-fed the experimental The apparent metabolizable-energy values diets as a meal-water mixture by using a syringe. corrected for nitrogen equilibrium (AME„) were calculated for the birds, as described by Hill and Anderson (1958). For calculating the AMEn, the birds are supposed to excrete an amount of ^anedin, Grimaud, 49450 Roussay, France. 3 urinary nitrogen equal to that of the digested 1FFA CREDO, BP 109, 69210 TArbrefle, France.
625
DIGESTIBILITY OF POLYSACCHARIDES TABLE 1. Ingredients used in the diets Diet Ingredients
Bran
Wheat bran Whole-wheat grain Defatted soybean meal, dehulled Defatted white-lupin meal, dehulled Soybean-protein isolate Corn starch Com oil DL-methionine Calcium carbonate Dicalcium phosphate Sodium chloride Choline chloride, 50% Vitamin mixture1 Mineral mixture2 Dry-matter content
19.7
Soybean meal
Wheat
Lupin meal
75.0 50.0 24.4 48.8 4.4 .15 1.0 1.0 .33 .1 .02 .1 87.6
24.9 15.4 51.9 5.1 .2 1.0 1.0 .28 .1 .02 .1 90.0
18.8 43.2 4.1 .15 1.0 1.0 .33 .1 .02 .1 89.6
3.7
1.6
1.0 .28 .1 .02 .1 88.3
Supplied (milligrams per kilogram of diet): retinol, 3; cholecalciferol, .037; a-tocopheryl acetate, 15; menadione sodium bisulfite, 5; riboflavin, 4; calcium pantothenate, 8; nicotinic acid, 25; pyridoxine hydrochloride, 1; folic acid, .2; biotin, .1; cyanocobalamin, .008; butylated hydroxytoluene, 124. Supplied (milligrams per kilogram of diet): Mn0 2 , 168; ZnO, 105; FeS0 4 -7H 2 0, 218; CuS0 4 -5H 2 0, 35; C0CO3, .7; Na 2 Se0 3 , .5; KI, 1.6.
TABLE 2. Composition, energy value, and feed intake for the diets, dry-matter basis Diet Measurement N times 6.25, % Lipids, %1 Water-insoluble cell wall, % Water-insoluble, nonstarch polysaccharides, % Water-soluble, nonstarch polysaccharides, % Gross energy, MJ per kg AME„, MJ per kg: cockerels (predicted) cockerels (measured) ducks (measured)4 DE, MJ per kg: cockerels (calculated)4,5 ducks (calculated)4'5 rats (measured)4 Feed intake:6 cockerels, g per 2 days4 ducks, g per 2 days rats, g per 5 days4
Bran
Soybean meal
Wheat 27.29 5.8 8.06 6.03 1.47 19.44
27.85 5.9 9.83 7.30 .91 19.52
Lupin meal
26.72 5.6 9.11 7.59 .66 19.00
27.82 6.5 7.42 6.35 .81 19.70
14.90 14.98 14.78
± .04 ± .03
15.15 14.90 ± 15.13 ±
.13 .08
14.64 14.33 ± .05 14.56 ± .03
15.49 15.84 ± 15.75 ±
.05 .05
16.32 16.12 17.27
± .04 ± .03 ± .03
16.21 ± 16.44 ± 17.28 ±
.13 .08 .03
15.61 ± .05 15.84 ± .03 17.05 ± .03
17.18 ± 17.09 ± 18.47 ±
.05 .05 .03
142.9 143.9 86.5
± .4 ± .9 ± .1
148.6 149.1 87.3
± .8 ± 1.8 ± .2
173.0 172.7 89.0
± .4 ± .4 ± .1
166.5 166.7 88.8
± .5 ± 1.7 ± .4
'Calculated value. Corrected for residual starch. ^Prediction of AME,, based on gross energy, crude protein, and the water-insoluble, cell-wall contents (Cane et at., 1984); 1 MJ = 239 kcal. Means ± SE obtained with seven animals. ^ e calculation of digestible energy (DE) was as follows: measured AME„ + .0300 x N (grams per kilogram of feed). The last factor, which corresponds to the correction for urinary nitrogen, was taken from Sibbald et al. (1963). •Teed intakes during the balance experiments.
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CARR£ ET AL.
nitrogen (Sibbald et al., 1963). Assuming an apparent digestibility value of 82.5% for protein, Sibbald et al. (1963) proposed an energy value for urinary nitrogen equivalent to .0300 MJ per g of ingested nitrogen. This calculation of urinary energy losses was applied in the present experiment, thus assuming the same apparent protein digestibility value of 82.5% for each experimental diet and each species. Then, the digestible energy (DE) values were calculated for the birds from the AMEn values, by correcting the amount of excreted energy for the amount of urinary energy losses. Starch was measured by the dimethylsulfoxide procedure (Boehringer Mannheim, 1980) as described previously (Carre" et al., 1987). The water-insoluble cell walls (WICW) were isolated from the feed (3-g samples), as described by Carre" et al. (1984). The water-soluble fractions of the feed were pooled, extensively dialyzed against water at 4 C, freeze-dried, refluxed in 60 mL of ethanol-water (80:20, vol/ vol) for 30 min, cooled at the ambient temperature, allowed to stand for 2 h, and centrifuged. The resulting precipitate represented the watersoluble, ethanol-insoluble fraction (WSEIF). The NSP of the feed was measured from the sugar determinations in the WICW and WSEIF. The neutral sugars of the diet WICW and WSEIF were measured by a gas-liquid-chromatography (GLC) analysis of their alditol-acetate derivatives (Blakeney et al., 1983), following sulfuric-acid hydrolysis (Brillouet and Carre, 1983). Only the diluted sulfuric-acid step was applied for the hydrolysis of the WSEIF. All of the data on glucose were corrected for residual starch. The uronic acids in the diet WICW and WSEIF were measured colorimetrically, using the w-phenylphenol method (Blumenkrantz and Asboe-Hansen, 1973), as described by Brillouet and Carre (1983). The total diet NSP was calculated by adding water-soluble NSP (from WSEIF) to water-insoluble NSP (from the WICW). The neutral sugars of the total NSP were measured in rat feces and bird excreta (30-mg samples) by GLC analysis performed on the acid hydrolysate of the 80% ethanol-insoluble fraction obtained after a-amylase (40 \ig, from Bacillus subtilis) treatment4 (95 C for 10 min, then 55 C for 150 min with enzyme) and a
4 Boehringer Mannheim, 6800 Mannheim 31, West Germany.
Pronase (50 u.g) treatment4 (20 C for 4 h in a 30-mM phosphate buffer, pH 7.5), a chloroformmethanol (2:1, vol/vol) extraction, refluxing in ethanol-water (80:20, vol/vol) for 30 min, and centrifuging. The glucose data were corrected for residual starch, measured on a duplicate sample of feces and excreta previously treated with the same procedure as that used before the acid hydrolysis and GLC analysis. The uronic acids from the total NSP were measured in the feces and excreta, as described previously for diets, directly and without the preparation of a treated residue. Statistical Analysis The NSP recovery values from the birds were analyzed by a two-way analysis of variance according to Snedecor and Cochran (1980). A one-way analysis of variance was used for the rat data. Duncan's multiple range test (Duncan, 1955) was used to compare the individual means of the NSP recovery values. RESULTS
Composition of Dietary Nonstarch Polysaccharides The total NSP contents (the sum of the watersoluble and water-insoluble NSP) varied little between the diets, ranging from 7.16% (Diet L) to 8.26% of the dry matter (Diet S, Table 3). The ratios for the water-soluble NSP to total NSP varied from .080 (Diet S) to .197 (Diet W). The WICW contained the following amounts of nonstarch polysaccharides (as a percentage of WICW): 74.26 (Diet B), 74.81 (Diet W), 83.32 (Diet S), and 85.58 (Diet L). The total NSP composition of Diets B and W were very similar; both appeared to be clearly different from those of Diets S and L (Table 3). The xylose content of the NSP was much higher in Diets B and W than in Diets S and L. Galactose was a minor component in Diets B and W (about 4% of the total NSP). The galactose contents were much higher in Diets S and L (28.09 and 55.31% of the total NSP, respectively) than in the other diets. Rhamnose was detected in Diets S and L, but not in Diets B and W. The main difference between the total NSP of Diets B and W related to their proportion of water-soluble components. The amount of water-soluble components represented 11.07% of
DIGESTIBILITY OF POLYSACCHARIDES
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the total NSP in Diet B, compared with 19.65% in Diet W (Table 3). The amount of the watersoluble pentosans (arabinose and xylose) represented 6% of the total pentosans in Diet B, versus 15% in Diet W. Lesser amounts of glucose, xylose, and uronic acids and greater amounts of galactose were found in the total NSP of Diet L, compared to Diet S.
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The recoveries of total nonstarch polysaccharides from excreta were high (78.1 to 92.1%) for both the cockerels and the ducks, irrespective of the diet (Table 4). The ducks excreted slightly more polysaccharides than the cockerels; but the differences between the two avian species were small in each case (differences of .6 to 5.1%). The most-pronounced differences between the two avian species were observed for minor components of polysaccharides, such as xylose (Diet L), mannose (all diets), and galactose (Diets B and W). The recovery of NSP was similar among the diets, except for Diet W (the lowest recovery of NSP from both avian species).
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Fecal Recovery of Nonstarch Polysaccharides from Rats The fecal recoveries of NSP were much lower from the rats than from the cockerels and ducks, ranging from 14.3% (Diet L) to 55.9% (Diet B, Table 5). The recovery of NSP from wheat bran (56%) and from whole wheat (48%) was higher than from soybean meal (34%) and white-lupin meal (14%). The fecal recovery of NSP from whole-wheat grain was significandy lower (P<.05) than that from wheat bran. In rats, the xylose and glucose units were much-less degraded than the arabinose, galactose, and uronic acids in Diets S and L (Table 5). Thus, the low recovery from the rats for NSP in Diets S and L was mainly accounted for by the low recovery of their arabinose, galactose, and uronic-acid units. The galactose value recovered from the rats was significandy lower (P<.001) with Diet L than with Diet S. Comparison of Digestible Energy Values Among Cockerels, Ducks, and Rats The mean AMEn value (megajoules per kilogram of dry matter) of the four diets
B W S L B W S L
Cockerels
***
1.63
92.3
b
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Fucose
NS
* ***
** *** **
92.1 c 76.5 d 92.1 c 99.7 b 94.3 bc 80.5^ 89.6C 112.9* 2.23
87.5*b 77.3C 87.2*b 84. l b 91.0* 83.0b 85.8 ab 87.8*b 1.79
Xylose
Arabinose
Means within columns with no common superscripts are significantly different (P<.05).
NS NS NS
128.9 127.3 7.72
125.1 122.6
Rhamnose
B = bran, W = wheat, S = soybean meal, L = lupin meal; NS = nonsignificant.
***P<.001.
**P<.01.
*P<.05.
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Diet
Species
NS
*** ***
29.9 e 40.0 de 69.1*b 47.9 cd 40.2 de 59.5 bc 74.2* 58.9 bc 4.32
(%\
Mannose
TABLE 4. Excreta recovery of dietary nonstarch polysaccharides from cockerels an
629
DIGESTIBILITY OF POLYSACCHARIDES
measured for ducks (15.06) was almost the same as that measured for cockerels (15.01, Table 2). The significant differences between the AMEn values for the cockerels and the ducks, for Diets B and S, did not exceed .23 MJ per kg of dry matter. The DE values from the four diets were significandy higher (P<.001) for the rats than for the birds. The greatest differences between the DE values for the rats and birds were observed with Diets S and L. The digestibility of the NSP in rats was also highest with Diets S and L.
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Diet W contained more water-soluble NSP than Diet B. This finding agrees with ones from previous works, showing a much higher ratio for water-soluble NSP to water-insoluble NSP in whole-wheat grain than in wheat bran (Englyst, 1981). The present finding also agrees with the observation that the ratio is much higher for wheat flour with a low extraction rate than for whole-wheat flour (Nyman et al., 1984). The composition of dietary NSP (Table 3) reflected the features found in cereal grains (Diets B and W) or in leguminosae cotyledons (Diets S and L), exhibiting the typical differences usually found between these two groups of plant material (Carre and Brillouet, 1986). The composition of the polysaccharides in Diets S and L was somewhat different from that of pure soybean cotyledons (Brillouet and Carre\ 1983) or of pure white-lupin cotyledons (Carre" et al, 1985), in that their xylose and glucose contents were higher than those of the polysaccharides from pure cotyledons. This outcome indicates that Diets S and L probably contained particles of hull in addition to cotyledons.
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The high NSP recovery values from birds on the four diets agree with the assumption proposed in a previous study (Carre" and Leclercq, 1985), namely, that the ability of cockerels to digest plant cell walls is very low. Lupin NSP, observed to be digested extensively by the rats, remained practically undigested by the cockerels and the ducks. The differences in the NSP recovery values between the cockerels and ducks were very low,
630
CARR£ ET AL.
a verification of the fact that the ability of the ducks to digest NSP is no greater than that of the cockerels. The ducks even excreted slightly more of the nonstarch polysaccharides. This was observed especially for minor components of the polysaccharides, suggesting that a part of the difference between the data for the cockerels and the ducks was due to a greater excretion of nondietary components by the ducks. That observation agrees with a previous report by Mohamed et al. (1984), showing that ducks excrete more endogenous energy than chickens. The nondietary losses probably were the reason why the recovery values exceeded 100% for some minor sugars (Table 4). Nondietary sugars could come from either endogenous or bacterial glycoproteins. However, the arabinose units in the excreta probably came entirely from dietary plant-cell walls, since this sugar is a very scarce component in animal tissues and in bacteria. With the cockerels and the ducks, the recovery of total NSP was less for Diet W than for the three other diets (Table 4). Since the main feature distinguishing the NSP of Diet W was its high proportion of water-soluble components, this water-soluble fraction may have been digested to a greater extent than the waterinsoluble fraction. The recovery of the watersoluble NSP was assumed to be different from the recovery of the water-insoluble NSP; also, the respective recovery of these units was assumed to be the same in Diets B and W (because of their very similar composition). Thus, the recovery of these units can be calculated easily. The recovery of the waterinsoluble NSP from Diets B and W would be 96.9% for the cockerels and 104% for the ducks; those of the water-soluble NSP from Diets B and W would be .5% for the cockerels and -12.5% for the ducks. Therefore, according to these calculations, the water-insoluble NSP was almost undegraded. Yet, the water-soluble NSP was extensively degraded in the intestinal tract of the birds. These observations are similar to those from a previous study (Carre" and Leclercq, 1985), showing that the water-insoluble NSP from white-lupin cotyledons was not digested in adult cockerels. These observations also agree with the equation of the AMEn prediction based on the measurement of the water-insoluble, cell walls (Carre et al., 1984). The fact that the cecal bacteria of domestic birds are devoid of cellulolytic activity (McNab, 1973) would explain why birds are unable to digest waterinsoluble, cell-wall material. This can also be explained by the ingesta-fractionation mecha-
nism of the intestinal tract, which only allows the water-soluble fraction and the very fine particles of ingesta to enter into the ceca of domestic birds (McNab, 1973). Assuming that the water-soluble NSP was completely degraded in the intestinal tract of the birds, the total NSP excreted by the birds would correspond to the water-insoluble NSP ingested. According to this assumption, the recovery of water-insoluble NSP was very similar for the four diets and very near 100% [cockerels-97% (Diet B), 97.3% (Diet W), 94.5% (Diet S), 96.8% (Diet L); ducks-102.6% (Diet B), 101.3% (Diet W), 95.1% (Diet S), 102.3% (Diet L)]. An examination of the carbohydrates with a low molecular weight occurring in the 80%-ethanolic supernatants of the excreta (Table 6) provided further information about the ability of birds to digest water-soluble carbohydrates through bacterial fermentation. The galactose level of this fraction was much higher for the birds on the leguminosae diets (Diets S and L, Table 6). This outcome probably is related to the high levels of galactose-containing oligosaccharides found in the leguminosae cotyledons (Quemener and Brillouet, 1983) and not in the wheat grain (Cerning-Beroard et al., 1977). Thus, one could expect the major part of the galactose units found in this ethanolic fraction of excreta to correspond with the undigested galactose-containing oligosaccharides (at least for the birds fed Diets S and L). Using the contents of raffinose, stachyose, and verbascose reported in the literature for soybean and white-lupin cotyledons (Quemener and Brillouet, 1983) and the amounts of galactose found in the ethanolic extract of the excreta, the apparent digestibility values for these oligosaccharides would be 82% (Diet S) and 87% (Diet L) for the cockerels and 78% (Diet S) and 82% (Diet L) for the ducks. Since these galactose-containing oligosaccharides supposedly are only degraded through bacterial fermentation, these data suggest that an extensive fermentation of water-soluble carbohydrates can occur within the intestinal tract of birds. The extent of the degradation of the watersoluble, nonstarch polysaccharides is likely to have been as high as that of the fermentable galactose-containing oligosaccharides (80 to 90%). By contrast, the water-insoluble, nonstarch polysaccharides remained almost undegraded by the cockerels and the ducks.
DIGESTIBILITY OF POLYSACCHARIDES
631
Fecal Recovery of Nonstarch Polysaccharides from Rats
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The NSP recovered from the rats (Table 5) was strikingly low, compared with that found in the birds. Moreover, variations between diets in the NSP recovered were much higher for the rats than for the birds. The fecal recovery of NSP from whole-wheat grain was significantly lower (P<.05) than that from wheat bran, but the amounts of fecal NSP were very similar (Diet B versus Diet W), expressed as a percentage of dietary waterinsoluble NSP (Diet B, 62.8%; Diet W, 59.7%). This observation, which is similar to the one for cockerels and ducks, leads to conclusions similar to those formulated for the two avian species: the water-soluble NSP is probably degraded extensively, versus the water-insoluble NSP, which is more resistant to degradation. The difference observed in rats between the cereal and leguminosae diets cannot be related to the difference in the relative amounts of watersoluble polysaccharides, since those amounts were either similar or lower for the leguminosae diets than for the cereal diets. Most likely, such differences are related to the composition of the WICW. A higher proportion of lignin is found in wheat WICW (7.2%; Carre" and Brillouet, 1986) than in soybean meal (1.9%; Carre and Brillouet, 1986) or in white-lupin cotyledon WICW (1.7%; Carre et al., 1985). In addition, the WICW of whole-wheat grain or of wheat bran contains almost no pectic substances (Carre and Brillouet, 1986); whereas the WICW of soybean meal or of white-lupin cotyledon contains high amounts of pectic substances (40 and 66%, respectively; Brillouet and Carre\ 1983; Carre" et al., 1985). The low recovery of NSP from rats fed Diets S and L resulted from the low recovery of their pectic sugars, namely the arabinose, galactose, and uronic-acid units, which are major components of the NSP in these diets. Therefore, by contrast with birds, rats digest water-insoluble cell walls to an extent that depends on their chemical structure. Comparison of Digestible Energy Values Among Cockerels, Ducks, and Rats The similarity observed between the energy values for cockerels and ducks agrees with the similarity found between the NSP recovered from cockerels and ducks. The present observations, which suggest similar energy values for
632
CARRE ET AL.
both avian species, agrees with most of the data reported by Siregar and Farrell (1980) and by Mohamed et al. (1984). The DE values for birds were calculated to allow for a comparison with the energy values for rats. This calculation of DE values was based on the assumption that the digestibility of proteins in birds would not vary among species and diets and would be equal to 82.5%, according to a mean value proposed by Sibbald et al. (1963). Similar levels of digestibility were observed for the proteins from soybean and white-lupin meal (Carre" and Leclercq, 1985), the main protein sources used in the present experimental diets. The apparent protein digestibility has, however, been reported as higher for ducks than for chicks, with a mean difference of 4.8% between species (Mohamed et al., 1984). This difference only accounts for .078 MJ per kg in the correction for urinary nitrogen and, thus, seems negligible in terms of energy value. Even though the DE values calculated for birds is slightly different from the actual in vivo DE values, this hypothetical difference cannot explain the large differences between the DE values reported here for rats and birds. The differences between the DE values for rats and birds were of similar magnitude to the NSP recovery values, suggesting that the differences in the DE values between rats and birds were due primarily to differences in the ability of these species to digest NSP. In conclusion, the present study showed that water-soluble NSP is the only fraction of the NSP that can be digested by both cockerels and ducks; whereas the water-insoluble NSP fraction remained almost undigested by both species. However, rats were able to digest the waterinsoluble NSP to an extent that depended on the chemical structure of the NSP. This would explain the differences between the DE values recorded for rats and birds. The results reported here support using the WICW measurement as an estimate of fiber content when predicting the energy value of poultry diets (Carre et al., 1984; Carre and Brillouet, 1989). ACKNOWLEDGMENTS
The authors are grateful to Mr. L. Conan of the Institut National de la Recherche Agronomique (INRA), Le Magneraud, France, for managing the rats. The authors also thank Mrs. N. Sellier and Mr. G. Guy (INRA, Nouzilly, France) for helpful assistance in feeding the experimental birds.
REFERENCES Asp, N. G., and C. G. Johansson, 1984. Dietary fibre analysis. Nutr. Abstr. Rev. Clin. Nutr. (A) 54:735-752. Blakeney, A. B., P. J. Harris, R. J. Henry, and B. A. Stone, 1983. A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr. Res.l 13:291-299. Blumenkrantz, N., and G. Asboe-Hansen, 1973. New method for quantitative determination of uronic acids. Anal. Biochem. 54:484-489. Boehringer Mannheim, 1980. Starch. UV-method for the determination of native starch in foodstuffs. In: Methods of Enzymatic Food Analysis. Boehringer Mannheim, 6800 Mannheim 31, West Germany. Brillouet, J. M., and B. Carre, 1983. Composition of cell walls from cotyledons of Pisum sativum, Vicia faba and Glycine max. Phytochemistry 22:841-847. Carre, B., and J. M. Brillouet, 1986. Yield and composition of cell wall residues isolated from various feedstuffs used for non-ruminant farm animals. J. Sci. Food Agric. 37:341-351. Carre, B., and J. M. Brillouet, 1989. Determination of waterinsoluble cell walls in feeds:interlaboratory study. J. Assoc. Off. Agric. Chem. 72:463-467. Carre, B., J. M. Brillouet, and J. F. Thibault, 1985. Characterization of polysaccharides from white lupin (Lupinus albus L.) cotyledons. J. Agric. Food Chem. 33: 285-292. Carre, B., R. Escartin, J. P. Melcion, M. Champ, G. Roux, and B. Leclercq, 1987. Effect of pelleting and associations with maize or wheat on the nutritive value of smooth pea (Pisum sativum) seeds in adult cockerels. Br. Poult. Sci. 28:219-229. Carre, B., and B. Leclercq, 1985. Digestion of polysaccharides, protein and lipids by adult cockerels fed on diets containing a pectic cell-wall material from white lupin (Lupinus albus L.) cotyledon. Br. J. Nutr. 54:669-680. Carre, B., B. Prevotel, and B. Leclercq, 1984. Cell wall content as a predictor of metabolisable energy value of poultry feedingstuffs. Br. Poult. Sci. 25:561-572. Cerning-Beroard, J., C. Mercier, and A. Guilbot, 1977. Composition glucidique du ble. Ann. Technol. Agric. (Paris) 26:79-115. Cowan, P. J., 1980. The goose: an efficient converter of grass? World's Poult. Sci. J. 36:112-116. Duncan, D. B., 1955. Multiple range and multiple F tests. Biometrics 11:1-42. Englyst, H., 1981. Determination of carbohydrate and its composition in plant materials. Pages 71-93 in: The Analysis of Dietary Fiber in Food. W.P.T. James and O. Theander, ed. Marcel Dekker, Inc., New York, NY, and Basel, Switzerland. Fonnesbeck, P. V., L. E. Harris, and L. C. Kearl, 1974. Comparative digestion of plant cell walls by animals. Utah Academy Proc. 51:85-92. Hill, F. W., and D. L. Anderson, 1958. Comparison of metabolizable energy and productive energy determinations with growing chicks. J. Nutr. 64:587-603. Janssen, W.M.M.A., and B. Carre\ 1985. Influence of fibre on digestibility of poultry feeds. Pages 71-86 in: Recent Advances in Animal Nutrition-1985. W. Haresign and D.J.A. Cole, ed. Butterworths, London, England, U.K. McNab, J. M., 1973. The avian caeca: a review. World's Poult. Sci. J. 29:251-263. Mohamed, K., B. Leclercq, A. Anwar, H. El-Alaily, and H. Soliman, 1984. A comparative study of metabolisable
DIGESTIBILITY OF POLYSACCHARIDES energy in ducklings and domestic chicks. Anim. Feed Sci. Technol. 11:199-209. Muztar, A. J., S. J. Slinger, and J. H. Burton, 1977. Metabolizable energy content of freshwater plants in chickens and ducks. Poultry Sci. 56:1893-1899. Nehring, K., and B. Knabe, 1961. Die Verdaulichkeit verschiedener Futterstoffe bei Enten. Arch. Geflugelkd. 25:263-289. Nyman, M , M. Siljestrom, B. Perdersen, K. E. Bach Knudsen, N. G. Asp, C. G. Johansson, and B. O. Eggum, 1984. Dietary fiber content and composition in six cereals at different extraction rates. Cereal Chem. 61: 14-19. Quemener, B., and J. M. Brillouet, 1983. Ciceritol, a pinitol digalactoside from seeds of chick pea, lentil and white lupin. Photochemistry 22:1745-1751.
633
Schubert, R., G. Richter, and K. Gruhn, 1982. Vergleichende untersuchungen zur verdauungsleistung von moschus-und pekingenten sowie legehennen. Arch. Tierernahr. 32:531-537. Sibbald, I. R., J. Czamocki, S. J. Slinger and G. C. Ashton, 1963. The prediction of the metabolizable energy content of poultry feedingstuffs from a knowledge of their chemical composition. Poultry Sci. 42:486-492. Sibbald, I. R., K. Price, and J. P. Barrette, 1980. True metabolizable energy values for poultry of commercial diets measured by bioassay and predicted from chemical data. Poultry Sci. 59:808-811. Siregar, A. P., and D. J. Farrell, 1980. A comparison of the energy and nitrogen metabolism of fed ducklings and chickens. Br. Poult. Sci. 21:213-227. Snedecor, G., and W. Cochran, 1980. Statistical Methods. 7th ed. Iowa State Univ. Press, Ames, IA.
The cell walls of plants represent the leastdigested components of diets in chickens. This explains why cell-wall related parameters are efficient predictors of the energy value in the diets for chickens (Sibbald et al., 1980; Carre et al., 1984; Janssen and Carre, 1985). Previous research (Carre" et al., 1984; Carre" and Leclercq, 1985) suggested that the waterinsoluble, cell-wall procedure probably is the most-convenient method of fiber determination in order to predict the energy value of diets for chickens. This suggestion was based mainly on the studies investigating cell walls from white lupin cotyledons, showing no digestion of this cell-wall material in cockerels (Carre and Leclercq, 1985; Carr6 et al., 1985). In the present study, this aspect was re-examined by measuring the digestibility of cell-wall components from other sources. For the current experiment, digestibility was measured in cockerels and also in Muscovy
' l MJ = 239 kcal.
ducks. Previous data on the ability of palmipeds to digest cell-wall fractions were somewhat confusing. In a review, Cowan (1980) concluded that cell-wall fractions are poorly digested by geese. Nehring and Knabe (1961) and Schubert et al. (1982) reported digestibility values for crude fiber ranging from 0 to 36% in ducks. Siregar and Farrell (1980) and Mohamed et al. (1984) did not find great differences between the energy values in the diets for chickens and ducks, suggesting that the digestibility values for cell-wall fractions probably are similar for chickens and ducks. By contrast, Muztar et al. (1977), who used fresh plants, observed great differences in the energy values between ducks and chickens. Previously, cell-wall digestibility for ducks was estimated by using a measurement of crude fiber. Further studies are needed, however, in order to obtain information about the digestibility of the whole cell-wall fraction in ducks, since crude fiber represents only a small part of the whole cell-wall (Asp and Johansson, 1984).
623
624
CARRE ET AL.
Because the colon of birds is much shorter than that of mammals, differences would be expected between birds and mammals with regard to cell-wall digestion (Fonnesbeck et al., 1974). Yet, studies dealing with a direct comparison between birds and mammals are very scarce in the literature. In the present study, cockerels, Muscovy ducks, and rats received diets in which the only source of cell walls was wheat bran, whole-wheat grain, soybean meal, or white lupin meal. The digestibility values for nonstarch polysaccharides (the main components of cell walls) and the energy values of diets were measured in the three animal species. MATERIALS AND METHODS
Diets Four diets containing similar amounts of protein (27.4% of the dry matter), lipids (5.9% of the dry matter), and total nonstarch polysaccharides (NSP, 7.8% of the dry matter) were tested (Tables 1 to 3). In each diet, cell walls were provided by a single source: wheat bran (Diet B), whole-wheat grain (Diet W), defatted and dehulled soybean meal (Diet S), or defatted and dehulled white-lupin meal (Diet L).
The feed mixtures were as follows (percentage of water in the mixture): Diet B, 59.3; Diet W, 58.3; Diet S, 54.5; Diet L, 54.5. About 40 g of dry matter were given with one force-feeding. The balance experiment was conducted using the following periods successively: 24 h of adaptation, including two force-feedings; 24 h of starvation, plus a 54-h balance period, including 30 h of feeding (four force-feedings); and 24 h of final starvation. The cockerels had free access to water throughout the experiment; but the ducks had access to water only twice daily for 30 min, 2 h after force-feeding. This procedure was used with the ducks in order to avoid any regurgitation of the feed during drinking and to reduce the amount of spilled water. The ducks had free access to water during fasting. Excreta were collected twice daily during the balance period, stored immediately at -20 C, freeze-dried, equilibrated at the ambient temperature, weighed, and finely ground. Rats
A balance experiment was conducted on male Wistar rats3 using the experimental diets given to the cockerels and ducks. The rats were 46 days of age and weighed 184 g (SD equals 10 g) at the start of the experiment. Each of the four diets was given as mash to seven replicates. A replicate was represented by one animal placed Cockerels and Ducks in an individual metal cage. The cages were provided with drinking water and with special A balance experiment was conducted using feeders designed to avoid spillage. A plastic tray cockerels and Muscovy ducks. The cockerels, covered with blotting-paper designed to absorb from a commercial broiler strain (Hubbard), urine was put under each cage for feces were 73 days of age and weighed 2,602 g (SD collection. Feed for ad libitum intake was equals 264 g) at the beginning of the balance available to the rats for 3 days (Day 1 to Day 3). experiment. The Muscovy ducks, from a com- Then, the rats were restricted to 20 g of feed per mercial strain,2 had a similar weight (2,770 g; day for 7 days (Day 4 to Day 10). The actual feed SD = 279 g) and were slightly younger (60 intake was measured from Day 5 to Day 9. Feces days). Each of the four diets was given to seven were collected twice daily, from Day 6 to Day replicates from each of the two species of bird. A 10. The feces were stored immediately at -20 C replicate constituted 1 bird placed in an individ- after collection; then freeze-dried, equilibrated ual, metal cage. The cages were provided with at the ambient temperature, weighed, and finely drinking water and plastic trays for excreta ground. collection. The sides of the duck cages were covered with plastic plates in order to recover the excreta ejected horizontally by these birds. Analyses The birds were force-fed the experimental The apparent metabolizable-energy values diets as a meal-water mixture by using a syringe. corrected for nitrogen equilibrium (AME„) were calculated for the birds, as described by Hill and Anderson (1958). For calculating the AMEn, the birds are supposed to excrete an amount of ^anedin, Grimaud, 49450 Roussay, France. 3 urinary nitrogen equal to that of the digested 1FFA CREDO, BP 109, 69210 TArbrefle, France.
625
DIGESTIBILITY OF POLYSACCHARIDES TABLE 1. Ingredients used in the diets Diet Ingredients
Bran
Wheat bran Whole-wheat grain Defatted soybean meal, dehulled Defatted white-lupin meal, dehulled Soybean-protein isolate Corn starch Com oil DL-methionine Calcium carbonate Dicalcium phosphate Sodium chloride Choline chloride, 50% Vitamin mixture1 Mineral mixture2 Dry-matter content
19.7
Soybean meal
Wheat
Lupin meal
75.0 50.0 24.4 48.8 4.4 .15 1.0 1.0 .33 .1 .02 .1 87.6
24.9 15.4 51.9 5.1 .2 1.0 1.0 .28 .1 .02 .1 90.0
18.8 43.2 4.1 .15 1.0 1.0 .33 .1 .02 .1 89.6
3.7
1.6
1.0 .28 .1 .02 .1 88.3
Supplied (milligrams per kilogram of diet): retinol, 3; cholecalciferol, .037; a-tocopheryl acetate, 15; menadione sodium bisulfite, 5; riboflavin, 4; calcium pantothenate, 8; nicotinic acid, 25; pyridoxine hydrochloride, 1; folic acid, .2; biotin, .1; cyanocobalamin, .008; butylated hydroxytoluene, 124. Supplied (milligrams per kilogram of diet): Mn0 2 , 168; ZnO, 105; FeS0 4 -7H 2 0, 218; CuS0 4 -5H 2 0, 35; C0CO3, .7; Na 2 Se0 3 , .5; KI, 1.6.
TABLE 2. Composition, energy value, and feed intake for the diets, dry-matter basis Diet Measurement N times 6.25, % Lipids, %1 Water-insoluble cell wall, % Water-insoluble, nonstarch polysaccharides, % Water-soluble, nonstarch polysaccharides, % Gross energy, MJ per kg AME„, MJ per kg: cockerels (predicted) cockerels (measured) ducks (measured)4 DE, MJ per kg: cockerels (calculated)4,5 ducks (calculated)4'5 rats (measured)4 Feed intake:6 cockerels, g per 2 days4 ducks, g per 2 days rats, g per 5 days4
Bran
Soybean meal
Wheat 27.29 5.8 8.06 6.03 1.47 19.44
27.85 5.9 9.83 7.30 .91 19.52
Lupin meal
26.72 5.6 9.11 7.59 .66 19.00
27.82 6.5 7.42 6.35 .81 19.70
14.90 14.98 14.78
± .04 ± .03
15.15 14.90 ± 15.13 ±
.13 .08
14.64 14.33 ± .05 14.56 ± .03
15.49 15.84 ± 15.75 ±
.05 .05
16.32 16.12 17.27
± .04 ± .03 ± .03
16.21 ± 16.44 ± 17.28 ±
.13 .08 .03
15.61 ± .05 15.84 ± .03 17.05 ± .03
17.18 ± 17.09 ± 18.47 ±
.05 .05 .03
142.9 143.9 86.5
± .4 ± .9 ± .1
148.6 149.1 87.3
± .8 ± 1.8 ± .2
173.0 172.7 89.0
± .4 ± .4 ± .1
166.5 166.7 88.8
± .5 ± 1.7 ± .4
'Calculated value. Corrected for residual starch. ^Prediction of AME,, based on gross energy, crude protein, and the water-insoluble, cell-wall contents (Cane et at., 1984); 1 MJ = 239 kcal. Means ± SE obtained with seven animals. ^ e calculation of digestible energy (DE) was as follows: measured AME„ + .0300 x N (grams per kilogram of feed). The last factor, which corresponds to the correction for urinary nitrogen, was taken from Sibbald et al. (1963). •Teed intakes during the balance experiments.
626
CARR£ ET AL.
nitrogen (Sibbald et al., 1963). Assuming an apparent digestibility value of 82.5% for protein, Sibbald et al. (1963) proposed an energy value for urinary nitrogen equivalent to .0300 MJ per g of ingested nitrogen. This calculation of urinary energy losses was applied in the present experiment, thus assuming the same apparent protein digestibility value of 82.5% for each experimental diet and each species. Then, the digestible energy (DE) values were calculated for the birds from the AMEn values, by correcting the amount of excreted energy for the amount of urinary energy losses. Starch was measured by the dimethylsulfoxide procedure (Boehringer Mannheim, 1980) as described previously (Carre" et al., 1987). The water-insoluble cell walls (WICW) were isolated from the feed (3-g samples), as described by Carre" et al. (1984). The water-soluble fractions of the feed were pooled, extensively dialyzed against water at 4 C, freeze-dried, refluxed in 60 mL of ethanol-water (80:20, vol/ vol) for 30 min, cooled at the ambient temperature, allowed to stand for 2 h, and centrifuged. The resulting precipitate represented the watersoluble, ethanol-insoluble fraction (WSEIF). The NSP of the feed was measured from the sugar determinations in the WICW and WSEIF. The neutral sugars of the diet WICW and WSEIF were measured by a gas-liquid-chromatography (GLC) analysis of their alditol-acetate derivatives (Blakeney et al., 1983), following sulfuric-acid hydrolysis (Brillouet and Carre, 1983). Only the diluted sulfuric-acid step was applied for the hydrolysis of the WSEIF. All of the data on glucose were corrected for residual starch. The uronic acids in the diet WICW and WSEIF were measured colorimetrically, using the w-phenylphenol method (Blumenkrantz and Asboe-Hansen, 1973), as described by Brillouet and Carre (1983). The total diet NSP was calculated by adding water-soluble NSP (from WSEIF) to water-insoluble NSP (from the WICW). The neutral sugars of the total NSP were measured in rat feces and bird excreta (30-mg samples) by GLC analysis performed on the acid hydrolysate of the 80% ethanol-insoluble fraction obtained after a-amylase (40 \ig, from Bacillus subtilis) treatment4 (95 C for 10 min, then 55 C for 150 min with enzyme) and a
4 Boehringer Mannheim, 6800 Mannheim 31, West Germany.
Pronase (50 u.g) treatment4 (20 C for 4 h in a 30-mM phosphate buffer, pH 7.5), a chloroformmethanol (2:1, vol/vol) extraction, refluxing in ethanol-water (80:20, vol/vol) for 30 min, and centrifuging. The glucose data were corrected for residual starch, measured on a duplicate sample of feces and excreta previously treated with the same procedure as that used before the acid hydrolysis and GLC analysis. The uronic acids from the total NSP were measured in the feces and excreta, as described previously for diets, directly and without the preparation of a treated residue. Statistical Analysis The NSP recovery values from the birds were analyzed by a two-way analysis of variance according to Snedecor and Cochran (1980). A one-way analysis of variance was used for the rat data. Duncan's multiple range test (Duncan, 1955) was used to compare the individual means of the NSP recovery values. RESULTS
Composition of Dietary Nonstarch Polysaccharides The total NSP contents (the sum of the watersoluble and water-insoluble NSP) varied little between the diets, ranging from 7.16% (Diet L) to 8.26% of the dry matter (Diet S, Table 3). The ratios for the water-soluble NSP to total NSP varied from .080 (Diet S) to .197 (Diet W). The WICW contained the following amounts of nonstarch polysaccharides (as a percentage of WICW): 74.26 (Diet B), 74.81 (Diet W), 83.32 (Diet S), and 85.58 (Diet L). The total NSP composition of Diets B and W were very similar; both appeared to be clearly different from those of Diets S and L (Table 3). The xylose content of the NSP was much higher in Diets B and W than in Diets S and L. Galactose was a minor component in Diets B and W (about 4% of the total NSP). The galactose contents were much higher in Diets S and L (28.09 and 55.31% of the total NSP, respectively) than in the other diets. Rhamnose was detected in Diets S and L, but not in Diets B and W. The main difference between the total NSP of Diets B and W related to their proportion of water-soluble components. The amount of water-soluble components represented 11.07% of
DIGESTIBILITY OF POLYSACCHARIDES
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the total NSP in Diet B, compared with 19.65% in Diet W (Table 3). The amount of the watersoluble pentosans (arabinose and xylose) represented 6% of the total pentosans in Diet B, versus 15% in Diet W. Lesser amounts of glucose, xylose, and uronic acids and greater amounts of galactose were found in the total NSP of Diet L, compared to Diet S.
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The recoveries of total nonstarch polysaccharides from excreta were high (78.1 to 92.1%) for both the cockerels and the ducks, irrespective of the diet (Table 4). The ducks excreted slightly more polysaccharides than the cockerels; but the differences between the two avian species were small in each case (differences of .6 to 5.1%). The most-pronounced differences between the two avian species were observed for minor components of polysaccharides, such as xylose (Diet L), mannose (all diets), and galactose (Diets B and W). The recovery of NSP was similar among the diets, except for Diet W (the lowest recovery of NSP from both avian species).
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Fecal Recovery of Nonstarch Polysaccharides from Rats The fecal recoveries of NSP were much lower from the rats than from the cockerels and ducks, ranging from 14.3% (Diet L) to 55.9% (Diet B, Table 5). The recovery of NSP from wheat bran (56%) and from whole wheat (48%) was higher than from soybean meal (34%) and white-lupin meal (14%). The fecal recovery of NSP from whole-wheat grain was significandy lower (P<.05) than that from wheat bran. In rats, the xylose and glucose units were much-less degraded than the arabinose, galactose, and uronic acids in Diets S and L (Table 5). Thus, the low recovery from the rats for NSP in Diets S and L was mainly accounted for by the low recovery of their arabinose, galactose, and uronic-acid units. The galactose value recovered from the rats was significandy lower (P<.001) with Diet L than with Diet S. Comparison of Digestible Energy Values Among Cockerels, Ducks, and Rats The mean AMEn value (megajoules per kilogram of dry matter) of the four diets
B W S L B W S L
Cockerels
***
1.63
92.3
b
109.6*
Fucose
NS
* ***
** *** **
92.1 c 76.5 d 92.1 c 99.7 b 94.3 bc 80.5^ 89.6C 112.9* 2.23
87.5*b 77.3C 87.2*b 84. l b 91.0* 83.0b 85.8 ab 87.8*b 1.79
Xylose
Arabinose
Means within columns with no common superscripts are significantly different (P<.05).
NS NS NS
128.9 127.3 7.72
125.1 122.6
Rhamnose
B = bran, W = wheat, S = soybean meal, L = lupin meal; NS = nonsignificant.
***P<.001.
**P<.01.
*P<.05.
]
a_e
SE Source of variation with probabilities Species effect Diet effect Species-by-diet interaction
Ducks
Diet
Species
NS
*** ***
29.9 e 40.0 de 69.1*b 47.9 cd 40.2 de 59.5 bc 74.2* 58.9 bc 4.32
(%\
Mannose
TABLE 4. Excreta recovery of dietary nonstarch polysaccharides from cockerels an
629
DIGESTIBILITY OF POLYSACCHARIDES
measured for ducks (15.06) was almost the same as that measured for cockerels (15.01, Table 2). The significant differences between the AMEn values for the cockerels and the ducks, for Diets B and S, did not exceed .23 MJ per kg of dry matter. The DE values from the four diets were significandy higher (P<.001) for the rats than for the birds. The greatest differences between the DE values for the rats and birds were observed with Diets S and L. The digestibility of the NSP in rats was also highest with Diets S and L.
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Composition of Dietary Nonstarch Polysaccharides ^ oo -^- t> ^ wS r-^ oo Tf f^
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Diet W contained more water-soluble NSP than Diet B. This finding agrees with ones from previous works, showing a much higher ratio for water-soluble NSP to water-insoluble NSP in whole-wheat grain than in wheat bran (Englyst, 1981). The present finding also agrees with the observation that the ratio is much higher for wheat flour with a low extraction rate than for whole-wheat flour (Nyman et al., 1984). The composition of dietary NSP (Table 3) reflected the features found in cereal grains (Diets B and W) or in leguminosae cotyledons (Diets S and L), exhibiting the typical differences usually found between these two groups of plant material (Carre and Brillouet, 1986). The composition of the polysaccharides in Diets S and L was somewhat different from that of pure soybean cotyledons (Brillouet and Carre\ 1983) or of pure white-lupin cotyledons (Carre" et al, 1985), in that their xylose and glucose contents were higher than those of the polysaccharides from pure cotyledons. This outcome indicates that Diets S and L probably contained particles of hull in addition to cotyledons.
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The high NSP recovery values from birds on the four diets agree with the assumption proposed in a previous study (Carre" and Leclercq, 1985), namely, that the ability of cockerels to digest plant cell walls is very low. Lupin NSP, observed to be digested extensively by the rats, remained practically undigested by the cockerels and the ducks. The differences in the NSP recovery values between the cockerels and ducks were very low,
630
CARR£ ET AL.
a verification of the fact that the ability of the ducks to digest NSP is no greater than that of the cockerels. The ducks even excreted slightly more of the nonstarch polysaccharides. This was observed especially for minor components of the polysaccharides, suggesting that a part of the difference between the data for the cockerels and the ducks was due to a greater excretion of nondietary components by the ducks. That observation agrees with a previous report by Mohamed et al. (1984), showing that ducks excrete more endogenous energy than chickens. The nondietary losses probably were the reason why the recovery values exceeded 100% for some minor sugars (Table 4). Nondietary sugars could come from either endogenous or bacterial glycoproteins. However, the arabinose units in the excreta probably came entirely from dietary plant-cell walls, since this sugar is a very scarce component in animal tissues and in bacteria. With the cockerels and the ducks, the recovery of total NSP was less for Diet W than for the three other diets (Table 4). Since the main feature distinguishing the NSP of Diet W was its high proportion of water-soluble components, this water-soluble fraction may have been digested to a greater extent than the waterinsoluble fraction. The recovery of the watersoluble NSP was assumed to be different from the recovery of the water-insoluble NSP; also, the respective recovery of these units was assumed to be the same in Diets B and W (because of their very similar composition). Thus, the recovery of these units can be calculated easily. The recovery of the waterinsoluble NSP from Diets B and W would be 96.9% for the cockerels and 104% for the ducks; those of the water-soluble NSP from Diets B and W would be .5% for the cockerels and -12.5% for the ducks. Therefore, according to these calculations, the water-insoluble NSP was almost undegraded. Yet, the water-soluble NSP was extensively degraded in the intestinal tract of the birds. These observations are similar to those from a previous study (Carre" and Leclercq, 1985), showing that the water-insoluble NSP from white-lupin cotyledons was not digested in adult cockerels. These observations also agree with the equation of the AMEn prediction based on the measurement of the water-insoluble, cell walls (Carre et al., 1984). The fact that the cecal bacteria of domestic birds are devoid of cellulolytic activity (McNab, 1973) would explain why birds are unable to digest waterinsoluble, cell-wall material. This can also be explained by the ingesta-fractionation mecha-
nism of the intestinal tract, which only allows the water-soluble fraction and the very fine particles of ingesta to enter into the ceca of domestic birds (McNab, 1973). Assuming that the water-soluble NSP was completely degraded in the intestinal tract of the birds, the total NSP excreted by the birds would correspond to the water-insoluble NSP ingested. According to this assumption, the recovery of water-insoluble NSP was very similar for the four diets and very near 100% [cockerels-97% (Diet B), 97.3% (Diet W), 94.5% (Diet S), 96.8% (Diet L); ducks-102.6% (Diet B), 101.3% (Diet W), 95.1% (Diet S), 102.3% (Diet L)]. An examination of the carbohydrates with a low molecular weight occurring in the 80%-ethanolic supernatants of the excreta (Table 6) provided further information about the ability of birds to digest water-soluble carbohydrates through bacterial fermentation. The galactose level of this fraction was much higher for the birds on the leguminosae diets (Diets S and L, Table 6). This outcome probably is related to the high levels of galactose-containing oligosaccharides found in the leguminosae cotyledons (Quemener and Brillouet, 1983) and not in the wheat grain (Cerning-Beroard et al., 1977). Thus, one could expect the major part of the galactose units found in this ethanolic fraction of excreta to correspond with the undigested galactose-containing oligosaccharides (at least for the birds fed Diets S and L). Using the contents of raffinose, stachyose, and verbascose reported in the literature for soybean and white-lupin cotyledons (Quemener and Brillouet, 1983) and the amounts of galactose found in the ethanolic extract of the excreta, the apparent digestibility values for these oligosaccharides would be 82% (Diet S) and 87% (Diet L) for the cockerels and 78% (Diet S) and 82% (Diet L) for the ducks. Since these galactose-containing oligosaccharides supposedly are only degraded through bacterial fermentation, these data suggest that an extensive fermentation of water-soluble carbohydrates can occur within the intestinal tract of birds. The extent of the degradation of the watersoluble, nonstarch polysaccharides is likely to have been as high as that of the fermentable galactose-containing oligosaccharides (80 to 90%). By contrast, the water-insoluble, nonstarch polysaccharides remained almost undegraded by the cockerels and the ducks.
DIGESTIBILITY OF POLYSACCHARIDES
631
Fecal Recovery of Nonstarch Polysaccharides from Rats
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The NSP recovered from the rats (Table 5) was strikingly low, compared with that found in the birds. Moreover, variations between diets in the NSP recovered were much higher for the rats than for the birds. The fecal recovery of NSP from whole-wheat grain was significantly lower (P<.05) than that from wheat bran, but the amounts of fecal NSP were very similar (Diet B versus Diet W), expressed as a percentage of dietary waterinsoluble NSP (Diet B, 62.8%; Diet W, 59.7%). This observation, which is similar to the one for cockerels and ducks, leads to conclusions similar to those formulated for the two avian species: the water-soluble NSP is probably degraded extensively, versus the water-insoluble NSP, which is more resistant to degradation. The difference observed in rats between the cereal and leguminosae diets cannot be related to the difference in the relative amounts of watersoluble polysaccharides, since those amounts were either similar or lower for the leguminosae diets than for the cereal diets. Most likely, such differences are related to the composition of the WICW. A higher proportion of lignin is found in wheat WICW (7.2%; Carre" and Brillouet, 1986) than in soybean meal (1.9%; Carre and Brillouet, 1986) or in white-lupin cotyledon WICW (1.7%; Carre et al., 1985). In addition, the WICW of whole-wheat grain or of wheat bran contains almost no pectic substances (Carre and Brillouet, 1986); whereas the WICW of soybean meal or of white-lupin cotyledon contains high amounts of pectic substances (40 and 66%, respectively; Brillouet and Carre\ 1983; Carre" et al., 1985). The low recovery of NSP from rats fed Diets S and L resulted from the low recovery of their pectic sugars, namely the arabinose, galactose, and uronic-acid units, which are major components of the NSP in these diets. Therefore, by contrast with birds, rats digest water-insoluble cell walls to an extent that depends on their chemical structure. Comparison of Digestible Energy Values Among Cockerels, Ducks, and Rats The similarity observed between the energy values for cockerels and ducks agrees with the similarity found between the NSP recovered from cockerels and ducks. The present observations, which suggest similar energy values for
632
CARRE ET AL.
both avian species, agrees with most of the data reported by Siregar and Farrell (1980) and by Mohamed et al. (1984). The DE values for birds were calculated to allow for a comparison with the energy values for rats. This calculation of DE values was based on the assumption that the digestibility of proteins in birds would not vary among species and diets and would be equal to 82.5%, according to a mean value proposed by Sibbald et al. (1963). Similar levels of digestibility were observed for the proteins from soybean and white-lupin meal (Carre" and Leclercq, 1985), the main protein sources used in the present experimental diets. The apparent protein digestibility has, however, been reported as higher for ducks than for chicks, with a mean difference of 4.8% between species (Mohamed et al., 1984). This difference only accounts for .078 MJ per kg in the correction for urinary nitrogen and, thus, seems negligible in terms of energy value. Even though the DE values calculated for birds is slightly different from the actual in vivo DE values, this hypothetical difference cannot explain the large differences between the DE values reported here for rats and birds. The differences between the DE values for rats and birds were of similar magnitude to the NSP recovery values, suggesting that the differences in the DE values between rats and birds were due primarily to differences in the ability of these species to digest NSP. In conclusion, the present study showed that water-soluble NSP is the only fraction of the NSP that can be digested by both cockerels and ducks; whereas the water-insoluble NSP fraction remained almost undigested by both species. However, rats were able to digest the waterinsoluble NSP to an extent that depended on the chemical structure of the NSP. This would explain the differences between the DE values recorded for rats and birds. The results reported here support using the WICW measurement as an estimate of fiber content when predicting the energy value of poultry diets (Carre et al., 1984; Carre and Brillouet, 1989). ACKNOWLEDGMENTS
The authors are grateful to Mr. L. Conan of the Institut National de la Recherche Agronomique (INRA), Le Magneraud, France, for managing the rats. The authors also thank Mrs. N. Sellier and Mr. G. Guy (INRA, Nouzilly, France) for helpful assistance in feeding the experimental birds.
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Schubert, R., G. Richter, and K. Gruhn, 1982. Vergleichende untersuchungen zur verdauungsleistung von moschus-und pekingenten sowie legehennen. Arch. Tierernahr. 32:531-537. Sibbald, I. R., J. Czamocki, S. J. Slinger and G. C. Ashton, 1963. The prediction of the metabolizable energy content of poultry feedingstuffs from a knowledge of their chemical composition. Poultry Sci. 42:486-492. Sibbald, I. R., K. Price, and J. P. Barrette, 1980. True metabolizable energy values for poultry of commercial diets measured by bioassay and predicted from chemical data. Poultry Sci. 59:808-811. Siregar, A. P., and D. J. Farrell, 1980. A comparison of the energy and nitrogen metabolism of fed ducklings and chickens. Br. Poult. Sci. 21:213-227. Snedecor, G., and W. Cochran, 1980. Statistical Methods. 7th ed. Iowa State Univ. Press, Ames, IA.