Applied Animal Behaviour Science 84 (2003) 23–39
Influences on the avoidance and approach behaviour of dairy cows towards humans on 35 farms S. Waiblinger a,∗ , C. Menke a , D.W. Fölsch b a
Institute of Animal Husbandry and Animal Welfare, University of Veterinary Medicine, Veterinärplatz 1, A-1210 Vienna, Austria b Farm Animal Behaviour and Management, Faculty of Organic Agriculture, University of Kassel, 37213 Witzenhausen, Germany Accepted 14 May 2003
Abstract The human–animal relationship is an important issue when assessing animal welfare on farms, but generally accepted and used methods for its practical assessment on dairy farms have been lacking until now. The aim of this study was to validate different farm test of cows reactions towards humans concerning the ability to reflect the quality of the human–animal relationship and investigate the relative importance of other factors influencing the relationship. On 35 dairy farms with loose housing, avoidance distance of cows in the stable, avoidance reactions in the feeding rack and approach behaviour towards an unfamiliar person as well as approach to a novel object were tested. The behaviour of stockpeople towards cows, their management of cows, social interactions of the herd and animal, herd and housing variables were recorded. Avoidance distances in the stable were highly correlated with intensity/quality and continuity of contact (herd median of avoidance distance, ADME: rs = −0.66; percentage of cows with avoidance distance 0, AD0: rs = 0.55; both P < 0.001) as well as with the frequency of friendly interactions by the milker (ADME: rs = −0.66; AD0: rs = 0.59; both P < 0.001). Stepwise regression identified the main influence of human–animal interaction variables on avoidance reactions towards man. Herd size, breed and age showed much lower or no relationship to cow behaviour. Further, low avoidance of the human was related to a high frequency of social licking in both correlation and regression analyses (P < 0.05–0.01). Approach reactions to a human showed lower and less consistent correlations but related well with approach to a ball. Avoidance distance of cows towards an unfamiliar person in the stable reflect well the human–animal relationship on the farm and can be used as a basis for its on-farm assessment. In contrast, the test in the feeding rack and the approach test relate more to other factors, for example, social behaviour of the herd, or individual motivation to approach, and thus, these reactions are less suitable measures. © 2003 Elsevier B.V. All rights reserved. Keywords: Human–animal relationship; Behaviour; Cows; On-farm assessment ∗
Corresponding author. Tel.: +43-1-25077-4905; fax: +43-1-25077-4990. E-mail address:
[email protected] (S. Waiblinger). 0168-1591/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0168-1591(03)00148-5
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1. Introduction The importance of stockmanship and the human–animal relationship for farm animal welfare, health and performance has been demonstrated in several investigations. Handling of farm animals in a positive or negative way can increase or decrease performance, for example, in reproductive success or milk yield of dairy cows (Seabrook, 1972, 1984, 1986; Unshelm, 1990; Hemsworth et al., 2000; Waiblinger et al., 2002b). Negative handling experiences can lead to a higher level of fear of man and hormonal stress reactions with negative effects on performance, welfare and on ease of handling with an increasing risk of injuries both for animal and man during handling (Mack, 1979; Hemsworth and Coleman, 1998; Rushen et al., 1999a, 1999b; Lensink et al., 2001), while positive handling might improve the welfare (Lensink et al., 2000a,b; Waiblinger et al., 2003). Accordingly, behaviour of cows towards man also can be related to performance and ease of handling (Seabrook, 1972; Albright, 1978; Breuer et al., 2000). Therefore, measuring the human–animal relationship is important when assessing animal welfare on farms or investigating the production success of commercial farms. However, generally accepted and used methods for its practical assessment on dairy farms have been lacking until now. The human–animal relationship involves both stockmen and farm animals; it develops from social interactions (Estep and Hetts, 1992) and therefore its quality should be reflected in the behaviour of both participants in the relationship. Observations of stockpeople could bias their behaviour and questionnaires include the risk of dishonest answers, if the aim of the assessment cannot be hidden, for example, in control situations. Behavioural tests of the farm animals’ reactions towards man could be more informative parameters if they really reflect the human–animal relationship, reflecting contributions from both the animal and the human. The cattle of the nomadic Fulbes are very tame and approachable because of the intensive daily contact beginning at birth (Hinrichsen, 1979; Lott and Hart, 1979). Avoidance distance from a person is supposed to reflect previous experience of animals with humans (Sambraus, 1974; Grandin, 1987; Purcell et al., 1988). In the on-farm context within one breed of dairy cows, avoidance distance of the animals in the stable was shown to relate well to the behaviour of the milker (Waiblinger et al., 2002b). However, other responses might be more feasible (less time consuming, easier to apply) or even more meaningful. Approach behaviour is interpreted as level of fear of man due to experiences of positive or negative handling (Hemsworth and Coleman, 1998). Approach behaviour of dairy cows in a standard test outside the herd relates to the milker’s behaviour (Hemsworth et al., 2000), but the test is not feasible for on-farm welfare assessment because it requires separating each animal for testing. Moreover, although the previous amount and quality of experiences with humans were shown to be important factors for the avoidance and approach behaviour towards man by the animals, further influences on an animals’ response to humans have been identified in the literature, such as rank position, age, genetics or the social environment (Dickson et al., 1970; Sambraus, 1974; Murphey et al., 1980, 1981; Price and Wallach, 1990; Le Neindre et al., 1993; Grignard et al., 2000; in pigs: Hemsworth et al., 1990). The relative importance of such factors on farms in influencing the animals’ reactions to humans besides the history of human–animal interactions has not been investigated in dairy
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cows to the authors’ knowledge, but should be able to be determined if farms differing in these aspects are compared with respect to their human–animal relationship. Also, knowledge about such influences is necessary for a suitable sample selection on the individual farm. Therefore, the aim of our study was to test reactions of cows towards humans on commercial farms on the hypothesis that these reactions reflect validly the human–animal relationship on these farms, determine what other factors might influence these reactions, their relative importance and which reaction test is the most suitable. For this purpose, the reactions of cows were investigated in 35 dairy herds, in conjunction with a survey on the social behaviour and the injuries of horned dairy cows in loose housing (Menke, 1996; Menke et al., 1999).
2. Methods 2.1. Farms and animals Thirty five farms with horned dairy cows in loose housing were selected for the investigation. There were three types of loose housing: cubicle housing (16), straw bedding pen (15) and straw flow pen (4). In 11 farms an outside yard existed and the space per cow varied from 4.8 to 25 m2 . The farms kept different breeds: Dapple Black (6), Dapple Red (3), Brown Race (7), Brindled Cattle (9), Red Cattle (3), Jersey (1), Yellow cattle (1), Vorderwälder (1) and different breeds within a herd (4). On eight farms, a bull ran with the herd. In total, 1100 cows were kept on the farms. The herd size ranged from 9 to 90 cows. On all farms, the rearing method was similar (calves being separated from the mother at the age of 0 to 14 days and fed by man). Thus all cows were artificially reared and suckled by man, giving all cows a certain degree of habituation to and contact with humans during rearing from birth on. Differences in experiences with humans during rearing depend on the human–animal relationship between the stockperson and the calf in a way similar to this relationship in adult cows. Mostly, both cows and calves were cared for by the same people. On a few farms different persons were responsible for calves and cows (farms 5 and 21) or staff had changed since the rearing of the dairy cows (farms 13 and 15). 2.2. Approach and avoidance behaviour of cows All tests were conducted by the same test person, dressed in the same manner, on all farms to reduce the possible influence of different experimenters. To allow individual recording of the cows, they were marked with painted numbers on the back. Three different reactions towards the test person and one reaction towards a novel object were tested: the avoidance distance in the stable, the avoidance distance in the feeding rack, approach behaviour to a standing person and the approach behaviour to a ball. The last test was included because in an earlier study (Wyss, 1988; Wyss et al., 1993) it correlated with the behaviour of the milker and may provide a measure of the general motivation to approach to a novel stimuli (unfamiliar human or unfamiliar object). When necessary, bulls were separated from the herd during tests.
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2.2.1. Avoidance—distance in the stable Standing animals were approached slowly (one step per second) from the front by the test person, who held the arm overhand in an angle of about 45◦ in front of the body. The distance between the person’s hand and the animal’s head was estimated at the moment of the cow’s withdrawal. The avoidance distance was tested on 50–100% of the cows in the herd (depending on herd size), once or twice per animal. For each herd the median of the avoidance distances (ADME) and the proportion of animals with an avoidance distance of zero (AD0 = animal could be touched at the head) were calculated. 2.2.2. Avoidance—distance in the feeding rack The animals were approached slowly (one step per second) by the test person during feeding in the feeding rack until withdrawal of the cow or until touching and the distance between the test person’s hand and the cow’s head was estimated at the moment of withdrawal. In most farms (29) this was done when cows were restrained in the feeding rack. On four farms cows were not restrained during feeding times. On two farms the test could not be conducted because of the feeding table being too small to reach the minimum start distance of 2 m or because of time problems (milking time and main feeding time were the same), respectively. The percentage of cows that tolerated touching (A0FR) was calculated for each farm. 2.2.3. Approach—behaviour towards an unknown person Just before starting the test, the test person went slowly to a central place of the stable (not in a corner, but more in the middle of the stable; good accessibility from both sides of the person, good visibility of the person) and stayed there for 15 min. The number of the cows approaching the test person until touching was recorded after 15 min. Because it was assumed that the motivation of a cow to approach a human is not high enough to rise from a lying position, the number of animals standing was recorded at the start of the test. The number of animals that touched the test person within the 15 min test was calculated as percentage of the animals standing (AM15). On farm 7 the approach test was interrupted because of the bull running in the herd. Values for this test are missing there. 2.2.4. Approach—behaviour towards a novel object A novel object (a pink and white ball) was hung up in a central part of the stable and stayed there for 15 min. The number of the cows approaching until touching the novel object within the 15 min was recorded and the percentage of animals standing at the beginning of ˆ the test that touched the ball was calculated (AB15). 2.3. Influencing factors 2.3.1. Behaviour and management of stockpeople The behaviour of the milkers towards the cows was observed during two milking times on two successive days (on most farms two evening milkings; on two farms one evening and the consecutive morning milking was observed to avoid observing a relief milker). The study was part of a project on social behaviour and injuries of horned dairy cows in loose housing and the milkers were told that the observations in the milking parlour serve to assess
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the behaviour of the cows in this situation also. Stockpeople were informed about the true aim (observation of their behaviour) after all relevant data recordings were finished on the farm. The number of times milkers touched the cows and talked to the cows was recorded, and categorised into four qualitative classes: (1) calm, friendly; (2) dominant, determined; (3) impatient, fierce; (4) aggressive (although the last category was never observed during milking). For further evaluation, the total number of touching/talking (TTT = sum of category 1, 2, 3) and the number of friendly touching/talking (TTF = category 1) per cow was calculated. If two persons milked together or by turns, the average of both was taken. On seven farms the person milking during the observation was not representative for the daily situation, e.g. because they were relief milkers or personnel had changed within the last 3 months. These seven farms therefore were disregarded when calculating correlations with the milkers’ behaviour. The handling of the cows, and the ability to identify individual cows were observed during routine work. The stockpeople completed a questionnaire about management practices. The 21 questions/variables were ranged on a 3-point ordinal scale according to increasing financial or work expenditure, increasing value for welfare or for a good human–animal relationship. The variables were grouped together to six indices using theoretical considerations and factor analysis. Only two of these indices are relevant to the present paper: • CONPS: ‘intensity/quality and continuity of contact’; average of the single variables frequency of brushing, identification of cows, handling gently, number of milkers and frequency of personnel changes; • MGF: ‘management and situation during feeding’, average of the single variables ratio of feeding places to animals, fixing of cows simultaneously, sorting cows in the feeding rack, opening feeding rack simultaneously. 2.3.2. Herd, animal and housing variables The social behaviour of the herd was observed on two consecutive evenings for 4 h beginning 1 h after opening the feeding rack or after the end of milking. The frequency of chasing away, pushing away, butting, horning and social licking was recorded with continuous behaviour sampling. Also, the age of the individual cows and housing dimensions were recorded. 2.4. Statistical methods For testing associations, Spearman rank correlation coefficients were calculated for the reactions of cows towards the test person with the influencing factors and interrelationships amongst the different reactions. To take into account the interrelationships of the influencing factors and to be able to evaluate the relative importance of these different factors for the reactions of the cows, a multivariate analysis was performed for the avoidance reactions. By this, partial correlations between two variables after the removal of a common relationship to a third variable can be done. A forward stepwise multiple regression was calculated separately for the dependent variables ADME, AD0 and A0FR. Transformations were carried out with dependent variables to get residuals with normal distributions. Models of regression were validated with analysis of residuals. If assumptions (normality of residuals, no heteroscedascity, autocorrelation,
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multicollinearity) were not fulfilled, a model was disregarded. No regression model was calculated for approach behaviour because of low correlations with stockpeople behaviour (see Section 3). To test the influence of age on avoidance distance, Spearman rank correlation coefficients were calculated within 27 herds, where ages of cows were recorded. All statistical analysis was done with the statistical program SYSTAT® 5.0 for Windows.
3. Results The 35 farms varied markedly with respect to both the behaviour of the cows and the behaviour of the stockpeople. 3.1. Avoidance and approach behaviour—comparison of herds and interrelationships
100 90 80
1.60
AD0 ADME herd size
1.40 1.20
70 1.00
60 50
0.80
40
0.60
30 0.40 20 0.20
10 0
0.00
median of avoidance distance in m (ADME)
herd size / % of cows with avoidance distance of 0 (AD0)
The median avoidance distance per herd (ADME) ranged from 0 to 1.5 m, and the percentage of cows with avoidance distance 0 (AD0) from 2 to 67% per herd of the tested animals (Fig. 1). However, for ADME, 50% of the farms were within a small range from 0.15 to 0.35 (25 and 75% percentile, respectively), while AD0 showed a greater range (25, 75% percentile: 7, 24, respectively). Because of the definition of the two variables, ADME and AD0 are complementary in most cases, but in a few herds (nr. 6, 16, 35) both values are low. There is a highly significant negative correlation between ADME and AD0 (rs = −0.67, n = 35, P ≤ 0.001; Fig. 2). The number of cows with an avoidance
2 1 27 4 28 24 34 3 30 31 32 26 33 5 25 35 18 29 19 10 9 21 6 15 22 16 7 11 23 13 17 14 8 20 12
Brown Swiss
Simmental
farms other mixed RedP GRed Black pied breed
Fig. 1. Median of avoidance distance (ADME) and percentage of animals that could be touched (AD0) on the 35 farms, sorted by breed and herd size.
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80 70 60 50 40 30 20 10 0 0,00
0,20
0,40
0,60
0,80
1,00
1,20
1,40
1,60
ADME (m) Fig. 2. Scatterplot of the median of avoidance distance (ADME) and the percentage of animals that could be touched (AD0).
distance of 0 in the feeding rack (A0FR) and AD0 both refer to animals accepting being touched by the unfamiliar experimenter and consequently a strong correlation was found between these two variables (rs = 0.74, n = 33, P ≤ 0.001). A0FR also correlates significantly with ADME, but the coefficient was lower (rs = −0.59, n = 33, P ≤ 0.001). Range and variation of approach to the test person and the ball is shown in Fig. 3. Herds with a higher percentage of animals approaching the person within 15 min also showed a higher approach to the ball (rs AM15/AB15 = 0.52, n = 34, P ≤ 0.001, Fig. 4). AB15 was higher compared to AM15 in 82% (28 of the 34) of the herds. Approach behaviour to a person correlated significantly with ADME (rs AM15/ADME = −0.54; n = 34, P ≤ 0.01; Fig. 5) and AD0 (rs AM15/AD0 = 0.34, n = 34, P ≤ 0.05), but not with A0FR (rs AM15/A0FR = 0.22, n.s.). 3.2. Associations with influencing factors 3.2.1. Avoidance distance and age A possible influence of the age of the animals on their avoidance distance was investigated by Spearman rank correlations within 27 herds. Both positive (12) and negative (15) correlation coefficients were found, but most of them were not significant and very low (≤0.2 in 18 herds, >0.2 < 0.35 in four herds). In one herd, the older cows had a significant larger avoidance distance than the younger cows (herd 13, n = 25, rs = 0.56, P ≤ 0.01) and in two further herds the older cows tended to withdraw at a larger distance (herd 18: n = 8, rs = 0.63, P = 0.097; herd 23: n = 25, rs = 0.36, P = 0.081). In two herds the older cows were more approachable than the younger ones (herd 19: n = 19,
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% cows approaching
80 70
AM15 AB15
60 50 40 30 20 10 0 7 29 4 8 34 21 12 19 16 13 14 22 15 20 2 5 24 27 30 33 11 17 3 9 10 23 35 1 31 32 6 25 26 28 18
farms Fig. 3. Percentage of cows that approached the test person (AM15) or a ball (AB15) until touching within 15 min from all cows standing at the start of the test, not of all cows in the herd, was calculated.
rs = 0.58, P ≤ 0.01; herd 21: n = 36, rs = 0.42, P ≤ 0.01). Altogether there was no uniform association between age and avoidance distance and in most herds there was no relationship at all. Further, there was no correlation between the herd values of avoidance distance (ADME, AD0) and average age of the herd. 60
AM 15 (%)
40
20
0 0
20
40
60
80
100
AB15 (% ) Fig. 4. Scatterplot of the percentage of cows that approached the test person (AM15) or a ball (AB15) until touching within 15 min from all cows standing at the start of the test.
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31
60
50
AM15 (%)
40
30
20
10
0 0,00
0,20
0,40
0,60
0,80
1,00
ADME (m) Fig. 5. Scatterplot of the median of avoidance distance (ADME) and the percentage of cows that approached the test person (AM15) until touching within 15 min from all cows standing at the start of the test.
3.2.2. Avoidance reactions and behaviour and management of stockpeople Spearman rank correlations between the behaviour of the animals and influencing factors are shown in Table 1. The strongest associations exist between the avoidance reaction in the stable (ADME and AD0) and the variables of daily contact and handling, i.e. the behaviour of the milker to the cows (TTT, TTF) and the intensity/quality and continuity of contact (CONPS). Within the measure CONPS the single variable “frequency of brushing” had the strongest relationship to the avoidance distances. The type of contact in the milking parlour was also important; the correlation coefficient for friendly touching/talking to (TTF) was higher than that for the total sum of touching/talking to (TTT). Here it is important to note that the percentage of TTF on most farms was quite high: the median percentage of friendly touching/talking to was 81.3%, ranging from 21 to 100%. Management practices which include close handling of animals (MGF; for example, confining the animals individually in the feeding rack) were correlated significantly with the avoidance distance measures. Using stepwise regression analysis, the variables of daily contact and handling were the strongest predictors for all three measures of avoidance distance (Tables 2–4). For example, the variable CONPS alone explained 49.3% (adj. R2 ) of the variance of the dependent variable ADME, while all other variables in the model only increased the adj. R2 by 11% up to a total of 61%. The behaviour of the milker could not be included in the same models because of the strong association between CONPS and TTT (rs = 0.59; P ≤ 0.01) or TTF (rs = 0.62; P ≤ 0.01) and therefore multicollinearity. Calculating the model with frequency of touching/talking to cows instead of intensity/quality of contact gave similar results. In the model of AD0, MGF was a significant predictor.
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Table 1 Spearman rank correlation coefficients between reactions of the cows towards the test person and possible influencing factorsa
Behaviour of the milker Total touch/talk to cows (TTT)d Friendly touch/talk to cows (TTF)d Intensity/quality of contact CONPSd Frequency of brushing Identification of cows Handling gently Number of milkers Frequency of personnel changes
Avoidance distance median (ADME)
Avoidance distance 0 (AD0)
rs
P-value
rs
−0.59
<0.001
0.46
<0.01
0.21
n.s.
0.48 <0.01
−0.66
<0.001
0.59
<0.001
0.35
<0.05
0.41 <0.05
−0.66 −0.51 −0.37 −0.44 −0.46 −0.39
<0.001 <0.01 <0.05 <0.01 <0.01 <0.05
0.55 0.59 0.51 0.33 0.29 0.19
<0.001 <0.001 <0.01 <0.05 <0.05 n.s.
0.51 0.58 0.39 0.34 0.19 0.23
<0.01 <0.001 <0.05 <0.05 n.s. n.s.
0.38 0.11 0.38 0.11 0.37 0.34
<0.05
0.53b
<0.01
0.39b
<0.05
0.11 n.s.
<0.05 <0.01 <0.01 n.s.
−0.40b 0.34b −0.32b −0.12b
<0.05 <0.05 <0.05 n.s.
Management, herd and animal variables 0.42b Management feeding rack (MGF)b Frequency of social behaviour Agonistic—pushing away 0.14 Affiliative—social licking −0.40 Herd size 0.26 Proportion of dehorned cows 0.35
n.s. <0.05 n.s. <0.05
Avoidance distance feeding rack 0 (A0FR)b
P-value rs
−0.27 0.51 −0.52 −0.28
Approach to a person within 15 min (AM15)c
P-value rs
P-value
−0.18 0.37 −0.16 −0.16
<0.05 n.s. <0.05 n.s. <0.05 <0.05
n.s. <0.05 n.s. n.s.
All others: n = 35. n = 32. c n = 34. d n = 28. a
b
3.2.3. Avoidance reactions and herd, animal and housing variables Beside the variables of contact with the stockman, the social behaviour within the herd was also related significantly to the avoidance behaviour of the cows. All three measures of avoidance reactions (ADME, AD0 and A0FR) were significantly correlated with the Table 2 Model of regression for estimating ADME (herd-median of avoidance distance)a Variable
Coefficient of regression
Standard regression of coefficient
P
CONPS Herd size Social licking Proportion of dehorned cows
−1.045 −0.015 −1.526 2.413
−0.668 −0.418 −0.406 0.200
0.000 0.007 0.007 0.098
a
R2adj. = 0.610, standard error = 0.453, P = 0.000, dependent variable Y = log(ADME + 1/16).
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Table 3 Model of regression for estimation of AD0 (percent of cows with avoidance distance of 0)a Variable
Coefficient of regression
P
CONPS MGF Breed
0.277 0.352
0.041 0.011 0.213
a
Adjusted R2 = 0.570, P = 0.000, dependent variable Y = log(AD0 + 1/8).
social licking (Table 1). Avoidance in the feeding rack (A0FR) also correlated significantly negatively with the agonistic behaviour pushing away (PUSH). Social licking appeared as a predictor in the regression analysis for ADME and A0FR (P < 0.01 and 0.05, respectively). Further factors apart from daily contact were correlated distinctly lower in most cases and not consistently over the three avoidance variables (Table 1). Herd size, breed and proportion of dehorned animals were included in the models of regression of A0FR, AD0 or ADME, respectively, as non-significant predictors (Tables 2–4). The time that the cows were confined in the feeding rack (Fgh) was a significant predictor for A0FR (Table 4). 3.2.4. Comparing the avoidance reactions The model for ADME shows the highest amount of variance accounted for (adj. R2 = 0.61). The explained variance of AD0 was similarly high with 57%. The explained variation is markedly lower (adj. R2 = 0.44) for A0FR compared to the former models. 3.2.5. Approach reactions and influencing factors Approach to the test person (AM15) correlated less strongly with the variables of daily contact and handling than the avoidance reactions (Table 1). However, cows approached more in herds with higher CONPS, TTT or TTF. Again, there was a correlation between approach and the social behaviour; both social licking and horning were positively correlated with approach behaviour. Approach to the ball only correlated with TTT, TTF and horning. Because the correlations were much lower compared to those of avoidance reactions, no regression analysis was calculated for approach reactions.
Table 4 Model of regression for estimation of A0FR (percent cows with avoidance distance of 0 in the feeding rack)a Variable
Coefficient of regression
Standard coefficient of regression
P
CONPS Time in feeding rack Social licking Herd size
1.890 0.349 3.199 0.036
0.552 0.433 0.398 0.387
0.004 0.008 0.042 0.090
a
Adjusted R2 = 0.437, standard error = 1.203, P = 0.001, dependent variable Y =
√
A0FG + 3/8.
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4. Discussion 4.1. Avoidance distance in the stable The results confirm our hypothesis, that the avoidance distance validly reflects the human– animal relationship. The proportion of variance of both the median of avoidance distance (ADME) and the proportion of animals that could be touched (AD0) explained by the variables of daily contact and handling (CONPS; TTT, TTF) were very high and were much lower for other variables. This is in line with earlier results, where avoidance distance was correlated with the behaviour of the milker (Waiblinger et al., 2002b). In experimental studies, avoidance reactions of cattle were influenced by previous experience of positive or negative handling (Boissy and Bouissou, 1988; Munksgaard et al., 1997, 2001). Breed did not have a significant relationship to the avoidance reactions in our study. In contrast, Murphey et al. (1980) found breed differences in avoidance distances in open pasture in cattle that were reared under the same conditions and concluded that avoidance distance is a relatively stable characteristic of a breed. However, Murphey et al. compared beef and dairy cattle. Differences within dairy or within beef might be less pronounced. Boivin et al. (1994) also did not find a difference in reactions to handling between Saler and Limousin cattle reared under the same conditions. However, though not significant, a breed effect cannot be excluded totally and we only have a limited number of herds with the same breed. A breed disposition, which is modified strongly by experiences, may exist. The average age of the cows did not confound the assessment of human–animal relationship on the farms in our study. Also within farms, there was no consistent influence of the age of the cows on avoidance distance. On most farms there was no effect at all. However, on few farms age was related to the avoidance reactions. Thus, it might be crucial to include animals of different age classes to get a valid measure on some farms. This has to be considered in sample selection. Besides indirect negative effects of increasing herd size on avoidance reactions via a decreasing intensity/quality and continuity of contact (Waiblinger and Menke, 1999), a larger herd seem to reduce avoidance distance. It might be that the individual animal feels more secure in a bigger herd. In sheep, individual animals had greater flight distance than flocks (Hutson, 1982). The negative relationship between social licking and avoidance distance (i.e. the avoidance distance was lower when cows performed more social licking) might have a similar basis of higher security. Social licking might have a calming effect, reduce social tension and stabilise dominance–subordinate relationships (Waiblinger et al., 2002a); see also effects of social grooming in other species (Aureli et al., 1999). Social licking is thought to strengthen bonds between animals and is performed most frequently with preferred partners (Reinhardt and Reinhardt, 1981; Sato et al., 1993). Thus, a high occurrence might be indicative of intact social bonds in the herd and high social stability. This might give the animals more security and social support and thus alter the animals’ reactions in a challenging situation, e.g. towards an unfamiliar human. Sheep with familiar peers grazed a preferred feeding site, situated in some distance from a socially attractive
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one, for longer and were less vigilant than those with unfamiliar companions (Boissy and Dumont, 2002). Boissy and Le Neindre (1990) showed that heifers are less likely to avoid an unusual noise in the presence of pen-mates. Veissier and Le Neindre (1992) found fewer fear reactions in heifers in a novel environment in groups compared to single animals. On the basis of regression and correlation analyses involving the different cow reactions, the most appropriate reaction for on-farm assessment of human–animal relationship is avoidance distance. Using herd averages (median) and the percentage of animals with AD0 it seems to be possible to differentiate between a very close, “personal” contact, where the stockperson regularly grooms (brushing, stroking) the animals and by this takes the role of a positively interacting social partner, and a less “personal”, less intensive contact, characterised by appropriate handling avoiding negative interactions, only limited grooming, but enough positive interactions to get animals with a very low level of fear. Though the relationship between both contact measures is high and, in general, in the opposite direction, in some farms both values are low, for example, in the biggest herd of the investigation, herd number 35. On those farms animals are not fearful of humans in close proximity, but do not accept being touched. The results suggest that those animals rarely have negative experience, but also most of the individuals are lacking the experience of being gentled by the stockperson. 4.2. Avoidance reaction in the feeding rack Again the variables of daily contact and handling were correlated most highly with the avoidance reaction of cows in the feeding rack (A0FR). However, correlations with most variables and the explained variance in the regression model were lower compared to ADME or AD0. Especially, the relationship to the behaviour of the milker was much lower. The reaction in the feeding rack was significantly correlated to agonistic behaviour. This might be due to the fact that the feeding area is an area of high competition, where most agonistic interactions take place. Here it is important to remember that we observed horned cows, where butts can be more aversive. A higher level of agonistic behaviour might enhance the animals’ alertness (to avoid being butted) and this also may influence the reactions to an unfamiliar person. On the other hand, the relationship between the social behaviour and the animals’ avoidance reactions might be mediated by a common relationship with human behaviour: stockpeople showing a higher intensity/quality and consistency of contact (leading to lower avoidance), better recognise individual cows’ problems, pay attention to and are able to apply an optimal herd management contributing to a balanced social behaviour (Menke et al., 1999; Waiblinger et al., 2001). Further, from theories on aggression and observations in cattle, it is evident that negative experiences with humans may enhance agonistic interactions. Frustration, pain and received aggression, respectively, can lead to aggression (Scott, 1958; Fox, 1968; Neumann and Steinbeck, 1971; Reinhardt, 1980). However, the part of the correlation between social behaviour and avoidance reaction that is due to CONPS is extracted by the regression analysis. Further, only avoidance in the feeding rack is correlated significantly to agonistic social behaviour. This supports our interpretation given above that the social behaviour affects the animals’ reactions to humans.
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4.3. Approach behaviour The results suggest that the human–animal relationship is one of the main factors influencing the approach behaviour towards human, but that simply measuring the number of animals approaching within 15 min (AM15) is only of limited suitability for on-farm assessment of human–animal relationship. AM15 correlated lower and less consistently to the variables of daily contact and handling compared to the avoidance distance in the stable (ADME, AD0). Other factors seem to have more influence here. The interrelationship between the approach to a ball (AB15) and a human (AM15), being as high as the correlation between AM15 and ADME, points to a common basis of the two approach tests making the approach test less specific for human–animal relationship. Approach behaviour is the result of several, possibly conflicting emotions and motivations: curiosity or the motivation to investigate a novel object, including unfamiliar humans, as well as positive expectations might motivate the animal to approach, on the other hand fear causes the animal to avoid the stimulus (Murphey et al., 1981; Hemsworth et al., 1996; Hemsworth and Coleman, 1998; Jago et al., 1999). Thus, the cow will not approach if the motivation to avoid is stronger than the motivation to approach or if there is no motivation to approach at all, e.g. because the human is lacking novelty. During the tests, the behaviour of the cows approaching as well as the cows not approaching until touching varied markedly in qualitative aspects. Three main types of behavioural reactions could be distinguished: (1) interest and approaching without hesitation (cow is looking at the test person and approaching determined, sometimes from a considerable distance); (2) no interest and no sign of fear (e.g. cow is briefly looking at the test person while passing by, no change in direction or speed of the movement); (3) interested cows with hesitation and signs of fear or caution (cow is looking at the test person but does not approach or approaches only step by step with far outstretched head interrupted by withdrawal and stops). We did not systematically record these different types of behaviour from the beginning and thus did not include them in the analysis, but these qualitative differences in the behaviour clearly are related to the different motivations described above and show that a low or high number of approaching animals might have different underlying causes. This was pointed out already by Murphey et al. (1981). If animals generally have a high propensity to investigate novel objects, they should show high motivation to approach both a novel object and an unfamiliar human, which might explain the relatively high correlation of AM15 and AB15. The motivation to approach might compete with and be modified by other motivations, for example, hunger, rumination, resting. Animals in the herds might have differed in these aspects which further can contribute to a higher variation. In sum, the approach test seems to be influenced too much by other factors to be a valid on-farm measure of human–animal relationship. In pigs, Marchant et al. (1997) also concluded that the approach test is influenced by motivation to explore rather than fearfulness of humans. Most of the herds showed more approach to the ball. This suggests that the ball was less fear-eliciting or more interesting. Because (i) cows had no experience with such a ball before, but at least some experience with several humans besides the caretaker, and (ii) the avoidance distance on most farms was low, it is likely that the ball was more interesting and the curiosity of cows was higher in the test with this novel object.
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5. Conclusion The variables of daily contact and handling, that is of the quality, quantity and continuity of human–animal interactions, show the strongest relationship to the animals’ reactions to humans, while other factors of the herd, the animal, the housing or the management are much less important. Despite other influences, avoidance distance of cows towards an unfamiliar person in the stable reflect well the human–animal relationship on the farm and can be used as a basis for its on-farm assessment. In contrast, the test in the feeding rack and the approach test relate more to other factors, for example, social behaviour of the herd, or individual motivation to approach, and thus these reactions are less appropriate. However, further refinement of the approach test by trying to consider the different motivations, might improve its validity. This should be investigated in future because of the shorter time necessary for this test compared to avoidance distance in the stable. Also, tests of animals’ reactions to humans have to be evaluated with respect to reliability and feasibility in the on-farm context before they can be used for on-farm assessment schemes.
Acknowledgements We want to thank very much the participating stockpeople for their cooperation and their hospitality, and G. Coleman for helpful comments and help in English language. The authors acknowledge financial support from the Felix-Wankel Donation, Swiss Federal Veterinary Office, Swiss Animal Protection, Bund gegen den Mißbrauch der Tiere and Swiss Federal Institute of Technology.
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