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Familiarity and group size affect emotional stress in Japanese Black heifers
Applied Animal Behaviour Science 82 (2003) 1–11
Familiarity and group size affect emotional stress in Japanese Black heifers Ken-ichi Takeda*, Shusuke Sato, Kazuo Sugawara Graduate School of Agricultural Science, Tohoku University, Kawatabi, Narugo, Miyagi 989-6711, Japan Accepted 26 January 2003
Abstract We compared behavioural and cardiac responses to emotional stresses between familiar and unfamiliar heifers in groups of two or five. Fourteen Japanese Black heifers were divided into two experimental groups of two individuals (F2) and two groups of five individuals (F5) that were familiar with each other. Four additional Holstein heifers were used in forming the unfamiliar groups (UF2 and UF5), in which the focal animals had never been seen. Experimental animals were equipped with heart-rate monitors and led into a test room (5:5 m 10:0 m) at the experimental station. Each animal was tethered inside a single stall, and the focal animals were monitored by two video cameras. We designed three stress tests for the heifers: (1) a novelty test (encountering a strange object); (2) a surprise test (hearing a loud sound); and (3) a conflict test (trying to eat formula food). In the first test, a red paper doll was presented to the focal animal for 10 min. In the second test, a tin bucket containing several weights was dropped from the ceiling (5 m high) diagonally in front of the focal animal. Three minutes later, the third test was conducted by placing a feed bin containing food pellets covered with wire mesh in front of each animal for 10 min. This series of tests was carried out in the order UF5, UF2, F5, and F2. There were the significant effects of familiarity on behavioural responses in the novelty and conflict test. Moreover, there were not only significant effects of familiarity but also a significant interaction between familiarity and group size on cardiac responses in the surprise and conflict tests. Especially, changes in the mean heart rate during the two tests were minimal in the group F5. Our results indicate that both familiarity and larger group size may reduce emotional stress, and the calming effect of affiliative groups of five may be higher than groups of two for cattle. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Cattle; Social behaviour; Novelty; Surprise; Conflict
* Corresponding author. Present address: Faculty of Agriculture, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, Japan. Tel.: þ81-265-77-1427; fax: þ81-265-77-1427. E-mail address: [email protected] (K. Takeda).
0168-1591/03/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0168-1591(03)00039-X
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K. Takeda et al. / Applied Animal Behaviour Science 82 (2003) 1–11
1. Introduction Communal pastures in which cattle are turned out together from a number of farms are very common in Japan. A major concern with communal pasturing is that the body weights of some animals drop during the initial grazing period. A change of the rearing environment can alter the circadian rhythm (Kondo et al., 1984; Oshio et al., 1985; Veissier et al., 1989) and increase the mean heart rate (Kondo and Hurnik, 1988) in cattle, and it can increase the serum cortisol concentration in pigs (Deguchi, 1998). Moreover, being with unfamiliar animals can increase the heart rate and change the behaviour of sheep (Baldock and Sibly, 1990) and cattle (Kenny and Tarrant, 1987), and animals have been shown to lose weight when associating with unfamiliar individuals (Rushen, 1987). Therefore, environmental and social stressors specific to communal pastures may be responsible for the weight loss of cows and heifers under such circumstances. On the other hand, familiar conspecifics can lower the stress responses of subjects (Arnone and Dantzer, 1980; Gunnar et al., 1980; Coe et al., 1982; Boissy and Le Neindre, 1990; Veissier and Le Neindre, 1992). Coe et al. (1982) found that when individual squirrel monkeys observed snakes, their plasma cortisol concentrations were higher than when they were tested in the presence of a cage mate. The authors suggested that this difference depended on the nature and number of conspecifics that were present. Stanton et al. (1985) taught squirrel monkeys to respond to incandescent light as a conditioned stimulus to electric shock (unconditioned stimulus), and showed that their plasma cortisol concentrations increased when they were tested individually or in pairs, but not when they were in a group of six animals. Takeda et al. (2000) found that those cows with two to four familiar farm mates were behaviourally more socially stable than cows with only one or no farm mates in a communal pasture. Cows with only one farm mate may therefore be more stressed than cows with two to four farm mates. The purpose of our study was to further examine the effects of social buffering. We compared behavioural and cardiac responses to emotional stimuli (strange object, loud sound, and mesh-covered food) among familiar and unfamiliar heifers in groups of two or five individuals.
2. Materials and methods 2.1. Animals and housing The heifers were divided into four experimental groups of two and five individuals (Table 1). Each group was reared separately in a deep-litter pen for 6 months with a space allowance of 3.4 m2 per animal. The pens were separated from each other by solid plywood partitions, which restricted visual and tactile contact between members of neighbouring groups. The heifers were allowed ad libitum access to grass silage, and were fed corn silage and a formulated ration according to the Japanese Feeding Standard for Beef Cattle (1995). Affiliative behaviour, such as allogrooming and contact, was observed among all individuals within each group. Before the study, we confirmed that the affiliative relationships in each of the four experimental groups were equally established among pen mates.
K. Takeda et al. / Applied Animal Behaviour Science 82 (2003) 1–11
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Table 1 Experimental groups Mean age (months)a
Mean body weight (kg)a
Group of two Group A Group B
6.0 15.5
117.0 224.5
Group of five Group C Group D
6.0 14.6
121.4 198.2
a
At the time of grouping.
We used four Holstein heifers aged 17.7 months as the unfamiliar animals. The Japanese Black heifers and the Holstein heifers had not seen each other prior to the experiment. 2.2. Setting up two groups: familiar and unfamiliar The familiar groups consisted of two sizes: F2 and F5. In F2, both heifers in Groups A and B were observed individually in a group of two (shown in the Table 1). In F5, two heifers each from Groups C and D were selected randomly and were observed individually in a group of five (Table 1, Fig. 1). The unfamiliar groups also consisted of two sizes: UF2 and UF5. In UF2, each of the two heifers not used as part of F5 in Groups C and D were observed as one of a group of two with one Holstein heifer. In UF5, one of the heifers not used in F5 and UF2 in Groups C and D was grouped with the four Holstein heifers. Each group was transported about 800 m by truck from the cattle shed to the experimental station and temporarily tethered individually in a corral adjacent to the station. A heart-rate monitor (Polar1 Accurex Plus) was attached to the chest of each focal animal and covered by a girth belt. Areas of electrode attachment on the focal animals were shaved and cleaned with alcohol just before attaching the monitors. The focal animals were left in the corral for approximately 1 h to minimise the effects of transportation. The heart rates of the test animals were confirmed to be stable before the test, and were recorded at 5 s intervals until the end of the test. To begin the test, groups of familiar (Japanese Black) and unfamiliar (Holstein) heifers were led into the test room (5:5 m 10:0 m), which was constructed with 2 m high wooden panels and had two doors (Fig. 2). There were five single stalls (1:0 m 1:5 m) in two rows facing each other. Two or five animals were tethered individually in the stalls, in which one or two focal animals were monitored by two video cameras. 2.3. Three stress tests We designed three stress tests: a novelty test (encountering a strange object), a surprise test (hearing a loud sound), and a conflict test (mesh-covered food). First, the focal animal was left tethered for 5 min in the stall to allow it to settle down. Next, a strange object
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Fig. 1. Setting up familiar and unfamiliar.
K. Takeda et al. / Applied Animal Behaviour Science 82 (2003) 1–11
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Fig. 2. Diagram of the experimental room for the novelty test, the surprise test, and conflict test. The experimental heifers could see each other and were accustomed to the experimental room.
(a red paper doll) was placed diagonally in front of the focal animal and left for 10 min (the novelty test). Two minutes after the strange object was removed, a tin bucket containing several weights was suddenly dropped from the ceiling (5 m high) diagonally in front of the focal animal (the surprise test). As soon as the bucket hit the ground, it was lifted back up to the ceiling. Three minutes later, a feed bin containing a formulated diet covered with wire mesh was placed in front of each animal for 10 min. The focal animals could not feed, although they could see and smell the food (the conflict test). This series of tests was carried out in the order: UF5, UF2, F5, and F2. The behavioural reactions of the focal animals during the experiment were recorded by video camera. The following reactions were recorded: (a) the number of steps with the right foreleg; (b) the number of investigative behaviours (sniffing and licking the strange object, own stall, or own food bin); and (c) the total time spent attempting to escape, especially in the novelty and surprise tests. In this study, an attempt to escape was defined as the focal animal pulling on the tether such that the rope became taut.
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2.4. Statistical analyses Statistical analyses were carried out with the StatView1 statistical package (SAS Institute Inc.). Since the behavioural data were not normally distributed, a square-root transformation was used after adding 0.5 (Martin and Bateson, 1986). The effects on behaviour and mean heart rate of familiarity (familiar versus unfamiliar) and group size (two versus five) were analysed using a two-way analysis of variance (ANOVA).
3. Results The behavioural responses to the three emotional stressors are presented in Table 2. There was a significant effect of familiarity on time spent attempting to escape during the novelty test (F1;10 ¼ 6:8; P < 0:05). The mean values of other behavioural categories were lower in the familiar groups than in the unfamiliar groups, although these differences were not significant. During the surprise test, the frequency of stepping tended to be lower in F5 than in the other groups (F1;10 ¼ 3:1; P ¼ 0:1). The frequency of stepping during the conflict test was lowest for F5, and there was a significant effect of familiarity (F1;10 ¼ 5:4; P < 0:05). The mean heart rate prior to the test was not statistically different among groups in each situation (74.4 (F2), 70.1 (UF2), 70.4 (F5) and 67.8 (UF5), respectively).
Table 2 Behavioural responses of heifers in four types of groups during three emotional stress tests No. of stepsa
No. of sniffs
Time spent attempting to escape (s)
Novelty test F2b UF2 F5 UF5
4.5 20.0 0.8 21.7
5.3 34.6 1.0 26.8
1.5 3.3 0.0 1.3
2.0 2.9 0.0 1.2
12.7 254.7 4.0 180.0
22.9* 310.1* 8.0* 170.5*
Surprise test F2 UF2 F5 UF5
12.5 3.7 1.3 3.6
12.0** 4.6** 1.0** 2.1**
1.3 0.0 0.0 0.3
2.5 0.0 0.0 0.6
52.3 110.0 68.5 74.3
44.4 88.2 80.3 92.4
Conflict test F2 UF2 F5 UF5
3.0 6.0 1.8 9.3
2.4* 3.0* 1.7* 7.6*
4.8 1.7 5.8 7.3
5.0 2.9 8.5 4.5
Data are presented as mean S:D. a Steps with right foreleg. b Familiar 2 denotes a group of two heifers that were familiar with each other. * P < 0:05 (effect of familiarity). ** P ¼ 0:10 (interaction of familiarity and group size).
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Fifteen seconds after presenting the strange object, the heart rates of the focal animals in F2, UF2, F5, and UF5 increased from 72.7 to 86.4, 74.1 to 81.0, 62.0 to 67.5, and 88.9 to 89.0 bpm, respectively (Fig. 3a). This corresponded to rate increases of 120, 110, 110 and 101%, respectively, but these differences were not significant. The mean heart rates in both the first and the second halves (in bpm) in the novelty test were 66.1 (F2), 74.9 (UF2), 63.4 (F5), 80.3 (UF5), and 66.4 (F2), 68.5 (UF2), 59.7 (F5), 71.3 (UF5), respectively (Table 3). Thus, the heart rate was lowest in F5 although there were no significant effects of
Fig. 3. (a) Cardiac responses of focal heifers in various social groups to an encounter with a strange object (the novelty test). (b) Cardiac responses of focal heifers in various social groups to dropping a tinplate bucket (the surprise test). (c) Cardiac responses of focal heifers in various social groups to hiding food (the conflict test).
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Fig. 3. (Continued ).
familiarity, group size and the interaction of familiarity and group size on mean heart rate during the test. There was an erratic heart rate of the UF2 that occurred around 8 min into the 10 min test during the novelty test, despite the fact that the room was kept very quiet. In the surprise test (Fig. 3b), heart rates (in bpm) increased from 62.8 to 90.0 (F2), 68.6 to 87.8 (UF2), 60.0 to 72.2 (F5), and 79.8 to 82.0 (UF5), immediately after the bucket was dropped. This corresponded to heart rate increases of 43, 28, 20, and 3%; however, these differences were not significant. During the second half of the surprise test, mean heart rates were 68.2 (F2), 69.5 (UF2), 60.1 (F5), and 78.4 (UF5). Again, the heart rate was lowest in F5 (Table 3). There was a significant effect of familiarity (F1;10 ¼ 8:6, P < 0:05), Table 3 Effects of familiarity and group size on mean heart rates (bpm) of heifers in four types of groups during three emotional stress tests Experimental groups
Novelty test The first 5 min The latter 5 min
Effects
F2
UF2
F5
UF5
67.9 5.9 64.4 6.6
71.2 9.5 68.5 9.8
61.8 10.0 73.1 9.9 59.7 9.0 71.3 6.6
Familiarity Group sizes
Interaction
NS NS
NS NS
NS NS
NS P < 0.05
NS NS
NS P < 0.05
Surprise test
The first 1.5 min The latter 1.5 min Conflict test The first 5 min The latter 5 min
77.6 12.8 80.3 20.5 66.8 8.7 68.2 7.2 69.5 4.1 60.1 7.0 64.8 6.9 62.1 5.5
68.4 4.3 65.4 3.8
82.2 9.2 78.4 5.1
63.3 7.0 82.8 7.2 P < 0.01 62.7 11.7 73.5 10.0 NS
P ¼ 0.10 P < 0.05 NS NS
Mean S:D: F2: familiar 2; UF2: unfamiliar 2; F5: familiar 5; UF5: unfamiliar 5 (see Fig. 1).
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and of the interaction between familiarity and group size (F1;10 ¼ 6:4, P < 0:05) on mean heart rate in the latter 1.5 min of the surprise test. The mean heart rates (in bpm) in the first 5 min during the conflict test (Fig. 3c and Table 3) were 64.8 (F2), 68.4 (UF2), 63.3 (F5), and 82.8 (UF5). Again, F5 had the lowest and UF5 the highest values. In the first half of the test, the effects of familiarity (F1;10 ¼ 10:5, P < 0:01) and the interaction between familiarity and group size (F1;10 ¼ 5:1, P < 0:05) of heart rate were significant.
4. Discussion Familiarity and group size had an effect on behavioural responses under some circumstances. Arnone and Dantzer (1980) found that the presence of a conspecific, with whom a social bond had been established, played a protective role against the behavioural and physiological consequences of frustration. However, Taylor (1981) reported that when rats were exposed to a stressful noise (surprise stimulus), the duration of freezing did not differ between familiar and unfamiliar groups. Gunnar et al. (1980) found that unfamiliar conspecifics were just as effective as familiar animals in reducing behavioural responses. Our results suggest that the surprise test and the conflict test had strong emotional effects on the heifers, based on their increased number of steps and heart rates. Heart-rate means for both halves of the novelty test showed that effect of the strange object was weak. However, there were differences in time spent attempting to escape during the test. Heart rate may not have differed in the first half of the surprise test because the stimulus of dropping the bucket was too strong. The lower heart rate in F5 animals during the second half of the test may have been due to a calming effect. Similarly, the conflict associated with the presence of food pellets was greater during the first 5 min than during the second half of the test. The stress stimuli for conflict might have been effective only for the first several minutes. In his review, Epley (1974) suggested that the presence of conspecifics did not suppress behavioural responses to aversive stimuli. On the other hand, Boissy and Le Neindre (1997) found that the introduction of a pen mate caused a more pronounced decline in the heart rate of an isolated heifer, although behavioural responses were not affected by familiarity. In our study, familiarity had a calming effect during the surprise and the conflict tests. In addition, there was a significant interaction between familiarity and group size. Of the four group treatments in the emotional stress challenge, the calming effect was greatest when five heifers, which were familiar with each other, were together. Coe et al. (1982) suggested that the influence of the social milieu on stress responsiveness might be dependent on group size, environmental familiarity, and the severity of the stressor. Stanton et al. (1985) confirmed this. It is clear from other studies that the sight of familiar conspecifics (not merely conspecifics) suppresses the cardiac responses of cattle to an emotional stress. This may explain one of our previous results (Takeda et al., 2000), in which cows that had only one farm mate present were more stressed than cows that had two to four farm mates in a communal pasture. In wild animals, one of the most important adaptive values of living in a group may be increased protection from predators and the increased likelihood of finding and acquiring food (Krebs and Davies, 1995), as well as the
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buffering effect to environmental pressures (Wilson, 1975). In our study, the mean heart rate of the familiar group of five was lower than that of the familiar group of two. When cattle experience multiple stressful stimuli, being with familiar animals could buffer the cardiac response, which may be an adaptive value of herding. The presence of social companions or the image of a conspecific has been found to reduce stress responses in cattle (Boissy and Le Neindre, 1990, 1997; Veissier and Le Neindre, 1992), sheep (Parrott et al., 1988; Vandenheede and Bouissou, 1994), pigs (Arnone and Dantzer, 1980), and alpacas (Pollard and Littlejohn, 1995). Sato and Yoshikawa (1996) quantified the recognition pattern of Japanese Black cows using degree of visual attention, and found that cows paid more attention to a familiar cow (a pen mate) than to unfamiliar cows, irrespective of breed. In conclusion, for cattle, the calming effect of affiliative groups of five may be higher than groups of two.
Acknowledgements We thank the staff of the Tohoku University Experimental Farm for providing heifers and facilities. We are also grateful to Mr. Yasuhiro Yashima, Ms. Chiaki Kato, Mr. Ryuji Tajima, and Mr. Daisuke Kohari for helping in our experiments.
References Arnone, M., Dantzer, R., 1980. Does frustration induce aggression in pigs? Appl. Anim. Ethol. 6, 351–362. Baldock, N.M., Sibly, R.M., 1990. Effects of handling and transportation on the heart rate and behaviour of sheep. Appl. Anim. Behav. Sci. 28, 15–39. Boissy, A., Le Neindre, P., 1990. Social influences on the reactivity of heifers: implications for learning abilities in operant conditioning. Appl. Anim. Behav. Sci. 25, 149–165. Boissy, A., Le Neindre, P., 1997. Behavioral, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiol. Behav. 61 (5), 693–699. Coe, C.L., Franklin, D., Smith, E.R., Levine, S., 1982. Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol. Behav. 29, 1051–1057. Deguchi, E., 1998. Relationship between behavior and plasma cortisol concentration during grouping of unfamiliar piglets. Anim. Sci. Technol. (Jpn.) 69 (4), 376–380 (in Japanese with English abstract). Epley, S.W., 1974. Reduction of the behavioral effects of aversive stimulation by the presence of companions. Psychol. Bull. 81 (5), 271–283. Gunnar, M.R., Gonzalez, C.A., Levine, S., 1980. The role of pairs in modifying behavioral distress and pituitary–adrenal responses to a novel environment in year-old rhesus monkey. Physiol. Behav. 25, 795–798. Japanese Feeding Standard for Beef Cattle, 1995. Agriculture, Forestry and Fisheries Research Council Secretariat, MAFF. Central Association of Livestock Industry, Tokyo, pp. 16–20 (in Japanese). Kenny, F.J., Tarrant, P.V., 1987. The reaction of young bulls to short-haul road transport. Appl. Anim. Behav. Sci. 17, 209–227. Kondo, S., Hurnik, J.F., 1988. Behavioral and physiological responses to spatial novelty in dairy cows. Can. J. Anim. Sci. 68, 339–343. Kondo, S., Kawakami, N., Kohama, H., Nishino, S., 1984. Changes in activity, spatial pattern and social behavior in calves after grouping. Appl. Anim. Ethol. 11, 217–228. Krebs, J.R., Davies, N.D., 1995. An Introduction to Behavioural Ecology, third ed. Blackwell Scientific Publications, Oxford, pp. 120–146. Martin, P., Bateson, P., 1986. Measuring Behaviour. Cambridge University Press, London, pp. 135–136.
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Oshio, S., Tahara, I., Kobayashi, H., 1985. Studies on the method of adaptation to a grazing environment IV. Changes of the some properties in the rumen and energy balance of heifers and steers in the early period of grazing. Bull. Natl. Grassl. Res. Inst. 32, 34–47 (in Japanese with English abstract). Parrott, R.F., Houpt, K.A., Misson, B.H., 1988. Modification of the responses of sheep to isolation stress by the use of mirror panels. Appl. Anim. Behav. Sci. 19, 331–338. Pollard, J.C., Littlejohn, R.P., 1995. Effects of isolation and restraint on heart rate and behaviour of alpacas. Appl. Anim. Behav. Sci. 45, 165–174. Rushen, J., 1987. A difference in weight reduces fighting when unacquainted newly weaned pigs first meet. Can. J. Anim. Sci. 67, 951–960. Sato, S., Yoshikawa, C., 1996. Estimation of cognition pattern of cattle by the visual attention to photographs and movie images. Anim. Sci. Technol. (Jpn.) 67 (1), 36–42. Stanton, M.E., Patterson, J.M., Levine, S., 1985. Social influences on conditioned cortisol secretion in the squirrel monkey. Psychoneuroendocrinology 10 (2), 125–134. Takeda, K., Sato, S., Sugawara, K., 2000. The number of farm mates influences social and maintenance behaviours of Japanese Black cows in a communal pasture. Appl. Anim. Behav. Sci. 67, 181–192. Taylor, G.T., 1981. Fear and affiliation in domesticated male rats. J. Comp. Physiol. Psychol. 95, 685–693. Vandenheede, M., Bouissou, M.F., 1994. Fear reactions of ewes to photographic images. Behav. Process. 32, 17– 28. Veissier, I., Le Neindre, P., 1992. Reactivity of Aubrac heifers exposed to a novel environment alone or in groups of four. Appl. Anim. Behav. Sci. 33, 11–15. Veissier, I., Le Neindre, P., Trillat, G., 1989. The use of circardian behaviour to measure adaptation of calves to changes in their environment. Appl. Anim. Behav. Sci. 22, 1–12. Wilson, E.O., 1975. Sociobiology: The New Synthesis. Belknap Press of Harvard University Press, Cambridge.
Familiarity and group size affect emotional stress in Japanese Black heifers Ken-ichi Takeda*, Shusuke Sato, Kazuo Sugawara Graduate School of Agricultural Science, Tohoku University, Kawatabi, Narugo, Miyagi 989-6711, Japan Accepted 26 January 2003
Abstract We compared behavioural and cardiac responses to emotional stresses between familiar and unfamiliar heifers in groups of two or five. Fourteen Japanese Black heifers were divided into two experimental groups of two individuals (F2) and two groups of five individuals (F5) that were familiar with each other. Four additional Holstein heifers were used in forming the unfamiliar groups (UF2 and UF5), in which the focal animals had never been seen. Experimental animals were equipped with heart-rate monitors and led into a test room (5:5 m 10:0 m) at the experimental station. Each animal was tethered inside a single stall, and the focal animals were monitored by two video cameras. We designed three stress tests for the heifers: (1) a novelty test (encountering a strange object); (2) a surprise test (hearing a loud sound); and (3) a conflict test (trying to eat formula food). In the first test, a red paper doll was presented to the focal animal for 10 min. In the second test, a tin bucket containing several weights was dropped from the ceiling (5 m high) diagonally in front of the focal animal. Three minutes later, the third test was conducted by placing a feed bin containing food pellets covered with wire mesh in front of each animal for 10 min. This series of tests was carried out in the order UF5, UF2, F5, and F2. There were the significant effects of familiarity on behavioural responses in the novelty and conflict test. Moreover, there were not only significant effects of familiarity but also a significant interaction between familiarity and group size on cardiac responses in the surprise and conflict tests. Especially, changes in the mean heart rate during the two tests were minimal in the group F5. Our results indicate that both familiarity and larger group size may reduce emotional stress, and the calming effect of affiliative groups of five may be higher than groups of two for cattle. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Cattle; Social behaviour; Novelty; Surprise; Conflict
* Corresponding author. Present address: Faculty of Agriculture, Shinshu University, 8304 Minami-minowa, Kami-ina, Nagano 399-4598, Japan. Tel.: þ81-265-77-1427; fax: þ81-265-77-1427. E-mail address: [email protected] (K. Takeda).
0168-1591/03/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0168-1591(03)00039-X
2
K. Takeda et al. / Applied Animal Behaviour Science 82 (2003) 1–11
1. Introduction Communal pastures in which cattle are turned out together from a number of farms are very common in Japan. A major concern with communal pasturing is that the body weights of some animals drop during the initial grazing period. A change of the rearing environment can alter the circadian rhythm (Kondo et al., 1984; Oshio et al., 1985; Veissier et al., 1989) and increase the mean heart rate (Kondo and Hurnik, 1988) in cattle, and it can increase the serum cortisol concentration in pigs (Deguchi, 1998). Moreover, being with unfamiliar animals can increase the heart rate and change the behaviour of sheep (Baldock and Sibly, 1990) and cattle (Kenny and Tarrant, 1987), and animals have been shown to lose weight when associating with unfamiliar individuals (Rushen, 1987). Therefore, environmental and social stressors specific to communal pastures may be responsible for the weight loss of cows and heifers under such circumstances. On the other hand, familiar conspecifics can lower the stress responses of subjects (Arnone and Dantzer, 1980; Gunnar et al., 1980; Coe et al., 1982; Boissy and Le Neindre, 1990; Veissier and Le Neindre, 1992). Coe et al. (1982) found that when individual squirrel monkeys observed snakes, their plasma cortisol concentrations were higher than when they were tested in the presence of a cage mate. The authors suggested that this difference depended on the nature and number of conspecifics that were present. Stanton et al. (1985) taught squirrel monkeys to respond to incandescent light as a conditioned stimulus to electric shock (unconditioned stimulus), and showed that their plasma cortisol concentrations increased when they were tested individually or in pairs, but not when they were in a group of six animals. Takeda et al. (2000) found that those cows with two to four familiar farm mates were behaviourally more socially stable than cows with only one or no farm mates in a communal pasture. Cows with only one farm mate may therefore be more stressed than cows with two to four farm mates. The purpose of our study was to further examine the effects of social buffering. We compared behavioural and cardiac responses to emotional stimuli (strange object, loud sound, and mesh-covered food) among familiar and unfamiliar heifers in groups of two or five individuals.
2. Materials and methods 2.1. Animals and housing The heifers were divided into four experimental groups of two and five individuals (Table 1). Each group was reared separately in a deep-litter pen for 6 months with a space allowance of 3.4 m2 per animal. The pens were separated from each other by solid plywood partitions, which restricted visual and tactile contact between members of neighbouring groups. The heifers were allowed ad libitum access to grass silage, and were fed corn silage and a formulated ration according to the Japanese Feeding Standard for Beef Cattle (1995). Affiliative behaviour, such as allogrooming and contact, was observed among all individuals within each group. Before the study, we confirmed that the affiliative relationships in each of the four experimental groups were equally established among pen mates.
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Table 1 Experimental groups Mean age (months)a
Mean body weight (kg)a
Group of two Group A Group B
6.0 15.5
117.0 224.5
Group of five Group C Group D
6.0 14.6
121.4 198.2
a
At the time of grouping.
We used four Holstein heifers aged 17.7 months as the unfamiliar animals. The Japanese Black heifers and the Holstein heifers had not seen each other prior to the experiment. 2.2. Setting up two groups: familiar and unfamiliar The familiar groups consisted of two sizes: F2 and F5. In F2, both heifers in Groups A and B were observed individually in a group of two (shown in the Table 1). In F5, two heifers each from Groups C and D were selected randomly and were observed individually in a group of five (Table 1, Fig. 1). The unfamiliar groups also consisted of two sizes: UF2 and UF5. In UF2, each of the two heifers not used as part of F5 in Groups C and D were observed as one of a group of two with one Holstein heifer. In UF5, one of the heifers not used in F5 and UF2 in Groups C and D was grouped with the four Holstein heifers. Each group was transported about 800 m by truck from the cattle shed to the experimental station and temporarily tethered individually in a corral adjacent to the station. A heart-rate monitor (Polar1 Accurex Plus) was attached to the chest of each focal animal and covered by a girth belt. Areas of electrode attachment on the focal animals were shaved and cleaned with alcohol just before attaching the monitors. The focal animals were left in the corral for approximately 1 h to minimise the effects of transportation. The heart rates of the test animals were confirmed to be stable before the test, and were recorded at 5 s intervals until the end of the test. To begin the test, groups of familiar (Japanese Black) and unfamiliar (Holstein) heifers were led into the test room (5:5 m 10:0 m), which was constructed with 2 m high wooden panels and had two doors (Fig. 2). There were five single stalls (1:0 m 1:5 m) in two rows facing each other. Two or five animals were tethered individually in the stalls, in which one or two focal animals were monitored by two video cameras. 2.3. Three stress tests We designed three stress tests: a novelty test (encountering a strange object), a surprise test (hearing a loud sound), and a conflict test (mesh-covered food). First, the focal animal was left tethered for 5 min in the stall to allow it to settle down. Next, a strange object
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Fig. 1. Setting up familiar and unfamiliar.
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Fig. 2. Diagram of the experimental room for the novelty test, the surprise test, and conflict test. The experimental heifers could see each other and were accustomed to the experimental room.
(a red paper doll) was placed diagonally in front of the focal animal and left for 10 min (the novelty test). Two minutes after the strange object was removed, a tin bucket containing several weights was suddenly dropped from the ceiling (5 m high) diagonally in front of the focal animal (the surprise test). As soon as the bucket hit the ground, it was lifted back up to the ceiling. Three minutes later, a feed bin containing a formulated diet covered with wire mesh was placed in front of each animal for 10 min. The focal animals could not feed, although they could see and smell the food (the conflict test). This series of tests was carried out in the order: UF5, UF2, F5, and F2. The behavioural reactions of the focal animals during the experiment were recorded by video camera. The following reactions were recorded: (a) the number of steps with the right foreleg; (b) the number of investigative behaviours (sniffing and licking the strange object, own stall, or own food bin); and (c) the total time spent attempting to escape, especially in the novelty and surprise tests. In this study, an attempt to escape was defined as the focal animal pulling on the tether such that the rope became taut.
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2.4. Statistical analyses Statistical analyses were carried out with the StatView1 statistical package (SAS Institute Inc.). Since the behavioural data were not normally distributed, a square-root transformation was used after adding 0.5 (Martin and Bateson, 1986). The effects on behaviour and mean heart rate of familiarity (familiar versus unfamiliar) and group size (two versus five) were analysed using a two-way analysis of variance (ANOVA).
3. Results The behavioural responses to the three emotional stressors are presented in Table 2. There was a significant effect of familiarity on time spent attempting to escape during the novelty test (F1;10 ¼ 6:8; P < 0:05). The mean values of other behavioural categories were lower in the familiar groups than in the unfamiliar groups, although these differences were not significant. During the surprise test, the frequency of stepping tended to be lower in F5 than in the other groups (F1;10 ¼ 3:1; P ¼ 0:1). The frequency of stepping during the conflict test was lowest for F5, and there was a significant effect of familiarity (F1;10 ¼ 5:4; P < 0:05). The mean heart rate prior to the test was not statistically different among groups in each situation (74.4 (F2), 70.1 (UF2), 70.4 (F5) and 67.8 (UF5), respectively).
Table 2 Behavioural responses of heifers in four types of groups during three emotional stress tests No. of stepsa
No. of sniffs
Time spent attempting to escape (s)
Novelty test F2b UF2 F5 UF5
4.5 20.0 0.8 21.7
5.3 34.6 1.0 26.8
1.5 3.3 0.0 1.3
2.0 2.9 0.0 1.2
12.7 254.7 4.0 180.0
22.9* 310.1* 8.0* 170.5*
Surprise test F2 UF2 F5 UF5
12.5 3.7 1.3 3.6
12.0** 4.6** 1.0** 2.1**
1.3 0.0 0.0 0.3
2.5 0.0 0.0 0.6
52.3 110.0 68.5 74.3
44.4 88.2 80.3 92.4
Conflict test F2 UF2 F5 UF5
3.0 6.0 1.8 9.3
2.4* 3.0* 1.7* 7.6*
4.8 1.7 5.8 7.3
5.0 2.9 8.5 4.5
Data are presented as mean S:D. a Steps with right foreleg. b Familiar 2 denotes a group of two heifers that were familiar with each other. * P < 0:05 (effect of familiarity). ** P ¼ 0:10 (interaction of familiarity and group size).
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Fifteen seconds after presenting the strange object, the heart rates of the focal animals in F2, UF2, F5, and UF5 increased from 72.7 to 86.4, 74.1 to 81.0, 62.0 to 67.5, and 88.9 to 89.0 bpm, respectively (Fig. 3a). This corresponded to rate increases of 120, 110, 110 and 101%, respectively, but these differences were not significant. The mean heart rates in both the first and the second halves (in bpm) in the novelty test were 66.1 (F2), 74.9 (UF2), 63.4 (F5), 80.3 (UF5), and 66.4 (F2), 68.5 (UF2), 59.7 (F5), 71.3 (UF5), respectively (Table 3). Thus, the heart rate was lowest in F5 although there were no significant effects of
Fig. 3. (a) Cardiac responses of focal heifers in various social groups to an encounter with a strange object (the novelty test). (b) Cardiac responses of focal heifers in various social groups to dropping a tinplate bucket (the surprise test). (c) Cardiac responses of focal heifers in various social groups to hiding food (the conflict test).
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Fig. 3. (Continued ).
familiarity, group size and the interaction of familiarity and group size on mean heart rate during the test. There was an erratic heart rate of the UF2 that occurred around 8 min into the 10 min test during the novelty test, despite the fact that the room was kept very quiet. In the surprise test (Fig. 3b), heart rates (in bpm) increased from 62.8 to 90.0 (F2), 68.6 to 87.8 (UF2), 60.0 to 72.2 (F5), and 79.8 to 82.0 (UF5), immediately after the bucket was dropped. This corresponded to heart rate increases of 43, 28, 20, and 3%; however, these differences were not significant. During the second half of the surprise test, mean heart rates were 68.2 (F2), 69.5 (UF2), 60.1 (F5), and 78.4 (UF5). Again, the heart rate was lowest in F5 (Table 3). There was a significant effect of familiarity (F1;10 ¼ 8:6, P < 0:05), Table 3 Effects of familiarity and group size on mean heart rates (bpm) of heifers in four types of groups during three emotional stress tests Experimental groups
Novelty test The first 5 min The latter 5 min
Effects
F2
UF2
F5
UF5
67.9 5.9 64.4 6.6
71.2 9.5 68.5 9.8
61.8 10.0 73.1 9.9 59.7 9.0 71.3 6.6
Familiarity Group sizes
Interaction
NS NS
NS NS
NS NS
NS P < 0.05
NS NS
NS P < 0.05
Surprise test
The first 1.5 min The latter 1.5 min Conflict test The first 5 min The latter 5 min
77.6 12.8 80.3 20.5 66.8 8.7 68.2 7.2 69.5 4.1 60.1 7.0 64.8 6.9 62.1 5.5
68.4 4.3 65.4 3.8
82.2 9.2 78.4 5.1
63.3 7.0 82.8 7.2 P < 0.01 62.7 11.7 73.5 10.0 NS
P ¼ 0.10 P < 0.05 NS NS
Mean S:D: F2: familiar 2; UF2: unfamiliar 2; F5: familiar 5; UF5: unfamiliar 5 (see Fig. 1).
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and of the interaction between familiarity and group size (F1;10 ¼ 6:4, P < 0:05) on mean heart rate in the latter 1.5 min of the surprise test. The mean heart rates (in bpm) in the first 5 min during the conflict test (Fig. 3c and Table 3) were 64.8 (F2), 68.4 (UF2), 63.3 (F5), and 82.8 (UF5). Again, F5 had the lowest and UF5 the highest values. In the first half of the test, the effects of familiarity (F1;10 ¼ 10:5, P < 0:01) and the interaction between familiarity and group size (F1;10 ¼ 5:1, P < 0:05) of heart rate were significant.
4. Discussion Familiarity and group size had an effect on behavioural responses under some circumstances. Arnone and Dantzer (1980) found that the presence of a conspecific, with whom a social bond had been established, played a protective role against the behavioural and physiological consequences of frustration. However, Taylor (1981) reported that when rats were exposed to a stressful noise (surprise stimulus), the duration of freezing did not differ between familiar and unfamiliar groups. Gunnar et al. (1980) found that unfamiliar conspecifics were just as effective as familiar animals in reducing behavioural responses. Our results suggest that the surprise test and the conflict test had strong emotional effects on the heifers, based on their increased number of steps and heart rates. Heart-rate means for both halves of the novelty test showed that effect of the strange object was weak. However, there were differences in time spent attempting to escape during the test. Heart rate may not have differed in the first half of the surprise test because the stimulus of dropping the bucket was too strong. The lower heart rate in F5 animals during the second half of the test may have been due to a calming effect. Similarly, the conflict associated with the presence of food pellets was greater during the first 5 min than during the second half of the test. The stress stimuli for conflict might have been effective only for the first several minutes. In his review, Epley (1974) suggested that the presence of conspecifics did not suppress behavioural responses to aversive stimuli. On the other hand, Boissy and Le Neindre (1997) found that the introduction of a pen mate caused a more pronounced decline in the heart rate of an isolated heifer, although behavioural responses were not affected by familiarity. In our study, familiarity had a calming effect during the surprise and the conflict tests. In addition, there was a significant interaction between familiarity and group size. Of the four group treatments in the emotional stress challenge, the calming effect was greatest when five heifers, which were familiar with each other, were together. Coe et al. (1982) suggested that the influence of the social milieu on stress responsiveness might be dependent on group size, environmental familiarity, and the severity of the stressor. Stanton et al. (1985) confirmed this. It is clear from other studies that the sight of familiar conspecifics (not merely conspecifics) suppresses the cardiac responses of cattle to an emotional stress. This may explain one of our previous results (Takeda et al., 2000), in which cows that had only one farm mate present were more stressed than cows that had two to four farm mates in a communal pasture. In wild animals, one of the most important adaptive values of living in a group may be increased protection from predators and the increased likelihood of finding and acquiring food (Krebs and Davies, 1995), as well as the
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buffering effect to environmental pressures (Wilson, 1975). In our study, the mean heart rate of the familiar group of five was lower than that of the familiar group of two. When cattle experience multiple stressful stimuli, being with familiar animals could buffer the cardiac response, which may be an adaptive value of herding. The presence of social companions or the image of a conspecific has been found to reduce stress responses in cattle (Boissy and Le Neindre, 1990, 1997; Veissier and Le Neindre, 1992), sheep (Parrott et al., 1988; Vandenheede and Bouissou, 1994), pigs (Arnone and Dantzer, 1980), and alpacas (Pollard and Littlejohn, 1995). Sato and Yoshikawa (1996) quantified the recognition pattern of Japanese Black cows using degree of visual attention, and found that cows paid more attention to a familiar cow (a pen mate) than to unfamiliar cows, irrespective of breed. In conclusion, for cattle, the calming effect of affiliative groups of five may be higher than groups of two.
Acknowledgements We thank the staff of the Tohoku University Experimental Farm for providing heifers and facilities. We are also grateful to Mr. Yasuhiro Yashima, Ms. Chiaki Kato, Mr. Ryuji Tajima, and Mr. Daisuke Kohari for helping in our experiments.
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