Livestock Production Science 87 (2004) 259 – 264 www.elsevier.com/locate/livprodsci
Short communication
Effect of restricting suckling on the social bond between ewes and their 10-week-old lambs A. Orihuela a,*, E. Sua´rez b, R. Va´zquez a a
Facultad de Ciencias Agropecuarias, Universidad Auto´noma del Estado de Morelos, Apartado Postal 5-78 Cuernavaca, Morelos 62051, Mexico b Posgrado Interinstitucional en Ciencias Pecuarias, Universidad de Colima, Mexico Received 30 August 2002; received in revised form 29 July 2003; accepted 8 August 2003
Abstract To determine the effect of restricting suckling in the behaviour and welfare of sheep, 40 ewes and their 10-week-old lambs were assigned to one of the following treatments for 10 days: T1 = lambs were free to suckle (control); T2 = the udder of the ewe was smeared with faeces; T3 = the udder of the ewe was covered; and T4 = ewe and lamb were separated by a wire fence. In T1, T2 and T3, lambs remained with their mothers. No differences ( P > 0.05) were found in food consumption or weight gains when treated groups were compared with the controls. Lambs in T2 and T3 performed the same number ( P > 0.05) of suckle episodes with similar ( P > 0.05) length, but less ( P < 0.05) frequent and shorter that in T1. Ewes in all treatments vocalized more than those in the control group ( P < 0.01). Among treatments, vocalization frequency in T4, remained higher for a longer period ( P < 0.05) than in the other groups. No difference was found in vocalization frequency of lambs among treatments, but lambs in T1 tended to vocalize less ( P > 0.05) than treated groups. Cortisol concentrations were similar ( P > 0.05) in all treatments. At the end of the experiment, no difference was found ( P > 0.05) in the number of lambs that attempted to suckle in treatments 2, 3 and 4 (30%, 30% and 20%, respectively). It was concluded that restricting 10-week-old lambs from suckling during a 10-day treatment period induced a minor short-term distress and the break of the social bond in 70 – 80% of the ewe – lamb pairs. D 2003 Elsevier B.V. All rights reserved. Keywords: Restricted suckling; Social bond; Weaning; Welfare; Behaviour
1. Introduction Under natural conditions, weaning involves two distinct processes; gaining independence from the mother as an essential food source and separation from the mother as a social companion. At birth, lambs are unable to digest solid food, but the rumen * Corresponding author. Tel.: +52-777-3174-268; fax: +52-7773137-252. E-mail address:
[email protected] (A. Orihuela). 0301-6226/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.livprodsci.2003.08.003
gradually develops over the ensuing 8 – 10 weeks enabling the lamb to progressively digest food other than milk, conferring the lamb autonomy from the mother as a food source before their separation as social companion (Houpt, 1988). On the other hand, under farm conditions, sheep are commonly weaned by abruptly separating ewes and lambs, terminating nursing but also preventing ewe –lamb contact and social interaction. Haley et al. (2001) established that milk feeding and segregation of young –mother pairs are distinct com-
260
A. Orihuela et al. / Livestock Production Science 87 (2004) 259–264
ponents of weaning that contribute in different ways to the response of the young. Furthermore, weaning by separation of ewes and lambs into adjacent corrals appears to be less stressful than methods in which the mother cannot be seen (McCall et al., 1985). In Africa, it has been reported that some tribes discourage calves from nursing during the weaning period by smearing fresh faeces on the udder of the dam each morning (Lott and Hart, 1979). This kind of process could be more similar to natural weaning (Fraser and Broom, 1998), as suckling is limited while the lamb may still be in contact with their mothers. Sua´rez and Orihuela (2002) found that dry cattle manure induced the highest avoidance behaviours in sheep compared to other types of excretas. This is in accordance with previous findings in cattle (Dohi et al., 1991) and goats (Aoyama et al., 1994). Suckling may also be impeded by physical methods such as covering the udder of the dam during the weaning process. Similar to the former practice, this will allow physical contact and social interactions of the young with their mothers inducing perhaps a less stressful situation during the weaning process. The purpose of the present experiment was to monitor some behavioural and physiological responses associated with restricting suckling in an attempt to break the social bond between ewes and their suckling lambs.
2. Materials and methods This study was conducted in an experimental station in Morelos, Mexico, 18j37VN and 99j19VW, located 899 m above sea level with an average annual rainfall of 800 mm and temperature of 23 jC. Forty crossbred tropical hair sheep females and their lambs were used. Ewes ranged from 24 to 28 months of age and averaged 28.5 F 4.2 kg at the beginning of the experiment. All lambs were single females 72 days old, weighing 10.9 F 2.4 kg. Each mother –young pair was randomly assigned to one of four treatments: T1 = Lambs were free to suckle with no restriction (control group). T2 = Each morning at 08:00 h sterilized dry bovine faeces were manually smeared on the dams udder.
The sterilization of the manure took place using steam at 97 jC for 3 h, 1 week before the experiment. Lambs remained with their mothers. T3 = The udder of the ewes was covered with nylon kept in place by harnesses from the first to the last day of the experiment. Ewes in this treatment were habituated to the use of these harnesses by wearing it for 4 h daily, 1 week before the beginning of the experiment. Lambs also remained with their mothers. T4 = Ewes were able to see, smell and hear their lambs, separated only by a wire fence, but could not make physical contact (or suckle). Each treatment was applied for 10 days. Except for animals in treatment four, where lambs were kept in a separate pen contiguous to their mothers, each ewe – lamb pair was housed separately in a 4 4 m enclosure, allowing the lambs access to a concentrate feed in a separate creep area, inaccessible to their mothers. Ewes were fed with 3 kg of commercial concentrate with 13% protein (Ovejitina, La Hacienda, Mexico), while 300 g of the same food were offered to the lambs. This diet was offered to ewes and lambs 2 weeks before the experiment. All animals had water available ad libitum. Each morning, the residual food was weighed and the daily consumption was calculated. Each lamb was weighed on a weekly basis to determine average daily gain and food conversion. Furthermore, initial and final weights were registered. A closed-circuit TV was used to record activities from 06:00 to 21:00 h. From these videos, vocalizations from the mother and lamb, attempts to suckle, length of suckling episodes and number of visits to the creep area were registered. Blood samples were collected from the lambs at the beginning of the experiment, and 12, 24, and 36 h later for cortisol determination. Samples were collected by venipuncture from the jugular vein into vacuum tubes and immediately transferred to centrifuge tubes cooled on ice, and within 30 min of collection centrifuged for 15 min at 4 jC and 3000 rpm. The serum was then recovered by decanting and stored at 20 jC until assayed. At the end of the 10-day weaning period, all ewes and lambs were placed together on a small pasture for 6 h to determine the number of lambs attempting to
A. Orihuela et al. / Livestock Production Science 87 (2004) 259–264
suckle. Direct observation was used to identify those lambs that attempted to suckle and the reaction of their mothers, nursing or rejecting them. Data on daily food consumption, average daily weight gain, initial and final weight, food conversion, suckling time and cortisol concentrations were evaluated using an Analysis of Variance under the following mathematical model: Yij ¼ l þ Ti þ EðiÞj where Yij = random sampling variables; l = mean of the distribution of Y for a population defined by the experimental conditions as a whole; Ti = the fixed (constant) effect of the ith treatment; and Eij = the random experimental error. When significant differences were detected between treatments as in time suckling or attempting to suckle, multiple comparisons were performed using Fisher’s post hoc protected least-squares difference (PLSD) test (Gill, 1978). Data on vocalizations, number of suckling episodes, number of visits to the creeping area and number of lambs attempting to suckle after 10 days of treatment, were analysed by a v2 test (Siegel and Castellan, 1988).
3. Results No differences ( P >0.05) were found among treatments when comparing initial and final weights of ewes (average = 28.5 F 4.2 and 28.9 F 4.5 kg, respectively) or lambs (average = 10.9 F 2.4 and 11.5 F 2.3
261
kg, respectively), or when comparing daily food consumption within ewes or lambs (Table 1). As expected, number of suckling attempts and average daily time suckling or attempting to suckle were more frequent ( P < 0.05) and lasted longer ( P < 0.05) in treatment one than in treatments two and three (Table 1). Lambs separated from their mothers (T1) visited the creep feeding area more frequently than animals in treatments two and one. However, no difference was found between T3 and the rest of the treatments (Table 1). No differences ( P > 0.05) were found in lambs’ cortisol concentrations among treatments during the first 36 h of the experiment, averaging 0.9 F 0.6, 0.7 F 0.4, 0.7 F 0.4 and 0.7 F 0.4 ng/ml for treatments one, two, three and four, respectively. On the first 3 days of the experiment, treated ewes vocalized more than those in the control group ( P < 0.01), regardless of the treatment used. In addition, all groups displayed a similar decrease in the number of vocalizations during each successive day (Fig. 1). No difference was found in vocalization frequency of lambs among groups. Nevertheless, a non-significant ( P >0.05) trend was found for less vocalization in the control group. Vocalization frequency in T2 and T3 decrease significantly ( P < 0.05) on day two, while it took up to 3 days before a similar effect was observed in T4 (Fig. 1). At the end of the experiment, no difference was found ( P > 0.05) in the number of lambs that attempted to suckle in treatments 2, 3 and 4 (30%, 30% and
Table 1 Average (F SD) food consumption, visits to the creep feeder, time spent suckling or attempting to suckle and number of suckling episodes of sheep under different treatmentsa during a 10-day weaning period Treatment
Food intake—ewe (kg concentrate/day)
Food intake—lamb (kg concentrate/day)
No. of visits to the creep feeder per 15 h observation periods/day
No. of suckling (episodes per hour)
Time spent suckling or attempting to suckle during each suckling episode (seconds)
1 2 3 4
1.3 F 0.3 1.4 F 0.2 1.3 F 0.2 1.4 F 0.2
0.6 F 0.2 0.6 F 0.3 0.7 F 0.3 0.8 F 0.3
11.7 F 1.8b 12.2 F 1.9b 13.1 F 2.2ab 15.3 F 2.1a
3.4 F 0.5a 1.1 F 1.0b 1.7 F 1.2b
105.3 F 16.3a 5.3 F 6.3b 16.1 F 12.3b
Values followed by different letters in each column differ among treatments ( P < 0.05). a Treatment 1—lambs not separated, able to suckle; Treatment 2—lambs not separated, udder smeared with faeces; Treatment 3—lambs not separated, udder covered; Treatment 4—lambs separated by wire.
262
A. Orihuela et al. / Livestock Production Science 87 (2004) 259–264
Fig. 1. Total number of vocalizations of ewes and lambs among treatments during the first 3 days after weaning.
20%, respectively). None of them being rejected by their mothers.
4. Discussion Previous studies (Owen et al., 1969a,b) have concluded that the transition from initiation of eating to substantial consumption of solid feed is strongly influenced by milk intake. Restriction of milk intake causes an early acceleration in solid feed consumption. Furthermore, according to Orskov et al. (1973) a lamb weaned before 2 months of age undergoes a reduction in live-weight gain when the energy intake is well below that of lambs maintained on full liquid feeding. In the present study, restriction of milk intake did not cause an increase in solid food intake. In addition, although lambs separated from their mothers (treatment
four) visited the creep feeding area more frequently than animals in treatments one and two, live weight gain and voluntary food intake did not differ significantly, suggesting that the rumens in the trial lambs had developed sufficiently such that they did not require milk for their nutritional well-being. Therefore, suckling response could be interpreted purely as a reinforcement of the mother – young bond. Under these conditions, similar results may be observed in other ruminants and possibly even other species. In practical terms, under the conditions of the present experiment, productivity may not be affected by treatments, perhaps because 10-week-old lambs had no further need of their mother as a food source. Further research is needed because different results could be observed when dealing with younger lambs. Parrot et al. (1988) found that pronounced physiological stress increases cortisol levels. However, in the present experiment, no differences were found in
A. Orihuela et al. / Livestock Production Science 87 (2004) 259–264
this hormone concentration within treatments, or in comparison with the control group. The results confirm that discouraging lambs that are not dependent on their mother as a food source from suckling was not stressful to the lamb. Perhaps the presence of the mother reduces the impact in the lamb, as the presence of other conspecifics in a group-feeding situation has proved to reduce the stress of weaning or isolation (Barton, 1983a,b; Carbajal and Orihuela, 2001). This is in accordance with Price et al. (2003) who reported that on the day of weaning, calves in the fence-line and control treatment vocalized less than calves totally separated from their dams. In horses, weaning by separation of mothers and foals into adjacent corrals for 1 week so that the foals can see and hear their mother but cannot make direct contact (or suckle), appears to be less stressful than methods in which the mare cannot be seen, probably because weaning is more gradual (McCall et al., 1985). Also Haley et al. (2001) found that termination of milk feeding and segregation of cow – calf pairs are distinct components of weaning that contribute in different ways to the response of the calves, concluding that separating these two factors may better simulate the natural process and reduce weaning distress. Mother – young interactions during the weaning process may have other complex effects on behaviour. Selman et al. (1970) found that calves kept with their dams but muzzled between meals have higher immune globulin concentrations than calves allowed to suckle for the same time but separated from their mothers between sucklings. The finding that lambs in treatment two and those in treatment three spent similar time suckling or attempting to suckle and performed the same number of suckling episodes suggests that smearing the udder with cattle faeces is as efficient as covering the udder to discourage lambs from nursing during the weaning period. Romeyer and Bouissou (1992) found that temporary removal of a sheep from its familiar group could produce behavioural changes often indicative of distress, such as increased vocalization. The fact that no difference was found among treatments two, three and four in the number of ewe vocalizations, indicate that distress was similar in these treatments, in comparison with the control group where lambs were allowed to suckle ad libitum.
263
The finding that lambs vocalized with similar frequency in all groups could be a result of social facilitation in T1, especially during the first day of the experiment, when the highest vocalization frequency in this group was observed. Lambs in this group may vocalize in response to lambs in other treatments, as they were able to hear each other. The reduction in vocalization frequency observed in T2 and T3 1 day before T4, suggests that impeding physical contact could be an additive distress effect to restricting suckling. The behavioural effects of the imposed treatments in terms of attempting to break the mother – young bond were independent of a need to derive milk for the nutritional well-being of the lamb. The finding that some lambs attempt to suckle after 10 days of treatment, regardless of the treatment assigned, suggests that a 10-day treatment period was not enough to break the social mother – young bond in all ewe – lamb pairs. Longer periods or more drastic treatments like ewe lamb complete separation with no visual or audible contact may be necessary to induce total independence from the mother as a social companion.
5. Conclusion It was concluded that restricting 10-week-old lambs from suckling during a 10-day treatment period induced a minor short-term distress and the break of the social bond in 70– 80% of the ewe – lamb pairs.
Acknowledgements Financial assistance was provided by the University of the State of Morelos, Mexico.
References Aoyama, M., Dohi, H., Shioya, S., Takeuchi, Y., Mori, Y., Odubo, T., 1994. Feeding-deterrent substance in cattle faeces: its effects on ingestive behavior in goats. Appl. Anim. Behav. Sci. 40, 253 – 262. Barton, M.A., 1983a. Behaviour of group-reared calves on acid milk replacer. Appl. Anim. Ethol. 11, 77 – 79. Barton, M.A., 1983b. The effects of management and behavioural
264
A. Orihuela et al. / Livestock Production Science 87 (2004) 259–264
factors on intake of acidified milk and concentrates by groupreared calves. Anim. Prod. 36, 512 – 519. Carbajal, S., Orihuela, A., 2001. Minimal number of peers needed to minimize the stress response of isolated sheep. J. Appl. Anim. Welf. Sci. 4, 249 – 255. Dohi, H., Yamada, A., Entsu, S., 1991. Cattle feeding deterrents emitted from cattle faeces. J. Chem. Ecol. 17, 1197 – 1203. Fraser, A.F., Broom, D.M., 1998. Farm Animal Behaviour and Welfare, 2nd ed. Cab International, UK, p. 244. Gill, L.J., 1978. Design and Analysis of Experiments in the Animal and Medical Sciences. The Iowa State University Press, Ames, pp. 135 – 152. Haley, D.B., Stookey, J.M., Clavelle, J.L., Watts, J.M., 2001. The simultaneous loss of milk and maternal contact compounds distress at weaning in beef calves. Proceedings of the 35th International Congress of the International Society for Applied Ethology. The Center for Animal Welfare, UC Davis, USA, p. 41. Houpt, K.A., 1988. Domestic Animal Behaviour for Veterinarians and Animal Scientists, 3rd ed. Iowa State Univ. Press, Ames, p. 197. Lott, D., Hart, B., 1979. Applied ethology in a nomadic cattle culture. Appl. Anim. Ethol. 5, 309 – 319. McCall, C.A., Salters, M.A., Simpson, M., 1985. Locomotor, vocal and other behavioural responses to varying methods of weaning foals. Appl. Anim. Behav. Sci. 14, 27 – 35.
Orskov, E.R., Fraser, C., Gill, J.C., 1973. A note on the effect of time of weaning and weight at slaughter on feed utilisation of intensively fed lambs. Anim. Prod. 16, 311 – 315. Owen, J.B., Davies, D.A.R., Ridgman, W.J., 1969a. Effects of varying the quantity and distribution of liquid feed in lambs reared artificially. Anim. Prod. 2, 1 – 9. Owen, J.B., Davies, D.A.R., Ridgman, W.J., 1969b. The control of voluntary food intake in ruminants. Anim. Prod. 2, 511 – 512. Parrot, 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. Price, E.O., Harris, J.E., Borgwardt, R.E., Sween, M.L., Connor, J.M., 2003. Fenceline contact of beef calves with their dams at weaning reduces the negative effects of separation on behavior and growth rate. J. Anim. Sci. 81, 116 – 121. Romeyer, A., Bouissou, M.F., 1992. Assessment of fear reactions in domestic sheep, and influence of breed and rearing conditions. Appl. Anim. Behav. Sci. 34, 93 – 111. Selman, I.E., Mc Ewan, A.D., Fisher, E.W., 1970. Studies on natural suckling in cattle during the 1st eight hours post partum: II. Behavioural studies (calves). Anim. Behav. 18, 284 – 289. Siegel, S., Castellan, N.J., 1988. Nonparametric Statistics for the Behavioral Sciences, 2nd ed. McGraw-Hill, New York. 399 pp. Sua´rez, E., Orihuela, A., 2002. The effect of exposure to feces from four farm species on the avoidance behaviour and feed consumption of sheep. Livest. Prod. Sci. 77, 119 – 125.