don 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 ...
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.
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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
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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
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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.
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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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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. Geflu¨gelkd. 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. Geflu¨gelkd. 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 Laufaktivita¨t auf die Knochenentwicklung und Beinsha¨den bei Broilern. Arch. Geflu¨gelkd. 62:247–253. Reiter, K., and W. Bessei. 1998b. Mo¨glichkeiten zur Verringerung ¨ bersicht). Arch. von Beinscha¨den bei Broilern und Puten (U Geflu¨gelkd. 62:145–149. Rodenhoff, G., and K. Dammrich. 1971. Effect of breeding and outside rearing on the skeleton of fattening cockerels. Zentralbl. Veterina¨rmed. 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 7e`me 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.
