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Repeated handling of pigs during rearing. I. Refusal of contact by the handler and reactivity to familiar and unfamiliar humans

Meat Research Unit, INRA de Theix, France

	Abstract

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Pigs housed in groups received different handling treatments for 40 d until slaughter age. Pigs of the human interaction (HI) and refusal of contact (RC) groups were individually introduced into a pen each day, where they remained for 3 min in the presence of a squatted handler. The handler tried to increase progressively physical reciprocal interactions with the HI pigs using eye and body contact and voice. The handler remained immobile and avoided eye contact and use of voice with RC pigs. These pigs were pushed away when they touched the handler. Control pigs remained in their home pens. Over sessions, HI pigs progressively increased physical interactions with the handler, up to 35% of their time. The RC pigs were motivated to interact with the handler as they tried to establish physical contact with the handler throughout the experiment. They increased levels of locomotion, rubbing, immobility, and snout contact with the wall, suggesting that they were frustrated by the refusal of contact. At the end of the experimental period, all pigs were subjected to three human exposure tests, where pigs were exposed to the handler and two other persons, one of which was unfamiliar, in a Latin square design. During this test, behavior of the humans was the same as for the RC treatment. The HI pigs discriminated between the handler and the other persons as indicated by their increased approach behavior towards the handler. Part of the prior handling experience was generalized to other humans as indicated by higher levels of proximity of HI and RC pigs with the different persons compared with controls. Physical contact with the human was associated with increased heart rates. Two possibilities are that these two characteristics are part of a general behavioral/physiological reactive profile, or that contact with humans provokes an arousal or emotional response. Despite this, behavioral data show that pigs are motivated to be in physical contact with a handler, even when the handler consistently refuses contact.

Key Words: Discrimination • Handling • Human–Animal Interaction • Pigs • Social Behavior

	Introduction

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Pigs are not only social toward conspecifics, but also to humans. Studies on growing pigs show that when encouraged by the behavior of humans toward them, motivation to approach or to physically contact humans increases (Paterson and Pearce, 1992; Hemsworth et al., 1994, 1996a, Hemsworth et al., b; Tanida et al., 1994, 1995). Negative behavior by the human toward the pig (e.g., by use of an electrical prod), decreased this motivation (Gonyou et al., 1986; Hemsworth et al., 1986).

The increase in farm sizes compared with several decades ago has led to a strong decrease in contact between animal caregivers and pigs. Many animal caregivers spend little time interacting socially with pigs beyond that required for routine management. One of our objectives was to determine whether pigs are motivated to approach and/or touch a handler even when such contact is refused on a long-term basis and to describe behavioral responses to this refusal. Heart rate and variability may be related to perceived aversion of the situation (Task Force, 1996) and were also measured. Comparisons were made with pigs that were encouraged to interact with the handler and unhandled controls.

Reactivity to humans may play an important role in stress reactions during slaughter. Such stress reactions are unwanted for ethical reasons and because they may deteriorate meat quality (Monin, 1988). During slaughter, mostly unfamiliar humans are present. Studies revealed that familiarity of context influences reactivity to humans (Koba and Tanida, 1999, 2001). The second objective was to establish, under controlled experimental conditions, effects of prior handling experience on reactions to familiar and unfamiliar humans, in a familiar and unfamiliar environment. Pigs were slaughtered in a commercial abattoir, in the presence or absence of their handler, and meat quality was measured (Terlouw et al., 2005).

	Materials and Methods

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Animals and Housing
Forty-two castrated male Large White pigs (2 mo of age) were purchased from a local breeder (tails had been cut at birth). Pigs were housed in six aligned straw-bedded pens (4.5 m x 1.5 m) in a single room (11 x 6.5 m), with seven pigs per pen. Pen sides allowed clear vision and limited physical contact through bars. The room was maintained at 20 ± 2°C and artificial light was switched on from 0900 to 2100. Water and concentrate food were available ad libitum by nipple drinkers and food dispensers. Feeders were refilled and pens were cleaned daily between 0900 and 1100 by a single male stockperson dressed in blue cloth overalls and green rubber boots. This person entered each pen briefly.

Handling Treatments
Handling treatments took place once a day, five times each week, from 5 wk after arrival on the experimental farm and lasted 10 wk until slaughter. Two handling treatments were used, human interaction (HI; n = 14) and refusal of contact (RC; n = 14). Remaining pigs (n = 14) were controls. Pens remained on the same handling treatment throughout the experimental period. Each treatment group comprised two adjacent pens (i.e., pigs in a same pen received the same handling treatment).

For the handling treatments, the handler (female), dressed in green overalls and green rubber boots, took each pig individually from its home pen to introduce it to an experimental pen (4 m x 1.70 m, short sides were barriers, concrete floor) in an adjacent corridor, where the handler and pig remained together for 3 min. The handler entered the pen simultaneously with the pig and squatted down in the corner opposite the entrance door. For the HI group, the handler tried gradually to interact physically with the pigs, using a predetermined protocol. Allowing and encouraging mutual interactions (i.e., social expression of the pig toward the human) was essential to the study (see fourth point below). Each time the objective of a step was reached, the handler moved on to the following step of the protocol. The protocol steps and objectives of each step were as follows: 1) by using words (friendly voice), the pig stops showing signs of fear (vocalization, pacing, turning away from the handler) and approaches the handler or accepts being approached by the handler; 2) by stroking the pig, the pig does not move away; 3) by touching the pig with other parts of the body (e.g., arm around neck of the pig), the pig does not move away; and 4) by having reciprocal interactions with the pig (e.g., catching the pig’s rooting disk, or catching the pig’s ears to cover its eyes), the pig accepts interaction. Behavioral indications of acceptance were the following: nibbling the handler’s hand (in response to catching of the pig’s rooting disk), shaking its head (in response to catching the pig’s ears), active participation in play (pig catches sleeve and shakes the handler’s arm, pig catches zip of overalls, etc.).

For pigs of the RC group, the handler discouraged any contact. She remained squatted, did not talk or move and looked down to avoid eye contact. If the pig touched the handler, it was pushed away. It received a tap on the nose if it insisted on nibbling the overalls or pushing the handler.

Controls had daily contact with the animal caretaker, during cleaning. In addition, they could see the handler, who entered the animal room daily to get each HI and RC pig successively for the handling treatment.

Behavior of the pigs during the handling was videotaped during wk 1, 3, 5, 7, 8, and 10 after initiation of the training. The first handling session was considered as a habituation session. The first recording, therefore, took place on d 2 (wk 1). Recordings were made on Wednesdays, to avoid an effect of the weekend, when handling did not take place (Tanida et al., 1995). Heart rate was also recorded during video recorded handling sessions during wk 3, 5, and 8 (Polar Vantage NV heart rate monitor, Polar Electro Oy, Kempele, Finland). The R peak is the highest peak on the electrocardiogram and reflects contraction of the ventricles. Accordingly, R-R intervals were chosen as measurement of the interbeat interval of successive ventricle contractions, allowing calculation of heart rate and of interbeat interval variability (Task Force, 1996). The Polar recording system consisted of a 3-cm belt with electrodes and a watch-sized device. The whole unit was enclosed by a second 10-cm elastic belt. Heart rate monitors were fitted a few minutes before the handling session and unnecessary pressure of the belt was avoided to give the pigs time to habituate and to limit disturbance.

Human Exposure Tests
Each pig was tested with three different test people (dressed in green overalls and green rubber boots), in three tests carried out on Thursdays of wk 8, 9, and 10 after the start of the handling sessions. They consisted of introducing each pig in the test pen and leaving it in the presence of a person for 3 min. The behavior of the person was identical to the behavior of the handler in the RC treatment: the person was squatting, avoided eye contact, and pushed the pig away when it touched him/her. Half the pigs were tested in the pen where handling sessions took place (unfamiliar only for the control pigs). The other half was tested in a neutral pen: a similar sized pen in a room adjacent to the corridor and unfamiliar to all pigs (specific differences compared with rearing pens and handling pen: antiskid tiled floor, more light, white walls, the absence of other pig sounds due to increased distance with animal rooms). Test environment was balanced for pens. Behavior was videotaped. Heart rate (R-R intervals) was recorded with the Polar Vantage NV heart rate monitor described previously.

The persons pigs were exposed to were as follows: 1) the handler (a female who carried out the handling treatments, 55 kg, 165 cm), 2) a female co-experimenter (55 kg, 170 cm, familiar to the animals because she assisted with weighing, but had no further interactions), and 3) a male co-experimenter (70 kg, 170 cm, unfamiliar to the animals). All persons wore clean dark-green cloth overalls and green boots. Order of exposure to the different persons was balanced for pen and for test environment. Koba and Tanida (1999) found that pigs discriminate mainly on visual cues, especially color of clothing; however, the possibility that gender plays a role cannot be discarded. The objective was to use two extremes: the female familiar handler and a male unfamiliar person. The female co-experimenter was chosen because she had the same gender but was much less familiar than the handler. Possible differences between responses to the female handler and co-experimenter are therefore not related to gender, but to familiarity or possibly physical aspects.

Aggression Tests
To study whether aggression levels were stable over time, across contexts and despite different handling treatments, three-group straw competition tests were carried out in the home pens, two tests on two successive days, 2 wk before starting the handling treatments, and one at the end of the experiment, 1 wk before slaughter. Used straw was removed from the pens and about 30 min later, each pen received a bundle of clean straw (±1 kg). Animals were directly observed from a gallery overlooking the animal room for 30 min, during which agonistic interactions were recorded on an audio tape recorder. A group food competition test was performed 1 wk before handling in the home pens. Pigs were food deprived for 17 h before the test. At 1000, 500 g of concentrate were deposited on the floor in the middle of the home pen. The protocol was repeated 10 min later. Agonistic interactions were recorded as above.

Behavioral and Cardiac Activity Analyses
Video recordings of the handling sessions as well as of the human exposure tests were analyzed using the Observer software (Version 3; Noldus, Wageningen, The Netherlands). Behavioral categories, of which duration and frequencies were recorded, are presented in Table 1. The pen was divided into two halves by an imaginary line, based on visual cues on the wall. Independent of posture and activity, records were taken of the time spent by the pig in the pen side containing the person. For the pen half away from the person, the pig’s orientation (toward person: person in prolongation of the axis of the head of the pig, or conversely, away from the person) was also recorded. This could not be done for the other pen half as distances between pig and person were too small and records would not have been reliable. Finally, frequency and duration of tail wagging (tail pointing upwards making rapid lateral movements) were also recorded.

Statistical Analyses
Data were analyzed using the Crunch 4 statistical package (Crunch Software Corp., Oakland, CA) after verification of normality of the data with the Shapiro-Wilkes test. Heart rate and behavioral comparisons were made between the two handling treatment groups and controls. Correlation analyses were used to study associations and competition between activities and to study possible relationships between behavioral expression and cardiac activity.

Total durations and total frequencies of activities observed during handling sessions were calculated over 3 min and subjected to an analysis of variance with one interindividual (two handling treatments) and one intraindividual factor (6 d). Behavior of the human exposure tests has been analyzed with one two-level factor (test environment) and two three-level factors (handling treatments and persons). Average heart rate was calculated over 1-min intervals, and an intraindividual factor (3 min) was added to the analysis. Where effects for three-level factors were found, the t-test was used to locate differences. Where two level interactions were found, simple main effects were used to locate differences.

Correlations between variables have been analyzed using Pearson and Spearman correlations, or to adjust for effects of inter-individual and intra-individual factors, using analyses of covariance. Significant effects of co-variables on the between-subjects level indicate correlations between average levels (depending on the analysis, averages over minutes or days) of the variable and co-variable on the level of the individual. Significant effects of co-variables at the within-subject level suggest that changes in the variable and co-variable are associated in time. Nonsignificant variables were excluded from models. A ² test was used to compare numbers of pigs that touched the test persons in the human exposure tests.

	Results

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Growth
Pigs of different handling treatments had similar growth rates (0.87 ± 0.10 kg/d).

Handling Treatments
With the exception of animal/handler interactions, only effects on durations will be shown, as analysis of frequencies of behavior showed similar effects. Frequencies will be expressed as number of times over the 3-min test, duration will be expressed as percentage of time. If activities presented in Table 1 are not described below, no significant effects were found.

Interactions with the Handler.
The duration and frequency of stroking initiated by the handler did not vary over weeks (e.g., frequency = 4.33 ± 0.80). Acceptance of strokes by the HI pigs also did not vary over weeks (e.g., durations; Figure 1). Despite the fact that RC pigs were pushed away by the handler, the duration and frequency of contact with the handler initiated by the pigs did not differ between handling groups or over weeks (mean duration and frequency = 4.6 ± 0.90 and 2.3 ± 0.4, respectively). Over weeks, HI pigs increased duration and frequency of reciprocal interactions (e.g., duration; Figure 1; P = 0.001), which was principally due to high levels in wk 10 compared with other weeks (t-test; P < 0.01). For HI pigs, summing acceptance of strokes, reciprocal interactions, and contact initiated by the pig created a variable called "physical contact." This variable showed a week effect (P < 0.01) as it increased from 16.5% in wk 1 to levels of approximately 35% in wk 10. Average durations of contact were 23.0 ± 5.1 and 4.2 ± 1.3% for HI and RC pigs (for RC pigs representing contact initiated by the pig before it was pushed away), respectively (P < 0.001). The RC pigs spent more time in the part of the pen away from the handler throughout the experimental period (Figure 2; P < 0.01), but when they were in the pen half away from the handler they oriented as often to the handler (85% of time) as HI pigs (89% of time).

View larger version (10K): [in this window] [in a new window]   Figure 1. Duration of accepting strokes (a), and reciprocal interactions (b) on wk 1 through 10 for pigs in the Human Interaction group. *Denotes a week effect, P < 0.01.

View larger version (37K): [in this window] [in a new window]   Figure 2. Percentage of time spent standing (a), in the pen halfway from the experimenter (b), in locomotion (c), immobile (d), in nose contact with the wall (e), and rubbing (f), for pigs of human interaction (black bars) and refusal of contact (hatched bars) treatments on wk 1 through 10. *Denotes an overall week effect, P < 0.05. Denotes a week effect for pigs of the refusal of contact group, P < 0.05. Marked weeks are different from the other weeks. For all activities represented in the graph, except for standing, pigs of the refusal of contact group had higher overall levels than the human interaction group.

Snout contact with any substrate showed no treatment or week effect and accounted for 40.6 ± 8.0% of time. Snout contact with the floor was the main component (34.7 ± 3.6% of total time) and also showed no clear trends. Overall, RC pigs spent more time in snout contact with the wall (Figure 2; handling group effect; P = 0.01); this time represented 18.5 ± 5.4% of total snout contact (11.8 ± 3.9% for HI pigs). Overall levels of nose contact with the wall in wk 1 were significantly higher than in other weeks (week effect; P < 0.01; t-test; P < 0.002). There was no handling group x week interaction. Levels of nose contact with other substrates were lower than 1% and showed no effects. Pigs of the RC group tended to rub themselves more often against the wall (Figure 2; P = 0.06). A week effect was found because rubbing did not occur in week 1 (P = 0.03). In some weeks, levels of tail movements were higher for HI pigs, but overall, differences did not reach significance (overall duration 8.9 and 2.4% for HI and RC pigs, respectively).

Correlations.
Analysis of covariance including all weeks, but carried out separately for the handling groups, showed that for HI pigs, various forms of contact with the handler were negatively correlated with time spent in snout contact with the floor, and to a lesser extent with immobility and locomotion (Table 2). For RC pigs, the most clear-cut effect was a negative correlation between being immobile and snout contact with the floor (Table 2).

View larger version (21K): [in this window] [in a new window]   Figure 3. Average heart rate of pigs of the human interaction (black bars) and refusal of contact (hatched bars) treatments, for wk 3, 5, and 8. *Denotes an overall week effect, P < 0.001.

Human Exposure Tests
General Behavior.
Pigs tested in the neutral pen stood more than pigs tested in the handling pen (Figure 4; P < 0.01) and had longer durations of nose contact with substrates (53.1 vs. 40.2%, for the neutral and handling pen, respectively; P = 0.01). Time spent in locomotion was similar for all groups, irrespective of handling group, environment, or test person (mean 6.89 ± 0.73% of time). Time spent immobile depended on handling group (Figure 4; P = 0.05), with significantly lower levels for HI than RC pigs (t-test; P < 0.05) and on environment (P < 0.01), with lower levels in the neutral pen (13.9 vs. 23.1%). There was no handling group x environment interaction. An environment x handling group interaction for duration of tail movements showed that in the handling pen, tail movements were increased in HI and RC pigs compared to controls (P < 0.05; t-tests; P < 0.05), and that in neutral pen, tail movements were higher in HI pigs than in the other two groups (t-tests; P < 0.001). Average duration of tail movements was 4.4 ± 2.3% of time.

View larger version (27K): [in this window] [in a new window]   Figure 4. Exposure to human test. Duration spent standing (a) and immobile (b), in the handling (black bars) and neutral pen (hatched bars), for pigs of the human interaction (HI), Refusal of contact (RC), and control groups (C). *Denotes that RC pigs spent more time immobile than HI pigs, P = 0.05. Pigs spent further generally more time standing and less time immobile in the neutral than handling pen, P < 0.01.

More HI pigs touched the handler than pigs of the other groups (14, 8, and 8 HI, RC, and control pigs, ² = 8.4; P < 0.05). This difference was not apparent for the other test persons. Overall, HI pigs touched the test persons more often than pigs of the other groups (Figure 5; P < 0.01; t-tests: P < 0.01). Latency to touch did not differ between groups or between test persons present (47.2 ± 8.8 s), unless latency to touch was set to 180 s (duration of the test) for those pigs that did not touch the person at all. In that case, there was an overall treatment effect due to shorter latencies of HI pigs (P < 0.001; t-tests; P < 0.01). Overall, pigs touched the handler less often than the two other persons (P < 0.01; t-tests; P < 0.01; Figure 5). Pigs were consistent in their touching behavior, as shown by positive correlations between frequency, duration, and latency to touch, across persons (e.g., frequency to touch; r = 0.46; r = 0.42; P < 0.01; for the handler vs. the female and male co-experimenter, respectively). Latency to touch the person tended to be negatively correlated with duration of tail movements on the within individual level (P = 0.06).

View larger version (20K): [in this window] [in a new window]   Figure 5. Total number of contacts of the different test persons (Handler = female person who carried out the handling treatments; a female co-exp. = female co-experimenter familiar to the animals because she assisted with weighing, but had no further interactions; and a male co-exp. = a male co-experimenter unfamiliar to the animals) for pigs of the human interaction (black bars), refusal of contact (dense hatches) and control pigs (wide hatches). *Denotes that overall, HI pigs touched the test persons more often than pigs of other groups, P < 0.01. Denotes that overall, pigs touched the handler less often than the two other persons, P < 0.01.

Heart Rate.
Heart rate decreased over test time (P < 0.001), but there were no effects of handling group, test person, or environment. The SD1 values were negatively correlated with heart rate on the within-subject level (P < 0.005). The SD1 values were positively correlated with posture and being immobile (e.g., immobile, within-subject level; P = 0.01). Heart rate tended to be negatively correlated with the latency to touch the person (within-subject level; P = 0.06) and with the proportion of time spent in locomotion while oriented towards the person (between-subject level; P < 0.02) but not with overall levels of locomotion.

Results of the food and straw competition tests will be published in another report (Terlouw et al., 2005).

	Discussion

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Pigs that received the interactive handling treatment accepted stroking at similar levels throughout the training period. Reciprocal interactions between the handler and these pigs increased significantly only at the very end of the training period, when these pigs spent approximately 35% of their time in physical contact with the handler during the handling sessions. Previous studies using recently weaned pigs reported approximately 65% of time spent in physical contact after 1 wk of handling; more training did not increase these contacts (Tanida et al., 1994, 1995). The faster increase in physical contact and the higher final levels in the latter studies may be related to their longer handling sessions (10 or 15 min) or to the pigs’ different genetic backgrounds; French Large White pigs are considered relatively reactive. The objective of the present study to develop reciprocal exchanges may also explain the difference with these earlier studies that aimed only to train pigs to accept stroking and brushing. The older age of pigs in our study is probably not a reason for their lower physical contact. Contrary to other species (Boivin et al., 1992, 2000; Boivin and Braastad, 1996; Mal and McCall, 1996), pigs are not specifically more receptive to handling during the postweaning period compared with other periods up to 12 wk of age (Hemsworth and Barnett, 1992).

Motivation to interact with the handler was high even for RC pigs. Although these pigs were consistently pushed away whenever they established physical contact with the handler, they persisted in trying to establish contact throughout the experimental period, and as often as HI pigs. Their interest in the handler is further underlined by the fact that, when in the pen half away from the handler, they were oriented toward her as often as HI pigs, and that during locomotion, they oriented more often toward her than HI pigs. The results from the present and other studies (Hemsworth et al., 1994, 1996; Tanida et al., 1994, 1995) indicate that pigs are generally motivated to interact with humans, although differences exist between individual pigs. For example, two HI pigs never accepted reciprocal interactions with humans (data not shown).

For HI pigs, decreased acceptance of strokes, initiation of contact, and reciprocal interactions were associated with more snout contact with the floor. Snout contact with the floor was a major component of the overall behavioral score; average snout contact with the floor was slightly higher than average physical interaction. The negative correlation between snout contact with the floor and physical interaction may therefore be related to the fact that being in contact with the person and in snout contact with the floor are incompatible. Alternative interpretations are possible. Snout contact with the floor was positively correlated with being away from the person, while oriented towards her, possibly indicating that the primary motivation was observation of person from a distance, while maintaining snout contact with the floor was an associated activity. Finally, this oral activity may reflect a specific emotional state of the animals, such as frustration. Frustration occurs when animals are unable to express behaviorally a motivation due to physical and psychological obstacles (Hinde, 1970). Previous studies found that frustration induced by the presence of an empty feeder increased oral activities in pigs (Dantzer et al., 1987; Lewis, 1999). Pigs with less interaction may have had greater fear of humans, which would have been a psychological obstacle to approaching the handler. Frustration was then expressed as snout contact with the floor.

Compared with HI pigs, RC pigs showed more snout contact with the wall, rubbing, locomotion, and immobility. Pigs of the RC group showed a shift in activities over treatment weeks. Levels of immobility were higher from the first recording day onward and showed a nearly fourfold increase over the treatment period, whereas locomotion and rubbing decreased. Increased levels of these activities compared with HI pigs may be partly explained by an altered time budget, as the pigs were denied continuous contact with the handler. Increased oral activity, locomotion, and immobility have further all been observed in various aversive situations, believed to cause frustration (see above; Vestergaard, 1984; Dantzer et al., 1987; Terlouw et al., 1991; Bishop et al., 1999; Lewis, 1999). The shift toward immobility may be caused by the increasing certainty on the part of the pigs that contact with the handler would not be allowed, resulting in increasing frustration. The constant levels of touching the human over weeks suggests that standing immobile was not related to a state of "learned helplessness" (Maier and Seligman, 1976).

Above we suggested that lower levels or absence of physical contact with the human might explain increased snout contact. The difference in substrate (HI pigs: floor vs. RC pigs: wall) suggests that different emotional or motivational states underlie these behaviors. Due to the treatment, the two handling groups were not in the same social context. First, contrary to HI pigs, RC pigs had no reciprocal visual contact with the human. Second, RC pigs had no control over the outcome of the interaction. In HI pigs, lower levels of contact with the human were due to refusal by the pig, whereas in RC pigs they were mostly due to refusal by the human. Behavioral and physiological responses to situations are influenced by the level of control the animal has on its environment (Weiss, 1972; Wiepkema and Koolhaas, 1993). Further investigation is needed to understand in detail how these contextual differences explain different choice of substrate.

Positive correlations between activities indicate that these activities are influenced by a single or related emotional or motivational state(s). Acceptance of strokes, initiation of contact by the pig, and reciprocal interactions were all uncorrelated, suggesting therefore that at least partly different processes control these activities.

In the human exposure tests, approach behavior and physical contact with the handler was higher for HI pigs than with the other test persons, indicating that they discriminated between the test persons. The increased approach of the RC pigs toward both the handler and the female co-experimenter may be related to some form of recognition, either because both were of the same gender or due to the earlier presence of the female co-experimenter in the animal rooms during weighing.

Other human-directed activities were influenced by the earlier handling experience but not by the person. Compared with controls, HI and RC pigs spent more time in the pen half containing the human than controls. The HI pigs persisted more in touching all test persons, regardless of the person who was in front of them. The different reactions toward familiar and unfamiliar humans support earlier work showing that pigs may discriminate between persons (Koba and Tanida, 2001). Differences between handling groups, independent of familiarity of the human, show there was also some generalization of earlier experience (Hemsworth et al., 1994, 1996a,Hemsworth et al., b).

Tail wagging was related to previous handling experience of the animal, as controls showed few occurrences. Little is known about the social meaning of tail movements. It has been reported that the domestic pig displays tail wagging in response to various situations, ranging from social greeting and food searching to aggressive approach or frustration (Kiley-Worthington, 1976). In the human exposure tests (but not during the handling tests), more tail wagging was associated with a shorter latency to touch the person, suggesting that tail wagging is related to motivation to touch or interact with the human. Possibly, tail wagging was a form of social greeting. The level of confidence of the pig may also play a role; in the unfamiliar test environment (neutral pen), only HI pigs showed increased levels.

Immobility levels of HI pigs were higher in the test than during handling sessions, possibly reflecting frustration for this group due to the unusual denial of contact. In the neutral pen, all groups, including controls, had more snout contact with substrates, and less immobility. Perhaps these activities were exploratory motivated due to neophobia caused by the unfamiliar room for all pigs, including controls (presence of tiles, different odors, less auditory contact).

The decreased heart rate during the handling and human exposure sessions indicates physical and/or emotional habituation of the animals during the session. During handling and human exposure sessions, physical interaction with the human, whether expressed reciprocally, was related to increased heart rates. Pigs from RC group and HI pigs at the earlier stages of training that touched more often the human also had higher heart rates. During human exposure tests, pigs that touched the human sooner had also higher heart rates. The effects were not explained by differences in posture or locomotion. Two explanations are possible. First, higher heart rate and higher levels of physical contact may have been part of a general behavioral/physiological profile. Pigs could be characterized as proactive or reactive using a series of behavioral tests. Proactive animals react more strongly to manual restraint, are more aggressive and show a stronger cardiac response to novelty (Hessing et al., 1993, 1994; Koolhaas et al., 1999; Ruis et al., 2000). Second, an increase in heart rate may have been caused specifically by physical interaction with the human. Heart rate increased immediately after pigs had been touched by a (unfamiliar) human (Marchant-Forde, 2002). This would suggest that physical contact, whether initiated by the human or by the pig, induced an emotional or arousal response, influencing heart rate. An arousal response may seem contradictory to the pig’s motivation to interact with humans but would explain initial, or for some pigs, long-lasting refusal to accept strokes and play. In other words, humans may evoke conflicting motivations, involving approach/interaction and maintenance or increase of distance. Repeated handling may attenuate these arousal responses as suggested by the negative or absent correlations between heart rate and physical contact during wk 8 for HI pigs.

The SD1 values over 3 min were strongly correlated with the square root of the mean squared difference of successive interbeat intervals, which quantifies high frequency components of heart rate variability (Task Force, 1996). These components reflect the influence of the parasympathetic input to overall cardiac activity (Task Force, 1996). The SD1 values are therefore likely to reflect vagal tone in pigs. Other studies found that the SD1 measure of the Poincaré plot is a measure of parasympathetic nervous activity in humans (Copie et al., 1996; Kamen et al., 1996). During human exposure tests, SD1 values tended to be negatively correlated with heart rate. The higher heart rates associated with physical contact may thus, in part, be mediated by lower vagal tone.

In summary, pigs are motivated to have visual and/or physical contact with humans, even if such contact is categorically refused by the human. Rejection of contact by the human is associated with increased levels of activities, such as immobility and rubbing, indicative of emotional discomfort and possibly frustration. Physical contact was associated with increased heart rate of the pig, reflecting an emotional or arousal response. Some behaviors showed that pigs discriminate between persons depending on familiarity. Other behaviors of the pigs showed that previous experience with the handler was partly generalized towards other humans.

	Implications

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Systematic refusal by the animal caretaker to have physical interactions and/or eye contact seems aversive for most pigs. Social motivation of pigs toward humans is, however, complex. Untrained pigs refused or became aroused when a human initiated reciprocal interactions. After training, pigs spent less time in interactions with the human than in exploration (snout contact). Behavioral signs of recognition of the handler were only observed in pigs to which reciprocal interactions were proposed and not in pigs where contact was refused. Increased proximity with the handler and other humans occurred in both groups. Therefore, to obtain familiarization with humans in general, the mere daily physical presence of the handler with the individual pig suffices, whereas individual recognition of the human needs prior closer interactions. Conclusions need to be confirmed for pigs from other genetic origins.

¹ Correspondence: 63122 St-Genès-Champanelle (phone: +33-473-624-569; fax: +33-473-624-168; e-mail: terlouw{at}clermont.inra.fr).

Received for publication February 5, 2004. Accepted for publication September 29, 2004.

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