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Play behaviour in dairy calves is reduced by weaning and by a low energy intake
Applied Animal Behaviour Science 122 (2010) 71–76
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Play behaviour in dairy calves is reduced by weaning and by a low energy intake Carla Krachun a,b,*, Jeffrey Rushen a, Anne Marie de Passille´ a a b
Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, PO Box 1000, 6947 Highway 7, Agassiz, BC, V0M 1A0, Canada Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, BC, V6T 1Z4, Canada
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 2 December 2009
We examined the effects of milk allowance and weaning on the duration of play running in group-housed dairy calves. Our predictions were that (1) calves on a lower milk allowance would run less than calves on a higher allowance; and (2) running would decrease at weaning, especially in calves weaned earlier rather than later. Milk allowance and age of weaning were varied across three treatments: ‘6L-early weaned’ (fed 6 L/d of milk and weaned at 7 weeks of age), ‘12L-early weaned’ (fed 12 L/d of milk and weaned at 7 weeks), and ‘12L-later weaned’ (fed 12 L/d of milk and weaned at 13 weeks). Weaning occurred gradually over 9 days. Calves were observed for 2 days at each of six ages (3, 5, 7, 9, 11 and 13 weeks) and their average daily duration of running at each age was calculated. At 3 weeks, the 6L-early weaned calves ran less than calves receiving 12 L/d of milk (P < 0.01), but by 5 weeks there were no differences among treatments (P = 0.52). All treatments showed a drop in running at weaning but the decrease was more pronounced in the earlyweaned calves (both Ps < 0.001) than in the later-weaned calves (P = 0.06). At 3 weeks (before weaning) and at 7 and 13 weeks (immediately after weaning), there were positive correlations between digestible energy intake and duration of running (r = 0.48, 0.56, and 0.29, respectively, all Ps < 0.05). Overall, our results show that running by calves is reduced by a low milk allowance and by weaning off milk, and they suggest that play behaviour may be a useful measure of how the welfare of calves is affected by feeding practices. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Welfare Dairy calves Play Running Milk feeding Weaning
1. Introduction There is growing recognition that the welfare of animals in our care depends not only on their being kept free of pain, discomfort and other negative experiences, but also on their ability to experience positive emotions (e.g., Fraser and Duncan, 1998; Boissy et al., 2007; Yeates and Main, 2008). Play behaviour has been suggested as one potentially useful measure of positive welfare (Jensen et al., 1998; Yeates and Main, 2008). Most young mammals give the impression of ‘having fun’ when playing (Sˇpinka
* Corresponding author at: Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, PO Box 1000, 6947 Highway 7, Agassiz, BC, VOM 1A0, Canada. Tel.: +1 604 796 2221; fax: +1 604 796 0359. E-mail address: [email protected] (C. Krachun). 0168-1591/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2009.12.002
et al., 2001) and they actively seek out opportunities to do so (Fagen, 1981). However, animals usually play only when their basic needs for food, shelter, safety, etc., are met (Fagen, 1981; Martin and Caro, 1985; Jensen et al., 1998). A decrease in play may therefore be an early warning sign that an animal’s welfare is compromised. Furthermore, housing or management conditions that prevent young animals from playing may compromise welfare by denying animals the potential emotional, social, and physical benefits of play (see reviews by Martin and Caro, 1985; Sˇpinka et al., 2001). Evidence that play behaviour may reflect good welfare comes from finding that factors that reduce welfare reduce play behaviour. Studies of play behaviour in calves have focused mainly on the influence of housing factors including pen size (Jensen and Kyhn, 2000), opportunities
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for social contact (Jensen et al., 1998), and lighting levels (Dannenmann et al., 1985). Although the role of nutrition in calves’ play behaviour has received little attention, decreased play during food shortages has been observed in other species including deer (Mu¨ller-Schwarze et al., 1982), monkeys (Baldwin and Baldwin, 1976; Sommer and Mendoza-Granados, 1995), and pigs (Schmidt and Alder, 1981). A number of studies show that dairy calves in many commercial farms are fed milk below the amount they would normally drink and that this under-feeding is associated with reduced weight gains and behavioural signs of hunger (Jasper and Weary, 2002; Khan et al., 2007; De Paula Vieira et al., 2008; Borderas et al., 2009). If play is affected by food shortages in calves, as it is in other species, we would expect to see less play in calves fed these smaller amounts of milk. Weaning off milk is another nutritional source of stress for calves in commercial settings, as they are typically weaned earlier and more abruptly than would occur in nature (Weary et al., 2008). Calves often lose weight at weaning and show behaviours indicative of distress such as increased vocalizations, more frequent shifts in body position, and a greater number of visits to the milk feeder (Jasper et al., 2008). In their study of the effects of pen size on play, Jensen and Kyhn (2000) speculated that an observed decrease in calves’ play behaviour with age was probably due in part to weaning. Weaning has been found to reduce play behaviour in piglets (Donaldson et al., 2002); however, the effect of weaning on play behaviour has not been directly investigated in calves. Various factors may influence how calves respond to weaning, such as their age. Calves weaned too early may not have time to gradually adapt to solid feed intake before the milk supply is cut off, and their rumen may not be developed enough to properly digest solid feed (Khan et al., 2007) resulting in greater hunger and stress at weaning than in calves weaned later. In the current study, we observed calves fed two different levels of milk (6 L/d or 12 L/d) and weaned at either 7 weeks or 13 weeks. We had two predictions: (1) that calves fed 6 L/d of milk would run less than calves fed 12 L/d; and (2) that duration of play running would decrease at weaning, with this effect being more pronounced in calves weaned at 7 weeks than in calves weaned at 13 weeks. We focused on locomotor play because it involves a high degree of energy expenditure (Mu¨ller-Schwarze et al., 1982) and should therefore be highly sensitive to food availability and energy intake. Furthermore, play running emerges earlier in calves’ development than social play (e.g., play fighting and play mounting), and may be more frequent than social play in all-female groups (Jensen et al., 1998). 2. Methods This study was carried out at the University of British Columbia’s Dairy Education and Research Centre in Agassiz, British Columbia, Canada. All procedures were approved by the Institutional Animal Care Committee, following the requirements of the Canadian Council on Animal Care.
2.1. Animals and housing We studied the play behaviour of 51 female Holstein calves with a mean birth weight of 42.3 kg (SD = 4.63 kg). The calves were separated from their mothers within 12 h of birth, bottle-fed 4 L of colostrum (55 g Ig/L) and then weighed and placed in individual pens (1.22 m 2.44 m) with wood shavings bedding. While in the single pens, calves were fed 6 L/d of fresh whole milk provided through a bottle attached to the door of each pen. They were dehorned with caustic paste at 4 d and their health was monitored throughout the study (at least three times/ week). At 5–7 d (M = 5.59, SD = 0.61), calves were moved into 7.08 m 4.74 m group pens with plastic coated expanded metal floors (2.48 m 4.74 m) at the front of the pen immediately behind the feeders, and a large sawdustbedded area at the back of the pen (4.60 m 4.74 m). There were nine calves in each pen. Calves were fed pasteurized milk (3.97% fat, 4.10% protein, 3.30% lactose) at 40 8C and had ad libitum access to calf starter (20.4% crude protein on a dry matter basis, Unifeed Ltd., Chilliwack, Canada) from automated milk and starter feeders (CF 1000 CS Combi, DeLaval Inc., Tumba, Sweden). Water and hay were also available ad libitum from automated feeders (Insentec, Marknesse, Holland), and all feeders were calibrated once a week. All the feeders had sensors that could identify individual calves through transponders attached to the calves’ ears. This allowed the daily milk, water, starter and hay intake for each calf to be measured, and it also allowed us to control the maximum amount of milk per day dispensed to any given calf. Three digital cameras (Panasonic WV-BP 334; Osaka, Japan) positioned 6 m above each pen recorded the calves’ activities 24 h/d throughout the duration of the experiment. Red lights were used for night recording. For most of the calves, distinctive markings made them easily identifiable on the video. For calves that were very similar in appearance (e.g., all black), letters or other symbols were marked on their hides using hair bleach. 2.2. Experimental treatments Calves were assigned to one of three experimental treatments, balancing for birthweight: ‘6L-early weaned’ (calves fed 6 L/d of milk and weaned off milk at 7 weeks of age), ‘12L-early weaned’ (fed 12 L/d of milk and also weaned at 7 weeks), or ‘12L-later weaned’ (fed 12 L/d of milk and weaned at 13 weeks of age). We carried out the weaning process gradually over 9 d, with an equal sized reduction in milk allowance each day. Five of the group pens included three calves from each of the three experimental treatments and one pen included two calves from each treatment plus three ‘filler’ calves. 2.3. Data collection 2.3.1. Feed intake The DeLaval milk and starter feeders were connected to the KalbManager Version 1.1 and Win_Institut V02.18.24 software programs (Foerster-Technik, Engen, Germany),
C. Krachun et al. / Applied Animal Behaviour Science 122 (2010) 71–76
and the intakes for each calf were recorded 24 h/d. Hay and water intake were recorded automatically by the Insentec feeders. 2.3.2. Behavioural observations Videos were recorded at normal speed and viewed at 4 normal speed using Omnicast software (Genetech Inc., Saint-Laurent, Quebec) to observe running behaviour (defined below), with six different viewers each watching one of the six group pens. We watched all calves for a total of 12 d each, with 2 d at each of six ages: (1) approximately 3 weeks old (M = 18.52 days, SD = 3.50) before any weaning began; (2) approximately 5 weeks old (M = 35.93 days, SD = 1.17) just before the early-weaned calves began the weaning process; (3) approximately 7 weeks old (M = 47.84 days, SD = 1.11) just after the early-weaned calves completed weaning; (4) approximately 9 weeks old (M = 62.42 days, SD = 1.65) after the early-weaned calves had had some time to recover from weaning; (5) approximately 11 weeks old (M = 76.25 days, SD = 1.39) just before the later-weaned calves began the weaning process; and (6) approximately 13 weeks old (M = 89.74 days, SD = 1.31) just after the later-weaned group was weaned. In the immediate post-weaning period, one of the days watched was each calf’s first or second day with zero milk allowance. The videos were watched only for 15 h/d from 8:00 h to 23:00 h since preliminary viewing of 6 video days (including a total of 16 calves) revealed that almost no running occurred during the night time hours. We recorded all instances of running, defined as rapid forward movement that lasted 3 s or longer (in real time) and could include instances of jumping or bucking. Both galloping and trotting, as described by Jensen (1999), were included as running. Jumping and bucking were not recorded when they occurred on their own, and moving forward quickly while engaged in head butting with another calf was also not counted as running. The start and end times of each run were noted to the nearest second. Running events with pauses of less than 3 s between them were considered to be the same running event. For each calf, we calculated the total duration of running for each day of observation. 2.4. Reliability To evaluate inter-observer reliability, all six viewers watched the same video day chosen at random from one of the groups and measured the total duration of running for each calf. Pearson correlations among all possible pairs of viewers were high (range of rs = 0.96–0.99, M = 0.98, all Ps < 0.001). Intra-observer reliability was also high, as all six viewers were very consistent in their judgments of running duration (broken down by hour) when viewing the same video day at two different times (range of rs = 0.94–1.00, M = 0.97, all Ps < 0.001). 2.5. Statistical analyses For each calf, we calculated the daily duration of running at each age by averaging across the 2 days of observation at each of the six ages. To determine whether
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running was related to the amount of food energy that calves were ingesting, we estimated the total daily digestible energy (DE) intake for each calf from their milk, starter and hay intake combined. Samples of calf starter and hay were analysed and DE was estimated from the ingredients (Bodycote Testing Group Inc., Lethbridge, AB, Canada). Milk was estimated to contain 23.40 MJ/kg of dry matter (National Research Council, 2001). We calculated the average DE intake in mega-joules, divided by the calf’s body weight in kg (MJ/kg). This was calculated for both days of observation at each age and then averaged across the 2 days to get the mean DE intake for each calf at each of the six ages. At week 13 there was no hay intake data available for two of the calves and so their DE intake could not be calculated. Since both the distributions of the duration of running and DE intake were positively skewed, we used non-parametric Kruskal–Wallis tests to examine overall differences between the treatments separately at each age. Where an overall significant effect was found, pair-wise Wilcoxon’s rank sum tests were used to examine the differences between each pair of treatments. We used the non-parametric procedure (NPAR1WAY) of SAS. As treatments were applied within pens, we used the calf as the experimental unit when analysing DE intake. However, in order to minimize the effects of interactions between calves, we used group means to analyse effects of treatment on the duration of running. In addition, we used the Signed Rank test to analyse changes both with age and following weaning in the duration of running and DE intake. We also calculated Spearman correlations to examine the relationship of DE intake to the duration of running. To minimize the contributions of the effect of treatment on these correlations, they were based on the values of the variables ranked within treatments. The significance value for all analyses was set at P < 0.05, twotailed. 3. Results Fig. 1 shows the average daily duration of running and Fig. 2 shows DE intake for the three treatment groups at each of the six different ages observed. In all treatments running decreased with age. In the 12L-later weaned treatment (where age changes up to 11 weeks were not confounded with weaning), the decrease in running from 3 to 11 weeks of age was significant (Signed rank test: P < 0.001), and there was a negative correlation between age and duration of running (r = 0.38, P < 0.001). Prior to weaning, in week 3, there was a significant overall effect of milk allowance on running (Kruskal– Wallis: P = 0.01), with the calves that received 12 L/d of milk running more than the calves allowed 6 L/d of milk (Wilcoxon’s: P < 0.05 for both 12L treatments). However, at 5 weeks there were no differences among treatments (Kruskal–Wallis: P = 0.52). In the two early-weaned treatments, weaning off milk at 7 weeks of age led to a marked decrease in the duration of running (Fig. 1) (Signed rank test: P < 0.001 for both treatments). This was associated with a drop in DE intake (Signed rank test: P < 0.001 for both treatments) (Fig. 2). At
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C. Krachun et al. / Applied Animal Behaviour Science 122 (2010) 71–76 Table 1 Spearman’s correlations between daily duration of running and digestible energy (DE) intake per kilogram of body weight (MJ/kg) at each age. Correlations were based on the variables ranked within treatments. Age (weeks)
N
r
P
3 5 7 9 11 13
51 51 51 51 51 49
0.48 0.08 0.56 -0.02 0.09 0.29
<0.001 0.57 <0.001 0.90 0.52 0.04
4. Discussion Fig. 1. Mean ( SE) daily duration of running for each treatment group at each age of observation. For each age, different letters (a and b) indicate significant differences between treatments at that age (Wilcoxon’s test P < 0.05).
7 weeks of age, both early-weaned groups also ran less than the later-weaned calves, which had not yet been weaned (Wilcoxon’s: P < 0.01 in both cases). However, the duration of running did not differ between the two earlyweaned treatments at 7 weeks (Fig. 1) despite the greater DE intake of the 6L-early weaned calves at that age (Fig. 2. Wilcoxon’s test: P < 0.001). During weeks 9 and 11, the duration of running by the two early weaned groups increased somewhat (Fig. 1) and there were no significant differences among the three treatments at these two ages (Kruskal–Wallis: P > 0.20 at both ages). When the 12L-later weaned calves were weaned at 13 weeks of age, they showed a tendency to decrease their duration of running (Signed rank test: P = 0.06). However, this drop was far less than in the two early-weaned groups, owing partly to the fact that the later-weaned calves’ daily duration of running had already decreased substantially from initial levels at 3 weeks of age by the time their weaning began (Fig. 1). Differences in running among the three treatment groups at 13 weeks of age were not significant (Kruskal–Wallis: P = 0.17). The correlations (based on rankings within treatments) across calves between DE intake and the daily duration of running were variable (Table 1). At 3, 7 and 13 weeks of age, the duration of running was positively correlated with DE intake, but there were no significant correlations at other ages.
Both feeding calves a smaller amount of milk before weaning and weaning calves off milk reduced the duration of running that the calves showed, supporting the idea that play behaviour can provide a useful measure of welfare in calves. Furthermore, the correlations between the amount of running shown by each calf and DE intake suggest that energy intake is an important variable affecting how much running a calf will do. Before weaning, calves fed smaller amounts of milk ran less than calves fed larger amounts of milk, but only at 3 weeks of age. There was a positive correlation at this time between the daily duration of running and DE intake, when these variables were ranked within treatments. This reduction in play is not the result of a decrease in overall activity, as previous studies have shown that feeding a smaller amount of milk increases the time that calves spend standing (De Paula Vieira et al., 2008; Borderas et al., 2009). At 5 weeks of age, the effect of milk allowance on running was no longer present. This was due to a decline in the duration of play by the calves fed larger amounts of milk and to a slight increase in running by the calves fed 6 L/d of milk. This may have reflected the fact that these calves were now beginning to consume more solid food (e.g., Borderas et al., 2009), leading to a higher DE intake. When calves were weaned off milk at 7 weeks of age, they ran significantly less than before weaning. Our findings agree with previous studies in which other behavioural signs of weaning distress have been observed in calves (Jasper et al., 2008; Weary et al., 2008) and in other domestic animals (e.g., Hoffman et al., 1995; Colson et al., 2006). This early weaning reduced DE intake and
Fig. 2. Mean (SE) daily digestible energy (DE) intake from milk, starter and hay combined, calculated per kilogram of body weight for each treatment group at each age of observation. For each age, different letters (a–c) indicate significant differences between treatments at that age (Wilcoxon’s test P < 0.05).
C. Krachun et al. / Applied Animal Behaviour Science 122 (2010) 71–76
there was a correlation between the duration of running and DE intake at this time. Such negative effects of weaning may be due to weaning too early, before the young animal is emotionally and physiologically ready (see Colson et al., 2006; Weary et al., 2008). In piglets, delaying weaning by 1 or 2 weeks has been shown to reduce the frequency of problematic behaviours such as ‘belly-nosing’ (massaging other piglets’ stomachs with their snouts) and nibbling on other piglets (Metz and Gonyou, 1990; Worobec et al., 1999). We found less pronounced decreases in running when calves were weaned at 13 weeks. The later weaning also resulted in a less pronounced decrease in DE intake. However, some of the reduction in the effects of weaning that we observed with delayed weaning may be due to the fact that running by the later-weaned calves had already decreased substantially with age. Furthermore, there was a positive correlation between the duration of running and DE intake at 13 weeks, suggesting that the delayed weaning did not eliminate an effect of reduced DE intake on running. Consequently, our results do not let us conclude that delayed weaning had less of an effect on the calves’ play behaviour. We expected that the early-weaned calves would show less of a decrease in running at weaning if they received 6 L/d of milk prior to weaning rather than 12 L/d, since lower milk rations help calves to increase their solid feed intake (e.g., Borderas et al., 2009), making them less dependent on milk at the time of weaning. Our results show that the 6L-early weaned calves were consuming more digestible energy at the end of weaning than the 12L-early weaned calves, and DE intake was positively correlated with running. However, both early-weaned groups reduced their running by equivalent amounts at weaning. Jasper et al. (2008) similarly found that calves that were eating more solid feed at weaning (because their milk had been gradually diluted with warm water) showed an equally strong weaning distress response as calves that were weaned abruptly. Nutritive factors alone do not fully explain weaning distress (Budzynska and Weary, 2008). Our results support others (Jensen et al., 1998; Jensen and Kyhn, 2000) in showing that play decreases with age. However, in our study the apparent age effect needs to be interpreted cautiously because there was also less space per calf in the pen as the calves became larger. Jensen and colleagues (Jensen et al., 1998; Jensen and Kyhn, 2000) found that calves performed more locomotor play in larger spaces than in smaller spaces, and so our apparent age effect could instead be a space effect. One limit on using play behaviour to assess welfare in practical conditions comes from the difficulty with which the behaviour can be recorded and measured. The methods we used for measuring play in this study (watching 180 h of video for each of the 51 calves over six different ages) would not be optimal for conducting on-farm assessments of welfare. For this, more efficient (perhaps automated) methods of assessing play behaviour are needed. Furthermore, play running constitutes just a small proportion of the calves’ daily activities. Our finding that calves ran for only a few minutes a day, even at their peak, is consistent with previous research (Jensen et al., 1998; Jensen and
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Kyhn, 2000). Finding ways to stimulate play, or concentrating on ages or times of the day when play is most frequent, may help to increase the efficiency of measurement. 5. Conclusion Play running in calves was reduced by decreasing energy intake, both by providing low quantities of milk and by weaning. Since other studies have shown that weaning and restricted food availability are distressing to young animals (Colson et al., 2006; Weary et al., 2008), our results support the idea of using play behaviour to assess calf welfare, although there are difficulties in recording play behaviour. Play behaviour may also be important for helping to create positive welfare in animals. Play may have long-term physical and social benefits, and it could help to mitigate the negative effects of stressful experiences such as weaning (Donaldson et al., 2002). Providing animals with diets more conducive to play may allow them to experience positive affective states and improve their positive welfare. Acknowledgements We thank the staff at the UBC dairy barn as well as Gosia Zdanowicz, Sue Vickers, Kiara La Fond, Erin Ryan, Erin Mintline, Fernando Borderas and Sara Wood for their help; Dan Weary, Nina von Keyserlingk, and Margit Bak Jensen for stimulating discussions; and the Natural Sciences and Engineering Research Council of Canada and Agriculture and Agri-Food Canada for funding. References Baldwin, J.D., Baldwin, J.I., 1976. Effects of food ecology on social play: a laboratory simulation. Z. Tierpsychol. 40, 1–14. Boissy, A., Manteuffel, G., Jensen, M.B., Moe, R.O., Spruijt, B., Keeling, L.J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., Bakken, M., Veissier, I., Aubert, A., 2007. Assessment of positive emotions in animals to improve their welfare. Physiol. Behav. 92, 375–397. Borderas, T.F., de Passille´, A.M.B., Rushen, J., 2009. Feeding behavior of calves fed small or large amounts of milk. J. Dairy Sci. 92, 2843– 2852. Budzynska, M., Weary, D.M., 2008. Weaning distress in dairy calves: effects of alternative weaning procedures. Appl. Anim. Behav. Sci. 112, 33–39. Colson, V., Orgeur, P., Foury, A., Morme`de, P., 2006. Consequences of weaning piglets at 21 and 28 days on growth, behaviour and hormonal responses. Appl. Anim. Behav. Sci. 98, 70–88. Dannenmann, K., Buchenauer, D., Fliegner, H., 1985. The behaviour of calves under four levels of lighting. Appl. Anim. Behav. Sci. 13, 243– 258. De Paula Vieira, A., Guesdon, V., de Passille´, A.M., von Keyserlingk, M.A.G., Weary, D.M., 2008. Behavioural indicators of hunger in dairy calves. Appl. Anim. Behav. Sci. 109, 180–189. Donaldson, T.M., Newberry, R.C., Sˇpinka, M., Cloutier, S., 2002. Effects of early play experience on play behaviour of piglets after weaning. Appl. Anim. Behav. Sci. 79, 221–231. Fagen, R.M., 1981. Animal Play Behaviour. Oxford University Press, New York. Fraser, D., Duncan, I.J.H., 1998. ‘Pleasures’, ‘pains’ and animal welfare: toward a natural history of affect. Anim. Welf. 7, 383–396. Hoffman, R.M., Kronfeld, D.S., Holland, J.L., Greiwe-Crandell, K.M., 1995. Preweaning diet and stall weaning method influences on stress response in foals. J. Anim. Sci. 73, 2922–2930. Jasper, J., Budzynska, M., Weary, D.M., 2008. Weaning distress in dairy calves: acute behavioural responses by limit-fed calves. Appl. Anim. Behav. Sci. 110, 136–143.
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Jasper, J., Weary, D.M., 2002. Effects of ad libitum milk intake on dairy calves. J. Dairy Sci. 85, 3054–3058. Jensen, M.B., 1999. Effects of confinement on rebounds of locomotor behaviour of calves and heifers, and the spatial preferences of calves. Appl. Anim. Behav. Sci. 62, 43–56. Jensen, M.B., Kyhn, R., 2000. Play behaviour in group-housed dairy calves, the effect of space allowance. Appl. Anim. Behav. Sci. 67, 35–46. Jensen, M.B., Vestergaard, K.S., Krohn, C.C., 1998. Play behaviour in dairy calves kept in pens: the effect of social contact and space allowance. Appl. Anim. Behav. Sci. 56, 97–108. Khan, M.A., Lee, H.J., Lee, W.S., Kim, H.S., Kim, S.B., Ki, K.S., Ha, J.K., Lee, H.G., Choi, Y.J., 2007. Pre- and postweaning performance of Holstein female calves fed milk through step-down and conventional methods. J. Dairy Sci. 90, 876–885. Martin, P., Caro, T.M., 1985. On the functions of play and its role in behavioral development. Adv. Stud. Behav. 15, 59–103. Metz, J.H.M., Gonyou, H.W., 1990. Effect of age and housing conditions on the behavioural and haemolytic reaction of piglets to weaning. Appl. Anim. Behav. Sci. 27, 299–309.
Mu¨ller-Schwarze, D., Stagge, B., Mu¨ller-Schwarze, C., 1982. Play behavior: persistence, decrease, and energetic compensation during food shortage in deer fawns. Science 215, 85–87. National Research Council, 2001. Nutrient Requirements of Dairy Cattle, Seventh Revised Addition 2001. National Research Council. Schmidt, M., Alder, H.C., 1981. Danish studies on behaviour of earlyweaned piglets: preliminary results. In: Sybesma, W. (Ed.), The Welfare of Pigs. Martin Nijhoff, The Hague, pp. 211–223. Sommer, V., Mendoza-Granados, D., 1995. Play as an indicator of habitat quality: a field study of langur monkeys (Presbytis entellus). Ethology 99, 177–192. Sˇpinka, M., Newberry, R.C., Bekoff, M., 2001. Mammalian play: training for the unexpected. Q. Rev. Biol. 76, 141–168. Weary, D.M., Jasper, J., Ho¨tzel, M.J., 2008. Understanding weaning distress. Appl. Anim. Behav. Sci. 110, 24–41. Worobec, E.K., Duncan, I.J.H., Widowski, T.M., 1999. The effects of weaning at 7, 14 and 28 days on piglet behaviour. Appl. Anim. Behav. Sci. 62, 173–182. Yeates, J.W., Main, D.C.J., 2008. Assessment of positive welfare: a review. Vet. J. 175, 293–300.
Contents lists available at ScienceDirect
Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Play behaviour in dairy calves is reduced by weaning and by a low energy intake Carla Krachun a,b,*, Jeffrey Rushen a, Anne Marie de Passille´ a a b
Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, PO Box 1000, 6947 Highway 7, Agassiz, BC, V0M 1A0, Canada Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, BC, V6T 1Z4, Canada
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 2 December 2009
We examined the effects of milk allowance and weaning on the duration of play running in group-housed dairy calves. Our predictions were that (1) calves on a lower milk allowance would run less than calves on a higher allowance; and (2) running would decrease at weaning, especially in calves weaned earlier rather than later. Milk allowance and age of weaning were varied across three treatments: ‘6L-early weaned’ (fed 6 L/d of milk and weaned at 7 weeks of age), ‘12L-early weaned’ (fed 12 L/d of milk and weaned at 7 weeks), and ‘12L-later weaned’ (fed 12 L/d of milk and weaned at 13 weeks). Weaning occurred gradually over 9 days. Calves were observed for 2 days at each of six ages (3, 5, 7, 9, 11 and 13 weeks) and their average daily duration of running at each age was calculated. At 3 weeks, the 6L-early weaned calves ran less than calves receiving 12 L/d of milk (P < 0.01), but by 5 weeks there were no differences among treatments (P = 0.52). All treatments showed a drop in running at weaning but the decrease was more pronounced in the earlyweaned calves (both Ps < 0.001) than in the later-weaned calves (P = 0.06). At 3 weeks (before weaning) and at 7 and 13 weeks (immediately after weaning), there were positive correlations between digestible energy intake and duration of running (r = 0.48, 0.56, and 0.29, respectively, all Ps < 0.05). Overall, our results show that running by calves is reduced by a low milk allowance and by weaning off milk, and they suggest that play behaviour may be a useful measure of how the welfare of calves is affected by feeding practices. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Welfare Dairy calves Play Running Milk feeding Weaning
1. Introduction There is growing recognition that the welfare of animals in our care depends not only on their being kept free of pain, discomfort and other negative experiences, but also on their ability to experience positive emotions (e.g., Fraser and Duncan, 1998; Boissy et al., 2007; Yeates and Main, 2008). Play behaviour has been suggested as one potentially useful measure of positive welfare (Jensen et al., 1998; Yeates and Main, 2008). Most young mammals give the impression of ‘having fun’ when playing (Sˇpinka
* Corresponding author at: Pacific Agri-Food Research Centre, Agriculture and Agri-Food Canada, PO Box 1000, 6947 Highway 7, Agassiz, BC, VOM 1A0, Canada. Tel.: +1 604 796 2221; fax: +1 604 796 0359. E-mail address: [email protected] (C. Krachun). 0168-1591/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2009.12.002
et al., 2001) and they actively seek out opportunities to do so (Fagen, 1981). However, animals usually play only when their basic needs for food, shelter, safety, etc., are met (Fagen, 1981; Martin and Caro, 1985; Jensen et al., 1998). A decrease in play may therefore be an early warning sign that an animal’s welfare is compromised. Furthermore, housing or management conditions that prevent young animals from playing may compromise welfare by denying animals the potential emotional, social, and physical benefits of play (see reviews by Martin and Caro, 1985; Sˇpinka et al., 2001). Evidence that play behaviour may reflect good welfare comes from finding that factors that reduce welfare reduce play behaviour. Studies of play behaviour in calves have focused mainly on the influence of housing factors including pen size (Jensen and Kyhn, 2000), opportunities
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for social contact (Jensen et al., 1998), and lighting levels (Dannenmann et al., 1985). Although the role of nutrition in calves’ play behaviour has received little attention, decreased play during food shortages has been observed in other species including deer (Mu¨ller-Schwarze et al., 1982), monkeys (Baldwin and Baldwin, 1976; Sommer and Mendoza-Granados, 1995), and pigs (Schmidt and Alder, 1981). A number of studies show that dairy calves in many commercial farms are fed milk below the amount they would normally drink and that this under-feeding is associated with reduced weight gains and behavioural signs of hunger (Jasper and Weary, 2002; Khan et al., 2007; De Paula Vieira et al., 2008; Borderas et al., 2009). If play is affected by food shortages in calves, as it is in other species, we would expect to see less play in calves fed these smaller amounts of milk. Weaning off milk is another nutritional source of stress for calves in commercial settings, as they are typically weaned earlier and more abruptly than would occur in nature (Weary et al., 2008). Calves often lose weight at weaning and show behaviours indicative of distress such as increased vocalizations, more frequent shifts in body position, and a greater number of visits to the milk feeder (Jasper et al., 2008). In their study of the effects of pen size on play, Jensen and Kyhn (2000) speculated that an observed decrease in calves’ play behaviour with age was probably due in part to weaning. Weaning has been found to reduce play behaviour in piglets (Donaldson et al., 2002); however, the effect of weaning on play behaviour has not been directly investigated in calves. Various factors may influence how calves respond to weaning, such as their age. Calves weaned too early may not have time to gradually adapt to solid feed intake before the milk supply is cut off, and their rumen may not be developed enough to properly digest solid feed (Khan et al., 2007) resulting in greater hunger and stress at weaning than in calves weaned later. In the current study, we observed calves fed two different levels of milk (6 L/d or 12 L/d) and weaned at either 7 weeks or 13 weeks. We had two predictions: (1) that calves fed 6 L/d of milk would run less than calves fed 12 L/d; and (2) that duration of play running would decrease at weaning, with this effect being more pronounced in calves weaned at 7 weeks than in calves weaned at 13 weeks. We focused on locomotor play because it involves a high degree of energy expenditure (Mu¨ller-Schwarze et al., 1982) and should therefore be highly sensitive to food availability and energy intake. Furthermore, play running emerges earlier in calves’ development than social play (e.g., play fighting and play mounting), and may be more frequent than social play in all-female groups (Jensen et al., 1998). 2. Methods This study was carried out at the University of British Columbia’s Dairy Education and Research Centre in Agassiz, British Columbia, Canada. All procedures were approved by the Institutional Animal Care Committee, following the requirements of the Canadian Council on Animal Care.
2.1. Animals and housing We studied the play behaviour of 51 female Holstein calves with a mean birth weight of 42.3 kg (SD = 4.63 kg). The calves were separated from their mothers within 12 h of birth, bottle-fed 4 L of colostrum (55 g Ig/L) and then weighed and placed in individual pens (1.22 m 2.44 m) with wood shavings bedding. While in the single pens, calves were fed 6 L/d of fresh whole milk provided through a bottle attached to the door of each pen. They were dehorned with caustic paste at 4 d and their health was monitored throughout the study (at least three times/ week). At 5–7 d (M = 5.59, SD = 0.61), calves were moved into 7.08 m 4.74 m group pens with plastic coated expanded metal floors (2.48 m 4.74 m) at the front of the pen immediately behind the feeders, and a large sawdustbedded area at the back of the pen (4.60 m 4.74 m). There were nine calves in each pen. Calves were fed pasteurized milk (3.97% fat, 4.10% protein, 3.30% lactose) at 40 8C and had ad libitum access to calf starter (20.4% crude protein on a dry matter basis, Unifeed Ltd., Chilliwack, Canada) from automated milk and starter feeders (CF 1000 CS Combi, DeLaval Inc., Tumba, Sweden). Water and hay were also available ad libitum from automated feeders (Insentec, Marknesse, Holland), and all feeders were calibrated once a week. All the feeders had sensors that could identify individual calves through transponders attached to the calves’ ears. This allowed the daily milk, water, starter and hay intake for each calf to be measured, and it also allowed us to control the maximum amount of milk per day dispensed to any given calf. Three digital cameras (Panasonic WV-BP 334; Osaka, Japan) positioned 6 m above each pen recorded the calves’ activities 24 h/d throughout the duration of the experiment. Red lights were used for night recording. For most of the calves, distinctive markings made them easily identifiable on the video. For calves that were very similar in appearance (e.g., all black), letters or other symbols were marked on their hides using hair bleach. 2.2. Experimental treatments Calves were assigned to one of three experimental treatments, balancing for birthweight: ‘6L-early weaned’ (calves fed 6 L/d of milk and weaned off milk at 7 weeks of age), ‘12L-early weaned’ (fed 12 L/d of milk and also weaned at 7 weeks), or ‘12L-later weaned’ (fed 12 L/d of milk and weaned at 13 weeks of age). We carried out the weaning process gradually over 9 d, with an equal sized reduction in milk allowance each day. Five of the group pens included three calves from each of the three experimental treatments and one pen included two calves from each treatment plus three ‘filler’ calves. 2.3. Data collection 2.3.1. Feed intake The DeLaval milk and starter feeders were connected to the KalbManager Version 1.1 and Win_Institut V02.18.24 software programs (Foerster-Technik, Engen, Germany),
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and the intakes for each calf were recorded 24 h/d. Hay and water intake were recorded automatically by the Insentec feeders. 2.3.2. Behavioural observations Videos were recorded at normal speed and viewed at 4 normal speed using Omnicast software (Genetech Inc., Saint-Laurent, Quebec) to observe running behaviour (defined below), with six different viewers each watching one of the six group pens. We watched all calves for a total of 12 d each, with 2 d at each of six ages: (1) approximately 3 weeks old (M = 18.52 days, SD = 3.50) before any weaning began; (2) approximately 5 weeks old (M = 35.93 days, SD = 1.17) just before the early-weaned calves began the weaning process; (3) approximately 7 weeks old (M = 47.84 days, SD = 1.11) just after the early-weaned calves completed weaning; (4) approximately 9 weeks old (M = 62.42 days, SD = 1.65) after the early-weaned calves had had some time to recover from weaning; (5) approximately 11 weeks old (M = 76.25 days, SD = 1.39) just before the later-weaned calves began the weaning process; and (6) approximately 13 weeks old (M = 89.74 days, SD = 1.31) just after the later-weaned group was weaned. In the immediate post-weaning period, one of the days watched was each calf’s first or second day with zero milk allowance. The videos were watched only for 15 h/d from 8:00 h to 23:00 h since preliminary viewing of 6 video days (including a total of 16 calves) revealed that almost no running occurred during the night time hours. We recorded all instances of running, defined as rapid forward movement that lasted 3 s or longer (in real time) and could include instances of jumping or bucking. Both galloping and trotting, as described by Jensen (1999), were included as running. Jumping and bucking were not recorded when they occurred on their own, and moving forward quickly while engaged in head butting with another calf was also not counted as running. The start and end times of each run were noted to the nearest second. Running events with pauses of less than 3 s between them were considered to be the same running event. For each calf, we calculated the total duration of running for each day of observation. 2.4. Reliability To evaluate inter-observer reliability, all six viewers watched the same video day chosen at random from one of the groups and measured the total duration of running for each calf. Pearson correlations among all possible pairs of viewers were high (range of rs = 0.96–0.99, M = 0.98, all Ps < 0.001). Intra-observer reliability was also high, as all six viewers were very consistent in their judgments of running duration (broken down by hour) when viewing the same video day at two different times (range of rs = 0.94–1.00, M = 0.97, all Ps < 0.001). 2.5. Statistical analyses For each calf, we calculated the daily duration of running at each age by averaging across the 2 days of observation at each of the six ages. To determine whether
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running was related to the amount of food energy that calves were ingesting, we estimated the total daily digestible energy (DE) intake for each calf from their milk, starter and hay intake combined. Samples of calf starter and hay were analysed and DE was estimated from the ingredients (Bodycote Testing Group Inc., Lethbridge, AB, Canada). Milk was estimated to contain 23.40 MJ/kg of dry matter (National Research Council, 2001). We calculated the average DE intake in mega-joules, divided by the calf’s body weight in kg (MJ/kg). This was calculated for both days of observation at each age and then averaged across the 2 days to get the mean DE intake for each calf at each of the six ages. At week 13 there was no hay intake data available for two of the calves and so their DE intake could not be calculated. Since both the distributions of the duration of running and DE intake were positively skewed, we used non-parametric Kruskal–Wallis tests to examine overall differences between the treatments separately at each age. Where an overall significant effect was found, pair-wise Wilcoxon’s rank sum tests were used to examine the differences between each pair of treatments. We used the non-parametric procedure (NPAR1WAY) of SAS. As treatments were applied within pens, we used the calf as the experimental unit when analysing DE intake. However, in order to minimize the effects of interactions between calves, we used group means to analyse effects of treatment on the duration of running. In addition, we used the Signed Rank test to analyse changes both with age and following weaning in the duration of running and DE intake. We also calculated Spearman correlations to examine the relationship of DE intake to the duration of running. To minimize the contributions of the effect of treatment on these correlations, they were based on the values of the variables ranked within treatments. The significance value for all analyses was set at P < 0.05, twotailed. 3. Results Fig. 1 shows the average daily duration of running and Fig. 2 shows DE intake for the three treatment groups at each of the six different ages observed. In all treatments running decreased with age. In the 12L-later weaned treatment (where age changes up to 11 weeks were not confounded with weaning), the decrease in running from 3 to 11 weeks of age was significant (Signed rank test: P < 0.001), and there was a negative correlation between age and duration of running (r = 0.38, P < 0.001). Prior to weaning, in week 3, there was a significant overall effect of milk allowance on running (Kruskal– Wallis: P = 0.01), with the calves that received 12 L/d of milk running more than the calves allowed 6 L/d of milk (Wilcoxon’s: P < 0.05 for both 12L treatments). However, at 5 weeks there were no differences among treatments (Kruskal–Wallis: P = 0.52). In the two early-weaned treatments, weaning off milk at 7 weeks of age led to a marked decrease in the duration of running (Fig. 1) (Signed rank test: P < 0.001 for both treatments). This was associated with a drop in DE intake (Signed rank test: P < 0.001 for both treatments) (Fig. 2). At
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C. Krachun et al. / Applied Animal Behaviour Science 122 (2010) 71–76 Table 1 Spearman’s correlations between daily duration of running and digestible energy (DE) intake per kilogram of body weight (MJ/kg) at each age. Correlations were based on the variables ranked within treatments. Age (weeks)
N
r
P
3 5 7 9 11 13
51 51 51 51 51 49
0.48 0.08 0.56 -0.02 0.09 0.29
<0.001 0.57 <0.001 0.90 0.52 0.04
4. Discussion Fig. 1. Mean ( SE) daily duration of running for each treatment group at each age of observation. For each age, different letters (a and b) indicate significant differences between treatments at that age (Wilcoxon’s test P < 0.05).
7 weeks of age, both early-weaned groups also ran less than the later-weaned calves, which had not yet been weaned (Wilcoxon’s: P < 0.01 in both cases). However, the duration of running did not differ between the two earlyweaned treatments at 7 weeks (Fig. 1) despite the greater DE intake of the 6L-early weaned calves at that age (Fig. 2. Wilcoxon’s test: P < 0.001). During weeks 9 and 11, the duration of running by the two early weaned groups increased somewhat (Fig. 1) and there were no significant differences among the three treatments at these two ages (Kruskal–Wallis: P > 0.20 at both ages). When the 12L-later weaned calves were weaned at 13 weeks of age, they showed a tendency to decrease their duration of running (Signed rank test: P = 0.06). However, this drop was far less than in the two early-weaned groups, owing partly to the fact that the later-weaned calves’ daily duration of running had already decreased substantially from initial levels at 3 weeks of age by the time their weaning began (Fig. 1). Differences in running among the three treatment groups at 13 weeks of age were not significant (Kruskal–Wallis: P = 0.17). The correlations (based on rankings within treatments) across calves between DE intake and the daily duration of running were variable (Table 1). At 3, 7 and 13 weeks of age, the duration of running was positively correlated with DE intake, but there were no significant correlations at other ages.
Both feeding calves a smaller amount of milk before weaning and weaning calves off milk reduced the duration of running that the calves showed, supporting the idea that play behaviour can provide a useful measure of welfare in calves. Furthermore, the correlations between the amount of running shown by each calf and DE intake suggest that energy intake is an important variable affecting how much running a calf will do. Before weaning, calves fed smaller amounts of milk ran less than calves fed larger amounts of milk, but only at 3 weeks of age. There was a positive correlation at this time between the daily duration of running and DE intake, when these variables were ranked within treatments. This reduction in play is not the result of a decrease in overall activity, as previous studies have shown that feeding a smaller amount of milk increases the time that calves spend standing (De Paula Vieira et al., 2008; Borderas et al., 2009). At 5 weeks of age, the effect of milk allowance on running was no longer present. This was due to a decline in the duration of play by the calves fed larger amounts of milk and to a slight increase in running by the calves fed 6 L/d of milk. This may have reflected the fact that these calves were now beginning to consume more solid food (e.g., Borderas et al., 2009), leading to a higher DE intake. When calves were weaned off milk at 7 weeks of age, they ran significantly less than before weaning. Our findings agree with previous studies in which other behavioural signs of weaning distress have been observed in calves (Jasper et al., 2008; Weary et al., 2008) and in other domestic animals (e.g., Hoffman et al., 1995; Colson et al., 2006). This early weaning reduced DE intake and
Fig. 2. Mean (SE) daily digestible energy (DE) intake from milk, starter and hay combined, calculated per kilogram of body weight for each treatment group at each age of observation. For each age, different letters (a–c) indicate significant differences between treatments at that age (Wilcoxon’s test P < 0.05).
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there was a correlation between the duration of running and DE intake at this time. Such negative effects of weaning may be due to weaning too early, before the young animal is emotionally and physiologically ready (see Colson et al., 2006; Weary et al., 2008). In piglets, delaying weaning by 1 or 2 weeks has been shown to reduce the frequency of problematic behaviours such as ‘belly-nosing’ (massaging other piglets’ stomachs with their snouts) and nibbling on other piglets (Metz and Gonyou, 1990; Worobec et al., 1999). We found less pronounced decreases in running when calves were weaned at 13 weeks. The later weaning also resulted in a less pronounced decrease in DE intake. However, some of the reduction in the effects of weaning that we observed with delayed weaning may be due to the fact that running by the later-weaned calves had already decreased substantially with age. Furthermore, there was a positive correlation between the duration of running and DE intake at 13 weeks, suggesting that the delayed weaning did not eliminate an effect of reduced DE intake on running. Consequently, our results do not let us conclude that delayed weaning had less of an effect on the calves’ play behaviour. We expected that the early-weaned calves would show less of a decrease in running at weaning if they received 6 L/d of milk prior to weaning rather than 12 L/d, since lower milk rations help calves to increase their solid feed intake (e.g., Borderas et al., 2009), making them less dependent on milk at the time of weaning. Our results show that the 6L-early weaned calves were consuming more digestible energy at the end of weaning than the 12L-early weaned calves, and DE intake was positively correlated with running. However, both early-weaned groups reduced their running by equivalent amounts at weaning. Jasper et al. (2008) similarly found that calves that were eating more solid feed at weaning (because their milk had been gradually diluted with warm water) showed an equally strong weaning distress response as calves that were weaned abruptly. Nutritive factors alone do not fully explain weaning distress (Budzynska and Weary, 2008). Our results support others (Jensen et al., 1998; Jensen and Kyhn, 2000) in showing that play decreases with age. However, in our study the apparent age effect needs to be interpreted cautiously because there was also less space per calf in the pen as the calves became larger. Jensen and colleagues (Jensen et al., 1998; Jensen and Kyhn, 2000) found that calves performed more locomotor play in larger spaces than in smaller spaces, and so our apparent age effect could instead be a space effect. One limit on using play behaviour to assess welfare in practical conditions comes from the difficulty with which the behaviour can be recorded and measured. The methods we used for measuring play in this study (watching 180 h of video for each of the 51 calves over six different ages) would not be optimal for conducting on-farm assessments of welfare. For this, more efficient (perhaps automated) methods of assessing play behaviour are needed. Furthermore, play running constitutes just a small proportion of the calves’ daily activities. Our finding that calves ran for only a few minutes a day, even at their peak, is consistent with previous research (Jensen et al., 1998; Jensen and
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Kyhn, 2000). Finding ways to stimulate play, or concentrating on ages or times of the day when play is most frequent, may help to increase the efficiency of measurement. 5. Conclusion Play running in calves was reduced by decreasing energy intake, both by providing low quantities of milk and by weaning. Since other studies have shown that weaning and restricted food availability are distressing to young animals (Colson et al., 2006; Weary et al., 2008), our results support the idea of using play behaviour to assess calf welfare, although there are difficulties in recording play behaviour. Play behaviour may also be important for helping to create positive welfare in animals. Play may have long-term physical and social benefits, and it could help to mitigate the negative effects of stressful experiences such as weaning (Donaldson et al., 2002). Providing animals with diets more conducive to play may allow them to experience positive affective states and improve their positive welfare. Acknowledgements We thank the staff at the UBC dairy barn as well as Gosia Zdanowicz, Sue Vickers, Kiara La Fond, Erin Ryan, Erin Mintline, Fernando Borderas and Sara Wood for their help; Dan Weary, Nina von Keyserlingk, and Margit Bak Jensen for stimulating discussions; and the Natural Sciences and Engineering Research Council of Canada and Agriculture and Agri-Food Canada for funding. References Baldwin, J.D., Baldwin, J.I., 1976. Effects of food ecology on social play: a laboratory simulation. Z. Tierpsychol. 40, 1–14. Boissy, A., Manteuffel, G., Jensen, M.B., Moe, R.O., Spruijt, B., Keeling, L.J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., Bakken, M., Veissier, I., Aubert, A., 2007. Assessment of positive emotions in animals to improve their welfare. Physiol. Behav. 92, 375–397. Borderas, T.F., de Passille´, A.M.B., Rushen, J., 2009. Feeding behavior of calves fed small or large amounts of milk. J. Dairy Sci. 92, 2843– 2852. Budzynska, M., Weary, D.M., 2008. Weaning distress in dairy calves: effects of alternative weaning procedures. Appl. Anim. Behav. Sci. 112, 33–39. Colson, V., Orgeur, P., Foury, A., Morme`de, P., 2006. Consequences of weaning piglets at 21 and 28 days on growth, behaviour and hormonal responses. Appl. Anim. Behav. Sci. 98, 70–88. Dannenmann, K., Buchenauer, D., Fliegner, H., 1985. The behaviour of calves under four levels of lighting. Appl. Anim. Behav. Sci. 13, 243– 258. De Paula Vieira, A., Guesdon, V., de Passille´, A.M., von Keyserlingk, M.A.G., Weary, D.M., 2008. Behavioural indicators of hunger in dairy calves. Appl. Anim. Behav. Sci. 109, 180–189. Donaldson, T.M., Newberry, R.C., Sˇpinka, M., Cloutier, S., 2002. Effects of early play experience on play behaviour of piglets after weaning. Appl. Anim. Behav. Sci. 79, 221–231. Fagen, R.M., 1981. Animal Play Behaviour. Oxford University Press, New York. Fraser, D., Duncan, I.J.H., 1998. ‘Pleasures’, ‘pains’ and animal welfare: toward a natural history of affect. Anim. Welf. 7, 383–396. Hoffman, R.M., Kronfeld, D.S., Holland, J.L., Greiwe-Crandell, K.M., 1995. Preweaning diet and stall weaning method influences on stress response in foals. J. Anim. Sci. 73, 2922–2930. Jasper, J., Budzynska, M., Weary, D.M., 2008. Weaning distress in dairy calves: acute behavioural responses by limit-fed calves. Appl. Anim. Behav. Sci. 110, 136–143.
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