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Behavioural response of grazing lambs to changes associated with feeding and separation from their mothers at weaning
Research in Veterinary Science 95 (2013) 913–918
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Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Behavioural response of grazing lambs to changes associated with feeding and separation from their mothers at weaning J.P. Damián a,⇑, M.J. Hötzel b, G. Banchero c, R. Ungerfeld d a
Departamento de Biología Molecular y Celular, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay Laboratório de Etologia Aplicada e Bem-Estar Animal, Departamento de Zootecnia e Desenvolvimento Rural, Universidade Federal de Santa Catarina, Florianópolis, Brazil c Unidad de Ovinos, INIA ‘‘La Estanzuela’’, Colonia, Uruguay d Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay b
a r t i c l e
i n f o
Article history: Received 9 February 2013 Accepted 2 August 2013
a b s t r a c t This study aimed to determine which behaviours were provoked in lambs in response to the separation from their dams or to the changes associated with feeding and separation from adults at weaning. Fourteen lambs were separated from their dams at 24–36 h after birth and artificially reared (AR) in presence of four adult ewes, while another 13 lambs remained with their dams from birth (DR). At 75 days of age on average (day 0) DR lambs were separated from their dams and AR lambs no longer received sheep’s milk and were separated from adults. Behaviours were recorded every 10 min (6 h per day) from day 3 to day 4. We observed an increase (p < 0.05) in pacing behaviour, as well as in the frequency in which lambs were observed vocalizing, walking and staying under shade, and a decrease (p < 0.05) in the frequency of grazing in the DR group in comparison to AR at weaning, but there were no differences in body weight gain from day 4 to day 5 after weaning. Additionally, we observed a decrease in the frequency in which lambs were observed standing and grazing (p < 0.05), and an increase in vocalizing and staying under shade (p < 0.05) in group AR at weaning in comparison to the previous days. Therefore, it was concluded that although some specific behaviours as pacing or vocalizing were clearly related with the separation from the mother at weaning, the change of food and separation from adults must be also considered as an important stressor in grazing lambs at weaning. In addition, the provision of shade when grazing is also important for lambs at the time of weaning. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Mother-offspring bond Stress Vocalizations Pacing Sheep
1. Introduction Natural weaning involves a progressive reduction in milk ingestion and an increase in solid feed intake, in addition to the acquisition of gradual social independence of the offspring (Arnold et al., 1979). In contrast, under some farming conditions, lambs are abruptly separated from the mother before the end of that process (see reviews: Napolitano et al., 2008; Newberry and Swanson, 2008) and the severance of the ewe-lamb bond at weaning triggers a stress response in both (Orgeur et al., 1998). Several factors influence stress in lambs after weaning, including social stressors (e.g. separation from their dam and regrouping with new animals), nutritional changes (the end of milk intake and access exclusively to solid food), and the end of access to the udder, and cessation of suckling behaviour (see reviews: Napolitano et al., 2008; Weary et al., 2008). Lambs prevented from suckling their dam one week prior to separation vocalized less than lambs that ⇑ Corresponding author. Tel.: +598 26221195; fax: +598 26280130. E-mail addresses: (J.P. Damián).
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0034-5288/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.rvsc.2013.08.001
were weaned abruptly (Schichowski et al., 2008), demonstrating the importance of the end of suckling, the loss of milk and the change in feeding in the lamb’s response to permanent separation. Similarly, two-step weaning managements with nose flaps in cattle, which prevent calves from suckling, reduce behaviours indicative of stress commonly observed after abrupt weaning, such as pacing and vocalising (Enríquez et al. 2010; Hötzel et al. 2012). The cessation of suckling partly explains the stress responses generated at weaning. On the other hand, no efforts have been made to determine the relative importance of changes associated with modifications in feeding (the loss of access to the udder, suckling and milk, and the change to a solid diet and water) and the loss of the mother on the behavioural changes displayed by lambs after weaning. The hypothesis of the present study was that the separation from their mother causes the greatest changes in behaviour of lambs at weaning, and that the changes associated with feeding and separation from adults represents an additional stressor. Our aim was to determine which behaviours displayed by lambs at weaning are caused in response either to changes associated with feeding or by the separation from their mother. The behavioural changes observed in lambs abruptly weaned, were compared with
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those observed in lambs separated from their dams since 24–36 h of age and reared with sheep milk in artificial udders and in the presence of four adult ewes. 2. Materials and methods 2.1. Location, animals and treatments The study was conducted at the Unidad Experimental de Ovinos, INIA La Estanzuela, Uruguay (34°190 S 57°400 E), from September to December 2011. The experimental procedures were approved by the Comisión Honoraria de Experimentación Animal (CHEA)-Universidad de la República (Uruguay). Twenty-seven male Polwarth lambs, sired by three rams and born as singles within 12 days of each other were used. Before lambing, the dams were handled in the same paddock and maintained under the same conditions. Lambing was carefully recorded 3–4 times day1, both members of the dyad were identified, and lambs were tagged. Lambs were assigned to two experimental groups according to lambing day and body weight at birth: (1) artificially reared lambs (AR group, n = 14) were separated from their dams at 24–36 h after birth; (2) dam-reared lambs (DR group, n = 13) remained with their dams until 75 days of age. 2.2. Management of artificially reared lambs Artificially reared lambs suckled sheep milk from artificial teats. The amount of milk was adjusted to maintain a body weight similar to that of DR lambs. Ewes from the same flock were milked, and milk was provided to lambs in a frequency similar to that of natural suckling. During the first seven days of age 0.5– 0.7 L lamb1 day1 of milk was provided 6 times day1 at 8, 10, 12, 14, 16 and, 19 h. From day 8 to day 15 of age 0.8–1.0 L lamb1 day1 of milk were provided four times daily at 8, 12, 16 and 19 h. From 16 days of age until weaning, milk was provided three times a day at 8, 12 and 19 h. From day 16 to day 30 they received 1.0– 1.3 L lamb1 day1, and from day 31 to day 75 of age, lambs received 1.4–1.6 L lamb1 day1. During feeding AR lambs had only minimum contact with humans. During the first 15 days of age all lambs were housed in two closed pens during the night at 20–23 °C. From then on, the two groups were handled in different paddocks of 25 m 50 m each. Lambs had free access to an artificial shadow of shade cloth supported by iron quadrants (surface of 4.5 m2 0.8 m height) and a piece of wood (0.2 m high 0.2 m 2 m), placed in the paddock where lambs could use it to play. Four adult ewes bearing single lambs were introduced to the AR group to avoid the potential confounding effect of the absence of adult ewes in this group, which grew up without mothers. All lambs received solid ration after 20 days of age, grazed on improved pastures, and had free access to water.
associated with feeding and the presence of other adult animals (the loss of access to the udder, suckling and milk, and the change to a solid diet and water). Therefore, changes in behaviour of the AR group are assumed to be provoked by the changes associated with feeding and separation from adults. Both groups were weighed on day 4 (AR: 25.6 ± 0.4 kg vs. DR: 24.3 ± 0.7 kg) (mean ± SEM) and on day 5. The evolution of body weight of lambs from birth to nine weeks of age is shown in Fig. 1. 2.4. Behavioural recordings On day 4 all lambs were identified with numbers painted on both body sides of the body. Behaviours of individual lambs were recorded while lambs remained in their paddocks, using instantaneous sampling every 10 min, performed by two observers, simultaneously in each group. The observers were located (under a parasol) always in the same position relative to the paddock (lateral) more than 30 m far from the fence line where the separation with the adult ewes was performed, on the opposite side. Data were recorded 38 times day1 during two observation periods (8–11 h; 17–20 h), from day 3 to day 4. The behaviours observed are described in Table 1. Vocalizations were recorded during 30 s every 10 min using 0/1 sampling (Lehner, 1996), as previously described in Enríquez et al. (2010). 2.5. Temperature, relative humidity, heliophany and precipitation Temperature, relative humidity, heliophany (number of hours of direct sunlight in the field) and precipitation during the period of behavioural observation were obtained from Grupo Agroclima y Sistemas de Información (GRAS) (INIA, La Estanzuela, Colonia, Uruguay) (Table 2). There were no precipitations during the recorded period. 2.6. Statistical analysis Frequencies of each behaviour, expressed as percentages of total observations, were compared with the mixed model of SAS (2003; SAS Institute, Cary, NC, USA). The model considered the group (AR or DR), time (day), and the interaction between group and time as fixed effects, and the lamb into each group as a random effect. Post hoc comparisons were performed with least significant difference (LSD). The data recorded from day 3 to day 1 were averaged and considered as a single value for the analysis, and are presented as a general mean of days before weaning (DBW). Body weight gain of AR and DR between day 4 and day 5 were compared with an ANOVA. The correlation between the mean temperature value during the observation period in each day and the
30
At 07:30 h of day 0, when lambs were on average 75 days old (69–81 days of age), dams from DR lambs and the four ewe-lamb dyads that remained with AR lambs were moved to a paddock located more than 500 m of distance, where there was a flock of more than 100 sheep, without visual, chemical, or acoustic communication with the experimental lambs. At the same time, the AR lambs no longer received milk. Therefore, lambs from both groups also lost the presence of adult animals on day 0: AR lambs the adult ewes that were originally introduced, and DR lambs the mothers of the other lambs. Therefore, on day 0 the DR group lost their dams and the other adult ewes, and the AR group the changes
Body Weight (Kg)
25
2.3. Weaning
20 15 10 5 0 0
1
2
3
4 5 Time (week)
6
7
8
9
Fig. 1. Body weight of lambs reared with their dams (DR: –h–) or artificially reared (AR: –d–) from birth until nine weeks of age. Data are presented as mean ± SEM.
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J.P. Damián et al. / Research in Veterinary Science 95 (2013) 913–918 Table 1 List of behaviours observed and their respective descriptions. Behaviour
Descritpion
Lying Standing Staying under shade Walking Grazing
Lying down in any resting position Maintaining an upright position on extended legs Lambs under shade
Drinking water Playing with objects Pacing Vocalizations
All four legs are moved with head raised or not Picking or consuming pasture, with the head above ground, still or moving slowly Mouth below the waterline in the trough ingesting water Lambs observed nuzzling, running or jumping on a log of wood and nuzzling objects of shade cloth with its head without any apparent function Repetitive rapid walk parallel to the fence Making oral sounds
Table 3 Effect of day, group and the interaction between day and group (Day ⁄ Group) on the behaviours of lambs at weaning. DR: lambs reared with their dams; AR: lambs artificially reared. Values for groups (recorded during six days) are the mean percentage of observations ± SEM. Behaviour
Lying Standing Staying under shade Walking Grazing Drinking water Playing with objects Pacing Vocalizations
Group
p value
DR
AR
Day
Group
Day ⁄ Group
20.7 ± 1.1 69.7 ± 1.2 19.2 ± 2.9
17.5 ± 1.0 77.3 ± 1.1 18.1 ± 2.8
<0.0001 <0.0001 <0.0001
0.049 <0.0001 ns
0.077 ns 0.04
8.2 ± 0.5 64.1 ± 1.3 1.2 ± 0.4 0.6 ± 0.4
5.2 ± 0.5 71.6 ± 1.3 0.8 ± 0.3 0.5 ± 0.3
<0.0001 <0.0001 ns 0.0003
0.0003 0.0004 ns ns
<0.0001 0.0007 ns ns
2.0 ± 0.3 9.3 ± 0.5
0.0 ± 0.3 2.9 ± 0.6
<0.0001 <0.0001
<0.0001 <0.0001
<0.0001 <0.0001
ns: non significant. Table 2 Ambient temperature (°C), relative humidity (%) and heliophany (h) during the days of behavioural observations. Days
DBW 0 1 2 3 4
Relative humidity (%)
Heliophany (h)
Mean
Temperature (°C) Min
Max
Mean
Mean
20.3 23.4 22.0 21.8 23.9 22.1
13.3 17.6 18.6 16.1 16.9 16.5
24.9 28.6 23.9 26.3 28.8 25.5
73.7 69.0 70.5 68.7 65.7 79.2
12.5 9.8 11.9 11.6 12.9 13.0
DBW: mean data recorded the three days before weaning.
frequency of observations in which lambs were under shade each day (considering all the lambs, regardless of group), as well as the correlation between heliophany value per day and the frequency of observations in which lambs were under shade each day was tested using Spearman’s rank correlation. Results were considered significant at a = 0.05; data are presented as mean ± SEM.
3.2.2. Standing The frequency in which lambs were observed standing was greater in AR than DR lambs (p < 0.0001) (Table 3). The frequency of lambs standing decreased significantly from DBW to day 0 (p = 0.0001), when the lowest value was observed (Fig. 2B). After day 0 the frequency of lambs observed standing increased significantly until day 2 (p < 0.0001), when the greatest value was observed (Fig. 2B). The frequency of this behaviour decreased from day 2 to days 3 and 4 (p < 0.0001), when it returned to values similar to those recorded before weaning. 3.2.3. Staying under shade The frequency of observations in which lambs were under shade increased significantly from DBW to day 0 (p < 0.0001), decreased on days 1 and 2 (p < 0.0001), and increased again on days 3 and 4 (p < 0.0001) (Fig. 2C). On day 0 DR lambs were observed staying under shade in greater frequency than AR (p = 0.006) (Fig. 2C). The frequency of observations in which lambs were under shade was positively correlated with temperature (rs = 0.89, p = 0.02), but unrelated to heliophany (rs = 0.54, p = 0.27).
3. Results 3.1. Body weight gain Body weight gain from day 4 to day 5 was similar between AR and DR lambs (2.5 ± 0.3 kg vs. 2.1 ± 0.4 kg, respectively, p = 0.4). 3.2. Behaviours The main effects of time, group and interactions between time and group for all recorded behaviours are presented in Table 3. All behaviours except drinking water changed with time (p < 0.001). There was an effect of the group for lying (p = 0.049), standing (p < 0.0001), walking (p = 0.0003), grazing (p = 0.0004), pacing (p < 0.0001) and vocalizations (p < 0.0001). Walking (p < 0.0001), grazing (p = 0.0007), staying under shade (p = 0.04), pacing (p < 0.0001) and vocalizations (p < 0.0001) showed an interaction between time and group, and the interaction tended to be significant (p = 0.077) in the frequency in which lambs were observed lying. 3.2.1. Lying The frequency of lambs lying was greater in DR than in AR lambs (p = 0.049) (Table 3). The frequency of lambs lying decreased from day 0 to days 1 and 2 (p < 0.01), and then increased, reaching its maximum value on day 4 (p < 0.0001) (Fig. 2A).
3.2.4. Walking Lambs reared by their mothers were observed more times walking than AR lambs (p = 0.0003) (Table 3). The frequency of lambs walking increased significantly from DBW to day 0 (p < 0.0001), when the greatest frequency was observed (Fig. 2D). The frequency of lambs walking decreased significantly from day 0 to day 1 (p < 0.0001), returning on day 2 to values similar to those observed DBW. The frequency of this behaviour continued decreasing and reached the lowest values on days 3 and 4 (p < 0.0001). Lambs reared by their mothers presented a greater frequency of walking than AR lambs on day 0 (p < 0.0001), 1 (p = 0.02) and 2 (p = 0.006) (Fig. 2D). 3.2.5. Grazing The frequency in which lambs grazed was greater in the AR than in the DR group (p = 0.0004) (Table 3). The frequency of lambs grazing decreased significantly from DBW to day 0 (p < 0.0001), then increased to its maximum value on day 2 (p < 0.0001), and decreased again from day 2 to day 4 (p < 0.0001) (Fig. 2E). The frequency of grazing on days 0 (p < 0.0001), 2 (p = 0.002) and 4 was greater in DR than in AR lambs (p = 0.019) (Fig. 2E). 3.2.6. Drinking water The frequency in which the lambs were observed drinking water was not affected by group (AR: 0.8 ± 0.17 % vs. DR:
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(A)
a
a
b
b
ac
(D)
c
35 30
b
c
a
c
25 20 15
15
*
**
10
10 5
5
0
0
(B) 95
a
***
20
Walking (%)
Lying (%)
a 25
DBW
0
1
2
3
4
a
b
a
c
a
a
(E)
x
x
w
w
w
w
DBW
0
1
2
3
4
b
c
c
ad
d
a
100 ** 90
65 55
60 50 40 30
0
ac
b
35
1
2
a
c
3
bd
4
d
**
30 25 20 15 10 5
w
x
w
w
xy
y
DBW
0
1
2
3
4
*
70
35 DBW
***
80
45
(C) Staying under shade (%)
Grazing (%)
75
(F) Playing with objects (%)
Standing (%)
85
w
x
y
z
wx
wx
DBW
0
1
2
3
4
a
a
b
b
b
ab
2
3
4
2 1.6 1.2 0.8 0.4 0
0
DBW
Time (d)
0
1
Time (d)
Fig. 2. Frequency in which lambs were observed (A) lying, (B) standing, (C) staying under shade, (D) walking, (E) grazing, (F) playing with objects in lambs reared with their dams (DR: –h–) or artificially reared (AR: –d–). The arrow indicates the day of weaning. DBW: mean data recorded 3 days before weaning. Data are presented as mean frequency ± SEM. Different letters indicate significant differences (p < 0.05) between days. In variables with an interaction between group and time (staying under shade, walking and grazing) the effect of time (day) into each group is indicated with different letters (p < 0.05): a, b, c, and d for DR and w, x, y, and z for AR lambs. Significant differences between DR and AR in the same day are indicated as: ⁄p < 0.05; ⁄⁄p < 0.01; and ⁄⁄⁄p < 0.001.
1.1 ± 0.18 %; p = 0.16), time (p = 0.56), or their interaction (p = 0.34) (Table 3).
3.2.7. Playing with an object The frequency of lambs playing with an object decreased from day 0 to day 1 (p = 0.0002) and remained low until day 3 (Fig. 2F).
3.2.8. Pacing The frequency in which lambs were observed pacing was greater in the DR than in the AR group (p < 0.0001) (Table 3). The frequency of lambs pacing increased from DBW to day 0 (p < 0.0001), when the greatest frequency was observed (Fig. 3A). After day 0 the frequency of lambs pacing decreased significantly and returned to values similar to DBW (p < 0.0001), remaining low (day 1: 1.27 ± 0.29 %, day 2: 0.10 ± 0.09 %, and day 3: 0.0 ± 0.0 %) until day 4 (0.0 ± 0.0 %) (Fig. 3A). Lambs reared by their mothers had a greater increase in their pacing frequency on days 0 (p < 0.0001) and 1 (p = 0.013) than AR lambs (Fig. 3A).
3.2.9. Vocalizations The frequency in which lambs were observed vocalizing was greater in the DR than in the AR group (p < 0.0001) (Table 3). The frequency of vocalizations increased significantly from DBW to day 0 (p < 0.0001), when the frequency peaked (Fig. 3B). On day 1 the frequency of lambs vocalizing decreased significantly (p < 0.0001), returning to values similar to those observed DBW on day 2, and remaining low until Day 4. The frequency of observations in which DR lambs were observed vocalizing was greater than in AR lambs on days 0 (p < 0.0001) and 1 (p = 0.0015) (Fig. 3B). 4. Discussion Separation from the dam at weaning is an important stressor of lambs, as was evidenced by the greater increase in the frequencies of pacing, vocalizing, walking and staying under shade, and greater decrease in the frequency of grazing in lambs that were reared with their dams compared with those reared without the mother. However, the effect of separation from the mother was not enough
J.P. Damián et al. / Research in Veterinary Science 95 (2013) 913–918
(A)
a
b
c
a
a
a
14
***
Pacing (%)
12 10 8 6
*
4 2
w
w
w
w
w
w
DBW
0
1
2
3
4
a
b
a
a
0
(B)
c
a
50
Vocalizations (%)
*** 40 30 20
** 10
w
y
DBW
0
xy
xy
w
wx
2
3
4
0 1
Time (d) Fig. 3. Frequency in which lambs were observed (A) pacing and (B) vocalizations of lambs reared with their dams (DR: –h–) and those artificially reared (AR: –d–). The arrow indicates the day of weaning. DBW: mean data recorded 3 days before of weaning. Data are presented as mean frequency ± SEM. The effect of time (day) into each group is shown with different letters (p < 0.05): a, b, c, and d for DR and w, x y and z for AR lambs. Significant differences between DR and AR in the same Day are indicated as: ⁄: p < 0.05, ⁄⁄: p < 0.01 and ⁄⁄⁄: p < 0.001.
to cause differences in body weight gain. Behavioural changes were also observed in AR lambs after weaning; but these changes, which were probably associated with the changes of feeding (i.e. loss of milk and change of feeding to solid diet and water) and separation from adults resulted in a reduced behavioural response compared to that observed in lambs that were also separated from their mothers. The presence of adult ewes with their lambs in the AR group (although could interfere in the final results by adding a social factor to the change in feeding management) avoided the possible negative influence of the lack of other mother-young dyads into the group, although no studies have been carried out addressing this question. When the response of both groups is compared, AR lambs did not pace, rarely vocalised, and displayed practically no changes in walking frequency. On the other hand, DR lambs were observed vocalising approximately 40% of the time and pacing approximately 10% of the time, and displayed a fourfold increase in walking frequency, specially on day 0 and day 1, suggesting that lambs were seeking their dams. Based on these results we reinforce the suggestion of Napolitano et al. (2008) and Newberry and Swanson (2008) that walking and vocalizing at weaning are behaviours directed at searching for the dam. Moreover, pacing, only observed in DR lambs, occurred alongside the fence where the dams were taken out at separation, suggesting that the lambs were searching for the dam. The observers were located more than 30 m far from the fence line where the separation was performed, and located on the opposite margins, so no effect on avoidance or approaching behaviour could produce those movements. In addition, observers were always located in the same position relative to the paddock, and the previous days (before weaning) lambs did not show pacing
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behaviour, confirming that observers did not interfere with the expression of this behaviour. Grazing frequency also decreased more in DR than AR lambs at weaning. Studying weaning behaviour in calves, Hötzel et al. (2010) suggested that the reduction in grazing observed at weaning could be associated with physiological or emotional changes triggered by the interruption of suckling. The differences in grazing behaviour observed between the two groups of lambs in this study at weaning supports the interpretation of an emotional response to the separation from the dam. Lambs reared by their dams showed a greater increase in the frequency of resting under the shade during the first day of weaning than artificially reared lambs. This differential behavioural response may be a strategy to seek protection, triggered by the loss of their dams. As reported in wild ruminants (Coss, 1991; Wiedenmayer, 2009), resting in the shade during the day of weaning could be an antipredator behaviour of lambs. The increase in the frequency of observations in which lambs from both groups were under shade on the day of weaning might also be explained by an increase in ambient temperature, as was evidenced by the high correlation between these two variables. However, the frequency of observations in which lambs were under shade not was correlated with heliophany. Therefore, temperature seems to have greater importance than direct sunlight. As high temperatures and humidity are important stressors for animals reared in open paddocks (Silanikove, 2000), the provision of shade contributes to maintain homeostasis and improves animal welfare (Sevi et al., 2001; Schütz et al., 2008). In brief, providing lambs with shelters may be useful to decrease the negative effects of weaning on lambs welfare. Lambs of both groups stopped playing after weaning. This result is consistent with reports in which it was observed that calves stop playing at weaning (Enríquez et al., 2010; Krachun et al., 2010; Hötzel et al., 2012) and lambs stop playing after castration (Thornton and Waterman-Pearson, 2002). Play has been suggested as a positive indicator of animal welfare (Boissy et al., 2007; Held and Špinka, 2011), therefore it might be concluded that the loss of access to milk, suckling and social separation from adults was stressful not only for DR, but also for AR lambs. The reduction in energy intake associated with weaning was offered as one explanation for the reduction of playing activity in dairy calves (Krachun et al., 2010). However, three months after having worn nose-flap antisucking devices, weaned beef calves still played less than control calves of the same age (Hötzel et al., 2012). As nutritional conditions and body weight were similar between the two groups of calves, the energy intake did not seem to explain the differences in the frequency of playing, suggesting an emotional or cognitive response. In conclusion, the current study shows that the loss of the dam is an important stressor, and that this loss plays a key role in the behavioural response to weaning in lambs. Pacing behaviour, as well as an increase in the frequency of vocalizing, walking and staying under shade, and a decrease in the frequency of grazing frequency are provoked by the separation from their dam at weaning in grazing lambs. Additionally, the changes associated with feeding and separation from adults are also an important component of the stress response to weaning. Finally, this study highlights the importance of providing shelter or shade to the lambs at the time of weaning in grazing conditions.
5. Conflict of interest None of the authors has any financial or personal relationship that could inappropriately influence in the content of the paper.
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Acknowledgements We thank Maria Jesus Ramírez, Laura Morena and Florencia Beracochea for their help in behavioural recordings, and Damián González, Alberto Garcia, Sofía Moraes and Nestor Sanguinetti de la Unidad Experimental de Ovinos, INIA La Estanzuela, for taking care of the animals. Financial support: Agencia Nacional de Investigación e Innovación (FCE2626-ANII). MJH was funded by CNPq, Brazil (Proc. 200792/2011-3).
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Hötzel, M.J., Quintans, G., Ungerfeld, R., 2012. Behaviour response to two-step weaning is disminished in beef calves previously submitted to temporary weaning with nose-flap. Livestock Production Science 149, 88–95. Krachun, C., Rushen, J., de Passillé, A.M., 2010. Play behavior in dairy calves is reduced by weaning and by a low energy intake. Applied Animal Behaviour Science 122, 71–76. Lehner, P.N., 1996. Handbook of ethological methods, 2nd edition. Cambridge University Press, Cambridge, UK. Napolitano, F., De Rosa, G., Sevi, A., 2008. Welfare implications of artificial rearing and early weaning in sheep. Applied Animal Behaviour Science 110, 58–72. Newberry, R.C., Swanson, J.C., 2008. Implications of breaking mother–young social bonds. Applied Animal Behaviour Science 110, 3–23. Orgeur, P., Mavric, N., Yvore, P., Bernard, S., Nowak, R., Schaal, B., Levy, F., 1998. Artificial weaning in sheep: consequences on behavioural, hormonal and immuno-pathological indicators of welfare. Applied Animal Behaviour Science 58, 87–103. Schichowski, C., Moors, E., Gauly, M., 2008. Effects of weaning lambs in two stages or by abrupt separation on their behavior and growth rate. Journal of Animal Science 86, 220–225. Schütz, K.E., Cox, N.R., Matthews, L.R., 2008. How important is shade to dairy cattle? Choice between shade or lying following different levels of lying deprivation. Applied Animal Behaviour Science 114, 307–318. Sevi, A., Annicchiarico, G., Albenzio, M., Taibi, L., Muscio, A., Dell’Aquila, S., 2001. Effects of solar radiation and feeling time on behavior, immune response and production of lactating ewes under high ambient temperature. Journal of Dairy Science 84, 629–640. Silanikove, N., 2000. Effects of heat stress on the welfare of extensively managed domestic ruminants. Livestock Production Science 67, 1–18. Thornton, P.D., Waterman-Pearson, A.E., 2002. Behavioural responses to castration in lambs. Animal Welfare 11, 203–212. Weary, D.M., Jasper, J., Hötzel, M.J., 2008. Understanding weaning distress. Applied Animal Behaviour Science 110, 24–41. Wiedenmayer, C.P., 2009. Plasticity of defensive behavior and fear in early development. Neuroscience and Biobehavioral Reviews 33, 432–441.
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Research in Veterinary Science journal homepage: www.elsevier.com/locate/rvsc
Behavioural response of grazing lambs to changes associated with feeding and separation from their mothers at weaning J.P. Damián a,⇑, M.J. Hötzel b, G. Banchero c, R. Ungerfeld d a
Departamento de Biología Molecular y Celular, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay Laboratório de Etologia Aplicada e Bem-Estar Animal, Departamento de Zootecnia e Desenvolvimento Rural, Universidade Federal de Santa Catarina, Florianópolis, Brazil c Unidad de Ovinos, INIA ‘‘La Estanzuela’’, Colonia, Uruguay d Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay b
a r t i c l e
i n f o
Article history: Received 9 February 2013 Accepted 2 August 2013
a b s t r a c t This study aimed to determine which behaviours were provoked in lambs in response to the separation from their dams or to the changes associated with feeding and separation from adults at weaning. Fourteen lambs were separated from their dams at 24–36 h after birth and artificially reared (AR) in presence of four adult ewes, while another 13 lambs remained with their dams from birth (DR). At 75 days of age on average (day 0) DR lambs were separated from their dams and AR lambs no longer received sheep’s milk and were separated from adults. Behaviours were recorded every 10 min (6 h per day) from day 3 to day 4. We observed an increase (p < 0.05) in pacing behaviour, as well as in the frequency in which lambs were observed vocalizing, walking and staying under shade, and a decrease (p < 0.05) in the frequency of grazing in the DR group in comparison to AR at weaning, but there were no differences in body weight gain from day 4 to day 5 after weaning. Additionally, we observed a decrease in the frequency in which lambs were observed standing and grazing (p < 0.05), and an increase in vocalizing and staying under shade (p < 0.05) in group AR at weaning in comparison to the previous days. Therefore, it was concluded that although some specific behaviours as pacing or vocalizing were clearly related with the separation from the mother at weaning, the change of food and separation from adults must be also considered as an important stressor in grazing lambs at weaning. In addition, the provision of shade when grazing is also important for lambs at the time of weaning. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Mother-offspring bond Stress Vocalizations Pacing Sheep
1. Introduction Natural weaning involves a progressive reduction in milk ingestion and an increase in solid feed intake, in addition to the acquisition of gradual social independence of the offspring (Arnold et al., 1979). In contrast, under some farming conditions, lambs are abruptly separated from the mother before the end of that process (see reviews: Napolitano et al., 2008; Newberry and Swanson, 2008) and the severance of the ewe-lamb bond at weaning triggers a stress response in both (Orgeur et al., 1998). Several factors influence stress in lambs after weaning, including social stressors (e.g. separation from their dam and regrouping with new animals), nutritional changes (the end of milk intake and access exclusively to solid food), and the end of access to the udder, and cessation of suckling behaviour (see reviews: Napolitano et al., 2008; Weary et al., 2008). Lambs prevented from suckling their dam one week prior to separation vocalized less than lambs that ⇑ Corresponding author. Tel.: +598 26221195; fax: +598 26280130. E-mail addresses: (J.P. Damián).
[email protected],
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0034-5288/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.rvsc.2013.08.001
were weaned abruptly (Schichowski et al., 2008), demonstrating the importance of the end of suckling, the loss of milk and the change in feeding in the lamb’s response to permanent separation. Similarly, two-step weaning managements with nose flaps in cattle, which prevent calves from suckling, reduce behaviours indicative of stress commonly observed after abrupt weaning, such as pacing and vocalising (Enríquez et al. 2010; Hötzel et al. 2012). The cessation of suckling partly explains the stress responses generated at weaning. On the other hand, no efforts have been made to determine the relative importance of changes associated with modifications in feeding (the loss of access to the udder, suckling and milk, and the change to a solid diet and water) and the loss of the mother on the behavioural changes displayed by lambs after weaning. The hypothesis of the present study was that the separation from their mother causes the greatest changes in behaviour of lambs at weaning, and that the changes associated with feeding and separation from adults represents an additional stressor. Our aim was to determine which behaviours displayed by lambs at weaning are caused in response either to changes associated with feeding or by the separation from their mother. The behavioural changes observed in lambs abruptly weaned, were compared with
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those observed in lambs separated from their dams since 24–36 h of age and reared with sheep milk in artificial udders and in the presence of four adult ewes. 2. Materials and methods 2.1. Location, animals and treatments The study was conducted at the Unidad Experimental de Ovinos, INIA La Estanzuela, Uruguay (34°190 S 57°400 E), from September to December 2011. The experimental procedures were approved by the Comisión Honoraria de Experimentación Animal (CHEA)-Universidad de la República (Uruguay). Twenty-seven male Polwarth lambs, sired by three rams and born as singles within 12 days of each other were used. Before lambing, the dams were handled in the same paddock and maintained under the same conditions. Lambing was carefully recorded 3–4 times day1, both members of the dyad were identified, and lambs were tagged. Lambs were assigned to two experimental groups according to lambing day and body weight at birth: (1) artificially reared lambs (AR group, n = 14) were separated from their dams at 24–36 h after birth; (2) dam-reared lambs (DR group, n = 13) remained with their dams until 75 days of age. 2.2. Management of artificially reared lambs Artificially reared lambs suckled sheep milk from artificial teats. The amount of milk was adjusted to maintain a body weight similar to that of DR lambs. Ewes from the same flock were milked, and milk was provided to lambs in a frequency similar to that of natural suckling. During the first seven days of age 0.5– 0.7 L lamb1 day1 of milk was provided 6 times day1 at 8, 10, 12, 14, 16 and, 19 h. From day 8 to day 15 of age 0.8–1.0 L lamb1 day1 of milk were provided four times daily at 8, 12, 16 and 19 h. From 16 days of age until weaning, milk was provided three times a day at 8, 12 and 19 h. From day 16 to day 30 they received 1.0– 1.3 L lamb1 day1, and from day 31 to day 75 of age, lambs received 1.4–1.6 L lamb1 day1. During feeding AR lambs had only minimum contact with humans. During the first 15 days of age all lambs were housed in two closed pens during the night at 20–23 °C. From then on, the two groups were handled in different paddocks of 25 m 50 m each. Lambs had free access to an artificial shadow of shade cloth supported by iron quadrants (surface of 4.5 m2 0.8 m height) and a piece of wood (0.2 m high 0.2 m 2 m), placed in the paddock where lambs could use it to play. Four adult ewes bearing single lambs were introduced to the AR group to avoid the potential confounding effect of the absence of adult ewes in this group, which grew up without mothers. All lambs received solid ration after 20 days of age, grazed on improved pastures, and had free access to water.
associated with feeding and the presence of other adult animals (the loss of access to the udder, suckling and milk, and the change to a solid diet and water). Therefore, changes in behaviour of the AR group are assumed to be provoked by the changes associated with feeding and separation from adults. Both groups were weighed on day 4 (AR: 25.6 ± 0.4 kg vs. DR: 24.3 ± 0.7 kg) (mean ± SEM) and on day 5. The evolution of body weight of lambs from birth to nine weeks of age is shown in Fig. 1. 2.4. Behavioural recordings On day 4 all lambs were identified with numbers painted on both body sides of the body. Behaviours of individual lambs were recorded while lambs remained in their paddocks, using instantaneous sampling every 10 min, performed by two observers, simultaneously in each group. The observers were located (under a parasol) always in the same position relative to the paddock (lateral) more than 30 m far from the fence line where the separation with the adult ewes was performed, on the opposite side. Data were recorded 38 times day1 during two observation periods (8–11 h; 17–20 h), from day 3 to day 4. The behaviours observed are described in Table 1. Vocalizations were recorded during 30 s every 10 min using 0/1 sampling (Lehner, 1996), as previously described in Enríquez et al. (2010). 2.5. Temperature, relative humidity, heliophany and precipitation Temperature, relative humidity, heliophany (number of hours of direct sunlight in the field) and precipitation during the period of behavioural observation were obtained from Grupo Agroclima y Sistemas de Información (GRAS) (INIA, La Estanzuela, Colonia, Uruguay) (Table 2). There were no precipitations during the recorded period. 2.6. Statistical analysis Frequencies of each behaviour, expressed as percentages of total observations, were compared with the mixed model of SAS (2003; SAS Institute, Cary, NC, USA). The model considered the group (AR or DR), time (day), and the interaction between group and time as fixed effects, and the lamb into each group as a random effect. Post hoc comparisons were performed with least significant difference (LSD). The data recorded from day 3 to day 1 were averaged and considered as a single value for the analysis, and are presented as a general mean of days before weaning (DBW). Body weight gain of AR and DR between day 4 and day 5 were compared with an ANOVA. The correlation between the mean temperature value during the observation period in each day and the
30
At 07:30 h of day 0, when lambs were on average 75 days old (69–81 days of age), dams from DR lambs and the four ewe-lamb dyads that remained with AR lambs were moved to a paddock located more than 500 m of distance, where there was a flock of more than 100 sheep, without visual, chemical, or acoustic communication with the experimental lambs. At the same time, the AR lambs no longer received milk. Therefore, lambs from both groups also lost the presence of adult animals on day 0: AR lambs the adult ewes that were originally introduced, and DR lambs the mothers of the other lambs. Therefore, on day 0 the DR group lost their dams and the other adult ewes, and the AR group the changes
Body Weight (Kg)
25
2.3. Weaning
20 15 10 5 0 0
1
2
3
4 5 Time (week)
6
7
8
9
Fig. 1. Body weight of lambs reared with their dams (DR: –h–) or artificially reared (AR: –d–) from birth until nine weeks of age. Data are presented as mean ± SEM.
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J.P. Damián et al. / Research in Veterinary Science 95 (2013) 913–918 Table 1 List of behaviours observed and their respective descriptions. Behaviour
Descritpion
Lying Standing Staying under shade Walking Grazing
Lying down in any resting position Maintaining an upright position on extended legs Lambs under shade
Drinking water Playing with objects Pacing Vocalizations
All four legs are moved with head raised or not Picking or consuming pasture, with the head above ground, still or moving slowly Mouth below the waterline in the trough ingesting water Lambs observed nuzzling, running or jumping on a log of wood and nuzzling objects of shade cloth with its head without any apparent function Repetitive rapid walk parallel to the fence Making oral sounds
Table 3 Effect of day, group and the interaction between day and group (Day ⁄ Group) on the behaviours of lambs at weaning. DR: lambs reared with their dams; AR: lambs artificially reared. Values for groups (recorded during six days) are the mean percentage of observations ± SEM. Behaviour
Lying Standing Staying under shade Walking Grazing Drinking water Playing with objects Pacing Vocalizations
Group
p value
DR
AR
Day
Group
Day ⁄ Group
20.7 ± 1.1 69.7 ± 1.2 19.2 ± 2.9
17.5 ± 1.0 77.3 ± 1.1 18.1 ± 2.8
<0.0001 <0.0001 <0.0001
0.049 <0.0001 ns
0.077 ns 0.04
8.2 ± 0.5 64.1 ± 1.3 1.2 ± 0.4 0.6 ± 0.4
5.2 ± 0.5 71.6 ± 1.3 0.8 ± 0.3 0.5 ± 0.3
<0.0001 <0.0001 ns 0.0003
0.0003 0.0004 ns ns
<0.0001 0.0007 ns ns
2.0 ± 0.3 9.3 ± 0.5
0.0 ± 0.3 2.9 ± 0.6
<0.0001 <0.0001
<0.0001 <0.0001
<0.0001 <0.0001
ns: non significant. Table 2 Ambient temperature (°C), relative humidity (%) and heliophany (h) during the days of behavioural observations. Days
DBW 0 1 2 3 4
Relative humidity (%)
Heliophany (h)
Mean
Temperature (°C) Min
Max
Mean
Mean
20.3 23.4 22.0 21.8 23.9 22.1
13.3 17.6 18.6 16.1 16.9 16.5
24.9 28.6 23.9 26.3 28.8 25.5
73.7 69.0 70.5 68.7 65.7 79.2
12.5 9.8 11.9 11.6 12.9 13.0
DBW: mean data recorded the three days before weaning.
frequency of observations in which lambs were under shade each day (considering all the lambs, regardless of group), as well as the correlation between heliophany value per day and the frequency of observations in which lambs were under shade each day was tested using Spearman’s rank correlation. Results were considered significant at a = 0.05; data are presented as mean ± SEM.
3.2.2. Standing The frequency in which lambs were observed standing was greater in AR than DR lambs (p < 0.0001) (Table 3). The frequency of lambs standing decreased significantly from DBW to day 0 (p = 0.0001), when the lowest value was observed (Fig. 2B). After day 0 the frequency of lambs observed standing increased significantly until day 2 (p < 0.0001), when the greatest value was observed (Fig. 2B). The frequency of this behaviour decreased from day 2 to days 3 and 4 (p < 0.0001), when it returned to values similar to those recorded before weaning. 3.2.3. Staying under shade The frequency of observations in which lambs were under shade increased significantly from DBW to day 0 (p < 0.0001), decreased on days 1 and 2 (p < 0.0001), and increased again on days 3 and 4 (p < 0.0001) (Fig. 2C). On day 0 DR lambs were observed staying under shade in greater frequency than AR (p = 0.006) (Fig. 2C). The frequency of observations in which lambs were under shade was positively correlated with temperature (rs = 0.89, p = 0.02), but unrelated to heliophany (rs = 0.54, p = 0.27).
3. Results 3.1. Body weight gain Body weight gain from day 4 to day 5 was similar between AR and DR lambs (2.5 ± 0.3 kg vs. 2.1 ± 0.4 kg, respectively, p = 0.4). 3.2. Behaviours The main effects of time, group and interactions between time and group for all recorded behaviours are presented in Table 3. All behaviours except drinking water changed with time (p < 0.001). There was an effect of the group for lying (p = 0.049), standing (p < 0.0001), walking (p = 0.0003), grazing (p = 0.0004), pacing (p < 0.0001) and vocalizations (p < 0.0001). Walking (p < 0.0001), grazing (p = 0.0007), staying under shade (p = 0.04), pacing (p < 0.0001) and vocalizations (p < 0.0001) showed an interaction between time and group, and the interaction tended to be significant (p = 0.077) in the frequency in which lambs were observed lying. 3.2.1. Lying The frequency of lambs lying was greater in DR than in AR lambs (p = 0.049) (Table 3). The frequency of lambs lying decreased from day 0 to days 1 and 2 (p < 0.01), and then increased, reaching its maximum value on day 4 (p < 0.0001) (Fig. 2A).
3.2.4. Walking Lambs reared by their mothers were observed more times walking than AR lambs (p = 0.0003) (Table 3). The frequency of lambs walking increased significantly from DBW to day 0 (p < 0.0001), when the greatest frequency was observed (Fig. 2D). The frequency of lambs walking decreased significantly from day 0 to day 1 (p < 0.0001), returning on day 2 to values similar to those observed DBW. The frequency of this behaviour continued decreasing and reached the lowest values on days 3 and 4 (p < 0.0001). Lambs reared by their mothers presented a greater frequency of walking than AR lambs on day 0 (p < 0.0001), 1 (p = 0.02) and 2 (p = 0.006) (Fig. 2D). 3.2.5. Grazing The frequency in which lambs grazed was greater in the AR than in the DR group (p = 0.0004) (Table 3). The frequency of lambs grazing decreased significantly from DBW to day 0 (p < 0.0001), then increased to its maximum value on day 2 (p < 0.0001), and decreased again from day 2 to day 4 (p < 0.0001) (Fig. 2E). The frequency of grazing on days 0 (p < 0.0001), 2 (p = 0.002) and 4 was greater in DR than in AR lambs (p = 0.019) (Fig. 2E). 3.2.6. Drinking water The frequency in which the lambs were observed drinking water was not affected by group (AR: 0.8 ± 0.17 % vs. DR:
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(A)
a
a
b
b
ac
(D)
c
35 30
b
c
a
c
25 20 15
15
*
**
10
10 5
5
0
0
(B) 95
a
***
20
Walking (%)
Lying (%)
a 25
DBW
0
1
2
3
4
a
b
a
c
a
a
(E)
x
x
w
w
w
w
DBW
0
1
2
3
4
b
c
c
ad
d
a
100 ** 90
65 55
60 50 40 30
0
ac
b
35
1
2
a
c
3
bd
4
d
**
30 25 20 15 10 5
w
x
w
w
xy
y
DBW
0
1
2
3
4
*
70
35 DBW
***
80
45
(C) Staying under shade (%)
Grazing (%)
75
(F) Playing with objects (%)
Standing (%)
85
w
x
y
z
wx
wx
DBW
0
1
2
3
4
a
a
b
b
b
ab
2
3
4
2 1.6 1.2 0.8 0.4 0
0
DBW
Time (d)
0
1
Time (d)
Fig. 2. Frequency in which lambs were observed (A) lying, (B) standing, (C) staying under shade, (D) walking, (E) grazing, (F) playing with objects in lambs reared with their dams (DR: –h–) or artificially reared (AR: –d–). The arrow indicates the day of weaning. DBW: mean data recorded 3 days before weaning. Data are presented as mean frequency ± SEM. Different letters indicate significant differences (p < 0.05) between days. In variables with an interaction between group and time (staying under shade, walking and grazing) the effect of time (day) into each group is indicated with different letters (p < 0.05): a, b, c, and d for DR and w, x, y, and z for AR lambs. Significant differences between DR and AR in the same day are indicated as: ⁄p < 0.05; ⁄⁄p < 0.01; and ⁄⁄⁄p < 0.001.
1.1 ± 0.18 %; p = 0.16), time (p = 0.56), or their interaction (p = 0.34) (Table 3).
3.2.7. Playing with an object The frequency of lambs playing with an object decreased from day 0 to day 1 (p = 0.0002) and remained low until day 3 (Fig. 2F).
3.2.8. Pacing The frequency in which lambs were observed pacing was greater in the DR than in the AR group (p < 0.0001) (Table 3). The frequency of lambs pacing increased from DBW to day 0 (p < 0.0001), when the greatest frequency was observed (Fig. 3A). After day 0 the frequency of lambs pacing decreased significantly and returned to values similar to DBW (p < 0.0001), remaining low (day 1: 1.27 ± 0.29 %, day 2: 0.10 ± 0.09 %, and day 3: 0.0 ± 0.0 %) until day 4 (0.0 ± 0.0 %) (Fig. 3A). Lambs reared by their mothers had a greater increase in their pacing frequency on days 0 (p < 0.0001) and 1 (p = 0.013) than AR lambs (Fig. 3A).
3.2.9. Vocalizations The frequency in which lambs were observed vocalizing was greater in the DR than in the AR group (p < 0.0001) (Table 3). The frequency of vocalizations increased significantly from DBW to day 0 (p < 0.0001), when the frequency peaked (Fig. 3B). On day 1 the frequency of lambs vocalizing decreased significantly (p < 0.0001), returning to values similar to those observed DBW on day 2, and remaining low until Day 4. The frequency of observations in which DR lambs were observed vocalizing was greater than in AR lambs on days 0 (p < 0.0001) and 1 (p = 0.0015) (Fig. 3B). 4. Discussion Separation from the dam at weaning is an important stressor of lambs, as was evidenced by the greater increase in the frequencies of pacing, vocalizing, walking and staying under shade, and greater decrease in the frequency of grazing in lambs that were reared with their dams compared with those reared without the mother. However, the effect of separation from the mother was not enough
J.P. Damián et al. / Research in Veterinary Science 95 (2013) 913–918
(A)
a
b
c
a
a
a
14
***
Pacing (%)
12 10 8 6
*
4 2
w
w
w
w
w
w
DBW
0
1
2
3
4
a
b
a
a
0
(B)
c
a
50
Vocalizations (%)
*** 40 30 20
** 10
w
y
DBW
0
xy
xy
w
wx
2
3
4
0 1
Time (d) Fig. 3. Frequency in which lambs were observed (A) pacing and (B) vocalizations of lambs reared with their dams (DR: –h–) and those artificially reared (AR: –d–). The arrow indicates the day of weaning. DBW: mean data recorded 3 days before of weaning. Data are presented as mean frequency ± SEM. The effect of time (day) into each group is shown with different letters (p < 0.05): a, b, c, and d for DR and w, x y and z for AR lambs. Significant differences between DR and AR in the same Day are indicated as: ⁄: p < 0.05, ⁄⁄: p < 0.01 and ⁄⁄⁄: p < 0.001.
to cause differences in body weight gain. Behavioural changes were also observed in AR lambs after weaning; but these changes, which were probably associated with the changes of feeding (i.e. loss of milk and change of feeding to solid diet and water) and separation from adults resulted in a reduced behavioural response compared to that observed in lambs that were also separated from their mothers. The presence of adult ewes with their lambs in the AR group (although could interfere in the final results by adding a social factor to the change in feeding management) avoided the possible negative influence of the lack of other mother-young dyads into the group, although no studies have been carried out addressing this question. When the response of both groups is compared, AR lambs did not pace, rarely vocalised, and displayed practically no changes in walking frequency. On the other hand, DR lambs were observed vocalising approximately 40% of the time and pacing approximately 10% of the time, and displayed a fourfold increase in walking frequency, specially on day 0 and day 1, suggesting that lambs were seeking their dams. Based on these results we reinforce the suggestion of Napolitano et al. (2008) and Newberry and Swanson (2008) that walking and vocalizing at weaning are behaviours directed at searching for the dam. Moreover, pacing, only observed in DR lambs, occurred alongside the fence where the dams were taken out at separation, suggesting that the lambs were searching for the dam. The observers were located more than 30 m far from the fence line where the separation was performed, and located on the opposite margins, so no effect on avoidance or approaching behaviour could produce those movements. In addition, observers were always located in the same position relative to the paddock, and the previous days (before weaning) lambs did not show pacing
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behaviour, confirming that observers did not interfere with the expression of this behaviour. Grazing frequency also decreased more in DR than AR lambs at weaning. Studying weaning behaviour in calves, Hötzel et al. (2010) suggested that the reduction in grazing observed at weaning could be associated with physiological or emotional changes triggered by the interruption of suckling. The differences in grazing behaviour observed between the two groups of lambs in this study at weaning supports the interpretation of an emotional response to the separation from the dam. Lambs reared by their dams showed a greater increase in the frequency of resting under the shade during the first day of weaning than artificially reared lambs. This differential behavioural response may be a strategy to seek protection, triggered by the loss of their dams. As reported in wild ruminants (Coss, 1991; Wiedenmayer, 2009), resting in the shade during the day of weaning could be an antipredator behaviour of lambs. The increase in the frequency of observations in which lambs from both groups were under shade on the day of weaning might also be explained by an increase in ambient temperature, as was evidenced by the high correlation between these two variables. However, the frequency of observations in which lambs were under shade not was correlated with heliophany. Therefore, temperature seems to have greater importance than direct sunlight. As high temperatures and humidity are important stressors for animals reared in open paddocks (Silanikove, 2000), the provision of shade contributes to maintain homeostasis and improves animal welfare (Sevi et al., 2001; Schütz et al., 2008). In brief, providing lambs with shelters may be useful to decrease the negative effects of weaning on lambs welfare. Lambs of both groups stopped playing after weaning. This result is consistent with reports in which it was observed that calves stop playing at weaning (Enríquez et al., 2010; Krachun et al., 2010; Hötzel et al., 2012) and lambs stop playing after castration (Thornton and Waterman-Pearson, 2002). Play has been suggested as a positive indicator of animal welfare (Boissy et al., 2007; Held and Špinka, 2011), therefore it might be concluded that the loss of access to milk, suckling and social separation from adults was stressful not only for DR, but also for AR lambs. The reduction in energy intake associated with weaning was offered as one explanation for the reduction of playing activity in dairy calves (Krachun et al., 2010). However, three months after having worn nose-flap antisucking devices, weaned beef calves still played less than control calves of the same age (Hötzel et al., 2012). As nutritional conditions and body weight were similar between the two groups of calves, the energy intake did not seem to explain the differences in the frequency of playing, suggesting an emotional or cognitive response. In conclusion, the current study shows that the loss of the dam is an important stressor, and that this loss plays a key role in the behavioural response to weaning in lambs. Pacing behaviour, as well as an increase in the frequency of vocalizing, walking and staying under shade, and a decrease in the frequency of grazing frequency are provoked by the separation from their dam at weaning in grazing lambs. Additionally, the changes associated with feeding and separation from adults are also an important component of the stress response to weaning. Finally, this study highlights the importance of providing shelter or shade to the lambs at the time of weaning in grazing conditions.
5. Conflict of interest None of the authors has any financial or personal relationship that could inappropriately influence in the content of the paper.
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Acknowledgements We thank Maria Jesus Ramírez, Laura Morena and Florencia Beracochea for their help in behavioural recordings, and Damián González, Alberto Garcia, Sofía Moraes and Nestor Sanguinetti de la Unidad Experimental de Ovinos, INIA La Estanzuela, for taking care of the animals. Financial support: Agencia Nacional de Investigación e Innovación (FCE2626-ANII). MJH was funded by CNPq, Brazil (Proc. 200792/2011-3).
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