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* Institute of Animal Husbandry and Animal Welfare, Department of Veterinary Public Health and Food Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
Equipe Adaptation et Comportements Sociaux de lUnité de Recherches 1213 sur les Herbivores, Institut National de la Recherche Agronomique, Laboratoire Adaptation des herbivores aux milieux, Centre de Recherche Zootechniques et vétérinaires de Theix, 63122 St Genés Champanelle, France
Corresponding author: claudia.schmied{at}vu-wien.ac.at
| ABSTRACT |
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3.75), whereas at least 50% of the cows in the other treatment groups did not accept it. The stationary person test did not reveal any differences between the treatment groups. In the arena test, the 3 stroked groups showed more approach behavior (median latencies to contact: from 145 to 240 s) compared with simple human presence (300 s), but stroking treatments did not differ from each other. Stroking, particularly the neck, reduced avoidance of and increased approach reactions to humans in both the home tie-stall and the arena. Increasing acceptance of being touched after being stroked on the neck suggests that this procedure should be adopted to improve routine handling of dairy cattle.
Key Words: cattle human-animal relationship tactile stimulation animal welfare
| INTRODUCTION |
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The manner of stroking (e.g., the body region onto which the tactile stimulation is directed) has received little attention, but may be influential. An uneven distribution of social licking at different body regions in cows (Sambraus, 1969), together with differing reactions of the licked animals (Schmied et al., 2005), suggests that tactile stimulation was perceived differently depending on the region. Because social licking was linked to affiliative social relationships in cattle, this could implicate that stroking the body regions licked most, like the dorsal (19%, median of total social licking) and ventral part (16%) of the neck, could be more effective for improving the relationship of cows to humans than body regions licked rarely such as the lateral part of the chest (0%). In a recent study in cattle, differences in immediate behavioral and physiological (heart rate) reactions to human stroking of body regions often or rarely licked in social licking were detected (Schmied et al., 2008). When the ventral part of the neck was stroked, cows more likely showed behavioral reactions similar to those observed during social licking (e.g., neck stretching) and had similar physiological responses (i.e., a decrease in heart rate). This variation in the dairy cattle perception of stroking different body regions leads to the question of whether this stroking has an effect on the cattle-human relationship. Different procedures were developed for testing the animal-human relationship with different human cues (Waiblinger et al., 2006). For example, the avoidance of an approaching human and voluntary approach behavior toward a stationary human are 2 measures widely used to assess the animal relationships to humans. Several tests seem necessary for assessing the animal-human relationship because they are all influenced by different emotions and motivations (e.g., fear due to isolation and novelty in an unfamiliar environment or exploratory motivation) apart from the animal-human relationship itself (de Passillé and Rushen, 2005; Waiblinger et al., 2006).
Therefore, the 2 aims were 1) to investigate whether dairy cows show less marked avoidance and more approach behavior when stroked regularly toward an experimenter as compared with cows exposed to simple human presence, and 2) to investigate if the body region stroked affects approach and avoidance behavior. We predict that cows will approach the human more and avoid less when stroked at the ventral side of the neck, an area commonly licked in allogrooming.
| MATERIALS AND METHODS |
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Treatment
The cows were divided into 4 treatment groups balanced for breed, age, state of pregnancy, number of lactations, and tethering position. There were 3 stroking groups and 1 control: in the first stroking group the experimenter (female, 175 cm, and 68 kg, unknown to the animals prior to the experiment) stroked the ventral part of the neck (neck, in Figure 1
). The second stroking group was stroked at the withers. These were body regions licked mostly in social licking of cows (Schmied et al., 2005). The third stroking group was stroked at a body region rarely licked during social licking, the lateral side of the chest (chest, Figure 1
). The experimenter approached the animals from the back by addressing them gently in a standardized manner ("cows name" and "good cow"), and then positioned herself by the left shoulder of the cow, remaining quiet for the entire procedure. The stroking treatment (d –21 to 0 in Figure 2
) was carried out for 5 min/d on 5 d/wk for 3 consecutive weeks (total 15 d for 75 min of tactile stimulation per cow). Leather protective gloves with a suede palmar side were used for the stroking, and stroking speed was between 40 to 60 strokes/min, thereby imitating the speed of social licking (Schmied et al., 2005). The control group consisted of cows exposed to simple human presence. In the presence-only treatment, the experimenter stood still by the left chest with arms by the side, using the same approach routine, time schedule, and position as in the stroking groups.
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Behavioral Tests
To detect changes in the reactions of cows to the experimenter, 3 behavioral tests measuring the reactions to a (stationary or moving) person in the home stall or a novel environment were carried out before and after the treatment with all animals of the 4 treatment groups (Figure 2
). The person who carried out the treatment was also the experimenter of these tests, and she wore the same clothing during both the treatment and the testing.
Two tests were carried out in the home environment:
In these 2 trials the cows were tested in the same place where they were tethered throughout the entire experiment.
One test was carried out in a novel environment:
APT.
The avoidance reactions were measured with a procedure used by Waiblinger et al. (2003), who conducted this test with loose-housed dairy cows restrained in the feed barrier. We modified the test for tethered cows.
The test procedure started with the experimenter positioned in the feeding aisle 1.5 m in front of a cow standing in her home tie-stall. The experimenter held her arm overhand (the backside of the hand was directed to the muzzle) in an angle of 45° in front of the body, looking at the muzzle, and waited for attention of the focus cow. Then, the experimenter approached the cow slowly with constant speed (1 step/s, practiced before the experiment) from the front until the animal withdrew or until the cow was touched. The distance between the back of the experimenters hand and the muzzle at the moment of withdrawal was determined (10 cm resolution) or the time (s) a cow tolerated touching was recorded. Withdrawal was defined as stepping back or turning the head away (>90°). If the cow accepted being touched at the muzzle, the experimenter ran the hand to the cheek and tried to stroke the cheek for up to 6 s. Table 1
lists and defines the reactions and the scores assigned to each animal. High interobserver reliability (r
0.97, P < 0.001) on these criteria was observed in another study (I. H. Windschnurer, C. Schmied, S. Waiblinger, Inst. Anim. Husb. and Anim. Welf.; X. Boivin; unpublished data).
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SPT.
This second test was carried out according to Munksgaard et al. (1997). In the home tie-stall, the experimenter (hands in pockets) walked slowly (1 step/s) toward a position in front of the standing cow. The test started when the experimenter had reached the test position 0.75 m in front of the bar to which the cow was tethered. During the actual test situation, the experimenter (hands in pockets) stood still for 60 s. The position of the cows was videotaped and scored every 5 s, beginning 5 s after the test had started, according to the criteria listed in Table 2
. One overall score per animal, averaged over the 12 scans, was calculated. The SPT was carried out once before the treatment (d –27) and for the second time immediately after the treatment (d 1; Figure 2
). Because no difference was observed between the treatment groups in these 2 test sessions, this test was not repeated.
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Latencies were measured for approaching within a distance of 3 m, 1 m, and to establish contact with the experimenter (cow sniffed at or licked the experimenter). The experimenter recorded the latencies directly by using a stop watch with interval memory in her pocket and recorded these values directly after the end of the test before the next cow was tested. The tests were video-recorded, but due to technical problems no additional observation was possible. The arena test was carried out 3 times, once before (d –26 to –25) and twice after the treatment (d 2 to 3 and wk 4; Figure 2
). Unfortunately, it was not possible to test the animals later on.
Statistics
Statistical analyses of behavioral test data were carried out with the software package SPSS, version 14.0. Due to nonnormal distributions, heterogeneity of the variances, and some measures on an ordinal scale, behavioral traits were analyzed using nonparametric statistics. Testing for differences between the 4 groups within 1 test session was done by means of the Kruskal-Wallis test followed by the Mann-Whitney test. The differences between the individual test sessions (development of reactions over time) within each treatment were tested by means of the Friedman test and the Wilcoxon test. Results with a P
0.05 were considered significant, whereas those with P > 0.05 but
0.1 were described as tendencies.
| RESULTS |
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3.75, which indicates that at least 75% of the animals accepted being touched on their heads after the ventral part of the neck had been stroked during the treatment. By contrast, at least 50% of the cows in the other treatment groups did not accept being touched on their heads (median: 4.00). The effect disappeared after 4 mo (P = 0.645). The 3 other treatment groups did not differ significantly from each other in the APT (Table 3
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SPT
The 4 treatment groups did not differ in the scores of the SPT on d –27 (P = 0.395) and d 1 (P = 0.671, Table 3
). In general, the scores of this test were rather low (no avoidance) in our 60 cows (median, 25th to 75th percentile: first test: 2.17, 1.75 to 2.92; second test: 2.00, 1.33 to 2.58).
Accordingly, there was no significant change between the time before and after the treatment (Table 3
). Because this test did not show any difference between the 4 treatment groups and no significant change over time, it was only performed twice.
Arena Test
In the first arena test before the treatment period (d –26 to –25), the latencies to come within a distance of 3 m, 1 m, or to establish contact with the experimenter did not differ among the 4 treatment groups (P > 0.471, Table 4
).
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0.05).
In the second arena test immediately after the treatment (d 2 to 3), cows of all 3 stroking groups approached to sniff at or lick the experimenter quicker than the 300 s for control cows (240 s, neck: P = 0.07; 186 s, withers: P < 0.01; 145 s, chest: P < 0.01, Table 4
). Yet, the 3 stroking groups did not differ from each other (P > 0.354). After 4 wk, cows stroked at the neck were faster (184 s) to approach the human compared with the controls (300 s; P < 0.05). After 4 wk, despite higher median the 75th percentile level was below 300 s in the neck-group in contrast to the other stroking groups, which indicated that at least 75% of the animals having been stroked at the ventral part of the neck during the treatment approached to sniff at or lick the experimenter in the arena.
The 4 groups differed in how the response in the arena test changed over time (Table 4
). Immediately after the treatment (d 2 to 3) cows of all 3 stroking groups approached within a distance of 3 m, 1 m, and established contact with the experimenter quicker than before (10, 67, and 240 s, neck: P < 0.01; 12, 95, and 186 s, withers: P < 0.01; 25, 83, and 145 s, chest: P < 0.05, respectively). These effects persisted over 4 wk. In contrast, there was no change in the control group, except for a reduction in the latency to come within 1 m 4 wk after the treatment compared with before treatment (92 vs. 300 s; P < 0.05).
| DISCUSSION |
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In the APT, the experimenter approached the cows from the front in their normal tethered position and, if possible, touched their muzzles. When the cow accepted contact, the experimenter ran the hand to the cheek and tried to stroke the cheek. The head area of cattle is particularly sensitive; it is involved in most social interactions and tactile contact of longer duration was seen during affiliative social interactions (Schmied et al., 2005). The specific result observed for stroking the neck, as compared with the other regions, suggests that stroking this region is effective to habituate cows to such touching. This result could be explained by habituation to being touched in the head region because the hand was closer to the head when stroking the neck compared with the other treatments. On the other hand, behavioral and physiological data suggest a relaxation state in the cows being stroked at the ventral part of the neck (Schmied et al., 2008).
The response to the experimenter during the APT may reflect an improvement of the animal-human relationship based on the rewarding effect stroking the ventral part of the neck. Stroking the body regions licked most (neck and withers) elicited more behavioral reactions that were similar to those observed during social licking (neck stretching, ear hanging) as compared with stroking the chest (Schmied et al., 2008). Additionally, stroking the ventral neck was the only treatment effective in eliciting a physiological response because it resulted in a significant decrease in heart rate (3 beats/min). Finally, the different responses of cows to a human approaching them from the front cannot be explained by the position of the experimenter during the treatment because the person stood by the left shoulder of the cows in all 4 treatment groups.
By contrast to the neck, no differences were found for stroking the lateral side of the chest in the APT compared with the control. This result indicated that this body region may be too far from the head for a generalization of the response to being stroked there or that stroking this body region probably does not have the same rewarding value as observed for the neck. The latter interpretation could explain why this body region is almost never licked during intraspecific social grooming.
SPT.
In the second test conducted by a stationary person in the home environment, no difference was found between the 3 stroking groups and the control as well as between the different stroking groups.
This lack of difference between the treatment groups may be explained by the cows being used to different people present in the feeding aisle at a distance similar to the distance between the experimenter and the barn in the SPT. Munksgaard et al. (1997) found differences when comparing the effects of positive (stroking, speaking friendly, offering food) and aversive (sudden movements, hitting with hand) handling treatments. In the beginning of their study, cows scored 3.4, after aversive treatment 3.1, and after gentle treatment 2.2 (all scores for the home stall). Still, the median avoidance score of our 60 cows was 2.17 before the treatment, similar to the value attained after gentle treatment in the study of Munksgaard et al. (1997). This suggests that this test may show differing results only for more fearful animals. Thus, if cows were not very fearful, this test may not be sufficiently sensitive for measuring effects of positive handling (Waiblinger et al., 2006).
Test in the Novel Environment: Arena Test
In the arena test, cows exposed only to the presence of the experimenter took longer to approach than any of the stroked treatments. Yet, cows did not differ significantly in time to approach based on the region stroked. Thus, our hypothesis on stroking body regions mostly licked in intraspecific social grooming being more effective for the purpose of improving the animal-human relationship, indicated by an increased approach of the cows to humans, was not supported in this test situation.
Stroking any region could have simply led to a habituation to the close presence of the human, as suggested by Boivin et al. (1998). The distance cows keep to humans was greater for cows that had experienced negative handling and less when they had experience with gentle contact including stroking (Munksgaard et al., 1997; Waiblinger et al., 2003). Thus, stroking in general may help reduce the approach distance such that cows are quicker to approach the human.
The arena test, also called a standard human approach test when it included a motionless human stimulus, was developed to test fear of humans in a standardized environment (Hemsworth and Coleman, 1998). The test conditions could possibly inhibit the expression of behavioral differences according to the stroked body regions because the test was designed to detect changes in another dimension of the animal-human relationship (i.e., fear of humans) and less the positive dimension of the relationship toward humans. Through testing in the arena, we may have potentially confounding factors of tests in an unfamiliar environment (e.g., pretest moving to the arena, novelty, social isolation) possibly overriding the effect depending on the body region stroked. The standard human approach test was generally performed with a first period of few minutes of familiarization to the test arena before the human entered the test pen (Hemsworth et al., 1996). But, in our experiment, the familiarization period was excluded due to time constraints and to standardize the starting distance of cows to the experimenter. This may have increased the impact of the confounding factors. Another possible explanation could be that the effects of stroking various body regions found in the home environment might not be generalized to a novel situation because cows may react according to the handling (stroking) only in the location of this handling (de Passillé et al., 1996; Jago et al., 1999). Nevertheless, our animals did generalize their perception of the human to another location when they were stroked as compared with experiencing mere presence of the human in the home pen.
Comparison of the Behavioral Tests
All tests had the same underlying principle. Animals that are the most fearful of humans will keep the greatest distance from them. Alternatively, animals which are the most confident might approach themselves, or allow a human to approach (de Passillé and Rushen, 2005). However, the discrepancies between the tests point to a difference in the perception of the different test situations. Such differences in the perception of cows are most likely related to differences in test conditions, namely variation in behavior of the experimenter (stationary or approaching) and the familiarity of the environment and the test location (Waiblinger et al., 2006). In general, tests assessing approach behavior and tests assessing avoidance reactions do not appear as alternative ways of measuring the same thing, but rather measure different dimensions of the relationship with humans (de Passillé and Rushen, 2005; Waiblinger et al., 2006). For example, Hemsworth et al. (2000) found negative associations of avoidance distances to an approaching human with positive behavior of milkers (positive dimension), whereas approach behavior in a standard arena test correlated negatively only with negative behavior of milkers (fear). This could be an explanation for the detection of differences between the stroked body regions only in the APT.
General Discussion about the Effect of Stroking on Cow Behavior
In cattle, few studies have tried to demonstrate the effect of gentle tactile stimulation per se, and Jago et al. (1999) with dairy calves as well as Boivin et al. (1998) with beef calves failed to observe such an effect despite 2 wk of daily stroking (without other forms of contact) in early life. In this last study, very few animals approached the familiar stationary person at all. Our study is the first to demonstrate the beneficial effects of stroking without other forms of contact for cattle.
Possible reasons to explain the difference between our results and those of previous studies are numerous and include the duration of the stroking period or the social environment of the treatment. But, one difference in the present experiment is that dairy cows were the subjects. Through the milking process and the tie-stall housing, dairy cows were used to close human presence and contact, suggesting they may have had a different perception of stroking as compared with the calves in previous studies. Indeed, calves stroked or brushed from an age of few days on were not habituated to close human presence before this treatment (Boivin et al., 1998; Jago et al., 1999). This interaction between the level of human-animal relationship and the perception of the cows should be considered in further studies, in particular in cattle with less human contact. Another possible important difference arises from the body regions stroked. In Jago et al. (1999), the body regions stroked were mainly the dorsal and lateral side of the neck and the shoulders (J. G. Jago, Dexcel Ltd., Hamilton, New Zealand; personal communication), and in Boivin et al. (1998) the backs of the calves were brushed. Results of our study show clearly that the best effect for improving the animal-human relationship, via decreasing avoidance reactions, was observed for stroking the ventral part of the neck.
Practical Implications and Future Research Questions
The ratio between positive and negative interactions is a decisive factor in the cattle-human relationship [i.e., necessary negative interactions due to farm management should be outweighed by rewarding elements of human-animal interactions (Hemsworth, 2003)]. Stroking the ventral part of the neck displayed most immediate beneficial effects for the cows (Schmied et al., 2007). Accordingly, the results of our present study show that stroking cows, particularly on their ventral neck, decreased avoidance of the human and facilitated touching the animals. This could make them easier to handle in daily routine with lower risk of accidents and improve their welfare. In commercial dairy farms for example, fewer avoidance reactions of the cows in test situations were related to decreased stepping during milking (Rousing et al., 2004), and Waiblinger et al. (2004) showed that gentle treatment including stroking (mainly the ventral neck) decreased kicking of cows during rectal palpation. Furthermore, the persistence of the effect of stroking the ventral neck over at least 8 wk without further stroking denotes that repeated tactile stimulations for a few minutes a day for 3 wk could have a long lasting effect on the reactions of dairy cows toward humans. Finally, because social licking, which is often directed to the ventral part of the neck accompanied with neck stretching and lowest heart rate of the licked animal (Schmied et al., 2005), is positively related to milk production in cows and weight gain in calves (Wood, 1977; Sato, 1984), stroking of this body region could have positive effects on health, well-being, and production of dairy cows.
In studies of loose-housed dairy herds, a higher percentage of cows accepting touching on their head was related to more positive behaviors of the stock people (talking quietly, petting, touching) toward their animals (Waiblinger et al., 2003); those farmers providing much gentle tactile interaction often targeted the ventral neck and start with such interactions early in the lives of calves (S. Waiblinger, personal observation). Nevertheless, general conditions might vary across farms and across categories of cattle. Adult dairy animals are handled twice or three times daily, whereas calves, heifers, or beef cattle often are handled less regularly, and occasions for handling are limited if interacting with the animals does not have priority for the stock person.
In future studies, stroking the ventral neck could be applied to loose-housed dairy or beef cattle with a higher level of fear of humans to investigate whether stroking this body region is effective in animals which are more naïve to human contact. Additionally, testing with unfamiliar experimenters would add information about whether stroked cows generalize their reactions across people. Recent studies found similar responses of cattle to familiar and unfamiliar persons after aversive as well as gentle handling (Krohn et al., 2001; Breuer et al., 2003), although cattle clearly are able to discriminate between people (Rybarczyk et al., 2001) and react differently according to former handling experiences (de Passillé et al., 1996; Munksgaard et al., 1997). Additionally, it could be interesting to test other possibly sensitive body regions that are far from the head (e.g., the basis of the tail, which is often used by farmers trying to calm down cows) using the same experimental design. As human contact was effective in young animals (Boivin et al., 2003), stroking different body regions could be tested in dairy and beef calves during these sensitive periods using regions of the body which are licked by the mother during suckling.
| CONCLUSIONS |
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| ACKNOWLEDGEMENTS |
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Received for publication May 11, 2007. Accepted for publication October 19, 2007.
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