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Energy balance of laying hens selected on

residual food consumption
J.F. GABARROU , P.A. GERAERT , N. FRANCOIS , S. GUILLAUMIN , M.
PICARD & A. BORDAS
Published online: 28 Jun 2010.

To cite this article: J.F. GABARROU , P.A. GERAERT , N. FRANCOIS , S. GUILLAUMIN , M. PICARD & A.
BORDAS (1998) Energy balance of laying hens selected on residual food consumption, British Poultry
Science, 39:1, 79-89, DOI: 10.1080/00071669889439

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 British Poultry Science (1998) 39: 79–89

Energy balance of laying hens selected on residual food

consumption
J. F. GABARROU, P. A. GERAERT, N. FRANÇOIS, S. GUILLAUMIN, M. PICARD AND
A. BORDAS1
Station de Recherches Avicoles, INRA, Nouzilly and Laboratoire de Génétique Factorielle, INRA, Jouy-en-Josas, France

Abstract 1. Energy balance of adult hens divergently selected for high (R 1 ) or low (R 2 ) residual food
consumption was investigated using indirect calorimetry. Three experiments were conducted: feeding
behaviour of individual hens, hens having free access to food or fasting and hens tube-fed at 70, 100 or
130% of the control intake of both lines.
2. R 1 hens ate signiŽ cantly more than R 2 ( 1 48%). This difference was maximum at the onset of the
light ( 1 120%) and not signiŽ cant during the rest of the light period. Although both lines spent the same
total time eating, R 1 hens exhibited more frequent but shorter meals than R 2 ones, suggesting a higher
feeding activity in R 1 hens.
3. True metabolisable energy (TME) intake was 28% greater in R 1 than in R 2 birds. Basal heat
production did not differ signiŽ cantly between genotypes. Heat increment of feeding (HI) or diet-induced
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thermogenesis was signiŽ cantly enhanced in R 1 birds: 1 23·9 vs 13·7 kJ/100 kJ TME intake in R 2 .
4. When tube-fed and placed in darkness, restricted-fed R 1 hens had the same HI as R 2 birds. When
fed at 100% and 130% of control intake, R 1 hens demonstrated a regulatory thermogenesis, which
allowed them to dissipate the excess of energy ingested compared to R 2 hens.
5. No signiŽ cant modiŽ cation was observed in plasma triglyceride, phospholipid, uric acid, glucose or
insulin concentrations between lines, suggestive of the use of similar thermogenic pathways. While plasma
triiodothyronine (T3) concentrations did not differ between genotypes, plasma thyroxine (T4) appeared
higher in unfed R 1 birds and equal in fed conditions in both lines.
6. A regulatory part of HI allowed R 1 hens to get rid of their excessive energy intake. An increased
turnover of lipids could be involved.

INTRODUCTION partly through increased zero activity heat pro-

In laying hens, food accounts for 60% to 70% of
egg production costs. Therefore, the Ž rst aim of the
breeder is to improve food efŽ ciency, that is egg
mass to food consumption ratio. Egg mass, body
weight and body weight changes are the most
important traits involved in variation of food con-
sumption (Fairfull and Chambers, 1984). These
traits can be used to predict food intake from
multiple linear regression (Byerly et al., 1980). Re-
sidual food consumption (RFC), deŽ ned as the
difference between observed and predicted food
consumption, is introduced in order to study the
sources of variations of food consumption not
taken into account by the regression (Bordas and
Mérat, 1981; Bordas and Mérat, 1984; Katle et al.,
1984; Luiting, 1990).
Using indirect calorimetry, Luiting (1991)
compared 6 high RFC and 6 low RFC White
Leghorn hens. She demonstrated that high RFC
hens produced more heat, partly through increased
physical activity expenditure: 1 30% to 50% and
duction: 1 35% to 50% (Luiting and Urff, 1991). A
higher heat increment of feeding in high RFC hens
was suggested. RFC heritability was high: between
0·42 and 0·62 in White Leghorn hens (Luiting and
Urff, 1991; Sabri et al., 1991; Katle and Kolstad,
1991; Schulman et al., 1994). However in the same
genotype, Wing and Nordskog (1982) found a
lower heritability in White Leghorn hens than
observed in Rhode Island Red hens: between 0·21
and 0·28 (Bentsen, 1983; Bordas et al., 1992).
Selection of efŽ cient hens with low RFC is thus
valuable.
Since 1976, from a Rhode Island Red popu-
lation, 2 divergent lines have been selected for high
(R 1 ) or low (R 2 ) RFC (Bordas and Mérat, 1984;
Bordas et al., 1992). In 1989, RFC differed by 3
phenotypic standard deviations between lines (Bor-
das et al., 1992). Geraert et al. (1991) observed a
difference in fed heat production in cockerels, with-
out a signiŽ cant difference in basal metabolic rate.
Moreover, a signiŽ cant difference was measured in

Correspondence to: J. F. Gabarrou,Station de Recherches Avicoles, Institut National de la Recherche Agronomique,37380 Nouzilly,France.
Accepted for publication 23rd May 1997
0007-1668 /98/010079-1 1 $7.00 Ó 1998, British Poultry Science Ltd
 80 J. F. GABARROU ET AL.
heat increment of food (84%) (Geraert et al., 1992).
Unlike males, hens have the ability to store an
excess of energy through egg lipid or body fat.
Large differences in energy intake between R 1
and R 2 hens might then be balanced by changes
either in egg energy, fat deposition or heat pro-
duction.
The present study was, therefore, performed
to investigate the food intake pattern and energy
balance of R 1 and R 2 laying hens. To deter-
mine the existence of a regulatory thermogenesis,
hens were tube-fed at different energy intakes.
Biological and endocrine variables were measured
in order to understand further the changes in
energy metabolism between lines.
MATERIALS AND METHODS
Animals and diets
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A total of 36 laying hens, 18 from each line, were
chosen from the 17th generation of the R 1 and
R 2 experimental lines (Bordas et al., 1992). When
18 weeks old, hens were individually housed and
fed on a complete diet containing 11·73 MJ ME/
kg and 178 g crude protein per kg. RFC was
estimated between 32 and 36 weeks of age. Hens of
37 to 45 weeks of age were used for the present
study.
Experiment 1
Food intake patterns of 8 R 1 and 8 R 2 laying
hens (RFC 5 1 10·2 and 2 10·0 g/d respectively)
were measured as described by Picard et al. (1992).
Feeders were weighed (to 6 0·01 g) 6 times per s.
Hens were adapted for 2 weeks to the experimental
device and food intake patterns were recorded
during a 24 h period. Eating was deŽ ned as a
period of time ( 6 0·1 s) during which the feeder
weight  uctuated. The amount of food consumed
during an access to the feeder was measured by
difference between the weight of the feeders before
and after a  uctuation period. A meal was deŽ ned
as a period of continuous eating not interrupted by
more than 120 s (Savory, 1979).
Experiment 2
Five hens with extreme RFC ( 1 18·4 and
2 11·9 g/day for the R 1 and the R 2 line re-
spectively) of both lines were transferred into indi-
vidual respiratory chambers (Geraert, 1990) to
measure energy balance. They were maintained at
20°C, on a 14L:10D lighting programme, starting
at 03·00 h. They had free access to food and water
for 4 d and were then fasted for 2 d. The Ž rst day
of each period (d 1 and 5) was considered as an
adaptation period and was not included in the
calculations. Heat production, respiratory quotient,
food and water intakes were measured daily. Ex-
creta and eggs were collected daily, weighed and
freeze-dried before analysis. Endogenous energy
and protein losses, and fasted heat production were
determined during the second day of fasting (d 6).
True metabolisable energy intake (TMEi) was cal-
culated, taking endogenous energy losses into ac-
count.
At the end of each period, 4 ml blood were
collected from the wing vein using a heparinised
syringe. Plasma was then separated and stored at
2 20°C until analysis. To determine the main fuel
for themogenesis in the 2 lines, both plasma glu-
cose and triglyceride concentration were deter-
mined. Phospholipid concentration was measured
to evaluate lipid transport, and uric acid to esti-
mate amino acid catabolism. Plasma insulin con-
centration was determined to give further
information relevant to the glucose-insulin balance
of the 2 lines. Plasma triiodothyronine and thyrox-
ine concentrations were measured to investigate
their relationship with thermogenesis.
Experiment 3
Five hens of each line (RFC 5 1 9·1 and
2 10·1 g/d in the R 1 and the R 2 line respect-
ively) were reared in the same conditions as above.
The same diet (experiment 2) was ground (diam-
eter , 0·5 m m) and mixed with water (50:50, w:w).
Hens were fed by crop intubation. After an adap-
tation to tube-feeding for 3 d, all 5 hens received
successively 70%, 100% and 130% of their individ-
ual ad libitum food intake. Hens were tube-fed twice
a day, at 10·00 and at 17·00 h. They had free
access to water. Heat production and respiratory
quotient were continuously recorded except for
15 min feeding time.
Heat production measurement
Oxygen consumption and carbon dioxide pro-
duction were measured using an automated indi-
rect multi-calorimetry system (Geraert, 1990). Heat
production (HP) was calculated as:
HP(kJ) 5 16·18 O2 (litre) 1 5·02 CO2 (litre) (Romijn
and Lokhorst, 1961). HP was measured continu-
ously (every 12 min) during 23 h per treatment (1 h
was necessary for maintenance and calibration).
Heat increment of feeding (HI) was estimated from
the difference between fasted and fed heat pro-
duction.
Analysis
Dry matter contents of food, droppings and eggs
were determined by oven-drying for 4 h at 103°C,
protein contents by the macro-Kjeldahl method
(N 3 6·25), gross energy by an isoperibole bomb
calorimeter (IKA-Calorimeter C700T) and egg
 ENERGY BALANCE AND RFC 81
Table 1. Food intake pattern in R 1 and R 2 laying hens (mean 6 SEM for 8 hens, experiment 1)

Line R1 R2 T1

03·00 to 09·00 h
Food intake (g/h) 8·5 6 0·9 3·9 6 0·4 ***
Time spent eating (%) 26·4 6 5·1 20·7 6 3·8 NS
Number of food access periods2 56 6 13 20 6 3 **
09·00 to 15·00 h
Food intake (g/h) 8·2 6 0·5 6·6 6 0·6 P5 0·06
Time spent eating (%) 28·0 6 4·6 28·0 6 4·1 NS
Number of food access periods2 32 6 4 20 6 3 *
15·00 to 17·00 h
Food intake (g/h) 14·9 6 1·6 12·0 6 1·6 NS
Time spent eating (%) 40·4 6 7·6 38·7 6 4·7 NS
Number of food access periods2 15 6 3 76 1 *
1
NS not signiŽ cant; * P , 0·05, ** P , 0·01, *** P , 0·001 according to two-tailed t
test. 2Food access is deŽ ned as eating period not interrupted by more than 2 min.

Table 2. Performance of the R 1 and R 2 hens (mean 6 SEM for 5 hens, experiment 2)

Line R1 R2 T1

Body weight (g) 2030 6 143 1906 6 60 NS

Consumption
Food intake (g/d) 126 6 12 85 6 9 **
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Water intake when fed (g/d) 281 6 27 146 6 9 **

Water intake when fasted (g/d) 97 6 16 96 6 11 NS
Water/food 2·27 6 0·23 2·00 6 0·18 NS
Fed—fasted water/food 1·47 6 0·14 0·76 6 0·19 *
Residual Food Consumption (g/day) 18·4 6 2·4 2 11·9 6 1·3 ***
Egg production
Total egg mass (g/d) 39·6 6 1·2 39·2 6 2·4 NS
1
NS not signiŽ cant; * P , 0·05, ** P , 0·01, *** P , 0·001 according to two-tailed t test.

lipid contents according to Folch & Loane-Stacey RESULTS

(1957). Plasma glucose was determined with a
glucose analyser (Beckman Instruments Model 2,
Palo Alto, CA). Plasma triglycerides, phospholipids
and non-esteriŽ ed fatty acids were measured by
enzymatic methods (Fossati and Prencipe, 1982;
Takayama et al., 1977, Okabe et al., 1980) using kits
provided by BioMerieux SA (Charbonnières-les-
Bains, France). Plasma uric acid was measured
according to Fossati et al. (1980) using kits provided
by Sigma Diagnostics (St Louis, USA). Plasma
triiodothyronine (T3) and thyroxine (T4) were de-
termined by radioimmunoassay using a commer-
cial kit (CIS-ORIS Industries, Gif-sur-Yvette,
France). Plasma insulin was measured by radio-im-
munoassay using a guinea pig antiporcine insulin
serum (Ab 27–6, a gift of G. Rosselin, Hôpital
Saint-Antoine, Paris) with chicken insulin as stan-
dard (Simon et al., 1974).
Statistical analysis
Data are given as means 6 SEM. When comparing
the 2 lines, statistical signiŽ cance between the
means was examined by a two-tailed t test P , 0·05
was considered signiŽ cant. To compare 3 means of
the same line for different tube-feeding inputs (ex-
periment 3) 3 paired-sample t tests were per-
formed. To take into account the fact that that a
value was compared twice, only t . 3·56 was con-
sidered signiŽ cant (Wilkinson, 1975).
Experiment 1
At the onset of light (03·00 h), the rate of food
intake (g/h) was signiŽ cantly higher in R 1 than in
R2 hens: 1 118% between 03·00 and 09·00 h
(Table 1). This divergence decreased during the
day to become not signiŽ cant between 15·00 and
17·00 h ( 1 24%). The rate of food consumption
increased during the day in both lines, particularly
in the R 2 one. Time spent eating was not
signiŽ cantly different between lines at any moment
of the day. The number of meals (deŽ ned as food
accesses not interrupted for more than 2 min) re-
mained constant during the day in the R 2 line at
about 5 meals per h while it decreased from 14 to
8 meals per hour in the R 1 line.
Experiment 2
R1 hens ate signiŽ cantly more than the R 2
ones: 1 48% for similar body weight and egg pro-
duction (Table 2). Water intake was also greater in
the R 1 line ( 1 92%) but the water/food intake
ratio did not differ between lines. When expressed
as the difference between fed and fasted conditions,
water intake as a proportion of food consumed
averaged 1·47 and 0·76 g/g in the R 1 and R 2
lines respectively. Chemical composition of the egg
(not given in the Table) of R 1 and R 2 hens was
similar: 27·8 g dry matter, 13·4 g lipid, 10·8 g pro-
 82 J. F. GABARROU ET AL.

Table 3. Energy balance of R 1 and R 2 laying hens (mean 6 SEM for 5 hens ;
kJ/kg 0.75.d, experiment 2)

Line R1 R2 T1

TME / GE2 0·743 6 0·031 0·772 6 0·026 NS

TME intake 823 6 73 641 6 64 **
Fed heat production 440 6 22 334 6 18 **
Fasted heat production 244 6 25 245 6 7 NS
Heat increment2 (HI) 197 6 32 89 6 19 **
Total retained energy 383 6 59 306 6 55 NS
as protein 144 6 34 127 6 14 NS
as fat 239 6 37 180 6 43 NS
HI (% TME) 23·9 6 2·9 13·7 6 2·2 **
RQ2Fed 0·94 6 0·04 0·93 6 0·04 NS
RQ2Fasted 0·72 6 0·01 0·72 6 0·01 NS
1
NS not signiŽ cant; ** : P , 0·01 according to two-tailed t test. 2TME/GE : true
metabolisable energy/gross energy ratio ; HI measured as the difference between
fed and fasted HP ; RQ : respiratory quotient.

Table4. Biological and endocrinological plasma concentrations in R 1 and R 2 fed and fasted
laying hens (mean 6 SEM for 5 hens, experiment 1)

Line R1 R2 T1
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Triglycerides (g/l) Fed 13·1 6 1·7 12·9 6 3·0 NS

Fasted 2·3 6 0·6 3·9 6 1·8 NS
Phospholipids (g/l) Fed 6·2 6 0·6 6·1 6 0·9 NS
Fasted 1·9 6 0·2 2·5 6 0·7 NS
Glucose (g/l) Fed 2·0 6 0·1 2·0 6 0·1 NS
Fasted 1·9 6 0·0 1·9 6 0·0 NS
Uric acid (mg/l) Fed 35·5 6 3·9 39·3 6 4·4 NS
Fasted 15·4 6 3·8 15·9 6 2·4 NS
T3 (nmol/l) Fed 1·94 6 0·11 1·73 6 0·20 NS
Fasted 0·79 6 0·14 0·94 6 0·17 NS
T4 (nmol/l) Fed 20·2 6 1·3 21·4 6 1·4 NS
Fasted 20·5 6 1·6 16·5 6 1·0 **
Insulin (m U/ml) Fed 26·7 6 6·0 27·7 6 5·1 NS
Fasted 22·5 6 3·4 21·4 6 4·0 NS
1
NS not signiŽ cant; ** P , 0·01 according to 2-tailed t test.

tein, 3·6 g ash and 696 kJ gross energy per 100 g of
egg.
Energy metabolisability was not signiŽ cantly
different between lines; the ratio true metabolisable
energy / gross energy (TME/GE, Table 3) was
0·74 and 0·77 in R 1 and R 2 birds respectively.
TME intake was thus 28% greater in R 1 birds.
Fasted HP did not differ signiŽ cantly between
genotypes. Conversely, fed HP was 32% greater in
the R 1 birds. Heat increment of feeding (HI),
calculated as the difference between fed and fasted
HP, was signiŽ cantly greater in the R 1 line, by
1 108 kJ/kg0.75.d. HI expressed per 100 kJ TME
(%) averaged 23·9 and 13·7% for the R 1 and
R 2 genotypes respectively. No signiŽ cant differ-
ence in retained energy either as protein or fat was
observed between lines. Moreover, respiratory
quotient either fed (0·94) or fasted (0·72) did not
differ between genotypes (Table 3).
Food and water intake patterns are presented
in Figures 1a and 1b. R 1 hens consumed more
food at the onset of light while R 2 birds ate more
just before the dark period. Water intake was
higher in R 1 than in R 2 hens, particularly from
10·00 to 17·00 h. During the dark period, food and
water consumptions remained very low. Plasma
glucose, triglyceride, phospholipid, uric acid, T3
and insulin concentrations were similar in both
lines, whether fed or fasted. Plasma T4 concen-
tration was greater in R 1 than in R 2 fasted hens
and similar when fed (Table 4).
Experiment 3
HP was measured after tube-feeding at 70%, 100%
and 130% of ad libitum food intake (Table 5).
Genotypes were thus compared at different (low
70%, normal 100%, high 130%) and similar (low,
R1 70% vs R 2 100% or high, R 1 100% vs
R 2 130%) energy intakes. HP, HI and total re-
tained energy (RE) were signiŽ cantly greater in the
R 1 hens than in the R 2 ones, irrespective of the
energy intake. Moreover, HP and HI increased
with energy intake in R 1 birds while there was no
change in R 2 birds. RE increased with TME
intake in both genotypes. When compared at the
same energy intake, whether low (600 kJ) or high
(800 kJ), R 1 hens exhibited higher heat pro-
duction and heat increment than R 2 ones. At the
low energy intake, retained energy was lower in the
R 1 hens than in the R 2 hens. However, there
 ENERGY BALANCE AND RFC 83
(a)
25

Light period Dark period Light period

20 *
*
Food intake (g/h)

15 R+ *
R±
*
10
*
*
5

0
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time
(b)
50
* Light period Dark period Light period
*
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40
Water intake (g/h)

* * * *
30 R+
R± *

20 *

10
*

0
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time

Figure 1. Hourly food (Figure 1a) and water (Figure 1b) intakes of R 1 and R 2 laying hens (g/h; n 5 5, experiment 2), * P , 0·05 according to two-tailed
t test.

was no difference in retained energy between lines There was no difference in respiratory quo-
at the high energy intake. tient (RQ) between lines, irrespective of the tube-
Tube-feeding was done in 2 meals. Irrespective feeding input (Figure 3). When compared at the
of the period of time considered, R 1 birds same energy intake, RQ did not differ between
demonstrated greater heat production and heat lines except during the dark period. Indeed, during
increment than R 2 ones (Table 6 and Figure 2). that period, RQ appeared signiŽ cantly lower in
When comparing lines at the same energy intake R 1 when restricted to the same energy intake as
(either low or high) during the light period (10·00 the R 2 hens: 0·98 vs 1·02. Variation of RQ with
to 17·00 h and 03·00 to 09·00 h), R 1 hens exhib- time might represent rates of lipogenesis (positive
ited greater HP and HI than R 2 ones. During the slope) or lipolysis (negative slope). Regressions were
dark period, for the same low energy intake, R 1 linear during 2 lipogenic (10·00 to 13·00 h and
and R 2 hens exhibited no differences in HP or 17·00 to 22·00 h) and 2 lipolytic (14·00 to 17·00 h
HI. For the same high energy intake, R 1 hens and 03·00 to 07·00 h) periods after tube-feeding
exhibited a greater HI and HP than R 2 hens. (Table 7). Regression slopes appeared greater in
During the light period following the Ž rst meal R 1 than in R 2 hens whatever the period and
(10·00 to 17·00 h) no signiŽ cant effect of energy tube-feeding dose. For the same low energy intake,
intake upon HI was observed. After the second R 1 and R 2 birds exhibited similar slopes, while
meal (17·00 to 03·00 h and 03·00 to 09·00 h), HI for the same high energy intake, slopes were higher
increased with TME intake in the R 1 . Although in R 1 than in R 2 .
HI decreased with food restriction in the R 2 line, Regression equations between HP and TME
high intake did not enhance HI in this line. intake were calculated in R 1 and R 2 ad libitum
 84 J. F. GABARROU ET AL.

Table 5. Energy balance of R 1 and R 2 laying hens tube-fed with 70%, 100% or 130%
of their ad libitum food intake1 (kJ/kg0.75.d; mean 6 SEM for 5 hens; experiment 3)
Tube-feeding input (%) R1 R2 D1 D2
TME intake
70 575 a 6 35 417a 6 13 ** NS
100 829b 6 56 606 b 6 14 ** NS
130 1072 c 6 73 790 c 6 20 **
Heat Production (HP)
70 362 a 6 22 284a 6 36 * *
100 397b 6 24 309a 6 6 ** *
130 430c 6 32 316a 6 15 **
Heat increment (HI)
70 163 a 6 20 69a 6 30 * *
100 198b 6 21 95a 6 17 ** *
130 232c 6 31 101a 6 10 **
Total retained energy
70 214 a 6 15 133a 6 34 P5 0·06 *
100 417b 6 34 296 b 6 12 ** NS
130 641c 6 47 474 c 6 17 *
HI (% TME)
70 28·1a 6 2·1 16·6a 6 2·9 * ***
100 24·2a 6 1·0 15·8a 6 2·9 * ***
130 21·5b 6 1·7 12·8a 6 1·4 **
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1
Values in the same column not sharing the same superscript are signiŽ cantly
different (P , 0·05) according to a paired sample t test between hens of the same
line.
D1 5 difference between lines at the same tube-feeding input; D2 5 differences
between lines for the same energy intake. R 1 hens tube-fed with 70% compared
with R 2 hens tube-fed with 100% of ad libitum feed intake and R 1 hens tube-fed
with 100% compared with R 2 hens tube-fed with 130% of ad libitum feed intake
according to a two-tailed t test. NS not signiŽ cant ; * P , 0·05 , ** P , 0·01 , ***
P , 0·001.

(experiment 2) or tube-fed (experiment 3) hens nique. Moreover, this coefŽ cient was slightly lower
(Table 8). There was no difference between lines in under tube-feeding conditions than with ad libitum
the heat production extrapolated to zero food in- feeding in the R 1 line: 0·264 vs 0·216.
take (constant B) irrespective of the feeding tech-
nique. The slope of the equations (A) representing
heat increment of food in kJ per kJ TME was DISCUSSION
higher in the R 1 line whatever the feeding tech-
Feeding rate was modiŽ ed by selection on
RFC
Table6. Heat increment of feeding1 of R 1 and R 2 laying hens tube-fed with Divergent selection on RFC resulted in a large
70%, 100% or 130% of their ad libitum food intake (kJ/kg0.75.d; mean 6 SEM difference in food intake: 41 g/d between R 1 and
for 5 hens; experiment 3) R 2 hens without a difference in body weight and
Tube-feeding input (%) R1 R2 egg production. The difference in food intake was
greater than that reported by Bordas et al. (1992) in
10·00 to 17·00 h (light period, after tube-feeding) males and females after 17 generations of selection:
70 215a 6 39 67a 6 29 * **
100 207a 6 10 89a 6 16 *** 20% to 40%. Such a divergence could result from
***
130 232a 6 31 86a 6 17 ** the extreme RFC hens used for the energy balance
17·00 to 03·00 h (dark period, after tube-feeding) measurements. The similar rates of food intake
70 120a 6 18 37a 6 21 * NS observed in the 2 lines might be explained by
100 180 6 25
b
92 b 6 17 *
130 211 c 6 22 99 b 6 12 **
* speciŽ c nutrient requirements for egg synthesis
(Savory, 1980). On the other hand, the divergence
03·00 to 09·00 h (light period)
70 161a 6 20 36a 6 23 ** in food intake, maximum at the onset of light,
**
100 223 b 6 25 93ab 6 16 ** ** could also suggest a more negative balance in the
130 277 c 6 32 113 b 6 11 ** R 1 birds after their overnight fast because of their
1
Values in the same column and the same period not sharing the same similar food intakes before the dark period and to
superscript are signiŽ cantly different (P , 0·05) according to a paired an increased energy expenditure. To explain the
sample Student’s t-test between hens of the same line. difference in food and water intake patterns it
D1 5 difference between lines at the same tube-feeding input;
D2 5 differences between lines for the same energy intake : R 1 hens could also be hypothesised that birds need water a
tube-fed with 70% compared with R 2 hens tube-fed with 100% of few hours after eating to eliminate HI. Indeed,
ad libitum feed intake and R 1 hens tube-fed with 100% compared taking into account the fasting water intake, the
with R 2 hens tube-fed with 130% of ad libitum feed intake according
to a two-tailed t test. water:food intake ratio doubled (94%) in the R 1
NS not signiŽ cant , * P , 0·05 , ** P , 0·01 , *** P , 0·001. line. Bordas et al. (1992) observed that shank and
 ENERGY BALANCE AND RFC 85
(a)
500

450 Dark period

Heat increment (kJ/kg0 75.min)

400
.

350
130%
100%
300 70%
ad libitum

250 Light period Light period

200
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time

(b)
500
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130%
100%
450 70%
Heat increment (kJ/kg0 75.min)

ad libitum Dark period Light period

400
.

350

300

250 Light period

200
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time

Figure 2. Effect of tube-feeding input (70%, 100% or 130% of ad libitum intake) on heat increment in R 1 hens (Figure 2a) and R 2 hens (Figure 2b)
(kJ/kg0.75.min, n 5 5, experiment 3).

wattle lengths were increased in the R 1 in both enhanced in R 1 hens, by 32%, while Luiting
sexes, reinforcing the idea of greater needs for heat (1991) found increases of 30% in one experiment
elimination. Because of the absence of signiŽ cant and 12% in another experiment, and Katle (1991)
difference in heat production or water intake be- 23% after only 3 generations of selection. Such
tween genotypes when fasted, these needs for heat results were similar to the 1 29% obtained with
loss must be related to the increased food intake or R 1 and R 2 males (Geraert et al., 1991). More-
activity. over, for 100 kJ TME ingested, R 1 hens dissipate
24 kJ vs 14 kJ in R 2 ones, that is twice as much in
the R 1 as in the R 2 line. The difference be-
R 1 shows greater heat increment of feed- tween lines in HP thus resulted from an increased
ing than R 2 hens HI allowing R 1 hens to get rid of their excessive
As previously reported in males from the same energy intake.
experimental lines (Geraert et al., 1991) or in fe-
males from a White Leghorn selection (Katle et al.,
1984; Luiting and Urff, 1991), both lines had
Evidence of regulatory thermogenesis in
similar digestive abilities. The divergence in food
R 1 hens
intake was thus also a divergence in TME intake. Tube-feeding equalises energy intake and drasti-
As in cockerels, the basal metabolic rate, estimated cally reduces activity-related HP in fowls
from fasted HP, did not differ between lines (Ger- (MacLeod, 1991). By using the dark period mea-
aert et al., 1991). Heat production was signiŽ cantly surements, where physical activity was at a mini-
 86 J. F. GABARROU ET AL.

(a)
1.10
Light period Light period
1.05

1.00

0.95

0.90
130%
100%
0.85 70%
ad libitum Dark period

0.80
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time

(b)
1.10
Light period Light period
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1.05

1.00

0.95

0.90
130%
100%
0.85 70%
ad libitum Dark period

0.80
10.00 12.00 14.00 16.00 18.00 20.00 22.00 00.00 02.00 04.00 06.00 08.00
Time

Figure 3. Effect of tube-feeding input (70%, 100% or 130% of ad libitum intake) on respiratory quotient in R 1 (Figure 3a) hens and R 2 (Figure 3b) hens
(n 5 5, experiment 3).

mum, no differences in HP or HI were observed
between lines fed at the same low energy intake
when restricted-fed, R 1 hens exhibited the same
HI as R 2 hens. When given energy in excess
compared to R 2 (100% and 130%), the R 1
demonstrated a regulatory thermogenesis which
led to dissipation of the excess energy intake. Such
regulatory thermogenesis was previously observed
in cafeteria-fed rats (Rothwell and Stock, 1979). In
this hyperphagic model, the increase in energy
intake resulting from highly palatable diets was
partially eliminated by enhanced thermogenesis
through b -adrenergic stimulation of the brown
adipose tissue (Rothwell and Stock, 1979).
Activity-related HP and heat increment of
feeding
HI represents both activity-related HP and diet-
induced thermogenesis. Katle et al. (1984) indicated
that high RFC hens were more active and exhib-
ited greater stress than low RFC hens. Moreover,
using a Doppler-radar system Luiting (1991) found
that 30% to 50% of the divergence in HP between
lines could be accounted for by changes in physical
activity. In experiment 3, hens were fed by crop
intubation which reduces feeding activity
(MacLeod, 1991). The decrease observed in the
slope (kJ HP/kJ TME) of regressions (Table 8)
obtained with hens fed ad libitum or by crop intuba-
tion could be accounted for by reduced activity
from tube-feeding. This decrease in the slope sug-
gests that 18% of the heat increment of feeding
could be related to feeding activity in the R 1 line
and only 4% in the R 2 line. Whereas both lines
spent the same amount of time eating, R 1 hens
exhibited more frequent but shorter meals than
R 2 ones. R 1 hens went more frequently to the
feeder and this might have increased activity-
related HP. Moreover, in the R 1 and R 2 lines,
the absence of difference in basal metabolic rate
suggests that the physical activity of both genotypes
was similar when fasted. By using the increment of
heat production at the onset of light to estimate
 ENERGY BALANCE AND RFC 87
Table7. Slope of regression between respiratory quotient and time of R 1and R 2 laying
hens tube-fed with 70%, 100% or 130% of their ad libitum food intake (kJ/kg0.75.d; n 5 5
hens, experiment 3)

Line R1 R2 D1 D2

10·00 to 13·00 h
70% 1097 a 6 55 761 c 6 85 ** NS
Tube-fed 100% 1333 a 6 100 917 a 6 83 * *
130% 1332 a 6 76 890 b 6 91 **
14·00 to 17·00 h
70% 2 1015 a 6 48 2 716 a 6 98 * **
Tube-fed 100% 2 840a 6 46 2 470 b 6 94 ** ***
130% 8b 6 64 51 c 6 32 NS
17·00 to 22·00 h
70% 400a 6 25 215 a 6 43 ** NS
Tube-fed 100% 629a 6 78 413 b 6 44 * *
130% 526a 6 29 355 b 6 10 **
03·00 to 07·00 h
70% 2 811a 6 95 2 456 b 6 34 ** NS
Tube-fed 100% 2 1010 a 6 104 2 707 a 6 37 * *
130% 2 694 b 6 140 2 172c 6 61 **
1
Values in the same column and the same period not sharing the same
superscript are different (P , 0·05) according to a paired sample Student’s t test
between hens of the same line.
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D1 5 difference between lines at the same tube-feeding input; D2 5 differences

between lines for the same energy intake, R 1 hens tube-fed with 70%
compared with R 2 hens tube-fed with 100% of ad libitum food intake and R 1
hens tube-fed with 100% compared with R 2 hens tube-fed with 130% of ad
libitum food intake according to a two-tailed t test. NS not signiŽ cant, * P , 0·05,
** P , 0·01, *** P , 0·001.

Table 8. Equations between heat production (HP) and true metabolisable energy intake (TMEi)
in R 1 and R 2 laying hens having free access to food or tube-fed at 70%, 100% or 130% of their
individual ad libitum intake (experiments 2 and 3) HP 5 A 3 TMEi 1 B with HP and TMEi in
kJ/kg 0.75.d

Feeding technique Line A B r1 SigniŽ cance1

Free access to food R1 0·264a 208a 0·742 **

n 5 15 R2 0·195c 221a 0·537 **
Tube-feeding R1 0·216 b 210a 0·783 **
n 5 20 R2 0·188c 197a 0·587 **
1
r 5 coefŽ cient of correlation; signiŽ cance of the regression, ** P , 0·01 2Values within
a column not sharing the same superscript are signiŽ cantly different (P , 0·05).

activity-related HP, fed R 1 hens exhibited higher
activity-related HP than R 2 ones (61 vs 18 kJ/
kg0·75 .d). This activity-related HP, which remained
independent of the energy intake in both lines,
accounted for only 30% of the difference in HI.
Lipid turnover
Regressions between RQ and time could be related
to the rate of lipid synthesis (positive slope) and
lipid catabolism (negative slope). After tube-feeding
(10·00 to 13·00 h and 17·00 to 22·00 h periods),
higher slopes might indicate enhanced rate of lipo-
genesis in the R 1 line. Conversely, during later
periods after crop intubation (14·00 to 17·00 h and
03·00 to 07·00 h), greater negative slopes suggested
an increased lipid degradation rate in R 1 hens
compared to R 2 . Such results might be related to
greater lipid turnover in R 1 hens. R 1 hens thus
appeared to be able to dissipate an excess of energy
partly by an immediate increase in thermogenesis
and partly by a transient storage of energy as lipids
which are rapidly catabolised. Fatty acids might
thus be the main fuel used for this thermogenesis,
as observed in cold-exposed ducklings which exhib-
ited an uncoupling effect of fatty acid in mitochon-
dria isolated from gastrocnemius and liver (Barré et
al., 1985). Such a result may explain that measur-
ing the energy balance of laying hens during a
shorter period overestimated the retained energy as
fat in R 1 hens compared to R 2 line. The trend
for an increased retained energy as fat in the R 1
line could not be explained by a difference in egg
production or egg composition. Moreover R 1
fowls were leaner than R 2 ones: R 2 fowls had
more carcase lipid and more abdominal fat. Diver-
gence in fatness appears before difference in food
consumption and RFC (Tixier et al., 1988). This
difference remains important at one year old (Zein
el Dein et al., 1985; El-Kazzi et al., 1995).
 88 J. F. GABARROU ET AL.
Metabolic pathways
To investigate metabolic pathways involved in
thermogenesis in both lines, concentration of sev-
eral plasma variables (triglycerides, phospholipids,
uric acid, glucose and insulin) were determined.
Whatever the nutritional state, no differences were
observed between genotypes, suggesting similar
thermogenic pathways. A similar RQ in either fed
or fasted conditions but at different rates conŽ rms
the similarity in metabolism of both genotypes.
Plasma T3 and T4 concentrations, similar in both
lines when fed, did not relate to the difference in
HP. Danforth and Burger (1989) showed that a
large increment in energy intake balanced by an
enhanced HP resulted in no difference in plasma
T3, T4 and insulin, although noradrenaline con-
centrations changed. Similar results were obtained
in cockerels in the case of hepatic deiodinase ac-
tivity (Geraert et al., 1996). However, the difference
between lines in plasma T4 concentration when
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fasted suggests a higher turnover of thyroid hor-
mones. Moreover, using 30 hens of each line,
Bordas (unpublished data) found that there was a
higher plasma T3 concentration in R 1 hens when
differences in RFC were detectable (18 weeks).
Turnover of thyroid hormones should be further
analysed to understand the control of thermogene-
sis in both lines.
R1 hens ate signiŽ cantly more than R 2
ones, especially at the onset of light. R 1 hens also
took more frequent but shorter meals, suggesting a
higher feeding activity. An increased heat in-
crement of feeding allowed R 1 hens to get rid of
their excessive energy intake without a signiŽ cant
difference in total retained energy. This higher
heat increment in R 1 hens could be explained by
an increased feeding activity and by an increased
diet-induced thermogenesis from a regulatory com-
ponent in the R 1 line. An increased turnover of
lipids may be involved but the metabolic pathways
used for this diet-induced thermogenesis are still
unclear. The same metabolic pathway is likely to
be involved in the 2 lines but with a higher rate in
the R 1 line. A neuro-humoral control of this DIT
and of food intake regulation should be demon-
strated. Further experiments should be undertaken
to understand the role of thyroid hormones in the
2 lines. As birds have no brown adipose tissue
(Saarela et al., 1989), mechanisms and sites of this
DIT should be further investigated.
REFERENCES
BARRE, H., NEDERGAARD, J. & CANNAN , B. (1985) Increased respir-
ation in skeletal muscle mitochondria from cold acclimated
ducklings: uncoupling effect of free fatty acids. Comparative
Biochemistry and Physiology, 85B: 343–348
BENTSEN, H.B. (1983) Genetic variations in feed efŽ ciency of
laying hens at constant body weight and egg production. II
Source of variation in feed consumption. Acta Agricultura Scan-
dinavia, 33: 305–320.
BORDAS, A. & MERAT, P. (1981) Genetic variation and phenotypic
correlations of food consumption of laying hens corrected for
body weight and production. British Poultry Science, 22: 25–33.
BORDAS, A. & MERAT, P. (1984) Correlated responses in a selec-
tion experiment on residual feed intake of adult Rhode Island
Red cock and hens. Annales Agriculturae Fenniae, 23: 233–237.
BORDAS, A., TIXIER-BOICHARD M. & MERAT, P. (1992) Direct and
correlated responses to divergent selection for residual food
intake in Rhode Island laying hens. British Poultry Science, 33:
741–754.
BYERLY, T.C., KESSLER, J.W., GOUS, R.M. & THOMAS, P. (1980)
Feed requirement for egg production. Poultry Science, 59:
2500–2507.
DANFORTH , E. & BURGER, A.G. (1989) The impact of nutrition on
thyroid hormone physiology and action. Annual Review of
Nutrition, 9: 201–227.
EL-KAZZI , M., BORDAS, A., GANDEMER, G. & MINVIELLE, F. (1995)
Divergent selection for residual food intake in Rhode Island
Red egg-laying lines: gross carcase composition, carcase
adiposity and lipid contents of tissues. British Poultry Science,
36: 719–728.
FAIRFULL, R.W. & CHAMBERS, J.R. (1984) Breeding for feed
efŽ ciency: poultry. Canadian Journal of Animal Science, 64: 513–
527.
FOLCH , J.L.M. & SLOANE- STACEY , G.H. (1957) A simple method
for the isolation and puriŽ cation of total lipids from animal
tissues. Journal of Biological Chemistry, 226: 497–509.
FOSSATI, P. & PRENCIPE , L. (1982) Serum triglycerides determined
colorimetrically with an enzyme that produces hydrogen
peroxide. Clinical Chemistry, 28: 2077–2080.
FOSSATI, P., PRENCIPE , L. & BERTI, G. (1980) Use of 3,5-dichloro-
2-hydroxybenzenesulfonic acid/4-aminophenazone chro-
mogenic system in direct enzymic assay of uric acid in serum
and urine. Clinical Chemistry, 26: 227–231.
GERAERT, P.A. (1990) Dépense énergétique et échanges respira-
toires: description d’une installation automatisée appliquée
aux oiseaux. Cahiers de Nutrition et de Diététique, 25: 205.
GERAERT, P.A., GUILLAUMIN, S., BORDAS, A. & MERAT, P. (1991)
Evidence of a genetic control of diet-induced thermogenesis
in poultry, Proceedings of the 12th Symposium of Energy Metabolism
of Farm Animals EAAP, 58: 380–383.
GERAERT, P.A., GUILLAUMIN, S., BORDAS, A. & MERAT, P. (1992)
Genetic variation in diet-induced thermogenesis in birds.
Proceedings of the Nutrition Society, 51: 86A.
GERAERT, P.A., GABARROU , J.F., GUILLAUMIN, S., PICARD, M. &
BORDAS, A. (1996) Genetic variation of diet-induced thermo-
genesis in birds. Journal of Nutrition, (in press).
KATLE, J. (1991) Selection for efŽ ciency of food utilisation in laying
hens: causal factors for variation in residual food consump-
tion. British Poultry Science, 32: 955–969.
KATLE, J., BENTSEN, H.B. & BRAASTAD , B.O. (1984) Correlated
traits with residual feed consumption. Proceedings of the 17th
World’s Poultry Congress and Exhibition, pp. 136–138 Helsinki,
Finland, World’s Poultry Science Association.
KATLE, J. & KOLSTAD, N. (1991) Selection for efŽ ciency in food
utilisation in laying hens: direct response in residual food
consumption and correlated responses in weight gain, egg
production and body weight. British Poultry Science, 32: 939–953.
LUITING, P. (1990) Genetic variation of energy partitioning in
laying hens: causes of variation in residual feed consumption.
World’s Poultry Science Journal, 46: 133–152.
LUITING, P. (1991) Metabolic differences between White Leghorns
selected for high and low residual feed consumption. British
Poultry Science, 32: 763–782.
LUITING, P. & URFF, E.M. (1991) Residual feed consumption in
laying hens: 2. Genetic variation and correlations. Poultry
Science, 70: 1663–1672.
MAC LEOD, M.G. (1991) Effect of feeding by crop intubation on
energy metabolism and physical activity in domestic cock-
erels. British Poultry Science, 32: 1089–1095.
OKABE, H., UJI, Y., NAGASHIMA , K. & NOMA, A. (1980) Enzymatic
determination of free fatty acids in serum. Clinical Chemistry,
26: 1540–1543.
 ENERGY BALANCE AND RFC
PICARD, M., BOUCHOT, C., ODORICO, J.F., SERVANT, P., TURRO, I.
& FAURE , J.M. (1992) Automatic measurement of individual
food intake in domestic chickens. Proceedings of the 19th World’s
Poultry Congress. 2: 448.
ROMIJN, C. & LOKHORST, W. (1961) Some aspect of energy
metabolism in birds. Proceedings of the 2nd Symposium on Energy
Metabolism of Farm Animals. Wageningen, Netherlands. EAAP,
10: 49–59.
ROTHWELL, N.J. & STOCK, M.J. (1979) A role of brown adipose
tissue in diet-induced thermogenesis. Nature, 281: 31–35.
SAARELA , S., HISSA, R., PYÖRNILÄ, A., HARJULA, R., OJANEN, M. &
ORELL, M. (1989) Do birds possess brown adipose tissue?
Comparative Biochemistry and Physiology, 92A: 219–228.
SABRI, H.M., WILCOX, C.J., WILSON, H.R. & HARMS, R.H. (1991)
Measurement of genetic variations in residual metabolisable
energy intake of laying hens. Poultry Science, 70: 222–228.
SAVORY, C.J. (1979) Feeding behaviour, in: BOORMAN, K.N. &
FREEMAN, B.M. (Eds) Food Intake Regulation in Poultry, pp. 277–
323 (Edinburgh, British Poultry Science).
SAVORY, C.J. (1980) Diurnal feeding patterns in domestic fowls: a
review. Applied Animal Ethology, 6: 71–82.
SCHULMAN , N., TUISKULA-HAAVISTO, M., SIITONEN, L. &
MÄNTYSAARI , E.A. (1994) Genetic variation of residual feed
Downloaded by [Dicle University] at 05:35 14 November 2014
89
consumption in a selected Finnish egg-layer population.
Poultry Science, 73: 1479–1484.
SIMON, J., FREYCHET, P. & ROSSELIN, G. (1974) Chicken insulin:
radioimmunnological characterization and enhanced activity
in rat fat cells and liver plasma membranes. Endocrinology, 95:
1439–1449.
TAKAYAMA , M., ITOH, S., NAGASAKI, T. & TANIMIZU, I. (1977) A
new enzymatic method for determination of serum choline-
containing phospholipids. Clinica Chimica Acta, 19: 1350–1355.
TIXIER, M., BORDAS, A. & MERAT, P. (1988) Divergent selection
for residual feed intake in laying hens: effect on growth and
fatness, in: LECLERCQ, B. & WHITEHEAD, C.C. (Eds) Leanness
in Domestic Birds, pp. 129–132 (London, Butterworths).
WILKINSON, L. (1975) Response variable hypothesis in the multi-
variate analysis of variance. Psychological Bulletin, 82: 408–412.
WING , T.L. & NORDSKOG, A.W. (1982) Use of individual feed
records in a selection program for egg production efŽ ciency.
1 Heritability of the residual component of feed efŽ ciency.
Poultry Science, 61: 226–230.
ZEIN-EL-DEIN, A., BORDAS, A. & MERAT, P. (1985) Selection diver-
gente pour la composante residuelle de la consommation
alimentaire des poules pondeuses: effets sur la composition
corporelle. Archiv für Geügelkunde, 49(4): 158–160.