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A comprehensive approach of the rabbit digestion:
consequences of a reduction in dietary fibre supply
a ,
*
a,b c˜
T. Gidenne
, V. Pinheiro
, L. Falcao e Cunha
a
INRA, Station de Recherches Cunicoles, BP 27, 31326 Castanet, France b
˜
UTAD, Secc¸ao de Zootecnia, apt. 201, 5000 Vila Real Codex, Portugal c
˜ ˜
ISA, Secc¸ao de Produc¸ao Animal, Tapada de Ajuda, 1399 Lisboa Codex, Portugal
Received 17 March 1999; received in revised form 9 July 1999; accepted 16 August 1999
Abstract
The effects of dietary fibre level (20–16–12% acid detergent fibre [ADF]), without variations in the proportions of the fibre fractions (hemicellulose, cellulose, lignin . . . ), were studied with respect to many aspects of rabbit digestion (ileal digestibility, transit, microbial activity), growth and health. For the lowest level of ADF, the voluntary intake of animals was reduced by 25% and weight gain by 9%, during the two weeks postweaning (28–42 days), and there was a sharp increase (P,0.01) of morbidity between 42 and 70 days old. A linear reduction of the whole tract digestibility for OM was observed according to ADF level (21.6 unit per % ADF), without significant changes in fibre digestibility. When ADF level passed from 20 to 12%, ileal digestibility of organic matter increased from 38 to 61%, while it decreased from 27 to 17% in the caeco-colic segment. Starch ileal digestibility was lowered by 5.7 units with the reduction of the ADF / starch ratio, but remained at a very high level (.93%). A sharp increase in mean retention time between ileum and rectum (138%) was noticed, reaching 19 h for the lowest ADF level. The bacterial fibrolytic activity was significantly reduced with the lowest ADF level (Fig. 1), and pectinolytic activity was more particularly affected (240%). Two weeks after weaning the VFA level decreased linearly and significantly (P,0.01) with reduction of ADF level, while at 10 weeks no significant effect was observed. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Ileal digestion; Caecal microbial activity; Retention time; Rabbit; Dietary fibre
1. Introduction adapted to more concentrated feeds that are
efficient-ly digested in the upper segment of the tract ˜
As a monogastric herbivorous animal, the rabbit (Carabano and Piquer, 1998). However, information
exhibits a digestive physiology adapted to high on the partition of digestion between small intestine intake of dietary fibre (DF) which is fermented in the and caeco-colic segment is very scarce (three studies
hindgut (caecum and proximal colon), but also only), and moreover does not relate digestion to rate
of passage or caecal microbial activity (CMA) or with zootechnical performances. Therefore, we
de-*Corresponding author. Tel.:133-56-128-5103; fax:1
33-56-veloped a new approach to obtain more
comprehen-128-5319.
E-mail address: gidenne@toulouse.inra.fr (T. Gidenne) sive information on rabbit digestion, that combined
Table 1
measurements of parameters cited previously in a set
Ingredients and composition of the experimental diets
of experiments using a single and a simplified dietary
Diets A20 A16 A12
model.
A reduced fibre intake is known to increase the Ingredients %
incidence of digestive disturbances in the growing Wheat 12.0 32.0 50.0
Soya bean meal 9.7 13.7 17.5
rabbit (Lebas et al., 1998). Digestive consequences
Wheat bran 22.0 9.8 –
of fibre are determined as well by the quantity of
Dehydrated lucerne meal 24.0 17.0 9.0
dietary fibre consumed as by the degradability of cell Dehydrated beet pulp 25.0 19.5 15.0
wall components in relation to their physico-chemi- Wheat straw 6.0 6.0 6.0
a
cal structure, such as particle size (Gidenne et al., Minerals and vitamins 1.3 2.0 2.5
1991a). However, very few studies separated the
Chemical analysis (g / kg air dry basis)
effect of the DF content from that of the nature of
Organic matter 858 861 864
the cell wall, because complex dietary models were Crude protein (Nx6.25) 153 161 170
b
often used. Thus in the present study, we studied Lysine 8.2 8.1 8.3
b
only the effect of a fibre level reduction, without Sulphur amino acids 6.8 6.9 7.0
Starch 104 213 295
variations in the proportions of the different fibre
Neutral-detergent fibre (NDF) 393 313 238
fractions (cellulose, lignin, etc.), and using an
origi-Acid-detergent fibre (ADF) 202 155 117
nal comprehensive approach of rabbit digestion. Acid-detergent lignin (ADL) 36 28 21
b
Water insoluble pectins 88 71 57 c
NNCC 312 387 456
ADF / starch ratio 1.9 0.7 0.4
2. Materials and methods
a
Sodium chloride, calcium carbonate, dibasic calcium phos-phate, DL methionine, L-lysine, premix (0.5%).
2.1. Experimental design and diets
b
Calculated from tabulated data on ingredients (IO7, 1993). c
NNCC: Non nitrogenous cellular content5OM2CP2NDF.
A set of four experiments was designed to test the impact of dietary fibre level on several parameters of
rabbit digestion and on health, feed intake and deficient levels of fibre. In parallel, the level of
growth. In the first, digestibility, ileal flow and starch increased from 10 to 30%, so the ratio ADF / bacterial fibrolytic activity (BFA) were measured in starch reduced four times. In addition, the ratio adult animals (New Zealand White3Californian) digestible crude protein / digestible energy was con-fitted with an ileal cannula. Using the same animals, trolled to obtain a similar digestible protein supply
the rate of passage between ileum and rectum was among diets in agreement with recommendations.
measured in the second experiment. Two further Diets were given in pelleted form, ad libitum
experiments were made on growing rabbits (from throughout the experiments.
weaning to slaughter), one to measure intake, growth
and health status, and the other to evaluate starch 2.2. Total tract and ileal digestibility, and digestion in the ileum and caecal fermentative activi- fibrolytic activity in the caecum
ty.
Three experimental diets were formulated (Table Ileal flow was measured in 12 adult female rabbits
1) to obtain a linear reduction of the different fibre (live weight 2.8–3.2 kg) surgically fitted with a glass fraction (hemicelluloses, cellulose, lignins), corre- cannula at the terminal ileum (Gidenne et al., 1988).
sponding to a 20 to 12% ADF reduction (respective- After a three week recovery period animals were
ly A20, A16, A12). Therefore, the proportions of the divided into two groups (GI and GII) of six animals.
different type of cell wall polysaccharides remained Animals of GI were successively fed with diets
unchanged. The dietary ADF level of 20% corres- containing 20–16–12% of ADF over three periods,
ponded to current recommendations (Maertens, while animals of GII received the diets in the inverse
1992; De Blas and Mateos, 1998), while 16 and 12% order. Within each period, total digestive tract
E.G.R.A.N. (1995), using total and individual faecal retention time of digest without a delay in the mixing collection over 4 days. Ileal flow was then measured compartments, and so represents the rate of passage using diets labelled with mordanted chromium cell in the tubular segment of the tract, i.e. mainly in the wall. Six samples of ileal digesta were collected (30 distal colon (Gidenne, 1994).
min duration at 12 or 16 h interval) from the
cannula, over a 3 day period, such that they covered 2.4. Health status, growth and caecal fermentation
a 24 h period (Gidenne, 1992). The calculation of activity
ileal digestibility coefficients (Gidenne and
Ruc-kebusch, 1989) implies for rabbit a measurement of From weaning (day 28) to slaughter (day 70) the
the intake of feed plus soft faeces. The composition three diets were given ad libitum to three groups of of soft faeces and its production were evaluated on 48 rabbits (New Zealand3Californian) housed in-rabbits wearing a collar to prevent caecotrophy dividually in cages, and submitted to a 12 h light 12
(Gidenne and Lebas, 1987) for two periods of 24 h h dark schedule. Health status was individually
separated by an interval of 24 h. recorded three times a week from weaning to
The enzymatic fibrolytic activity of caecal bacteria slaughter: all clinical signs of sickness (transitory was determined on soft faeces since it give a similar diarrhoea, presence of mucus in excreta, abnormal result compared to sample of caecal content (Jehl et behaviour, etc.) were registered. In addition, feed
al., 1996). Immediately after excretion a sample of intake and live weight were measured weekly and
soft faces was collected in precooled (48C) tubes allowed us to detect any growth disturbances. Mor-containing an anaerobic buffer, and then stored at bidity was defined as animals having abnormally low
2808C until further processing. intake or growth (,mean22.2 sd) or clinical signs
of sickness, and they were not included in growth
2.3. Rate of passage of solid phase in the caeco- performances analyses (Table 3).
colic segment of the tract To evaluate caecal fermentative activity and starch
level in the ileum (segment of 20 cm prior to the The rate of passage between ileum and rectum was ileo-caecal junction), samples of digesta were
ob-measured on the two groups of 6 ileo-cannulated tained from animals slaughtered (between 11:30 and
adult rabbits, following the same design previously 12:30) at 42 days and 70 days of age (10 samples per
described. Caecotrophy was not prevented. Digesta diet and per age). The caecal VFA pool was
calcu-mean retention time of solid phase was obtained by lated by multiplying the caecal content (g digesta) following the rate of faecal excretion of a dose of and the caecal VFA level.
141
Ce-labelled fibre particles (Gidenne, 1994),
intro-duced in the ileum via the cannula. The faecal 2.5. Analytical methods
excretion was fractionated in 36 samples during 96 h
by means of an automatic faecal sampler (API, Organic matter (OM) was determined by ashing
Castanet, France) adapted for use in the rabbit samples at 5508C for 5 h. Measurements of fibre
metabolism cages. After drying, faeces were directly fractions (neutral detergent fibre: NDF, acid
de-analysed for their marker content in a gamma tergent fibre: ADF, acid detergent lignin: ADL) were
spectrometer (Packard Instrument, model 5530, made according to the sequential Van Soest
pro-Downergrove, IL, USA). The digesta mean retention cedure (Van Soest et al., 1991) using an amylolytic
(MRT) was calculated by numerical integration of pre-treatment with a thermostable amylase. Nitrogen
the quantity of marker excreted in faeces: MRT5o was determined by DUMAS combustion method
M .t /i i o M , were t is the time that has elapsedi i using Leco apparatus (model FP-428, Leco Corp., St between marker administration and the ith defecation Joseph, MI, USA), and converted to crude protein
and M is the quantity of marker excreted. MRTi (CP) using the factor 6.25. Gross energy was
mea-includes transit time (TT), which is the time that has sured by an adiabatic calorimeter (PARR Instrument; elapsed between marker administration and the first Moline, IL). Starch was hydrolysed enzymically and
hexokinase (EC 2.7.1.1)-glucose-6-phosphate dehy- were subjected to a statistical analysis in three steps. ¨
drogenase (NAD) (EC1.1.1.49) system (Boehringer First, the effect of the animal group (I vs. II) was
Mannheim). Non-nitrogenous cellular content controlled using data from the two groups fed
(NNCC) was calculated as follows: NNCC5OM2 simultaneously (period 2) the same feed
(inter-(NDF1CP). This fraction corresponds mainly to mediate ADF level). The second step consisted of a
starch but also pectin substances, plus free sugars, two factorial variance analysis (period and diet). As oligosaccharides, and lipids. Particle size distribution no significant effect of group and no interaction
of feeds were analysed on pellets by wet sieving (P.0.2) were observed between period and diet
(Table 2). effect we presented only the results concerning the
Volatile fatty acids (VFA) were analysed on caecal diet effect (Tables 4–6). Means comparison was
digesta samples by gas liquid chromatography performed using the Scheffe test.
(CP9000, Chrompack, Middelburg, The Netherlands) on a semi-capillary column (Bellier, 1994).
After sonication of caecal content, fibrolytic en- 3. Results
zymes were extracted from bacteria according to Jehl
et al. (1996). Cellulolytic, xylanolytic and pec- According to dietary formulation constraints, the
tinolytic activities were assayed respectively on the ratio ADF / starch effectively decreased from 1.9 to following substrates: carboxymethylcellulose, wood 0.4, and the proportions (in % of total dietary fibre)
xylan and citrus pectin (Jehl et al., 1996). The of the different type of cell wall polysaccharides
amount of reducing sugars released after incubation remained unchanged as determined with Van-Soest
with enzyme preparation was then measured and criteria (Table 1). We expressed, however, the fibre
expressed asmmol of reducing sugars released per h level using only the ADF level, for simplicity and
and per g of digesta. because this unit is presently used to define
recom-mendations. Besides, the particle size distribution
2.6. Statistical analysis remained unchanged among the diets (Table 2),
except a slight increase in very fine particles (,0.1
Data on growth and BFA were examined by one- mm).
way analysis of variance using the GLM procedure
of SAS (Statistical Analysis System, 1988). Catmod 3.1. Regulation of feed intake, growth, and health
procedure (SAS) was utilised for data of morbidity status
and mortality. Data from unhealthy animals or
animals having a reversed VFA pattern (propionate / With the reduction of the dietary fibre level (from
butyrate ratio over 2) were not included in the A20 to A12), the voluntary intake of animals was
statistical analysis of VFA. Results were subjected to significantly reduced by 25% during the two weeks
a two factorial (age and diet) analysis of variance postweaning (Table 3) and by 18% during the
according to general linear model (GLM) procedure. finishing fattening period (42–70 days). In adult
Data on digestibility coefficients and rate of passage rabbits the intake was reduced by only 8% (39.2 vs. 35.9 g / kg LW) when fed the A12 diet instead of A20 (Table 7). The growth was also significantly lower (29%, significant linear effect) with the
Table 2
21
Class of particle size (g.kg DM) in the experimental diets lowest fibre supply (diet A12) during the postwean-ing period (Table 3). Feed conversion was lowered
Diets A20 A16 A12
by 20% over the complete period of growth (28–70
Particle size
days), mainly because of the reduction of the feed
x.1 mm 236 242 224
intake.
1 mm.x.0.5 mm 151 159 133
0.5 mm.x.0.315 mm 85 84 84 Intake variations combined with differences in the
0.315 mm.x.0.1 mm 158 137 152 dietary chemical composition produced exaggerated
x,0.1 mm 370 378 407
reduc-Table 3
a Feed intake and growth according to dietary fibre level, in growing rabbits from weaning (28 days old) to slaughter (70 days old)
b
Diets A20 A16 A12 SEM P level
Weaning–42 days old
Daily feed intake (g) 84.8a 73.3b 64.1c 0.73 ,0.001
Daily weight gain (g) 43.3a 41.2ab 39.5b 0.49 0.010
Feed conversion ratio 1.97c 1.77b 1.65a 0.016 ,0.001
42–70 days old
Daily feed intake (g) 139.1a 126.3b 112.8c 1.44 ,0.001
Daily weight gain (g) 39.4 43.6 41.5 0.82 0.119
Feed conversion ratio 3.42c 2.88b 2.59a 0.020 ,0.001
Weaning–70 day old
Daily feed intake (g) 121.6a 108.3b 96.2c 1.18 ,0.001
Daily weight gain (g) 41.0 42.6 39.6 0.58 NS
Feed conversion ratio 2.89c 2.52b 2.28a 0.032 ,0.001
a
Means having a common letter did not differ significantly at level P50.05. Number of animals per diet5number of animal at weaning (n548) minus morbidity and mortality.
b
SEM: Standard error of the mean; NS5P.0.15
tion of dietary ADF (20 vs. 12%) led to a higher 3.2. Digestion in the whole tract and partition reduction in ADF intake (253%) for growing rabbits between small intestine and caeco-colic segment over the 28–70 day period, inversely the starch
intake increased from 13 to 28 g / d. The expected differences of digestibility for OM
Over the complete growth period, the mortality and energy in the whole digestive tract (TTAD,
rate remained relatively low (,10%) and was not Table 5) were observed according to fibre level
significantly affected by dietary treatment (Table 4), (21.6 point per % ADF). In parallel, crude protein
although the sanitary risk (mortality1morbidity) digestibility increased by 10% (P,0.001) as
ex-tended to increase (P50.11). Nevertheless from 42 pected from feed formulation (substitution of protein
to 70 days old there was a linear increase (P50.02) from alfalfa by those of soya and wheat), and
of morbidity when the dietary fibre level was re- growing rabbits thus consumed a similar quantity of duced. No mortality or morbidity was observed in digestible protein (13 g / d) among diets. Starch was
any adult rabbits. almost completely digested (mean 99.5%), although
a slight increase was obtained with reduction of the
Table 4
ratio ADF / starch. No significant change in fibre
Morbidity and mortality between weaning (day 28) and slaughter
digestibility was registered according to the dietary
(day 70), according to dietary fibre level
fibre level. The soft faeces production corresponded
Diets A20 A16 A12 P level
to almost 12% of the feed intake with the highest
Weaning to day42 supply in fibre (A20) and was significantly reduced
Morbidity (n) 7 6 5 NS
(225%) with the lowest supply of fibre (A12).
Mortality (n) 0 0 1 NE
For a dietary ADF reduction from 20 to 12%, the ileal digestibility (between mouth and ileal cannula)
Day42 to slaughter
Morbidity (n) 5a 9ab 16b 0.02 of OM increased from 38 to 61% (Table 6), while it
Mortality (n) 2 1 1 NE decreased from 27 to 17% in the caeco-colic segment
(between ileum and rectum). Crude protein ileal
Weaning to slaughter
digestibility improved by 10 units (57 vs. 67%) with
Morbidity (n) 12 15 21 0.12
fibre reduction, whereas caeco-rectal digestibility
Mortality (n) 2 1 2 NE
Total 14 16 23 0.11 remained at a low level (,14%) and was similar
among the diets. The mean ileal recovery (ileal
n: Number of rabbits (initial number per diet548); a,b: See
Table 5
a Total tract apparent digestibility (TTAD) and soft faeces production in adult rabbits, according to dietary fibre level
Diets A20 A16 A12 SEM P level
(n512) (n511) (n512)
TTAD coefficients (%)
Organic matter 64.7a 72.7b 78.2b 0.5 ,0.001
Crude protein (N36.25) 70.9a 76.6b 78.5b 0.8 ,0.001
NNCC 92.5a 95.8b 97.4b 0.4 ,0.001
Starch 99.2b 99.5a 99.7a 0.09 ,0.01
Energy 63.3a 71.4b 76.8c 0.5 ,0.001
NDF 41.8 43.8 42.9 0.9 NS
ADF 34.2 33.8 32.5 1.2 NS
Soft faeces (g DM / d) 14.5a 13.4a 10.8b 0.78 0.005
a
SEM: Standard error of the mean; n: Number of rabbits; a,b,c: See Table 3; NNCC: Non nitrogenous cellular content5OM2CP2NDF.
Table 6
a Ileal and caeco-rectal digestibility in adult rabbits, according to dietary fibre level
Diets A20 A16 A12 SEM P level
(n59) (n59) (n58)
Ileal digestibility coefficients (%)
Organic matter 37.6c 46.3b 61.1a 1.6 ,0.001
Crude protein (N36.25) 57.0b 62.4ab 66.5a 2.2 ,0.001
Starch 98.7a 97.1a 93.0b 0.7 ,0.001
NNCC 49.2a 64.6b 75.1c 1.9 ,0.001
NDF 22.9 19.1 28.6 2.9 NS
ADF 16.8 7.9 18.4 3.2 NS
Caeco-rectal digestibility coefficients (%)
Organic matter 26.8a 25.8a 17.0b 1.6 ,0.001
Crude protein (N36.25) 13.1 13.4 11.7 2.5 NS
Starch 0.5b 2.4b 6.7a 1.4 0.011
NNCC 43.2a 31.2b 22.3c 2.2 ,0.001
NDF 18.7 23.6 14.3 3.0 NS
ADF 17.2 24.7 14.9 3.5 NS
a
SEM, a,b,c: See Table 3.
NDF was lower (78.5%), and no significant varia- with the increase in dietary starch level
(corre-tions in ileal or caecal fibre digestibility (NDF or sponding to fibre level reduction). Similarly, in
ADF) were observed. growing rabbits, ileal starch concentration rose from
Ileal digestibility of starch was lowered by almost 0.9 to 2.6% with dietary starch level (Table 8). No 6 units with the reduction of the ADF / starch ratio in significant differences in ileal starch concentration the diet (inverse trend for faecal digestibility), but were noticed at 6 or 10 weeks of age among diets.
remained at a very high level (.93%). Starch However, a significantly lower starch level (1.9 vs.
concentration at the ileum was very low in adults 2.9%) was found for adult (.16 wk old) compared
(mean 1.3% DM, and less than 0.4% in faeces), but to 10 wk old rabbits, for the diet with the higher
3.3. Rate of passage in caeco-colic segment and The bacterial fibrolytic activity (BFA) in soft bacterial fibrolytic activity in adult rabbit faeces of adult rabbits was significantly reduced with the feed having the lowest fibre level (Fig. 1). The Although feed intake of adult rabbits was only pectinolytic activity was more particularly affected slightly reduced with the reduction of the fibre level (250%).
(28%, Table 7), there was a sharp increase in mean retention time (MRT) between ileum and rectum
3.4. Caecal fermentation pattern in the growing (138%), reaching 19 h for the lowest fibre level
rabbits (A12). Besides, the ileo-rectal minimal transit time
(TTm) was not affected by dietary treatments.
There-A significant interaction (P,0.05) between the fore, we estimated the retention in the caecum and
effect of the age (6 vs. 10 weeks old) and the effect proximal colon (difference between MRT and TTm)
of the diets was detected for the caecal VFA that was 10.4 and 15.2 h respectively for diets A20
concentration, therefore we present our results ac-and A12.
Table 7
Ileo-rectal rate of passage in adult rabbits, according to dietary fibre level reduction
a
Diets A20 A16 A12 SEM P level
(n59) (n510) (n59)
b
Feed intake (g / d kg LW) 39.2a 39.0a 35.9b 1.0 0.050
Ileo-rectal rate of passage
Mean retention time (MRT, h) 13.7a 15.0ab 19.0b 1.3 0.014
Minimal transit time (TTm, h) 3.3 3.1 3.8 0.05 NS
a
SEM, a,b: see Table 3. b
Intake during measurements (4 days).
Fig. 2. Caecal total VFA concentration (mmol / l, mean6sd), according to age and dietary fibre level.
cording to age and fibre level in Fig. 2. In 6 weeks with a change in the VFA molar proportion: increase
old rabbits (2 wk after weaning), the VFA level in butyrate compensated by a decrease in acetate.
decreased linearly and significantly (P,0.01) from A20 to A12. For instance, VFA level reached 72
mM / l for rabbits fed A20, compared to only 52 4. Discussion
mM / l for those fed A12. Conversely at 10 weeks of
age no significant effect of the dietary treatments was 4.1. Comprehensive approach of the rabbit
observed. Besides the VFA molar proportion evolved digestion
similarly with age according to the diets (no
signifi-cant interaction): the fermentation profile was char- Previous studies of digestion in the rabbit provide acterised by a higher butyrate and a lower acetate little quantitative information on the partition of the
proportion for 10 weeks old rabbits compared to 6 digestion from enzymes of the host (in the small
weeks old (Table 8). In addition, the caecal pool of intestine) or from bacteria (in the caeco-colic
seg-VFA almost doubled between 6 and 10 wk old. With ment). Furthermore, such measurements were never
the reduction of the fibre supply, we observed a correlated with other parameters such as rate of
linear reduction of the VFA pool (215%) associated passage or microbial activity. The present set of
Table 8
Volatile fatty acids molar proportions in the caecum, and starch concentration in the ileum of growing rabbits
a
mol / 100 mol Fibre level Age SEM P level
A20 A16 A12 6 wk 10 wk Diet Age Diet3Age
(n520) (n520) (n520) (n530) (n530)
Acetate 82.1b 81.3b 78.0a 82.5 78.4 0.56 ,0.001 ,0.001 NS
Propionate 4.01 4.43 4.38 3.86 4.72 0.18 NS ,0.001 NS
Butyrate 13.6b 13.8b 16.9a 13.1 16.4 0.56 ,0.001 ,0.001 NS
0.3b 0.34b 0.52a 0.36 0.41 0.04 ,0.01 NS NS
Caecal VFA
pool (mmol) 5.66b 5.11ab 4.44a 3.84 6.38 0.32 0.041 ,0.001 NS
Ileal Starch
(% DM) 0.9b 1.4b 2.9a 1.8 1.7 0.3 ,0.01 NS 0.14
a
experiments aimed to gather these various digestive criteria and animal performances to obtain a com-prehensive view of rabbit digestion in relation to dietary fibre level.
Compared to other monogastric animals, serious methodological problems were encountered in the measurement of the digestibility of nutrients anterior to the terminal ileum, as suggested here by the higher variability of these values compared to faecal digestibility results. Similar variability was previous-ly reported for rabbits (Gidenne, 1992; Merino and
˜
Carabano, 1992). This relatively high variability in ileal digestibility could be attributed to several factors, but particularly to the following points: the necessity of a supplementary measure (compared to other monogastric) that is a quantification of the soft faeces production, the impossibility to obtain a complete collection of the ileal flow (as for pigs), the smallness of ileal digesta sample that limits chemical analysis, and particularly the feeding system of rabbit (ad libitum) that implies circadian changes in feed intake (and in composition of digesta) and
differing feeding patterns between animals. How- Fig. 3. Partition of the digestion between small intestine and caeco-colic segment (in % of digestible nutrients, organic matter
ever, we observed reliable results for the partition of
or crude protein), according to dietary fibre level.
the digestion between small intestine and caeco-colic segment, showing that about two thirds of organic matter was digested before the caecum (Fig. 3).
Crude protein digestion in ranged from 80 to 90% in be active during their passage through the stomach the small intestine, as found previously by Gidenne and small intestine. This recycling may explain (at
(1992). least in part) that positive ileal digestibility was
The estimation of the digestibility of fibre before found for uronic acids (from 20 to 38%; Gidenne,
the caecum is more questionable and seemed here 1992). However, further investigations into fibre
slightly overestimated, as already observed by digestion in the pre-ileal tract (stomach, small intes-˜
Merino and Carabano (1992). We measured in the tine) are necessary to elucidate this phenomenon that
present study a high ileal recovery rate for ADF seemed specific to the rabbit among monogastric
(mean 87%), but if we consider that fibre degra- herbivores.
dation only occurred in the caeco-colic segment it The caecum is the major organ where microbial
should be close to 100%, as previously observed by activity takes place in rabbits. The caecal microbial
Gidenne and Ruckebusch (1989) and Gidenne population secretes enzymes that can hydrolyse the
(1992). Our results suggest that fibre digestion was main components of dietary fibre. In agreement with
as important before the caecum as after. However, two previous studies on rabbits (Marounek et al.,
we cannot exclude that some fibre degradation could 1995; Jehl et al., 1996), we found greater enzymatic
occur before the caeco-colic segment, since activity for degrading pectins and hemicelluloses
Marounek et al. (1995) found relatively high pec- than for degrading cellulose. These results reflect the tinolytic activities in the stomach of rabbits that faecal digestibility of the corresponding dietary fibre would originate from soft faeces consumption. This constituents in rabbits (Gidenne et al., 1998), and are recycling of pectinolytic enzymes causes us to also consistent with the smaller counts of cellulolytic
xylanolytic or pectinolytic bacteria (Boulahrouf et MJ / kg for diets containing 20–16–12% ADF).
al., 1991). Rabbits vary their energy intake according to dietary
The relationship between BFA and caecal fermen- digestible energy (DE) content (Lebas et al. 1982;
tation pattern has not previously been studied in the Partridge et al. 1989), but within moderate limits. rabbit. Our results suggest that BFA is related to For instance, the DE intake of the growing rabbits caecal VFA pool in finishing growing rabbits (10 slightly decreased for the lowest dietary fibre level
week old), since it decreased according to fibre compared to the two others (respectively 1280 vs.
supply. Conversely no clear relation between the 1210 kJ / d over the period 28–70 days), thus explain-fermentation pattern (VFA level or molar proportion) ing the lower weight gain during the postweaning
and BFA was found. period.
It is particularly of interest to evaluate the flow of The health status of our growing rabbits was starch to the terminal ileum in growing rabbits, as an moderately affected by the reduction of the dietary overflow of starch in the caecum may be responsible fibre supply, except an increase of morbidity during
for microbial imbalance and thus for digestive the finishing fattening period. However, the animals
troubles (Cheeke and Patton, 1980). However, direct were kept in individual cages thus reducing the
measurement of ileal flow is only possible in an possibility of interindividual contamination and
ileum-cannulated adult animal. Nevertheless, the therefore the risk of digestive troubles. In addition, to combination of a quantitative approach to ileal be convincing, studies of rabbit nutritional pathology digestion in the adult with a qualitative study of ileal should involve several experimental locations and content in growing animals allowed us to estimate over 300 rabbits per dietary treatment, as achieved the ileal flow of nutrients in growing animals. We recently by Perez et al. (1996).
hypothesised that the ileal flow of dry matter in Digestion of OM or energy before the caecum was
finishing growing rabbits (6–10 week old) can be more affected by the reduction of the fibre than
estimated from that measured in the adult, according digestion in the whole tract. Consequently, there was to the relevant feed intake. Thus, we calculated that an important change in partition of the OM digestion
ileal flow of starch in finishing growing rabbits between enzymatic and fermentative processes (Fig.
would be very low, ranging from 0.7 to 1.8 g / d 3). Conversely, the partition of the digestion of
respectively for the highest and lowest ADF / starch protein was not greatly affected, although the level ratio in our experimental diets. Therefore it seems of digestibility varied among diets. We reported a
unlikely that overflow of starch into the caecum large increase in NNCC ileal digestibility with
caused the digestive trouble observed here for grow- decreasing level of fibre, while NNCC digestibility ing rabbits. Besides, we found here a low level of decreased in the caeco-colic segment. Since starch
ileal starch (0.9–2.9% DM) compared to results of was almost totally degraded before the caecum
Blas et al. (1994) ranging from 3 to 7% at the same whatever the starch content, most of this effect was age, but using maize starch that is less fully digested probably related to differences in pectin digestion.
in the rabbit (Blas and Gidenne, 1998). Conse- Fibre digestibility was not greatly affected by the
quently, a possible effect of an overflow of starch reduction of level of DF, while the quantity of fibre
into the caecum should not be excluded when low- degraded decreased (combination of a lower feed
quality starch is given, or in rabbits around weaning intake and of a lower dietary fibre level). Contrary to
which have a low secretion of pancreatic amylase. Bellier and Gidenne (1996), two weeks after
wean-ing we registered a linear decrease in caecal VFA level according to the decrease in fibre supply,
4.2. Impact of dietary fibre level whereas, no changes in the caecal VFA were found
for finishing rabbits, as previously reported
˜
ratio decreased (Gidenne et al., 1991b; Bellier and rabbit remains difficult, particularly to quantify
pre-Gidenne, 1996). cisely the flow of nutrients entering the caecum.
We can suppose that the quantity of low digestible Further studies are necessary in this area, particularly fibre (such as cellulose) entering the caecum is not a to reduce inter-individual variability of the measure-limiting factor for the fermentation processes, proba- ments. Similarly, the quantitative approach to micro-bly because the digesta retention time in the caecum bial activity needs to be improved. The present study is too short to produce a significant hydrolyses. In confirmed the validity of the bacterial fibrolytic return, caecal retention time seems sufficiently long activity measurement that should be further studied, to allow substantial degradation of easily digestible particularly in relation to the development of the
fibre fractions such as pectins or hemicelluloses. caeco-colic segment.
Furthermore, the BFA decreased with the reduction The nutritional impact of dietary fibre level for the
of the fibre supply particularly for pectinolytic growing rabbit was now better understood (Fig. 4),
activities (240%), although the retention time in the but it should be completed with studies around the caecum increased. Therefore, a reduction of the flow weaning period when digestive ability is developing.
of easily digestible fibre would limit the caecal Other comprehensive studies should be performed to
fermentation, which would explain the reduction in determine the effects of the quality of cell wall, as
NNCC digestibility in the caeco-colic segment this will vary greatly across the wide range of
agro-(mainly due to pectins). industrial by-products used in rabbit feeding.
5. Conclusion Acknowledgements
´
The study of digestion in the small intestine of the The authors thank Muriel Segura, Carole Beranger
Gidenne, T., 1992. Effect of fibre level, particle size and
adapta-´
and Andre Lapanouse (Station de Recherches
tion period on digestibility and rate of passage as measured at
Cunicoles, INRA, Toulouse) for their technical
assis-the ileum and in assis-the faeces in assis-the adult rabbit. Br. J. Nutr. 67,
tance. The authors thank Dr F. Enjalbert and Mrs 133–146.
Nico for their help in marker analysis (National Gidenne, T., 1994. Effets d’une reduction de la teneur en fibres´ Veterinary Highschool of Toulouse, Feed labora- alimentaires sur le transit digestif du lapin. Comparaison et
` ´ ´
validation de modeles d’ajustement des cinetiques d’excretion
tory), and to Dr R.B.N. Kay (Scotland) for his
´
fecale des marqueurs. Reprod. Nutr. Dev. 34, 295–306.
helpful advice in preparing the manuscript. This
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caecotrophie chez le lapin en croissance: variations en
fonc-the frame of a research cooperation program between tions de l’age. Ann. Zootech. 36, 225–236.ˆ
Portugal and France (ICCTI–French Embassy), and Gidenne, T., Ruckebusch, Y., 1989. Flow and rate of passage by a grant from FCG (Foundation Calloust Gulben- studies at the ileal level in the rabbit. Reprod. Nutr. Dev. 29,
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