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Does nutritive and non-nutritive sucking reduce other oral behaviors and stimulate rest in calves?¹

I. Veissier^*,2, A. M. de Passillé, G. Després^*, J. Rushen, I. Charpentier^*, A. R. Ramirez de la Fe^*,3 and P. Pradel

^* INRA URH-ACS Centre de Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France; and Dairy and Swine Research and Development Centre, Agriculture and Agri-Food Canada, Lennoxville, Quebec, J1M 1Z3, Canada; and and INRA, Domaine de Marcenat, 15190 Marcenat, France

² Correspondence:
E-mail:
veissier{at}clermont.inra.fr.

	Abstract

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After a milk meal, bucket-fed calves show non-nutritive oral activities, including cross-sucking, and this can discourage producers from rearing them in groups. Sucking is known to induce a quiet state in humans and rats. We examined if nutritive sucking affects non-nutritive oral activities in calves, if it reduces arousal (assessed through behavior and cardiac activity), and if sucking a dry teat can compensate for the lack of nutritive sucking. In Exp. 1, the behavior and the cardiac activity of individually housed calves fed milk from a bucket were compared to those of calves fed milk through a teat. During the meal, the heart rate of bucket-fed calves was higher than that of teat-fed calves (P < 0.0001). After the meal, only bucket-fed calves displayed bar sucking. Compared to the teat-fed calves, they spent more time licking their pen or their neighbor (P < 0.001 and P < 0.05), their heart rate was less variable (P < 0.01), and they lay down with the head unsupported by the neck less quickly (latency to lie down: 51 min vs 42 min, P < 0.05). In Exp. 2, individually-housed bucket-fed and teat-fed calves were observed with or without access to a non-nutritive teat after the meal. Bucket-fed calves sucked the dry teat for longer than teat-fed calves (P < 0.001). In bucket-fed calves, access to the dry teat reduced the time spent nibbling (P < 0.01) and tended to shorten the latency to lie down (P < 0.10). In Exp. 3, group-housed bucket-fed calves were compared with group-housed calves fed with an automatic teat feeder system. Bucket-fed calves spent more time nibbling at 1 mo, but at 3 mo they spent less time nibbling and cross-sucking; they drank more milk and put on more weight. We conclude that, for calves housed individually, teat-feeding reduces non-nutritive oral activities after the meal and induces a calmer state than bucket-feeding. Providing calves with a dry teat partly compensates for the lack of nutritive sucking. For calves housed in groups, the use of an automatic teat feeder may not reduce calves’ motivation for sucking. No improvement of growth was observed with teat-feeding either with a teat-bucket or with an automatic feeder.

Key Words: Behavior • Calves • Heart Rate • Stress • Sucking

	Introduction

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After drinking milk, calves often suck each other or suck parts of their pen, especially when they are bucket-fed (Kopp et al., 1986; de Passillé, 2001; Loberg and Lidfors, 2001). Cross-sucking can discourage producers from rearing milk-fed calves in groups despite labor advantages (Kung et al., 1997). Thus it is important to understand calves’ sucking behavior.

In infant humans and rats, non-nutritive sucking has a calming effect, reducing behavioral agitation due to stressful events (Blass, 1994; McCain, 1995). Sucking also promotes the secretion of insulin, CCK and gastrin, and reduces that of somatostatin (Uvnäs-Moberg et al., 1987). These influences, mediated by the vagal nerves, might explain the higher weight gain of young mammals that suck for milk or suck a pacifier (Uvnäs-Moberg et al., 1987; Blass, 1994).

In calves, sucking behavior is stimulated by milk (de Passillé et al., 1992; 1997; de Passillé, 2001). Sucking motivation, however, appears to be reduced more by sucking behavior than by the ingestion of milk (Rushen and de Passillé, 1995). Non-nutritive sucking increases plasma concentrations of CCK and insulin (de Passillé et al., 1993), but little is known of the effect of sucking on other physiological systems associated with vagal activity or on other aspects of the calves’ behavior. Growth rates of teat-fed calves are either higher (Hammel et al., 1988), equal (Hopkins, 1997) or slightly lower (Szucs et al., 1983) than those of bucket-fed ones. These discrepancies may be due to increased risk of microbial contamination of teats due to inadequate cleaning (Hepola et al., 1999).

The present article examines the effect of nutritive and non-nutritive sucking on oral and resting behavior, cardiac activity, and growth of calves. Heart rate variability is taken as an index of the vagal tone (Task Force, 1996). Since calves readily suck a non-nutritive teat, we also compare the effects of non-nutritive sucking after a meal with nutritive sucking.

	Materials and Methods

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General Procedures
In Exp. 1, we assessed the combined effect of nutritive and non-nutritive sucking behavior by comparing the behavior and cardiac activity of calves fed milk through a teat ("teat-fed") and calves fed milk in a bucket ("bucket-fed"). In Exp. 2, we examined the relative effects of nutritive and non-nutritive sucking on resting and oral behaviors of calves. Experiment 3 was a practical trial investigating the usefulness of an automatic feeding device, based on teat-feeding, in order to satisfy the need for sucking of calves. Stress-related parameters (presence of ulcers, thymus and adrenals weight, synthesis of catecholamines) were also taken into account in Exp. 1 and 3. Experiments 1 and 3 took place at the INRA experimental farms based, respectively, at Marcenat and Orcival (France). Following French regulations for experiments on animals, I. Veissier and G. Després are licensed for experimentation on animals, and all the people taking care of the animals or taking samples from them had received a special course approved by the French Ministry of Agriculture. Experiment 2 took place at the Lennoxville Research Center of Agriculture and Agri-Food Canada, where the animals were reared and housed in accordance with recommended guidelines (CARC, 1998) and where all experimental procedures were approved by the local animal care committee in accordance with the requirements of the Canadian Council on Animal Care.

Experiment 1
Animals and Housing.
Twenty-four male Holstein calves were purchased from commercial farms at 2 wk of age, and housed in 0.9 x 2 m individual pens, with wooden slatted floors (slats, 6 cm wide and slots, 4 cm wide). Pens were separated from each other by wooden partitions, which were solid on one side and open on the other one (slats, 10 cm and slots, 5 cm), so that each calf could see another calf in an adjacent pen. The two neighboring calves that could see each other were always fed in the same way. The partitions were extended 40 cm beyond the front of the pens in order to prevent calves touching each other when passing their head through the feeding barrier, which was made of metal bars. The bottoms of the pens were made of solid wood. The calves were fed milk replacer (Cremunic Sanders, Paris, France; proteins, 21.5%) at 0830 and 1600 according to feeding plans used to produce pale veal meat (Toullec, 1988); the milk was prepared at 40°C and served between 36 and 37°C to the calves. The amount of milk given each day increased from 840 g milk replacer powder at the beginning of the experiment to 3,040 g at 4 mo of age. The milk replacer was provided in buckets which were removed when less than 100 mL was left, which is the amount of milk the calves could not take out of the bucket. Calves were also provided with small amounts of solid food: 100 to 200 g concentrates (Startivo Sanders, Paris, France; fiber, 7%; proteins, 16%; components, cereals, by-products of cereals, oilseeds, fruits, and sugar) and 450 g chopped straw, which was served between the two milk meals. The lights were on in the barn between 0700 and 1730, the air temperature was maintained between 12 and 15°C, and the humidity ranged between 70 and 80%. The health of the calves was checked three times a day, during the distribution of feed, and appropriate medical treatments were given when necessary. Hematocrits were measured when the calves were 2 mo old, and 1 mL of iron (Imferon, Sanofi, Paris, France, 0.1 g iron/mL) was injected per point of packed-cell volume below 32%. Calves were slaughtered at 4 mo of age.

Experimental Treatments.
The calves were randomly divided into two treatment groups. Twelve calves received their milk in open buckets (bucket-fed calves). Twelve calves received their milk in teat buckets: a rubber teat (11.5 x 3 cm; wall thickness, 3 mm, orifice, 5 mm; Noe Elevage, Ucaab, France) was placed at the bottom of the bucket, which was placed 40 cm above the floor, and the calves had to suck the teat to ingest the milk (teat-fed calves). To control for non-nutritive sucking, bucket-fed calves did not have access to any object they could easily suck (such as a piece of tire as in Veissier et al., 1997), although they could suck the bars of the pen. In addition, the calves could lick each other through the gaps in the side partitions.

Measures
Behavior.
When the calves were 1.5 mo old and 2.5 mo old on average (that is about 79 and 105 kg body weight), they were observed continuously from 15 min before the delivery of milk until 60 min after the removal of the bucket. In addition, on two consecutive days when the calves were 3 mo old, their behavior was scan sampled between 0700 and 1800, that is when the lights were on. For these observations, scans were 5 s long, and intervals between scans were 3 min; only the initial state of the animal at the very beginning of each scan was noted (see description below of the states considered). Observations (both for continuous observations and scan samples) were made via video cameras (Sony SPT-M128CE; Sony Corp., Tokyo, Japan). Recording was done at a rate of 50 frames/s on time-lapse video recorders (Sony SVT-1000P; Sony Corp.). The behavior was encoded and analyzed using Observer software (Noldus, The Netherlands). Two categories of behavioral states were used, the states within each category being mutually exclusive. The first category involved the general postures of the calves and included: standing, lying head supported (lying with head up supported by the neck), lying head unsupported (chin on the floor or head on the back of the calf). The second category involved specific behavioral activities and included: drinking or sucking milk (having the muzzle in the bucket or sucking the teat), sucking the bars of the pen (part of a bar of the feeding barrier is in the mouth of the calf and repeated sucking movement is observed), licking a neighboring calf (the tongue is outside of the mouth and reaches another calf through the slots), self-licking (the calf licks itself), licking parts of the pen (the calf licks a bar of the feeding barrier, a partition, or the floor), nibbling at parts of the pen (the calf takes part of a bar or a partition in its mouth and bites it), eating solid feeds (the muzzle of the calf is in the bucket of solid feeds), and inactivity (none of the previous activities). Butting was recorded as an event, that is, without a duration and not interrupting behavioral states. The frequency and duration of all behaviors were calculated per unit of time except for butting, for which only the frequency was recorded. The unit of time was 5 min for observations around meals, and 30 min for observations over daytime. In addition, the latency to lie down after the meal was calculated.

Cardiac Activity.
An electrocardiogram was recorded around morning milk meals, during the same time periods as behavioral observations (from -15 min to +60 min after the meal). Calves were accustomed to the presence of the experimenters and to having electrodes on their thorax during the first 3 wk after their arrival. Two electrodes (Vitrode, Nihon Koeden, Tokyo, Japan) were fixed on the skin of the animal, 45 min before the meal. One electrode was placed just behind the right scapula, and the other on the chest, just behind the left elbow. The area of skin where the electrodes were attached was shaved the day before a recording. The electrodes were connected to a telemetric transmitter-receiver system (Lifescope; Nihon Koeden), and the signal was then transferred to a MacLab system (A.D. Instruments, Hastings, United Kingdom) connected to an Apple computer, with 100 samples taken per second. Two series of recordings were run. The first series took place 2 wk after the completion of the first series of behavioral observations. For the second series, the electrocardiogram and the behavior were recorded simultaneously. The MacLab software was used to calculate the mean instantaneous heart rate and its standard deviation over each minute. All electrocardiograms were visually inspected to remove any portion where artifacts were suspected (no QRS observed). On the first 10 recordings, we checked that the mean instantaneous heart rate calculated corresponded to the number of QRS waves seen on the electrocardiogram.

Feed Intake, Growth, and Post-Mortem Measurements.
Feed refusals were noted every day. Calves were weighed 2 h before the evening meal when they were 3 and 5 mo old. Feed efficiency was calculated by dividing the amount of milk powder eaten by a calf by its growth during the same period. At slaughter, the abomasi were opened and inspected, and any erosion, ulcer, or scar was noted (Wiepkema et al., 1987). The adrenal glands were weighed and then frozen in liquid nitrogen. The activity of tyrosine hydroxylase (TH) and that of phenylethanolamine N-methyl transferase (PNMT), two enzymes limiting the synthesis of catecholamines, were further determined in the adrenal medulla, using the method described in Lemaire et al. (1993). Intra- and interassay CV are 3.04 and 13.05% for TH and 12.00 and 10.85% for PNMT.

Statistical Analyses.
The SAS software (SAS Inst. Inc., Cary, NC) was used to process the data. Durations of behaviors were expressed as a percentage of time and transformed into arcsines before analyses. GLM analyses were run to test the effects of the feeding treatment (bucket-feeding vs teat-feeding). In all analyses, the calf was taken as the unit of observation. Data on behavior and cardiac activity that were collected around the morning milk meal were analyzed with a model that included the age of the calf and the time of observation as repeated measures factors except for latencies of behavior for which the only repeated measures factor was the age of the calf. The day and the time within the day were considered as repeated measures factors for data collected during the whole daytime. When the hypothesis of either a Gaussian distribution or homogeneous variances was rejected, Mann-Whitney analyses were performed. The results section will focus on significant results (P < 0.05). However a P-value between 0.05 and 0.10 will be considered as a trend. Untransformed data are presented in the text and in the figures.

Experiment 2
Animals and Housing.
Twenty-nine male Holstein calves were purchased from commercial farms at 2 wk of age, housed in individual pens, 2.1 x 1.85 m and separated by metal bars, with wood shavings as bedding. They were fed milk replacer (Lacvor Élevage, Quebec, Canada; proteins, 20%) twice a day at 0800 and 1600, according to a feeding plan similar to that of Experiment 1. The milk replacer was at 30 ± 3°C when distributed. Calves were also provided with 200 g alfa-alfa hay served after the 1600 milk meal. The minimum air temperature was 20°C with variations of less than 8°C over a day. The air humidity was not controlled. The lights were on from 0600 to 1800. The health of the calves was checked twice a day, during distribution of feed, and appropriate medical treatments were given when necessary. The calves were given an i.m. injection of 2 mL of Ironol at their arrival and then were given a vitamin and mineral supplement added to the milk during the first 10 d in order to ensure good health.

Experimental Treatments.
The calves were randomly divided into two treatment groups. One group of 14 received their milk replacer through a teat feeding system described in Haley et al. (1998). The other group of 15 calves was fed milk replacer in ordinary buckets, and during the meal a dry teat was fixed to the bars of the pens so the calves could suck it after the meal (see Rushen and de Passillé, 1995). The dry teat was removed no earlier than 10 min after the end of the meal. Both nutritive and dry teats were 20 x 100 mm, made of rubber, with wall thickness of 4 mm and a 4-mm orifice (Group C.A.L.F. supersuckler; Milk Specialities Co., Dundee, IL). They were fixed 70 cm above the floor.

The week before the start of the experiment, we checked that each calf sucked the dry teat immediately after drinking milk and we measured the time it sucked. This was taken as the reference for the duration of non-nutritive sucking. During the experimental period of 4 d, the calves had access to the non-nutritive teat on two of these days, while for the other 2 d, the calves did not have access to the non-nutritive teat. For teat-fed calves, the presence of a non-nutritive teat was ensured by leaving the teat available to the calf for at least 20 min after the meal as opposed to removing it immediately after the milk was consumed. The order of the condition of observation (dry teat/no dry teat) was balanced across calves and was reversed from 1 d to the next for each calf.

Measures
Behavior.
The calves were observed using video cameras (Panasonic WV-BL200; Panasonic Canada Inc., Mississauga, ON, Canada) with recordings made at a rate of 15 frames/s on time-lapse video cassette recorders (Panasonic AG-6730; Panasonic Canada Inc.). When they were 3 mo old, that is about 130 kg, they were observed after the morning milk meal for 60 min from the removal of the bucket. The same software (Observer; Noldus, The Netherlands), and the same behavioral patterns (with the addition of sucking the dry teat) were used as in Experiment 1. The time spent by calves in any behavioral state and the frequency of butting were calculated per unit of time. In addition, the latency to lie down after the meal was calculated.

Cardiac Activity.
The heart beats of the 15 bucket-fed calves were recorded by a remote system (Polar Electro Oy, Kempele, Finland) described in de Passillé et al. (1995). Belts containing the sensors were attached around the chest of the calves at least an hour before recording was started. Using 5 other calves, of the same breed, weight, and age of those used in Experiment 2, we checked that the mean heart rate given by this system was similar to that obtained with the Lifescope system used in Experiment 1. We calculated the mean heart rate during a 5-min interval between 20 and 10 min before meal, during milk intake, during sucking (or estimated sucking time if the teat was absent), and from 12 to 18 min after the meal.

Feed Intake and Growth.
Feed refusals were noted everyday. Calves were weighed 2 h before the evening meal on arrival and at the end of the experiment, 19 wk later. Feed efficiency was calculated as in Experiment 1.

Statistical Analyses.
The SAS software (SAS Inst. Inc.) was used to process the data. GLM analyses were run with the following factors included in the models:

where a_i, b_j, and c_k represent the fixed effect of the feeding treatment (bucket-feeding vs teat-feeding), the condition of observation (dry teat vs no dry teat), and the time of observation, d_l/j represents the random effect of the calf (nested in the feeding treatment), and e_ij, f_ik, g_jk, and h_ijk represent interactions between feeding treatment and condition of observation, between feeding treatment and time, between condition of observation and time, and between feeding treatment, condition of observation, and time. Fixed effects were tested against the random effect of the calf so that the calf was taken as the unit of observation. For data on feed intake and growth, the factors condition of observation and time were removed from the model and for data on latencies of behavior, only the time factor was removed. When the hypothesis of either a Gaussian distribution or homogeneous variances was rejected, Mann-Whitney analyses were performed on data summed over a whole observation period. The results section will focus on significant results (P < 0.05). However a P between 0.05 and 0.10 will be considered as a tendency.

Experiment 3
Animals and Housing.
Twenty male Holstein calves were purchased from commercial farms at 2 wk of age. They were fed milk replacer (Cremunic) as in Experiment 1 (same feeding plan and same temperature). Calves were also provided with 100 to 200 g concentrates (Startivo; see Experiment 1) everyday at 1000. The health of the calves was checked three times a day, during the distribution of feed, and appropriate medical treatments were given when necessary. Hematocrits were measured and iron (Imferon; Sanofi) was injected as in Experiment 1. The calves were group housed in two 4.5 x 6 m pens, separated with bars which allowed them to see, smell, lick, or rub against each other. Wood-shavings were used for bedding, and fresh shavings were added twice a week. The air temperature of the barn varied between 2 and 12°C. The lights were on between 0600 and 1930. Calves were slaughtered at 4 mo of age.

Experimental Treatments.
The calves were randomly allocated to two groups. In one group (bucket-feeding), calves were fed milk replacer from buckets twice a day at 0830 and 1600. The buckets (one per calf) were placed beyond a self-locking barrier so that each calf could drink only from its bucket. In the other group (automatic feeding), milk was delivered by an automatic device fitted with a teat (Alpha-Laval Feed-Veaux, Delaval, Tumba, Sweden). The 35 x 101 mm teat was made of rubber with walls of 3.5 mm and an orifice of 5 mm. It was placed 65 cm above the floor and was always available. Each calf of this group was identified by an electronic key to control individual intakes. The calves had free access to the feeder but had to take at least two meals to get all of their ration (one between 0000 and 1200 and one between 1200 and 2400). Within these two periods, a calf could come and drink from the feeder several times until it drank half its daily ration. The amount of milk available per day was equal to that drunk by bucket-fed calves. The teat remained available all day, that is, a calf could suck it even if it had already drunk its ration of milk.

Measures
Behavior.
Scan sampling with direct observation was used. The calves were observed every 10 min from 0600 to 1930 (that is when the lights were on), when they were 20, 33, 54, 75, and 96 d old. Every 10 min, the behavior of each calf was recorded at first glance. The behavioral patterns recorded were the same as in Experiment 1. In addition, when the calves were 105 d old, they were continuously observed from 0900 to 1600, and cross-sucking (defined as a calf sucking any part of another calf’s body) was recorded. At this age, the time spent for milk intake was assessed by direct observation for bucket-fed calves and via the records of the automatic device for the others. The time spent by calves in any behavioral state and the frequency of cross-sucking were calculated per 30 min of observation.

Feed Intake, Growth, and Post-Mortem Measurements.
Milk and concentrate refusals were noted everyday. Calves were weighed every 2 wk, 2 h before the evening meal. As in Experiment 1, feed efficiency was calculated, and at slaughter, the abomasi were inspected and the adrenal glands were weighed and frozen in liquid nitrogen for further determination of the activity of tyrosine hydroxylase and of phenylethanolamine N-methyl transferase using the same method as in Experiment 1.

Statistical Analyses.
In this experiment, because we had only two groups of calves, the treatment effect was linked to the group effect, which must be borne in mind when interpreting the results. The SAS software (SAS Inst. Inc.) was used to process the data. Duration of behaviors was expressed in percentage of time and arcsine transformed before analyses. GLM analyses were used to compare the two groups of calves (bucket-feeding vs automatic feeding). Behavioral data were analyzed using a model in which the age of the calf was a repeated measures factor. When the hypothesis of either a Gaussian distribution or homogeneous variances could not be accepted, Mann-Whitney analyses were performed. Proportions of calves were compared with a ² test.

	Results

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Experiment 1: Behavior
Morning Milk Meals.
Teat-fed calves took more time to drink the milk than bucket-fed ones (9 min 44 s vs 2 min 58 s, SE = 19 s, F_1,22 = 68.33, P < 0.001). Meals were interrupted more frequently in teat-fed calves (number of drinking bouts: 3 vs 1 bout, SE = 0.4, F_1,22 = 11.7, P < 0.01), due to more frequent butting (11 vs 1 butt during the meal, SE = 1.9, F_1,22 = 15.7, P < 0.01). Activities around the morning meal and their related statistics are shown in Figure 1. Sucking bars of the pen were observed only in bucket-fed calves and during the 10 min following the meal. Licking parts of the pen or a neighboring calf was frequent during the 25 min following the meal. Compared to their teat-fed counterparts, bucket-fed calves spent more time licking a neighboring calf during the first 15 min, and more time licking parts of their pen between 5 and 25 min after the meal. Calves lay down about 20 min after the end of the meal. Teat-fed calves adopted the head-unsupported position sooner than the bucket-fed ones (latency to lie down with head unsupported: 42 vs 51 min, SE = 1.5, F_1,22 = 6.2, P < 0.05) and spent more time in this posture than bucket-fed calves between 35 and 45 min after the meal (Figure 2).

View larger version (16K): [in this window] [in a new window]   Figure 1. Experiment 1. Activities of bucket-fed calves vs teat-fed calves around the morning milk meal. ANOVA for repeated measures revealed significant differences between treatments (respectively, for bar-sucking, licking a neighbor calf, and licking parts of the pen: between SEM = 3.5, 6.7, and 9.5, F1,22 = 7.5, 18.6, and 6.3, P < 0.01, 0.001, and 0.05), changes over time (within SEM = 0.8, 1.6, and 1.5, F13,286 = 7.3, 7.1, and 8.4, P < 0.0001 in all cases), and interaction between treatment and time (F13,286 = 7.1, 7.4, and 2.6, P < 0.0001 in all cases but the last, 0.01). **P < 0.01 and *P < 0.05 for comparison between bucket-fed and teat-fed calves at specific intervals.

View larger version (14K): [in this window] [in a new window]   Figure 2. Experiment 1. Postures of bucket-fed calves vs teat-fed calves around the morning milk meal. ANOVA for repeated measures revealed significant changes over time for standing (within SEM = 5.1, F13,286 = 72, P < 0.0001) and lying with the head unsupported (within SEM = 5.5, F13,286 = 36, P < 0.0001), and a significant interaction between treatment and time for lying with the head unsupported (F13,286 = 1.84, P < 0.05). *P < 0.05 for the comparison between bucket-fed and teat-fed calves at specific intervals.

Cardiac Activity.
The changes and variability in heart rate around the morning milk meal, and their related statistics, are shown in Figure 3. Heart rate increased during the meal, declined rapidly afterward but remained higher than before the meal. During the meal and the following 6 min, the increase in heart rate was more marked in bucket-fed than in the teat-fed calves, whereas the opposite was observed during the next 4 min. Due to unstable heart rate during the milk intake, the heart rate variability was analyzed only after the meal. Between 5 and 10 min after the meal, the standard deviation of the instantaneous heart rate was higher in teat-fed than in bucket-fed calves (Figure 3).

View larger version (14K): [in this window] [in a new window]   Figure 3. Experiment 1. Heart rate and heart rate variability of bucket-fed calves vs teat-fed calves around the morning milk meal. ANOVA for repeated measures revealed significant changes over time (respectively, for heart rate mean and standard deviation: within SEM = 0.41 and 0.14, F25,550 = 40.2 and 9.2, P < 0.0001 in both cases), and significant interactions between treatment and time (F25,550 = 3.4 and 1.9, P < 0.0001 and 0.01). **P < 0.01 and *P < 0.05 for comparison between bucket-fed and teat fed calves at specific intervals.

View larger version (16K): [in this window] [in a new window]   Figure 4. Experiment 2. Heart rate of bucket-fed calves around milk meal with and without access to a dry teat. ANOVA for repeated measures revealed significant changes over time (SEM = 1.77, F3,27 = 14.4, P < 0.0001), with heart rate during milk intake being significantly higher than at any other time. The absence of a dry teat did not affect heart rate (SEM = 6.8, F1,9 = 0.3, P > 0.10).

Experiment 3
Two teat-fed calves and one bucket-fed calf died before the end of the experiment; it was suspected that they had eaten too many wood shavings. The data collected on these calves were removed from the analyses.

Behavior.
At the beginning of the experiment, the calves spent about 2% of the observation time nibbling parts of the pen (Figure 5). This proportion increased with age up to about 7% when the calves were 3 mo old. An interaction between feeding treatment and age was observed, with the bucket-fed calves spending more time nibbling at 33 d of age than calves fed with the automatic device, while the opposite was observed at 96 d of age. When the calves were observed at 105 d, the frequency of cross-sucking was higher for those fed with the automatic device than for the bucket-fed ones (0.23 ± 0.04 vs 0.05 ± 0.03 cross-sucking per hour, U = 8.5, P < 0.01). In fact, all the calves fed with the automatic device displayed cross-sucking at least once during the day while only two out of the nine bucket-fed calves did so (²= 0.6, P < 0.001). Bucket-fed calves took less time to drink their milk than the calves fed with the automatic device (6.1 ± 1.8 vs 14.3 ± 2.7 min/d, F_1,16 = 54, P < 0.001).

View larger version (10K): [in this window] [in a new window]   Figure 5. Experiment 3. Proportion of the daytime spent nibbling at parts of the pen by calves fed milk from open buckets or with an automatic device fitted with a teat. ANOVA for repeated measures revealed a significant increase with age (within SEM = 0.36, F4,60 = 9.8, P < 0.001) and an interaction between treatment and age (F4,60 = 3.0, P < 0.05). **P < 0.01 and *P < 0.05 for comparison between bucket-fed and teat-fed calves at specific intervals.

	Discussion

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Individually-housed teat-fed calves took longer than bucket-fed calves to consume their milk, showed less non-nutritive oral activity, and lay down more quickly after the meal. Sucking for milk was associated with a lower increase in heart rate during the meal and a greater heart rate variability after the meal. However, no improvement in health or weight gain as a result of nutritive sucking was observed. Sucking a non-nutritive teat after the meal had similar effects on behavior after the meal as nutritive sucking but these effects were smaller. In contrast, allowing group-housed calves to suck for their milk from an automatic milk delivery system had apparently opposite effects, leading to more cross-sucking and more nibbling at parts of the pen.

As reported by Hammel et al. (1988) and Loberg and Lidfors (2001), ingesting milk by sucking decreased the time individually-housed calves spent in non-nutritive sucking after the meal. For example, in Experiment 1, only bucket-fed calves sucked the bars of their pens, and in Experiment 2, bucket-fed calves sucked the non-nutritive teat for longer. This agrees with the findings of Rushen and de Passillé (1995), who showed that the performance of sucking behavior reduced sucking motivation more than did the ingestion of milk. The calves that had to suck to get their milk also had longer meals than bucket-fed calves, which supports previous work showing that a longer time drinking milk is associated with less non-nutritive sucking after the meal (Haley et al., 1998; Loberg and Lidfors, 2001). In addition, in Experiments 1 and 2, calves that were bucket-fed also spent more time licking themselves, parts of their pen or a neighboring calf, and nibbling at parts of their pen.

However, in contrast to our expectations based on the results of Experiments 1 and 2, we observed an increase in cross-sucking and in nibbling at parts of the pen in group-housed calves that were fed with an automatic device fitted with a teat, when compared with bucket-fed calves. This puzzling result must be taken with caution since only one group of calves per treatment was observed. In contrast, de Passillé (unpublished observations, 2000) found a very low incidence of cross-sucking in group-housed calves fed with the same type of machine, while Weber and Wechsler (2001) showed that the amount of cross-sucking is greatly affected by the physical design of the machine: a door attached to the milk feeding system that allowed the calves to continue sucking after the meal reduced the amount of cross-sucking that occurred. It might be that in our experiment, calves that continued to suck the teat after the meal were pushed away from the teat by other calves. However, we found no overt sign of such disturbances when we observed the calves continuously during daytime. Thus, it is difficult to draw general conclusions about the effect of teat feeding in groups on the incidence of cross-sucking.

Compared with bucket feeding, nutritive sucking by individually-housed calves shortened the latency to lie down and, in some cases, lengthened the time spent lying down. This was particularly true in the case of lying down with the head unsupported by the neck (that is, the chin on the floor or the head on the back of the animal). According to Ruckebush (1975) and Nomura et al. (1980), cardiac or cortical indicators of arousal are lower when cattle are lying down than when they are standing. Moreover, the arousal is lower when they lie down with the head unsupported by the neck (Veissier et al., 1989), a posture which has been related to the occurrence of REM sleep (Ruckebush, 1975). Hence nutritive sucking may decrease arousal in calves. However this effect is not long-lasting since it was most apparent immediately following the meal, while there was no difference between bucket-fed and teat-fed calves during the rest of the day.

Non-nutritive sucking has already been reported to induce a quiet behavioral state in human babies (Blass, 1994; McCain, 1995; Pickler et al., 1993). In bucket-fed calves, having access to a non-nutritive teat after the meal shortened the latency to lie down and increased the time calves spent lying down with the head unsupported by the neck. However, in our study, bucket-fed calves that had access to a non-nutritive teat still took more time to lie down and spent less time lying with the head supported by the neck than teat-fed calves having no access to a non-nutritive teat. Hence, it seems that non-nutritive sucking compensates only partly for the lack of nutritive sucking. In teat-fed calves, having access to a non-nutritive teat did not decrease arousal. In fact, it delayed lying down. Hence there seems to be no additional effects of nutritive and non-nutritive sucking, suggesting a common underlying mechanism. De Passillé et al. (1993) found that calves that were able to suck a teat soon after a meal had a higher secretion of CCK and insulin, both of which have been implicated in satiety. This might be the physiological mechanism underlying the apparently greater degree of relaxation of calves allowed to suck a teat.

Heart rate is usually increased during milk feeding due to a high sympathetic tone, which is responsible for the glucagon release shortly after the meal (lambs: Bloom et al., 1975; calves: Bowman et al., 1997). In contrast, some time after the meal, the presence of nutrients in the stomach stimulates the release of gastrointestinal peptides (gastrin, CCK, and secretin), which in turn promote the release of insulin (see Uvnas-Moberg et al., 1987, for a review). This phenomenon, which facilitates the absorption of nutrients, is enhanced by the activation of the vagal nerves. In our study, the heart rate of the calves before the meal was around 120 beats per minute (BPM) in Experiment 1 and 135 BPM in Experiment 2, which is higher than the basal heart rate of calves reported in the literature (around 100 BPM; Bowman et al., 1997; de Passillé et al., 1995). We cannot exclude the possibility that our calves anticipated feeding, probably from noises made by the caretaker preparing the milk. During the milk meal, the heart rate increased rapidly up to 150 to 170 BPM. Previous reports showed that the heart rate can reach 200 BPM in calves drinking milk (Bloom et al., 1975; Bowman et al., 1997). The increase in heart rate was less marked in teat-fed calves than in bucket-fed ones. Hence, it seems that nutritive sucking reduces the activation of the sympathetic tone during the meal. In addition, we observed a higher heart rate variability in teat-fed calves after the meal. The heart rate variability results mainly from the vagal tone (Bernston et al., 1993; Porges, 1995). Nutritive sucking might thus help the changeover from a predominantly sympathetic tone during milk intake to a predominantly vagal tone thereafter and this would facilitate absorption of nutrients. However, this needs further investigation since in our study the higher heart rate variability after the meal in teat-fed calves, compared with bucket-fed ones, was associated with a higher heart rate. As observed in dogs, a vagally mediated release of vasoactive intestinal polypeptide at the cardiac level could explain the cardioacceleration (Henning, 1992; Feliciano and Henning, 1998; Roossien et al., 1997). Non-nutritive sucking also stimulates the release of gastrointestinal peptides and insulin in calves as in human babies, suggesting a facilitation of the vagal tone (De Passillé et al., 1993; Üvnas-Moberg et al., 1987). However, we did not find any effect of non-nutritive sucking on the heart rate of calves. This lack of effect might be due to the short duration of non-nutritive sucking in our study. As a matter of fact, our calves sucked the dry teat for only 2.5 min compared with 4 to 6 min in de Passillé et al. (1992, 1993).

We did not find any evidence that the lower sympathetic tone during the meal and the higher vagal tone after the meal in teat-fed calves had profound effects on the functioning of the autonomic nervous system. In rats, repeated stressful situations, which probably trigger the sympathetic branch of the autonomic nervous system, result in higher TH and PNMT activities (Mormede et al., 1990). There are very few data on the activity of these catecholamine-synthesizing enzymes in calves. The TH activity of our calves was twice as high while their PNMT activity was lower than that previously reported by Veissier et al. (1997, 2001). However, no differences were observed in TH and PNMT activities between teat-fed and bucket-fed calves. According to Lemaire et al. (1993), TH and PNMT activities are (directly or indirectly) under the control of the splanchnic innervation. It might be that the effect on the autonomic nervous system of sucking was too transient for any effect on the synthesis of catecholamines to be seen.

In infants, sucking accelerates growth (Blass, 1994; Üvnas-Moberg et al., 1987). This is thought to result from the higher vagal tone. We did not observe any beneficial effect of teat-feeding on calves’s growth or feed efficiency in any of our experiments. Similarly, Hopkins (1997) did not find any effect of giving a starter to calves via a nipple bottle or an open container, and Szucs et al. (1983) observed a decrease in growth. Previous studies (reviewed in Rushen, 1994) have found variable effects of teat feeding on milk intake and growth rates. The thoroughness with which the teat is cleaned can be a complicating factor (Hepola et al., 1999). In Experiment 3, calves fed with the automatic device fitted with a teat drank less milk than bucket-fed calves and put on less weight. In contrast, Kung et al. (1997) and Boe and Havrevoll (1993) found no difference in feed intake or growth rate between calves on a teat feeding system and individually housed bucket-fed calves. The discrepancy between their results and ours may come from the fact that our bucket-fed calves were in a group, whereas in the studies by Kung et al. (1997) and Boe and Havrevoll (1993), only the calves fed with the automatic device were in groups. Social facilitation might have enhanced milk intake in bucket-fed calves, which were fed together, while teat-fed calves sucked their milk one at a time. Kung et al. (1997) reported less use of medication in calves fed with an automated feeding system, but we found no significant effects on the calves’s health.

We did not find any evidence of a higher level of stress in calves that did not have access to a teat. As mentioned above, the activities of the catecholamine-synthesizing enzymes (as part of the autonomic nervous system) were not altered by nutritive sucking. In addition, the weights of the thymus and of the adrenals, which depend on activation of the hypothalamo-corticotropic axis (Lemaire et al., 1993), did not differ between bucket-fed and teat-fed calves. This absence of difference in stress parameters may account for the lack of effect of sucking on calves’s growth.

In conclusion, teat-feeding stimulates rest after the meal, probably due to a higher vagal tone. Although it might be beneficial for the ingestion of nutrients, this does not seem to improve the growth of calves. In individually-housed calves, teat-feeding reduces the occurrence of non-nutritive oral activities such as non-nutritive sucking, licking, and nibbling. Non-nutritive sucking compensates the lack of nutritive sucking to some extent. Feeding group-housed calves with an automatic device fitted with a teat may not necessarily reduce calves’ motivation for sucking and other oral behaviors, especially if calves do not have sufficient opportunity to perform non-nutritive sucking on the teat.

	Implications

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
When individually housed calves drink milk by sucking a teat, less time is spent in non-nutritive oral activities after the meal, and the calves begin resting sooner after the meal. This suggests that allowing calves to suck a teat to obtain milk may have some beneficial effects upon welfare despite the lack of an effect on health and growth. However, sucking through a teat is not guaranteed to reduce cross-sucking in group-housed calves. The incidence of this behavior varies greatly between groups, and we need to understand more about the environmental factors that influence it.

	Footnotes

 
¹ The authors thank the staff of the three experimental farms (at Marcenat, Orcival, and Lennoxville) for the rearing and the handling of the calves. The exchanges between the French and the Canadian research teams were covered by a collaborative agreement between INRA and AAFC.

³ Present address: Dpto. de Producción Animal, Facultad de Veterinária, Universidad de Múrcia, Spain.

Received for publication December 6, 2001. Accepted for publication May 3, 2002.

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Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 


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