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Social licking patterns in cattle (Bos taurus): influence of environmental and social factors
Applied Animal Behaviour Science, 32 ( 1991 ) 3-12
3
Elsevier Science Publishers B.V., A m s t e r d a m
Social licking patterns in cattle (Bos taurus)" influence of environmental and social factors S. Sato, S. Sako and A. Maeda Faculty qf.-lgriculture, Mivazaki University Mivazaki-shi 889-2l Japan (Accepted 8 March 1991 )
ABSTRACT Sato, S., Sako, S. and Maeda, A., 1991. Social licking patterns in cattle (Bos taurus): influence of environmental and social factors. Appl. ,4him. Behav. Sci., 32:3-12. To investigate the functions of social licking in cattle, four calves (one heifer and one steer in each of two herds), known to exhibit frequent social licking were observed continuously for 2 h before sunset for 13 days, using the focal animal sampling method. Calves were observed under various cnvironrnental conditions. Social licking significantly decreased on rainy days and tended to increase in a dirty barn and when food was restricted. Solicitation for social licking occurred not only from dominant animals of pairs but also from subordinates. Of the licking interactions, 31% occurred following solicitation, and these accounted for 39% of the total time spent licking. Following solicitation, 78% of social licking was oriented to the head and the neck regions that were inaccessible to selflicking animals. Unsolicited licking, however, was oriented not only to the head and the neck but also to the back and the rump regions, and these two latter regions were the major ones to receive licking. The effect of social relationships on social licking was investigated using least-squares analysis of variance. Social factors investigated were the difference of dominance values, the dominancc-subordinance relationship, and kinship and familiarity: the sex of calves involved was also considered. Only familiarity had a significant effect on licking: exchanges of social licking increased with length of cohabitation. We suggest Ihat social licking may have a cleaning effect, a tension-reducing effect and a bonding effect.
INTRODUCTION
Various kinds of animals from rodents to primates exhibit social grooming as a non-aggressive behaviour. There have been many studies on social grooming in primates, as primates frequently groom socially. These suggest cleaning and eating functions based on grooming site preferences (Hutchins and Barash, 1976; Barton, 1985) and removal of dirt or ectoparasites (Simonds, 1965), social bonding functions (Stammbach and Kummer, 1982; O'Keeffe et al., 1982/1983 ) and tension-reducing functions based on grooming methods (Boccia, 1983 ), physiological changes (Boccia et al., 1989 ), biochemical changes (Panksepp et al., 1980; Keverne et al., 1989) and behavioural changes (Schino et al., 1988 ). 0168-1591/91/$03.50
© 1991 Elsevier Science Publishers B.V. All rights reserved.
4
s. SATO ET AL
On the other hand, little has been published on social grooming in cattle, though Brownlee (1950) recognized social grooming as one of the most important behaviours in cattle. Hafez et al. (1969) suggested that the cleaning and eating functions also occur in cattle and Rich ( 1973 ) confirmed this hypothesis with evidence that cows removed some ticks from their calves by maternal licking. Sambraus ( 1969 ) suggested another function in addition to cleaning and eating, from anecdotal evidence that social licking occurred frequently after disturbance and that bulls licked oestrous cows more frequently than anoestrous cows. Wood (1977) found a positive relationship between the time spent receiving licking and milk production. Sato (1984) found a positive relationship between the time spent receiving licking and liveweight gain. Wood and Sato both suggested that these physical effects were due to a reduction in tension: a calming effect of the social grooming. In addition, Fraser and Broom (1990) considered that it is likely that social licking has effects on the psychological stability of the animals concerned as well as cleaning skin and hair. The above studies, however, have been insufficient to confirm the cleaning, eating and tension-reducing functions, and the social bonding hypothesis has not been investigated at all. In this study, the nature of social licking and the influence of social factors on social licking in cattle were investigated to obtain evidence for the importance of the various functions discussed above.
ANIMALS, MATERIALS AND METHODS
A steer and a heifer were selected as focal animals from each of two rearing Holstein herds. Preliminary observation indicated that social licking was particularly frequent during the 2 h before sunset. Consequently, the two animals in each herd were individually observed during this period for 13 days under various environmental conditions. Observations were made using two video recording systems, one for each animal.
Experimental animals The first herd consisted of seven steers and six heifers aged from about 12 to about 15 months old. The second herd consisted of seven steers and seven heifers aged from about 11 to about 15 m o n t h s old, eight calves from Herd 1 and six new calves. From the preliminary observations, two calves in Herd 1 were selected as the most frequent performers of social licking and two calves in Herd 2 were selected as the most frequent receivers.
SOCIAL LICKING PATTERNS IN CATTLE
5
The rearing method Calves were reared in a pen measuring 9 m X 13.5 m covered with a half roof. They were fed concentrates ad libitum and silage at 10:00 and 13:30 h. The barn was cleaned every 5 days.
Observation periods Herd 1 was observed for 13 days between the end of July and the end of August. Herd 2 was observed for 13 days between the end of September and the end of October. In order to investigate the cleaning hypothesis, calves were observed under various environmental conditions. The weather conditions were rainy for 5 days and clear for 21 days of observation. The barn was clean for 15 days (had been cleaned on the observation day) and dirty for 11 days (more than 3 days had passed since cleaning). In addition, the effect of restricted feeding was investigated to test Sambraus' (1969) suggestion that social licking occurs after feeding, that is, after the appetitive drive has been fulfilled. Calves were fed twice a day for 18 days and fed only in the morning for 8 days. The influence of various environmental conditions on social licking was investigated using least-squares analysis of variance in 13 × 4 days. A mathematical model was as follows
Yijklm = M+ Wi + Bj+ Fk+ Il+ Eijklm where Yijkhn is the time (s h-~ ) for which each focal animal was involved in social licking in each observation day; M is the total mean; Wi is the effect of the ith weather condition; Bj is the effect of t h e j t h barn condition; Fk is the effect of the/cth feeding condition;//is the effect of the/th focal animal; Eijkhn is a random error specific to this observation.
Analysis of behaviour All occurrences of social licking involving focal animals were recorded during playback of the video tapes. The performers and receivers of solicitation or social licking were identified, durations were recorded and the parts of the body which were licked were noted. The body was divided into nine parts: head, neck, shoulders, forelegs, back, belly, rump, hindlegs and tail. Solicitation of licking is the behaviour in which one animal puts its cheek near another's mouth, or gently nudges or pushes the other's nose or cheek with its nose, just before being licked. The influence of social relationships on the time that each focal animal was involved in social licking with each other herd m e m b e r was investigated using least-squares analysis of variance. For each pair considered, independent factors were the difference of d o m i n a n c e values (under and over 15 ° ), the dom-
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inance-subordinance relationship, kinship (closer than half-sib and others), and familiarity (cohabiting periods of 1-2 months, 3-4 months and over 4 months ). The sex of the licking calf was also included. A mathematical model was as follows
Yijkhnqr= M+ Di + Rj + Kk+ FI+ Sin + Iq + Eijkhnqr where Yijkhnqr is the time (s h - ~) when each focal animal performed to each of remaining herd members or received from each of remaining members of a herd; M is the total mean; Di is the effect of the ith difference of dominance values; Rk is the effect of the jth dominance-subordinate relationship, Kk is the effect of t h e / a h kinship; FI is the effect of the lth familiarity; Sm is the effect of the ruth sex; Iq is the effect of the qth focal animal; Eijkhnqr is a random error specific to this observation. The dominance-subordinance relationship in every pair of calves was determined from attack-escape or avoidance behaviour during preliminary observations and main observations. There was no aggressive behaviour observed in 19 out of the 78 possible pair combinations in Herd 1 or in 27 out of 91 pairs in Herd 2. Each of these pairs was therefore entered in a small pen, where the calves were forced to feed competitively from restricted feed trough space. The dominance-subordinance relationships in these pairs were then decided from the attack and escape or avoidance behaviour which occurred during this competition. In spite of these trials, fighting was not observed at all in four pairs in Herd 1 and in two pairs in Herd 2. Dominance values of calves were calculated using the arcsin transform method (Beilharz et al., 1966 ). The ranges of dominance values were 12-78 ° in Herd 1, and 14-90 ° in Herd 2. RESULTS
The nature o[social licking A mean frequency of social licking interaction from four focal individuals was 4.8 times h - ~. A licking bout was identified when a time interval between licking acts exceeded 30 s. Bout lengths ranged from 1 s to 343 s and the mean bout length was 43.3 s. Mean time spent in social licking was 210 s h -~, which occupied 5.8% of the total observation time. Table 1 shows least-squares means of the time spent in social licking under each environmental condition and the significance (F-value) of each environmental factor on social licking. Only the weather factor was significant, and showed that social licking decreased on rainy days to about half that on clear days. Social licking tended to increase when the barn was dirty ( P < 0.20) or when calves had not been fed in the afternoon ( P < 0.08 ).
SOCIAL LICKING PATTERNS IN CATTLE
7
TABLE 1 Effects o f environmental conditions on social licking time (s h-~ ) Independent variable
Class
Least-squares mean + SE
Fvalue
Probabilily
Weather
Clear Rainy Clean Dirty Twice Once
258 _+24 138 _+48 171 + 34 225+35 158 + 28 239 + 42
5.189
*
Barn Feeding Individuality
1.668 3.257 6.663
***
*P<0.05; ***P<0.001. TABLE 2 Percent o f frequency a n d d u r a t i o n of social licking with a n d without solicitation Solicitation
Frequency Time T i m e per interaction (s)
With
Without
31.3 39.4 55 _+ 74
62.5 54.7 38 _+ 51
Unknown
Probability ~
6.2 5.9
** ** *
~The Z 2 test was used for frequency a n d time, and the Welch's t-test for time per interaction: *P<0.05;**P<0.01.
Classification of social licking with or without solicitation Licking solicitation occurred not only from dominant animals of pairs but also subordinate animals. Dominant animals and subordinate animals of pairs were licked after solicitation in 34.8% and 31.3% of total licking interactions, respectively, and occupied 44.8% and 36.5% of total licking time, respectively. Table 2 shows that social licking without solicitation was more frequent than that with solicitation (P<0.01). However, social licking following solicitation continued for longer than that without solicitation, partly because receivers which solicited licking initially, frequently solicited again when social licking had stopped. Solicitation was quite effective in eliciting licking and was frequently used by receivers.
Licking of d~fferent parts of the body Figure 1 shows the distribution of licking to different parts of the body with and without solicitation. Overall, parts of the body received the following
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s. SATO ET AL.
qOCO W i t h SOIIC ,t a t ion
w,,~ou, ~o,,c,,a,,oo
•
[]
3000
2000
1000
HeJd
[,lec ~
I r'll
Slqo~Jlder #-or elec •aCI'
Oeql't
Ru~lp
TQI1
14~ndleg
Fig. I. Distribution of all social licking observed with and without solicitation to various pans of the body.
proportions of total licking time: neck, 27%; head, 25%; back, 15%; shoulders, 13%; rump, 12%; belly, 4%; hindlegs, 3%; forelegs, 1%; tail, 1%. Social licking with solicitation was mainly oriented to the neck and the head areas which receivers could not themselves reach in self-licking, and licking of these areas accounted for 78% of the total time. Social licking without solicitation was not only oriented to the neck and the head, accounting for 28% of the total time, but also to the back and the rump, accounting for 47% of the total time, although this difference was not significant (t-test in paired samples).
Effect of social relationships on social licking Tables 3 (A) and 3 (B) show the least-squares means of time performing social licking and time receiving social licking, respectively, and the significance of various social relationships (F-values). Coefficients of determination by all independent factors were 49.6% and 37.5% in licking performed and licking received, respectively. Only the familiarity factor was significant, such that exchanges of social licking increased with the length of cohabitation.
SOCIAL LICKING PATTERNS IN CATTLE TABLE 3 (A) Influence of social factors on the social licking time (s h - ' ) performed by four focal animals Independent variable
Category
Difference in rank
< 15 ° > 15 ° Dominant Subordinate Steer Heifer 1-2 months 3-4 months > 4 months > 0.25 <0.25
Rank Sex Cohabitation
Kinship
Least-squares mean + SE
Fvalue
9.6_+ 3.3 9.8_+2.4 11.3_+ 3.9 8. I _+3.6 9.8_+ 2.8 9.7 _+2.9 4.6 _+4.5 5.7 _+4.2 18.9_+ 3.4 10.3 _+2.1 9.2_+3.6
Probability
0.003 0.269 0.000 3.471
0.068
Individuality
1.369
(B) Influence of social factors on the received social licking time (s h - ' ) Independent variable
Category
Least-squares mean + SE
Fvalue
Difference in rank
< 15 ° > 15: Dominant Subordinate Steer Heifer 1-2 months 3-4 months > 4 months > 0.25 <0.25
7.6 + 3.4 7.2+2.5 4.1 +4.0 10.7 + 3.7 5. I + 2.9 9.8+3.0 - 2.6 + 4.6 3.8 + 4.3 21.1 +3.5 4.6 + 2.1 10.2+3.7
0.008
Rank Sex Cohabitation
Kinship Individuality
Probability
1.070 1.246 7.441
1.709 1.287
*P< 0.05, ***P<0.001. DISCUSSION
Influence of environmental factors The frequency of social licking and the time spent licking in this study were higher than in Sambraus' ( 1969 ) study and Wood's (1977) study, partly because calves involved in a lot of social licking were chosen as focal animals and calves were observed when the most social licking occurred in this study. Sambraus and Wood reported that there were periods when social licking occured frequently and that these periods related to the feeding rhythm. One model of behavioural motivation which could account for this pattern has
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been proposed by Hurnik and Lehmann (1985), who suggested three categories of 'need'. Social licking behaviour may be thought of as an 'attitude sustaining need'. It may therefore follow 'life sustaining needs' such as feeding behaviour and 'health sustaining needs' such as shelter-seeking behaviour, either in importance or in time. As the twilight may be a spare time when life sustaining needs and health sustaining needs have been satisfied, social licking behaviour might occur frequently to fulfill an attitude sustaining need at this time. Furuya (1957) and Bernstein (1972) reported, similarly, that social grooming in primates decreased drastically on rainy days. One possible explanation is that social licking may be suppressed showing the elasticity characteristics of less important needs, on rainy days when shelter-seeking behaviour is motivated. Social licking tended to increase when the barn was dirty ( P < 0.20 )or when calves had not been fed in the afternoon ( P < 0.08 ). The former suggests the hypothesis that dirty skin and hair may be cleaned by social licking. The latter suggests the hypothesis that social licking may be performed as a displacement activity, in a conflict situation (Wood-Gush, 1983). However, these tendencies were not significant, so these functions of social licking are unlikely to be major ones.
Influence of socialfactors Sambraus ( 1969 ) reported that social licking with solicitation in dairy cows was oriented only to the head and the neck. In the present study, licking was also restricted to just the head and the neck immediately after solicitation, but then tended to move gradually to other areas. Sambraus (1969) also reported that 76% of total licking was oriented to the head and the neck, even if receivers did not solicit, while the back and the rump were the main licking areas without solicitation in this study. It is well-known (Kiley-Worthington and de la Plain, 1983; Sato et al., 1990) that bulls frequently lick oestrous cows and that this licking is mainly oriented to the back, the rump and the hindlegs. In this study, steers licked the back, the rump and the hindlegs (39% of the total time) significantly more than heifers (21% of the total time). The difference between Sambraus' (1969) results and our results may partly derive from the different sex of the animals in the two studies. It was found, in agreement with Sambraus (1969) for dairy cattle (Bos taurus) and Scheurman ( 1975 ) for the Mithan (Bibosfrontalis), that licking solicitation mutually occurred from dominant and subordinate animals of pairs. It suggests that licking interactions are independent of social dominance. The effectiveness of licking solicitation suggests that social licking might be beneficial for receivers. As suggested above, benefits may include first, a cleaning function, because body regions that were inaccessible to receivers
SOCIAL L I C K I N G PATTERNS IN CATTLE
I [
were chosen as the parts of social licking (Fig. 1 ). Second, a psychological and physiological calming effect is possible. Evidence for this tension reduction hypothesis comes from the observation that cattle sometimes half closed their eyes while receiving social licking, as also reported by Brownlee (1950). Wood ( 1977 ) reported that social licking in monozygotic twins was prominent. Though it is likely from the viewpoint of evolutionary theory that altruistic behaviour such as social licking will indeed be prominent among relatives, the present study suggests that frequent licking among relatives in cattle may derive not from kinship but cohabitation. It has also been suggested that feral cattle may form matrilineal groups by adopting overlapping home ranges (Kimura and Ihobe, 1985; Sato, 1991 ). It is possible then that monozygotic twins may lick each other primarily as a result of their cohabitation from birth. Kin recognition in cattle may, in fact, derive from familiarity. Cohabitation from young ages influences later social bonding (Sato et al., 1987 ), and this social bonding may cause social stability by depressing aggressive behaviour (Bouissou and Andrieu, 1978 ). These results suggest that social licking may reduce behavioural tension. Schloeth (1961) and Sato (1984) showed that much social licking occurred between cattle which are close in dominance rank. As the social rank strongly correlates with age (Reinhardt and Reinhardt, 1975), similarity in ranking may mean similarity in age. As cattle with similar ages may live together for a long time, much social licking among cattle with similar dominance ranks may not be derived from the rank itself but from familiarity. ACKNOWLEDGEMENT
We are very grateful to Dr. M.C. Appleby for helpful comments on this manuscript. REFERENCES Barton, R., 1985. Grooming site preferences in primates and their functional implications. Int. J. Primatol., 6: 519-532. Beilharz, R.G., Butcher, D.F. and Freeman, A.E., 1966. Social dominance and milk production in Holsteins. J. Dairy Sci., 49: 887-892. Bernstein, I.S., 1972. Daily activity cycles and weather influences on a pigtail monkey group. Folia Primatol., 18: 390-415. Boccia, M.L., 1983. A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys. Int. J. Primatol., 4:399-418. Boccia, M.L., Retie, M. and Laudenslager, M., 1989. On the physiology of grooming in a pigtail macaque. Physiol. Behav., 45: 667-670. Bouissou, M.-F. and Andrieu, S., 1978. Etablissement des relations preferentielles chez les bovins domestiques. Behaviour, 54: 148-157. Brownlee, A., 1950. Studies in the behaviour of domestic cattle in Britain. Bull. Anim. Behav., 8:11-20.
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Fraser, A.F. and Broom, D.M., 1990. Farm Animal Behaviour and Welfare, 3rd edn. Bailliere Tindall, London, pp. 156-161. Furuya, Y., 1957. Grooming behavior in the wild Japanese monkeys. Primates, 1:47-68 (in Japanese, with English abstract). Hafcz. E.S.E., Schein, M.W. and Ewbank, R., 1969. The behavior of cattle. In: E.S.E. Hafez ( Editor ), The Behavior of Domestic Animals, 2nd edn. Bailliere, Tindall & Cassell, London, pp. 235-295. Hurnik, J.F. and Lehmann, H., 1985. The philosophy of farm animal welfare: a contribution to the assessment of farm animal well-being. In: R.-M. Wegner (Editor), Second European Symposium on Poultry Welfare, 10-13 June 1985, Celle, Germany, pp. 256-266. Hutchins, M. and Barash, D.P., 1976. Grooming in primates: Implications for its utilitarian function. Primates, 17:145-150. Keverne, E.B., Martensz, N.D. and Tuite, B., 1989. Beta-endrophin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinolog,v, 14: 155-161. Kiley-Worthinglon, M. and de la Plain, D., 1983. The Behaviour of Beef Suckler Cattle (Bos lattrtts ). Birkhauser, Basel, p. 41. Kimura, D. and lhobe, H., 1985. Feral cattle (Bos taurus) on Kuchinoshima Island, southwestern Japan: Their stable ranging and unstable grouping. J. Ethol., 3: 39-47. O'Keeffe, R.T., Lifshitz, K. and Linn, G., 1982/1983. Relationships among dominance, interanimal spatial proximity and afliliative social behaviour in stumptail nacaques (Macaca arctoides). Appl. Anim. Ethol., 9:331-339. Panksepp, J., Herman, B.H., Vilberg, T., Bishop, P. and DeEskinazi, F.G., 1980. Endogenous opiods and social behavior. Neurosci. Biobehav. Rev., 4: 473-487. Reinhardt, V. and Reinhardt, A., 1975. Dynamics of social hierarchy in a dairy herd. Z. Ticrpsychol., 38:315-323. Rich, G.B., 1973. Grooming and yarding of spring-born calves prevent paralysis caused by the Rocky Mountain wood tick. Can. J. Anita. Sci., 53: 377-378. Sambraus, H.H., 1969. Das Soziale Lecken des Rindes. Z. Ticrpsychol., 26: 805-810. Sato, S., 1984. Social licking pattern and its relationships to social dominance and livcwcight gain in weaned calves. Appl. Anita. Behav. Sci., 12: 25-32. Sato. S., 1991. The behaviour of Kuchinoshima feral cows. Anim. Sci. Technol. (Jpn.), 62: 390-397 ( in Japanese with English abstract ). Sato. S., Wood-Gush, D.G.M. and Wetherill, G., 1987. Observations on creche behaviour in suckler cah, cs. Behav. Proccss., 15: 333-343. Sato, S., Honda, Y., Komatsu, S. and Sonoda, T., 1990. Behavioural interaction of a bull with newly calved cows before resumption ofestrous. Jpn. J. Zootech. Sci., 61:487-492 (in Japanese, with English abstract). Schcurmann, E., 1975. Observations on the behaviour of the Mithan (Bibos./i'onta/is Lambert 1837) in captivity. Appl. Anim. Ethol., 1: 321-355. Schino, G.. Scucchi, S., Maestripicri, D. and Turillazzi, P.G., 1988. Allogrooming as a tensionreduction mechanism: a behavioral approach. Am. J. Primatol., 16: 43-50. Schloeth, R., 1961. Das Sozialleben des Camargue-Rindes. Qualitative und quantitative Untcrsuchungen fiber die sozialen Beziehungen - insbesondere die soziale Rangordnung - des halbwildcn franzosischen Kampfrindes. Z. Tierpsychol., 18: 574-627. Stammbach, E. and Kummer, H., 1982. Individual contributions to a dyadic interaction: an analysis of baboon grooming. Anim. Behav., 30:964-971. Wood, M.T., 1977. Social grooming patterns in two herds of monozygotic twin dairy cows. Anim. Bchav., 25: 635-642. Wood-Gush, D.G.M., 1983. Element of Ethology. Chapman and Hall, London, New York, p. 134.
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Elsevier Science Publishers B.V., A m s t e r d a m
Social licking patterns in cattle (Bos taurus)" influence of environmental and social factors S. Sato, S. Sako and A. Maeda Faculty qf.-lgriculture, Mivazaki University Mivazaki-shi 889-2l Japan (Accepted 8 March 1991 )
ABSTRACT Sato, S., Sako, S. and Maeda, A., 1991. Social licking patterns in cattle (Bos taurus): influence of environmental and social factors. Appl. ,4him. Behav. Sci., 32:3-12. To investigate the functions of social licking in cattle, four calves (one heifer and one steer in each of two herds), known to exhibit frequent social licking were observed continuously for 2 h before sunset for 13 days, using the focal animal sampling method. Calves were observed under various cnvironrnental conditions. Social licking significantly decreased on rainy days and tended to increase in a dirty barn and when food was restricted. Solicitation for social licking occurred not only from dominant animals of pairs but also from subordinates. Of the licking interactions, 31% occurred following solicitation, and these accounted for 39% of the total time spent licking. Following solicitation, 78% of social licking was oriented to the head and the neck regions that were inaccessible to selflicking animals. Unsolicited licking, however, was oriented not only to the head and the neck but also to the back and the rump regions, and these two latter regions were the major ones to receive licking. The effect of social relationships on social licking was investigated using least-squares analysis of variance. Social factors investigated were the difference of dominance values, the dominancc-subordinance relationship, and kinship and familiarity: the sex of calves involved was also considered. Only familiarity had a significant effect on licking: exchanges of social licking increased with length of cohabitation. We suggest Ihat social licking may have a cleaning effect, a tension-reducing effect and a bonding effect.
INTRODUCTION
Various kinds of animals from rodents to primates exhibit social grooming as a non-aggressive behaviour. There have been many studies on social grooming in primates, as primates frequently groom socially. These suggest cleaning and eating functions based on grooming site preferences (Hutchins and Barash, 1976; Barton, 1985) and removal of dirt or ectoparasites (Simonds, 1965), social bonding functions (Stammbach and Kummer, 1982; O'Keeffe et al., 1982/1983 ) and tension-reducing functions based on grooming methods (Boccia, 1983 ), physiological changes (Boccia et al., 1989 ), biochemical changes (Panksepp et al., 1980; Keverne et al., 1989) and behavioural changes (Schino et al., 1988 ). 0168-1591/91/$03.50
© 1991 Elsevier Science Publishers B.V. All rights reserved.
4
s. SATO ET AL
On the other hand, little has been published on social grooming in cattle, though Brownlee (1950) recognized social grooming as one of the most important behaviours in cattle. Hafez et al. (1969) suggested that the cleaning and eating functions also occur in cattle and Rich ( 1973 ) confirmed this hypothesis with evidence that cows removed some ticks from their calves by maternal licking. Sambraus ( 1969 ) suggested another function in addition to cleaning and eating, from anecdotal evidence that social licking occurred frequently after disturbance and that bulls licked oestrous cows more frequently than anoestrous cows. Wood (1977) found a positive relationship between the time spent receiving licking and milk production. Sato (1984) found a positive relationship between the time spent receiving licking and liveweight gain. Wood and Sato both suggested that these physical effects were due to a reduction in tension: a calming effect of the social grooming. In addition, Fraser and Broom (1990) considered that it is likely that social licking has effects on the psychological stability of the animals concerned as well as cleaning skin and hair. The above studies, however, have been insufficient to confirm the cleaning, eating and tension-reducing functions, and the social bonding hypothesis has not been investigated at all. In this study, the nature of social licking and the influence of social factors on social licking in cattle were investigated to obtain evidence for the importance of the various functions discussed above.
ANIMALS, MATERIALS AND METHODS
A steer and a heifer were selected as focal animals from each of two rearing Holstein herds. Preliminary observation indicated that social licking was particularly frequent during the 2 h before sunset. Consequently, the two animals in each herd were individually observed during this period for 13 days under various environmental conditions. Observations were made using two video recording systems, one for each animal.
Experimental animals The first herd consisted of seven steers and six heifers aged from about 12 to about 15 months old. The second herd consisted of seven steers and seven heifers aged from about 11 to about 15 m o n t h s old, eight calves from Herd 1 and six new calves. From the preliminary observations, two calves in Herd 1 were selected as the most frequent performers of social licking and two calves in Herd 2 were selected as the most frequent receivers.
SOCIAL LICKING PATTERNS IN CATTLE
5
The rearing method Calves were reared in a pen measuring 9 m X 13.5 m covered with a half roof. They were fed concentrates ad libitum and silage at 10:00 and 13:30 h. The barn was cleaned every 5 days.
Observation periods Herd 1 was observed for 13 days between the end of July and the end of August. Herd 2 was observed for 13 days between the end of September and the end of October. In order to investigate the cleaning hypothesis, calves were observed under various environmental conditions. The weather conditions were rainy for 5 days and clear for 21 days of observation. The barn was clean for 15 days (had been cleaned on the observation day) and dirty for 11 days (more than 3 days had passed since cleaning). In addition, the effect of restricted feeding was investigated to test Sambraus' (1969) suggestion that social licking occurs after feeding, that is, after the appetitive drive has been fulfilled. Calves were fed twice a day for 18 days and fed only in the morning for 8 days. The influence of various environmental conditions on social licking was investigated using least-squares analysis of variance in 13 × 4 days. A mathematical model was as follows
Yijklm = M+ Wi + Bj+ Fk+ Il+ Eijklm where Yijkhn is the time (s h-~ ) for which each focal animal was involved in social licking in each observation day; M is the total mean; Wi is the effect of the ith weather condition; Bj is the effect of t h e j t h barn condition; Fk is the effect of the/cth feeding condition;//is the effect of the/th focal animal; Eijkhn is a random error specific to this observation.
Analysis of behaviour All occurrences of social licking involving focal animals were recorded during playback of the video tapes. The performers and receivers of solicitation or social licking were identified, durations were recorded and the parts of the body which were licked were noted. The body was divided into nine parts: head, neck, shoulders, forelegs, back, belly, rump, hindlegs and tail. Solicitation of licking is the behaviour in which one animal puts its cheek near another's mouth, or gently nudges or pushes the other's nose or cheek with its nose, just before being licked. The influence of social relationships on the time that each focal animal was involved in social licking with each other herd m e m b e r was investigated using least-squares analysis of variance. For each pair considered, independent factors were the difference of d o m i n a n c e values (under and over 15 ° ), the dom-
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s. SATO ET AL.
inance-subordinance relationship, kinship (closer than half-sib and others), and familiarity (cohabiting periods of 1-2 months, 3-4 months and over 4 months ). The sex of the licking calf was also included. A mathematical model was as follows
Yijkhnqr= M+ Di + Rj + Kk+ FI+ Sin + Iq + Eijkhnqr where Yijkhnqr is the time (s h - ~) when each focal animal performed to each of remaining herd members or received from each of remaining members of a herd; M is the total mean; Di is the effect of the ith difference of dominance values; Rk is the effect of the jth dominance-subordinate relationship, Kk is the effect of t h e / a h kinship; FI is the effect of the lth familiarity; Sm is the effect of the ruth sex; Iq is the effect of the qth focal animal; Eijkhnqr is a random error specific to this observation. The dominance-subordinance relationship in every pair of calves was determined from attack-escape or avoidance behaviour during preliminary observations and main observations. There was no aggressive behaviour observed in 19 out of the 78 possible pair combinations in Herd 1 or in 27 out of 91 pairs in Herd 2. Each of these pairs was therefore entered in a small pen, where the calves were forced to feed competitively from restricted feed trough space. The dominance-subordinance relationships in these pairs were then decided from the attack and escape or avoidance behaviour which occurred during this competition. In spite of these trials, fighting was not observed at all in four pairs in Herd 1 and in two pairs in Herd 2. Dominance values of calves were calculated using the arcsin transform method (Beilharz et al., 1966 ). The ranges of dominance values were 12-78 ° in Herd 1, and 14-90 ° in Herd 2. RESULTS
The nature o[social licking A mean frequency of social licking interaction from four focal individuals was 4.8 times h - ~. A licking bout was identified when a time interval between licking acts exceeded 30 s. Bout lengths ranged from 1 s to 343 s and the mean bout length was 43.3 s. Mean time spent in social licking was 210 s h -~, which occupied 5.8% of the total observation time. Table 1 shows least-squares means of the time spent in social licking under each environmental condition and the significance (F-value) of each environmental factor on social licking. Only the weather factor was significant, and showed that social licking decreased on rainy days to about half that on clear days. Social licking tended to increase when the barn was dirty ( P < 0.20) or when calves had not been fed in the afternoon ( P < 0.08 ).
SOCIAL LICKING PATTERNS IN CATTLE
7
TABLE 1 Effects o f environmental conditions on social licking time (s h-~ ) Independent variable
Class
Least-squares mean + SE
Fvalue
Probabilily
Weather
Clear Rainy Clean Dirty Twice Once
258 _+24 138 _+48 171 + 34 225+35 158 + 28 239 + 42
5.189
*
Barn Feeding Individuality
1.668 3.257 6.663
***
*P<0.05; ***P<0.001. TABLE 2 Percent o f frequency a n d d u r a t i o n of social licking with a n d without solicitation Solicitation
Frequency Time T i m e per interaction (s)
With
Without
31.3 39.4 55 _+ 74
62.5 54.7 38 _+ 51
Unknown
Probability ~
6.2 5.9
** ** *
~The Z 2 test was used for frequency a n d time, and the Welch's t-test for time per interaction: *P<0.05;**P<0.01.
Classification of social licking with or without solicitation Licking solicitation occurred not only from dominant animals of pairs but also subordinate animals. Dominant animals and subordinate animals of pairs were licked after solicitation in 34.8% and 31.3% of total licking interactions, respectively, and occupied 44.8% and 36.5% of total licking time, respectively. Table 2 shows that social licking without solicitation was more frequent than that with solicitation (P<0.01). However, social licking following solicitation continued for longer than that without solicitation, partly because receivers which solicited licking initially, frequently solicited again when social licking had stopped. Solicitation was quite effective in eliciting licking and was frequently used by receivers.
Licking of d~fferent parts of the body Figure 1 shows the distribution of licking to different parts of the body with and without solicitation. Overall, parts of the body received the following
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s. SATO ET AL.
qOCO W i t h SOIIC ,t a t ion
w,,~ou, ~o,,c,,a,,oo
•
[]
3000
2000
1000
HeJd
[,lec ~
I r'll
Slqo~Jlder #-or elec •aCI'
Oeql't
Ru~lp
TQI1
14~ndleg
Fig. I. Distribution of all social licking observed with and without solicitation to various pans of the body.
proportions of total licking time: neck, 27%; head, 25%; back, 15%; shoulders, 13%; rump, 12%; belly, 4%; hindlegs, 3%; forelegs, 1%; tail, 1%. Social licking with solicitation was mainly oriented to the neck and the head areas which receivers could not themselves reach in self-licking, and licking of these areas accounted for 78% of the total time. Social licking without solicitation was not only oriented to the neck and the head, accounting for 28% of the total time, but also to the back and the rump, accounting for 47% of the total time, although this difference was not significant (t-test in paired samples).
Effect of social relationships on social licking Tables 3 (A) and 3 (B) show the least-squares means of time performing social licking and time receiving social licking, respectively, and the significance of various social relationships (F-values). Coefficients of determination by all independent factors were 49.6% and 37.5% in licking performed and licking received, respectively. Only the familiarity factor was significant, such that exchanges of social licking increased with the length of cohabitation.
SOCIAL LICKING PATTERNS IN CATTLE TABLE 3 (A) Influence of social factors on the social licking time (s h - ' ) performed by four focal animals Independent variable
Category
Difference in rank
< 15 ° > 15 ° Dominant Subordinate Steer Heifer 1-2 months 3-4 months > 4 months > 0.25 <0.25
Rank Sex Cohabitation
Kinship
Least-squares mean + SE
Fvalue
9.6_+ 3.3 9.8_+2.4 11.3_+ 3.9 8. I _+3.6 9.8_+ 2.8 9.7 _+2.9 4.6 _+4.5 5.7 _+4.2 18.9_+ 3.4 10.3 _+2.1 9.2_+3.6
Probability
0.003 0.269 0.000 3.471
0.068
Individuality
1.369
(B) Influence of social factors on the received social licking time (s h - ' ) Independent variable
Category
Least-squares mean + SE
Fvalue
Difference in rank
< 15 ° > 15: Dominant Subordinate Steer Heifer 1-2 months 3-4 months > 4 months > 0.25 <0.25
7.6 + 3.4 7.2+2.5 4.1 +4.0 10.7 + 3.7 5. I + 2.9 9.8+3.0 - 2.6 + 4.6 3.8 + 4.3 21.1 +3.5 4.6 + 2.1 10.2+3.7
0.008
Rank Sex Cohabitation
Kinship Individuality
Probability
1.070 1.246 7.441
1.709 1.287
*P< 0.05, ***P<0.001. DISCUSSION
Influence of environmental factors The frequency of social licking and the time spent licking in this study were higher than in Sambraus' ( 1969 ) study and Wood's (1977) study, partly because calves involved in a lot of social licking were chosen as focal animals and calves were observed when the most social licking occurred in this study. Sambraus and Wood reported that there were periods when social licking occured frequently and that these periods related to the feeding rhythm. One model of behavioural motivation which could account for this pattern has
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been proposed by Hurnik and Lehmann (1985), who suggested three categories of 'need'. Social licking behaviour may be thought of as an 'attitude sustaining need'. It may therefore follow 'life sustaining needs' such as feeding behaviour and 'health sustaining needs' such as shelter-seeking behaviour, either in importance or in time. As the twilight may be a spare time when life sustaining needs and health sustaining needs have been satisfied, social licking behaviour might occur frequently to fulfill an attitude sustaining need at this time. Furuya (1957) and Bernstein (1972) reported, similarly, that social grooming in primates decreased drastically on rainy days. One possible explanation is that social licking may be suppressed showing the elasticity characteristics of less important needs, on rainy days when shelter-seeking behaviour is motivated. Social licking tended to increase when the barn was dirty ( P < 0.20 )or when calves had not been fed in the afternoon ( P < 0.08 ). The former suggests the hypothesis that dirty skin and hair may be cleaned by social licking. The latter suggests the hypothesis that social licking may be performed as a displacement activity, in a conflict situation (Wood-Gush, 1983). However, these tendencies were not significant, so these functions of social licking are unlikely to be major ones.
Influence of socialfactors Sambraus ( 1969 ) reported that social licking with solicitation in dairy cows was oriented only to the head and the neck. In the present study, licking was also restricted to just the head and the neck immediately after solicitation, but then tended to move gradually to other areas. Sambraus (1969) also reported that 76% of total licking was oriented to the head and the neck, even if receivers did not solicit, while the back and the rump were the main licking areas without solicitation in this study. It is well-known (Kiley-Worthington and de la Plain, 1983; Sato et al., 1990) that bulls frequently lick oestrous cows and that this licking is mainly oriented to the back, the rump and the hindlegs. In this study, steers licked the back, the rump and the hindlegs (39% of the total time) significantly more than heifers (21% of the total time). The difference between Sambraus' (1969) results and our results may partly derive from the different sex of the animals in the two studies. It was found, in agreement with Sambraus (1969) for dairy cattle (Bos taurus) and Scheurman ( 1975 ) for the Mithan (Bibosfrontalis), that licking solicitation mutually occurred from dominant and subordinate animals of pairs. It suggests that licking interactions are independent of social dominance. The effectiveness of licking solicitation suggests that social licking might be beneficial for receivers. As suggested above, benefits may include first, a cleaning function, because body regions that were inaccessible to receivers
SOCIAL L I C K I N G PATTERNS IN CATTLE
I [
were chosen as the parts of social licking (Fig. 1 ). Second, a psychological and physiological calming effect is possible. Evidence for this tension reduction hypothesis comes from the observation that cattle sometimes half closed their eyes while receiving social licking, as also reported by Brownlee (1950). Wood ( 1977 ) reported that social licking in monozygotic twins was prominent. Though it is likely from the viewpoint of evolutionary theory that altruistic behaviour such as social licking will indeed be prominent among relatives, the present study suggests that frequent licking among relatives in cattle may derive not from kinship but cohabitation. It has also been suggested that feral cattle may form matrilineal groups by adopting overlapping home ranges (Kimura and Ihobe, 1985; Sato, 1991 ). It is possible then that monozygotic twins may lick each other primarily as a result of their cohabitation from birth. Kin recognition in cattle may, in fact, derive from familiarity. Cohabitation from young ages influences later social bonding (Sato et al., 1987 ), and this social bonding may cause social stability by depressing aggressive behaviour (Bouissou and Andrieu, 1978 ). These results suggest that social licking may reduce behavioural tension. Schloeth (1961) and Sato (1984) showed that much social licking occurred between cattle which are close in dominance rank. As the social rank strongly correlates with age (Reinhardt and Reinhardt, 1975), similarity in ranking may mean similarity in age. As cattle with similar ages may live together for a long time, much social licking among cattle with similar dominance ranks may not be derived from the rank itself but from familiarity. ACKNOWLEDGEMENT
We are very grateful to Dr. M.C. Appleby for helpful comments on this manuscript. REFERENCES Barton, R., 1985. Grooming site preferences in primates and their functional implications. Int. J. Primatol., 6: 519-532. Beilharz, R.G., Butcher, D.F. and Freeman, A.E., 1966. Social dominance and milk production in Holsteins. J. Dairy Sci., 49: 887-892. Bernstein, I.S., 1972. Daily activity cycles and weather influences on a pigtail monkey group. Folia Primatol., 18: 390-415. Boccia, M.L., 1983. A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys. Int. J. Primatol., 4:399-418. Boccia, M.L., Retie, M. and Laudenslager, M., 1989. On the physiology of grooming in a pigtail macaque. Physiol. Behav., 45: 667-670. Bouissou, M.-F. and Andrieu, S., 1978. Etablissement des relations preferentielles chez les bovins domestiques. Behaviour, 54: 148-157. Brownlee, A., 1950. Studies in the behaviour of domestic cattle in Britain. Bull. Anim. Behav., 8:11-20.
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Fraser, A.F. and Broom, D.M., 1990. Farm Animal Behaviour and Welfare, 3rd edn. Bailliere Tindall, London, pp. 156-161. Furuya, Y., 1957. Grooming behavior in the wild Japanese monkeys. Primates, 1:47-68 (in Japanese, with English abstract). Hafcz. E.S.E., Schein, M.W. and Ewbank, R., 1969. The behavior of cattle. In: E.S.E. Hafez ( Editor ), The Behavior of Domestic Animals, 2nd edn. Bailliere, Tindall & Cassell, London, pp. 235-295. Hurnik, J.F. and Lehmann, H., 1985. The philosophy of farm animal welfare: a contribution to the assessment of farm animal well-being. In: R.-M. Wegner (Editor), Second European Symposium on Poultry Welfare, 10-13 June 1985, Celle, Germany, pp. 256-266. Hutchins, M. and Barash, D.P., 1976. Grooming in primates: Implications for its utilitarian function. Primates, 17:145-150. Keverne, E.B., Martensz, N.D. and Tuite, B., 1989. Beta-endrophin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinolog,v, 14: 155-161. Kiley-Worthinglon, M. and de la Plain, D., 1983. The Behaviour of Beef Suckler Cattle (Bos lattrtts ). Birkhauser, Basel, p. 41. Kimura, D. and lhobe, H., 1985. Feral cattle (Bos taurus) on Kuchinoshima Island, southwestern Japan: Their stable ranging and unstable grouping. J. Ethol., 3: 39-47. O'Keeffe, R.T., Lifshitz, K. and Linn, G., 1982/1983. Relationships among dominance, interanimal spatial proximity and afliliative social behaviour in stumptail nacaques (Macaca arctoides). Appl. Anim. Ethol., 9:331-339. Panksepp, J., Herman, B.H., Vilberg, T., Bishop, P. and DeEskinazi, F.G., 1980. Endogenous opiods and social behavior. Neurosci. Biobehav. Rev., 4: 473-487. Reinhardt, V. and Reinhardt, A., 1975. Dynamics of social hierarchy in a dairy herd. Z. Ticrpsychol., 38:315-323. Rich, G.B., 1973. Grooming and yarding of spring-born calves prevent paralysis caused by the Rocky Mountain wood tick. Can. J. Anita. Sci., 53: 377-378. Sambraus, H.H., 1969. Das Soziale Lecken des Rindes. Z. Ticrpsychol., 26: 805-810. Sato, S., 1984. Social licking pattern and its relationships to social dominance and livcwcight gain in weaned calves. Appl. Anita. Behav. Sci., 12: 25-32. Sato. S., 1991. The behaviour of Kuchinoshima feral cows. Anim. Sci. Technol. (Jpn.), 62: 390-397 ( in Japanese with English abstract ). Sato. S., Wood-Gush, D.G.M. and Wetherill, G., 1987. Observations on creche behaviour in suckler cah, cs. Behav. Proccss., 15: 333-343. Sato, S., Honda, Y., Komatsu, S. and Sonoda, T., 1990. Behavioural interaction of a bull with newly calved cows before resumption ofestrous. Jpn. J. Zootech. Sci., 61:487-492 (in Japanese, with English abstract). Schcurmann, E., 1975. Observations on the behaviour of the Mithan (Bibos./i'onta/is Lambert 1837) in captivity. Appl. Anim. Ethol., 1: 321-355. Schino, G.. Scucchi, S., Maestripicri, D. and Turillazzi, P.G., 1988. Allogrooming as a tensionreduction mechanism: a behavioral approach. Am. J. Primatol., 16: 43-50. Schloeth, R., 1961. Das Sozialleben des Camargue-Rindes. Qualitative und quantitative Untcrsuchungen fiber die sozialen Beziehungen - insbesondere die soziale Rangordnung - des halbwildcn franzosischen Kampfrindes. Z. Tierpsychol., 18: 574-627. Stammbach, E. and Kummer, H., 1982. Individual contributions to a dyadic interaction: an analysis of baboon grooming. Anim. Behav., 30:964-971. Wood, M.T., 1977. Social grooming patterns in two herds of monozygotic twin dairy cows. Anim. Bchav., 25: 635-642. Wood-Gush, D.G.M., 1983. Element of Ethology. Chapman and Hall, London, New York, p. 134.