Influence of Increased Environmental Complexity on Leg Condition

Influence of Increased Environmental Complexity on Leg Condition,
Performance, and Level of Fearfulness in Broilers
D. Bizeray,* I. Estevez,†,1 C. Leterrier,* J. M. Faure*
*Station de Recherches Avicoles, INRA de Tours, 37380 Nouzilly, France;
and †Department of Animal and Avian Sciences, University of Maryland,
College Park, Maryland 20742
(W) wheat was dispersed on the floor from Days 8 to
17. Control birds (C) were maintained under standard
management. Body weights and consumption were obtained throughout the rearing period. Gait score (GS),
tibia length and diameter, fluctuating asymmetry (FA),
bone ash, tibial dyschondroplasia (TD), bone breaking
strength, and tonic immobility (TI) were measured at
slaughter age.
Mortality, body weight, feed conversion, FA, bone ash,
TD, bone breaking strength, and TI duration did not differ
significantly among groups. L birds had a higher GS than
C and B birds and W birds had a higher GS than C birds
(P < 0.05). Provision of barriers significantly increased the
diameter of the tibia diaphysis (P = 0.05), which is a
promising result for further studies to improve leg condition.
ABSTRACT We hypothesized that increased distance
between resources and stimulation of foraging behavior,
through altering the degree of environmental complexity
by using moving lights and scattering whole wheat in the
litter, would improve physical activity of broiler chickens.
Increased activity may potentially improve leg condition
and performance and decrease the level of fearfulness
in broilers.
To test this hypothesis, 1,800 1-d-old male broilers were
divided into 40 groups of 45 birds each (10 birds/m2).
Each group was assigned to one of four treatments (10
replicates) as follows: barrier treatment (B) contained
three barriers placed between the drinker line and the
feeder. The light treatment (L) consisted of brightly colored moving lights projected on the pen floor for four 1h periods/d throughout rearing. For the wheat treatment
(Key words: broiler, enrichment, physical exercise, fearfulness, leg problem)
2002 Poultry Science 81:767–773
broiler chickens spend around 80% of the time lying (Bessei,
1992; Weeks et al., 2000). Several authors suggested that
this lack of exercise is one of the causal factors responsible
for the failure of the structure of the long bones to
strengthen, thus resulting in a high incidence of twisted
legs in commercial meat-type chickens (Rodenhoff and
Dammrich, 1971; Reiter and Bessei, 1998a,b). Increasing
activity via environmental management may improve leg
condition in broilers (Simons, 1986; Hester, 1994; Balog et
al., 1997). Factors such as rearing on litter vs. in cages (Haye
and Simons, 1978), increasing the distance between feeder
and drinker (Reiter and Bessei, 1996), the use of high light
intensity (Newberry et al., 1988), and implementing an
intermittent light regime (Buckland et al., 1976) are known
to improve leg conditions of broilers. These beneficial effects are generally explained as a consequence of increased
activity of the birds when kept under these management
practices.
INTRODUCTION
Meat-type chickens throughout the world are reared in
a variety of production systems, from very large homogenous houses to outdoor systems that are more heterogeneous and complex. Increased environmental complexity
in standard poultry houses has been investigated as a
means to achieve practical goals and resolve welfare problems (Newberry, 1995; Wemelsfelder and Birke, 1997;
Mench, 1998), such as decreasing fear responses (Hughes
and Black, 1974; Gvaryahu et al., 1989; Jones and Waddington, 1992). Furthermore, increased complexity may improve performance in broiler production systems (Shalev
et al., 1990).
Environmental management has also been studied with
the purpose of decreasing health problems, especially leg
problems in broilers. Behavioral studies have indicated that
2001 Poultry Science Association, Inc.
Received for publication June 4, 2001.
Accepted for publication December 28, 2001.
1
To whom correspondence should be addressed: ie7@umail.
umd.edu.
Abbreviation Key: C = control treatment; B = barrier treatment; FA
= fluctuating asymmetry; GS = gait score; L = light treatment; TD =
tibial dyschondroplasia; TI = tonic immobility; W = wheat treatment.
767
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BIZERAY ET AL.
In an attempt to increase activity level in broilers, Fiscus
Le Van et al. (2000) and Pettit-Riley and Estevez (2001)
provided birds with access to perches. However both experiments reported that the level of perch use was too low
to have any relevant impact on leg condition. The low
frequency of perch use seemed to be related to difficulties
in climbing on and off the perches, particularly toward the
end of the rearing period as the birds became heavier.
Other techniques, such as adding barriers or ramps between essential resources, increase physical exercise and
affect muscular conformation in broilers (Sandusky and
Heath, 1988a,b), although the effect on leg condition is
unknown. Modification of light programs and intensity
have significant effects on behavior, growth, and leg problems of broilers (Hester, 1994; Manser, 1996). Although
spotlights have been used to enrich floor pens in turkeys
(Sherwin et al., 1999), the effects of spotlights are not documented in broilers. However, spotlights are believed to
attract broilers and to increase activity. Because stimulating
foraging activity induces movement (Newberry, 1999), the
search for food can make animals more active (Koene,
1998). Therefore addition of variable food items may be
attractive for broilers and could potentially increase the
amount of time spent foraging (Chamove, 1989).
The aim of this study was to investigate the effect of
manipulating the broiler pen environment with the intent
of altering the amount of time spent foraging and to increase the difficulty of gaining access to resources as a
way of increasing activity and the reducing impact of leg
problems in broiler chickens. Two approaches were investigated: a) forcing birds to negotiate 15 cm high barriers to
gain access to the feeder and the drinkers, by walking
around the barriers or by jumping over them, and b) inducing foraging activity through light stimulation and by dispersing alternative palatable feed (i.e., whole wheat). Dispersion of whole wheat on the pen floor was conducted
at an early age because the majority of bone consolidation
occurs during the first 3 wk of age (Rose et al., 1996), and
increasing activity during this early period was the most
appropriate age to improve bone quality. We measured the
effects of these three methods of increasing environmental
complexity on the level of fearfulness, performance, and
leg condition in commercial broilers.
MATERIALS AND METHODS
This experiment was conducted at the Applied Poultry
Research Facility of the University of Maryland during the
fall of 2000. One thousand eight hundred male 1-d-old
broilers (Ross 308) were divided in 40 groups of 45 birds
each and were reared in 40 2.44-m × 1.83-m pens at a
density of 10 birds/m2. The pen floors were covered with
a 6 cm layer of wood shavings. The birds were raised under
commercial management practices. Water was provided
by nipple drinkers (seven nipples/pen) positioned along
the side wall of the pen. Feed was provided in two feed
trays on the floor until 7 d of age. From the start until the
end of the rearing period feed was provided also in a tube
feeder. Birds were fed a two-phase commercial diet ad
libitum: a starter ration (3,113 kcal/kg, 21.80% crude protein) from 0 to 21 d and a grower ration (3,216 kcal/kg,
20.83% crude protein) from 21 to 44 d, the end of the
experimental period.
An artificial lighting program (24L:0D, 0 to 1 d; 23L:1D,
2 to 44 d) and a standard temperature program were followed. When the set temperature was exceeded, wall curtains opened automatically to allow fresh air and natural
light to enter the house. Temperatures were maintained
between 28 and 33 C at the beginning of the growing period
and were gradually decreased to reach 22 C at the end of
the growing period. Supplementary heat was supplied in
each pen during the brooding period via hanging brooder
lamps until 20 d. Due to cold ambient weather, wall curtains rarely opened. Positive pressure ventilation was used
to provide 10 total air changes for each of the two rooms per
hour during the brooding period and 12 total air changes
during the grow-out period. Light intensity in the pens
was 28 lx at the floor level supplied by incandescent 150W bulbs (10 bulbs in each experimental room).
Experimental Design
The experiment consisted of three environmental complexity treatments and one control (C) treatment with 10
replications for each treatment. To control for potential
environmental variation throughout the poultry house, the
treatments were arranged in a complete randomized block
design. Two blocks consisted of 12 pens with treatments
repeated three times in each block. Two more blocks consisted of eight pens with treatments repeated two times.
Two blocks were assigned to each of the rooms within the
same building.
The barrier treatment pens (B) contained two 1.0 m long
× 0.15 m high × 0.04 m wide wood barriers and one 1.5 m
long × 0.15 m high × 0.04 m wide wood barrier placed
between the drinkers and the feeder, requiring birds to
walk around or climb the barriers to go from the feeder to
the drinkers (Figure 1). Each barrier was supported by a
0.2 m wide wood board laying on the floor, which was
covered with the wood shavings.
Each light treatment pen (L) was illuminated with one
light projector consisting of a black plastic sphere containing an incandescent 15-W bulb, 45 multicolored translucent spots for light projection, and a small engine to rotate
the sphere (1 rotation/3 s). Each light projector was hung
at the center of the pen at 0.9 m above the floor. By automatically controlling the projector with a timer, each L pen
received the treatment of brightly colored, moving lights
on the pen floor for four 1-h periods/d throughout rearing
(at 0800, 1000, 1200, 1400 h). The size of each projected
spotlight on the floor was 7 cm in diameter.
In addition to the standard feed ad libitum, commercial
whole wheat was randomly thrown on the litter of the
wheat treatment pens (W) from 8 to 17 d (10 g/bird per
day) twice a day (at 0800 and 1130 h). The same experimenter always randomly threw the wheat in the pens.
The C consisted of standard pens with feed and water as
described above.
ENVIRONMENTAL COMPLEXITY AND LEG PROBLEMS
769
difficulty and only when strongly motivated. A score of 5
was not included because birds categorized as such are
unable to walk; therefore, they would have been culled
prior to the GS test. Any equipment (barriers and lights)
was removed from the pens prior to the GS test to avoid any
treatment bias influencing the judgement of the observers.
Bone Quality
FIGURE 1. Diagram of the barriers treatment pen. The same experimental design without barriers was used for three other treatments.
Side and front walls of the pens were covered with black
plastic to prevent colored moving lights from influencing
adjacent pens with different treatments. Twelve birds per
pen were tagged for individual recognition using the Swiftack2 identification system for poultry. Each bird was double-tagged, one through the back of the neck and one
through the wing, with a 16-ga needle.
Mortality, Body Weights,
and Feed Conversion
Mortality and culls per pen were recorded daily. Individual body weights of the 12 tagged birds per pen were taken
at 0, 21, and 42 d. Feed consumption per pen was calculated
for 0 to 42 d. Wheat dispersed in the W treatment was not
included as feed consumed because we were unable to
determine the amount of wheat remaining in the litter of
the pen. Feed conversion per pen was calculated by dividing the total feed consumed by the sum of the weights of
the dead birds and the mean weight per bird multiplied
by the number of live birds.
Gait Score
Of the 12 tagged birds, a subsample of seven tagged birds
per pen was chosen randomly. Each bird was observed and
classified into different categories of lameness in its home
pen at 41 d by two observers consulting together following
guidelines of Kestin et al. (1992). There were five categories
of gait score (GS), where 0 = a bird that walked normally
with no detectable abnormality to 4 = a bird that had a
severe gait defect but was still capable of walking with
At 42 d, four tagged birds per pen were randomly selected and euthanized by cervical dislocation. Right and
left tibiotarsi were removed, and tibial length and diameter
of the mid-diaphysis were measured with a digital caliper.
Relative fluctuating asymmetry (FA) of leg diameter and
length was defined as absolute unsigned left-minus-right
value divided by the mean of the left and the right measures
(Møller et al., 1995).
The left tibiotarsi were dried (100 C for 24 h), defatted
in ethanol for 16 h, dried a second time (100 C for 24 h),
and weighed. Bones were ashed (630 C for 16 h) and ash
weight was calculated relative to tibial dry weight to obtain
ash percentage.
The right tibiotarsi were frozen until processed. A threepoint test3 was carried out on the bones when thawed. The
rate of travel of the mobile anvil was 5 mm/min and the
width of the bearer was 50 mm. Stiffness was calculated
as the slope of the loading curve before the bio yield point
(Hirano et al., 1999), i.e., the inflection point of the loading curve.
Tibial dyschondroplasia (TD) scores were determined
on right tibias. The TD scores ranged from 0 (normal) to
3 (severe) and were based on the amount of cartilage proliferation as follows: 0 = no TD lesions present, 1 = lesions
less than 4.5 mm, 2 = lesions greater than 4.5 mm and less
than 10 mm, and 3 = lesions greater than 10 mm (scale
adapted from Edwards and Veltmann, 1983).
Tonic Immobility
Tonic immobility (TI) reactions were examined in 44-dold birds. Four tagged birds per pen were randomly chosen, and TI tests were run by two experimenters in two
independent identical rooms adjacent to the two rearing
rooms. Each bird was tested individually by placing it on
its back on a table and restrained for 10 s [one of the
experimenter’s hands over the chick’s body and one hand
over its head (Mills and Faure, 1991)]. The observer sat still
within sight of the bird. The duration of TI was recorded
(i.e., the time until the bird stood up). If an attempt of
induction was unsuccessful (no TI or TI lasting less than
10 s), the experimenter immediately resumed the induction
procedure. If TI could not be induced after three attempts,
the bird was deemed not to be susceptible and its TI duration score was 0 s. If the bird did not stand after 5 min, a
maximum score of 300 s was recorded for TI duration.
Statistical Analyses
2
Heartland Animal Health, Inc., Fair Play, MO 65649.
Instron Number 1102, High Wycombe, Bucks HP12 35Y, UK.
3
A mean value per pen was calculated for all the analyzed
variables, except GS. These same variables were analyzed
770
BIZERAY ET AL.
TABLE 1. Least square means (±SE) for mortalities, feed conversion
and body weights at hatch, 21 and 42 d of age
Treatment effect
Treatment
Mortality (%)
Feed conversion
Body weights (g)
Hatching
Day 21
Day 42
Control
Barrier
Light
Wheat
F-value*
P-value
5.111 ± 0.03
1.798 ± 0.03
6.444 ± 0.03
1.801 ± 0.03
5.111 ± 0.03
1.825 ± 0.03
5.333 ± 0.03
1.751 ± 0.03
0.43
1.83
0.735
0.212
45.9 ± 0.49
629.2 ± 18.9
2,017.4 ± 28.9
45.4 ± 0.49
641.9 ± 19.0
2,052.5 ± 29.3
45.4 ± 0.49
653.7 ± 18.9
2,096.2 ± 28.8
46.08 ± 0.49
664.3 ± 18.8
2,113.6 ± 28.9
0.44
1.26
2.31
0.728
0.345
0.144
*ANOVA test, numerator df = 3, denominator df = 9.
using a mixed model ANOVA after testing for homogeneity of variance and normality. Percentage mortality was
analyzed after using an arcsine square root transformation.
GS was an ordinal variable and was analyzed nonparametrically using a variation of Friedman’s rank test for randomized block designs (SAS, 1996). Replicates within blocks
were treated as blocks and pens were considered to be the
fundamental experimental unit.
An exact randomization distribution of the test statistic
under the null hypothesis was calculated using a program
developed in SAS software by a method described in Manly
(1991). To construct this distribution, pens were randomly
shuffled among treatments within each of 10 blocks and a
test statistic computed. This process was repeated 4,000
times and a null hypothesis distribution was calculated for
the overall statistic as well as for the difference in average
ranks between each pair of treatments. A P-value was computed for the overall test by looking at the percentage of
values that exceeded the observed statistic. For multiple
comparisons, a P-value was computed by first calculating
the absolute value of the difference in the average ranks
for each pair of treatments and then computing the percentage of times the observed statistic exceeded this value. The
Bonferroni test was then used for the mean GS comparisons. Finally, we report the distribution of GS within each
treatment. All analyses were performed by statistical software (SAS, 1996).
RESULTS
Mortality, Body Weights,
and Feed Conversion
No significant differences in mortality were found
among the four treatment groups (Table 1). A total of 17,
25, 20, and 20 birds died throughout the rearing period
including three, two, two, and two birds that were culled
due to leg problems in the C, B, L, and W treatment groups,
respectively. Body weights at 21 and 42 d and feed conversion did not differ across treatments.
GS
GS were significantly affected by experimental treatment
(P < 0.05). The L birds had a significantly higher GS than
C birds (P < 0.05) and B birds (P < 0.05), whereas W birds
had a significantly higher GS than C birds (P < 0.05) (Table 2).
Bone Quality
No significant differences in FA for leg length or diameter
were found among treatments (Table 3). Mean lengths of
both tibiae were not significantly affected by the treatment,
whereas the mean diameters of both tibiae were higher in
the B treatment in comparison to the other three treatments
(Table 3). These differences were not significant for the
right tibia (mean diameter) 13.45 ± 0.16 mm for C, 13.84 ±
0.16 mm for B, 13.15 ± 0.16 mm for L, and 13.37 ± 0.16
mm W treatment groups (F3,9 = 3.02; P = 0.086) and were
significant for the left tibia (mean diameter) 13.42 ± 0.15
mm for C, 13.99 ± 0.15 mm for B, 13.30 ± 0.15 mm for L,
and 13.41 ± 0.15 mm for W treatments (F3,9 = 4.24; P =
0.039). No significant differences in percentage of bone ash
or in biomechanical parameters were found among the
groups (Table 3).
In our experiment, the number of sampled birds with
TD lesions was not sufficiently numerous to be statistically
analyzed. Only 13% of birds had TD lesions. A total of 5,
7, 5, and 5 birds with TD lesions were found in C, B, L,
and W treatments respectively, with a total of one, one,
three, and two birds with severe lesions (TD level 3), respectively.
TI
TI duration at 44 d did not differ among treatments
(107.2 ± 16.7 s for C, 110.2 ± 14.9 s for B, 120.3 ± 19.6 s for
L, and 109.6 ± 20.8 s for W treatments; F3,9 = 0.10; P =
0.95). The number of TI inductions was not affected by the
treatment (2.42 ± 0.12 for C, 2.27 ± 0.12 for B, 2.34 ± 0.12
for L, and 2.40 ± 0.12 for W treatments; F3,9 = 0.30; P = 0.82).
TABLE 2. Distribution of the frequencies (%) of gait score1
Treatment
GS0
GS1
GS2
GS3
GS4
Control
Barrier
Light
Wheat
8.57
4.53
2.86
4.29
47.14
44.93
31.43
31.43
28.57
37.68
48.57
37.14
11.43
10.14
15.71
21.43
4.29
2.90
1.43
5.71
1
GS0 = gait score of 0; GS1 = gait score of 1, etc.
771
ENVIRONMENTAL COMPLEXITY AND LEG PROBLEMS
TABLE 3. Least square means (± SE) for FA and bone quality measures on tibiotarsi
Treatment effect
Treatment
Length (mm)
Diameter (mm)
Asymmetry length
Asymmetry diameter
Bone ash (%)
Stiffness (N/mm)
Bio yield point (N)
Breaking strength (N)
Control
67.6
13.43
0.034
0.035
55.37
209.68
226.13
370.28
±
±
±
±
±
±
±
±
0.71
0.15b
0.004
0.005
0.22
7.20
10.30
12.20
Barrier
68.55
13.91
0.028
0.032
54.99
196.12
211.59
364.19
±
±
±
±
±
±
±
±
0.71
0.15a
0.004
0.005
0.22
7.20
10.30
12.20
Light
68.06
13.22
0.029
0.028
55.35
194.79
190.77
339.41
±
±
±
±
±
±
±
±
0.71
0.15b
0.004
0.005
0.22
7.20
10.30
12.20
Wheat
F-value
P-value
±
±
±
±
±
±
±
±
0.62
3.81
0.94
0.52
1.10
1.13
2.06
1.21
0.617
0.051
0.459
0.680
0.396
0.386
0.175
0.360
67.47
13.39
0.037
0.035
55.44
204.78
203.73
361.65
0.71
0.15b
0.004
0.005
0.22
7.20
10.30
12.20
Means with different letters deonte significant differences across treatments P < 0.05.
*ANOVA test, numerator df = 3, denominator df = 9.
a,b
DISCUSSION
The aim of this experiment was to determine the effect
of three types of environmental complexity designed to
enhance foraging behavior and walking. It was hypothesized that those changes would have an effect on leg condition, performance, or level of fearfulness in broilers. However, no treatment had a significant effect on body weight,
feed conversion, or mortality. Shalev et al. (1990) found
that adding barriers between feeders and drinkers had no
effect on body weight. This finding was consistent with
our results but tended to decrease feed efficiency in highly
active groups of broilers, an effect that was undetected in
the present experiment. In contrast, Balog et al. (1997) found
differences in muscle conformation and live body weight
and decreased mortality when adding obstacles to the path
of movement of broilers to reach the food. Other studies
have shown that increasing complexity in the captive environments of production animals rarely alters performance
as indicated for pigs (O’Connell and Beattie, 1999) or broilers (Fiscus Le Van et al., 2000; Su et al., 2000; Cornetto and
Estevez, 2001; Pettit-Riley and Estevez, 2001) or induces
some improvements depending on age (Gvaryahu et al.,
1989) or genotype (Hill et al., 1998).
Duration of TI was similar for all the treatments. TI
duration has been widely described as a good predictor of
the level of fearfulness in domestic chickens (Jones, 1986).
Previous studies have shown that chicks raised in an environment with increased complexity such as by addition of
perches (Brake et al., 1994; Rose et al., 1995); music (Gvaryahu et al., 1989); objects such as balls, strings, or drawings
on the wall (Jones, 1982; Jones and Waddington, 1992); or
the addition of these three types of enrichment (Nicol,
1992) were less fearful than birds raised in a standard
environment. In this experiment we expected less fearfulness in pens containing the B and L treatments and
initially also for the W treatment. However, because scattering the wheat into the litter induced a panic-like response
with the birds running toward the pen walls, we expected
birds in this treatment to have a higher TI response. However, we found no differences across treatments in TI.
The absences of differences in TI time correspond with
the lack of divergences in the FA of bone measurements.
These results could be explained by the fact that birds were
kept at a relatively low density in our experiment and had
very similar growth rates, which are positively related to
symmetry, and is consistent with the positive relationship
between TI duration and FA (Møller et al., 1995). These
authors found that the mean of the relative asymmetries
of different morphological characteristics (radius, carpometacarpus, tarsometatarsus, joint, and second primary
feathers) was approximately 0.041 ± 0.006 in Ross broilers,
which is slightly higher than the FA found in the tibiotarsi
of our experiment, possibly because of the greater density
used in their experiments. In addition, the lack of effects
of our treatments may be due to a relative low effect of our
experimental treatments in enhancing locomotor activity in
broilers. Behavioral effects of these experimental treatments
are currently being analyzed.
Although there was no treatment effect on bone mechanical characteristics or on bone mineralization, the diameter
of the tibial diaphysis was increased in the B treatment.
Direct observations on the behavior of the birds (Bizeray
personal observations) indicated that birds within the B
treatment used the barriers as perches, which could explain
the differences in the tibiae diameters of the birds in the B
treatment. Maintaining balance while perching and stepping onto and over barriers exercises leg muscles and joints
in a way that is different from simply walking and might
have influenced bone morphology. However, this change
in diameter had no effect on the biomechanical characteristics of the tibiotarsi as indicated by bone breaking strength
and bone stiffness. This change was in contrast to genetic
selection for increased shank width that improved bone
mechanical properties in turkeys (Nestor et al., 1985).
Perching increases trabecular bone volume and mechanical
properties in laying hens (Wilson et al., 1993) and seems
less effective in strengthening bone in broilers, probably
because of their lower response to mechanical stimuli (Pitsillides et al., 1999). This lack of effect on bone biomechanical characteristics is consistent with the lack of effect on
GS between B and C birds. Similarly, increased distance
between feed and water has been reported to have no effect
on the walking ability in turkeys, even when additional
exercise is provided (Noble et al., 1996).
Surprisingly, adding brightly colored moving spotlights
to the pen floor did not have any effect on performance
or fearfulness. The effect of light characteristics has been
extensively studied for its influence on the behavior and
physiology of poultry (intensity, photoperiod, light source,
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BIZERAY ET AL.
and wavelength, reviewed by Manser, 1996). Growth, feed
consumption, and feed conversion are often reported to be
influenced by the color of the light (Lewis and Morris,
2000), and incidence of leg problems is influenced by light
intensity (Newberry et al., 1988), photoperiod (Buckland
et al., 1976; Wilson et al., 1984), and light color (Prayitno
et al., 1997).
Our results are contrary to the effects reported by Sherwin et al. (1999) for turkeys, as our light device impaired
GS. They found that by adding a variety of pecking substrates to the pens of commercial turkeys, including an
apparatus giving two sources of supplemental spotlighting
over the center of the room, seemed to improve the musculo-skeletal system. In their experiment, the birds in the
enriched pens had greater latency to sit after 2.5 min of
forced standing than the C birds. The increased GS in the
L treatment may be related to the enhancement in body
weight (Kestin et al., 2001). Even if body weight was not
significantly different at slaughter age across groups, the
differences may be large enough to induce changes in GS,
as impairment of GS was found in L and W treatments in
which the birds were the heaviest.
Dispersing whole wheat on the floor from 8 to 17 d of
age did not have any significant effect on performance,
TI, or bone quality, but it impaired GS. The results on
performance however are not surprising as the majority of
grains were uneaten and remained in the litter until the
end of the experiment, explaining the absence of difference
from the other treatments. Previous studies have shown
that early experience influences later food preferences, especially in the choice of feeding systems between whole
wheat and pellet food, and it has been suggested that chicks
be exposed to a variation of grains from an early age (Cumming et al., 1987). However, exposure to grains must not
be too early in life so as to prevent a possible aversion to
the grain because the gizzard may be physically unable to
break down the whole wheat quickly because of its hardness (Covasa and Forbes, 1996). In this experiment, whole
wheat was a novel feed for 1-wk-old birds, and it was
supplied on the floor rather than at the feeder, perhaps
making it difficult for the birds to recognize it as feed. It
is also possible that broilers may prefer to eat pellets from
the feeder rather than foraging for whole grains in the litter.
Although this method would not be suitable for commercial operations, it could still be possible to increase foraging
activity for experimental purposes by dispersing the feed
on the litter while temporarily removing other feed sources
or by simply supplying part of the commercial feed dispersed on the floor. This schedule of diet distribution, alternating complete diet and other feed on litter may reduce
the negative effect found on GS. Indeed, dispersing whole
wheat on the floor from 8 to 17 d of age may have enhanced
diet consumption during this period even though differences in final body weight could not be statistically detected. This increase could help to explain the negative
effect on GS as feed restriction is recommended during this
period to improve leg condition (Leterrier and Constantin, 1996)
In conclusion, certain management practices such as providing barriers between feed and water, designed to enhance foraging and walking in broiler chickens, can potentially be a means to improve leg strength without affecting
growth rate or feed conversion. Barriers seem to have many
practical advantages: their fabrication is easy and inexpensive, they induce perching, and they result in increased
tibial diameter of the birds. Other alternatives such as providing spotlights into the broiler environment or food on
the floor have to be designed differently in further studies
in order to avoid the surprisingly negative effects that we
found on GS.
ACKNOWLEDGMENTS
We thank Estelle Russek-Cohen at the Department of
Animal and Avian Sciences at the University of Maryland
for her advice regarding statistical analysis. We also thank
Sabrina McGary, Mason Freed, Mark Spicknall, Hollis
Sequea, Glen Hahn, Paul Constantin, and Vanessa Guesdon for their technical help.
REFERENCES
Balog, J. M., G. R. Bayyari, N. C. Rath, W. E. Huff, and N. B.
Anthony. 1997. Effect of intermittent activity on broiler production parameters. Poult. Sci. 76:6–12.
Bessei, W. 1992. Behaviour of intensively managed broilers. Arch.
Geflügelkd. 56:1–7.
Brake, J., T. P. Keeley, and R. B. Jones. 1994. Effect of age and
presence of perches during rearing on tonic immobility fear
reactions of broiler breeder pullets. Poult. Sci. 73:1470–1474.
Buckland, R. B., D. E. Bernon, and A. Goldrosen. 1976. Effect of
four lighting regimes on broiler performance, leg abnormalities
and plasma corticoid levels. Poult. Sci. 55:1072–1076.
Chamove, A. S. 1989. Environmental enrichment: A review. Anim.
Technol. 40:155–178.
Cornetto, T., and I. Estevez. 2001. Influence of vertical panels
on use of space by domestic fowl. Appl. Anim. Behav. Sci.
71:141–153.
Covasa, M., and J. M. Forbes. 1996. Effects of prior experience
and training on diet selection of broiler chickens using wheat.
Appl. Anim. Behav. Sci. 46:229–242.
Cumming, R. B., I. M. Mastika, M. Wodzicka-Tomaszewska. 1987.
Practical aspects of choice feeding in poultry and its future
role. Pages 283–289 in Recent Advances in Animal Nutrition
in Australia. D. J. Farrell, ed. University of New England,
Armidale, Australia.
Edwards, H. M., Jr., and J. R. Veltmann, Jr. 1983. The role of
calcium and phosphorus in the etiology of tibial dyschondroplasia in young chicks. J. Nutr. 113:1568–1575.
Fiscus Le Van, N., I. Estevez, and W. R. Stricklin. 2000. Use of
horizontal and angled perches by broiler chickens. Appl. Anim.
Behav. Sci. 65:359–365.
Gvaryahu, G., D. L. Cunningham, and A. Van Tienhovan. 1989.
Filial imprinting, environmental enrichment, and music application effects on behavior and performance of meat strain
chicks. Poult. Sci. 68:211–217.
Haye, U., and P. C. M. Simons. 1978. Twisted legs in broilers. Br.
Poult. Sci. 19:549–557.
Hester, P. Y. 1994. The role of environment and management on
leg abnormalities in meat-type fowl. Poult. Sci. 73:904–915.
Hill, J. D., J. J. McGlone, S. D. Fullwood, and M. F. Miller. 1998.
Environmental enrichment influences on pig behavior, performance and meat quality. Appl. Anim. Behav. Sci. 57:51–68.
Hirano, T., D. B. Burr, C. H. Turner, M. Sato, R. L. Cain, and J.
M. Hock. 1999. Anabolic effects of human biosynthetic para-
ENVIRONMENTAL COMPLEXITY AND LEG PROBLEMS
thyroid hormone fragment (1-34), LY333334, on remodelling
and mechanical properties of cortical bone in rabbits. J. Bone
Miner. Res. 14:536–545.
Hughes, B. O., and A. J. Black. 1974. The effect of environmental
factors on activity, selected behaviour patterns and “fear” of
fowl in cages and pens. Br. Poult. Sci. 15:375–380.
Jones, R. B. 1982. Effects of early environmental enrichment upon
open-field behavior and timidity in the domestic chick. Dev.
Psychobiol. 15:105–111.
Jones, R. B. 1986. The tonic immobility reaction of the domestic
fowl: a review. World Poult. Sci. J. 42:82–96.
Jones, R. B., and D. Waddington. 1992. Modification of fear in
domestic chicks, Gallus gallus domesticus, via regular handling
and early environmental enrichment. Anim. Behav. 43:1021–
1033.
Kestin, S. C., S. Gordon, G. Su, and P. Sørensen. 2001. Relationship
in broiler chickens between lameness, liveweight, growth rate
and age. Vet. Rec. 148:195–197.
Kestin, S. C., T. G. Knowles, A. E. Tinch, and N. G. Gregory.
1992. Prevalence of leg weakness in broiler chickens and its
relationship with genotype. Vet. Rec. 131:190–194.
Koene, P. 1998. When feeding is just eating: how do farm and
zoo animals use their spare time. Pages 13–19 in Regulation
of Feed Intake. Proceedings of the 5th Zodiac Symposium. D.
Van der Heide, ed. CAB International, Wageningen, Netherlands.
Leterrier, C., and P. Constantin. 1996. Reducing the occurrence
of Varus-Valgus deformations in broiler chickens with a low
energy diet or an increasing lighting schedule. Arch. Geflügelkd. 60:181–187.
Lewis, P. D., and T. R. Morris. 2000. Poultry and colored lights.
World Poult. Sci. J. 56:189–207.
Manly, B. J. F. 1991. Randomization and Monte Carlo Methods
in Biology. Chapman and Hall, New York.
Manser, C. E. 1996. Effects of lighting on the welfare of domestic
poultry: A review. Anim. Welfare 5:341–360.
Mench, J. A. 1998. Environmental enrichment and the importance
of exploratory behavior. Pages 30–46 in Second Nature, Environmental Enrichment for Captive Animals. D. J. Shepherdson,
J. D. Mellen, and M. Hutchins, ed. Smithsonian Institution,
Washington, DC.
Mills, A. D., and J. M. Faure. 1991. Divergent selection for duration
of tonic immobility and social reinstatement behavior in Japanese quail (Coturnix coturnix japonica) chicks. J. Comp. Psychol.
105:25–38.
Møller, A. P., G. S. Sanotra, and K. S. Vestergaard. 1995. Developmental stability in relation to population density and breed of
chickens Gallus gallus. Poult. Sci. 74:1761–1771.
Nestor, K. E., W. L. Bacon, Y. M. Saif, and P. A. Renner. 1985.
The influence of genetic increases in shank width on body
weight, walking ability, and reproduction of turkeys. Poult.
Sci. 64:2248–2255.
Newberry, R. C. 1995. Environmental enrichment: increasing the
biological relevance of captive environments. Appl. Anim. Behav. Sci. 44:229–243.
Newberry, R. C. 1999. Exploratory behaviour of young domestic
fowl. Appl. Anim. Behav. Sci. 63:311–321.
Newberry, R. C., J. R. Hunt, and E. E. Gardiner. 1988. Influence
of light intensity on behavior and performance of broiler chickens. Poult. Sci. 67:1020–1025.
Nicol, C. J. 1992. Effects of environmental enrichment and gentle
handling on behaviour and fear responses of transported broilers. Appl. Anim. Behav. Sci. 33:367–380.
Noble, D. O., K. K. Krueger, and K. E. Nestor. 1996. The effect
of altering feed and water location and of activity on growth,
performance, behavior, and walking ability of hens from two
strains of commercial turkeys. Poult. Sci. 75:833–837.
773
O’Connell, N. E., and V. E. Beattie. 1999. Influence of environmental enrichment on aggressive behaviour and dominance relationships in growing pigs. Anim. Welfare 8:269–279.
Pettit-Riley, R., and I. Estevez. 2001. Effects of density on perching
behavior of broiler chickens. Appl. Anim. Behav. Sci.
71:127–140.
Pitsillides, A. A., S. C. Rawlinson, J. R. Mosley, and L. E. Lanyon.
1999. Bone’s early responses to mechanical loading differ in
distinct genetic strains of chick: Selection for enhanced growth
reduces skeletal adaptability. J. Bone Miner. Res. 14:980–987.
Prayitno, D. S., C. J. C. Phillips, and D. K. Stokes. 1997. The effects
of color and intensity on behavior and leg disorders in broiler
chickens. Poult. Sci. 76:1674–1681.
Reiter, K., and W. Bessei. 1996. Effect of the distance between
feeder and drinker on behaviour and leg disorders of broilers.
Pages 131 in 30th ISAE International Congress. I. J. H. Duncan,
T. M. Widowski, and D. B. Haley, ed. Centre for the Study of
Animal Welfare, Guelph, Ontario, Canada.
Reiter, K., and W. Bessei. 1998a. Einfluss der Laufaktivität auf
die Knochenentwicklung und Beinshäden bei Broilern. Arch.
Geflügelkd. 62:247–253.
Reiter, K., and W. Bessei. 1998b. Möglichkeiten zur Verringerung
von Beinschäden bei Broilern und Puten (Übersicht). Arch.
Geflügelkd. 62:145–149.
Rodenhoff, G., and K. Dammrich. 1971. Effect of breeding and
outside rearing on the skeleton of fattening cockerels. Zentralbl. Veterinärmed. Reihe A 18:297–309.
Rose, N., P. Constantin, and C. Leterrier. 1996. Sex differences in
bone growth of broiler chickens. Growth Dev. Aging 60:49–59.
Rose, S. P., M. Fielden, W. R. Foote, and P. Gardin. 1995. Sequential
feeding of whole wheat to growing broiler chickens. Br. Poult.
Sci. 36:97–111.
Sandusky, C. L., and J. L. Heath. 1988a. Effect of age, sex, and
barriers in experimental pens on muscle growth. Poult. Sci.
67:1708–1716.
Sandusky, C. L., and J. L. Heath. 1988b. Growth characteristics
of selected broiler muscles as affected by age and experimental
pen design. Poult. Sci. 67:1557–1567.
SAS. 1996. SAS-STAT Software. Version 6.12. SAS Institute Inc.,
Cary, NC.
Shalev, U., B. Robinzon, and G. Gvaryahu. 1990. The effect of
activity and exercise on behavioral and physiological parameters in male broilers. Poult. Sci. 69(Suppl. 1):121. (Abstr.)
Sherwin, C. M., P. D. Lewis, and G. C. Perry. 1999. The effects
of environmental enrichment and intermittent lighting on the
behaviour and welfare of male domestic turkeys. Appl. Anim.
Behav. Sci. 62:319–333.
Simons, P. C. M. 1986. The incidence of leg problems in broilers as
influenced by management. Pages 289–297 in 7ème Conference
Europeenne d’Aviculture. M. Larbier, ed. World’s Poultry Science Association, Paris, France.
Su, G., P. Sørensen, and S. C. Kestin. 2000. A note on the effects of
perches and litter substrate on leg weakness in broiler chickens.
Poult. Sci. 79:1259–1263.
Weeks, C. A., T. D. Danbury, H. C. Davies, P. Hunt, and S. C.
Kestin. 2000. The behaviour of chickens and its modification
by lameness. Appl. Anim. Behav. Sci. 67:111–125.
Wemelsfelder, F., and L. Birke. 1997. Environmental challenge.
Pages 35–47 in Animal Welfare. M. C. Appleby and B. O.
Hughes, ed. CAB International, Wallingford, UK.
Wilson, J. L., W. D. Weaver, Jr., W. L. Beane, and J. A. Cherry.
1984. Effects of light and feeding space on leg abnormalities
in broilers. Poult. Sci. 63:565–567.
Wilson, S., B. O. Hughes, M. C. Appleby, and S. F. Smith. 1993.
Effects of perches on trabecular bone volume in laying hens.
Res. Vet. Sci. 54:207–211.