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Do beef cattle react consistently to different handling situations?
Applied Animal Behaviour Science 71 (2001) 263±276
Do beef cattle react consistently to different handling situations? Laurence Grignard*, Xavier Boivin, Alain Boissy, Pierre Le Neindre I.N.R.A. Theix, URH-ACS, F 63122, St GeneÁs Champanelle, France Accepted 7 September 2000
Abstract Beef cattle responses to handling depend partly on the genetic characteristics of the animals. However, the various methods used in order to assess these responses differ to a great extent. The purpose of this work is to study the relationship between two different situations extensively used to evaluate cattle reactions to handling. Moreover, the genetic variability of cattle responses to these two handling situations was investigated. Behavioural reactions of 245 Limousine heifers, from 10 sires, were evaluated both in a docility test and in a crush test. In the docility test, a human tried to lead and then to maintain the animal in the corner of a pen during 30 consecutive seconds, with a maximum duration of the test of 3.5 min. A docility score summarised the animal's behavioural reactions to the test. The crush test procedure consisted of social isolation of the animal in a crush, with the head maintained in a head gate (5 min), then exposure to a stationary human (30 s), and ®nally stroking on the forehead (30 s). An agitation index for each part of this test was computed from PCA analyses based on agitation behaviours. Sire effect was signi®cant for every part of both tests (P < 0:05). Heifers' behavioural responses to the docility test were signi®cantly correlated with their responses to the crush test, when the animals were in isolation (r 0:29; P < 0:001), when the human stood motionless in front of the animals (r 0:37; P < 0:001), and when the human stroked them (r 0:28; P < 0:001). Sires' behavioural reactions to the docility test (computed from their daughters' scores) were correlated with their reactions to the crush test only when the human was present, both when motionless (r 0:88; P < 0:001) and when stroking the heifer (r 0:81; P < 0:05). No relationship appeared between sires' behavioural reactions to the docility test and their responses to restraint in the crush when the human was absent (P 0:17). Furthermore, the crush test did not reveal the animals which presented aggressive reactions to handling in the docility test. The results exposed in this paper pointed out the existence of a general reactivity of beef cattle to handling, whether the animals are restrained or not, which appears in¯uenced by the sire. Such reactivity is suggested to be mainly a consequence of the animals * Corresponding author. Tel.: 33-473624405; fax: 33-473624622. E-mail address: [email protected] (L. Grignard).
0168-1591/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 0 ) 0 0 1 8 7 - 8
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reactions to humans. The human environment needs to be precisely de®ned in the handling test procedures before using them as a selection criteria. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Cattle-handling; Docility; Crush; Genetic variability
1. Introduction European beef cattle husbandry has undergone many changes in the last 30 years in order to cope with economic pressures. Extensive production systems widespread and herd size has grown considerably (Le Neindre et al., 1996). Farmers now have an increasing number of animals to care of (Boivin et al., 1998). In this context, both the quantity and the quality of the interactions between cattle and their caretakers are affected: the number of contacts is reduced and, when they occur, they are often associated with aversive handling (Boivin et al., 1998). Handling of animals which are not accustomed to humans produces risks both for the stockperson's safety and the animal's welfare (Grandin, 1994). In addition, a strong reactivity of animals to humans can have negative effects on productive traits, such as carcass bruising (Fordyce et al., 1988). Regular positive contacts with humans, especially at an early age, can help to overcome handling dif®culties (Boivin et al., 1994). However, reactions of domestic animals to handling also depend on their genetic characteristics. Difference in the ¯ight zone size was found between dairy and beef cattle breeds reared under the same extensive conditions (Murphey et al., 1981). Several estimates of heritability of different measures of cattle handling have been published (for a review, see Burrow, 1997; Grandin and Deesing, 1998). In particular, Le Neindre et al. (1995) estimated the heritability of the reactions to handling imposed by a human of 904 Limousine heifers of 0.22 in the docility test. In this test, a human tried to maintain the animal in the corner of a pen during 30 consecutive seconds, in the visual presence of its peers. Moreover, the heritability of a movement score in a crush of 957 beef cattle was estimated to 0.25 by Fordyce et al. (1982). As heritability estimates of measures of beef cattle reactions to handling are generally moderate to high (Burrow, 1997), it seems possible, within a breed, to select animals that are more docile and so better adapted to speci®c management conditions (Le Neindre et al., 1996). However, great differences exist between the various methods which are used in order to estimate cattle reactions to handling. They differ especially in both the possibility offered to the animal to move (animal restrained or not) and the human behaviour (passive or active). In the restrained tests, the animal's movements are physically restricted by using a crush (Hearnshaw et al., 1979; Grandin and Deesing, 1998) or a weighing scale (Sato, 1981). In the non-restrained tests, the animal which is free to move, is confronted either by a motionless human (Fordyce et al., 1982; Hemsworth et al., 1989) or by an active human handling it (Le Neindre et al., 1995). As a consequence, the heritability estimates of cattle reactions to these various situations could correspond in fact to different behavioural traits. To our knowledge, no attempt to study the relationships between these different tests has been reported except by Fordyce et al. (1982). In this study, signi®cant correlations were found between agitation scores recorded in different tests where cattle were restrained and
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their reactivity to the presence of a motionless human or their ¯ight distance in response to the approach by a human. However, and as the authors stated, before using any speci®c test in a selection program, performance tests should have been correlated with handling in real farming situations. So, in this experiment, beef cattle were tested both while free to move in the docility test and while restrained in a crush. These two tests have been chosen because they have both shown genetic in¯uence of cattle reactions to handling. Moreover, they seem representative of current beef cattle husbandry conditions. On one hand, the docility test discerns cattle that are easy to handle in open situations where the use of human-made facilities is not always suf®cient to achieve a tight control of animals, which corresponds to beef producers' needs (Burrow, 1997). On the other hand, crushes belong to restraint facilities ordinarily employed by farmers (Grandin, 1997). As several procedures of crush test exist (for a review, see Burrow, 1997), and also because the human environment is not precisely reported in the different crush tests, a new procedure was used in this experiment. After a social isolation while restrained in a cage, the animal was confronted with a human, ®rst motionless, then touching the animal. The aim of this study is to compare beef cattle reactions to these two handling situations. In addition, showing genetic in¯uence of the sire could lead to a process of genetic selection of the sires. So, evaluations of the sires' performances computed from the reactions of their daughters in the docility and in the crush test are also compared. 2. Methods 2.1. Experimental animals The experiment was lead in an arti®cial insemination progeny testing farm (Station of Moussours, Uzerche, France), where cows are tested for their maternal abilities. Two hundred and forty-®ve Limousine heifers, which were descended from 10 sires (in average 24.5 heifers per sire), were used for this work. The heifers, each originated from a different farm, arrived at the testing farm when 8 months old. They were then reared in free-stables, in groups of 16 animals except for one group of 21 heifers. The heifers were randomly distributed among the 15 groups according to their sire. 2.2. Testing procedure Heifers were submitted to a docility test at 9 months old and to a crush test at 1 year of age. The tests were performed from 8.00 a.m. to 6.00 p.m. Because some heifers were observed aggressive towards the handler during the docility test, another docility test was performed at 16 months old to check the repeatability of this aggressiveness. Only 231 heifers could be tested in this second docility test. 2.2.1. Docility test The experimental set-up included two unfamiliar adjacent pens each of 5 m 5 m. The test pen had solid walls on two sides and was separated from the peers' pen by barred
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fencing. For the test, one group of heifers was split in half and led from its stable to the peers pen (the remaining heifers of the group stayed in their stable). The heifer to be tested was drafted out from this half-group according to a predetermined order and moved to the test pen, from which peers of the half-group were visible. The animal was left alone for 30 s before a human came into the test pen and stood motionless in the centre for another 30 s. The human was unfamiliar to the heifer, but experienced with beef cattle handling; he was wearing usual overalls and used voice, arm waving, and a stick to handle the heifer. The human then attempted to contain the heifer in a 2 m 2 m area that was located in the corner of the pen with the two walls (therefore, at the opposite from the peers' pen). If he succeeded in keeping the heifer in the corner for 30 consecutive seconds, he then tried to stroke it while still maintaining it in the same area. The maximum duration of this third period of the test was 2.5 min. Otherwise, the test was terminated when the animal remained in the corner for 30 s, or if it charged the human. Following the test, the heifer was taken back in the peers pen with its conspeci®cs (Fig. 1). During the docility test, behavioural events were recorded on a portable microcomputer, using software developed at our laboratory (Le Neindre et al., 1995). The events recorded were when the heifer began to stand still, walk or run; the attempts to escape (by jumping or passing the head under the fence); the beginning and end of the handling period; the aggressiveness towards the human (threats or attacks); the beginning and end of the period spent in the corner; and the success or otherwise of the human in stroking the heifer. To summarise the behavioural reaction of the animal to the docility test, a docility score,
Fig. 1. Experimental set-up used for the docility test.
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which included all the informations collected over all the durations of the test, was calculated by the software. The procedure of estimation of the docility score had been set up by Le Neindre et al. (1995) on a sample of 300 individuals. As several of the recorded criteria were not normally distributed, the docility score consisted of a linear combination of each behavioural event corrected in proportion to its frequency or its duration. The determination of the corrected values was based on a multidimensional analysis. The docility score was continuous and ranged from 6.5 for the most aggressive animal to 17 for the most docile animal. 2.2.2. Crush test All heifers from each rearing group were submitted to the crush test successively. However, within each group, heifers were tested at random. The group to be tested was led from its stable to an unfamiliar waiting pen (7 m 7 m). The heifer to be tested was taken from its group according to a predetermined order and led, through a single ®le race, to a manual crush. In the crush, the heifer's head was restrained by two bars squeezing its neck. Conspeci®cs were not visible for the animal restrained in the crush. Before the beginning of the test, four electrodes were set on the animal in order to record its heart rate. The test began just after handlers' disappearance from the heifer's sight. The test was divided into three periods: ®rst, the animal was left alone for 5 min; second, it was in the presence of an unfamiliar human standing motionless in front of it, at a distance of 1 m, for 30 s; and third, the human stroked the heifer's forehead for 30 s. After a 1 min interval during which the human was out of the heifer's sight, the two last periods were repeated a second time (presence of the motionless human for 30 s, then stroking for 30 s; Fig. 2). During the duration of the test, the heifer's following behaviours were recorded on a portable microcomputer, using a computer program elaborated at our laboratory: when the heifer began to stand still, move (weak movements of two legs or more) or ®ght (sweep movements of the four legs, i.e. the animal was ®ghting to escape); the beginning and end of tail's movements; horizontal and vertical head's movements (which correspond to attempts to escape from the two bars restraining the head); urination or defecation; vocalisation; human snif®ng and licking. The computer program calculated, for each behaviour, the number of items performed by the animal and the duration when body, tail or head were moving. In addition, the heart rate was evaluated. The four electrodes on the animal were connected to an electrocardiograph (Cardioline Epsilon) which continuously recorded the heartbeats. Measurements of the heart rate were then evaluated on four inter-beats, each 30 s during the isolation period and each 15 s during the four other periods of the test (28 heart rate measurements were calculated in this way). 2.3. Statistical analyses All statistical analyses were carried out with the SAS1 (1988) statistical package. Pearson correlations were performed to analyse the relationships between the different variables. The same variables recorded during the ®rst and second sessions of the motionless human period of the crush test were signi®cantly correlated (P < 0:001). In like manner,
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Fig. 2. Experimental set-up used for the crush test.
the same variables recorded during the ®rst and second sessions of the stroke period of the crush test were highly signi®cantly correlated (P < 0:001). Hence, means between the same variables recorded during the two sessions of each of these two periods were computed in order to summarise the information. To increasingly synthesise the relationships between behavioural variables, PCA analyses were performed for each period of the crush test (isolation, presence of the motionless human, stroke). First components axes for each period of the crush test were extracted as synthetic behavioural variables for further analyses. Analyses of variances using the general linear model procedure were performed to analyse the effects of the sire and the social group on the behavioural and physiological variables of the crush test, and on the docility score. The statistic model used for the crush test included the sire of the heifer and the social group as ®xed effects, and the order in which the heifers were tested as a co-variable. The model employed for the docility test was the same as the one previously described, but it also included the half-group as a ®xed factor (before being tested in the docility test, each group of heifers was randomly split in half). As the factors order of testing (for the two tests), social group (for the docility test) and half-group (for the docility test) had no signi®cant effects (P > 0:1), they were excluded from the ®nal models. So the ®nal model employed for the crush test included the sire and the social group, while the one used for the docility test only included the sire.
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In order to investigate the repeatability of the heifers' reactions to the docility test, a procedure for repeated data was used; the model included the sire, the session of the test (®rst or second) and the interaction between both. The relationships between the reactions observed during the docility and the crush tests were only evaluated on the ®rst time animals were tested in the docility test. The effects of the sire and the social group could biased the correlation study between heifers' reactions to docility and crush tests. So, the residual values obtained from the variance analyses were used to evaluate correlation coef®cients between heifers' responses to the two handling situations. Correlations between sires' performances to docility and crush tests were also evaluated. The sires' performances in the two tests were estimated by computing the mean of their daughters' scores in each criteria (i.e. docility score, ®rst components extracted from the PCA performed on the behavioural variables of the crush test, and heart rate data). 3. Results 3.1. Animals' reactions to the docility test The heifers docility scores increased slightly but signi®cantly from the ®rst test to the second one (12:55 2:17 versus 13:61 2:69, respectively; F9221 46:18; P < 0:001). However, both scores were highly correlated (r 0:56, P < 0:001). Ten heifers displayed aggressive behaviours towards the human (threats and/or attacks) during the ®rst docility test; they were scored from 7.5 to 9.0 while docility scores observed for all the animals ranged from 7.5 to 17. During the second docility test, eight of these 10 heifers could be tested. They were scored from 6.5 to 7.5, while docility scores observed for all the animals ranged from 6.5 to 17. Five of them reacted once again aggressively to the handling. 3.2. Animals' reactions to the crush test PCA analyses were run on nine variables for the isolation period, and on 10 variables for the two periods with the human (Fig. 3). The ®rst axes of these three PCA explained an average of 45% of the total variation of the original variables (45.95, 43.98 and 44.73% for each period, respectively). The ®rst principal components characterised animal agitation in the crush (important motor activity pointed out by movements of body, tail and head) (Fig. 3). We calculated factor scores for each heifer on the basis of the ®rst principal component loading, and took these scores as an indication of each individual's reactivity. Similarly, to the docility score, the lower the value of the ``reactivity score'' is, the more agitated the animal is. At the beginning of the test, the individual mean heart rate ranged from 73.17 to 239.04 beats/min, with a mean of 179:56 26:14 beats/min (Fig. 4). Then it felt gradually to about 132:93 26:45 beats/min at the end of the isolation period. The heart rate tended to stabilise over the last minute of the isolation period; so we estimated the ``basal'' heart rate as the mean heart rate between the fourth and ®fth minutes of the isolation period even if it probably did not represent the heart rate measured in absence of perturbation. The basal heart rate in the crush stayed in average at 131:82 23:24 beats/min. Nevertheless, when
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Fig. 3. Principal component analyses performed on behavioural variables recorded during the isolation period (a), the motionless human period (b), and the stroke period (c) of the crush test. Interpretation of axes: im, duration of body immobility; smn, number of sweep body movements; smd, duration of sweep body movements; sc, number of body movements' speed changes; tan, number of tail movements; tad, duration of tail movements; he, number of head movements; mi, number of mictions and defections; vo, number of vocalisations; ho, number of human sniffing and licking.
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Fig. 4. Evolution of the heifers' mean heart rate during the crush test.
the human arrived and stood motionless in front of the animal, the heart rate increased clearly compared to the initial heart rate (24:37 19:74 beats/min; F1235 382:35; P < 0:001), and even more when the human stroked the animal (30:58 23:73 beats/ min; F1235 314:06; P < 0:001). Heifers' behavioural and physiological reactions to the crush test were related. Signi®cant negative correlations were found between the reactivity score of the isolation period and the basal heart rate (r ÿ0:20, P 0:001). Moreover, reactivity scores obtained for the period in the presence of the motionless human were signi®cantly correlated with the increase in heart rates when the human appeared (r ÿ0:46, P < 0:001). A signi®cant correlation coef®cient was also found between heifers' reactivity scores for the stroke period and the increase in their heart rates during the stroke (r ÿ0:43, P < 0:001). 3.3. Effects of the sire and the social group on the heifers' reactions to the docility and the crush tests There was a signi®cant effect of the sire on the docility score of their daughters, both for the ®rst and second docility tests (F9235 2:11; P < 0:05 and F9221 2:82; P < 0:01, respectively), but there was no signi®cant effect of the interaction between the sire and the session of the test on the docility score (F9221 0:92; P 0:50).
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Differences were found between sires in the behavioural responses of their daughters for two periods of the crush test. The sire had a signi®cant effect on the reactivity scores, for the isolation period (F9221 4:08; P < 0:001) and for the stroking period (F9221 2:23; P < 0:05). No in¯uence of the sire was detected on the reactivity score when the human was motionless (F9221 1:55; P 0:13). Concerning the physiological data, the initial heart rate and the increase in heart rate recorded in presence of the motionless human differed signi®cantly between sires (F92219.58; P < 0:001 and F9221 1:93; P < 0:05, respectively). Conversely, no sire effect on the increase in heart rate recorded during the stroke period was found (F9235 0:94; P 0:49). The social group in¯uenced signi®cantly the behavioural and physiological responses of the heifers to the isolation period (F14;221 4:09; P < 0:001 and F14;221 2:28; P < 0:01, respectively), as well as to the stroking period (F14;221 1:99; P < 0:05 and F14;221 1:83; P < 0:05, respectively). For the period with the motionless human, the social group had an signi®cant effect on the heart rate (F14;221 2:31; P < 0:01), but not on the reactivity score (F14;221 1:67; P 0:06). 3.4. Relationships between the docility and the crush tests 3.4.1. Relationships between heifers' reactions to the docility and the crush tests Signi®cant positive correlations were found between the docility score and the reactivity scores of each period of the crush test (isolation: r 0:29, P < 0:001; motionless human: r 0:37, P < 0:001; stroke: r 0:28, P < 0:001). Individual docility scores were also signi®cantly related to the basal heart rate (r ÿ0:25, P < 0:001). No signi®cant correlations between the docility score and the increases in the heart rate recorded in the presence of the motionless human and during the stroke were found (r ÿ0:11, P 0:09 and r ÿ0:08; P 0:19, respectively). As mentioned above, the ten heifers which displayed aggressive behaviours towards the human during the docility test were scored from 7.5 to 9.0 while docility scores observed for all the animals ranged from 7.5 to 17. By contrast, their reactivity scores in the crush were distributed through the whole range of the scores of all the animals observed: for the isolation period, from ÿ9.47 to 1.91 while all the animals' scores ranged from ÿ9.47 to 2.14; for the motionless human period, from ÿ10.92 to 1.02 while all the animals' scores ranged from ÿ10.92 to 1.64; for the stroke period, from ÿ6.42 to 1.76 while all the animals' scores ranged from ÿ7.21 to 2.62. 3.4.2. Relationships between sires' performances in the docility and the crush tests Sires' docility and reactivity scores were positively correlated for the crush test's periods where the human was present (motionless human: r 0:88, P < 0:001; stroke: r 0:81, P < 0:05). However, when the human was absent in the crush test, no relation between sires' reactivity and docility scores was found (r 0:47, P 0:17). No signi®cant correlation was found between sires' docility score and heart rate measurements (basal heart rate: r ÿ0:53, P 0:12; increase in heart rate with the motionless human: r ÿ0:56, P 0:09; increase in heart rate during the stroke: r ÿ0:37; P 0:29).
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4. Discussion Relationships were found between the docility scores and the different behavioural reactivity scores or heart-rate recordings measured in the crush in the presence or absence of the human. Moreover, the present experiment tends to con®rm the genetic in¯uence on cattle reactions to handling procedures. Our ®ndings showed that handling procedures, whether the animals are directly confronted to the human or constrained by handling facilities, are related each other in some way. Indeed moderate but statistically signi®cant correlations were detected between heifers' behavioural and heart rate responses to the docility test and to the crush procedure. The relationships between heart rate and docility scores seem indicate that the heart rate can be interpreted as an independent set of measurements of the animal's reactivity which supports the behavioural measures of reactivity; previous studies provided similar results (Veissier et al., 1987; Mc Cann et al., 1988). Our results con®rm and complete the conclusions drawn by Fordyce et al. (1982) who found signi®cant correlations between behavioural scores of bulls and heifers submitted to three restrained and two non-restrained tests. However, in this previous study, the presence and the behaviour of the human during the restrained tests were not speci®ed clearly. Moreover, as pointed out by the authors, neither of their non-restrained tests re¯ect the behavioural reaction of a free animal towards handling imposed by humans, as in farming situations. One of these non-restrained tests assessed the cattle response to a passive human, while the other evaluated the animal ¯ight distance to the approach by a human. In our experiment, both the docility test and the crush test appear to better correspond to handling situations which are representative of current beef cattle husbandry conditions. However, the signi®cant relationship between the docility test and the crush test, whether the human was present or not, does not explain the nature of the common basis of these two test situations. At least three hypotheses, which are not exclusive, can be proposed. First, the persistence of individual differences in the behavioural reactions to these two challenging situations could re¯ect divergences in emotional reactivity. Emotional reactivity has been de®ned as a basic characteristic of the individual which predisposes it to respond with the same strength to a variety of potentially challenging events (Boissy, 1995). So individual emotional reactivity could modulate heifers' reactivity to docility and crush tests, which are both anxiogenic situations. Second, the relationships between heifers' reactions to the docility and the crush tests can be explained by their response to separation from social partners. In quails, Mills and Faure (1991) have shown that sociality can be selected independently from tonic immobility, which is a current measure of emotional reactivity in birds. Cattle are social animals for which separation from peers induces behavioural and physiological responses indicating a important stress (Boissy and Le Neindre, 1997). Both in the crush test and in the docility test, the heifers were removed from their social group and isolated. In the docility test, the social peers were visible, but the fence was a physical separation between the tested heifer and its peers. Third, the human factor could be of importance in determining the animal's response to these two situations. To perform our crush test, it was necessary to handle the animals, leading them in the crush and putting electrodes. This handling can in¯uence the heifers'
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reactions during the ®rst part of the crush test, even if animals' reactions were recorded in absence of the human. Moreover, if the initial response of a farm animal to humans could be mainly explained by emotional reactivity, its subsequent experience of humans induces the development of a speci®c response to humans (Hemsworth et al., 1996). Crushes are currently employed by farmers in order to facilitate handling procedures. So, it is possible that the heifers associated the crush test situation with previous experiences of handling by humans, which could lead to a signi®cant correlation between the docility test and the crush test even in the absence of human. Besides, the strongest correlation between heifers' reactions to the docility test and to the crush one was found when the heifers were in presence of the human. Furthermore, sires' performances computed from the reactions of their daughters in the docility and in the crush tests are only signi®cantly related when the human is present in the crush test. Then the human presence in the crush test improves the correlation between the two tests, suggesting that cattle reaction to humans could effectively be assumed as the common characteristic of these two handling tests. Further research is needed in order to distinguish between these different hypotheses. Evidence obtained in our experiment supports previous studies (for a review: Grandin and Deesing, 1998), by showing that heifers' reactions both to the docility test and to a crush test are in¯uenced by the sire from which they descended. Despite these results would be more convincing if other relevant variables (like the farm source) could have been included in the analysis, it appears possible to genetically select animals on their ease of handling, whether animals are restrained or not. Nevertheless, the best test as a basis for this selection is questionable. A good test should be relevant, safe, discriminating, repeatable, and quick to perform. Both the docility and the crush tests correspond to practical situations, are easily performed in a farm environment, and appear repeatable (Boivin et al., 1992; Grandin, 1993). On one hand, the docility test corresponds to open situations where the human-made facilities are not suf®cient to control the animals, and where the human directly confronts the animals. However, this test can be dangerous both for the human, who can be attacked, and for the animal, which can try to escape the fences. In addition, its maximum duration of 3.5 min can be practically disadvantageous when testing thousands of animals, as in selection programs. On the other hand, the crush test appears safer, but it seems not able to detect aggressive animals just by using agitation scoring, as it is usually done. In addition, the previous experience of animals in crushes may in¯uence their reactions to this handling test. Further investigations are requested to determine the test which is better adapted to this ®eld of research, especially according to the type of animals tested. In cattle types known for their aggressiveness in response to handling, such as free-range zebus and their crossbred (Becker and Lobato, 1997), the crush test in the presence of a motionless human is probably better adapted, at least for handler security. When testing animals which are generally less aggressive, the docility test appears more ef®cient. 5. Conclusions The results exposed in this paper point out the existence of a general reactivity of beef cattle to handling, whether the animals are restrained or not. Despite the complexity of
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handling situations, it is likely that the human factor represents the most important parameter of such situations and so needs to be precisely de®ned in the test procedures. Moreover, the existence of a variability between sires in their daughters' responses to handling situations could lead to a selection program by using the handling test the most adapted to the type of cattle. However, before engaging such a selection program, further investigations are needed in order to evaluate the potential relationships between the reactivity to handling and other traits, such as, maternal ability. Acknowledgements This project received ®nancial support from the UPRA Limousine. Many thanks are due to Guy Brunet and all the staff of the station of Moussours (in particular Philippe and Patrick) for their welcome and their participation to the experiment. We are grateful to Gilbert Trillat (I.N.R.A. Theix) for his assistance and to Bruno Fredot and JoeÈl Ballet (I.N.R.A. Theix, Domaine de Redon) for their help during the tests. We also would like to thank Tania Ngapo (I.N.R.A. Theix) for reviewing this paper.
References Becker, B.G., Lobato, J.F.P., 1997. Effect of gentle handling on the reactivity of zebu crossed calves to humans. Appl. Anim. Behav. Sci. 53, 219±224. Boissy, A., 1995. Fear and fearfulness in animals. Q. Rev. Biol. 70, 165±191. Boissy, A., Le Neindre, P., 1997. Behavioral, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiol. Behav. 61, 693±699. Boivin, X., Le Neindre, P., Chupin, J.M., Garel, J.P., Trillat, G., 1992. Influence of breed and early management on ease of handling and open-field behaviour of cattle. Appl. Anim. Behav. Sci. 32, 313±323. Boivin, X., Le Neindre, P., Garel, J.P., Chupin, J.M., 1994. Influence of breed and rearing management on cattle reactions during human handling. Appl. Anim. Behav. Sci. 39, 115±122. Boivin, X., Boissy, A., Chupin, J.M., Le Neindre, P., 1998. Herbivores, caretakers and range management. In: Goddard, P.J. (Ed.), Proceedings of the Implication of Extensification for the Health and Welfare of Beef Cattle and Sheep, Aberdeen, Scotland, 5±6 March 1998. Burrow, H.M., 1997. Measurements of temperament and their relationships with performance traits of beef cattle. Anim. Breeding Abstracts 65, 477±495. Fordyce, G., Goddard, M.E., Seifert, G.W., 1982. The measurement of temperament in cattle and the effect of experience and genotype. Proceedings of the Australian Society of Animal Production 14, 329±332. Fordyce, G., Wythes, J.R., Shortose, W.R., Underwood, D.W., Sheperd, R.K., 1988. Cattle temperament in extensive beef herds in northern Queensland. II. Effect of temperament on carcass and meat quality. Aust. J. Exp. Agric. 28, 689±693. Grandin, T., 1993. Behavioral agitation during handling of cattle is persistent over time. Appl. Anim. Behav. Sci. 36, 1±9. Grandin, T., 1994. Solving livestock handling problems. Vet. Med. 89, 989±998. Grandin, T., 1997. Livestock Handling and Transport. CAB International, Wallingford, Oxon, 320 pp. Grandin, T., Deesing, M.J., 1998. Genetics and behavior during handling, restraint, and herding. In: Grandin, T. (Ed.), Genetics and the Behavior of Domestic Animals. Academic Press, San Diego, USA, pp. 113±144. Hearnshaw, H., Barlow, R., Want, G., 1979. Development of temperament or handling difficulty score for cattle. Proceedings of the Australian Association of Animal Breeding and Genetics 1, 164±166. Hemsworth, P.H., Barnett, J.L., Tilbrook, A.J., Hansen, C., 1989. The effects of handling by humans at calving
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and during milking on the behaviour and milk cortisol concentrations of primiparous dairy cows. Appl. Anim. Behav. Sci. 22, 313±326. Hemsworth, P.H., Price, E.O., Borgwardt, R., 1996. Behavioural responses of domestic pigs and cattle to humans and novel stimuli. Appl. Anim. Behav. Sci. 50, 43±56. Le Neindre, P., Trillat, G., Sapa, J., MeÂnissier, F., Bonnet, J.N., Chupin, J.M., 1995. Individual differences in docility in Limousine cattle. J. Anim. Sci. 73, 2249±2253. Le Neindre, P., Boivin, X., Boissy, A., 1996. Handling of extensively kept animals. Appl. Anim. Behav. Sci. 49, 73±81. Mc Cann, J.S., Heird, J.C., Bell, R.W., Lutherer, L.O., 1988. Normal and more highly reactive horses. I. Heart rate, respiration rate and behavioral observations. Appl. Anim. Behav. Sci. 19, 201±214. Mills, A.D., Faure, J.M., 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. Murphey, R.M., Moura Duarte, F.A., Torres Penedo, M.C., 1981. Responses of cattle to humans in open-spaces: breed comparisons and approach-avoidance relationships. Behav. Genet. 11, 37±48. SAS1 User's guide 1988. Statistics, version 6.11. SAS Institute Inc., Cary, NC. Sato, S., 1981. Factors associated with temperament in beef cattle. Jpn. J. Zootech. Sci. 52, 595±605. Veissier, I., Le Neindre, P., Trillat, G., 1987. The influence of mother-young relationships on behavioural reactivity and learning in calves. Biol. Behav. 12, 222±238.
Do beef cattle react consistently to different handling situations? Laurence Grignard*, Xavier Boivin, Alain Boissy, Pierre Le Neindre I.N.R.A. Theix, URH-ACS, F 63122, St GeneÁs Champanelle, France Accepted 7 September 2000
Abstract Beef cattle responses to handling depend partly on the genetic characteristics of the animals. However, the various methods used in order to assess these responses differ to a great extent. The purpose of this work is to study the relationship between two different situations extensively used to evaluate cattle reactions to handling. Moreover, the genetic variability of cattle responses to these two handling situations was investigated. Behavioural reactions of 245 Limousine heifers, from 10 sires, were evaluated both in a docility test and in a crush test. In the docility test, a human tried to lead and then to maintain the animal in the corner of a pen during 30 consecutive seconds, with a maximum duration of the test of 3.5 min. A docility score summarised the animal's behavioural reactions to the test. The crush test procedure consisted of social isolation of the animal in a crush, with the head maintained in a head gate (5 min), then exposure to a stationary human (30 s), and ®nally stroking on the forehead (30 s). An agitation index for each part of this test was computed from PCA analyses based on agitation behaviours. Sire effect was signi®cant for every part of both tests (P < 0:05). Heifers' behavioural responses to the docility test were signi®cantly correlated with their responses to the crush test, when the animals were in isolation (r 0:29; P < 0:001), when the human stood motionless in front of the animals (r 0:37; P < 0:001), and when the human stroked them (r 0:28; P < 0:001). Sires' behavioural reactions to the docility test (computed from their daughters' scores) were correlated with their reactions to the crush test only when the human was present, both when motionless (r 0:88; P < 0:001) and when stroking the heifer (r 0:81; P < 0:05). No relationship appeared between sires' behavioural reactions to the docility test and their responses to restraint in the crush when the human was absent (P 0:17). Furthermore, the crush test did not reveal the animals which presented aggressive reactions to handling in the docility test. The results exposed in this paper pointed out the existence of a general reactivity of beef cattle to handling, whether the animals are restrained or not, which appears in¯uenced by the sire. Such reactivity is suggested to be mainly a consequence of the animals * Corresponding author. Tel.: 33-473624405; fax: 33-473624622. E-mail address: [email protected] (L. Grignard).
0168-1591/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 0 ) 0 0 1 8 7 - 8
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reactions to humans. The human environment needs to be precisely de®ned in the handling test procedures before using them as a selection criteria. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Cattle-handling; Docility; Crush; Genetic variability
1. Introduction European beef cattle husbandry has undergone many changes in the last 30 years in order to cope with economic pressures. Extensive production systems widespread and herd size has grown considerably (Le Neindre et al., 1996). Farmers now have an increasing number of animals to care of (Boivin et al., 1998). In this context, both the quantity and the quality of the interactions between cattle and their caretakers are affected: the number of contacts is reduced and, when they occur, they are often associated with aversive handling (Boivin et al., 1998). Handling of animals which are not accustomed to humans produces risks both for the stockperson's safety and the animal's welfare (Grandin, 1994). In addition, a strong reactivity of animals to humans can have negative effects on productive traits, such as carcass bruising (Fordyce et al., 1988). Regular positive contacts with humans, especially at an early age, can help to overcome handling dif®culties (Boivin et al., 1994). However, reactions of domestic animals to handling also depend on their genetic characteristics. Difference in the ¯ight zone size was found between dairy and beef cattle breeds reared under the same extensive conditions (Murphey et al., 1981). Several estimates of heritability of different measures of cattle handling have been published (for a review, see Burrow, 1997; Grandin and Deesing, 1998). In particular, Le Neindre et al. (1995) estimated the heritability of the reactions to handling imposed by a human of 904 Limousine heifers of 0.22 in the docility test. In this test, a human tried to maintain the animal in the corner of a pen during 30 consecutive seconds, in the visual presence of its peers. Moreover, the heritability of a movement score in a crush of 957 beef cattle was estimated to 0.25 by Fordyce et al. (1982). As heritability estimates of measures of beef cattle reactions to handling are generally moderate to high (Burrow, 1997), it seems possible, within a breed, to select animals that are more docile and so better adapted to speci®c management conditions (Le Neindre et al., 1996). However, great differences exist between the various methods which are used in order to estimate cattle reactions to handling. They differ especially in both the possibility offered to the animal to move (animal restrained or not) and the human behaviour (passive or active). In the restrained tests, the animal's movements are physically restricted by using a crush (Hearnshaw et al., 1979; Grandin and Deesing, 1998) or a weighing scale (Sato, 1981). In the non-restrained tests, the animal which is free to move, is confronted either by a motionless human (Fordyce et al., 1982; Hemsworth et al., 1989) or by an active human handling it (Le Neindre et al., 1995). As a consequence, the heritability estimates of cattle reactions to these various situations could correspond in fact to different behavioural traits. To our knowledge, no attempt to study the relationships between these different tests has been reported except by Fordyce et al. (1982). In this study, signi®cant correlations were found between agitation scores recorded in different tests where cattle were restrained and
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their reactivity to the presence of a motionless human or their ¯ight distance in response to the approach by a human. However, and as the authors stated, before using any speci®c test in a selection program, performance tests should have been correlated with handling in real farming situations. So, in this experiment, beef cattle were tested both while free to move in the docility test and while restrained in a crush. These two tests have been chosen because they have both shown genetic in¯uence of cattle reactions to handling. Moreover, they seem representative of current beef cattle husbandry conditions. On one hand, the docility test discerns cattle that are easy to handle in open situations where the use of human-made facilities is not always suf®cient to achieve a tight control of animals, which corresponds to beef producers' needs (Burrow, 1997). On the other hand, crushes belong to restraint facilities ordinarily employed by farmers (Grandin, 1997). As several procedures of crush test exist (for a review, see Burrow, 1997), and also because the human environment is not precisely reported in the different crush tests, a new procedure was used in this experiment. After a social isolation while restrained in a cage, the animal was confronted with a human, ®rst motionless, then touching the animal. The aim of this study is to compare beef cattle reactions to these two handling situations. In addition, showing genetic in¯uence of the sire could lead to a process of genetic selection of the sires. So, evaluations of the sires' performances computed from the reactions of their daughters in the docility and in the crush test are also compared. 2. Methods 2.1. Experimental animals The experiment was lead in an arti®cial insemination progeny testing farm (Station of Moussours, Uzerche, France), where cows are tested for their maternal abilities. Two hundred and forty-®ve Limousine heifers, which were descended from 10 sires (in average 24.5 heifers per sire), were used for this work. The heifers, each originated from a different farm, arrived at the testing farm when 8 months old. They were then reared in free-stables, in groups of 16 animals except for one group of 21 heifers. The heifers were randomly distributed among the 15 groups according to their sire. 2.2. Testing procedure Heifers were submitted to a docility test at 9 months old and to a crush test at 1 year of age. The tests were performed from 8.00 a.m. to 6.00 p.m. Because some heifers were observed aggressive towards the handler during the docility test, another docility test was performed at 16 months old to check the repeatability of this aggressiveness. Only 231 heifers could be tested in this second docility test. 2.2.1. Docility test The experimental set-up included two unfamiliar adjacent pens each of 5 m 5 m. The test pen had solid walls on two sides and was separated from the peers' pen by barred
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fencing. For the test, one group of heifers was split in half and led from its stable to the peers pen (the remaining heifers of the group stayed in their stable). The heifer to be tested was drafted out from this half-group according to a predetermined order and moved to the test pen, from which peers of the half-group were visible. The animal was left alone for 30 s before a human came into the test pen and stood motionless in the centre for another 30 s. The human was unfamiliar to the heifer, but experienced with beef cattle handling; he was wearing usual overalls and used voice, arm waving, and a stick to handle the heifer. The human then attempted to contain the heifer in a 2 m 2 m area that was located in the corner of the pen with the two walls (therefore, at the opposite from the peers' pen). If he succeeded in keeping the heifer in the corner for 30 consecutive seconds, he then tried to stroke it while still maintaining it in the same area. The maximum duration of this third period of the test was 2.5 min. Otherwise, the test was terminated when the animal remained in the corner for 30 s, or if it charged the human. Following the test, the heifer was taken back in the peers pen with its conspeci®cs (Fig. 1). During the docility test, behavioural events were recorded on a portable microcomputer, using software developed at our laboratory (Le Neindre et al., 1995). The events recorded were when the heifer began to stand still, walk or run; the attempts to escape (by jumping or passing the head under the fence); the beginning and end of the handling period; the aggressiveness towards the human (threats or attacks); the beginning and end of the period spent in the corner; and the success or otherwise of the human in stroking the heifer. To summarise the behavioural reaction of the animal to the docility test, a docility score,
Fig. 1. Experimental set-up used for the docility test.
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which included all the informations collected over all the durations of the test, was calculated by the software. The procedure of estimation of the docility score had been set up by Le Neindre et al. (1995) on a sample of 300 individuals. As several of the recorded criteria were not normally distributed, the docility score consisted of a linear combination of each behavioural event corrected in proportion to its frequency or its duration. The determination of the corrected values was based on a multidimensional analysis. The docility score was continuous and ranged from 6.5 for the most aggressive animal to 17 for the most docile animal. 2.2.2. Crush test All heifers from each rearing group were submitted to the crush test successively. However, within each group, heifers were tested at random. The group to be tested was led from its stable to an unfamiliar waiting pen (7 m 7 m). The heifer to be tested was taken from its group according to a predetermined order and led, through a single ®le race, to a manual crush. In the crush, the heifer's head was restrained by two bars squeezing its neck. Conspeci®cs were not visible for the animal restrained in the crush. Before the beginning of the test, four electrodes were set on the animal in order to record its heart rate. The test began just after handlers' disappearance from the heifer's sight. The test was divided into three periods: ®rst, the animal was left alone for 5 min; second, it was in the presence of an unfamiliar human standing motionless in front of it, at a distance of 1 m, for 30 s; and third, the human stroked the heifer's forehead for 30 s. After a 1 min interval during which the human was out of the heifer's sight, the two last periods were repeated a second time (presence of the motionless human for 30 s, then stroking for 30 s; Fig. 2). During the duration of the test, the heifer's following behaviours were recorded on a portable microcomputer, using a computer program elaborated at our laboratory: when the heifer began to stand still, move (weak movements of two legs or more) or ®ght (sweep movements of the four legs, i.e. the animal was ®ghting to escape); the beginning and end of tail's movements; horizontal and vertical head's movements (which correspond to attempts to escape from the two bars restraining the head); urination or defecation; vocalisation; human snif®ng and licking. The computer program calculated, for each behaviour, the number of items performed by the animal and the duration when body, tail or head were moving. In addition, the heart rate was evaluated. The four electrodes on the animal were connected to an electrocardiograph (Cardioline Epsilon) which continuously recorded the heartbeats. Measurements of the heart rate were then evaluated on four inter-beats, each 30 s during the isolation period and each 15 s during the four other periods of the test (28 heart rate measurements were calculated in this way). 2.3. Statistical analyses All statistical analyses were carried out with the SAS1 (1988) statistical package. Pearson correlations were performed to analyse the relationships between the different variables. The same variables recorded during the ®rst and second sessions of the motionless human period of the crush test were signi®cantly correlated (P < 0:001). In like manner,
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Fig. 2. Experimental set-up used for the crush test.
the same variables recorded during the ®rst and second sessions of the stroke period of the crush test were highly signi®cantly correlated (P < 0:001). Hence, means between the same variables recorded during the two sessions of each of these two periods were computed in order to summarise the information. To increasingly synthesise the relationships between behavioural variables, PCA analyses were performed for each period of the crush test (isolation, presence of the motionless human, stroke). First components axes for each period of the crush test were extracted as synthetic behavioural variables for further analyses. Analyses of variances using the general linear model procedure were performed to analyse the effects of the sire and the social group on the behavioural and physiological variables of the crush test, and on the docility score. The statistic model used for the crush test included the sire of the heifer and the social group as ®xed effects, and the order in which the heifers were tested as a co-variable. The model employed for the docility test was the same as the one previously described, but it also included the half-group as a ®xed factor (before being tested in the docility test, each group of heifers was randomly split in half). As the factors order of testing (for the two tests), social group (for the docility test) and half-group (for the docility test) had no signi®cant effects (P > 0:1), they were excluded from the ®nal models. So the ®nal model employed for the crush test included the sire and the social group, while the one used for the docility test only included the sire.
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In order to investigate the repeatability of the heifers' reactions to the docility test, a procedure for repeated data was used; the model included the sire, the session of the test (®rst or second) and the interaction between both. The relationships between the reactions observed during the docility and the crush tests were only evaluated on the ®rst time animals were tested in the docility test. The effects of the sire and the social group could biased the correlation study between heifers' reactions to docility and crush tests. So, the residual values obtained from the variance analyses were used to evaluate correlation coef®cients between heifers' responses to the two handling situations. Correlations between sires' performances to docility and crush tests were also evaluated. The sires' performances in the two tests were estimated by computing the mean of their daughters' scores in each criteria (i.e. docility score, ®rst components extracted from the PCA performed on the behavioural variables of the crush test, and heart rate data). 3. Results 3.1. Animals' reactions to the docility test The heifers docility scores increased slightly but signi®cantly from the ®rst test to the second one (12:55 2:17 versus 13:61 2:69, respectively; F9221 46:18; P < 0:001). However, both scores were highly correlated (r 0:56, P < 0:001). Ten heifers displayed aggressive behaviours towards the human (threats and/or attacks) during the ®rst docility test; they were scored from 7.5 to 9.0 while docility scores observed for all the animals ranged from 7.5 to 17. During the second docility test, eight of these 10 heifers could be tested. They were scored from 6.5 to 7.5, while docility scores observed for all the animals ranged from 6.5 to 17. Five of them reacted once again aggressively to the handling. 3.2. Animals' reactions to the crush test PCA analyses were run on nine variables for the isolation period, and on 10 variables for the two periods with the human (Fig. 3). The ®rst axes of these three PCA explained an average of 45% of the total variation of the original variables (45.95, 43.98 and 44.73% for each period, respectively). The ®rst principal components characterised animal agitation in the crush (important motor activity pointed out by movements of body, tail and head) (Fig. 3). We calculated factor scores for each heifer on the basis of the ®rst principal component loading, and took these scores as an indication of each individual's reactivity. Similarly, to the docility score, the lower the value of the ``reactivity score'' is, the more agitated the animal is. At the beginning of the test, the individual mean heart rate ranged from 73.17 to 239.04 beats/min, with a mean of 179:56 26:14 beats/min (Fig. 4). Then it felt gradually to about 132:93 26:45 beats/min at the end of the isolation period. The heart rate tended to stabilise over the last minute of the isolation period; so we estimated the ``basal'' heart rate as the mean heart rate between the fourth and ®fth minutes of the isolation period even if it probably did not represent the heart rate measured in absence of perturbation. The basal heart rate in the crush stayed in average at 131:82 23:24 beats/min. Nevertheless, when
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Fig. 3. Principal component analyses performed on behavioural variables recorded during the isolation period (a), the motionless human period (b), and the stroke period (c) of the crush test. Interpretation of axes: im, duration of body immobility; smn, number of sweep body movements; smd, duration of sweep body movements; sc, number of body movements' speed changes; tan, number of tail movements; tad, duration of tail movements; he, number of head movements; mi, number of mictions and defections; vo, number of vocalisations; ho, number of human sniffing and licking.
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Fig. 4. Evolution of the heifers' mean heart rate during the crush test.
the human arrived and stood motionless in front of the animal, the heart rate increased clearly compared to the initial heart rate (24:37 19:74 beats/min; F1235 382:35; P < 0:001), and even more when the human stroked the animal (30:58 23:73 beats/ min; F1235 314:06; P < 0:001). Heifers' behavioural and physiological reactions to the crush test were related. Signi®cant negative correlations were found between the reactivity score of the isolation period and the basal heart rate (r ÿ0:20, P 0:001). Moreover, reactivity scores obtained for the period in the presence of the motionless human were signi®cantly correlated with the increase in heart rates when the human appeared (r ÿ0:46, P < 0:001). A signi®cant correlation coef®cient was also found between heifers' reactivity scores for the stroke period and the increase in their heart rates during the stroke (r ÿ0:43, P < 0:001). 3.3. Effects of the sire and the social group on the heifers' reactions to the docility and the crush tests There was a signi®cant effect of the sire on the docility score of their daughters, both for the ®rst and second docility tests (F9235 2:11; P < 0:05 and F9221 2:82; P < 0:01, respectively), but there was no signi®cant effect of the interaction between the sire and the session of the test on the docility score (F9221 0:92; P 0:50).
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Differences were found between sires in the behavioural responses of their daughters for two periods of the crush test. The sire had a signi®cant effect on the reactivity scores, for the isolation period (F9221 4:08; P < 0:001) and for the stroking period (F9221 2:23; P < 0:05). No in¯uence of the sire was detected on the reactivity score when the human was motionless (F9221 1:55; P 0:13). Concerning the physiological data, the initial heart rate and the increase in heart rate recorded in presence of the motionless human differed signi®cantly between sires (F92219.58; P < 0:001 and F9221 1:93; P < 0:05, respectively). Conversely, no sire effect on the increase in heart rate recorded during the stroke period was found (F9235 0:94; P 0:49). The social group in¯uenced signi®cantly the behavioural and physiological responses of the heifers to the isolation period (F14;221 4:09; P < 0:001 and F14;221 2:28; P < 0:01, respectively), as well as to the stroking period (F14;221 1:99; P < 0:05 and F14;221 1:83; P < 0:05, respectively). For the period with the motionless human, the social group had an signi®cant effect on the heart rate (F14;221 2:31; P < 0:01), but not on the reactivity score (F14;221 1:67; P 0:06). 3.4. Relationships between the docility and the crush tests 3.4.1. Relationships between heifers' reactions to the docility and the crush tests Signi®cant positive correlations were found between the docility score and the reactivity scores of each period of the crush test (isolation: r 0:29, P < 0:001; motionless human: r 0:37, P < 0:001; stroke: r 0:28, P < 0:001). Individual docility scores were also signi®cantly related to the basal heart rate (r ÿ0:25, P < 0:001). No signi®cant correlations between the docility score and the increases in the heart rate recorded in the presence of the motionless human and during the stroke were found (r ÿ0:11, P 0:09 and r ÿ0:08; P 0:19, respectively). As mentioned above, the ten heifers which displayed aggressive behaviours towards the human during the docility test were scored from 7.5 to 9.0 while docility scores observed for all the animals ranged from 7.5 to 17. By contrast, their reactivity scores in the crush were distributed through the whole range of the scores of all the animals observed: for the isolation period, from ÿ9.47 to 1.91 while all the animals' scores ranged from ÿ9.47 to 2.14; for the motionless human period, from ÿ10.92 to 1.02 while all the animals' scores ranged from ÿ10.92 to 1.64; for the stroke period, from ÿ6.42 to 1.76 while all the animals' scores ranged from ÿ7.21 to 2.62. 3.4.2. Relationships between sires' performances in the docility and the crush tests Sires' docility and reactivity scores were positively correlated for the crush test's periods where the human was present (motionless human: r 0:88, P < 0:001; stroke: r 0:81, P < 0:05). However, when the human was absent in the crush test, no relation between sires' reactivity and docility scores was found (r 0:47, P 0:17). No signi®cant correlation was found between sires' docility score and heart rate measurements (basal heart rate: r ÿ0:53, P 0:12; increase in heart rate with the motionless human: r ÿ0:56, P 0:09; increase in heart rate during the stroke: r ÿ0:37; P 0:29).
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4. Discussion Relationships were found between the docility scores and the different behavioural reactivity scores or heart-rate recordings measured in the crush in the presence or absence of the human. Moreover, the present experiment tends to con®rm the genetic in¯uence on cattle reactions to handling procedures. Our ®ndings showed that handling procedures, whether the animals are directly confronted to the human or constrained by handling facilities, are related each other in some way. Indeed moderate but statistically signi®cant correlations were detected between heifers' behavioural and heart rate responses to the docility test and to the crush procedure. The relationships between heart rate and docility scores seem indicate that the heart rate can be interpreted as an independent set of measurements of the animal's reactivity which supports the behavioural measures of reactivity; previous studies provided similar results (Veissier et al., 1987; Mc Cann et al., 1988). Our results con®rm and complete the conclusions drawn by Fordyce et al. (1982) who found signi®cant correlations between behavioural scores of bulls and heifers submitted to three restrained and two non-restrained tests. However, in this previous study, the presence and the behaviour of the human during the restrained tests were not speci®ed clearly. Moreover, as pointed out by the authors, neither of their non-restrained tests re¯ect the behavioural reaction of a free animal towards handling imposed by humans, as in farming situations. One of these non-restrained tests assessed the cattle response to a passive human, while the other evaluated the animal ¯ight distance to the approach by a human. In our experiment, both the docility test and the crush test appear to better correspond to handling situations which are representative of current beef cattle husbandry conditions. However, the signi®cant relationship between the docility test and the crush test, whether the human was present or not, does not explain the nature of the common basis of these two test situations. At least three hypotheses, which are not exclusive, can be proposed. First, the persistence of individual differences in the behavioural reactions to these two challenging situations could re¯ect divergences in emotional reactivity. Emotional reactivity has been de®ned as a basic characteristic of the individual which predisposes it to respond with the same strength to a variety of potentially challenging events (Boissy, 1995). So individual emotional reactivity could modulate heifers' reactivity to docility and crush tests, which are both anxiogenic situations. Second, the relationships between heifers' reactions to the docility and the crush tests can be explained by their response to separation from social partners. In quails, Mills and Faure (1991) have shown that sociality can be selected independently from tonic immobility, which is a current measure of emotional reactivity in birds. Cattle are social animals for which separation from peers induces behavioural and physiological responses indicating a important stress (Boissy and Le Neindre, 1997). Both in the crush test and in the docility test, the heifers were removed from their social group and isolated. In the docility test, the social peers were visible, but the fence was a physical separation between the tested heifer and its peers. Third, the human factor could be of importance in determining the animal's response to these two situations. To perform our crush test, it was necessary to handle the animals, leading them in the crush and putting electrodes. This handling can in¯uence the heifers'
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reactions during the ®rst part of the crush test, even if animals' reactions were recorded in absence of the human. Moreover, if the initial response of a farm animal to humans could be mainly explained by emotional reactivity, its subsequent experience of humans induces the development of a speci®c response to humans (Hemsworth et al., 1996). Crushes are currently employed by farmers in order to facilitate handling procedures. So, it is possible that the heifers associated the crush test situation with previous experiences of handling by humans, which could lead to a signi®cant correlation between the docility test and the crush test even in the absence of human. Besides, the strongest correlation between heifers' reactions to the docility test and to the crush one was found when the heifers were in presence of the human. Furthermore, sires' performances computed from the reactions of their daughters in the docility and in the crush tests are only signi®cantly related when the human is present in the crush test. Then the human presence in the crush test improves the correlation between the two tests, suggesting that cattle reaction to humans could effectively be assumed as the common characteristic of these two handling tests. Further research is needed in order to distinguish between these different hypotheses. Evidence obtained in our experiment supports previous studies (for a review: Grandin and Deesing, 1998), by showing that heifers' reactions both to the docility test and to a crush test are in¯uenced by the sire from which they descended. Despite these results would be more convincing if other relevant variables (like the farm source) could have been included in the analysis, it appears possible to genetically select animals on their ease of handling, whether animals are restrained or not. Nevertheless, the best test as a basis for this selection is questionable. A good test should be relevant, safe, discriminating, repeatable, and quick to perform. Both the docility and the crush tests correspond to practical situations, are easily performed in a farm environment, and appear repeatable (Boivin et al., 1992; Grandin, 1993). On one hand, the docility test corresponds to open situations where the human-made facilities are not suf®cient to control the animals, and where the human directly confronts the animals. However, this test can be dangerous both for the human, who can be attacked, and for the animal, which can try to escape the fences. In addition, its maximum duration of 3.5 min can be practically disadvantageous when testing thousands of animals, as in selection programs. On the other hand, the crush test appears safer, but it seems not able to detect aggressive animals just by using agitation scoring, as it is usually done. In addition, the previous experience of animals in crushes may in¯uence their reactions to this handling test. Further investigations are requested to determine the test which is better adapted to this ®eld of research, especially according to the type of animals tested. In cattle types known for their aggressiveness in response to handling, such as free-range zebus and their crossbred (Becker and Lobato, 1997), the crush test in the presence of a motionless human is probably better adapted, at least for handler security. When testing animals which are generally less aggressive, the docility test appears more ef®cient. 5. Conclusions The results exposed in this paper point out the existence of a general reactivity of beef cattle to handling, whether the animals are restrained or not. Despite the complexity of
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handling situations, it is likely that the human factor represents the most important parameter of such situations and so needs to be precisely de®ned in the test procedures. Moreover, the existence of a variability between sires in their daughters' responses to handling situations could lead to a selection program by using the handling test the most adapted to the type of cattle. However, before engaging such a selection program, further investigations are needed in order to evaluate the potential relationships between the reactivity to handling and other traits, such as, maternal ability. Acknowledgements This project received ®nancial support from the UPRA Limousine. Many thanks are due to Guy Brunet and all the staff of the station of Moussours (in particular Philippe and Patrick) for their welcome and their participation to the experiment. We are grateful to Gilbert Trillat (I.N.R.A. Theix) for his assistance and to Bruno Fredot and JoeÈl Ballet (I.N.R.A. Theix, Domaine de Redon) for their help during the tests. We also would like to thank Tania Ngapo (I.N.R.A. Theix) for reviewing this paper.
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