The social environment influences the behavioural responses of beef cattle to handling

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1 Ž. Applied Animal Behaviour Science The social environment influences the behavioural responses of beef cattle to handling L. Grignard a,), A. Boissy a, X. Boivin a, J.P. Garel b, P. Le Neindre a a URH-ACS, Ins. National de la Recherche Agronomique, Cnt. de Clermont-FerrandrTheix, F 63122, St. Genes ` Champanelle, France b I.N.R.A., Domaine de la Borie, F 15190, Marcenat, France Accepted 7 December 1999 Abstract In cattle, a gregarious species, the social group influences individual stress responses to fear-eliciting situations. As handling can be stressful for farm animals, it can be hypothesised that social partners modify individual responses to handling. The present experiment investigated the effect of the presence or absence of social partners on behavioural reactions of beef calves in a handling test. At the age of 10 months, 38 calves from two breeds Ž Salers and Limousine. were individually subjected to the docility test, once while in visual contact with four familiar peers, and once in the absence of peers, following a crossover design. The docility test procedure included physical separation from peers Ž 30 s; period 1., exposition to a stationary human Ž30 s; period 2., and handling by human Ž 30 s 2.5 min, according to the success in handling; period 3.. In absence of human Ž period 1., calves in visual contact with their peers spent more time motionless than when peers were totally absent Ž P The social environment also influenced the duration of handling Ž period 3.; the human required more time to successfully handle calves when peers were present Ž P In conclusion, the presence of peers affects individual calves reactions to the docility test. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Cattle handling; Gregariousness; Social influence; Human animal relationships; Docility ) Corresponding author. Tel.: q ; fax: q Ž. address: grignard@clermont.inra.fr L. Grignard r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. Ž. PII: S X

2 2 L. Grignard et al.rapplied Animal BehaÕiour Science Introduction Recent developments in European husbandry systems for domestic ungulates increasingly lead the farmers to rear their animals in free-stables or outdoors. These changes are associated with an increase in the number of animals per caretaker. The resulting lack of familiarity of animals towards humans can lead to difficulties in handling, which, in large animals, can present a safety risk both for the stockperson and the animal Ž Grandin, Moreover, the welfare and performances of animals can be adversely affected Ž O Connor et al., 1985; Fordyce et al., 1988; Hemsworth and Barnett, In order to improve cattle handling, several methods have been set up to evaluate their reactions to handling, also called docility Ž for review, Burrow, Some of these methods are based on a restraint of the animal in a crush Ž Grandin, In other methods, the animal is unconstrained; one of these methods, the docility test, has been developed by Boivin et al. Ž 1992b.. The application of the docility test has provided information on the influence of the previous experience of the animal ŽBoivin et al., 1992a,b; and genetic background Ž Le Neindre et al., on the reactivity of cattle to humans. Cattle responses to handling are probably not only a reaction to human, but also depend on other elements of the situation Žsuch as social context, physical environment, and the novelty of the situation.. In particular, the social context may be important for cattle, which, in common with other species of domestic ungulates, are very gregarious. Several studies have demonstrated how the social environment can influence the responses of farm animals to their environment Ž for review, Nicol, The mere presence of peers reduces stress responses of cattle to potentially fear-eliciting situations; the distress behaviour of Aubrac heifers in response to a novel object is less when peers are in sight Ž Boissy and Le Neindre, Aubrac heifers exposed to a novel environment in groups of four show less escape attempts than do isolated ones ŽVeissier and Le Neindre, Since handling commonly induces fear reactions in farm animals Ž Hemsworth and Barnett, 1987., it can be supposed that the presence or absence of the social group has an effect on the ease with which animals can be handled. Nevertheless, no work has been done with cattle to determine whether the presence of peers during handling can modify the animal responses to the human. The aim of the present study was to investigate whether the presence or absence of familiar peers influences cattle reactions during the docility test. The experiment was conducted with beef calves, which were subjected to docility tests with or without visual contact with familiar peers. 2. Animals, materials and methods 2.1. Animals Forty-six calves from two beef breeds Ž 24 Salers and 22 Limousine. were used. During the first 3 months after birth, the calves were reared in free-stables, with their mothers, in four groups Žtwo groups of 12 Salers calves, one group of 12 Limousine

3 L. Grignard et al.rapplied Animal BehaÕiour Science calves, and one group of 10 Limousine calves. The calves were then reared on pasture with their mothers, with the minimum level of human contact. The four groups were kept separated Testing procedure At 10 months of age, calves were maintained in groups outdoors with their mothers. Before being tested, all calves of the two groups of the same breed were placed indoors Ž without their mothers. in one waiting pen Ž Fig. 1.. The calf to be tested was drafted out according to a predetermined order; so the time past by calves in the waiting pen prior to testing depended on their order of testing. The tested calf was then moved to a pen of 3.5=5 m Ž test pen.; this pen had wooden panels on two sides and was separated from an adjacent pen of 3.5=5 m by barred fencing. The calf was left in the pen for 30 s Ž period 1.. Then a human Žan experienced but unfamiliar human, wearing usual overalls and carrying a stick. came into the test pen and stood motionless in the centre for another 30 s Ž period 2.. The human then tried to move the calf into the corner of the pen contained by the two plain walls and attempted to contain the animal in this 2=2 m area for 30 consecutive seconds Ž period 3.. If he succeeded in keeping the calf in the Fig. 1. Experimental set-up used for the docility test.

4 4 L. Grignard et al.rapplied Animal BehaÕiour Science corner for 30 s, 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 calf was moved to another pen Ž final pen.. Each animal was tested in the presence and in the absence of four familiar peers, which were placed in the adjacent pen, following a crossover experimental design. Only 38 calves were tested Ž 20 Salers and 18 Limousine calves.. The eight calves remaining Ž two calves of each group, so four Salers and four Limousine calves., randomly chosen, were used as peers during the tests in the presence of peers Žthe four Salers were used for testing the Salers calves and the four Limousine were used for the Limousine calves.. These eight calves were placed in the testing area Ž in groups of each breed. for 3 h in the morning before the first day of testing, in order to familiarise them to this environment. Thus, 19 calves were tested, firstly in presence of peers, and secondly in absence of peers, whereas the other 19 calves were tested in the inverse order. Tests were conducted during the morning Ž from 8 to 12 h. over 4 days; half of the 38 calves Ž10 Salers and nine Limousine. were tested each day Ža quarter with peers and the other quarter without peers.. The order of testing was the same on days 1 and 3, and on days 2 and Measurements During the docility test, behavioural events were recorded on a portable microcomputer, using software developed at our laboratory Ž Le Neindre et al., The events recorded were when the calf began to stand still, walk or run; attempts to escape Žby jumping or passing the head under the fence.; beginning and end of the handling period; aggressiveness towards the handler Ž threats or attacks.; beginning and end of the periods spent in the corner; and success or otherwise of the handler in stroking the calf. From these recorded criteria, we calculated five variables: the time spent still during each of the 1st and 2nd periods Ž without human and with motionless human, respectively., the difference between these two last variables, the duration of the handling period Žwhich can vary from 30 s to 2.5 min. and the docility score. The docility score is a synthetic criterion including all the information collected over all the duration of the test. The procedure of estimation of the docility score had been set up by Le Neindre et al. Ž on a sample of 300 individuals. As several of the recorded criteria were not normally distributed, the docility score consists in 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 is continuous and ranges from 6.5 Ž the most aggressive animal. to 17 Žthe most docile animal Statistical analyses A mixed model was used, including social environment Žpresence or absence of peers., order of test presentation Žwith peers then without peers or without peers then

5 L. Grignard et al.rapplied Animal BehaÕiour Science with peers., and repetition Ž first or second docility test. as fixed factors, animal Ž breed. as a random factor, and breed Ž Salers or Limousine. as a block factor. As the factors order of test presentation and repetition had no significant effect Ž P) 0.1., they were excluded from the final model. Analyses of variance using the General Linear Model procedure of SAS Žversion 6.11, SAS, were performed for the five variables Žthe time spent still during each of the first and second periods; the difference in the time spent still between the first period and the second one; the duration of the handling period; and the docility score.. In order to evaluate the effect of the human entry on the time spent still, regardless the social environment, analysis of variance for repeated data ŽG.L.M. procedure of S.A.S.. was performed on the means of immobility duration during the first and the second periods. Data distribution and homogeneity of variance were analysed for the five variables; logarithmic transformation was used to normalise the data distribution and homogenise the variance if necessary Žhowever non-transformed mean and standard error values are presented to make the results more understandable.. Moreover, in order to study the consistency of reactions across the two docility tests Ž with or without peers., Pearson s correlation coefficient Ž r. was calculated between the docility scores obtained during the test with peers and those obtained during the test without peers. 3. Results The Table 1 summarises the results of the analyses of variances Description of the studied sample In general, the calves were weakly active during the docility tests. They spent 85.5% of time still when the human was absent and 75.8% of time still with the motionless Table 1 Effects of the social environment and of the breed on the behavioural reactions of calves in the docility test variances analyses Variable Mean"standard Effect of the social Effect of the deviation Ž. s environment F breed F UUU 1,37 1,36 Time spent still during 1st 25.66" period Ž.Ž s absence of human. Time spent still during 2nd 22.74" period Ž.Ž s motionless human. Difference in the immobility 2.92" duration between the 1st and the 2nd period Ž. s Duration of the 3rd period 99.71"32.12 U Ž.Ž s handling. Docility score Žcalculated 12.87" over all the duration of the test. Level of significance: U P F0.05; UU P F0.01; UUU P F0.001.

6 6 L. Grignard et al.rapplied Animal BehaÕiour Science human. They spent little time running regardless of the period of the test Žabsence of human: 0.2%; with the motionless human: 0.6%; handling: 3.6% of the total duration of the period.. In addition, attempts to escape were scarce Žabsence of human: 0.2; with the motionless human: 0.6; handling: 0.02., and no calves were aggressive towards the human. The handler was able to maintain 50% of the calves in the corner, and 73.7% of these calves could be stroked. The mean docility score ranged from 9.8 to First period of the test absence of human When calves were tested with peers, they spent more time still than when they were tested without peers Ž F s14.0, P-0.001; Fig , Second period of the test animal with motionless human The social environment had no significant influence on the time spent still in the presence of the motionless human Žin presence of peers: 23.4"7.4 s; in absence of peers: 22.0"7.7 s; F s1.1. 1,37. However, calves were significantly less still when the human was present than when he was absent Ž22.7"7.6 vs. 25.7"5.4 s, respectively; F s16.4, P ,36. This difference in the duration of immobility between the first and second periods was not influenced by the social environment Ž3.7" 6.3 s with peers; 2.1"5.2 s without peers; F s , Third period of the test handling The calves were easier to handle in the absence of peers, with the duration of handling being significantly shorter when calves were tested in absence of peers than in presence of peers Ž F s6.1, P-0.05; Fig ,37 Fig. 2. Influence of the social environment on the duration of calves immobility in absence of human Žperiod U UU UUU 1. in the docility test. Levels of significance: P F0.05; P F0.01; P F0.001.

7 L. Grignard et al.rapplied Animal BehaÕiour Science Ž. Fig. 3. Influence of the social environment on the duration of the handling period period 3 in the docility test. Levels of significance: U P F0.05; UU P F0.01; UUU P F Fig. 4. Correlation between docility scores obtained by calves in docility tests in presence and in absence of peers. Levels of significance: U P F0.05; UU P F0.01; UUU P F0.001.

8 8 L. Grignard et al.rapplied Animal BehaÕiour Science Docility score The social environment had no significant effect on the docility score Žin presence of peers: 12.8" 2.9; in absence of peers: 13.0" 3.2; F s ,37. The calculation of Pearson s coefficient indicated a highly significant correlation between the two docility tests Ž with peers and without peers. performed by each animal Žr s 0.6, P- 0.01; Fig Discussion This experiment shows that the presence or the absence of familiar peers has an influence on the behavioural reactions of beef calves to the docility test. The social environment modifies the behaviour of calves during the period of the absence of human just after having been separated from peers, as the presence of partners increased the duration of the test animal s immobility. According to previous studies, cattle s behaviour in a novel environment Žwhich was the situation of this 1st period of the docility test. include several components, such as escape, search of social partners, and exploration Ž De Passille et al., Concerning ambulatory activity in novel environments, it is usually considered as attempts to escape and as an indication of fear Ž Le Neindre, 1989; Kilgour, Therefore, we suggest that the visual presence of partners moderate the animal s fear responses in the novel environment. This is supported by the results of other studies showing that sight of conspecifics reduces behavioural distress. The mere presence of social partners reduced heifers behavioural signs of disturbance towards fear-eliciting stimulation Ž Boissy and Le Neindre, Ewes displayed lower fear reactions to a conspecific image of own vs. different breed Ž Bouissou et al., In red deer stags, Pollard et al. Ž found that confinement in isolation increased behavioural activities and heart rate, so was more stressful than confinement with members of the same social group. Another interpretation of our result could be the next; calves ambulatory activity in the pen in absence of peers would reflect attempts both to escape and to return to the social group, while, in presence of peers, calves ambulatory activity would only reflect attempts to escape, thus would be less. This interpretation is in agreement with that of Veissier and Le Neindre Ž who found that Aubrac heifers exposed to a novel environment in groups of four had lower ambulatory scores compared with heifers tested alone. Their explanation was that grouped and isolated heifers were equally fearful in the novel arena but differed in the way they reacted; the former stayed together in the group where they felt comfortable while the latter tried to escape in order to re-establish contact with their conspecifics. In our case, it would have been interesting to have recorded the position of the animal in the test pen, in order to know if it stayed motionless near its peers Ž as we suspect. or somewhere else in the test pen. The introduction of the human in the test pen modifies the animal s activity; it moves more during the period of the absence of human. However, the reactivity to the human is independent of the social context. Thus, it seems that the calves are more disturbed

9 L. Grignard et al.rapplied Animal BehaÕiour Science when they are in the presence of the stationary human than when the human was absent from the pen. Hemsworth et al. Ž have also found that the exposure of farm animals to a stationary human causes behavioural and physiological changes, which are characteristic of animals responses to fear-eliciting stimuli. It supports that the ambulatory activity can be considered as an indicator of the animal s level of fear. When the human is no longer still, an influence of the social environment is found; the human required more time to restrain the calf in the corner Žwhich is placed opposite to the adjacent pen containing the peers. when the conspecifics were present. Therefore, animals are more difficult to constrain in the presence of their peers. Boivin et al. Ž 1992b. have suggested that the reactions of others animals could influence the performance of the animal being tested in the docility test. Our result tends to agree with this hypothesis: the presence of peers affects the individual handling of animals within the context of the docility test. It seems likely that, in presence of its peers, the calf was motivated to stay near them, and it was thus more difficult for the human to lead the calf in the opposite direction to the peers pen. However, if the presence of peers increases the time required by the human to constrain the animal, it may not influence the animal s docility per se. It would be interesting to investigate the contribution of the social motivation in the acceptation by the animal of the human handling in the docility test. Furthermore, we found that the social environment does not affect the docility score. This docility score is a synthetic criterion established from all the events recorded during the docility test, with particular emphasis placed on the variable aggressiveness ŽLe Neindre et al., But in the animals studied in this experiment, there was no aggression displayed during the docility tests. Moreover, few attempts to escape were recorded and calves spent a very low percentage of time running. These results show that our calves were relatively calm animals. It would be interesting to examine whether they may be generalised to cattle breeds known to be more reactive toward humans, as zebus and their crossbred Ž Becker and Lobato, Another fact should be underlined; in the presence of peers, the time spent still during the first period is higher Žwhich leads to increase the docility score. than in the absence of peers, while the duration of the handling period is longer Ž which leads to decrease the docility score.. Therefore, as these two variables were included in the calculation of the docility score ŽLe Neindre et al., 1995., the effect of the social environment diminishes. Nevertheless, docility scores obtained in docility tests with peers were strongly correlated with the docility scores obtained in tests without peers. This result shows that the repeatability of the docility test is good, regardless of the social environment. It seems that the docility score provides an effective measure of the ease of handling of cattle in such a test. This study confirms the role of social partners in influencing the reactivity of individuals to the constraints imposed by the environment ŽBoissy and Le Neindre, The mere presence of peers should be considered as a factor that can modify the behaviour of domestic animals towards humans. It would be interesting to define the importance of this social factor on the cattle docility by testing different types of animals Ž according to their reactivity towards humans and their gregariousness. and different types of social environment Žaccording to the familiarity or the affinity between the tested animal and the social peers..

10 10 L. Grignard et al.rapplied Animal BehaÕiour Science Acknowledgements With many thanks to the staff of the Experimental Husbandry Farm of Marcenat for the care and maintenance of animals, and particularly to Alain Mante for his assistance during tests. We are grateful to Dr. Andrew Fisher ŽRuakura Agricultural Centre, Hamilton, New Zealand. for reviewing the first version of this paper, and to Jean-Paul Brun Ž I.N.R.A. Theix, St Genes ` Champanelle, France. for the elaboration of the software for the docility test. References Becker, B.G., Lobato, J.F.P., Effect of gentle handling on the reactivity of zebu crossed calves to humans. Appl. Anim. Behav. Sci. 53, Boissy, A., Le Neindre, P., Social influences on the reactivity of heifers: implications for learning abilities in operant conditioning. Appl. Anim. Behav. Sci. 25, Boissy, A., Le Neindre, P., Behavioural, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiol. Behav. 61, Boivin, X., Le Neindre, P., Chupin, J.M., 1992a. Establishment of cattle human relationships. Appl. Anim. Behav. Sci. 32, Boivin, X., Le Neindre, P., Chupin, J.M., Garel, J.P., Trillat, G., 1992b. Influence of breed and early management on ease of handling and open-field behaviour of cattle. Appl. Anim. Behav. Sci. 32, Boivin, X., Le Neindre, P., Garel, J.P., Chupin, J.M., Influence of breed and rearing management on cattle reactions during human handling. Appl. Anim. Behav. Sci. 39, Bouissou, M.F., Porter, R.H., Boyle, L., Ferreira, G., Influence of a conspecific image of own vs. different breed on fear reactions of ewes. Behav. Processes 38, Burrow, H.M., Measurements of temperament and their relationships with performance traits of beef cattle. Anim. Breed. Abstr. 65, De Passille, A.M., Rushen, J., Martin, F., Interpreting the behaviour of calves in an open-field test: a factor analysis. Appl. Anim. Behav. Sci. 45, Fordyce, G., Dodt, R.M., Wythes, J.R., Cattle temperaments in extensive beef herds in northern Queensland. Aust. J. Exp. Agric. 28, Grandin, T., Behavioral agitation during handling of cattle is persistent over time. Appl. Anim. Behav. Sci. 36, 1 9. Hemsworth, P.H., Barnett, J.L., Human animal interactions. In: Price, E.O. Ž Ed.., The Veterinary Clinics of North America, Food Animal Practice 3 Saunders, Philadelphia, PA, pp Hemsworth, P.H., Barnett, J.L., The effects of aversively handling pigs, either individually or in groups, on their behaviour, growth and corticosteroids. Appl. Anim. Behav. Sci. 30, Hemsworth, P.H., Barnett, J.L., Coleman, G.J., Fear of humans and its consequences for the domestic pig. In: Davis, H., Balfour, D. Ž Eds.., The Inevitable Bond: Examining Scientist Animal Interactions Cambridge Univ. Press, Cambridge, pp Kilgour, R.J., The open-field as an assessment of the temperament of dairy cows. Anim. Behav. 23, Le Neindre, P., Influence of rearing conditions and breed on social behaviour and activity of cattle in novel environments. Appl. Anim. Behav. Sci. 23, Le Neindre, P., Trillat, G., Sapa, J., Menissier, F., Bonnet, J.N., Chupin, J.M., Individual differences in docility in Limousin cattle. J. Anim. Sci. 73, Nicol, C.J., The social transmission of information and behaviour. Appl. Anim. Behav. Sci. 44, O Connor, C.E., Jay, N.P., Nicol, A.M., Beatson, P.R., Ewe maternal behaviour score and lamb survival. Proc. N.Z. Soc. Anim. Prod. 45,

11 L. Grignard et al.rapplied Animal BehaÕiour Science Pollard, J.C., Littlejohn, R.P., Suttie, J.M., Effects of isolation and mixing of social groups on heart rate and behaviour of red deer stags. Appl. Anim. Behav. Sci. 38, SAS, SASrSTAT, User s guide. Cary, NCrSAS Institute. Veissier, I., Le Neindre, P., Reactivity of Aubrac heifers exposed to a novel environment alone or in groups of four. Appl. Anim. Behav. Sci. 33,