- Email: [email protected]
Stroking of different body regions by a human: Effects on behaviour and heart rate of dairy cows
Applied Animal Behaviour Science 109 (2008) 25–38 www.elsevier.com/locate/applanim
Stroking of different body regions by a human: Effects on behaviour and heart rate of dairy cows Claudia Schmied a, Susanne Waiblinger a,*, Theresa Scharl c, Friedrich Leisch c, Xavier Boivin b a
Department of Veterinary Public Health and Food Science, Institute of Animal Husbandry and Welfare, University of Veterinary Medicine Vienna, Veterina¨rplatz 1, 1210 Vienna, Austria b URH-ACS, INRA, Laboratoire Adaptation des herbivores aux milieux, CRZV de Theix, 63122 St Gene´s Champanelle, France c Department of Statistics and Probability Theory, Vienna University of Technology, Wiedner Hauptstraße 8-10/1071, 1040 Vienna, Austria Accepted 29 January 2007 Available online 9 March 2007
Abstract From observations of intra-specific social grooming in cattle and studies on human stroking in other species, we hypothesised that cows’ reactions to human stroking differ depending on the body regions being stroked. Moreover, we tested, whether cows ‘reactions to stroking change with the animals’ experience of stroking. Sixty dairy cows were stroked in three different body regions, i.e. the withers, W, neck ventral, NV (both licked often in social grooming) and the lateral chest, LC (licked rarely), in a balanced order during 10-min sessions. Behavioural reactions and heart rate during stroking as well as reactions to the human just after stroking were recorded. Two test sessions were carried out with 3 weeks of treatment in-between. During this period, the cows were randomly allocated to four treatment groups: three groups received 5 min of daily stroking in either W, NV or LC and the last one (control group) was exposed to simple human presence. During stroking W and NV, cows showed longer neck stretching and ear hanging than during stroking LC (P < 0.001). Moreover, ear hanging was shown longer when W was stroked as compared to NV (P < 0.001), but neck stretching was observed longer during stroking NV as compared to W only after the treatment period (P < 0.01). In the first test session, more animals showed head shaking and head throwing during stroking W and NV than LC (P < 0.01), whereas in the second test session these behaviours were observed only in few animals. In the first test session heart rate was higher during stroking W than the other body regions (P 0.01). In the second test session, the lowest heart rate was found during stroking NV (P < 0.05). Finally, contact with the experimenter following stroking differed for the three body regions
* Corresponding author. Tel.: +43 1 25077 4905; fax: +43 1 25077 4990. E-mail address: [email protected] (S. Waiblinger). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.01.013
26
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
stroked in both test sessions (first: P = 0.06, second: P < 0.01); contact was shortest for LC. When comparing both test sessions, stretching the neck and ear hanging increased (P < 0.001), while head shaking and head throwing decreased (P < 0.05); there was no difference for heart rate and contact with the experimenter. The four treatments had no influence on reactions to stroking. To conclude, stroking of body regions often licked during social grooming led to more responses than stroking the one licked rarely. Some reactions, such as stretching the neck, are also observed during social licking. This suggests that cows may in part perceive human stroking of body regions often licked similarly to social licking. This knowledge could be of interest for an improvement in quality of human–cattle interactions. # 2007 Elsevier B.V. All rights reserved. Keywords: Cattle; Tactile stimulation; Human–animal relationship; Social licking
1. Introduction Stroking and other gentle tactile contact is used regularly during daily stockperson–animal interactions in dairy cattle husbandry (Waiblinger, 1996; Hemsworth et al., 2000; Breuer et al., 2000). Stroking by humans as part of gentle contact has also been used in experimental studies in many farm animal species, e.g. chicken, goats, sheep, pigs, or cattle (for review e.g. Boivin et al., 2003), but mostly it was combined with other forms of contact like talking or offering food. Gentle handling involving stroking has shown to decrease farm animals’ fear of humans (Rushen et al., 1999), thereby having beneficial effects, such as improved ease of handling (Boivin et al., 1992), reduced distress behaviour, e.g. vocalisations in the presence of a human during isolation (Tallet et al., 2005), increased productivity (Seabrook, 1994), improved meat quality (Lensink et al., 2000, 2001), and improved immune response reducing the risk of disease (Gross and Siegel, 1982; Caroprese et al., 2006; for review Waiblinger et al., 2006). Specific and immediate reactions to gentle tactile contact were demonstrated in various studies, but mostly investigated in other than farm animal species (for review McMillan, 1999). In particular, stroking decelerated the heart rate in horses, dogs and rats (Lynch et al., 1974; Kostarczyk, 1992; Kurosawa et al., 1995; Lund et al., 1999) and evoked various particular types of behaviour interpreted by the authors as indicators of a relaxation state (horse: head lowered, eyes half closed, standing motionless, Lynch et al., 1974; rat: less locomotor activity, Uvna¨sMoberg et al., 1996). In several species, e.g. rats, tactile stimulation was found to trigger oxytocin release, thereby physiologically leading to a lower heart rate, lower blood pressure and lower cortisol levels as immediate effects in addition to long term effects, e.g. effects on social bonding (Uvna¨s-Moberg and Petersson, 2005). Furthermore, tactile stimulation was able to decrease behavioural and physiological responses induced by fear and painful stimuli in dogs (Anderson and Gantt, 1966; Lynch and Gantt, 1968; Lynch, 1977; Hennessy et al., 1998). In cattle, too, there is some evidence suggesting direct beneficial effects of stroking by humans, e.g. stroking combined with gently talking was able to reduce the heart rate increase of dairy cows during an aversive treatment (Waiblinger et al., 2004). Similarly, cows showed during isolation lower heart rates when they were brushed by a human than in situations without human contact (Rushen et al., 2001). However, in both of these studies the effect of gentle tactile contact was not distinguished from simple human presence, nor were different body regions considered. These effects of tactile stimulation by a human are consistent with results found in intraspecific social grooming in animals. The heart rates of pig-tailed macaques and cattle being groomed/licked by conspecifics decreased, for example (Boccia et al., 1989; Sato and Tarumizu,
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
27
1993). In cattle, the time an animal is being licked was positively related to milk production in cows or live weight gains in calves (Wood, 1977; Sato, 1984). However, observations of intraspecific social grooming and experimental studies on tactile stimulation by humans suggest that the effects could depend on the body region onto which it is directed. In horses, more than 50% of mutual nibbling is performed at the withers (Feh and de Mazie´res, 1993); a human scratching a horse in imitation of nibbling led to a lower heart rate and more affiliative behaviour when performed at the withers than when performed at other body regions (Feh and de Mazie´res, 1993; McBride et al., 2004). Similarly in cats, mutual face rubbing is known to fulfil a social bonding function (Bradshaw, 1992) and stroking by humans in the body region preferred for this intraspecific contact has been found to lead to more affiliative responses than contact with other body regions (Soenichsen and Chamove, 2002). There is no study about such possible differences in reaction to human tactile contact for cattle. However, several authors described an uneven distribution of social licking (Sambraus, 1969; Kiley-Worthington and de la Plain, 1983). A recent study found that 64% of social licking between adult cows is directed to the neck, especially the dorsal and ventral part (Schmied et al., 2005). Furthermore, the reactions of the licked animals differed depending on the body region licked; the heart rate was found to be lower during social licking of the ventral part of the neck than of other neck regions (Schmied et al., 2005). Therefore the aim of this study was to investigate whether dairy cows’ behavioural and physiological reactions to human stroking of different body regions often or rarely licked in social grooming differ. We hypothesized that stroking of body regions often licked would lead to more behavioural reactions, similar to those shown by licked cows, and to lower heart rate, as compared to stroking a rarely licked body region. In addition, the direct reactions to stroking were measured again after a treatment period, to find out, whether a previous experience with being stroked in special body regions could have an effect on the cow’s reactions. 2. Animals, material and methods 2.1. Animals and housing The experiment was carried out from January 2003 to March 2003 on 30 Brown Swiss and 30 Austrian Simmental cows (age: 4.7 years 1.8, average milk yield: 5700 kg milk/year) of the dairy herd of the University of Veterinary Medicine’s Teaching and Research Estate. The experimental cows were randomly selected from a herd of 80 cows, excluding, however, cows in late pregnancy (dry cows, 4–6 weeks before parturition). All cows were reared under the same housing (loose housing, pasture during summer) and management conditions. The whole year round the cows were tied starting with the first lactation, except for some weeks during the dry period when they were pastured. During the experiment the cows were milked twice a day by their regular milkers. The cows were used to different stockpeople and to frequent human contact, but they were not used to being stroked regularly. However, during the experiment, human contact was reduced to daily management routines or necessary treatment. 2.2. Experimental design According to previous research on social licking (Schmied et al., 2005) three body regions were chosen for comparison: the withers (W) and the neck ventral (NV), which are licked most often, and one body region licked rarely (the lateral chest [LC]). The location of the three body regions is shown in Fig. 1. Two test sessions for measuring the cows’ immediate behavioural and physiological reactions in response to stroking were carried out at an interval of 3 weeks. During these 3 weeks, cows were allocated to different treatment groups, which involved stroking of these three body regions or human presence, respectively.
28
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Fig. 1. Location of the three body regions stroked and position of the heart rate equipment (black girth).
2.2.1. First test session In the first test session each of the two experimenters (one female, 175 cm, 68 kg, and one male, 180 cm, 80 kg), who were unknown to the cows until then, stroked half of the test session animals. Both wore overalls and jackets of the same colour (different to the caretakers) as well as leather working gloves with a suede palmar side for stroking the cows during the entire experiment. Before the start of the test session, the experimenters harmonized speed and pressure of stroking. Speed of stroking was between 40 and 60 strokes/min, thereby imitating the speed of social licking found earlier (Schmied et al., 2005). Both used a similar medium pressure for all stroking. The test session for the 60 cows took place on three successive days, i.e. 20 cows were tested per day. Test sessions started 30 min after the end of morning milking and stopped at least 30 min before evening milking (incl. a break around midday when cows were fed). Each of the 60 cows was stroked in one 10-min session in all three body regions for 2 min each followed by a 1-min pause before moving on to the next the body region. All the six different possible sequences of the three body regions were applied with each of them being used on 10 cows. At the beginning of the 10-min procedure the experimenter approached the cow from the back by addressing her gently in a standardized manner (‘‘cow’s name’’ and ‘‘good cow’’), and then walked slowly to the left chest of the cow, keeping quiet throughout the entire test session. During the first minute of the test session the experimenter stood motionless beside the cow, arms by the side. This was followed by 2 min of stroking body region 1; 1 min standing motionless beside the cow, hand resting on the chest; 2 min stroking body region 2; 1 min standing motionless beside the cow, hand resting on the chest again; 2 min stroking body region 3; 1 min standing motionless beside the cow, arms by side at the end. The order of body regions was evenly distributed on the basis of the experimenter’s identity and cows’ breed, age and status of gravidity. 2.2.2. Treatment The 60 cows were divided into 4 groups balanced for breed, age and gravidity. In three groups either the withers (WL = long term group W) or the neck ventral (NVL = long term group NV) were stroked, or the lateral chest (LCL = long term group LC). Cows were stroked for 5 min/day on 5 days per week in 3 consecutive weeks (a total of 15 days). One group (control) was not stroked, but the experimenter stood still by the animals with arms by the side, using the same time schedule. The treatment was carried out by the female experimenter of the previous test session and stroking was done in the same manner as described there. 2.2.3. Second test session The procedure was performed as described for the first test session by the female experimenter. One cow from the NVL treatment group got sick and died before the second test session. All remaining 59 cows were stroked in a balanced order, taking into consideration the treatment group they belonged to. 2.3. Behavioural observations The behaviour of the cows was videotaped during the test sessions. The camera was located in the feeding path and the cow was recorded from left and front. The behaviour was observed continuously from video with the observational software The Observer Video ProTM, Noldus Information Technology, NL.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
29
Table 1 Definition of behavioural parameters used for observation in both test sessions Behavioural parameters
Definition
Stretching the neck
Positioning neck and head in an outstretched line, either up, down, or forward; duration in seconds Pinna/external ear pendulous; duration in seconds Consecutive quick movements of the head; frequency Head and neck is thrown quickly in a certain direction once, either quickly up and down, or to the side; frequency Top of the head is brought up quickly against the experimenter; frequency Bringing the muzzle near the experimenter, <5 cm; duration in seconds Touching the experimenter with the tongue; duration in seconds Front head resting against the experimenter with continued contact; duration in seconds Softly rubbing the head up and down the body of the experimenter; duration in seconds
Ear hanginga Head shaking Head throwing Butting Sniffing at b Lickingb Head leaningb Head rubbingb a
For ear hanging only the one ear that was visible throughout the test session was observed; it was mostly the left one; due to head movements, however, the right ear was visible and observed sometimes. b These parameters were combined for further analysis in one variable of soft physical ‘‘contact with the experimenter’’ and were calculated for the pause minutes after stroking only.
The main focus was on the head area because cattle use mostly head movements and postures for social interactions (Schloeth, 1961; Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983; Schmied et al., 2005). Table 1 lists and defines the behavioural parameters recorded. Inter-observer-reliability was tested with three different observers. The behaviour of 8 cows randomly chosen from all 60 cows was observed from video. Spearman rank correlation coefficients were calculated. Reliability was high with coefficients ranging from 0.92 to 1.00. 2.4. Heart rate During the test session, heart rate was recorded by means of a commercial heart rate monitoring system (horse trainer transmitters and S810 monitors from Polar Elektro Oy, Helsinki, Finland), attached to identical horse girths and fitted to the cows (see Fig. 1 for position). The spots where the electrodes were placed were not shorn or shaved but electrode gel was applied liberally to ensure contact and an additional elastic girth kept the transmitter in place. In the week before the experiment the cows were made familiar with the entire procedure by putting the equipment on them twice for about 2 h, which corresponds to the longest duration cows had to wear it during tests. During the experiment the equipment was fitted on the cows at least 30 min before the start of a test session. Beat-to-beat intervals were measured and the average heart rate calculated for the phases: ‘‘before’’ without human presence (the first 10 min after the heart rate equipment had been put on and the last 10 min before the start of the test session were excluded; usually the 10-min timeframe out of a 20–10-min period before the test session was used; another 10-min timeframe was used only when the heart rate measurement graph showed too many irregularities); ‘‘first minute’’ of the test session, i.e. standing still beside the cow without touching her, and the 2 min of stroking each body region (NV, W, LC). In the second test session the heart rate monitor of one cow failed and therefore the data of this cow were not included in the analysis. 2.5. Statistics For statistical analyses of behavioural data the software package SPSS1, Version 11.5 was used. Due to non-normal distributions and variances’ heterogeneity behavioural parameters were analysed by nonparametric statistics (Siegel, 1997). The Friedman test was used to test for differences between body regions of each cow. In the case of significant differences (P 0.05) between the body regions, each pair of body regions was compared using the Wilcoxon test (Z statistic given in the results). Because of independent data
30
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
the Kruskal–Wallis test was used to test the effects of the treatment for each body region stroked; and in case of significant differences (P 0.05) each pair of treatments was compared by using the Mann–Whitney U-test. For rarely occurring behavioural reactions the number of animals which showed this behaviour was used for the calculation with the Cochran-Q test for dependent data rather than the frequency. In the case of significant differences the McNemar test was used to compare pairs of body regions. For testing on treatment effects we used a x2-test for independent data. The heart rate was analysed with the statistical computing environment R version 2.0.1 (R Development Core Team, 2004). We fitted a mixed-effects model (Pinheiro and Bates, 2000) to heart rate data with random effects for each cow and fixed effects for the different body regions stroked and the different orders of stroking (F-value of the model and t-values for comparisons of pairs of body regions given in the results). Significant differences between the body regions stroked were found. The order of stroking, however, did not result in any differences. Therefore these data are not presented in the results.
3. Results 3.1. First test session 3.1.1. Behavioural reactions The cows differed in their reactions to stroking of the three body regions (Table 2). They stretched their necks longer during stroking both the W (Z = 4.68, P < 0.001) and the NV (Z = 4.81, P < 0.001) than LC, where only six cows showed neck stretching at all. The duration of ear hanging was longer when the W was stroked as compared to the NV (Z = 3.42, P < 0.001). It was much shorter when the LC was stroked (as compared to W: Z = 6.53, P < 0.001 and NV: Z = 6.20, P < 0.001). Head shaking and head throwing occurred only rarely during stroking; most of the cows did not express these behaviours at all, and for those few animals that did, frequency was low, i.e. the median at each body region was 2 (maximum: 7). Nevertheless, head shaking was performed by more cows when the W was stroked (P < 0.01) and also the NV (P < 0.01) as compared to LC. More cows showed head throwing when the W was stroked as compared to the NV (P < 0.01) and, in tendency, as compared to LC (P < 0.1). Table 2 Behavioural parameters in the first test session, observed at the three body regions (withers, neck ventral and lateral chest), body regions with different letter (abc or def) differ significantly, N = 60 Behavioural parameters Stretching of the neck (duration in s); median (25–75 percentiles) Ear hanging (duration in s); median (25–75 percentiles) Head shaking; number of animals Head throwing; number of animals Butting; number of animals Contact to experimenter (duration in s); median (25–75 percentiles) abc, Wilcoxon-test; def, McNemar-test. a x2-test. b Friedman-test, d.f. = 2. c Q-value. d Cochran Q-test, d.f. = 2.
Withers
Neck ventral
Lateral chest
Value
P
0 b (0–0)
29.545
a
0.000b
0.8 a (0–17)
3.7 a (0–28)
51 a (28–94)
32 b (20–65)
6 c (0–19)
82.279a
0.000b
16 d 20 d 3 3.5 a (0–12)
18 d 8e 1 3.3 ab (0–9)
6e 12 de 0 0.5 b (0–7)
12.087c 10.182c 3.500c 5.670a
0.002d 0.006d 0.174d 0.059b
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
31
The number of animals expressing butting was extremely low and was not affected by the body region stroked. The duration of contact with the experimenter during the pause after stroking tended to differ depending on the body regions stroked before, with contact being longer after stroking the W (Z = 2.52, P < 0.05) and – as a tendency – the NV (Z = 1.79, P = 0.07) as compared to the LC. 3.1.2. Heart rate Heart rate differed between periods investigated (Fig. 2A). Compared to the period before the test session (67.3 0.9 beats/min; average S.E.M.), heart rate was higher in the first minute of the test session when the human stood still beside the cow (70.3 1.2 beats/min, t = 4.18, P < 0.001) and during stroking the three body regions (W: 71.7 1.4, t = 6.19; NV: 69.9 1.1, t = 3.73; LC: 69.3 1.2, t = 2.81; for all body regions: P < 0.01). During the test session, cows had a higher heart rate when the W was stroked as compared to the NV (t = 2.46, P 0.01) or LC (t = 3.37, P < 0.001). Additionally, heart rate was higher when the W was stroked than in the first minute of the test session (t = 2.01, P < 0.05). This was not the case for the other body regions stroked. 3.2. Second test session The different treatments had no effect on neck stretching independent of the different body regions being stroked (x2 < 3.35, P > 0.34), nor on ear hanging (x2 < 4.47, P > 0.22), contact with the experimenter after stroking (x2 < 3.34, P > 0.34), head throwing (x2 < 3.85, P > 0.28), butting (no statistics calculated by SPSS because of constant value) or heart rate (F 3,54 = 0.35, P = 0.79). For head shaking there was also no significant effect during stroking the NV (x2 = 5.38, P = 0.15) and the LC (x2 = 3.27, P = 0.35). The only significant result was found for head shaking during stroking the W (x2 = 7.92, P < 0.05). More animals (four cows) of the control group showed head shaking than of the NVL (0; x2 = 4.33, P < 0.05) and LCL group (0; x2 = 4.62, P < 0.05). Due to this low number of animals and the lack of a difference in all other behaviours and body regions, the second test session was analysed without considering the treatment groups. 3.2.1. Behavioural reactions Cows again reacted differently to stroking depending on the body regions (Table 3). Cows stretched their necks longer when the NV was stroked as compared to the W (Z = 2.92, P < 0.01). Moreover, the duration of neck stretching was much shorter when the LC was stroked (as compared to NV: Z = 5.55, P < 0.001, and W: Z = 5.05, P < 0.001), with most cows (55) showing no stretching at all. As in the first test session, the duration of ear hanging was longer when the W was stroked than the NV (Z = 5.45, P < 0.001), and it was again much shorter when the LC was stroked (compared to W: Z = 6.57, P < 0.001 and NV: Z = 5.87, P < 0.001). Only few animals were performing head shaking, and for those animals the frequency was also very low, i.e. the median at each body region was 1 (maximum: 5). Nevertheless, head shaking was observed in more cows when the NV was stroked as compared to LC (P < 0.01). The number of animals performing head throwing and primarily butting was extremely low and did not show any difference for the body regions stroked. Duration of contact in the pause after stroking differed significantly between the body regions; after stroking the NV more contact with the experimenter was found compared to LC (Z = 2.42, P < 0.01), W lay between both.
32 C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Fig. 2. Heart rate (mean S.E.M.) during stroking the three body regions (withers: W, neck ventral: NV, lateral chest: LC) and during phases before the test session (before) and the first minute of test session (1st min), phases/body regions with different letters (abc) differ significantly (P 0.05). (A) First test session, N = 60. (B) Second test session, N = 58.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
33
Table 3 Behavioural parameters in the second test session, observed at the three body regions (withers, neck ventral and lateral chest), body regions with different letter (abc or def) differ significantly, N = 59 Behavioural parameters Stretching of the neck (duration in s); median (25–75 percentiles) Ear hanging (duration in s); median (25–75 percentiles) Head shaking; number of animals Head throwing; number of animals Butting; number of animals Contact to experimenter (duration in s); median (25–75 percentiles)
Withers
Value
P
7.3 b (0-31)
Neck ventral 23.8 a (0–52)
Lateral chest 0 c (0-0)
49.333a
0.000b
86 a (51–107)
42 b (21–72)
10 c (0–30)
76.025a
0.000b
6 de 4 1 2.1 ab (0–8)
11 d 3 0 3.3 a (0–9)
1e 3 0 0 b (0–6)
9.375c 0.222c 2.000c 10.503a
0.009d 0.895d 0.368d 0.005b
abc, Wilcoxon-test; def, McNemar-test. a x2-test. b Friedman-test, d.f. = 2. c Q-value. d Cochran Q-test, d.f. = 2.
3.2.2. Heart rate As in the first test session, heart rate differed between periods investigated (Fig. 2B). Heart rate increased from the period before the test session (72.6 0.9 beats/min) until the first minute of the test session when the human was standing still beside the cow (78.1 1.1, t = 8.36, P < 0.001), and also from the period before the test session until the periods of stroking the three body regions (W: 77.1 1.1, t = 6.84; NV: 75.4 1.0, t = 4.27; LC: 77.0 1.1, t = 6.69; for all body regions: P < 0.001). As opposed to the first test session, heart rate was lower when the NV was stroked as compared to W (t = 2.57, P < 0.01) and LC (t = 2.41, P < 0.05). Moreover, heart rate was lower during stroking the NV than during the first minute of the test session (t = 4.09, P < 0.001). This was not observed for the other two body regions stroked. 3.3. Difference in behavioural reactions from the first to the second test session Duration of neck stretching and ear hanging increased when certain body regions were stroked. The duration of neck stretching increased from the first to the second test session when the NV was stroked (first session: 3.7 s, second session: 23.8 s; Z = 3.59, P < 0.001). Ear hanging increased from the first to the second test session only during stroking the W (first session: 51 s, second session: 86 s; Z = 4.04, P < 0.001). In contrast, the number of animals performing the other behaviours decreased when certain body regions were stroked. The number of animals performing head shaking when the NV was stroked tended to decrease from the first to the second test session (first session: 18, second session: 11; P < 0.1). When the W was stroked, the number of animals showing head shaking (first session: 16, second session: 6; P < 0.05) and head throwing (first session: 20, second session: 4; P < 0.001) both decreased. Finally, when the LC was stroked, the number of animals throwing their heads decreased (first session: 12, second session: 3; P < 0.05). Duration of contact with the experimenter after stroking did not change from the first to the second test session independent of the body regions stroked (Z > 0.25, P > 0.80).
34
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
4. Discussion 4.1. Differences between body regions stroked in both test sessions The results clearly confirm our hypothesis that the animals differ in their reaction to human tactile stimulation depending on the body region stroked. Much more behavioural reactions were observed when cows’ withers (W) and neck ventral (NV), both body regions often licked during social grooming, were stroked as compared to the lateral chest (LC), a body region rarely licked. In both test sessions, cows responded consistently to stroking the W and NV mainly by neck stretching and ear hanging. Head shaking and head throwing also differed for the various body regions stroked (more for W and NV), but they were observed in a minority of the cows, were expressed rarely, and the occurrence further decreased in the second test session. Heart rate responses also differed for the body regions stroked, being higher when the W was stroked as compared to NV and LC in the first, and lower during stroking the NV as compared to W and LC in the second test session. The behavioural and physiological reactions were not affected by the 3-week treatment of repeated stroking of specific body regions or human presence between the two test sessions. The results are in line with other studies in different species showing that animals’ behavioural and/or physiological responses to human tactile stimulation depend on the body region (horse: Feh and de Mazie´res, 1993; McBride et al., 2004; rat: Kurosawa et al., 1995; Lund et al., 1999; cat: Soenichsen and Chamove, 2002). This study is the first to demonstrate this difference also for cattle. Many previous studies have used tactile stimulation to improve the cattle–human relationship (for review Boivin et al., 2003). However; they did not target specific body regions. This new information could be interesting in order to understand variability in cattle reaction to stroking and to improve the quality of human–cattle interactions. The behavioural and physiological responses to human stroking of the three body regions included in our experiment showed some similarities to the ones observed in intra-specific social licking, depending on the body region stimulated. Neck stretching and ear hanging are typical behaviours during social licking and licking solicitation (Schloeth, 1961; Sambraus, 1969; Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983; Sato et al., 1991). Both behaviours occurred in particularly high proportions during social licking of W and NV, and differed significantly from other body regions including LC (Schmied et al., 2005). The decrease in heart rate, as did occur in the present study during human stroking of the NV in the second test session, could also be found during intra-specific social licking. Sato and Tarumizu (1993) found a decrease in heart rate when calves licked each other, but they did not differentiate the regions that were licked. In a recent study, heart rate was found to be lower when a cow’s ventral neck was licked by a peer as compared to other neck regions (Schmied et al., 2005). This also is in line with studies in horses. A human scratching a body region preferred for social nibbling, e.g. withers, elicited a decrease in heart rate and caused more relaxed and affiliative responses, as compared to massage of a non-preferred area, e.g. shoulder (Feh and de Mazie´res, 1993; McBride et al., 2004). These results taken together suggest the hypothesis that cows may perceive human stroking, at least partly, like intra-specific social licking. Social licking in cattle plays a significant role in strengthening and maintaining social bonds, in relieving social tension and enhancing social cohesion (Sambraus, 1969; Reinhardt, 1980; Sato et al., 1991; Waiblinger et al., 2002). The occurrence of social licking is related to affinities between individuals (Zimmermann-Mu¨ller, 1978; Reinhardt, 1980; Sato et al., 1993) and was shown to have calming effects (lowering heart
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
35
rate; Sato and Tarumizu, 1993). Based on the similarities found in reactions during intra-specific social licking and the differences between body regions, we assume that human stroking of particular body regions, where mutual licking occurs most, could have similar affiliative and maybe rewarding effects on the cow–human relationship as intra-specific social licking has on cows’ social bonds. This could explain the difference observed in soft physical contact with the human (sniffing, head rubbing, . . .) during the 1-min pause after stroking. In the intra-specific social situation, these behaviours are generally seen in a non-agonistic, affiliative context (Simonsen, 1979; Kiley-Worthington and de la Plain, 1983; Mu¨lleder et al., 2003). Indeed, the duration of physical contact with the human established by the cows was shortest after stroking the LC, the rarely licked body region. Of course such interpretation needs to be strengthened by further research. 4.2. Differences between first and second test session The similarities of cows’ responses to human stroking and to social grooming were more pronounced in the second test session, while in the first test session the behavioural and physiological responses less clearly conformed to the hypothesis. The duration of neck stretching and ear hanging during stroking the NV or W were longer as compared to the LC, too, but nevertheless much briefer than during the second test session. More cows showed head throwing or shaking during stroking the NVor W which could be interpreted as a negative perception of stroking these particular body regions. For instance, head throwing is a threat performed to displace another cow (Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983), and head shaking is also described to be a mild threat (Simonsen, 1979; Kiley-Worthington and de la Plain, 1983). These behaviours may indicate that some animals did not accept such contact. In the same way, heart rate did not decrease with stroking as it was expected from the hypothesis, but even increased for W as compared to the two other body regions stroked. All in all, it seems that in the first test session stroking did not have the same quality for the animals as in the second test session. There is no factor in this experiment that can be really tested to explain this difference between the two test sessions, as the treatment factor (regular stroking of particular body regions) had no effect in comparison to control (simple human presence). We could, however, assume that both the novelty of the experimental situation and the difference in sensitivity of the body regions stroked were probably responsible for these discrepancies. Heart rate, for example, increases with respect to the novelty of events (for review Boissy and Boissou, 1995), i.e. in the actual experiment it was the novelty of the unknown experimenters and/or the stroking procedure itself. This may explain the heart rate increase found when stroking the W and the lack of difference observed during stroking the NV, as the possible calming effect may have been overridden by the increase. This could also be the case for other behaviours (head throwing, head shaking) that were shown by some cows in the first, but not in the second test session. In the second test session, which followed 3 weeks of repeated human contact, the experimenter had lost her novelty status. This could explain why the results of this second test session were more in line with our hypothesis. Despite the novelty of the situation in the first stroking session, the reactions of the cows nevertheless differed depending on the body region stroked, which enhances the significance of the findings and supports the hypothesis of a body-region-specific sensibility, possibly caused by differences in the density of somatosensory afferent innervation, as suggested by Kurosawa et al. (1995) and Lund et al. (1999). Reactions of cows to stroking of other body regions such as the basis of the tail (commonly used by farmers, but licked rarely in social interactions) or the back side of the hind legs (licked
36
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
by the mother in suckling calves) would be interesting to compare with the body regions used in this experiment. This additional information would extend our understanding of the animals’ perception of such contact in the purpose of improving human–animal interactions. 5. Conclusion In this experiment, stroking the body regions often licked during social grooming led to much more responses than stroking the one licked rarely; in addition, a lot of these reactions are similar to those observed during intra-specific social licking. This suggests that cows could perceive human stroking of body regions often licked – at least partly – like social licking, which again indicates that stroking these body regions is an especially interesting way of tactile contact with cows. Whether stroking the body regions most often licked is also associated with a more effective improvement of the cow’s relationship to humans is currently being investigated at our Institute. Acknowledgements The authors thank the staff of the University of Veterinary Medicine’s Teaching and Research Estate for the help in performing the experiment. Moreover, we are grateful to Isabella ChorolezPerner for reviewing the English language. References Anderson, S., Gantt, W.H., 1966. The effect of person on cardiac and motor responsivity to shock in dogs. Cond. Reflex 1, 181–189. Boccia, M., Reite, M., Laudenslager, M., 1989. On the physiology of grooming in a pigtail macaque. Physiol. Behav. 45, 667–670. Boissy, A., Boissou, M.-F., 1995. Assessment of individual differences in behavioural reactions of heifers exposed to various fear-eliciting situations. Appl. Anim. Behav. Sci. 46, 17–31. Boivin, X., Le Neindre, P., Chupin, J.M., 1992. Establishment of cattle–human relationships. Appl. Anim. Behav. Sci. 32, 325–335. Boivin, X., Lensink, J., Tallet, C., Vessier, I., 2003. Stockmanship and farm animal welfare. Anim. Welf. 12, 479–492. Bradshaw, J., 1992. The Behaviour of the Domestic Cat. CABI, Wallingford. Breuer, K., Hemsworth, P.H., Barnett, J.L., Matthews, L.R., Coleman, G., 2000. Behavioural response to humans and the productivity of commercial dairy cows. Appl. Anim. Behav. Sci. 66, 273–288. Caroprese, M., Napolitano, F., Albenzio, M., Annicchiarico, G., Musto, M., Sevi, A., 2006. Influence of gentling on lamb immune response and human–lamb interactions. Appl. Anim. Behav. Sci. 99, 118–131. Feh, C., de Mazie´res, J., 1993. Grooming at a preferred site reduces heart rate in horses. Anim. Behav. 46, 1191– 1194. Gross, W.B., Siegel, P.B., 1982. Socialization as a factor in resistance to infection, feed efficiency, and response to antigen in chickens. Am. J. Vet. Res. 43, 2010–2012. Hemsworth, P.H., Coleman, G., Barnett, J.L., Borg, S., 2000. Relationships between human–animal interactions and productivity of commercial dairy cows. J. Anim. Sci. 78, 2821–2831. Hennessy, M.B., Williams, M.T., Miller, D.D., Douglas, C.W., Voith, V.L., 1998. Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Appl. Anim. Behav. Sci. 61, 63–77. Kiley-Worthington, M., de la Plain, S., 1983. The Behaviour of Beef Suckler Cattle (Bos taurus). Birka¨user Verlag, Basel. Kostarczyk, E., 1992. The use of dog–human interaction as a reward in instrumental conditioning and its impact on dogs’ cardiac regulation. In: Davis, H., Balfour, D. (Eds.), The Inevitable Bond, Examining Scientist–Animal Interactions. Cambridge University Press, Cambridge, pp. 109–131. Kurosawa, M., Lundeberg, T., Agren, G., Lund, I., Uvna¨s-Moberg, K., 1995. Massage-like stroking of the abdomen lowers blood pressure in anesthetized rats: influence of oxytocin. J. Autonom. Nerv. Syst. 56, 26–30.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
37
Lensink, B.J., Boivin, X., Pradel, P., Le Neindre, P., Vessier, I., 2000. Reducing veal calves’ reactivity to people by providing additional human contact. J. Anim. Sci. 78, 1213–1218. Lensink, B.J., Vessier, I., Florand, L., 2001. The farmer’s influence on calves’ behaviour, health and production of a veal unit. J. Anim. Sci. 72, 105–116. Lund, I., Lundeberg, T., Kurosawa, M., Uvna¨s-Moberg, K., 1999. Sensory stimulation (massage) reduces blood pressure in unanaesthetized rats. J. Autonom. Nerv. Syst. 78, 30–37. Lynch, J.J., 1977. The Broken Heart: the Medical Consequences of Loneliness. Basic Books Inc., New York, pp. 156–180. Lynch, J.J., Gantt, W.H., 1968. The heart rate component of the social reflex in dogs: the conditioned reflex of petting and person. Cond. Reflex 3, 69–80. Lynch, J.J., Fregin, G.F., Mackie, J.B., Monroe Jr., R.R., 1974. Heart rate changes in the horse to human contact. Psychophysiology 11, 472–478. McBride, S.D., Hemmings, A., Robinson, K., 2004. A preliminary study on the effect of massage to reduce stress in the horse. J. Equine Vet. Sci. 24, 76–81. McMillan, F.D., 1999. Effects of human contact on animal health and well-being. J. Am. Vet. Med. Assoc. 215, 1592– 1598. Mu¨lleder, C., Palme, R., Menke, C., Waiblinger, S., 2003. Individual differences in behaviour and in adrenocortical activity in beef-suckler cows. Appl. Anim. Behav. Sci. 84, 167–183. Pinheiro, J.C., Bates, D.M., 2000. Mixed-effects Models in S and S-Plus. Statistics and Computing Series. SpringerVerlag, New York. R Development Core Team, 2004. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. Reinhardt, V., 1980. Untersuchung zum Sozialverhalten des Rindes: Eine 2-ja¨hrige Beobachtung an einer halb-wilden Rinderherde (Bos indicus). Birkha¨user Verlag, Basel. Rushen, J., Taylor, A.A., de Passille´, A.M., 1999. Domestic animals’ fear of humans and its effect on their welfare. Appl. Anim. Behav. Sci. 65, 285–303. Rushen, J., Munksgaard, L., Marnet, P.G., DePassille´, A.M., 2001. Human contact and the effects of acute stress on cows at milking. Appl. Anim. Behav. Sci. 73, 1–14. Sambraus, H.H., 1969. Das soziale Lecken des Rindes. Z. Tierpsychol. 26, 805–810. Sato, S., 1984. Social licking pattern and its relationships to social dominance and live weight gain in weaned calves. Appl. Anim. Behav. Sci. 12, 25–32. Sato, S., Tarumizu, K., 1993. Heart rates before, during and after allo-grooming in cattle (Bos taurus). J. Ethol. 11, 149–150. Sato, S., Sako, S., Maeda, A., 1991. Social licking patterns in cattle (Bos taurus): influence of environmental and social factors. Appl. Anim. Behav. Sci. 32, 3–12. Sato, S., Tarumizu, K., Hatae, K., 1993. The influence of social factors on allogrooming in cows. Appl. Anim. Behav. Sci. 38, 235–244. Schloeth, R., 1961. Das Sozialleben des Camargue-Rindes. Z. Tierpsychol. 18, 574–627. Schmied, C., Boivin, X., Waiblinger, S., 2005. Ethogramm des sozialen Leckens beim Rind: Untersuchungen in einer Mutterkuhherde/Ethogram of social licking: investigations in a beef suckler herd. KTBL-Schrift 441, aktuelle Arbeiten zur artgema¨ßen Tierhaltung 2005. Kuratorium fu¨r Technik und Bauwesen in der Landwirtschaft e.V. (KTBL), Darmstadt, pp. 86–92. Seabrook, M.F., 1994. Psychological Interaction between the Milker and the Dairy Cow. Dairy Systems for the 21st Century. ASAE, St. Joseph, MI, pp. 49–58. Siegel, S., 1997. Nicht parametrische statistische Methoden. Verlag Dietmar Klotz GmbH, Frankfurt am Main, 4. Auflage, ISBN 3-88074-102-6. Simonsen, H.B., 1979. Grooming behaviour of domestic cattle. Nord. Vet.-Med. 31, 1–5. Soenichsen, S., Chamove, A.S., 2002. Responses of cats to petting by humans. Anthrozoo¨s 15, 258–265. Tallet, C., Veissier, I., Boivin, X., 2005. Human contact and feeding as rewards for the lamb’s affinity to their stockperson. Appl. Anim. Behav. Sci. 94, 59–73. Uvna¨s-Moberg, K., Petersson, M., 2005. Oxytocin, ein Vermittler von Antistress, Wohlbefinden, sozialer Interaktion, Wachstum und Heilung. Z. Psychosom. Med. Psychother. 51, 57–80. Uvna¨s-Moberg, K., Alster, P., Lund, I., Lundeberg, T., Kurosawa, M., Ahlenius, S., 1996. Stroking of the abdomen causes decreased locomotor activity in conscious male rats. Physiol. Behav. 60, 1409–1411. Waiblinger, S., 1996. Die Mensch-Tier-Beziehung bei der Laufstallhaltung von behornten Milchku¨hen. Reihe Tierhaltung Bd. 24, Gesamthochschule Kassel, Witzenhausen. Waiblinger, S., Fresdorf, A., Spitzer, G., 2002. The role of social licking in cattle for conflict resolution. In: Proceedings of the First European Conference of Behavioural Biology, August 1–4 in Mu¨nster, Germany, p. 122.
38
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Waiblinger, S., Menke, C., Korff, J., Bucher, A., 2004. Previous handling and gentle interactions affect behaviour and heart rate of dairy cows during a veterinary procedure. Appl. Anim. Behav. Sci. 85, 31–42. Waiblinger, S., Boivin, X., Pedersen, V., Tosi, M.-V., Janczak, A.M., Visser, E.K., Jones, R.B., 2006. Assessing the human–animal relationship in farmed species: a critical review. Appl. Anim. Behav. Sci. 101, 185–242. Wood, M.T., 1977. Social grooming patterns in two herds of monozygotic twin dairy cows. Anim. Behav. 25, 635–642. Zimmermann-Mu¨ller, M.E., 1978. Zur Sozialstruktur des Hausrindes Bos Taurus–Ein Vergleich des Sozialverhaltens auf der Weide und im Laufstall. Inauguraldissertation, Basel.
Stroking of different body regions by a human: Effects on behaviour and heart rate of dairy cows Claudia Schmied a, Susanne Waiblinger a,*, Theresa Scharl c, Friedrich Leisch c, Xavier Boivin b a
Department of Veterinary Public Health and Food Science, Institute of Animal Husbandry and Welfare, University of Veterinary Medicine Vienna, Veterina¨rplatz 1, 1210 Vienna, Austria b URH-ACS, INRA, Laboratoire Adaptation des herbivores aux milieux, CRZV de Theix, 63122 St Gene´s Champanelle, France c Department of Statistics and Probability Theory, Vienna University of Technology, Wiedner Hauptstraße 8-10/1071, 1040 Vienna, Austria Accepted 29 January 2007 Available online 9 March 2007
Abstract From observations of intra-specific social grooming in cattle and studies on human stroking in other species, we hypothesised that cows’ reactions to human stroking differ depending on the body regions being stroked. Moreover, we tested, whether cows ‘reactions to stroking change with the animals’ experience of stroking. Sixty dairy cows were stroked in three different body regions, i.e. the withers, W, neck ventral, NV (both licked often in social grooming) and the lateral chest, LC (licked rarely), in a balanced order during 10-min sessions. Behavioural reactions and heart rate during stroking as well as reactions to the human just after stroking were recorded. Two test sessions were carried out with 3 weeks of treatment in-between. During this period, the cows were randomly allocated to four treatment groups: three groups received 5 min of daily stroking in either W, NV or LC and the last one (control group) was exposed to simple human presence. During stroking W and NV, cows showed longer neck stretching and ear hanging than during stroking LC (P < 0.001). Moreover, ear hanging was shown longer when W was stroked as compared to NV (P < 0.001), but neck stretching was observed longer during stroking NV as compared to W only after the treatment period (P < 0.01). In the first test session, more animals showed head shaking and head throwing during stroking W and NV than LC (P < 0.01), whereas in the second test session these behaviours were observed only in few animals. In the first test session heart rate was higher during stroking W than the other body regions (P 0.01). In the second test session, the lowest heart rate was found during stroking NV (P < 0.05). Finally, contact with the experimenter following stroking differed for the three body regions
* Corresponding author. Tel.: +43 1 25077 4905; fax: +43 1 25077 4990. E-mail address: [email protected] (S. Waiblinger). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.01.013
26
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
stroked in both test sessions (first: P = 0.06, second: P < 0.01); contact was shortest for LC. When comparing both test sessions, stretching the neck and ear hanging increased (P < 0.001), while head shaking and head throwing decreased (P < 0.05); there was no difference for heart rate and contact with the experimenter. The four treatments had no influence on reactions to stroking. To conclude, stroking of body regions often licked during social grooming led to more responses than stroking the one licked rarely. Some reactions, such as stretching the neck, are also observed during social licking. This suggests that cows may in part perceive human stroking of body regions often licked similarly to social licking. This knowledge could be of interest for an improvement in quality of human–cattle interactions. # 2007 Elsevier B.V. All rights reserved. Keywords: Cattle; Tactile stimulation; Human–animal relationship; Social licking
1. Introduction Stroking and other gentle tactile contact is used regularly during daily stockperson–animal interactions in dairy cattle husbandry (Waiblinger, 1996; Hemsworth et al., 2000; Breuer et al., 2000). Stroking by humans as part of gentle contact has also been used in experimental studies in many farm animal species, e.g. chicken, goats, sheep, pigs, or cattle (for review e.g. Boivin et al., 2003), but mostly it was combined with other forms of contact like talking or offering food. Gentle handling involving stroking has shown to decrease farm animals’ fear of humans (Rushen et al., 1999), thereby having beneficial effects, such as improved ease of handling (Boivin et al., 1992), reduced distress behaviour, e.g. vocalisations in the presence of a human during isolation (Tallet et al., 2005), increased productivity (Seabrook, 1994), improved meat quality (Lensink et al., 2000, 2001), and improved immune response reducing the risk of disease (Gross and Siegel, 1982; Caroprese et al., 2006; for review Waiblinger et al., 2006). Specific and immediate reactions to gentle tactile contact were demonstrated in various studies, but mostly investigated in other than farm animal species (for review McMillan, 1999). In particular, stroking decelerated the heart rate in horses, dogs and rats (Lynch et al., 1974; Kostarczyk, 1992; Kurosawa et al., 1995; Lund et al., 1999) and evoked various particular types of behaviour interpreted by the authors as indicators of a relaxation state (horse: head lowered, eyes half closed, standing motionless, Lynch et al., 1974; rat: less locomotor activity, Uvna¨sMoberg et al., 1996). In several species, e.g. rats, tactile stimulation was found to trigger oxytocin release, thereby physiologically leading to a lower heart rate, lower blood pressure and lower cortisol levels as immediate effects in addition to long term effects, e.g. effects on social bonding (Uvna¨s-Moberg and Petersson, 2005). Furthermore, tactile stimulation was able to decrease behavioural and physiological responses induced by fear and painful stimuli in dogs (Anderson and Gantt, 1966; Lynch and Gantt, 1968; Lynch, 1977; Hennessy et al., 1998). In cattle, too, there is some evidence suggesting direct beneficial effects of stroking by humans, e.g. stroking combined with gently talking was able to reduce the heart rate increase of dairy cows during an aversive treatment (Waiblinger et al., 2004). Similarly, cows showed during isolation lower heart rates when they were brushed by a human than in situations without human contact (Rushen et al., 2001). However, in both of these studies the effect of gentle tactile contact was not distinguished from simple human presence, nor were different body regions considered. These effects of tactile stimulation by a human are consistent with results found in intraspecific social grooming in animals. The heart rates of pig-tailed macaques and cattle being groomed/licked by conspecifics decreased, for example (Boccia et al., 1989; Sato and Tarumizu,
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
27
1993). In cattle, the time an animal is being licked was positively related to milk production in cows or live weight gains in calves (Wood, 1977; Sato, 1984). However, observations of intraspecific social grooming and experimental studies on tactile stimulation by humans suggest that the effects could depend on the body region onto which it is directed. In horses, more than 50% of mutual nibbling is performed at the withers (Feh and de Mazie´res, 1993); a human scratching a horse in imitation of nibbling led to a lower heart rate and more affiliative behaviour when performed at the withers than when performed at other body regions (Feh and de Mazie´res, 1993; McBride et al., 2004). Similarly in cats, mutual face rubbing is known to fulfil a social bonding function (Bradshaw, 1992) and stroking by humans in the body region preferred for this intraspecific contact has been found to lead to more affiliative responses than contact with other body regions (Soenichsen and Chamove, 2002). There is no study about such possible differences in reaction to human tactile contact for cattle. However, several authors described an uneven distribution of social licking (Sambraus, 1969; Kiley-Worthington and de la Plain, 1983). A recent study found that 64% of social licking between adult cows is directed to the neck, especially the dorsal and ventral part (Schmied et al., 2005). Furthermore, the reactions of the licked animals differed depending on the body region licked; the heart rate was found to be lower during social licking of the ventral part of the neck than of other neck regions (Schmied et al., 2005). Therefore the aim of this study was to investigate whether dairy cows’ behavioural and physiological reactions to human stroking of different body regions often or rarely licked in social grooming differ. We hypothesized that stroking of body regions often licked would lead to more behavioural reactions, similar to those shown by licked cows, and to lower heart rate, as compared to stroking a rarely licked body region. In addition, the direct reactions to stroking were measured again after a treatment period, to find out, whether a previous experience with being stroked in special body regions could have an effect on the cow’s reactions. 2. Animals, material and methods 2.1. Animals and housing The experiment was carried out from January 2003 to March 2003 on 30 Brown Swiss and 30 Austrian Simmental cows (age: 4.7 years 1.8, average milk yield: 5700 kg milk/year) of the dairy herd of the University of Veterinary Medicine’s Teaching and Research Estate. The experimental cows were randomly selected from a herd of 80 cows, excluding, however, cows in late pregnancy (dry cows, 4–6 weeks before parturition). All cows were reared under the same housing (loose housing, pasture during summer) and management conditions. The whole year round the cows were tied starting with the first lactation, except for some weeks during the dry period when they were pastured. During the experiment the cows were milked twice a day by their regular milkers. The cows were used to different stockpeople and to frequent human contact, but they were not used to being stroked regularly. However, during the experiment, human contact was reduced to daily management routines or necessary treatment. 2.2. Experimental design According to previous research on social licking (Schmied et al., 2005) three body regions were chosen for comparison: the withers (W) and the neck ventral (NV), which are licked most often, and one body region licked rarely (the lateral chest [LC]). The location of the three body regions is shown in Fig. 1. Two test sessions for measuring the cows’ immediate behavioural and physiological reactions in response to stroking were carried out at an interval of 3 weeks. During these 3 weeks, cows were allocated to different treatment groups, which involved stroking of these three body regions or human presence, respectively.
28
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Fig. 1. Location of the three body regions stroked and position of the heart rate equipment (black girth).
2.2.1. First test session In the first test session each of the two experimenters (one female, 175 cm, 68 kg, and one male, 180 cm, 80 kg), who were unknown to the cows until then, stroked half of the test session animals. Both wore overalls and jackets of the same colour (different to the caretakers) as well as leather working gloves with a suede palmar side for stroking the cows during the entire experiment. Before the start of the test session, the experimenters harmonized speed and pressure of stroking. Speed of stroking was between 40 and 60 strokes/min, thereby imitating the speed of social licking found earlier (Schmied et al., 2005). Both used a similar medium pressure for all stroking. The test session for the 60 cows took place on three successive days, i.e. 20 cows were tested per day. Test sessions started 30 min after the end of morning milking and stopped at least 30 min before evening milking (incl. a break around midday when cows were fed). Each of the 60 cows was stroked in one 10-min session in all three body regions for 2 min each followed by a 1-min pause before moving on to the next the body region. All the six different possible sequences of the three body regions were applied with each of them being used on 10 cows. At the beginning of the 10-min procedure the experimenter approached the cow from the back by addressing her gently in a standardized manner (‘‘cow’s name’’ and ‘‘good cow’’), and then walked slowly to the left chest of the cow, keeping quiet throughout the entire test session. During the first minute of the test session the experimenter stood motionless beside the cow, arms by the side. This was followed by 2 min of stroking body region 1; 1 min standing motionless beside the cow, hand resting on the chest; 2 min stroking body region 2; 1 min standing motionless beside the cow, hand resting on the chest again; 2 min stroking body region 3; 1 min standing motionless beside the cow, arms by side at the end. The order of body regions was evenly distributed on the basis of the experimenter’s identity and cows’ breed, age and status of gravidity. 2.2.2. Treatment The 60 cows were divided into 4 groups balanced for breed, age and gravidity. In three groups either the withers (WL = long term group W) or the neck ventral (NVL = long term group NV) were stroked, or the lateral chest (LCL = long term group LC). Cows were stroked for 5 min/day on 5 days per week in 3 consecutive weeks (a total of 15 days). One group (control) was not stroked, but the experimenter stood still by the animals with arms by the side, using the same time schedule. The treatment was carried out by the female experimenter of the previous test session and stroking was done in the same manner as described there. 2.2.3. Second test session The procedure was performed as described for the first test session by the female experimenter. One cow from the NVL treatment group got sick and died before the second test session. All remaining 59 cows were stroked in a balanced order, taking into consideration the treatment group they belonged to. 2.3. Behavioural observations The behaviour of the cows was videotaped during the test sessions. The camera was located in the feeding path and the cow was recorded from left and front. The behaviour was observed continuously from video with the observational software The Observer Video ProTM, Noldus Information Technology, NL.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
29
Table 1 Definition of behavioural parameters used for observation in both test sessions Behavioural parameters
Definition
Stretching the neck
Positioning neck and head in an outstretched line, either up, down, or forward; duration in seconds Pinna/external ear pendulous; duration in seconds Consecutive quick movements of the head; frequency Head and neck is thrown quickly in a certain direction once, either quickly up and down, or to the side; frequency Top of the head is brought up quickly against the experimenter; frequency Bringing the muzzle near the experimenter, <5 cm; duration in seconds Touching the experimenter with the tongue; duration in seconds Front head resting against the experimenter with continued contact; duration in seconds Softly rubbing the head up and down the body of the experimenter; duration in seconds
Ear hanginga Head shaking Head throwing Butting Sniffing at b Lickingb Head leaningb Head rubbingb a
For ear hanging only the one ear that was visible throughout the test session was observed; it was mostly the left one; due to head movements, however, the right ear was visible and observed sometimes. b These parameters were combined for further analysis in one variable of soft physical ‘‘contact with the experimenter’’ and were calculated for the pause minutes after stroking only.
The main focus was on the head area because cattle use mostly head movements and postures for social interactions (Schloeth, 1961; Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983; Schmied et al., 2005). Table 1 lists and defines the behavioural parameters recorded. Inter-observer-reliability was tested with three different observers. The behaviour of 8 cows randomly chosen from all 60 cows was observed from video. Spearman rank correlation coefficients were calculated. Reliability was high with coefficients ranging from 0.92 to 1.00. 2.4. Heart rate During the test session, heart rate was recorded by means of a commercial heart rate monitoring system (horse trainer transmitters and S810 monitors from Polar Elektro Oy, Helsinki, Finland), attached to identical horse girths and fitted to the cows (see Fig. 1 for position). The spots where the electrodes were placed were not shorn or shaved but electrode gel was applied liberally to ensure contact and an additional elastic girth kept the transmitter in place. In the week before the experiment the cows were made familiar with the entire procedure by putting the equipment on them twice for about 2 h, which corresponds to the longest duration cows had to wear it during tests. During the experiment the equipment was fitted on the cows at least 30 min before the start of a test session. Beat-to-beat intervals were measured and the average heart rate calculated for the phases: ‘‘before’’ without human presence (the first 10 min after the heart rate equipment had been put on and the last 10 min before the start of the test session were excluded; usually the 10-min timeframe out of a 20–10-min period before the test session was used; another 10-min timeframe was used only when the heart rate measurement graph showed too many irregularities); ‘‘first minute’’ of the test session, i.e. standing still beside the cow without touching her, and the 2 min of stroking each body region (NV, W, LC). In the second test session the heart rate monitor of one cow failed and therefore the data of this cow were not included in the analysis. 2.5. Statistics For statistical analyses of behavioural data the software package SPSS1, Version 11.5 was used. Due to non-normal distributions and variances’ heterogeneity behavioural parameters were analysed by nonparametric statistics (Siegel, 1997). The Friedman test was used to test for differences between body regions of each cow. In the case of significant differences (P 0.05) between the body regions, each pair of body regions was compared using the Wilcoxon test (Z statistic given in the results). Because of independent data
30
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
the Kruskal–Wallis test was used to test the effects of the treatment for each body region stroked; and in case of significant differences (P 0.05) each pair of treatments was compared by using the Mann–Whitney U-test. For rarely occurring behavioural reactions the number of animals which showed this behaviour was used for the calculation with the Cochran-Q test for dependent data rather than the frequency. In the case of significant differences the McNemar test was used to compare pairs of body regions. For testing on treatment effects we used a x2-test for independent data. The heart rate was analysed with the statistical computing environment R version 2.0.1 (R Development Core Team, 2004). We fitted a mixed-effects model (Pinheiro and Bates, 2000) to heart rate data with random effects for each cow and fixed effects for the different body regions stroked and the different orders of stroking (F-value of the model and t-values for comparisons of pairs of body regions given in the results). Significant differences between the body regions stroked were found. The order of stroking, however, did not result in any differences. Therefore these data are not presented in the results.
3. Results 3.1. First test session 3.1.1. Behavioural reactions The cows differed in their reactions to stroking of the three body regions (Table 2). They stretched their necks longer during stroking both the W (Z = 4.68, P < 0.001) and the NV (Z = 4.81, P < 0.001) than LC, where only six cows showed neck stretching at all. The duration of ear hanging was longer when the W was stroked as compared to the NV (Z = 3.42, P < 0.001). It was much shorter when the LC was stroked (as compared to W: Z = 6.53, P < 0.001 and NV: Z = 6.20, P < 0.001). Head shaking and head throwing occurred only rarely during stroking; most of the cows did not express these behaviours at all, and for those few animals that did, frequency was low, i.e. the median at each body region was 2 (maximum: 7). Nevertheless, head shaking was performed by more cows when the W was stroked (P < 0.01) and also the NV (P < 0.01) as compared to LC. More cows showed head throwing when the W was stroked as compared to the NV (P < 0.01) and, in tendency, as compared to LC (P < 0.1). Table 2 Behavioural parameters in the first test session, observed at the three body regions (withers, neck ventral and lateral chest), body regions with different letter (abc or def) differ significantly, N = 60 Behavioural parameters Stretching of the neck (duration in s); median (25–75 percentiles) Ear hanging (duration in s); median (25–75 percentiles) Head shaking; number of animals Head throwing; number of animals Butting; number of animals Contact to experimenter (duration in s); median (25–75 percentiles) abc, Wilcoxon-test; def, McNemar-test. a x2-test. b Friedman-test, d.f. = 2. c Q-value. d Cochran Q-test, d.f. = 2.
Withers
Neck ventral
Lateral chest
Value
P
0 b (0–0)
29.545
a
0.000b
0.8 a (0–17)
3.7 a (0–28)
51 a (28–94)
32 b (20–65)
6 c (0–19)
82.279a
0.000b
16 d 20 d 3 3.5 a (0–12)
18 d 8e 1 3.3 ab (0–9)
6e 12 de 0 0.5 b (0–7)
12.087c 10.182c 3.500c 5.670a
0.002d 0.006d 0.174d 0.059b
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
31
The number of animals expressing butting was extremely low and was not affected by the body region stroked. The duration of contact with the experimenter during the pause after stroking tended to differ depending on the body regions stroked before, with contact being longer after stroking the W (Z = 2.52, P < 0.05) and – as a tendency – the NV (Z = 1.79, P = 0.07) as compared to the LC. 3.1.2. Heart rate Heart rate differed between periods investigated (Fig. 2A). Compared to the period before the test session (67.3 0.9 beats/min; average S.E.M.), heart rate was higher in the first minute of the test session when the human stood still beside the cow (70.3 1.2 beats/min, t = 4.18, P < 0.001) and during stroking the three body regions (W: 71.7 1.4, t = 6.19; NV: 69.9 1.1, t = 3.73; LC: 69.3 1.2, t = 2.81; for all body regions: P < 0.01). During the test session, cows had a higher heart rate when the W was stroked as compared to the NV (t = 2.46, P 0.01) or LC (t = 3.37, P < 0.001). Additionally, heart rate was higher when the W was stroked than in the first minute of the test session (t = 2.01, P < 0.05). This was not the case for the other body regions stroked. 3.2. Second test session The different treatments had no effect on neck stretching independent of the different body regions being stroked (x2 < 3.35, P > 0.34), nor on ear hanging (x2 < 4.47, P > 0.22), contact with the experimenter after stroking (x2 < 3.34, P > 0.34), head throwing (x2 < 3.85, P > 0.28), butting (no statistics calculated by SPSS because of constant value) or heart rate (F 3,54 = 0.35, P = 0.79). For head shaking there was also no significant effect during stroking the NV (x2 = 5.38, P = 0.15) and the LC (x2 = 3.27, P = 0.35). The only significant result was found for head shaking during stroking the W (x2 = 7.92, P < 0.05). More animals (four cows) of the control group showed head shaking than of the NVL (0; x2 = 4.33, P < 0.05) and LCL group (0; x2 = 4.62, P < 0.05). Due to this low number of animals and the lack of a difference in all other behaviours and body regions, the second test session was analysed without considering the treatment groups. 3.2.1. Behavioural reactions Cows again reacted differently to stroking depending on the body regions (Table 3). Cows stretched their necks longer when the NV was stroked as compared to the W (Z = 2.92, P < 0.01). Moreover, the duration of neck stretching was much shorter when the LC was stroked (as compared to NV: Z = 5.55, P < 0.001, and W: Z = 5.05, P < 0.001), with most cows (55) showing no stretching at all. As in the first test session, the duration of ear hanging was longer when the W was stroked than the NV (Z = 5.45, P < 0.001), and it was again much shorter when the LC was stroked (compared to W: Z = 6.57, P < 0.001 and NV: Z = 5.87, P < 0.001). Only few animals were performing head shaking, and for those animals the frequency was also very low, i.e. the median at each body region was 1 (maximum: 5). Nevertheless, head shaking was observed in more cows when the NV was stroked as compared to LC (P < 0.01). The number of animals performing head throwing and primarily butting was extremely low and did not show any difference for the body regions stroked. Duration of contact in the pause after stroking differed significantly between the body regions; after stroking the NV more contact with the experimenter was found compared to LC (Z = 2.42, P < 0.01), W lay between both.
32 C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Fig. 2. Heart rate (mean S.E.M.) during stroking the three body regions (withers: W, neck ventral: NV, lateral chest: LC) and during phases before the test session (before) and the first minute of test session (1st min), phases/body regions with different letters (abc) differ significantly (P 0.05). (A) First test session, N = 60. (B) Second test session, N = 58.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
33
Table 3 Behavioural parameters in the second test session, observed at the three body regions (withers, neck ventral and lateral chest), body regions with different letter (abc or def) differ significantly, N = 59 Behavioural parameters Stretching of the neck (duration in s); median (25–75 percentiles) Ear hanging (duration in s); median (25–75 percentiles) Head shaking; number of animals Head throwing; number of animals Butting; number of animals Contact to experimenter (duration in s); median (25–75 percentiles)
Withers
Value
P
7.3 b (0-31)
Neck ventral 23.8 a (0–52)
Lateral chest 0 c (0-0)
49.333a
0.000b
86 a (51–107)
42 b (21–72)
10 c (0–30)
76.025a
0.000b
6 de 4 1 2.1 ab (0–8)
11 d 3 0 3.3 a (0–9)
1e 3 0 0 b (0–6)
9.375c 0.222c 2.000c 10.503a
0.009d 0.895d 0.368d 0.005b
abc, Wilcoxon-test; def, McNemar-test. a x2-test. b Friedman-test, d.f. = 2. c Q-value. d Cochran Q-test, d.f. = 2.
3.2.2. Heart rate As in the first test session, heart rate differed between periods investigated (Fig. 2B). Heart rate increased from the period before the test session (72.6 0.9 beats/min) until the first minute of the test session when the human was standing still beside the cow (78.1 1.1, t = 8.36, P < 0.001), and also from the period before the test session until the periods of stroking the three body regions (W: 77.1 1.1, t = 6.84; NV: 75.4 1.0, t = 4.27; LC: 77.0 1.1, t = 6.69; for all body regions: P < 0.001). As opposed to the first test session, heart rate was lower when the NV was stroked as compared to W (t = 2.57, P < 0.01) and LC (t = 2.41, P < 0.05). Moreover, heart rate was lower during stroking the NV than during the first minute of the test session (t = 4.09, P < 0.001). This was not observed for the other two body regions stroked. 3.3. Difference in behavioural reactions from the first to the second test session Duration of neck stretching and ear hanging increased when certain body regions were stroked. The duration of neck stretching increased from the first to the second test session when the NV was stroked (first session: 3.7 s, second session: 23.8 s; Z = 3.59, P < 0.001). Ear hanging increased from the first to the second test session only during stroking the W (first session: 51 s, second session: 86 s; Z = 4.04, P < 0.001). In contrast, the number of animals performing the other behaviours decreased when certain body regions were stroked. The number of animals performing head shaking when the NV was stroked tended to decrease from the first to the second test session (first session: 18, second session: 11; P < 0.1). When the W was stroked, the number of animals showing head shaking (first session: 16, second session: 6; P < 0.05) and head throwing (first session: 20, second session: 4; P < 0.001) both decreased. Finally, when the LC was stroked, the number of animals throwing their heads decreased (first session: 12, second session: 3; P < 0.05). Duration of contact with the experimenter after stroking did not change from the first to the second test session independent of the body regions stroked (Z > 0.25, P > 0.80).
34
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
4. Discussion 4.1. Differences between body regions stroked in both test sessions The results clearly confirm our hypothesis that the animals differ in their reaction to human tactile stimulation depending on the body region stroked. Much more behavioural reactions were observed when cows’ withers (W) and neck ventral (NV), both body regions often licked during social grooming, were stroked as compared to the lateral chest (LC), a body region rarely licked. In both test sessions, cows responded consistently to stroking the W and NV mainly by neck stretching and ear hanging. Head shaking and head throwing also differed for the various body regions stroked (more for W and NV), but they were observed in a minority of the cows, were expressed rarely, and the occurrence further decreased in the second test session. Heart rate responses also differed for the body regions stroked, being higher when the W was stroked as compared to NV and LC in the first, and lower during stroking the NV as compared to W and LC in the second test session. The behavioural and physiological reactions were not affected by the 3-week treatment of repeated stroking of specific body regions or human presence between the two test sessions. The results are in line with other studies in different species showing that animals’ behavioural and/or physiological responses to human tactile stimulation depend on the body region (horse: Feh and de Mazie´res, 1993; McBride et al., 2004; rat: Kurosawa et al., 1995; Lund et al., 1999; cat: Soenichsen and Chamove, 2002). This study is the first to demonstrate this difference also for cattle. Many previous studies have used tactile stimulation to improve the cattle–human relationship (for review Boivin et al., 2003). However; they did not target specific body regions. This new information could be interesting in order to understand variability in cattle reaction to stroking and to improve the quality of human–cattle interactions. The behavioural and physiological responses to human stroking of the three body regions included in our experiment showed some similarities to the ones observed in intra-specific social licking, depending on the body region stimulated. Neck stretching and ear hanging are typical behaviours during social licking and licking solicitation (Schloeth, 1961; Sambraus, 1969; Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983; Sato et al., 1991). Both behaviours occurred in particularly high proportions during social licking of W and NV, and differed significantly from other body regions including LC (Schmied et al., 2005). The decrease in heart rate, as did occur in the present study during human stroking of the NV in the second test session, could also be found during intra-specific social licking. Sato and Tarumizu (1993) found a decrease in heart rate when calves licked each other, but they did not differentiate the regions that were licked. In a recent study, heart rate was found to be lower when a cow’s ventral neck was licked by a peer as compared to other neck regions (Schmied et al., 2005). This also is in line with studies in horses. A human scratching a body region preferred for social nibbling, e.g. withers, elicited a decrease in heart rate and caused more relaxed and affiliative responses, as compared to massage of a non-preferred area, e.g. shoulder (Feh and de Mazie´res, 1993; McBride et al., 2004). These results taken together suggest the hypothesis that cows may perceive human stroking, at least partly, like intra-specific social licking. Social licking in cattle plays a significant role in strengthening and maintaining social bonds, in relieving social tension and enhancing social cohesion (Sambraus, 1969; Reinhardt, 1980; Sato et al., 1991; Waiblinger et al., 2002). The occurrence of social licking is related to affinities between individuals (Zimmermann-Mu¨ller, 1978; Reinhardt, 1980; Sato et al., 1993) and was shown to have calming effects (lowering heart
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
35
rate; Sato and Tarumizu, 1993). Based on the similarities found in reactions during intra-specific social licking and the differences between body regions, we assume that human stroking of particular body regions, where mutual licking occurs most, could have similar affiliative and maybe rewarding effects on the cow–human relationship as intra-specific social licking has on cows’ social bonds. This could explain the difference observed in soft physical contact with the human (sniffing, head rubbing, . . .) during the 1-min pause after stroking. In the intra-specific social situation, these behaviours are generally seen in a non-agonistic, affiliative context (Simonsen, 1979; Kiley-Worthington and de la Plain, 1983; Mu¨lleder et al., 2003). Indeed, the duration of physical contact with the human established by the cows was shortest after stroking the LC, the rarely licked body region. Of course such interpretation needs to be strengthened by further research. 4.2. Differences between first and second test session The similarities of cows’ responses to human stroking and to social grooming were more pronounced in the second test session, while in the first test session the behavioural and physiological responses less clearly conformed to the hypothesis. The duration of neck stretching and ear hanging during stroking the NV or W were longer as compared to the LC, too, but nevertheless much briefer than during the second test session. More cows showed head throwing or shaking during stroking the NVor W which could be interpreted as a negative perception of stroking these particular body regions. For instance, head throwing is a threat performed to displace another cow (Zimmermann-Mu¨ller, 1978; Kiley-Worthington and de la Plain, 1983), and head shaking is also described to be a mild threat (Simonsen, 1979; Kiley-Worthington and de la Plain, 1983). These behaviours may indicate that some animals did not accept such contact. In the same way, heart rate did not decrease with stroking as it was expected from the hypothesis, but even increased for W as compared to the two other body regions stroked. All in all, it seems that in the first test session stroking did not have the same quality for the animals as in the second test session. There is no factor in this experiment that can be really tested to explain this difference between the two test sessions, as the treatment factor (regular stroking of particular body regions) had no effect in comparison to control (simple human presence). We could, however, assume that both the novelty of the experimental situation and the difference in sensitivity of the body regions stroked were probably responsible for these discrepancies. Heart rate, for example, increases with respect to the novelty of events (for review Boissy and Boissou, 1995), i.e. in the actual experiment it was the novelty of the unknown experimenters and/or the stroking procedure itself. This may explain the heart rate increase found when stroking the W and the lack of difference observed during stroking the NV, as the possible calming effect may have been overridden by the increase. This could also be the case for other behaviours (head throwing, head shaking) that were shown by some cows in the first, but not in the second test session. In the second test session, which followed 3 weeks of repeated human contact, the experimenter had lost her novelty status. This could explain why the results of this second test session were more in line with our hypothesis. Despite the novelty of the situation in the first stroking session, the reactions of the cows nevertheless differed depending on the body region stroked, which enhances the significance of the findings and supports the hypothesis of a body-region-specific sensibility, possibly caused by differences in the density of somatosensory afferent innervation, as suggested by Kurosawa et al. (1995) and Lund et al. (1999). Reactions of cows to stroking of other body regions such as the basis of the tail (commonly used by farmers, but licked rarely in social interactions) or the back side of the hind legs (licked
36
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
by the mother in suckling calves) would be interesting to compare with the body regions used in this experiment. This additional information would extend our understanding of the animals’ perception of such contact in the purpose of improving human–animal interactions. 5. Conclusion In this experiment, stroking the body regions often licked during social grooming led to much more responses than stroking the one licked rarely; in addition, a lot of these reactions are similar to those observed during intra-specific social licking. This suggests that cows could perceive human stroking of body regions often licked – at least partly – like social licking, which again indicates that stroking these body regions is an especially interesting way of tactile contact with cows. Whether stroking the body regions most often licked is also associated with a more effective improvement of the cow’s relationship to humans is currently being investigated at our Institute. Acknowledgements The authors thank the staff of the University of Veterinary Medicine’s Teaching and Research Estate for the help in performing the experiment. Moreover, we are grateful to Isabella ChorolezPerner for reviewing the English language. References Anderson, S., Gantt, W.H., 1966. The effect of person on cardiac and motor responsivity to shock in dogs. Cond. Reflex 1, 181–189. Boccia, M., Reite, M., Laudenslager, M., 1989. On the physiology of grooming in a pigtail macaque. Physiol. Behav. 45, 667–670. Boissy, A., Boissou, M.-F., 1995. Assessment of individual differences in behavioural reactions of heifers exposed to various fear-eliciting situations. Appl. Anim. Behav. Sci. 46, 17–31. Boivin, X., Le Neindre, P., Chupin, J.M., 1992. Establishment of cattle–human relationships. Appl. Anim. Behav. Sci. 32, 325–335. Boivin, X., Lensink, J., Tallet, C., Vessier, I., 2003. Stockmanship and farm animal welfare. Anim. Welf. 12, 479–492. Bradshaw, J., 1992. The Behaviour of the Domestic Cat. CABI, Wallingford. Breuer, K., Hemsworth, P.H., Barnett, J.L., Matthews, L.R., Coleman, G., 2000. Behavioural response to humans and the productivity of commercial dairy cows. Appl. Anim. Behav. Sci. 66, 273–288. Caroprese, M., Napolitano, F., Albenzio, M., Annicchiarico, G., Musto, M., Sevi, A., 2006. Influence of gentling on lamb immune response and human–lamb interactions. Appl. Anim. Behav. Sci. 99, 118–131. Feh, C., de Mazie´res, J., 1993. Grooming at a preferred site reduces heart rate in horses. Anim. Behav. 46, 1191– 1194. Gross, W.B., Siegel, P.B., 1982. Socialization as a factor in resistance to infection, feed efficiency, and response to antigen in chickens. Am. J. Vet. Res. 43, 2010–2012. Hemsworth, P.H., Coleman, G., Barnett, J.L., Borg, S., 2000. Relationships between human–animal interactions and productivity of commercial dairy cows. J. Anim. Sci. 78, 2821–2831. Hennessy, M.B., Williams, M.T., Miller, D.D., Douglas, C.W., Voith, V.L., 1998. Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Appl. Anim. Behav. Sci. 61, 63–77. Kiley-Worthington, M., de la Plain, S., 1983. The Behaviour of Beef Suckler Cattle (Bos taurus). Birka¨user Verlag, Basel. Kostarczyk, E., 1992. The use of dog–human interaction as a reward in instrumental conditioning and its impact on dogs’ cardiac regulation. In: Davis, H., Balfour, D. (Eds.), The Inevitable Bond, Examining Scientist–Animal Interactions. Cambridge University Press, Cambridge, pp. 109–131. Kurosawa, M., Lundeberg, T., Agren, G., Lund, I., Uvna¨s-Moberg, K., 1995. Massage-like stroking of the abdomen lowers blood pressure in anesthetized rats: influence of oxytocin. J. Autonom. Nerv. Syst. 56, 26–30.
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
37
Lensink, B.J., Boivin, X., Pradel, P., Le Neindre, P., Vessier, I., 2000. Reducing veal calves’ reactivity to people by providing additional human contact. J. Anim. Sci. 78, 1213–1218. Lensink, B.J., Vessier, I., Florand, L., 2001. The farmer’s influence on calves’ behaviour, health and production of a veal unit. J. Anim. Sci. 72, 105–116. Lund, I., Lundeberg, T., Kurosawa, M., Uvna¨s-Moberg, K., 1999. Sensory stimulation (massage) reduces blood pressure in unanaesthetized rats. J. Autonom. Nerv. Syst. 78, 30–37. Lynch, J.J., 1977. The Broken Heart: the Medical Consequences of Loneliness. Basic Books Inc., New York, pp. 156–180. Lynch, J.J., Gantt, W.H., 1968. The heart rate component of the social reflex in dogs: the conditioned reflex of petting and person. Cond. Reflex 3, 69–80. Lynch, J.J., Fregin, G.F., Mackie, J.B., Monroe Jr., R.R., 1974. Heart rate changes in the horse to human contact. Psychophysiology 11, 472–478. McBride, S.D., Hemmings, A., Robinson, K., 2004. A preliminary study on the effect of massage to reduce stress in the horse. J. Equine Vet. Sci. 24, 76–81. McMillan, F.D., 1999. Effects of human contact on animal health and well-being. J. Am. Vet. Med. Assoc. 215, 1592– 1598. Mu¨lleder, C., Palme, R., Menke, C., Waiblinger, S., 2003. Individual differences in behaviour and in adrenocortical activity in beef-suckler cows. Appl. Anim. Behav. Sci. 84, 167–183. Pinheiro, J.C., Bates, D.M., 2000. Mixed-effects Models in S and S-Plus. Statistics and Computing Series. SpringerVerlag, New York. R Development Core Team, 2004. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. Reinhardt, V., 1980. Untersuchung zum Sozialverhalten des Rindes: Eine 2-ja¨hrige Beobachtung an einer halb-wilden Rinderherde (Bos indicus). Birkha¨user Verlag, Basel. Rushen, J., Taylor, A.A., de Passille´, A.M., 1999. Domestic animals’ fear of humans and its effect on their welfare. Appl. Anim. Behav. Sci. 65, 285–303. Rushen, J., Munksgaard, L., Marnet, P.G., DePassille´, A.M., 2001. Human contact and the effects of acute stress on cows at milking. Appl. Anim. Behav. Sci. 73, 1–14. Sambraus, H.H., 1969. Das soziale Lecken des Rindes. Z. Tierpsychol. 26, 805–810. Sato, S., 1984. Social licking pattern and its relationships to social dominance and live weight gain in weaned calves. Appl. Anim. Behav. Sci. 12, 25–32. Sato, S., Tarumizu, K., 1993. Heart rates before, during and after allo-grooming in cattle (Bos taurus). J. Ethol. 11, 149–150. Sato, S., Sako, S., Maeda, A., 1991. Social licking patterns in cattle (Bos taurus): influence of environmental and social factors. Appl. Anim. Behav. Sci. 32, 3–12. Sato, S., Tarumizu, K., Hatae, K., 1993. The influence of social factors on allogrooming in cows. Appl. Anim. Behav. Sci. 38, 235–244. Schloeth, R., 1961. Das Sozialleben des Camargue-Rindes. Z. Tierpsychol. 18, 574–627. Schmied, C., Boivin, X., Waiblinger, S., 2005. Ethogramm des sozialen Leckens beim Rind: Untersuchungen in einer Mutterkuhherde/Ethogram of social licking: investigations in a beef suckler herd. KTBL-Schrift 441, aktuelle Arbeiten zur artgema¨ßen Tierhaltung 2005. Kuratorium fu¨r Technik und Bauwesen in der Landwirtschaft e.V. (KTBL), Darmstadt, pp. 86–92. Seabrook, M.F., 1994. Psychological Interaction between the Milker and the Dairy Cow. Dairy Systems for the 21st Century. ASAE, St. Joseph, MI, pp. 49–58. Siegel, S., 1997. Nicht parametrische statistische Methoden. Verlag Dietmar Klotz GmbH, Frankfurt am Main, 4. Auflage, ISBN 3-88074-102-6. Simonsen, H.B., 1979. Grooming behaviour of domestic cattle. Nord. Vet.-Med. 31, 1–5. Soenichsen, S., Chamove, A.S., 2002. Responses of cats to petting by humans. Anthrozoo¨s 15, 258–265. Tallet, C., Veissier, I., Boivin, X., 2005. Human contact and feeding as rewards for the lamb’s affinity to their stockperson. Appl. Anim. Behav. Sci. 94, 59–73. Uvna¨s-Moberg, K., Petersson, M., 2005. Oxytocin, ein Vermittler von Antistress, Wohlbefinden, sozialer Interaktion, Wachstum und Heilung. Z. Psychosom. Med. Psychother. 51, 57–80. Uvna¨s-Moberg, K., Alster, P., Lund, I., Lundeberg, T., Kurosawa, M., Ahlenius, S., 1996. Stroking of the abdomen causes decreased locomotor activity in conscious male rats. Physiol. Behav. 60, 1409–1411. Waiblinger, S., 1996. Die Mensch-Tier-Beziehung bei der Laufstallhaltung von behornten Milchku¨hen. Reihe Tierhaltung Bd. 24, Gesamthochschule Kassel, Witzenhausen. Waiblinger, S., Fresdorf, A., Spitzer, G., 2002. The role of social licking in cattle for conflict resolution. In: Proceedings of the First European Conference of Behavioural Biology, August 1–4 in Mu¨nster, Germany, p. 122.
38
C. Schmied et al. / Applied Animal Behaviour Science 109 (2008) 25–38
Waiblinger, S., Menke, C., Korff, J., Bucher, A., 2004. Previous handling and gentle interactions affect behaviour and heart rate of dairy cows during a veterinary procedure. Appl. Anim. Behav. Sci. 85, 31–42. Waiblinger, S., Boivin, X., Pedersen, V., Tosi, M.-V., Janczak, A.M., Visser, E.K., Jones, R.B., 2006. Assessing the human–animal relationship in farmed species: a critical review. Appl. Anim. Behav. Sci. 101, 185–242. Wood, M.T., 1977. Social grooming patterns in two herds of monozygotic twin dairy cows. Anim. Behav. 25, 635–642. Zimmermann-Mu¨ller, M.E., 1978. Zur Sozialstruktur des Hausrindes Bos Taurus–Ein Vergleich des Sozialverhaltens auf der Weide und im Laufstall. Inauguraldissertation, Basel.