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ANIMAL PRODUCTION |
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* ENVL, Unité de zootechnie, 69280 Marcy LEtoile;
and
INRA, Unité de Recherche sur les Herbivores, Adaptation et Comportements Sociaux, 63122 Saint Genes Champanelle, France
| Abstract |
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Key Words: farmer attitude finishing bull handling meat pH stress survey
| INTRODUCTION |
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The ability of animals to cope with stressors depends, at least in part, on their previous experience. Fear responses of animals to handling vary according to their previous experience of human contact, which in turn is influenced by farmers attitudes toward animals (for a review see Hemsworth and Coleman, 1998
), and living in a cohesive social group can lower arousal during stressful situations, especially when animals know each other from birth (Boissy and Le Neindre, 1990
).
We conducted a survey to assess the impact of the conditions of transfer to slaughter (duration of journey, waiting time at lairage, mixing of animals, etc.) and the previous living conditions of the animals (mixing, previous transport, farmers attitudes) on bulls reactions to transfer and on meat quality. Bulls were transported and slaughtered under commercial conditions, enabling us to survey a wide range of contexts. Reactions of bulls were evaluated through their behavior at loading and unloading and their blood cortisol concentration at slaughter. Meat quality was assessed through its pH.
| MATERIALS AND METHODS |
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A survey was conducted on 61 transfers of bulls by road from commercial finishing units to a slaughter plant in June and July 2004. A total of 1,202 bulls from 108 farms affiliated with the same beef producers organization (CIALYN; Coopérative Interdépartementale de lAube, du Loiret, de lYonne et de la Nièvre) based in the center of France were observed. Some observations were missed because the data were collected under commercial conditions.
All bulls had been loose-housed and fed with a complete ration (beet pulp and concentrates) during finishing. They were transported by truck to the slaughter plant when they were 17.3 ± 1.5 mo old. Mountings were prevented in all trucks by the low height of the compartments. All bulls were slaughtered in the same commercial slaughter plant, which was affiliated with the beef producers organization. Bulls arriving at the slaughter plant were led through a corridor, which was equipped with a restrainer to prevent mounting, to individual stalls, where they stayed before being slaughtered. They were not fed at the slaughter plant, but they did receive water ad libitum.
Data Collected
On Farms. Interviews with farmers and observations of bulls were conducted on farms. Farmers were asked to answer a written questionnaire consisting of 11 questions and aimed at broadly assessing their attitudes toward bulls and working with bulls. These questions were: how do you enjoy feeding bulls/observing bulls/taking care of bulls at their arrival at the finishing unit?; do you agree that bulls are sensitive to feeding schedules/bulls are sensitive to gentle human contacts/bulls are able to recognize several persons/it is difficult to work with bulls?; how often do you observe/speak to/touch/or name your bulls? Farmers were asked to give their opinion on each statement by marking a cross on a 10-cm horizontal scale, in which the left and right ends referred to unpleasant and very pleasant for the first 3 questions; strongly disagree and strongly agree for the 4 following questions; and never and always for the last 4 questions. Distances were measured from the left end of the scale. Farmers were also asked to give information on the type of farm [a breeder-finisher unit (i.e., a unit that produces and finishes calves) vs. a specialized finisher unit (i.e., a unit that finishes only bulls purchased at weaning)], the presence of a corridor or a ramp to lead animals from their finishing pen to the truck, and the distance from the pen to the truck. The questionnaire was completed by 88 farmers (81%), giving results for 1,073 bulls (89%).
Farm records were analyzed to obtain information on each bull, including its origin (animal from a different breeding farm that was transported to the finishing unit vs. animal staying in the same farm from rearing to finishing); whether it had been mixed with unfamiliar bulls at the beginning of finishing, during the finishing period, or before loading into the truck for transport to slaughter; the size of its group at the beginning of finishing; and the number of bulls left in the finishing pen after the target bull was loaded in the truck. Complete records for these variables were obtained for 1,000 bulls (83%).
Drivers were asked to record the frequency of the following events during loading of bulls into the truck: human interventions for pushing bulls with an object (stick, electric prod); bulls falling down; bulls turning back; and the number of attempts needed to successfully load all of the bulls into the truck. Drivers were also asked to note the time needed to load the animals; the number of bulls loaded; the exact time when the animals were all in the truck (i.e., the departure time); and to give their perception of the loading in terms of 1) the nervousness of the bulls (i.e., calmed, nervous, or very nervous) and ease of loading compared with other loadings, 2) during the same journey, and 3) during journeys in general (easier, similar, or more difficult than average). Their perceptions were further scored and added to give a global perception score of loading (described later). Complete information on loading was obtained on 102 loadings, giving results for 715 bulls (59%).
During the Journey. A technician completed records on the actual transport when the truck arrived at the slaughter plant. The technician recorded the exact arrival time of the truck, and calculated the duration of transport. The technician noted the position of each bull in the various compartments of the truck. This information was used to calculate the number of bulls, the number of familiar bulls (i.e., those originating from the same finishing group), and the mixing of bulls from different finishing units within the compartment. Complete records were obtained for 1,114 bulls (93%).
The technician asked the driver if he had stopped in other farms to load new bulls and noted the name of the driver and the truck used. Complete records were obtained for 1,166 bulls (97%).
Data on the weather (temperature and wind) were extracted from Météo France weather center records (local Yonne center, 89000 Saint Georges sur Baulche). Data were obtained for all transports.
The length of time that the bulls stayed in the truck after arrival at the slaughter plant was noted for all bulls. The bulls were then observed by the same unique observer during unloading from the truck to the slaughter plant restrainer. The frequency of the same variables as for loading was noted: human interventions for pushing bulls with an object (stick, electric prod), bulls falling down, bulls turning back, and the number of attempts needed to successfully unload all bulls from the truck. The observer also noted his perception of the unloading (as was done for loading) and the time taken to unload all bulls. Observations were obtained for 1,171 bulls (97%). The time between unloading of a bull and its slaughter was recorded for all the bulls.
At Slaughter. Carcass weight and age of bulls at slaughter were extracted from the records of the slaughter plant for 1,073 bulls (89%).
Blood samples were collected into heparinized plasma separator tubes (Vacutainer LH PST 2, BD, Plymouth, UK). Blood samples were taken from the jugular vein during the poststunning bleeding of 1,000 bulls (83%). They were centrifuged at 3,000 x g for 10 min, and the plasma was stored at 20° C until determination of cortisol concentrations. Cortisol concentrations were determined using solid-phase extraction and high-pressure liquid chromatography with UV absorbance detection (242 nm; Hay and Mormède, 1997
). The detection limit was 0.76 ng/mL, and the quantification limit was 2.8 ng/mL. Both within- and between-assay CV were 17.5% for a control sample (22 ng/mL).
Meat pH was measured in the LM of 891 carcasses (74%) between 19 and 24 h after slaughter. The ultimate pH of LM is generally used to assess carcass quality (Monin, 1998
). It was not possible to measure the pH of the LM at a precise time after slaughter because some carcasses were cut the first day after slaughter and no sample could be taken from this muscle for marketing-related reasons. We also measured pH in the rectus abdominis (RA) muscles that we were able to excise from 821 carcasses between 20 and 24 h after slaughter, and the samples were stored at 4° C until determination of the pH at 30 h after slaughter. This second muscle was chosen because it contains many oxidative slow-contracting fibers that may be prone to dark-cutting as a result of emotional reactions (Gire and Monin, 1979
; Pinkas et al., 1982
). The pH of these muscles was measured using an ISFET silicon probe and a portable pH meter (IQ 200; IQ Scientific Instruments, Carlsbad, CA).
Data Analyses
Statistical analyses were conducted using SAS (Version 8.1, SAS Inst., Inc., Cary, NC).
Preliminary Calculations. The frequency of all events recorded during loading and the time needed to load the bulls into the truck were divided by the number of bulls loaded. The perception score of loading was the sum of the 3 scores given by the drivers, where calm bulls and an easier than average loading was scored as 1, nervous bulls and a similar to average loading scored a 2, and very nervous bulls and a more difficult than average loading scored a 3. Data on unloading were transformed in the same way.
Principal component analyses were conducted to obtain synthetic variates describing loading and unloading (Coleman et al., 1998
). Only axes with an eigenvalue greater than 1 were kept for further analyses. To interpret these axes, we took into account the variables with an eigenvector greater than 0.3.
The principal component analysis run on the loading of bulls gave 1 axis with an eigenvalue of 3.1 and accounted for 52% of the variability in the initial variables. The eigenvectors of variables on the axis were: frequency of bulls turning back, 0.53; attempts to successfully load the bulls, 0.51; perception score, 0.42; human interventions, 0.42; and time needed to load, 0.30. This axis is hereafter labeled loading score. A high loading score indicated that loading was difficult.
The principal component analysis run on the unloading of bulls gave 1 axis with an eigenvalue of 2.5 and accounted for 41% of the variability in the initial variables. The eigenvectors of variables on this axis were: frequency of bulls turning back, 0.53; perception score, 0.51; human interventions, 0.47; and attempts to successfully unload the bulls, 0.46. This axis is labeled unloading score. A high unloading score indicated that unloading was difficult.
Analysis of the Relationships Between Components. Each bull was considered as 1 statistical unit because each of them represented a specific combination of factors (age, mixing, conditions for transfer, etc.). The path analysis method, which is a multiple regression that enables a time sequence to be entered into the analysis, was used.
Data collected on farms (concerning bulls, farmers attitudes, and farm structures), carcass weight (considered highly correlated with BW of the bulls), and age of the bulls were used as regressors for analysis of the loading score. These elements plus loading score, information collected on transport, and the length of time the bulls waited in the truck at the slaughter plant were used as regressors for analysis of unloading score. All of these elements plus unloading score and the length of time that the bulls stayed at lairage at the slaughter plant were used as regressors for analysis of blood cortisol at slaughter. Finally, blood cortisol results were included for the analyses of meat pH.
For regression analyses, qualitative variables with 2 alternatives (no/yes) were converted to binary variables with 2 possible values (0/1). For qualitative variables with more than 2 possible classes (drivers, n = 12; trucks, n = 5), the mean values of meat pH and blood cortisol at slaughter were calculated for the different classes. Classes were then ranked from the one that resulted in the lower pH/mean cortisol to the one that resulted in the greater pH/mean cortisol. Ranks were then used in the regression analyses.
For regression, the stepwise procedure was used (Chesterton et al., 1989
). Explanatory variables were progressively introduced, the best predictor being first to enter the regression equation. Variables associated with a P-value smaller than or equal to 0.10 were included. Variables were excluded if their P-value exceeded 0.05 after the later variables had been introduced. The results are expressed in terms of regression coefficients (ß) and their standard errors (SE[ß]), the proportions of the variability explained (R2), and the probability (P). All significant results are shown in tables, but only variables or associations of variables that accounted for more than 4% of the variability are discussed in the text.
| RESULTS |
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Results of the regression analysis of loading into the truck at departure from the farm are shown in Table 4
. Loading depended essentially on the farm equipment installed to lead animals to the truck (R2 = 40.3%). The loading of bulls into the truck was more difficult on farms not equipped with a corridor or a ramp for leading bulls to the truck. Loading was also more difficult when farmers enjoyed observing bulls, reported frequent contacts with the bulls, and when they believed that bulls are able to recognize several persons (R2 = 7.38% for attitude variables taken together).
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Results of the regression analysis of the unloading of bulls on arrival at the slaughter plant are shown in Table 5
. Unloading was more difficult when the temperature was lower (R2 = 11.4%) and when transfer from the finishing unit to the slaughter plant was longer (R2 = 6.17%). Unloading also depended on the truck (R2 = 7.29%). Moreover, unloading was more difficult when bulls had been mixed immediately before loading into the truck for transport (R2 = 4.24%). Lastly, unloading was more difficult when the farmer reported frequently naming the bulls but speaking rarely to them, when he believed that bulls are not sensitive to feeding schedules (R2 = 11.77% for attitude variables taken together).
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Results of the regression analysis of the blood cortisol concentrations at slaughter are presented in Table 6
. Cortisol concentrations were greater when the farmer believed that bulls are sensitive to feeding schedules but not sensitive to gentle human contacts, and when the farmer enjoyed taking care of bulls at their arrival at the finishing unit (R2 = 15.73% for attitude variables taken together). Cortisol concentrations increased with the number of bulls left in the finishing pen after loading of the target bulls into the truck (R2 = 4.01%).
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Results of the regression analysis of the pH of the LM are shown in Table 7
. The greater the temperature on arrival of the truck at the slaughterhouse, the greater the pH of the LM (R2 = 7.99%). The pH of the LM was also greater when the farmer enjoyed taking care of bulls on their arrival at the finishing unit but did not enjoy feeding them, and when the farmer believed that bulls are not sensitive to feeding schedules (R2 = 6.20% for attitude variables taken together).
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Results of the regression analysis of the pH of the RA are presented in Table 8
. Rectus abdominis pH was greater when bulls waited for a short time in the slaughter plant (R2 = 6.79%) and when they had been mixed during finishing (R2 = 4.83%). Rectus abdominis pH was also greater when the farmer believed that bulls are not sensitive to feeding schedules and when he did not enjoy feeding them (R2 = 4.79% for attitude variables taken together).
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| DISCUSSION |
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Transfer to slaughter begins by loading bulls into the truck. We found that loading was easier on farms equipped with a corridor or a loading ramp (R2 = 40.3%), which is in accordance with previous recommendations for the handling of animals (Grandin, 1990
; Lapworth, 1990
).
Loading was also linked to farmers attitudes (R2 = 7.38%). Loading was more difficult when the farmer reported that he enjoyed observing bulls and that he touched them often. A farmer with such positive attitudes is likely to spend more time close to the bulls. In pigs and calves, gentle contacts reduce animals fear responses to humans (pigs: Hemsworth and Barnett, 1991
; Hemsworth et al., 1986
; calves: Lensink et al., 2000
, 2001
), whereas handlers of large animals such as beef bulls usually take advantage of the animals flight zone to direct them to a specific area (Grandin, 2000
, Broom, 2003
). In bulls, too many contacts with humans may render them too familiar of people and not at all afraid of them, which in turn might make them more difficult to handle. This hypothesis is supported by previous results obtained in pigs (Day et al., 2002
) and heifers (Breuer et al., 2003
) where positively handled animals were found to be more difficult to move. In contrast, loading was easier when the farmer believed that bulls are able to recognize several persons. Such a belief might reflect a better understanding of cattle behavior, making the farmer more skilled in using the animals spontaneous behavior (such as flight distance) to move them to the truck. Results suggest that loading is affected by loading facilities on farms and by farmers attitudes. Handling seems more efficient when farmers do not have attitudes that may render beef bulls familiar with them.
Unloading of bulls from the truck was not affected by the same factors as loading. Unloading was influenced by the truck in which bulls were transported (R2 = 7.29%). Moreover, unloading was easier when the journey was short (R2 = 6.17%) and when the local temperature was high (R2 = 11.4%). First, long journeys give cattle the opportunity to acclimatize (Tarrant et al., 1992
; Gregory and Grandin, 1998
; Honkavaar et al., 2003
), probably because as the journey progresses, the environment inside the truck becomes less novel and thus less stressful. Second, during the journey, discomfort due to heat is stressful (Hartung et al., 2003
). Short transport and heat are likely to result in animals being more disturbed in the truck and probably more ready to get out of it when they arrive at the slaughter plant, thus making unloading easier. Hence, unloading seems to depend largely on the journey itself. Nevertheless, unloading was also influenced by farmers attitudes (R2 = 11.77%). Unloading at the slaughter plant proved easier when the farmer had overall positive attitudes toward his bulls (naming them or speaking to them often and believing that bulls are sensitive to feeding schedules). It is difficult to put forward a firm conclusion on a causal relationship between farmers attitudes and difficulty in unloading bulls. It could be argued that farmers believing that bulls are sensitive to feeding schedule and who often interact orally with their bulls provide the bulls with a quieter and more predictable environment. Thereafter, animals could be more disturbed by the journey, which would represent a greater change from their usual environment, and thus be still more ready to get out of the truck. Lastly, beef bulls that have been mixed immediately before loading appear to be more difficult to unload from the truck (R2 = 4.24%). Mixing induces aggressions between cattle and also mounting in males (for review see Bouissou et al., 2001
). During the journey, confinement in the truck limits interactions between animals, which may make them more excitable when the doors of the truck are opened, rendering unloading more difficult. However, this hypothesis requires thorough observations of interactions between bulls at unloading before a firm conclusion can be put forward. Thus, our results suggest that at unloading, bulls seem more ready to leave the truck when they have been more disturbed by the journey, whereas social interactions between animals that have been mixed immediately before the journey would make unloading more difficult.
At the precise moment of slaughter, cortisol concentrations in the blood of the bulls that we observed were around 21 ng/mL. This value is above basal values generally measured in this type of animals (e.g., around 5 ± 1 ng/mL in Ladewig and Smidt, 1989
), suggesting a moderate stress reaction as in cattle exposed to an open-field test (Veissier and Le Neindre, 1988
). Blood cortisol concentrations increase during the minutes after a stressful event and return to baseline about 1 h after the end of that event (Dantzer and Mormede, 1979
; Veissier and Le Neindre, 1988
). In this study, average lairage before slaughter was 12 h. Hence, blood cortisol concentrations measured during the bleeding probably reflected the way animals reacted to being at lairage or to the final handling before slaughter, or both, rather than their reaction to earlier events during transfer (loading, journey, unloading). Nevertheless, we cannot rule out that the journey had an effect on the level of stress at slaughter. Blood cortisol concentrations were greater when the farmer enjoyed taking care of his bulls and believed that they are sensitive to feeding schedules (R2 = 6.15%). As suggested earlier for the journey, the slaughter procedure may represent a greater contrast for bulls used to quietness and regularity in their environment during finishing, thereby leading to more stress. In contrast, the cortisol increase at slaughter was limited when the farmer believed that bulls are sensitive to human contacts (R2 = 9.58%). We may suppose that farmers with such attitudes could be more skilled in handling their animals and paid more attention when handling is necessary during the finishing period. Bulls were thus probably less afraid of handling, and this could attenuate the animals fear responses to humans during slaughter.
Finally, blood cortisol concentrations were lower when the majority of the finishing group was loaded, transported, and slaughtered at the same time (R2 = 4.01%). Bulls that arrived at the same time (e.g., from the same finishing pen) were housed 1 by 1 in adjacent stalls. They were thus more likely to be led to slaughter at the same time. In bulls as in other animals, the presence of familiar partners can lower stress reactions to unusual events (pigs: Hayne and Gonyou, 2003
; monkeys: Hennessy et al., 1982
; bulls: Mounier et al., 2005; heifers: Veissier and Le Neindre, 1992
). In our study, the calming role of the familiar partners at slaughter could have been effective. Results therefore suggest that bulls are more stressed during slaughter when they have been separated from their usual social partners before arrival at the slaughter plant. They also suggest that the bulls are probably more stressed at slaughter when the environment represents a major contrast with their previous environment, which may depend notably on farmers attitudes.
The main problem resulting from transfer of bulls to slaughter is DFD meat characterized by a high pH. In our survey, 2 factors similarly influenced pH of the 2 muscles studied. First, the pH of these muscles was lower when waiting time at lairage was longer (R2 = 6.79% for RA and 2.43% for LM). The major influence of preslaughter handling on lean meat quality is through depletion of muscle glycogen content that limits the extent of muscle/meat acidification. This results as much from emotional stress as from physical exhaustion (Warriss, 1990
). Glycogen resources can be restored at lairage, and bulls can recover from physical exhaustion even if they are not fed (Warriss et al., 1984
). Knowles (1999)
suggested that a 24-h period at lairage is necessary for adequate behavioral and physiological recovery. This recovery is not observed when unfamiliar animals are mixed at lairage (Price and Tennessen, 1981
; Kenny and Tarrant, 1987a
). Indeed, animals maintained in individual pens before slaughter produce 4 or 5 times less dark-cutting carcasses than bulls kept in pairs (Matzke et al., 1985
). In our study, bulls stayed between 20 min and 48 h at lairage where they were housed in individual stalls. Muscle glycogen content could therefore increase with waiting time, leading to a lower meat pH. More precisely, 3 main waiting times were recorded in our study: bulls waited at lairage for about 1, 17, or 40 h before slaughter, and pH decreased accordingly. A pH greater than 6 was observed for some bulls that waited for 1 or 17 h but not for the bulls that waited 40 h. It would appear that bulls should stay at lairage more than 17 h to avoid DFD meat. Nevertheless, our data do not enable us to recommend a specific waiting time.
Second, meat pH varied inversely with farmers believing that bulls are sensitive to feeding schedules and with farmer enjoyment in feeding bulls (R2 = 4.79% for RA and 3.53% for LM). Depletion of glycogen reserves depends on feeding of animals before transport (Hartung et al., 2003
; Marahrens et al., 2003
). A highly energetic diet seemed to protect cattle from potentially glycogen-depleting stressors (Immonen et al., 2000
). Farmers who place more importance on feeding may provide feed to the bulls before transfer, helping them to better withstand the physical aspects of transfer, whereas other farmers may avoid feeding an animal before transfer because it will not benefit from the feed in terms of putting on more BW. The former may also provide animals with a more energetic diet throughout finishing, increasing their greater glycogen content. Our results lend support to the importance of feeding bulls up to their transfer to slaughter.
The pH of both muscles was influenced differentially by other factors. The pH of LM was lower when the temperature during journey was lower (R2 = 7.99%). This result is in accordance with the literature (Fabiansson et al., 1984
; Scanga et al., 1998
; Hartung et al., 2003
). During our survey, the external temperature was high (18° C on average, with peaks at 30° C), and we can suppose that when the temperature was above 18° C, the journey was physically demanding for the bulls. The decline in pH in the LM was also more pronounced when the farmer did not enjoy taking care of the bulls (R2 = 2.67%). As suggested earlier (see results on unloading and cortisol), animals that normally receive a lot of care from their farmer may be more stressed at slaughter due to a larger contrast with the previous environment.
The pH of RA was lower when bulls had not been mixed during finishing (R2 = 4.83%). This is probably due to the calming effect of the social group reducing the emotional stress during transfer to slaughter, as was also observed through cortisol concentrations at bleeding (see previously).
In view of our results, LM pH seems more influenced by physical aspects (including temperature), whereas RA pH seems more influenced by emotional aspects (that may be reduced by familiar partners). In lambs, fast fibers are more abundant in the LM, whereas low fibers are more abundant in the RA (Gire and Monin, 1979
; Pinkas et al., 1982
). Our results support previous findings that fast fibers are prone to dark-cutting due to physical constraints, whereas low fibers are prone to dark-cutting due to psychological constraints (Lacourt, 1985
).
Although some of our results suggest that meat pH is affected by stress, we did not find evidence of a link between blood cortisol at the exact moment of slaughter and meat pH. This lack of a link is probably due to the kinetics of cortisol responses. Cortisol concentrations that we measured could not reflect events that occurred several hours previously or during the very last minutes before slaughter. A follow-up of physiological responses of animals during the whole transfer would be necessary to understand what part of the transfer is the most stressful and most affects meat pH. This could be done by monitoring animal heart rate, as reported in calves by Lensink et al. (2001)
. Such heart monitoring could not be undertaken in our study.
The conclusions of this study are drawn from the association between factors. In most cases, one factor occurred before another one (e.g., mixing before loading), suggesting a causal link. In other cases, like for attitudes of the farmer, it is more likely that a factor not measured in this survey (e.g., the behavior of the farmer) was the cause of the effects observed. However, in any case, such causality remains to be examined in controlled conditions. Thus, in conclusion, appropriate equipment (loading ramp) should be used to load animals into the truck. Whereas a positive attitude toward the sensitivity of animals should be promoted, close contacts with bulls should be limited to facilitate later animal handling. Groups of bulls should be maintained throughout finishing and for transfer to slaughter. Transport of animals on warm days should be avoided.
| Footnotes |
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2 Corresponding author: l.mounier{at}vet-lyon.fr
Received for publication April 26, 2005. Accepted for publication December 14, 2005.
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