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J. Anim. Sci. 2005. 83:1664-1672
© 2005 American Society of Animal Science


ANIMAL PRODUCTION

Repeated handling of pigs during rearing. II. Effect of reactivity to humans on aggression during mixing and on meat quality

E. M. C. Terlouw1, J. Porcher and X. Fernandez

Meat Research Unit, National Institute for Agricultural Research of Theix, 63122 St-Genès-Champanelle, France


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The present study was designed to determine whether reactivity toward humans can be used to predict a pig’s reactivity to the slaughter procedure as measured by postmortem muscle metabolism. Forty-two pigs were group-reared in six pens with straw-bedding. Pigs received regular positive (HI) or mildly negative (RC) handling training in a separate pen for 40 d before slaughter. Control pigs remained in their home pens throughout rearing. Pigs were slaughtered at a commercial packing plant, and half of each treatment group (HI, RC, or controls) was accompanied by the handler throughout mixing and transportation, as well as a portion of the lairage time and introduction to the holding pens situated before the slaughter room, whereas the other half was not accompanied by the handler. Muscle pH and temperature, objective color (L*, a*, and b* values), and drip loss were measured on the LM, biceps femoris, semimembranosus, and adductor femoris. Prior handling experience did not in itself influence ultimate meat quality (P > 0.37); however, the presence of the negative handler (RC pigs) at slaughter accelerated (P < 0.06) preslaughter glycogen breakdown in the LM. Fighting behavior during mixing explained between 13 and 32% of the variability of lightness (L* values) of the LM, biceps femoris, and semimembranosus. Visual contact with the handler at the start of the handling training and number of fights initiated explained between 31 and 42% of the variability in ultimate muscle pH. Latency to approaching the handler during human exposure tests explained 20% of the variability in initial muscle temperature of two muscles. Fighting behavior during mixing could be partly predicted from fighting during a food competition test conducted at the start of the rearing period. Results indicate that reactivity to humans and the tendency to fight determined, in part, meat quality in pigs of similar genetic and rearing backgrounds. These behavioral characteristics were, to some extent, determined early in life. Handling experience modified behavior toward the handler but correlations between behavioral characteristics and meat quality were not influenced by prior handling experience.

Key Words: Aggression • Handling • Meat Quality • Pigs • Slaughter • Stress Factors


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
There is considerable variation in pork quality, some of which can be attributed to stress responses during the preslaughter period (D’Souza et al., 1998aGo, 1999Go; Monin, 1988Go). Stress responses occur to physical (food restriction, fatigue, and pain in response to slaps, shocks, or fights) and psychological discomfort (disruption of the social hierarchy and fear). Behavioral stress reactions involve flight or, conversely, immobilization of the animals, making moving them more difficult. Physiological reactions involve an increase in heart rate and secretion of stress hormones, such as cortisol and catecholamines.

Pork is markedly influenced by the rapidness and magnitude of postmortem pH decline, which is related to antemortem locomotor responses and physiological changes that accompany stress (Bendall, 1973Go; Monin, 1988Go). To explain variations in meat quality, differences in stress reactivity between pigs must be considered. Like other species, pigs show consistency in their reactivity to various situations, and can be characterized using behavioral tests. Proactive pigs react more strongly to manual restraint, are more aggressive, and show a stronger cardiac response to novelty than reactive pigs (Lyons, 1989Go; Lawrence et al., 1991Go; Ruis et al., 2000Go). However, reactivity to stress is partly related to prior experience. Rearing environment influenced behavioral and physiological responses of pigs to pre-slaughter handling and mixing at transport and at slaughter (D’Souza et al., 1998aGo; De Jong et al., 2000Go). Repeated interactive handling and repeated refusal of visual and physical contact modified reactivity to humans differently (Terlouw and Porcher, 2005Go). The present study was designed to determine whether reactivity toward humans, at the start or end of a handling procedure, can be used to predict a pig’s reactivity to the slaughter procedure, as well as changes in postmortem muscle metabolism and pork quality.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Animals and Housing
Experimental procedures and animal-holding facilities respected French animal protection legislation, including licensing of experimenters. Licenses, procedures, and holding facilities were controlled and/or approved by the French Veterinary Services.

Forty-two 2-mo-old Large White barrows were purchased from a local breeder and housed in six aligned straw-bedded pens (4.5 m x 1.5 m) in a single 11.0 x 6.5 m room (seven pigs per pen). Pen sides allowed for clear vision but limited physical contact. The room was maintained at 20 ± 2°C, and artificial light was switched on from 9 to 21 h. Water and concentrate food (70% wheat, corn, and barley, 30% soybeans, peas, and rape-seed) were available ad libitum from nipple drinkers and food dispensers. Pens were cleaned daily between 0900 and 1100 by a single stock person dressed in blue cloth overalls entering each pen briefly.

Handling Treatments and Human Exposure Tests
Handling treatments took place once daily (five times each week), from 5 wk after arrival on the experimental farm until slaughter (15 wk after arrival). The two handling treatments included human interaction (HI; n = 14) and refusal of contact (RC; n = 14), and the remaining 14 pigs served as controls. Treatments remained the same throughout the 10-wk experimental period, and pigs in each treatment group were kept in adjacent pens (two pens per handling treatment).

For the handling treatments, the handler, dressed in green overalls and green rubber boots, took each pig individually from its home pen to an experimental pen (4.0 x 1.70 m) in an adjacent corridor, where 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 and playfully with the pigs, using a predetermined protocol. Each time the objective of one step was reached, the handler moved on to the next step of the protocol: 1) using words in a friendly voice (pig stops showing signs of fear, such as vocalization, pacing, and turning away from the handler, and pig approaches handler or accepts the approaching handler); 2) stroking the pig (pig does not move away); 3) touching other parts of the pig (pig does not move away); and 4) having reciprocal interactions with the pig, such as catching the pig’s rooting disk, or covering the pig’s eyes with its ears (pig accepts this interaction with the handler). Behavioral indications of acceptance included nibbling the handler’s hand in response to the handler catching the pig’s rooting disk, the pig shaking its head in response to the handler catching the pig’s ears, and active participation in play (pig catches the handler’s sleeve and shakes the handler’s arm, pig catches zip of overalls, etc.).

For the RC group, the handler discouraged any contact. The handler did not talk or move and looked down to avoid eye contact. If the pig touched the handler, it was pushed away, and received a tap on the nose if it insisted on nibbling the overalls or pushing the handler. Pigs in the control group could see the handler, who entered the animal room daily to get each HI and RC pig for the handling treatment; otherwise, control pigs received minimal human contact.

To evaluate initial reactivity to humans, as well as short-term and long-term effects of the handling treatments, behavior during the handling treatments was videotaped once every 2 wk. Day 1 was considered a habituation session, whereas video recording occurred on d 2, and levels of the various activities observed on d 2 will be referred to as levels at the start of training.

Eight, nine, and ten weeks after the start of the handling training, all pigs (including controls) were exposed to three 3-min human exposure tests (one test per week). The procedure was identical to the RC-handling treatment. In a Latin squares design, pigs were exposed to the handler, to a female coexperimenter who was moderately familiar to the pigs due to her participation in weighing, and to an unfamiliar male coexperimenter, and behavior was videotaped as described by Terlouw and Porcher (2005)Go. Behavior during the recorded handling sessions and human exposure tests was analyzed from videotapes with the Observer statistical package (Version 3; Observer, Wageningen, Netherlands). Levels of activities were expressed as the total number of occurrences (frequency) and duration relative to total observation time (duration = percentage of time).

Behavioral Aggression Tests
To study whether aggression levels were stable over time and independent of different handling treatments, three-group straw competition tests were carried out. Two straw competition tests were carried out on successive days 2 wk before initiating the handling treatments, whereas an additional test was conducted 1 wk before slaughter. Used straw was removed from the pens, and, approximately 30 min later, each pen received an approximately 1-kg bundle of clean straw. Pigs were individually marked and observed from a gallery overlooking the room for 30 min, during which time agonistic interactions of initiators (head knocks, bites, and/or pushes) and receivers (aggressive response, no reaction, turns away) were audiotaped.

A food competition test was performed 1 wk before the start of the handling training. Feed was withheld from pigs for 17 h before the test. At 1000, after drawing the attention of all pigs in the pen, 500 g of a standard concentrate feed was deposited in the middle of the floor in the home pen, which allowed four pigs access at a time. Ten minutes later, a second 500-g feed allocation was deposited in the pen. Pigs were observed from the gallery for 30 min and agonistic interactions were recorded as described for the straw competition test. Each day, the test was conducted in a single pen, and the order of testing was balanced over treatments. Lastly, aggression levels were assessed during preslaughter mixing. These different behavioral tests allowed for the studying of the degree of consistency in behaviors over time and among different situations.

Slaughter and Measurements
Animals were slaughtered at a commercial abattoir (Clermont-Ferrand, France) when pigs weighed 117 ± 2 kg (approximately 6 mo of age). Two groups of seven pigs were slaughtered on each of three days.

The afternoon (1400) before slaughter, one or two pigs were taken from each pen, weighed, and introduced simultaneously to a 4.0 x 1.70 m waiting pen, which was visually and partially auditorially isolated from the animal rooms. All activities were videotaped and analyzed using the same descriptions as for the straw-and food-competition tests. After 1 h of mixing, the group was transported in a 1.85 x 2.90 m truck for 45 min (20 km) to the commercial abattoir, where the pigs were unloaded and placed in 3.0 x 3.0 m holding pens at the abattoir. Immediately after the first group, a second group of seven pigs was subjected to the previously described mixing and transportation procedures.

The following morning, pigs were marked for carcass identification purposes 30 min before movement into the restrainer, and slaughtered between 0500 and 0600. All pigs were electrically stunned and exsanguinated immediately. Slaughtering and stunning of all commercial pigs lasted approximately 120 min and took place before the slaughter of the experimental pigs. The two groups of pigs slaughtered on a particular day were not mixed together.

The term "slaughter procedure" refers to all procedures preceding slaughter, starting with food deprivation and mixing on the farm, and ending with stunning in the abattoir. During the slaughter procedure, pigs were either "accompanied" by the handler, or "unaccompanied" (control slaughter procedure). For the "accompanied" procedure, the handler remained with the pigs during mixing on the experimental site, during transportation to the abattoir in the truck, and, upon arrival, the handler remained with the pigs in the holding pen for 1 h. The following morning, the handler returned with the pigs in the holding pen for 1 h, and she drove the pigs approximately 30 m to the restrainer, where she remained until all pigs had been introduced into the restrainer by the animal caretaker of the abattoir (one pig every 2 min). For the "unaccompanied" procedure, the handler was absent during mixing, transportation, and lairage, and pigs were moved from the holding pens to the restrainer by the animal caretaker employed by the abattoir. These slaughter conditions were balanced across pens and previous handling training. Additionally, on each slaughter day, "unaccompanied" pigs were slaughtered first, followed by the accompanied pigs. Electrical prods were not used in any of the treatments. This experimental approach was designed to evaluate the effect on postmortem metabolism of the presence of, and handling by, the familiar handler during the preslaughter period, depending on earlier handling experience.

A muscle shot biopsy was taken from the LM 30 min before slaughter according to the procedure described by Talmant et al. (1989)Go. The actual biopsy lasted less than 1 s, and approximately 1 g of LM was immediately frozen in liquid N2, and stored at –80°C until assayed for glycogen and lactate content. Two-gram samples from the LM and biceps femoris (BF) were excised immediately after exsanguination and 40 min after exsanguination. Samples were immediately homogenized in 18 mL of 5 mM iodoacetate, and the pH of the homogenate was measured with a glass electrode (Inlab 427, Mettler Toledo, Greifensee, Switzerland) connected to a portable pH meter (Schött-Geräte, Germany). Muscle temperature of the LM and BF was measured at the same times when pH samples were collected using a thermocouple connected to an electronic thermometer (98004PK and Sefram 9810, St-Etienne, France). Twenty-four hours after slaughter, carcasses were fabricated, and pH and objective color (L*, a*, b*) of the LM, BF, semimembranosus (SM) and adductor femoris (AF) were measured directly on the fresh-cut surface with a Minolta chromameter (CR-300, Minolta Corp., Osaka, Japan) equipped with a 0° viewing angle and using illuminant C. Additionally, two 2-cm-thick LM slices were cut on the level of the last rib 24 h after slaughter, placed on a tray, wrapped with a polyvinyl chloride film, and stored at 4°C. The amount of moisture loss was measured 24 (Drip 1) and 72 h (Drip 2) later, and expressed as a percentage of the initial sample weight.

Glycogen and Lactic Acid Assay
Approximately 200 mg of lyophilized LM was ground and suspended in 10 mL of 0.5 M perchloric acid for 15 s with a homogenating device (Polytron, Luzern, Steinhofhalde, Switzerland). After hydrolysis of the glycogen by amyloglucosidase (38°C for 3 h) and centrifugation for 10 min at 4,000 x g, the glucose content of the filtered supernatant was determined by spectrophotometric determination of NADH at 340-nm wavelength after the addition of hexokinase and glucose-6-phosphate-dehydrogenase (Dalrymple and Hamm, 1973Go). Lactic acid was determined before hydrolysis of glycogen on the supernatant fraction after addition of lactate dehydrogenase, glutamate, and glutamate-pyruvate-transaminase by spectrophotometric determination of NADH at 340-nm wavelength (Bergmeyer, 1974Go). Glycolytic potential (GP), the sum of compounds likely to produce lactic acid postmortem, was calculated using the formula GP = 2[lactate] + [glycogen] (Monin and Sellier, 1985Go). Concentrations were expressed as micromoles of lactate equivalents per gram of fresh tissue. Assays were carried out in triple with a within variation of 4%.

Statistical Analyses
Data were analyzed with the Crunch Statistical package (v. 4, Crunch Software Corp., Oakland, CA). For the food competition tests, different straw competition tests, and preslaughter mixing, total number of interactions initiated and received was calculated per pig and per test. In addition, for the mixing test, the total number of aggressive interactions (i.e., initiated and received) was calculated to obtain the total number of fights each pig was involved in, and aggressive interactions initiated relative to total amount of aggressive interactions was calculated to estimate aggression level and efficiency of fighting.

Straw and food competition tests were analyzed using ANOVA including a stratum containing one interindividual factor (three handling treatments) and a stratum containing one intraindividual factor (four repetitions). Meat quality data and aggressive behavior during mixing were analyzed using ANOVA including a single stratum containing three interindividual factors (three handling treatments, two slaughter methods, and three slaughter dates). Pens were nested within treatments. If interactions or effects for higher-level factors were found in any of the ANOVA, t-tests were used to identify differences.

Correlations between meat quality, aggression, and activities observed during handling training and human exposure tests were calculated using simple (Pearson correlation coefficients) and multiple regression analyses. For handling training and human exposure tests, the following main behavioral categories were considered: posture (standing), human directed activities (visual contact with person, approach person, acceptance of strokes, physical contact by pig, reciprocal interaction), locomotion, immobility, and nose contact (Terlouw and Porcher, 2005Go). For multiple regression, adjusted R2 values were used to estimate variability explained by behavioral observations. When a meat measurement was correlated with a behavioral characteristic and also influenced by other factors (handling training and/or slaughter condition), the final ANOVA used included this characteristic as a covariate. Analysis of covariance is used to test the main and interaction effects of treatment factors on a continuous dependent variable, adjusted for the effects of selected other continuous variables, which covary with the dependent variable (Mead, 1992Go). To correct for pen effects, Pearson correlations between competition tests were pooled over pens, basing the correlation on pen means rather than on overall means.


    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Aggressive interactions were lower (P < 0.001) during the straw competition test implemented at the end (0.14 ± 0.05) than at the start of the rearing period (first test = 0.85 ± 0.15; second test = 0.63 ± 0.13). Handling treatments, which occurred between the second and third straw-competition test, did not (P > 0.50) influence agonistic behavior. Aggressive behavior across straw competition tests was not consistent because levels of aggression in the first and second test were not (P = 0.29) correlated with each other. Levels during Straw Competition Test 3 were too low to calculate meaningful correlations. Aggression during the straw competition tests was lower (P < 0.01) than during the food competition test (4.38 ± 1.21).

After mixing, pigs lay down sooner and for a longer total time (P < 0.01) in the presence of the handler (48.6 ± 3.6% of time), than in her absence (34.7 ± 4.1% of time). Despite this difference, the total amount of aggressive interactions was similar (P = 0.59) whether the handler was present (5.1 ± 1.1) or absent (6.2 ± 1.1) during mixing. After receiving an act of aggression, HI and RC pigs turned away from their aggressor less (P < 0.05) often than control pigs (0.9 ± 0.2 and 1.1 ± 0.3 vs. 2.2 ± 0.5 times, respectively).

Aggressive behavior showed some consistency across different situations. Numbers of aggressive interactions received during straw distribution, totaled over the first two tests or across all three tests, were positively correlated with those received during the food competition test (Tests 1 and 2: r = 0.36; P < 0.05). The number of aggressive interactions initiated during mixing before slaughter tended to be positively correlated with those initiated during the food (r = 0.42; P < 0.02) and straw competition (r = 0.28; P = 0.10) tests.

Accompanying pigs had little overall effect on mean pork quality characteristics (Table 1Go). Ultimate pH of the LM from "accompanied" pigs (Table 1Go) tended to be lower (P = 0.06) than that of the LM from "unaccompanied" pigs, and their SM was less (P = 0.07) yellow (lower b* values). Prior handling experience did not in itself influence ultimate meat quality (P > 0.37), but the BF from "accompanied" HI pigs was redder (larger a* values) and more yellow than that of "unaccompanied" HI pigs, as well as more yellow than the BF from accompanied RC pigs (handling treatment x slaughter procedure; P = 0.06).


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Table 1. Means (±SEM) for pork quality traits
 
The number of aggressive acts initiated, total number of aggressive acts, and the relative proportions of these two measurements were significantly correlated with 14, 11, and 12 pork quality indicators, respectively (Table 2Go). Initiated fights during food competition were correlated with LM pH at 45 min (r = 0.47; P < 0.01) and SM L* values (r = –0.42; P = 0.01). Frequency and duration of visual contact with the handler in the beginning of the training sessions (wk 1) were negatively correlated (P < 0.05) with ultimate pH of the BF (duration: r = –0.48), SM (r = –0.41), AF (r = –0.46), and LM (r = –0.49; Figure 1Go). Visual contact with the handler and fighting during mixing were not correlated (r = 0.16; P = 0.43), and regression equations including duration of visual contact with the handler and aggressive acts initiated explained 42, 32, 37, and 31% of the variability in ultimate pH of the LM, BF, SM, and AF, respectively.


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Table 2. Pearson correlation coefficients between aggressive interactions during mixing before slaughter and meat quality traits
 


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Figure 1. Relationship between visual contact with the handler at the start of handling training and ultimate pH of the LM. Black circles represent human interaction (reciprocal visual contact), and grey triangles represent refusal of contact pigs (unidirectional visual contact).

 
Glycogen content and GP in the LM were negatively correlated (P < 0.001) with ultimate LM pH, and positively correlated (P = 0.02) with visual contact with the handler at the beginning of the handling period (r = 0.50). Other activities during the handling sessions showed no consistent correlations with meat quality indicators.

Visual contact was included as a covariate in ANOVA for LM glycogen content and GP. Handling treatment x slaughter condition interactions (P < 0.04) were detected for muscle glycogen (Figure 2Go) and GP values, with "accompanied" RC pigs having lower adjusted levels than "unaccompanied" RC pigs (P < 0.05) and "accompanied" HI pigs (P < 0.06). The glycogen content of the LM explained 42% of the variability in LM ultimate pH. Absence of an effect of slaughter conditions on ultimate LM pH in RC pigs was explained by relatively low pH of two "accompanied" RC pigs, despite their decreased glycogen levels.



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Figure 2. Glycogen content of the LM 30 min before slaughter of human interaction (HI), refusal of contact (RC), and control pigs. Values of the handled pigs have been adjusted for visual contact with the handler at the start of the handling training. Hatched bars represent unaccompanied pigs, and grey bars represent accompanied pigs. Bars that do not have common letters differ (P ≤ 0.06). Controls were excluded from this analysis, as visual contact with the handler had not been assessed. See text for details.

 
Latency of a pig to touch the handler during human exposure tests was negatively correlated (P < 0.05) to LM and BF temperature (Figure 3Go) measured at exsanguination (r = –0.44 and –0.38, respectively) and 45 min after exsanguination (r = –0.47 and –0.46, respectively); however, latency to touching the handler was not correlated with fighting during mixing (r = –0.04; P = 0.84). Multiple regression on BF temperature at 1 min found that latency to touching the handler was significant (P < 0.02), and initiated fights approached significance (P = 0.08).



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Figure 3. Relationship between latency to touch the handler during the human exposure test and postexsanguination temperature of the LM. Black circles, grey triangles, and grey squares represent human interaction, refusal of contact, and control pigs, respectively.

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Results show that characteristics measured in behavioral tests and during mixing predict meat quality. The number of fights initiated explained between 13 and 32% of variability in lightness (L* values) of the LM, BF, and SM muscle. The tendency to fight during mixing could only be partly predicted from the tendency to fight for food or straw during rearing. Visual contact with the handler at the start of the handling training sessions, combined with the number of fights initiated before slaughter, explained about 35% of the variability in ultimate pH of the four muscles studied. Latency to approach the handler during human exposure tests explained approximately 20% of the variability in initial muscle temperature of the LM and BF. Prior handling experience did not in itself influence ultimate meat quality, but the presence of the negative handler at slaughter enhanced preslaughter glycogen breakdown as observed in RC pigs.

Glycogen was measured in a LM shot biopsy. Earlier work found a 15-min increase in heart rate and a salivary cortisol response immediately after shot biopsy (Geverink et al., 1999Go). The heart rate response was partly due to the presence of the technician (Geverink et al., 1999Go). In the present study, the biopsy was carried out by a person wearing a white coat, differentiating himself from the handler, who always wore dark green overalls. Stress due to the biopsy, if any, was expected to be similar in all slaughter groups and effects on muscle metabolism small, although variation in reactions of pigs may have increased variation in postmortem metabolism.

Meat quality, including color and water-holding capacity, is influenced markedly by the rate and magnitude of postmortem pH decline (Bendall, 1973Go; Monin, 1988Go). The magnitude of pH decline depends mainly on muscle glycogen reserves, and the rapidness of pH decline depends on muscle metabolic activity (mainly ATPase activity) at slaughter (Bendall, 1973Go; Monin, 1988Go). Physical activity increases muscle metabolism, leading to net glycogen loss. Physical effort and psychological stress increase the secretion of hormones that exacerbate effects of muscular activity on muscular glycogen depletion (Fernandez et al., 1994aGo; Febbraio et al., 1998Go). Moving pigs with an electric prod (D’Souza et al., 1998aGo), treadmill exercise (Henckel et al., 2000Go; Rosenvold and Andersen, 2003Go), and mixing of unfamiliar pigs resulting in fights (Karlsson and Lundström, 1992Go; Geverink et al., 1996Go; D’Souza et al., 1999Go) have been shown to accelerate antemortem muscle metabolism, resulting in lower preslaughter muscle glycogen reserves. Postmortem effects of exercise or stress immediately before slaughter include higher muscle temperature and lactic acid content and faster pH drop, whereas low preslaughter muscle glycogen reserves result in higher pH, darker color, and less drip loss (Wismer-Pedersen, 1959Go).

Fighting decreases glycogen stores due to physical activity and increased catecholamine secretion (Warriss and Brown, 1985Go; Fernandez et al., 1994aGo). In the present study, the more pigs fought before slaughter, the lower preslaughter glycogen stores were due to increased antemortem glycogenolysis, resulting in elevated ultimate pH.

Interpretation of correlations between reactivity to humans and meat quality is complex. First, pigs that had less visual contact with the handler before training had higher ultimate pH and, therefore, presumably more glycogen breakdown during the preslaughter period, suggesting that they were more reactive to the whole, or aspects of, the slaughter procedure. Second, initial muscle temperature increases when pigs are exercised immediately before slaughter (Henckel et al., 2000Go; Rosenvold and Andersen, 2003Go). The higher postexsanguination muscle temperatures of pigs that approached the handler or coexperimenters more quickly or more often during the human exposure tests suggest that these pigs had a higher muscle metabolic activity, possibly due to an increased reactivity to the procedures immediately before stunning.

Shorter latency to approach humans reflects lower fear levels and/or a stronger motivation to interact with humans (McFarland, 1985Go; Toates, 1986Go; Hemsworth et al., 2002Go). Thus, pigs that are less fearful or more motivated to touch humans were more reactive to the procedure immediately before slaughter. This paradox may be explained by an earlier study showing that pigs with lower fear levels of humans moved consequently more slowly through corridors and races during slaughter, and received, therefore, more negative interactions from slaughter personnel. These pigs were more reactive to slaughter as shown by higher plasma lactate concentrations at exsanguination and higher fiber optic probe values 6 to 8 h after slaughter (Hemsworth et al., 2002Go).

Correlations between reactivity to the handler and preslaughter muscle glycogen might be due to different resting concentrations of glycogen. Such correlations may be explained by differences in stress levels during rearing (due to training or rearing conditions) and/or metabolic differences. However, further studies are needed to understand the exact motivation underlying visual contact with the handler, and the correlation between this behavior and preslaughter glycogen content.

The effect of the presence of the negative handler on preslaughter glycogenolysis in RC pigs was not related to differences in fighting behavior. Glycogen results indicate that the mere presence of the negative handler at slaughter caused increased glycogen breakdown, suggesting aversive reactions. This finding supports the earlier suggestion that repeated refusal of contact during handling sessions was aversive (Terlouw and Porcher, 2005Go). The absence of an effect on pH may be related to variations in the buffering capacity of the muscle (Bendall, 1973Go). The absence of a positive handler effect on glycogen in the present study may be due to the stressful context of slaughter, reducing possible beneficial effects of previous positive handling.

Despite the lack of an effect on glycogen, accompanied HI pigs were not the only ones that tended to have a lower pH; the same phenomenon was observed for accompanied controls (no handling training), suggesting that the presence of a familiar but neutral person at slaughter may have effects on antemortem muscle metabolism. This difference is consistent with the observed glycogen concentrations in the range of 50 to 100 µmol, where a difference of 5 µmol of glycogen explains approximately 0.1 pH units (Bendall, 1973Go). Increased yellowness (b* values) of the BF in presence of the positive handler (HI pigs) was explained by lower ultimate pH values (Brewer et al., 2001Go).

The HI and RC handling treatments seem to have decreased the fear of attacking pigs during mixing compared with controls. Competition for food induced more aggression than competition for straw, possibly because food restriction induces increased activity as well as reactivity (Teghtsoonian and Campbell, 1960Go; Terlouw et al., 1991Go; Fernandez et al., 1994bGo) and/or motivation for feed may be stronger than motivation for straw (Pedersen et al., 2002Go). Food competition produced more aggression than mixing before slaughter (per unit of time), although in both cases pigs were deprived of food. Differences may be related to different contexts (fighting for food and fighting to reestablish hierarchy), but age may also play a role. Levels of aggression were much lower at the end than at the start of the fattening period, as shown by the straw competition tests. This finding may be explained by heavier BW and decreased agility of pigs or a more stable social structure of the group. Finally, previous studies observed that attack latency in a resident-intruder paradigm predicted aggression levels during mixing (Erhard et al., 1997Go; Erhard and Mendl, 1997Go); however, in the present study, the tendency to fight for food and straw explained only a small part of total variability.


    Implications
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Increased physical contact between caretakers and pigs during rearing did not influence subsequent meat quality. Ultimate meat quality could be predicted by levels of fighting during mixing and reactivity to humans observed early in life rather than after handling training. Thus, selecting pigs with less agrressive behavior and positive human reactivity may improve pork quality.

1 Correspondence—phone: + 33 (0)4 73 62 45 69; fax: + 33 (0)4 73 62 41 68; e-mail: terlouw{at}clermont.inra.fr.

Received for publication February 6, 2004. Accepted for publication March 18, 2005.


    Literature Cited
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


Bendall, J. R. 1973. Postmortem changes in muscle. Pages 244–309 in Structure and Function of Muscle. 2nd ed. G. H. Bourne, ed. Academic Press, New York, NY.

Bergmeyer, H. U. 1974. Pages 1127–1196 in Methods of Enzymatic Analysis. G. H. Bourne, ed. Academic Press, New York, NY.

Brewer, M. S., L. G. Zhu, B. Bidner, D. J. Meisinger, and F. K. McKeith. 2001. Measuring pork color: Effects of bloom time, muscle, pH and relationship to instrumental parameters. Meat Sci. 57:169–176.

Dalrymple, R. H., and R. Hamm. 1973. A method for the extraction of glycogen and metabolites from a single muscle sample. J. Food Technol. 8:439–444.

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E. M. C. Terlouw and J. Porcher
Repeated handling of pigs during rearing. I. Refusal of contact by the handler and reactivity to familiar and unfamiliar humans
J Anim Sci, July 1, 2005; 83(7): 1653 - 1663.
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