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GENETICS |
Departamento de Mejora Genética Animal, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Apartado 8.111, 28080 Madrid, Spain
1 Corresponding author: jlcampo{at}inia.es
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: housing system • cold stress • heterophil-to-lymphocyte ratio • fluctuating asymmetry • tonic immobility
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Heterophil-to-lymphocyte ratio, fluctuating asymmetry, and duration of tonic immobility may be used as criteria for measuring levels of stress, welfare, and fear in chickens (Gallup, 1979; Gross and Siegel, 1983; Parsons, 1990). Studies on the effect of housing system on these criteria are very scarce and only have compared the tonic immobility duration of hens housed in cages or on litter. Adult White Leghorn hens housed in cages showed significantly longer durations of tonic immobility than those housed in floor pens (Jones and Faure, 1981a; Kujiyat et al., 1983). Hansen et al. (1993) did not find significant differences in tonic immobility duration between White Leghorn hens housed in cages and in aviaries at 30 wk of age, although hens in cages showed tonic immobility of longer duration than hens in aviaries at 70 wk of age.
On the other hand, although the degree to which animals suffer when experiencing cold stress is unknown (Curtis and Stricklin, 1991), Hangalapura et al. (2004b) indicated that during the winter season, thermoregulation in homeotherms is an important energy-demanding process and may be a constraint to immune function. They concluded that the phagocytes of the immune system responded immediately to cold stress. On the contrary, Hangalapura et al. (2003, 2004a) found that antibody responses of chickens were not significantly affected by cold stress. Studies on the effect of cold stress on those criteria of stress, welfare, and fear are lacking, too. Hester et al. (1996) found that caged hens exposed to a cold environment (0°C for 72 h) had higher heterophil-to-lymphocyte ratios than those of the control environment. Yalcin and Siegel (2003) found that relative asymmetry of wing, shank, tibia, and femur lengths increased in broiler embryos exposed to cooling. Campo and Carnicer (1994) found that the effect of cold stress (1°C for 24 h) on tonic immobility duration varied from breed to breed, the difference between treatments (cold stress vs. control) being significant in a breed (Red-Barred Vasca).
The purpose of the present study was to analyze the effects of housing system (litter pens with or without access to an outdoor area) and a cold stress on the heterophil-to-lymphocyte ratio, the fluctuating asymmetry, and the tonic immobility duration of different breeds of chickens. It would be hypothesized that housing in litter pens with access to an outdoor area would decrease the stress and fear levels of birds, whereas a cold stress would increase them. As far as the authors know, the relationships between the outdoor or indoor housing systems and the heterophil-to-lymphocyte ratio, the fluctuating asymmetry, or the tonic immobility duration have not been studied yet, whereas the relationship between a cold stress and these criteria of stress and welfare has only been studied in 1 experiment each (Campo and Carnicer, 1994; Hester et al., 1996; Yalcin and Siegel, 2003). Duration of tonic immobility was not measured in the second experiment, because it had been previously analyzed by Campo and Carnicer (1994).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Birds were reared with a density of 10 birds/m2 until 8 wk of age (sexes mixed). Artificial light was only provided during the first week of age (23L:1D). Temperature was controlled with gas heaters (33 to 35°C at the chick level during the first week followed by a reduction of 3°C each week until to reach 18 to 20°C in the sixth week of age). Birds were moved to another all-litter house and reared with a density of 6 birds/m2 from 8 to 20 wk of age. The lighting regimen was 8L:16D. Birds were fed standard rearing diets containing 19% CP, 2,800 kcal of ME/kg, 1% Ca, and 0.5% available P until 8 wk and 15% CP, 2,700 kcal of ME/kg, 0.9% Ca, and 0.4% available P until 20 wk.
Two different replicates (hatches) separated by 14 d were used in experiments 1 and 2. Hatches were made in April 12 and April 26 (experiment 1) and in June 14 and June 28 (experiment 2). A total of 120 hens was used in experiment 1 (housing system), to study the effect of the housing system on the heterophil-to-lymphocyte ratio, the fluctuating asymmetry, and the tonic immobility duration at 36 wk of age. Birds were housed at 20 wk of age in pens with a raised slatted floor covering a dropping pit and straw litter on the rest of the floor; the slatted area occupied one-third of the floor. Bird density was 4 birds/m2. Birds were fed a diet containing 16% CP, 2,700 kcal of ME/kg, 3.5% Ca, and 0.5% available P. Feed and water were supplied for ad libitum consumption. The room temperature was 16 to 20°C. Feeders, drinkers, and nest boxes were in the slatted floor area. Two housing systems (deep litter and free range) without any differences in the construction were used in this experiment; birds in the free-range system had access to an outdoor area providing 4 m2 per bird. The birds were equally divided into 2 groups. Group 1 consisted of 60 birds (randomly selected), 10 birds of each population in 2 replicates of 5 birds, housed in deep litter. Group 2 consisted of 60 additional birds (randomly selected), 10 birds of each population in 2 replicates of 5 birds, housed in the free-range system.
Similarly, a total of 120 cocks was used in experiment 2 (temperature effect), to study the effect of a cold stress on the heterophil-to-lymphocyte ratio, the fluctuating asymmetry, and the tonic immobility duration at 36 wk of age. Birds were housed at 24 wk of age in cages; bird density was 8 birds/m2. The birds were equally divided into 2 groups. Group 1 consisted of 60 birds (randomly selected), 10 birds of each population in 2 replicates of 5 birds, kept in cages with a cold stress for 12 wk, temperature being 0 to 10°C. Group 2 consisted of 60 additional birds (randomly selected), 10 birds of each population in 2 replicates of 5 birds, kept in cages without a cold stress (control), the room temperature being 16 to 20°C.
On 2 different days, birds were tested for heterophil-to-lymphocyte ratio and tonic immobility duration at 36 wk of age. To obtain the heterophil-to-lymphocyte ratio, hens were carried to a separate room, and blood was collected immediately. Two drops of blood were taken from a small puncture in the comb of each bird, 1 drop being smeared on each of 2 glass slides. The smears were stained using May-Grünwald and Giemsa stains (Lucas and Jamroz, 1961), approximately 2 to 4 h after methyl alcohol fixation. One hundred leukocytes, including granular (heterophils, eosinophils, and basophils) and nongranular (lymphocytes and monocytes), were counted on 1 slide of each bird (the other slide was supplementary), and the heterophil-to-lymphocyte ratio was calculated. Square root transformation was used before analysis.
All hens were tested for tonic immobility in a separate room on the day after the blood sampling. Tonic immobility was induced, as soon as a hen was caught, by placing the animal on its back with the head hanging in a U-shaped wooden cradle (Jones and Faure, 1981b). The bird was restrained for 10 s. The observer sat in full view of the bird, about 1 m away, and fixed his eyes on the bird because of the fear-inducing properties of eye contact. If the bird remained immobile for 10 s after the experimenter removed his hands, a stopwatch was started to record latencies (s) until the bird righted itself. If the bird righted itself in less than 10 s, then it was considered that tonic immobility had not been induced, and the restraint procedure was repeated (3 times maximum). If the bird did not show a righting response over the 10-min test period, a maximum score of 600 s was given for righting time. Thus, tonic immobility duration ranged from 0 to 600 s. Logarithmic transformation was used before analysis.
The morphological traits (measured on the same day as the blood sampling) were both right (R) and left (L) middle toe length, leg (metatarsus) length, wing (radius) length, wattle length, and leg width. Right and left values of an animal were taken during the same session. All 4 lengths and leg width were measured in millimeters using a digital calliper. Trait size was the mean of the right and left traits [(R + L)/2]. All traits showed normal frequency distributions. The fluctuating asymmetry for a trait was defined by the absolute difference between sides [|R – L|], equivalent to the mean deviation. A series of steps (Palmer, 1994; Knierim et al., 2007) was followed before identifying exhibited asymmetry as fluctuating asymmetry (normal distribution of signed right minus left differences with a mean of zero), because there are several confounding factors that complicate the analysis of asymmetry: different types of bilateral asymmetry (fluctuating asymmetry, directional asymmetry, and antisymmetry), measurement error, and relation between fluctuating asymmetry and trait size (details can be found in Campo et al., 2008). Relative fluctuating asymmetry was used for all traits [2|R – L|/(R + L)]; it had distributions that were not normal and were transformed to arc sin square root before analysis. Mean relative asymmetry was defined as the mean of the relative asymmetries of the different traits.
To test the differences in heterophil-to-lymphocyte ratio, fluctuating asymmetry, and tonic immobility duration between treatments, a 3-way ANOVA (Sokal and Rohlf, 1981) was used with the statistical model xijkl = µ + Ti + Bj + TBij + rk + Trik + Brjk + TBrijk + 
ijkl, where xijkl = the analyzed measurement; µ = the overall mean; Ti = the effect of treatment (deep-litter vs. free-range housing in experiment 1 and cold stress vs. control in experiment 2); Bj = the effect of breed (j = 1 ... 6); rk = the effect of replicate (k = 1 ... 2); TBij, Trik, Brjk, and TBrijk = the interactions; and ijkl = the residual (l = 1 ... 5). Treatment and breed were considered fixed effects, and replicates were assumed to be a random effect. Significant differences among breeds were estimated using the Student-Newman-Keuls multiple-range test (Snedecor and Cochran, 1980).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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ijk). Because housing system x breed interaction was significant for heterophil-to-lymphocyte ratio (P < 0.05), heterophil number (P < 0.05), and lymphocyte number (P < 0.05), subclass means are summarized in Table 1
. The effects of housing system on heterophil-to-lymphocyte ratio, heterophil number, and lymphocyte number varied from breed to breed, differences between housing systems being significant in 2 breeds (Red-Barred Vasca and Birchen Leonesa). In these breeds, heterophil-to-lymphocyte ratio and heterophil number were significantly greater in hens housed in deep litter and smaller in free-ranged hens, with the opposite being true for lymphocyte number. In the deep-litter group of hens, there were no significant differences among breeds in terms of heterophil-to-lymphocyte ratio, although the Black Menorca breed had significant smaller heterophil number and greater lymphocyte number than the other 5 breeds. There were no significant differences among breeds in terms of heterophil-to-lymphocyte ratio, heterophil number, and lymphocyte number in the free-range group of hens.
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differed from those calculated with the presented means for heterophils and lymphocytes (0.64, 0.35, etc.) due to the effect of variance and covariance on the value of the ratio: H/L = mH/mL + 2mHs2L/mL3– sHL/mL2, where mH and mL = the mean values of the numerator and denominator; sHL = the covariance between them; and s2L = the variance of the denominator.
Mean values indicating the effect of the housing system and breed on relative asymmetry measurements are summarized in Table 2. Housing effect was significant for the relative asymmetry of leg length (P < 0.01), wattle length (P < 0.05), and the combined relative asymmetry of the 5 measurements (P < 0.05). The relative asymmetry of birds housed in deep litter was larger than that of birds housed in free range. Housing effect was not significant for the relative asymmetry of toe length, wing length, and leg width, although all asymmetry measurements, whether significant or not, point in the same direction, birds housed in deep litter having the most asymmetrical toes, legs, wings, and wattles. Breed effect and treatment x breed interaction were not significant for any measurement.
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). There were significant differences among breeds (P < 0.001), birds from the Red Villafranquina breed having longer tonic immobility duration, with tonic immobility of birds from the White-Faced Spanish breed being shorter. Treatment x breed interaction was not significant.
Cold x breed interaction was significant for heterophil-to-lymphocyte ratio (P < 0.05) and heterophil number (P < 0.05), subclass means being summarized in Table 3. The effects of cold stress on heterophil-to-lymphocyte ratio and heterophil number varied from breed to breed, differences between cold-stressed and control birds being significant in 2 breeds (Red-Barred Vasca and Buff Prat). In these breeds, heterophil-to-lymphocyte ratio and heterophil number were significantly greater in cold-stressed birds and smaller in control birds. There were significant differences among breeds in terms of heterophil-to-lymphocyte ratio and heterophil number, in the cold-stressed and the control group of birds. Ratio and heterophil number were significantly greater in the Red-Barred Vasca breed and smaller in the White Leghorn population in the cold-stressed group, whereas the Quail Castellana breed had significant greater heterophil-to-lymphocyte ratio and heterophil number than the other 5 breeds in the control group. Cold x breed interaction was not significant for lymphocyte number. There was a significant difference between treatments for lymphocyte number (P < 0.01), with lymphocytes of birds with cold stress being higher than that of control birds (Table 4). There were significant differences among breeds in terms of lymphocyte number (P < 0.05). Lymphocyte number was significantly smaller in the Quail Castellana breed and greater in the White Leghorn population and the Buff Prat breed.
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. Cold stress effect was significant for the relative asymmetry of toe length (P < 0.001) and the combined relative asymmetry of the 5 measurements (P < 0.05). The relative asymmetry of birds with cold stress was larger than that of control birds. Cold effect was not significant for the relative asymmetry of leg length, wing length, wattle length, and leg width, although all asymmetry measurements, whether significant or not, point in the same direction, cold-stressed birds having the most asymmetrical toes, legs, wings, and wattles. Breed effect and treatment x breed interaction were not significant for any measurement. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The no significant housing effect on tonic immobility duration found in the current study at 36 wk of age agrees with the results reported by Hansen et al. (1993), who found that the duration of the tonic immobility response was unaffected by type of system in White Leghorn hens at 30 wk of age housed in cages and in aviaries, suggesting that the fearfulness is similar in both types of housing. Similarly, Weeks et al. (1993) found few differences in the behavior of broiler chickens housed in indoor and free-range environments, although it should be expected that chickens in an outdoor system performed more behavioral repertoire and suffered less from stress.
As expected in experiment 2, the cold stress significantly affected heterophil-to-lymphocyte ratio and fluctuating asymmetry. Cold-stressed birds had the heterophil-to-lymphocyte ratio significantly higher, more than 50% in the Buff Prat and more than 2x in the Red-Barred Vasca, than control birds without cold stress, cold-stressed birds from these breeds having significant greater heterophil number (heterophilia); lymphocyte number was significantly smaller (lymphopenia) in cold-stressed birds from all 6 breeds. This was in agreement with the result reported by Hangalapura et al. (2004a), who found a significant enhancing effect of cold stress (10°C for 7 d) on in vitro lymphocyte proliferation. With respect to the heterophil-to-lymphocyte ratio, Hester et al. (1996) also found that caged White Leghorn hens exposed to a cold environment had higher heterophil-to-lymphocyte ratios than those of the control hens (39.5 vs. 37.6). In relation to plasma corticosterone concentration (another stress indicator), Buckland et al. (1974) reported that the application of cold stress resulted in significant increases in plasma corticosterone levels in chicks, and Hester et al. (1996) found that caged hens exposed to a cold environment (0°C for 72 h) had higher plasma corticosterone levels than those of the control environment (39.5 vs. 37.6). In disagreement with these results, Hangalapura et al. (2004a) found a significant suppressive effect of cold stress (10°C for 7 d) on plasma corticosterone levels.
The significant cold x breed interaction for heterophil-to-lymphocyte ratio suggests that, depending on the genotype, the animals respond differently to different temperatures. A similar cold x breed interaction was found by Campo and Carnicer (1994) for the tonic immobility duration of several Spanish breeds of chickens including the Red-Barred Vasca, the Black Castellana, and the Buff Prat. In all 3 breeds, cold stress decreased the duration of tonic immobility, significantly in the Red-Barred Vasca breed (173 vs. 349 s), in agreement with the negative correlation between heterophil-to-lymphocyte ratio and tonic immobility duration reported by Campo and Redondo (1996, 1997) and Campo et al. (2007).
Cold-stressed birds had the combined fluctuating asymmetry of morphological traits almost 15% larger than control birds without cold stress, the fluctuating asymmetry of middle toe length being more than 35% larger. This result is consistent with those found by Yalcin and Siegel (2003) in broiler embryos exposed to cooling. Relative asymmetry of wing, shank, and tibia lengths at 10 d of incubation increased in embryos exposed to cooling to 36.9°C six hours per day from 0 to 8 d of incubation, whereas the larger relative asymmetry of tibia and femur lengths at 18 d of incubation was for embryos exposed to 24 h to 21°C on d 14 of incubation, and for shank length at hatch, it was largest for embryos exposed to cooling to 36.9°C six hours per day from 10 to 18 d of incubation. Therefore, deviations from optimum environmental temperatures for chickens and embryos could contribute to larger fluctuating asymmetry of morphological traits, because cold stress results in the use of resources that could otherwise be used for developmental control.
In conclusion, results of the current study indicate that housing in deep litter with access to an outdoor area resulted in smaller heterophil-to-lymphocyte ratio and smaller fluctuating asymmetry compared with housing in deep litter without access to an outdoor area, suggesting that the housing system is associated with some measures of stress and welfare. Duration of tonic immobility was not significantly longer in the deep-litter housing, indicating that indoor vs. outdoor systems did not contribute to the fearfulness of birds. Low ambient temperatures (0 to 10°C from 24 to 36 wk of age) resulted in greater heterophil-to-lymphocyte ratios and higher fluctuating asymmetry, suggesting that a cold stress seriously negatively affects the welfare of birds. The significant housing x breed and cold x breed interactions for heterophil-to-lymphocyte ratio suggest that, depending on the genotype, the animals respond differently to different environments, the Red-Barred Vasca being more sensitive to the environment.
Received for publication November 19, 2007. Accepted for publication January 10, 2008.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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