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Suckling, weaning, and the development of oral behaviours in dairy calves
Applied Animal Behaviour Science 147 (2013) 11–18
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Suckling, weaning, and the development of oral behaviours in dairy calves Isabelle Veissier a,b,∗ , Sara Caré c , Dominique Pomiès a,b a b c
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR 1213 Herbivores, BP 10448, F-63000 Clermont-Ferrand, France Istituto di Zootecnica, Università Cattolica del Sacro Cuore, I-29122 Piacenza, Italy
a r t i c l e
i n f o
Article history: Accepted 10 May 2013 Available online 12 June 2013 Keywords: Suckling Oral behaviours Dairy calves Weaning
a b s t r a c t Dairy calves are generally separated from their dam at birth. They express non-nutritive oral activities such as licking or sucking other calves or objects, nibbling, or tongue-playing, which have been related to the absence of sucking a teat and ingestive chewing. We hypothesized that the dam, by its presence, can help focus the oral behaviour of calves towards nutritive activities and thereby limit the development of non-nutritive oral activities. To test this hypothesis, we compared calves suckled by their dam against calves separated from their dam at birth and fed milk through a teat (automatic milk feeder). Cow and calf behaviour was observed before weaning and after weaning at 10 wk of age. Before weaning, the suckled calves were less active than the artificially fed calves. After weaning, suckled calves tended to spend less time on non-nutritive oral activities than non-suckled calves. Before weaning, suckling cows and non-suckling cows showed similar behaviour. Both cows and calves reacted to weaning: cows showed vocalization and agitation, and calves showed increased blood cortisol levels. We conclude that keeping dairy calves with their dam for 10 wk can be beneficial to calves, although weaning induces a degree of stress. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Commercially reared animals are generally separated from their dam before the age at which they would naturally be weaned in free-leaving conditions. Dairy calves are typically separated from their dams within hours of birth and then artificially milk-fed for several weeks (Budzynska and Weary, 2008). Milk is often provided in a bucket, which does not always satisfy the calf’s motivation to suckle (de Passillé, 2001). Behavioural disorders such as excessive sucking on body parts of other calves (cross-sucking) and on pen equipment can be common in calves kept in groups (Lidfors, 1993; de Passillé, 2001). These oral activities can
∗ Corresponding author at: INRA, UMR1213 Herbivores, F-63122 SaintGenès-Champanelle, France. Tel.: +33 473624098; fax: +33 473624518. E-mail address: [email protected] (I. Veissier). 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.05.002
discourage producers from rearing calves in groups due to the higher risks of disorders (navel abscesses, calves drinking urine, etc.), despite the advantages in terms of labour (Kung et al., 1997). Non-nutritive oral activities of calves (cross-sucking, licking, tongue-playing) may be related to insufficient feeding behaviours, i.e. sucking a teat or ingestive chewing (Wiepkema et al., 1987; Sato and Abe, 1993; Veissier et al., 1998). They are also less common when calves are with their dams, even when they are not suckled (Krohn et al., 1999; Fröberg et al., 2008; Roth et al., 2009). Some species-specific behaviours can be learned from the dam, like hunting in spiders (Punzo and Ludwig, 2002) and food preferences (Melo et al., 2006) or recognizing social cues (Levy et al., 2003) in rodents. Proper development of species-specific behaviour likely limits the development of ‘abnormal’ behaviours. Indeed, early weaning has been linked to the development of stereotypic behaviour (Latham and Mason, 2008). For instance,
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in lab mice and in farmed minks, it results in increased rearing, bar-biting or tail-biting (Mason, 1994; Würbel and Stauffacher, 1997). Similarly, once they are weaned, piglets that were reared with a sow whose movements were restricted show higher levels of belly nosing and manipulative activities post-weaning compared to piglets reared with a loose-housed sow (Oostindjer et al., 2011). The quality of the dam-young interaction is thus likely to play a role in the behavioural development of the young animal. As the suckling may thus help young calves develop species-specific behaviours, maternal rearing could limit the development of undesirable non-nutritive oral activities. If this hypothesis was confirmed, then young calves reared with their dam should develop less non-nutritive oral activities than artificially reared calves even if they suck a teat to get their milk, and this effect should be visible after weaning. Nevertheless, even when kept with the dams after birth, young farm animals will still be separated from their dams later in life, typically at 6–9 months of age in beef suckler herds. The separation between the dam and its offspring is particularly stressful for both partners, as shown by vocalization and agitation in cows and calves (Lidfors, 1996) and a slower growth rate in calves (Price et al., 2003; Haley et al., 2004). The aim of the study reported here was to analyze the impact of suckling on the behaviour of cows and calves, to assess the disturbances caused by separation from the dam at weaning, and to check whether non-nutritive oral activities in calves are dependent on previous presence of their dam. 2. Materials and methods 2.1. Animals and experimental design The experiment was conducted at the INRA’s UE1296 Monts d’Auvergne experimental farm (Orcival, France). Fourty-six Holstein cows and calves were followed from calving to 16 wk later. Calving took place in autumn in two consecutive years (Year 1, 24 cows and 24 calves; Year 2, 24 cows and 24 calves). Each year, half the cows suckled their calves (24 suckling cows and 24 suckled calves). During Year 1, the suckling cows and their respective calves stayed together all day long (24 h), whereas in Year 2 they stayed together only from 07:30 h to 18:00 h (i.e. 10.5 h). The remaining cows and their calves were separated immediately after calving (24 non-suckling and 24 artificially reared calves). In each year, two batches of cows and calves were observed: Batch 1 consisted of the 12 cows that calved first and their 12 calves, and Batch 2 consisted of the next 12 cows and their 12 calves. Within each year, calf sex (24 males, 24 females), date of calving (and consequently batch) and calf weight at birth were balanced between the two treatments. In addition, the cows were chosen so that date of calving, cow weight at calving, body condition scores, lactation rank, and milk yield and composition (from previous lactation or estimated from milk index in primiparous cows) were balanced between suckling cows and non-suckling cows. Due to the numerous factors to be balanced between treatments, artificially reared calves and
non-suckling cows were not necessarily related. The interaction between treatment, year and batch corresponds to a group of animals. There were 4 groups of calves or cows per treatment. On Year 1 one male calf suckled by its dam died by accident just before the time of weaning. The data collected from this calf and from another male calf of the same age but artificially reared were removed from the analyses.
2.2. Housing and feeding Calves were followed more closely than cows. Details will thus be given on their living conditions. The suckled calves stayed in a calving pen with their dam for the first 3–4 days of life. They were then moved to a 4.90 m × 5.26 m pen next to the pen where the cows were held. The calves’ pen was bounded by a barrier on the side next to the cow pen that prevented the cows from entering the calves’ pen but allowed the calves to join the cows. On the other three sides of the calves’ pen was bounded by bundles of straw. The floor of the calves’ pen was concrete covered with straw. Five infrared heaters were suspended 1.5 m above the floor of the calves’ pen. The cows’ pen was 9.60 m × 12.20 m, concrete-floored, and the animals had access to cubicles (one cubicle per cow) covered with mats and woodchip. The artificially reared calves were first housed in a pen with a concrete floor covered in woodchip and tethered for 10 days. They were then moved to a 8.50 m × 7.75 m pen where they were free to move. The pen was bounded by a barrier on one side, concrete walls on two sides, and bundles of straw on one side. The floor was concrete covered with straw. The calves were weaned at 10 wk of age, either by separation from their dam (suckled calves) or suppression of milk feeding (artificially reared calves). After weaning, the calves from the two treatments (suckled calves and artificially reared calves) were accommodated in a common 4 m × 7 m pen similar to the pen used to house the artificially reared calves before weaning (walls: one barrier, two concrete walls, bundles of straw; floor: concrete plus straw). The cows did not change pen from before to after weaning. All cows were milked once a day between 06:30 h and 07:30 h. Before weaning, suckled calves received milk from their dams. Artificially reared calves were fed 2.5 L colostrum through a nipple bottle twice on Day 1 after birth, then 2 L of milk twice on Day 2 using the same bottle, and 4 L of milk twice a day from Day 3 to Day 9 using a bucket. From Day 10, these calves were fed milk from an automatic milk feeder fitted with a rubber teat left available at all times (Nutri-Calf Suprême, BouMatic Europe, Saint-Nom-la-Bretèche, France). The calves could drink a maximum of 12 L/day of milk from Day 10 to Day 49, then 9.2 L/day from Day 50 to Day 56, 6.4 L/day from Day 56 to Day 63 and finally 3.6 L/day from Day 64 to Day 70. Before and after weaning, all calves had free access to commercial concentrates (before weaning: Croustivo HP, CCPA Deltavit, Janzé, France; after weaning: Startivo, Union Altitude, Aurillac, France), hay or silage (Dactilis glomerata),
I. Veissier et al. / Applied Animal Behaviour Science 147 (2013) 11–18
and water. After weaning, they were also provided with salt from a block. 2.3. Measurements 2.3.1. Behaviour 2.3.1.1. Time budget. The animals were identified by large numbers painted on their flanks, back and forehead to allow the observer to recognize them from a distance. Before weaning, the behaviour of the calves was observed on two days, —one when the calves were 25.7 days old (SE 1.3 days) and one when they were 49.8 days old (SE 1.3 days). All calves from one treatment (suckled calves or artificially reared calves) in a given batch were observed on a given day, and the same-batch calves in the other treatment were observed the next day. The observer entered the shed and stayed next to the pens from 06:30 h. Scan sampling was performed from 07:30 h to 18:00 h with 10-min intervals between scans. At each scan, the observer noted the activity of each calf as detected at first glance. Six exclusive behavioural classes were distinguished in calves: suckling (a cow or the rubber teat of the milk feeder), nonnutritive oral activities, eating (concentrate, hay, silage or straw), miscellaneous activities (licking salt, drinking water, self-scratching, social interaction, or walking), idling (standing up, no activity), and lying down. Non-nutritive oral activities included licking or sucking another animal or an object, nibbling at an object (prehending part of it), and tongue-rolling (making circular movements with the tongue in or outside the mouth). Thereafter, at 28.1 days (SE, 1.2 days) after weaning, the calves were observed on two consecutive days. Scan sampling was performed from 06:00 h to 18:00 h at 5-min intervals between scans. The same list of behavioural classes was used, except that suckling was removed. As the two observation days were consecutive, individual data were averaged over these two days. In Year 2, the behaviour of the cows was also observed before weaning. This was done at the same time as the observation of suckled calves. The same behavioural classes were distinguished in calves and cows, except that suckling a calf and licking another animal were pooled together (social activities) and that walking was considered separately from other activities. The observed behaviours were then encoded using Observer Video Pro® software (Noldus Information Technology, Wageningen, The Netherlands). 2.3.1.2. Cows behaviour at weaning. The behaviour of the cows was observed on the day of weaning and the following 9 days. On each day, we noted which cows vocalized during the day (from after milking to 18:00 h); which cows were agitated on their way from their pen to the milking parlour (vocalizing, stopping, or stepping back), and which cows were agitated during milking (vocalizing, stamping, or kicking). 2.3.2. Cortisol Blood samples (5 mL) were taken from calves by puncture of the jugular vein around weaning. Blood samples were taken at 16:00 h on the day before weaning, at
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weaning, and on the following two days. The samples were immediately centrifuged 3000 × g for 5 min, and plasma aliquots were stored at −20 ◦ C until assayed for cortisol assay. In Year 2, milk samples were taken on the day of weaning and then at 1, 2, 5, 7 and 9 days post-weaning. The milk was immediately stored at −20 ◦ C. Milk samples were defrosted at room temperature, defatted by centrifugation (2400 × g for 20 min at 4 ◦ C). Corticosteroids were extracted from skimmed milk with ethyl acetate. Milk or blood cortisol concentrations were determined by radioimmunoassay with an antibody produced by Cognié and Poulin (INRA, Tours, France; Boissy, 1990). Limit of detection was 0.02 ng/mL and the within and between-assay coefficients of variation were 11% and 22% for low (4 ng/mL) controls and 7% and 14% for high (32 ng/mL) controls. 2.3.3. Calf growth The calves were weighed at birth, then once a week until the end of the experiment using an electronic scale (690 KES, Mettler Toledo, Viroflay, France) with a precision of 200 g. We calculated daily weight gain from birth to weaning and from weaning to 16 wk of age. 2.4. Statistical analyses Statistical analyses were performed using SAS v8.1 (SAS Inst. Inc., Cary, NC). Cortisol concentrations were logtransformed, and percentages of time spent in a given behavioural class were arcsine-transformed to fit the conditions for ANOVA. ANOVA was conducted on quantitative data (% time, cortisol concentration, weight) using mixed models. The following factors were included in the analyses of calf data: treatment, year, batch, sex, time (when appropriate), plus all treatment × year × batch interactions, the treatment × sex interaction, the time × treatment (except for pre-weaning behaviour) interaction, and animal (random factor nested into the treatment, included only when data were collected on the same animals at several time points). The following factors were included in the analyses of cow data: treatment, batch, time, the treatment × batch or time interaction, and animal (random factor nested into the treatment). The time corresponded to the day of observation for pre-weaning behaviours (two separate observation days), to the various days of sampling for cortisol, and to period (before vs. after weaning) for calf growth. In case of repeated measurements (when time is included), the covariance matrix was considered to have a compound symmetry. The treatment × day interaction was not included in analysis of pre-weaning behaviour as the day here had the same meaning whatever the treatment. The results of quantitative data are presented as means ± standard error (SE). Qualitative data (proportion of cows in the various behavioural classes at weaning) were analyzed day-by-day using 2 tests. Only significant effects (P < 0.05) and tendencies (P < 0.10) are reported. We will focus on the effects of the treatment and the year and the interactions between the treatment and other factors.
0.06 0.74 0.01 0.95 0.21 3.65 0.11 7.18 0 1.66 4.96 31.0 5.11 5.21 53.5
a, b, c: values with no common letter differ significantly (P < 0.05; information provided when P < 0.10 for the interaction between treatment and year). a Treat = treatment (suckling vs. artificial rearing).
0.00 0.85 <0.0001 <0.0001 <0.0001 9.7 0.04 47.49 39.69 30.08 0.30 0.13 0.96 0.78 0.17 1.12 2.44 0 0.08 1.93 0.48 b 1.78 0.81 a 1.30 1.79 ± ± ± ± ± 3.44 27.8 9.46 12.1 47.2 0.88 a 2.05 0.65 b 0.94 2.26 ± ± ± ± ± 6.76 28.7 6.66 5.15 52.6 0.50 b 2.27 0.80 a 1.11 2.22 ± ± ± ± ± 3.99 30.0 11.1 12.6 42.2 0.49 b 1.32 0.38 b 0.50 1.24
0.07 0.20 <0.001 <0.001 <0.001 0.34 3.44 1.68 28.1 15.0 44.7 0.93 0.93 0.04 <0.001 0.76 <0.001 0.59 0.01 4.22 60.9 0.10 16.7 0.30 0.40 c 0.78 0.70 0.87 1.15 b 1.79 a ± ± ± ± ± ± 2.08 6.35 6.09 5.88 14.1 65.5 0.41 a 0.80 0.71 0.89 1.2 c 1.83 b ± ± ± ± ± ±
Year 2 12 calves Year 1 11 calves
4.95 8.27 10.4 9.87 8.52 57.9 0.40 ab 0.78 0.70 0.87 1.15 a 1.79 b ± ± ± ± ± ±
After weaning Non-nutritive oral activities Eating Miscellaneous activities Idling Lying down
± ± ± ± ±
<0.001 0.27 0.42 0.72 0.04 0.00 22.9 1.24 0.65 0.13 4.48 11.46
F(treat × year) P(year) F(year) P(treat) F(treat)a Year 2 12 calves
4.15 8.75 1.00 6.45 21.4 58.3 0.4 bc 0.81 0.71 0.89 1.18 bc 1.84 ab ± ± ± ± ± ± 3.09 8.90 4.35 9.76 10.8 62.9 Before weaning Suckling Non-nutritive oral activities Eating Miscelllaneous activities Idling Lying down
3.1.1.3. Time budget of cows before weaning. Before weaning, cow behaviour did not depend on whether or not they suckled calves (percentage time spent eating,
Year 1 11 calves
3.1.1.2. Time budget of calves after weaning. Calf behaviour post-weaning is also reported in Table 1. Calves spent less time on non-nutritive oral activities or lying down and more time on miscellaneous activities or idling in Year 2 than Year 1. There were treatment × year interactions on non-nutritive activities (tendency) and miscellaneous activities (significant). Non-nutritive activities were more frequent in artificially reared calves from Year 1 than in all other calves, and the year effect on miscellaneous activities was more marked in suckled calves. We did not find any other significant effects of the treatment as main factor nor in interaction with other factors. Considering the various non-nutritive oral activities (sucking, licking, nibbling, tongue-playing) separately did not reveal differences between treatments.
Artificial reared calves
3.1.1. Time budget 3.1.1.1. Time budget of calves before weaning. The behaviour of calves before weaning is reported in Table 1. In Year 1, suckled calves spent significantly less time suckling their dam or another cow than artificially reared calves spent time suckling at the milk feeder. In Year 2, the opposite pattern was observed. In general, calves tended to spend less time suckling in Year 2 than Year 1. Suckled calves spent more time performing nonnutritive oral activities than artificially reared calves. More specifically, suckled calves spent more time licking other calves or objects than artificially reared calves (8.05 vs. 5.96% of time, SE = 0.47, F1,39 (treatment) = 9.86, P = 0.003). In contrast, suckled calves spent less time sucking other calves or objects than artificially reared calves (0.397 vs. 1.211, SE = 0.178, F1,39 (treatment) = 13, P < 0.001). Time spent nibbling at objects or tongue-playing was similar between suckled and artificially reared calves (0.220 ± 0.085 and 0.033 ± 0.041, P > 0.10). Suckled calves spent significantly less time eating and more time idling than artificially reared calves. In Year 2, calves generally spent less time eating or on miscellaneous activities and more time idling than in Year 1, and the between-treatment difference in time spent idling was stronger. Artificially reared calves from Year 2 spent significantly more time lying down than suckled calves from the same year and the artificially reared calves from Year 1. We did not find any other significant effects of the treatment as main factor nor in interaction with other factors, except that time spent idling varied between groups of calves (F1,39 (treatment × year × batch) = 10.4, P = 0.003) and that time spent on oral non-nutritive activities depended on batch and treatment (F1,38 (treatment × batch) = 6.42, P = 0.01, with suckled calves from Batch 1 spending more time on such activities than all other calves (10.3 vs. 7.32, SE = 0.79).
Suckled calves
3.1. Behaviour
Behaviour (% scans)
3. Results
P(treat × year)
I. Veissier et al. / Applied Animal Behaviour Science 147 (2013) 11–18 Table 1 Calf behaviour before and after weaning. Calves were either suckled (n = 23) or artificially reared (n = 23). Suckled calves stayed with their dam all day long in Year 1 but only from 07:30 to 18:00 h in Year 2. Weaning took place at 10 wk of age. Observations took place from 07:30 to 18:00 h. Data are expressed as means ± standard errors.
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Fig. 2. Plasma cortisol levels around weaning in suckled calves (–䊉–, n = 23) vs. artificially reared calves (––, n = 23). Blood samples were taken the day before weaning (Day 0), on the day of weaning (Day 1), then on the next two days (Days 2 and 3). Weaning took place at 10 wk of age. Means and standard errors are shown.
(2 = 12.3 on the day of weaning, 31.4 one day after, 15.6 two days after, P < 0.001 in all cases). Cows that had suckled their calves also reacted by showing agitation on the way to the milking parlour and during milking. The difference in the proportion of cows agitated between suckling and non-suckling cows was significant on the day after weaning (2 = 10.8 on the way to milking and 6.62 during milking, P = 0.001 and P = 0.01, respectively). The same difference between suckling and non-suckling cows was observed on the next day on the way to the milking parlour (2 = 10.8, P = 0.001), and to a lesser extent at 5 and 7 days post-weaning on the way to milking and two days post-weaning during milking (2 = 3.07, P = 0.08 in all cases). 3.2. Cortisol
Fig. 1. Cow behaviour at weaning. The proportions of cows that vocalized or were agitated are compared between suckling cows (–䊉–, n = 24) and cows not suckling (––, n = 24).
walking, interacting with another animal, idling, and lying by suckling vs. not suckling cows: 24.1 vs. 22.3 (SE = 1.55), 2.11 vs. 2.71 (SE = 0.40), 1.65 vs. 0.85 (SE = 0.38), 25.9 vs. 24.5 (SE = 1.82), 39.8 vs. 44.7 (SE = 2.79), P > 0.10 in all cases).
3.1.2. Cows’ behaviour at weaning On the day of weaning and the following 9 days, the nonsuckling cows never vocalized during the day and never displayed agitation on the way to the milking parlour or during milking (Fig. 1). Most cows that had suckled their calves vocalized during the day of weaning and then on following days up to Day 7 post-weaning. Vocalization was strong on the day after weaning, when 17 out of the 24 suckling cows vocalized. The difference in the proportion of cows vocalizing between suckling and non-suckling cows was significant from weaning to two days after weaning
Suckled calves had significantly higher blood cortisol concentrations than artificially reared calves (cortisol from the day before weaning to two days after weaning, 9.65 vs. 8.10 ng/mL, SE = 0.52, F1,36 (treatment) = 4.83, P = 0.03). Cortisol concentrations increased significantly from the day before weaning to the next days, and tended to decrease thereafter (F3,132 (day) = 10.9, P < 0.001, Fig. 2). Similar changes over time were observed in both suckled and artificially reared calves (F3,132 (day × treatment) = 0.44, P > 0.10). Calf plasma cortisol concentrations were significantly higher in Year 2 than Year 1 (11.5 ± 0.51 vs. 6.20 ± 0.54 ng/mL, F1,36 (year) = 67.2, P < 0.001), regardless of how calves were reared (F1,36 (year × treatment) = 1.33, P > 0.10). Plasma cortisol levels tended to be higher in female than male calves (9.71 ± 0.52 vs. 8.03 ± 0.56, F1,36 (sex) = 3.69, P = 0.06), whatever the treatment (F1,36 (sex × treatment) = 2.67, P > 0.10). milk cortisol concentration averaged Cow 1.45 ± 0.23 ng/mL, regardless of treatment, day postweaning, batch, or their interactions (P > 0.10 in all cases).
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Fig. 3. Weight of calves suckled by their dam (–䊉–, n = 23) or artificially milk-fed (––, n = 23). Calves were weighed once a week from birth to 16 wk of age. Weaning took place at 10 wk of age. Means and standard errors are shown.
3.3. Growth Calves suckled by their dam grew less fast than artificially reared calves (average daily weight gain, 0.966 ± 0.033 vs. 0.859 ± 0.033 kg, F1,36 (treatment) = 5.19, P = 0.03). The difference was especially significant after weaning (artificially reared calves, 1.01 ± 0.045; suckled calves, 0.800 ± 0.045 kg, F1,42 (treatment × period) = 6.86, P = 0.01) (Fig. 3). There was a significant treatment × year × period interaction on calf growth (F1,42 = 4.45, P = 0.04). In Year 1, suckled calves showed a slower growth rate after weaning (0.647 ± 0.066 kg) compared to their own growth before weaning (0.971 ± 0.066 kg) or to all other calves at the same period (artificially reared calves after weaning, 1.019 ± 0.066 kg in Year 1 and 1.021 ± 0.062 kg in Year 2; suckled calves after weaning, 0.953 ± 0.063 kg in Year 2). Male calves grew faster than female calves, whatever the treatment, year, or period (0.975 ± 0.036 vs. 0.850 ± 0.033 kg, F1,36 (sex) = 5.99, P = 0.01). 4. Discussion In brief, prior to weaning, cows behaved similarly whether or not they fed their calves, and calves fed by their dam spent less time eating and sucking other calves than artificially fed calves. Weaning induced vocalizations and agitation in the cows and increased blood cortisol levels in the calves. The calves that had been maintained all day long with their dam before weaning (suckled calves, Year 1) exhibited fewer non-nutritive oral activities after weaning. First, prior to weaning, we did not observe differences in behaviour between cows that suckled their calves and those that did not. Calves suckled for 23 (±2.5) min per day. Suckling and non-suckling cows were equally active during the day, as assessed through time spent walking, eating, idling, and lying down. Suckling cows performed more social activities, but the difference was not significant. We assumed that if cows were frustrated by not being able to suckle their calves, they would be more active, e.g.
spending more time walking and looking for calves, but this was not the case. Therefore, our results do not find evidence that cows are affected by being unable to suckle. Second, prior to weaning, the behaviour of calves reared with their dam differed from that of calves fed artificially. In Year 2, the suckled calves were more often observed suckling their dam than the artificially fed calves were seen at the milk feeder, as reported by Fröberg and Lidfors (2009). This pattern was opposite in Year 1, leading to a significant interaction between treatment and year. This interaction may be only apparent because in Year 1, suckled calves stayed with their dams all day long (except while cows were being milked). Hence, although not observable here, it is logical to assume they also suckled during the night and that on the whole day they spent more time suckling than artificially fed calves as observed on Year 2. Suckled calves were less active than artificially reared calves: they spent more time lying down or idling, especially in Year 2, and less time eating, as in Fröberg and Lidfors (2009). Suckled calves had access to the cubicle pen housing their dams, and they were often observed next to the cows. The presence of the dam may have had a calming effect on the calves, resulting in lower activity levels. Again a significant interaction between treatment and year was noticed; with suckled calves spending more time idling and less time lying down in Year 2 than in Year 1. It thus seems that the calming effect of cows is less efficient when calves are separated from them at night. More surprisingly, prior to weaning, suckled calves spent more time licking objects and other calves than artificially fed calves. We speculate that suckled calves, being in a larger environment and with cows, had more opportunities to perform oral activities, e.g. they had access to more objects in their environment (cubicles bars for instance). By contrast suckled calves spent less time sucking other calves or objects, a result consistent with those of Roth et al. (2009). Cross-sucking can be due to the high motivation of calves to suck that is not satisfied when they are fed milk artificially (de Passillé, 2001). Our results suggest that this may be true also when an artificial teat is available at all time during the day. Therefore, it seems that a milk feeder is far less efficient than a dam to drive the sucking activity of calves. Third, after weaning, although all the calves were kept together, we still observed differences in behaviour between calves that had been suckled by their dam and those separated from their dam at birth. The calves that had been suckled by their dam tended to spend less time on non-nutritive oral activities, which included licking or sucking another calf or an object, nibbling at an object, and tongue-rolling. These behaviours remained rare, since calves spent only about 5% of their day performing them. This difference between suckled and artificially reared calves was more marked in Year 1. In Year 1, suckled calves spent all day with their dam – except while the cows were being milked – whereas in Year 2 they were separated from the dam during the night. This result suggests that the presence of the dam at an early age can have an impact on the later behaviour of the calves, namely on their tendency to express non-nutritive oral activities. Krohn et al. (1999) already observed that calves that stayed with their dam for the first four days of life express less non-nutritive sucking
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after their weaning, especially if they had suckled their dam during these first two days. These activities are linked to the lack of sucking (especially for milk intake) and to ingestive chewing (needed for the intake of solid foods) (Illmann and Spinka, 1993; Veissier et al., 1998; de Passillé, 2001). It has been well described that the dam has an influence on it offspring, especially for the development of species-specific behaviour (see Section 1). We hypothesized that cows help young calves focus their oral activities towards nutritive elements, i.e. milk (when suckling the udder) or solid foods, or towards their dam (suckling again, licking). This hypothesis is confirmed by the fact that in our experiment, before weaning, suckled calves spent less time sucking objects or other calves than artificially fed calves. We also hypothesized that the mere presence of the dam can further reduce non-nutritive oral activities in calves after the calves have been separated from their dam. Our results do not fully confirmed that hypothesis since we only observed a tendency in Year 1 and no significant effect in Year 2 (when cows and calves were separated at night). Nevertheless, together with those from Krohn et al. (1999), they bring evidence that the dam has strong effect on the development of the oral behaviour of calves. The underlying processes also need to be investigated —does a calf learn by observing cows? do olfactory cues play a role, by focusing the calf’s attention on the udder? do interactions between dam and calf influence the calf’s behaviour towards other stimuli? Fourth, at weaning, cows that had suckled their calves demonstrated a response to the separation from their calves. Cattle separated from their social partners vocalize and display intense agitation, their heart rate increases, and cortisol gets released into the blood (Boissy and Le Neindre, 1997), and these responses suggest that cattle are highly disturbed by separation from peers. In our experiment, when cows were separated from their calves, behavioural responses (vocalization, agitation) remained marked for 2 days post-weaning and some cows even reacted for up to 7 days post-weaning. We measured cortisol concentrations in the milk of the cows during the two daily milkings after weaning. Regardless of whether or not the cows were separated from their calves, their milk cortisol content was 1.45 (±0.23) ng/mL. Given that the proportion of cortisol in milk is about 10% that of blood (Mormede et al., 2007), our cows had about 14.5 ng/mL in blood, which is visibly higher than basal cortisol levels in cattle (generally reported as around 5 ng/mL) but nevertheless far lower than in acutely stressed cattle (Ting et al., 2003; Orihuela and Hernandez, 2007). Therefore, there is evidence that cows are disturbed by the absence of their calves after weaning (at least for two days), but not enough to induce clear neuroendocrine stress responses. Fifth, weaning was followed by an increase in blood cortisol levels in calves. Although calves that had been suckled by their dams had higher average blood cortisol levels, the increase post-weaning was not significantly more marked than in calves that had previously been artificially milkfed. Calves are known to react strongly to the separation from their dam: they vocalize, are restless, and their weight gain remains slower for several weeks (Haley et al., 2001; Price et al., 2003). Like for cows, weaning suckled calves is likely to have induced behavioural responses (vocalization,
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agitation). These responses may have spread among all calves as they were accommodated together, resulting in increased cortisol in both suckled and non-suckled calves. However, this explanation remains speculative, as we did not monitor calf behaviour immediately after weaning. Suckled calves put on less weight after weaning than their artificially fed counterparts (−0.2 kg/day). This result is consistent with the literature (Price et al., 2003; Haley et al., 2005; Froberg et al., 2011). The suppression of milk cannot explain this effect, since all calves were weaned off milk at the same age. Since maintaining visual contact between cows and calves can limit the lower post-weaning growth (Price et al., 2003; Haley et al., 2005), it is likely that stress due to the separation is, at least in part, the causal factor. As a matter of fact, calves remain attached to their dam for at least 3 wk after weaning (Veissier and Le Neindre, 1989; Veissier et al., 1990). Strategies for reducing stress at weaning have been proposed, such as maintaining visual communication between cows and calves (Price et al., 2003) or suppressing milk first before separating the two animals (Haley et al., 2005). In the present experiment, the negative effects of weaning on the growth of suckled calves was more marked in Year 1 when the calves had been with their dam all day long, than in Year 2 when cows and calves were separated at night. It is likely that in Year 2, the suckled calves were already accustomed to being separated from their dam and did not experience as much stress as those of Year 1 at the definitive separation at weaning. Our work confirms that weaning, combining both the suppression of milk and separation from the dam, is stressful for suckled calves, especially when they are not used to being separated from their dam. In conclusion, cows do not seem to miss suckling when they are separated from their calves soon after birth, but they are disturbed when the separation occurs later, after 10 wk of suckling. Similarly, suckled calves are disturbed when they are separated from their dam at weaning, and this separation can reduce their growth rate. Calves that are suckled by their dam later display fewer oral non-nutritive activities than artificially fed calves. The presence of the dam may orient the oral behaviour of the calf to the point that the calf is less ready to develop abnormal behaviours (in this case non-nutritive oral activities). We conclude that suckling may be beneficial to calves, but that the weaning process requires a special attention in order to minimize separation-induced stress. Acknowledgements The authors thank Marc Barbet from the UE1296 Monts d’Auvergne farm for helping with the execution of the experiment. We also thank the UMR1213 Herbivores staff for their valuable assistance, especially Stéphane Andanson and Christine Ravel for the cortisol assays and Christophe Mallet for his help with the behavioural recordings. References Boissy, A., 1990. Les réactions émotives chez les bovins domestiques femelles (Bos taurus L.). Quantification et variations sous l’influence de facteurs environnementaux et hormonaux. Thèse de Doctorat de l’Université de Paris XIII, 224 pp.
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Boissy, A., Le Neindre, P., 1997. Behavioral cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiol. Behav. 61, 693–699. Budzynska, M., Weary, D.M., 2008. Weaning distress in dairy calves: effects of alternative weaning procedures. Appl. Anim. Behav. Sci. 112, 33–39. de Passillé, A.M., 2001. Sucking motivation and related problems in calves. Appl. Anim. Behav. Sci. 72, 175–187. Fröberg, S., Gratte, E., Svennersten-Sjaunja, K., Olsson, I., Berg, C., Orihuela, A., Galina, C.S., García, B., Lidfors, L., 2008. Effect of suckling (‘restricted suckling’) on dairy cows’ udder health and milk let-down and their calves’ weight gain feed intake and behaviour. Appl. Anim. Behav. Sci. 113, 1–14. Fröberg, S., Lidfors, L., 2009. Behaviour of dairy calves suckling the dam in a barn with automatic milking or being fed milk substitute from an automatic feeder in a group pen. Appl. Anim. Behav. Sci. 117, 150–158. Froberg, S., Lidfors, L., Svennersten-Sjaunja, K., Olsson, I., 2011. Performance of free suckling dairy calves in an automatic milking system and their behaviour at weaning. Acta Agric. Scand. Sect. A Anim. Sci. 61, 145–156. Haley, D.B., Bailey, D.W., Stookey, J.M., 2005. The effects of weaning beef calves in two stages on their behavior and growth rate. J. Anim. Sci. 83, 2205–2214. Haley, D.B., Stookey, J.M., Clavelle, J.L., Watts, J.M., 2001. The simultaneous loss of milk and maternal contact compounds distress at weaning in beef calves. In: Garner, J.P., Mench, J.A., Heekin, S.P. (Eds.), Proceedings of the 35th International Congress of the ISAE. University of California, Davis, p. 41. Haley, D.B., Stookey, J.M., Weary, D.M., Bailey, D.W., 2004. A new way to wean minimises the behavioural responses of cattle over traditional weaning methods. In: Hänninen, L., Valros, A. (Eds.), Proceedings of the 38th International Congress of the ISAE. University of Helsinki, Helsinki, p. 58. Illmann, G., Spinka, M., 1993. Maternal behavior of dairy heifers and sucking of their newborn calves in group housing. Appl. Anim. Behav. Sci. 36, 91–98. Krohn, C.C., Foldager, J., Mogensen, L., 1999. Long-term effect of colostrum feeding methods on behaviour in female dairy calves. Acta Agric. Scand. Sect. A Anim. Sci. 49, 57–64. Kung, L. JR., Demarco, S., Siebenson, L.N., Joyner, E., Haenlein, G.F.W., MorrisF R.M., 1997. An evaluation of two management systems for rearing calves fed milk replacer. J. Dairy Sci. 80, 2529–2533. Latham, N.R., Mason, G.J., 2008. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 110, 84–108. Levy, F., Melo, A.I., Galef, G., Madden, M., Fleming, A.S., 2003. Complete maternal deprivation affects social but not spatial learning in adult rats. Dev. Psychobiol. 43, 177–191. Lidfors, L.M., 1993. Cross-sucking in group-housed dairy calves before and after weaning off milk. Appl. Anim. Behav. Sci. 38, 15–24. Lidfors, L.M., 1996. Behavioural effects of separating the dairy calf immediately or 4 days post-partum. Appl. Anim. Behav. Sci. 49, 269–283.
Mason, G.J., 1994. Tail-biting in mink (Mustela vison) is influenced by age at removal from the mother. Anim. Welfare 3, 305–311. Melo, A.I., Lovic, V., Gonzalez, A., Madden, M., Sinopoli, K., Fleming, A.S., 2006. Maternal and littermate deprivation disrupts maternal behavior and social-learning of food preference in adulthood Tactile stimulation, nest odor, and social rearing prevent these effects. Dev. Psychobiol. 48, 209–219. Mormede, P., Andanson, S., Auperin, B., Beerda, B., Guemene, D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C.G., Richard, S., Veissier, I., 2007. Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol. Behav. 92, 317–339. Oostindjer, M., van den Brand, H., Kemp, B., Bolhuis, J.E., 2011. Effects of environmental enrichment and loose housing of lactating sows on piglet behaviour before and after weaning. Appl. Anim. Behav. Sci. 134, 31–41. Orihuela, A., Hernandez, C., 2007. Cortisol response of restricted suckling or artificially milk-feeding to a short term emotional stressor in dairy calves and their dams. Anim. Welfare 16, 49–52. Price, E.O., Harris, J.E., Borgwardt, R.E., Sween, M.L., Connor, J.M., 2003. Fenceline contact of beef calves with their dams at weaning reduces the negative effects of separation on behavior and growth rate. J. Anim. Sci. 81, 116–121. Punzo, F., Ludwig, L., 2002. Contact with maternal parent and siblings affects hunting behavior, learning, and central nervous system development in spiderlings of Hogna carolinensis (Araeneae Lycosidae). Anim. Cogn. 5, 63–70. Roth, B.A., Barth, K., Gygax, L., Hillmann, E., 2009. Influence of artificial vs. mother-bonded rearing on sucking behaviour health and weight gain in calves. Appl. Anim. Behav. Sci. 119, 143–150. Sato, S., Abe, M., 1993. The nature of tongue-playing of cattle under various rearing systems. In: Proceedings of the International Congress on Applied Ethology, Berlin, Germany, p. 78. Ting, S.T., Earley, B., Hughes, J.M., Crowe, M.A., 2003. Effect of ketoprofen, lidocaine local anesthesia, and combined xylazine and lidocaine caudal epidural anesthesia during castration of beef cattle on stress responses, immunity, growth, and behavior. J. Anim. Sci. 81, 1281–1293. Veissier, I., Le Neindre, P., 1989. Weaning in calves: its effects on social organization. Appl. Anim. Behav. Sci. 24, 43–54. Veissier, I., Le Neindre, P., Garel, J.P., 1990. Decrease in cow-calf attachment after weaning. Behav. Proc. 21, 95–105. Veissier, I., Ramirez, d., la, Fe A.R., Pradel, P., 1998. Non-nutritive oral activities and stress responses of veal calves in relation to feeding and housing conditions. Appl. Anim. Behav. Sci. 57, 35–49. Wiepkema, P.R., Van Hellemond, K.K., Roessingh, P., Romberg, H., 1987. Behaviour and abomasal damage in individual veal calves. Appl. Anim. Behav. Sci. 18, 257–268. Würbel, H., Stauffacher, M., 1997. Age and weight at weaning affect corticosterone level and development of stereotypies in ICR-mice. Anim. Behav. 53, 891–900.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Suckling, weaning, and the development of oral behaviours in dairy calves Isabelle Veissier a,b,∗ , Sara Caré c , Dominique Pomiès a,b a b c
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR 1213 Herbivores, BP 10448, F-63000 Clermont-Ferrand, France Istituto di Zootecnica, Università Cattolica del Sacro Cuore, I-29122 Piacenza, Italy
a r t i c l e
i n f o
Article history: Accepted 10 May 2013 Available online 12 June 2013 Keywords: Suckling Oral behaviours Dairy calves Weaning
a b s t r a c t Dairy calves are generally separated from their dam at birth. They express non-nutritive oral activities such as licking or sucking other calves or objects, nibbling, or tongue-playing, which have been related to the absence of sucking a teat and ingestive chewing. We hypothesized that the dam, by its presence, can help focus the oral behaviour of calves towards nutritive activities and thereby limit the development of non-nutritive oral activities. To test this hypothesis, we compared calves suckled by their dam against calves separated from their dam at birth and fed milk through a teat (automatic milk feeder). Cow and calf behaviour was observed before weaning and after weaning at 10 wk of age. Before weaning, the suckled calves were less active than the artificially fed calves. After weaning, suckled calves tended to spend less time on non-nutritive oral activities than non-suckled calves. Before weaning, suckling cows and non-suckling cows showed similar behaviour. Both cows and calves reacted to weaning: cows showed vocalization and agitation, and calves showed increased blood cortisol levels. We conclude that keeping dairy calves with their dam for 10 wk can be beneficial to calves, although weaning induces a degree of stress. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Commercially reared animals are generally separated from their dam before the age at which they would naturally be weaned in free-leaving conditions. Dairy calves are typically separated from their dams within hours of birth and then artificially milk-fed for several weeks (Budzynska and Weary, 2008). Milk is often provided in a bucket, which does not always satisfy the calf’s motivation to suckle (de Passillé, 2001). Behavioural disorders such as excessive sucking on body parts of other calves (cross-sucking) and on pen equipment can be common in calves kept in groups (Lidfors, 1993; de Passillé, 2001). These oral activities can
∗ Corresponding author at: INRA, UMR1213 Herbivores, F-63122 SaintGenès-Champanelle, France. Tel.: +33 473624098; fax: +33 473624518. E-mail address: [email protected] (I. Veissier). 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.05.002
discourage producers from rearing calves in groups due to the higher risks of disorders (navel abscesses, calves drinking urine, etc.), despite the advantages in terms of labour (Kung et al., 1997). Non-nutritive oral activities of calves (cross-sucking, licking, tongue-playing) may be related to insufficient feeding behaviours, i.e. sucking a teat or ingestive chewing (Wiepkema et al., 1987; Sato and Abe, 1993; Veissier et al., 1998). They are also less common when calves are with their dams, even when they are not suckled (Krohn et al., 1999; Fröberg et al., 2008; Roth et al., 2009). Some species-specific behaviours can be learned from the dam, like hunting in spiders (Punzo and Ludwig, 2002) and food preferences (Melo et al., 2006) or recognizing social cues (Levy et al., 2003) in rodents. Proper development of species-specific behaviour likely limits the development of ‘abnormal’ behaviours. Indeed, early weaning has been linked to the development of stereotypic behaviour (Latham and Mason, 2008). For instance,
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in lab mice and in farmed minks, it results in increased rearing, bar-biting or tail-biting (Mason, 1994; Würbel and Stauffacher, 1997). Similarly, once they are weaned, piglets that were reared with a sow whose movements were restricted show higher levels of belly nosing and manipulative activities post-weaning compared to piglets reared with a loose-housed sow (Oostindjer et al., 2011). The quality of the dam-young interaction is thus likely to play a role in the behavioural development of the young animal. As the suckling may thus help young calves develop species-specific behaviours, maternal rearing could limit the development of undesirable non-nutritive oral activities. If this hypothesis was confirmed, then young calves reared with their dam should develop less non-nutritive oral activities than artificially reared calves even if they suck a teat to get their milk, and this effect should be visible after weaning. Nevertheless, even when kept with the dams after birth, young farm animals will still be separated from their dams later in life, typically at 6–9 months of age in beef suckler herds. The separation between the dam and its offspring is particularly stressful for both partners, as shown by vocalization and agitation in cows and calves (Lidfors, 1996) and a slower growth rate in calves (Price et al., 2003; Haley et al., 2004). The aim of the study reported here was to analyze the impact of suckling on the behaviour of cows and calves, to assess the disturbances caused by separation from the dam at weaning, and to check whether non-nutritive oral activities in calves are dependent on previous presence of their dam. 2. Materials and methods 2.1. Animals and experimental design The experiment was conducted at the INRA’s UE1296 Monts d’Auvergne experimental farm (Orcival, France). Fourty-six Holstein cows and calves were followed from calving to 16 wk later. Calving took place in autumn in two consecutive years (Year 1, 24 cows and 24 calves; Year 2, 24 cows and 24 calves). Each year, half the cows suckled their calves (24 suckling cows and 24 suckled calves). During Year 1, the suckling cows and their respective calves stayed together all day long (24 h), whereas in Year 2 they stayed together only from 07:30 h to 18:00 h (i.e. 10.5 h). The remaining cows and their calves were separated immediately after calving (24 non-suckling and 24 artificially reared calves). In each year, two batches of cows and calves were observed: Batch 1 consisted of the 12 cows that calved first and their 12 calves, and Batch 2 consisted of the next 12 cows and their 12 calves. Within each year, calf sex (24 males, 24 females), date of calving (and consequently batch) and calf weight at birth were balanced between the two treatments. In addition, the cows were chosen so that date of calving, cow weight at calving, body condition scores, lactation rank, and milk yield and composition (from previous lactation or estimated from milk index in primiparous cows) were balanced between suckling cows and non-suckling cows. Due to the numerous factors to be balanced between treatments, artificially reared calves and
non-suckling cows were not necessarily related. The interaction between treatment, year and batch corresponds to a group of animals. There were 4 groups of calves or cows per treatment. On Year 1 one male calf suckled by its dam died by accident just before the time of weaning. The data collected from this calf and from another male calf of the same age but artificially reared were removed from the analyses.
2.2. Housing and feeding Calves were followed more closely than cows. Details will thus be given on their living conditions. The suckled calves stayed in a calving pen with their dam for the first 3–4 days of life. They were then moved to a 4.90 m × 5.26 m pen next to the pen where the cows were held. The calves’ pen was bounded by a barrier on the side next to the cow pen that prevented the cows from entering the calves’ pen but allowed the calves to join the cows. On the other three sides of the calves’ pen was bounded by bundles of straw. The floor of the calves’ pen was concrete covered with straw. Five infrared heaters were suspended 1.5 m above the floor of the calves’ pen. The cows’ pen was 9.60 m × 12.20 m, concrete-floored, and the animals had access to cubicles (one cubicle per cow) covered with mats and woodchip. The artificially reared calves were first housed in a pen with a concrete floor covered in woodchip and tethered for 10 days. They were then moved to a 8.50 m × 7.75 m pen where they were free to move. The pen was bounded by a barrier on one side, concrete walls on two sides, and bundles of straw on one side. The floor was concrete covered with straw. The calves were weaned at 10 wk of age, either by separation from their dam (suckled calves) or suppression of milk feeding (artificially reared calves). After weaning, the calves from the two treatments (suckled calves and artificially reared calves) were accommodated in a common 4 m × 7 m pen similar to the pen used to house the artificially reared calves before weaning (walls: one barrier, two concrete walls, bundles of straw; floor: concrete plus straw). The cows did not change pen from before to after weaning. All cows were milked once a day between 06:30 h and 07:30 h. Before weaning, suckled calves received milk from their dams. Artificially reared calves were fed 2.5 L colostrum through a nipple bottle twice on Day 1 after birth, then 2 L of milk twice on Day 2 using the same bottle, and 4 L of milk twice a day from Day 3 to Day 9 using a bucket. From Day 10, these calves were fed milk from an automatic milk feeder fitted with a rubber teat left available at all times (Nutri-Calf Suprême, BouMatic Europe, Saint-Nom-la-Bretèche, France). The calves could drink a maximum of 12 L/day of milk from Day 10 to Day 49, then 9.2 L/day from Day 50 to Day 56, 6.4 L/day from Day 56 to Day 63 and finally 3.6 L/day from Day 64 to Day 70. Before and after weaning, all calves had free access to commercial concentrates (before weaning: Croustivo HP, CCPA Deltavit, Janzé, France; after weaning: Startivo, Union Altitude, Aurillac, France), hay or silage (Dactilis glomerata),
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and water. After weaning, they were also provided with salt from a block. 2.3. Measurements 2.3.1. Behaviour 2.3.1.1. Time budget. The animals were identified by large numbers painted on their flanks, back and forehead to allow the observer to recognize them from a distance. Before weaning, the behaviour of the calves was observed on two days, —one when the calves were 25.7 days old (SE 1.3 days) and one when they were 49.8 days old (SE 1.3 days). All calves from one treatment (suckled calves or artificially reared calves) in a given batch were observed on a given day, and the same-batch calves in the other treatment were observed the next day. The observer entered the shed and stayed next to the pens from 06:30 h. Scan sampling was performed from 07:30 h to 18:00 h with 10-min intervals between scans. At each scan, the observer noted the activity of each calf as detected at first glance. Six exclusive behavioural classes were distinguished in calves: suckling (a cow or the rubber teat of the milk feeder), nonnutritive oral activities, eating (concentrate, hay, silage or straw), miscellaneous activities (licking salt, drinking water, self-scratching, social interaction, or walking), idling (standing up, no activity), and lying down. Non-nutritive oral activities included licking or sucking another animal or an object, nibbling at an object (prehending part of it), and tongue-rolling (making circular movements with the tongue in or outside the mouth). Thereafter, at 28.1 days (SE, 1.2 days) after weaning, the calves were observed on two consecutive days. Scan sampling was performed from 06:00 h to 18:00 h at 5-min intervals between scans. The same list of behavioural classes was used, except that suckling was removed. As the two observation days were consecutive, individual data were averaged over these two days. In Year 2, the behaviour of the cows was also observed before weaning. This was done at the same time as the observation of suckled calves. The same behavioural classes were distinguished in calves and cows, except that suckling a calf and licking another animal were pooled together (social activities) and that walking was considered separately from other activities. The observed behaviours were then encoded using Observer Video Pro® software (Noldus Information Technology, Wageningen, The Netherlands). 2.3.1.2. Cows behaviour at weaning. The behaviour of the cows was observed on the day of weaning and the following 9 days. On each day, we noted which cows vocalized during the day (from after milking to 18:00 h); which cows were agitated on their way from their pen to the milking parlour (vocalizing, stopping, or stepping back), and which cows were agitated during milking (vocalizing, stamping, or kicking). 2.3.2. Cortisol Blood samples (5 mL) were taken from calves by puncture of the jugular vein around weaning. Blood samples were taken at 16:00 h on the day before weaning, at
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weaning, and on the following two days. The samples were immediately centrifuged 3000 × g for 5 min, and plasma aliquots were stored at −20 ◦ C until assayed for cortisol assay. In Year 2, milk samples were taken on the day of weaning and then at 1, 2, 5, 7 and 9 days post-weaning. The milk was immediately stored at −20 ◦ C. Milk samples were defrosted at room temperature, defatted by centrifugation (2400 × g for 20 min at 4 ◦ C). Corticosteroids were extracted from skimmed milk with ethyl acetate. Milk or blood cortisol concentrations were determined by radioimmunoassay with an antibody produced by Cognié and Poulin (INRA, Tours, France; Boissy, 1990). Limit of detection was 0.02 ng/mL and the within and between-assay coefficients of variation were 11% and 22% for low (4 ng/mL) controls and 7% and 14% for high (32 ng/mL) controls. 2.3.3. Calf growth The calves were weighed at birth, then once a week until the end of the experiment using an electronic scale (690 KES, Mettler Toledo, Viroflay, France) with a precision of 200 g. We calculated daily weight gain from birth to weaning and from weaning to 16 wk of age. 2.4. Statistical analyses Statistical analyses were performed using SAS v8.1 (SAS Inst. Inc., Cary, NC). Cortisol concentrations were logtransformed, and percentages of time spent in a given behavioural class were arcsine-transformed to fit the conditions for ANOVA. ANOVA was conducted on quantitative data (% time, cortisol concentration, weight) using mixed models. The following factors were included in the analyses of calf data: treatment, year, batch, sex, time (when appropriate), plus all treatment × year × batch interactions, the treatment × sex interaction, the time × treatment (except for pre-weaning behaviour) interaction, and animal (random factor nested into the treatment, included only when data were collected on the same animals at several time points). The following factors were included in the analyses of cow data: treatment, batch, time, the treatment × batch or time interaction, and animal (random factor nested into the treatment). The time corresponded to the day of observation for pre-weaning behaviours (two separate observation days), to the various days of sampling for cortisol, and to period (before vs. after weaning) for calf growth. In case of repeated measurements (when time is included), the covariance matrix was considered to have a compound symmetry. The treatment × day interaction was not included in analysis of pre-weaning behaviour as the day here had the same meaning whatever the treatment. The results of quantitative data are presented as means ± standard error (SE). Qualitative data (proportion of cows in the various behavioural classes at weaning) were analyzed day-by-day using 2 tests. Only significant effects (P < 0.05) and tendencies (P < 0.10) are reported. We will focus on the effects of the treatment and the year and the interactions between the treatment and other factors.
0.06 0.74 0.01 0.95 0.21 3.65 0.11 7.18 0 1.66 4.96 31.0 5.11 5.21 53.5
a, b, c: values with no common letter differ significantly (P < 0.05; information provided when P < 0.10 for the interaction between treatment and year). a Treat = treatment (suckling vs. artificial rearing).
0.00 0.85 <0.0001 <0.0001 <0.0001 9.7 0.04 47.49 39.69 30.08 0.30 0.13 0.96 0.78 0.17 1.12 2.44 0 0.08 1.93 0.48 b 1.78 0.81 a 1.30 1.79 ± ± ± ± ± 3.44 27.8 9.46 12.1 47.2 0.88 a 2.05 0.65 b 0.94 2.26 ± ± ± ± ± 6.76 28.7 6.66 5.15 52.6 0.50 b 2.27 0.80 a 1.11 2.22 ± ± ± ± ± 3.99 30.0 11.1 12.6 42.2 0.49 b 1.32 0.38 b 0.50 1.24
0.07 0.20 <0.001 <0.001 <0.001 0.34 3.44 1.68 28.1 15.0 44.7 0.93 0.93 0.04 <0.001 0.76 <0.001 0.59 0.01 4.22 60.9 0.10 16.7 0.30 0.40 c 0.78 0.70 0.87 1.15 b 1.79 a ± ± ± ± ± ± 2.08 6.35 6.09 5.88 14.1 65.5 0.41 a 0.80 0.71 0.89 1.2 c 1.83 b ± ± ± ± ± ±
Year 2 12 calves Year 1 11 calves
4.95 8.27 10.4 9.87 8.52 57.9 0.40 ab 0.78 0.70 0.87 1.15 a 1.79 b ± ± ± ± ± ±
After weaning Non-nutritive oral activities Eating Miscellaneous activities Idling Lying down
± ± ± ± ±
<0.001 0.27 0.42 0.72 0.04 0.00 22.9 1.24 0.65 0.13 4.48 11.46
F(treat × year) P(year) F(year) P(treat) F(treat)a Year 2 12 calves
4.15 8.75 1.00 6.45 21.4 58.3 0.4 bc 0.81 0.71 0.89 1.18 bc 1.84 ab ± ± ± ± ± ± 3.09 8.90 4.35 9.76 10.8 62.9 Before weaning Suckling Non-nutritive oral activities Eating Miscelllaneous activities Idling Lying down
3.1.1.3. Time budget of cows before weaning. Before weaning, cow behaviour did not depend on whether or not they suckled calves (percentage time spent eating,
Year 1 11 calves
3.1.1.2. Time budget of calves after weaning. Calf behaviour post-weaning is also reported in Table 1. Calves spent less time on non-nutritive oral activities or lying down and more time on miscellaneous activities or idling in Year 2 than Year 1. There were treatment × year interactions on non-nutritive activities (tendency) and miscellaneous activities (significant). Non-nutritive activities were more frequent in artificially reared calves from Year 1 than in all other calves, and the year effect on miscellaneous activities was more marked in suckled calves. We did not find any other significant effects of the treatment as main factor nor in interaction with other factors. Considering the various non-nutritive oral activities (sucking, licking, nibbling, tongue-playing) separately did not reveal differences between treatments.
Artificial reared calves
3.1.1. Time budget 3.1.1.1. Time budget of calves before weaning. The behaviour of calves before weaning is reported in Table 1. In Year 1, suckled calves spent significantly less time suckling their dam or another cow than artificially reared calves spent time suckling at the milk feeder. In Year 2, the opposite pattern was observed. In general, calves tended to spend less time suckling in Year 2 than Year 1. Suckled calves spent more time performing nonnutritive oral activities than artificially reared calves. More specifically, suckled calves spent more time licking other calves or objects than artificially reared calves (8.05 vs. 5.96% of time, SE = 0.47, F1,39 (treatment) = 9.86, P = 0.003). In contrast, suckled calves spent less time sucking other calves or objects than artificially reared calves (0.397 vs. 1.211, SE = 0.178, F1,39 (treatment) = 13, P < 0.001). Time spent nibbling at objects or tongue-playing was similar between suckled and artificially reared calves (0.220 ± 0.085 and 0.033 ± 0.041, P > 0.10). Suckled calves spent significantly less time eating and more time idling than artificially reared calves. In Year 2, calves generally spent less time eating or on miscellaneous activities and more time idling than in Year 1, and the between-treatment difference in time spent idling was stronger. Artificially reared calves from Year 2 spent significantly more time lying down than suckled calves from the same year and the artificially reared calves from Year 1. We did not find any other significant effects of the treatment as main factor nor in interaction with other factors, except that time spent idling varied between groups of calves (F1,39 (treatment × year × batch) = 10.4, P = 0.003) and that time spent on oral non-nutritive activities depended on batch and treatment (F1,38 (treatment × batch) = 6.42, P = 0.01, with suckled calves from Batch 1 spending more time on such activities than all other calves (10.3 vs. 7.32, SE = 0.79).
Suckled calves
3.1. Behaviour
Behaviour (% scans)
3. Results
P(treat × year)
I. Veissier et al. / Applied Animal Behaviour Science 147 (2013) 11–18 Table 1 Calf behaviour before and after weaning. Calves were either suckled (n = 23) or artificially reared (n = 23). Suckled calves stayed with their dam all day long in Year 1 but only from 07:30 to 18:00 h in Year 2. Weaning took place at 10 wk of age. Observations took place from 07:30 to 18:00 h. Data are expressed as means ± standard errors.
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Fig. 2. Plasma cortisol levels around weaning in suckled calves (–䊉–, n = 23) vs. artificially reared calves (––, n = 23). Blood samples were taken the day before weaning (Day 0), on the day of weaning (Day 1), then on the next two days (Days 2 and 3). Weaning took place at 10 wk of age. Means and standard errors are shown.
(2 = 12.3 on the day of weaning, 31.4 one day after, 15.6 two days after, P < 0.001 in all cases). Cows that had suckled their calves also reacted by showing agitation on the way to the milking parlour and during milking. The difference in the proportion of cows agitated between suckling and non-suckling cows was significant on the day after weaning (2 = 10.8 on the way to milking and 6.62 during milking, P = 0.001 and P = 0.01, respectively). The same difference between suckling and non-suckling cows was observed on the next day on the way to the milking parlour (2 = 10.8, P = 0.001), and to a lesser extent at 5 and 7 days post-weaning on the way to milking and two days post-weaning during milking (2 = 3.07, P = 0.08 in all cases). 3.2. Cortisol
Fig. 1. Cow behaviour at weaning. The proportions of cows that vocalized or were agitated are compared between suckling cows (–䊉–, n = 24) and cows not suckling (––, n = 24).
walking, interacting with another animal, idling, and lying by suckling vs. not suckling cows: 24.1 vs. 22.3 (SE = 1.55), 2.11 vs. 2.71 (SE = 0.40), 1.65 vs. 0.85 (SE = 0.38), 25.9 vs. 24.5 (SE = 1.82), 39.8 vs. 44.7 (SE = 2.79), P > 0.10 in all cases).
3.1.2. Cows’ behaviour at weaning On the day of weaning and the following 9 days, the nonsuckling cows never vocalized during the day and never displayed agitation on the way to the milking parlour or during milking (Fig. 1). Most cows that had suckled their calves vocalized during the day of weaning and then on following days up to Day 7 post-weaning. Vocalization was strong on the day after weaning, when 17 out of the 24 suckling cows vocalized. The difference in the proportion of cows vocalizing between suckling and non-suckling cows was significant from weaning to two days after weaning
Suckled calves had significantly higher blood cortisol concentrations than artificially reared calves (cortisol from the day before weaning to two days after weaning, 9.65 vs. 8.10 ng/mL, SE = 0.52, F1,36 (treatment) = 4.83, P = 0.03). Cortisol concentrations increased significantly from the day before weaning to the next days, and tended to decrease thereafter (F3,132 (day) = 10.9, P < 0.001, Fig. 2). Similar changes over time were observed in both suckled and artificially reared calves (F3,132 (day × treatment) = 0.44, P > 0.10). Calf plasma cortisol concentrations were significantly higher in Year 2 than Year 1 (11.5 ± 0.51 vs. 6.20 ± 0.54 ng/mL, F1,36 (year) = 67.2, P < 0.001), regardless of how calves were reared (F1,36 (year × treatment) = 1.33, P > 0.10). Plasma cortisol levels tended to be higher in female than male calves (9.71 ± 0.52 vs. 8.03 ± 0.56, F1,36 (sex) = 3.69, P = 0.06), whatever the treatment (F1,36 (sex × treatment) = 2.67, P > 0.10). milk cortisol concentration averaged Cow 1.45 ± 0.23 ng/mL, regardless of treatment, day postweaning, batch, or their interactions (P > 0.10 in all cases).
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Fig. 3. Weight of calves suckled by their dam (–䊉–, n = 23) or artificially milk-fed (––, n = 23). Calves were weighed once a week from birth to 16 wk of age. Weaning took place at 10 wk of age. Means and standard errors are shown.
3.3. Growth Calves suckled by their dam grew less fast than artificially reared calves (average daily weight gain, 0.966 ± 0.033 vs. 0.859 ± 0.033 kg, F1,36 (treatment) = 5.19, P = 0.03). The difference was especially significant after weaning (artificially reared calves, 1.01 ± 0.045; suckled calves, 0.800 ± 0.045 kg, F1,42 (treatment × period) = 6.86, P = 0.01) (Fig. 3). There was a significant treatment × year × period interaction on calf growth (F1,42 = 4.45, P = 0.04). In Year 1, suckled calves showed a slower growth rate after weaning (0.647 ± 0.066 kg) compared to their own growth before weaning (0.971 ± 0.066 kg) or to all other calves at the same period (artificially reared calves after weaning, 1.019 ± 0.066 kg in Year 1 and 1.021 ± 0.062 kg in Year 2; suckled calves after weaning, 0.953 ± 0.063 kg in Year 2). Male calves grew faster than female calves, whatever the treatment, year, or period (0.975 ± 0.036 vs. 0.850 ± 0.033 kg, F1,36 (sex) = 5.99, P = 0.01). 4. Discussion In brief, prior to weaning, cows behaved similarly whether or not they fed their calves, and calves fed by their dam spent less time eating and sucking other calves than artificially fed calves. Weaning induced vocalizations and agitation in the cows and increased blood cortisol levels in the calves. The calves that had been maintained all day long with their dam before weaning (suckled calves, Year 1) exhibited fewer non-nutritive oral activities after weaning. First, prior to weaning, we did not observe differences in behaviour between cows that suckled their calves and those that did not. Calves suckled for 23 (±2.5) min per day. Suckling and non-suckling cows were equally active during the day, as assessed through time spent walking, eating, idling, and lying down. Suckling cows performed more social activities, but the difference was not significant. We assumed that if cows were frustrated by not being able to suckle their calves, they would be more active, e.g.
spending more time walking and looking for calves, but this was not the case. Therefore, our results do not find evidence that cows are affected by being unable to suckle. Second, prior to weaning, the behaviour of calves reared with their dam differed from that of calves fed artificially. In Year 2, the suckled calves were more often observed suckling their dam than the artificially fed calves were seen at the milk feeder, as reported by Fröberg and Lidfors (2009). This pattern was opposite in Year 1, leading to a significant interaction between treatment and year. This interaction may be only apparent because in Year 1, suckled calves stayed with their dams all day long (except while cows were being milked). Hence, although not observable here, it is logical to assume they also suckled during the night and that on the whole day they spent more time suckling than artificially fed calves as observed on Year 2. Suckled calves were less active than artificially reared calves: they spent more time lying down or idling, especially in Year 2, and less time eating, as in Fröberg and Lidfors (2009). Suckled calves had access to the cubicle pen housing their dams, and they were often observed next to the cows. The presence of the dam may have had a calming effect on the calves, resulting in lower activity levels. Again a significant interaction between treatment and year was noticed; with suckled calves spending more time idling and less time lying down in Year 2 than in Year 1. It thus seems that the calming effect of cows is less efficient when calves are separated from them at night. More surprisingly, prior to weaning, suckled calves spent more time licking objects and other calves than artificially fed calves. We speculate that suckled calves, being in a larger environment and with cows, had more opportunities to perform oral activities, e.g. they had access to more objects in their environment (cubicles bars for instance). By contrast suckled calves spent less time sucking other calves or objects, a result consistent with those of Roth et al. (2009). Cross-sucking can be due to the high motivation of calves to suck that is not satisfied when they are fed milk artificially (de Passillé, 2001). Our results suggest that this may be true also when an artificial teat is available at all time during the day. Therefore, it seems that a milk feeder is far less efficient than a dam to drive the sucking activity of calves. Third, after weaning, although all the calves were kept together, we still observed differences in behaviour between calves that had been suckled by their dam and those separated from their dam at birth. The calves that had been suckled by their dam tended to spend less time on non-nutritive oral activities, which included licking or sucking another calf or an object, nibbling at an object, and tongue-rolling. These behaviours remained rare, since calves spent only about 5% of their day performing them. This difference between suckled and artificially reared calves was more marked in Year 1. In Year 1, suckled calves spent all day with their dam – except while the cows were being milked – whereas in Year 2 they were separated from the dam during the night. This result suggests that the presence of the dam at an early age can have an impact on the later behaviour of the calves, namely on their tendency to express non-nutritive oral activities. Krohn et al. (1999) already observed that calves that stayed with their dam for the first four days of life express less non-nutritive sucking
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after their weaning, especially if they had suckled their dam during these first two days. These activities are linked to the lack of sucking (especially for milk intake) and to ingestive chewing (needed for the intake of solid foods) (Illmann and Spinka, 1993; Veissier et al., 1998; de Passillé, 2001). It has been well described that the dam has an influence on it offspring, especially for the development of species-specific behaviour (see Section 1). We hypothesized that cows help young calves focus their oral activities towards nutritive elements, i.e. milk (when suckling the udder) or solid foods, or towards their dam (suckling again, licking). This hypothesis is confirmed by the fact that in our experiment, before weaning, suckled calves spent less time sucking objects or other calves than artificially fed calves. We also hypothesized that the mere presence of the dam can further reduce non-nutritive oral activities in calves after the calves have been separated from their dam. Our results do not fully confirmed that hypothesis since we only observed a tendency in Year 1 and no significant effect in Year 2 (when cows and calves were separated at night). Nevertheless, together with those from Krohn et al. (1999), they bring evidence that the dam has strong effect on the development of the oral behaviour of calves. The underlying processes also need to be investigated —does a calf learn by observing cows? do olfactory cues play a role, by focusing the calf’s attention on the udder? do interactions between dam and calf influence the calf’s behaviour towards other stimuli? Fourth, at weaning, cows that had suckled their calves demonstrated a response to the separation from their calves. Cattle separated from their social partners vocalize and display intense agitation, their heart rate increases, and cortisol gets released into the blood (Boissy and Le Neindre, 1997), and these responses suggest that cattle are highly disturbed by separation from peers. In our experiment, when cows were separated from their calves, behavioural responses (vocalization, agitation) remained marked for 2 days post-weaning and some cows even reacted for up to 7 days post-weaning. We measured cortisol concentrations in the milk of the cows during the two daily milkings after weaning. Regardless of whether or not the cows were separated from their calves, their milk cortisol content was 1.45 (±0.23) ng/mL. Given that the proportion of cortisol in milk is about 10% that of blood (Mormede et al., 2007), our cows had about 14.5 ng/mL in blood, which is visibly higher than basal cortisol levels in cattle (generally reported as around 5 ng/mL) but nevertheless far lower than in acutely stressed cattle (Ting et al., 2003; Orihuela and Hernandez, 2007). Therefore, there is evidence that cows are disturbed by the absence of their calves after weaning (at least for two days), but not enough to induce clear neuroendocrine stress responses. Fifth, weaning was followed by an increase in blood cortisol levels in calves. Although calves that had been suckled by their dams had higher average blood cortisol levels, the increase post-weaning was not significantly more marked than in calves that had previously been artificially milkfed. Calves are known to react strongly to the separation from their dam: they vocalize, are restless, and their weight gain remains slower for several weeks (Haley et al., 2001; Price et al., 2003). Like for cows, weaning suckled calves is likely to have induced behavioural responses (vocalization,
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agitation). These responses may have spread among all calves as they were accommodated together, resulting in increased cortisol in both suckled and non-suckled calves. However, this explanation remains speculative, as we did not monitor calf behaviour immediately after weaning. Suckled calves put on less weight after weaning than their artificially fed counterparts (−0.2 kg/day). This result is consistent with the literature (Price et al., 2003; Haley et al., 2005; Froberg et al., 2011). The suppression of milk cannot explain this effect, since all calves were weaned off milk at the same age. Since maintaining visual contact between cows and calves can limit the lower post-weaning growth (Price et al., 2003; Haley et al., 2005), it is likely that stress due to the separation is, at least in part, the causal factor. As a matter of fact, calves remain attached to their dam for at least 3 wk after weaning (Veissier and Le Neindre, 1989; Veissier et al., 1990). Strategies for reducing stress at weaning have been proposed, such as maintaining visual communication between cows and calves (Price et al., 2003) or suppressing milk first before separating the two animals (Haley et al., 2005). In the present experiment, the negative effects of weaning on the growth of suckled calves was more marked in Year 1 when the calves had been with their dam all day long, than in Year 2 when cows and calves were separated at night. It is likely that in Year 2, the suckled calves were already accustomed to being separated from their dam and did not experience as much stress as those of Year 1 at the definitive separation at weaning. Our work confirms that weaning, combining both the suppression of milk and separation from the dam, is stressful for suckled calves, especially when they are not used to being separated from their dam. In conclusion, cows do not seem to miss suckling when they are separated from their calves soon after birth, but they are disturbed when the separation occurs later, after 10 wk of suckling. Similarly, suckled calves are disturbed when they are separated from their dam at weaning, and this separation can reduce their growth rate. Calves that are suckled by their dam later display fewer oral non-nutritive activities than artificially fed calves. The presence of the dam may orient the oral behaviour of the calf to the point that the calf is less ready to develop abnormal behaviours (in this case non-nutritive oral activities). We conclude that suckling may be beneficial to calves, but that the weaning process requires a special attention in order to minimize separation-induced stress. Acknowledgements The authors thank Marc Barbet from the UE1296 Monts d’Auvergne farm for helping with the execution of the experiment. We also thank the UMR1213 Herbivores staff for their valuable assistance, especially Stéphane Andanson and Christine Ravel for the cortisol assays and Christophe Mallet for his help with the behavioural recordings. References Boissy, A., 1990. Les réactions émotives chez les bovins domestiques femelles (Bos taurus L.). Quantification et variations sous l’influence de facteurs environnementaux et hormonaux. Thèse de Doctorat de l’Université de Paris XIII, 224 pp.
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