TY - JOUR AU - Gonyou, H. W. AB - Abstract The process of transportation can be seen as a succession of stressors, from which pigs may not have time to recover before slaughter. The aim of this study was to determine the extent to which the duration of the rest time given to near-market-weight pigs after an initial exposure to exercise affected their recovery from subsequent exercise. Eighteen groups of 3 gilts were exercised (Ex1) through a standard handling course, including two 19° ramps, and then were held in a holding pen for either 35 (RT35), 75 (RT75), or 150 (RT150) min (Rest Period 1, RP1). Afterward, pigs were exercised a second time (Ex2) and left to rest for 150 min. Recovery from Ex2 (Rest Period 2, RP2) was assessed using measures of heart rate (HR), respiratory rate (RR), skin temperature (ST), and posture. Repeated measures and regression analysis were used to analyze the data. For RT75 pigs, there were no detrimental effects of Ex2 on HR, RR, and handling time (P > 0.05, for all) during the exercise and recovery periods. Skin temperature during Ex2 was greater than ST during Ex1 (P < 0.001), whereas ST during RP1 did not differ from ST during RP2 (P > 0.05). Doubling the rest period did not provide any more beneficial effects in regard to RR and HR (P > 0.05 for both) during Ex2 and RP2 compared to RT75 pigs, as shown by the similar latencies to recover for these 2 variables. However, ST did not increase between exercises, and RT150 pigs required less time to complete the handling course during Ex2. The results show that a lack of rest after an initial exposure to exercise made pigs more susceptible to stress during Ex2 and RP2, as demonstrated by greater (P < 0.001 for all) HR, RR, and ST during RP2 compared to RP1 and Ex2 compared to Ex1. When given more than 35 min to rest during RP2, RT35 pigs eventually recovered. Latencies of recovery for HR, ST, RR, and posture were all greater (P < 0.05 for HR, ST, and RR and P < 0.001 for posture) than those obtained for RT75 and RT150 pigs. This study highlights that if pigs are not initially given enough rest to recover from exercise, a subsequent exposure to the same exercise will cause an increase in these physiological variables during exercise and recovery. Further research is needed to investigate factors contributing to the quality of rest, with a particular focus on conditions not allowing a proper rest on the truck or in lairage. INTRODUCTION Giving pigs the opportunity to recover from transport stress is crucial from meat quality and welfare standpoints (Warriss, 2003). Loading has been shown to be 1 of the most stressful steps of the transport process (Grandin, 1997). After loading, animals are exposed to additional stressors associated with transport, such as vibrations (Perremans et al., 2001), careless driving (Peeters et al., 2008), and crowding (Warriss, 1998), which may affect the quality of rest during transit. Afterward, the positive effects of any recovery during transport may be counteracted by the stress of unloading (Torrey et al., 2013). Ritter et al. (2009a) have demonstrated that concurrent stressors occurring during transport had an additive effect on body temperature, blood acid-base balance, and lactate values in market-weight pigs. Inadequate recovery times from the stress of loading at the farm (Chevillon, 2001), on the truck (Pilcher et al., 2011), or at the abattoir (Warriss, 2003) have been shown to have a negative impact on pig meat quality and welfare. The issue of the lack of recovery during transport may be illustrated by the case of fatigued pigs, which represent a significant portion of transport losses (Benjamin, 2005). Although the majority of fatigued pigs will recover if given enough time to rest (2 to 3 h), further exposure to stressful events may lead to death in these animals (Ritter et al., 2009b). The extent to which the physiology and behavior of pigs subjected to multiple stressors is affected by rest duration is still unclear. The objective of this study was therefore to investigate the effects of the duration of recovery time from an initial exposure to stress (i.e., handling and exercise) on the subsequent stress response and recovery of near-market-weight pigs to a second stress exposure. Our hypothesis is that an appropriate rest period will help pigs cope better with the succession of stressors to which they are exposed during transport. MATERIALS AND METHODS All experimental procedures performed in this study were approved by the University of Saskatchewan's Animal Research and Ethics Board and adhered to the Canadian Council on Animal Care's guidelines for humane animal use (Canadian Council on Animal Care, 2009). Animals and Treatments This study was undertaken at the Prairie Swine Centre Inc. (Saskatoon, SK, Canada). Over 6 replicates, 18 groups of 3 gilts (n = 54; negative for the HAL-1843 mutation and a cross between an L-42 sow and 337 boar; Pig Improvement Company, Winnipeg, MB, Canada), weighing approximately 110 kg, were randomly allocated to 1 of 3 treatments, consisting of rest periods of either 35 min (RT35), 75 min (RT75), or 150 min (RT150). Within a replicate, treatments were randomly assigned to a group of 3 animals and had their own test day. The rest durations respectively corresponded to 0.5, 1, or 2 times the duration of a full recovery time (FRT, 75 ± 11.4 min) from exposure to a standard handling course (Fig. 1). The FRT was determined in a preliminary study (at an ambient temperature ranging from 18.5°C to 21.9°C; data not shown), in which 7 groups of 3 gilts, weighing around 110 kg, were used. The same variables as in the current experiment were evaluated during and after a single exposure to exercise in the same handling course. From this preliminary study, it was determined that for pigs exposed to our handling course, cardiac, respiratory, thermal, and behavioral (posture) variables returned to baseline levels after rest periods of 18, 15, 75, and 55 min, respectively (Table 1). Figure 1. View largeDownload slide Diagram of (top) the bridge and (bottom) the standard handling course. Figure 1. View largeDownload slide Diagram of (top) the bridge and (bottom) the standard handling course. Table 1. Average skin temperature, heart rate, and respiratory rate at rest and latency to return to rest after a unique exposure to exercise for the 7 groups of 3 pigs used in the preliminary study Item  Skin temperature  Heart rate  Respiratory rate      beats/min  breaths/min  Resting value (RV)  36.9 ± 0.1°C  96.2 ± 2.7  28.4 ± 0.3  Latency to return to RV, min  75.2 ± 11.4  18.1 ± 4.3  15.1 ± 3.9  Item  Skin temperature  Heart rate  Respiratory rate      beats/min  breaths/min  Resting value (RV)  36.9 ± 0.1°C  96.2 ± 2.7  28.4 ± 0.3  Latency to return to RV, min  75.2 ± 11.4  18.1 ± 4.3  15.1 ± 3.9  View Large Table 1. Average skin temperature, heart rate, and respiratory rate at rest and latency to return to rest after a unique exposure to exercise for the 7 groups of 3 pigs used in the preliminary study Item  Skin temperature  Heart rate  Respiratory rate      beats/min  breaths/min  Resting value (RV)  36.9 ± 0.1°C  96.2 ± 2.7  28.4 ± 0.3  Latency to return to RV, min  75.2 ± 11.4  18.1 ± 4.3  15.1 ± 3.9  Item  Skin temperature  Heart rate  Respiratory rate      beats/min  breaths/min  Resting value (RV)  36.9 ± 0.1°C  96.2 ± 2.7  28.4 ± 0.3  Latency to return to RV, min  75.2 ± 11.4  18.1 ± 4.3  15.1 ± 3.9  View Large Before testing, pigs were not subjected to any handling besides weighing, or previous exposure to a ramp. Gilts were housed in groups of 12 animals at a space allowance of 0.72 m2/100 kg. Pigs had ad libitum access throughout the experiment to water and barley/wheat and canola diets formulated to meet their requirements. Procedures Within each group of 12 animals, 3 pigs were selected using an open door test (adapted from Brown et al., 2009) a week before the trial. Treatments [Rest Period 1 (RP1) of 35, 75, or 150 min] were then randomly assigned to the groups of 3 animals. The open door test was used to select test pigs to assess the effect of the treatment across various coping strategies (proactive, intermediate, and reactive). Just before performing the test, a person entered the home pen to mark the pigs from 1 to 10 to identify them during the test. The pen door was then opened by the observer from a distance of 1 m away from the pen entrance. Over a 3-min period, pigs were free to leave the pen and go into a hallway. For each pig, the latency to get out of the pen (hind feet crossing the entrance of the pen) was recorded. Pigs received a rank (from 1 to 10) according to their latency to exit. Pigs that did not exit the pen got the maximum latency (180 s) and were scored as last (rank 10). The first, fifth, and the last pigs were selected to be fitted with the heart rate monitors. Before each test, pigs were moved out of their home pen into a hallway. Pigs had been fasted for approximately 6 h before being tested. Each test pig was restrained between 2 gates, shaved, fitted with a heart rate monitor belt, and marked on the back using spray paint. After being fitted with the monitor on the experiment day, the 3 test pigs were then returned to the room and housed for 1 h in 3 individual rest pens (1.95 × 0.6 m) adjacent to each other (Fig. 1) to recover from handling associated with belting (initial rest period, RP0). The 3 pens were also adjacent to the home pen containing the remaining pen mates to provide a familiar environment to the test pigs. The purpose of isolating pigs was to prevent their recovery from being disturbed by other pigs chewing the heart rate monitors. Pigs were assigned to the same individual pens throughout the study to reduce any novelty effects later on. After 1 h of recovery, the tests began by moving the group of pigs out of the room and exercising them (exercise 1: Ex1) in the hallway. A session of exercise consisted of walking at a moderate pace in the standard handling course, up and down a bridge (6 times each) over a total distance of 500 m (Fig. 1). The bridge was made of aluminum and consisted of 2 ramps (slope: 19.4°) joined by a horizontal platform. Pigs were moved according to a standard handling protocol. The same handler walked each group of 3 pigs using a paddle to hit the floor 3 times every 15 s and using the voice every 5 s. On the bridge, a handling board was used to push reluctant pigs up or to block pigs trying to turn back. Each pig was tapped with a paddle, twice on the back on the way up and twice on the way down. After completing the course, pigs were returned to their individual pens. Pigs were then given a rest period (RP1) of either 35, 75, or 150 min. Afterward, all pigs were moved a second time through the handling course (exercise 2, Ex2) in the same way as in Ex1, returned to their pens, and then given a rest period of 150 min (Rest Period 2, RP2; Fig. 2). Figure 2. View largeDownload slide Timeline of the experiment. RP0, initial rest; RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. Figure 2. View largeDownload slide Timeline of the experiment. RP0, initial rest; RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. Data Collection Heart Rate. Heart rate (HR) was recorded at 5-s intervals, using Polar heart rate monitors (Team Polar, Polar Electro Canada, Quebec, QC, Canada), during rest and exercise periods. Average heart rate over the entire period was considered during exercise, whereas only the last 5 min were considered as a response during the rest periods. The cardiac baseline was defined as the average HR measured from the 30th min to the 40th min during RP0. Video recordings (HandyCam DCR-SR68,Sony, Mississauga, ON, Canada) were used to make sure that the pigs were resting and not in activity during this period, which was the case for all the tested animals in this experiment. Respiratory Rate. The respiratory rate (RR) was only monitored during the rest periods using video cameras (HandyCam DCR-SR68, Sony, Mississauga, ON, Canada) and analyzed by counting rib cage movements over 1 min at 3-min intervals during the rest periods. Average respiratory rate over the entire period was considered during exercise, whereas only the last 6 min were considered as a response during the rest periods. Respiratory baseline was defined as the average RR monitored during 1 min periods at 3 min intervals from the 30th min to the 40th min of RP0. Skin Temperature. Skin temperature (ST) was assessed on the sternal area using iButton data loggers (High Resolution Thermochron iButton DS1921H, Maxim Integrated Products Inc., Sunnyvale, CA) attached with Velcro to the belt used for heart rate monitoring. iButtons recorded temperature at 1-min intervals throughout the experiment. Average skin temperature over the entire period was considered during exercise, whereas only the last 5 min were considered as a response during the rest periods. Temperature baseline was determined as the average ST recorded over the last 10 min of RP0. Posture. Using video recording (HandyCam DCR-SR68, Sony), posture (standing, sitting, and lying) and activity (drinking, exploring environment) were noted for each pig, every minute of the rest periods, using the scan sampling method. Pigs were considered as having recovered during RP2 when their physiological variables returned to the respective baselines. As for the behavioral variable, pigs were considered as having recovered when they resumed activity for at least 3 min after lying and being inactive for at least 3 min. Recovery times for all variables were calculated for each pig on the basis of its own baseline. Environmental Conditions. Environmental temperature was monitored at 1-min intervals throughout the experiment using iButtons (DS1923 Hygrochron Temperature/Relative Humidity Logger, Maxim Integrated Products Inc., Sunnyvale, CA) suspended at a height of 1 m in the room and 1.5 m in the hallway. Statistical Analysis The experiment was designed as a randomized complete block design. Each group of 3 pigs tested together on a given treatment was considered as the experimental unit. Normality and homogeneity of variance (Shapiro-Wilk test) were tested before the analysis. For each treatment, the effect of exposure to exercise on the stress responses was analyzed by repeated measures ANOVA with the PROC MIXED procedure in SAS (v9.2, SAS Inst. Inc., Cary, NC). Environmental temperature during the rest and exercise periods was also analyzed by repeated measures ANOVA with PROC MIXED. The models used for stress responses and environmental temperature included the fixed effects of treatment, repeated effect of period (rest and exercise periods), and the random effect of replicate. Recovery times during RP2 were compared across treatments by ANOVA using PROC MIXED with rest duration treated as a fixed effect and replicate as the random effect. Tukey-Kramer adjustments were used to compare treatment means. When residual normality was not met, transformations using the BOXCOX procedure in SAS were performed. Untransformed least squares means and SEM are reported. Regression analyses, where the number of exposures to the handling course (0, 1, or 2) or the number of rest periods (0, 1, or 2) was the independent variable, were conducted using PROC REG in SAS to determine if the stressors had an additive effect on the dependent variables: heart rate, respiratory rate, and skin temperature. The values used for the regressions analyses for number of exposure to exercise were baseline values for no exposure, Ex1 values for 1 exposure and Ex2 values for 2 exposures. In the case of the number of rest periods, the values used were baseline values for no rest period, RP1 values for 1 rest period, and RP2 values for 2 rest periods. A probability level of P < 0.05 was chosen as the limit for statistical significance in all tests. RESULTS Heart Rate For all 3 treatments (Fig. 3), average HR measured during Ex1 and Ex2 did not differ (P > 0.05) but was greater (P < 0.001 and P < 0.001, respectively) than HR measured during the baseline period and RP1. Heart rate recorded during RP2 was lower than HR recorded during Ex1 and Ex2 (P < 0.001 for both) for all 3 treatments but was greater than HR recorded during baseline and RP1 for RT35 pigs (P < 0.001 for both). The HR during RP2 was not different (P > 0.05) from baseline and RP1 for RT75 and RT150 pigs. The effect of the number of exercise bouts and rest periods on HR was not linear (P > 0.05; Table 2) for all 3 treatments. The latency to return to a baseline HR was greater (P = 0.024) for RT35 pigs compared to RT75 and RT150 pigs (Table 3). Figure 3. View largeDownload slide Comparison of the heart rate response throughout the experiment of (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; P < 0.001), and (c) RT150 (n = 7; P < 0.001) pigs. RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a–cWithin each treatment, means with different superscripts differ (P < 0.05). Figure 3. View largeDownload slide Comparison of the heart rate response throughout the experiment of (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; P < 0.001), and (c) RT150 (n = 7; P < 0.001) pigs. RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a–cWithin each treatment, means with different superscripts differ (P < 0.05). Table 2. Regression analysis of the number of rest (RP) and exercise (Ex) periods on heart and respiratory rates and temperature for each treatment     RT351(n = 7)  RT752 (n = 7)  RT1503 (n = 7)  Variable  Periods  r2  P  r2  P  r2  P  Heart rate  RP  0.41  0.217  0.03  0.509  0.77  0.779    Ex  0.51  0.366  0.33  0.393  0.34  0.391  Temperature  RP  0.98  0.064  0.74  0.238  0.97  0.078    Ex  0.99  0.003  0.99  0.038  0.05  0.515  Respiratory rate  Ex  0.29  0.406  0.71  0.25  0.98  0.061      RT351(n = 7)  RT752 (n = 7)  RT1503 (n = 7)  Variable  Periods  r2  P  r2  P  r2  P  Heart rate  RP  0.41  0.217  0.03  0.509  0.77  0.779    Ex  0.51  0.366  0.33  0.393  0.34  0.391  Temperature  RP  0.98  0.064  0.74  0.238  0.97  0.078    Ex  0.99  0.003  0.99  0.038  0.05  0.515  Respiratory rate  Ex  0.29  0.406  0.71  0.25  0.98  0.061  1RT35: pigs given 35 min rest. 2RT75: pigs given 75 min rest. 3RT150: pigs given 150 min rest. View Large Table 2. Regression analysis of the number of rest (RP) and exercise (Ex) periods on heart and respiratory rates and temperature for each treatment     RT351(n = 7)  RT752 (n = 7)  RT1503 (n = 7)  Variable  Periods  r2  P  r2  P  r2  P  Heart rate  RP  0.41  0.217  0.03  0.509  0.77  0.779    Ex  0.51  0.366  0.33  0.393  0.34  0.391  Temperature  RP  0.98  0.064  0.74  0.238  0.97  0.078    Ex  0.99  0.003  0.99  0.038  0.05  0.515  Respiratory rate  Ex  0.29  0.406  0.71  0.25  0.98  0.061      RT351(n = 7)  RT752 (n = 7)  RT1503 (n = 7)  Variable  Periods  r2  P  r2  P  r2  P  Heart rate  RP  0.41  0.217  0.03  0.509  0.77  0.779    Ex  0.51  0.366  0.33  0.393  0.34  0.391  Temperature  RP  0.98  0.064  0.74  0.238  0.97  0.078    Ex  0.99  0.003  0.99  0.038  0.05  0.515  Respiratory rate  Ex  0.29  0.406  0.71  0.25  0.98  0.061  1RT35: pigs given 35 min rest. 2RT75: pigs given 75 min rest. 3RT150: pigs given 150 min rest. View Large Table 3. Comparison of the latencies (min) for heart and respiratory rates, temperature, and posture to return to baseline values during the full Rest Period 2 (150 min) among the 3 treatments   Treatment    Item  RT351 (n = 7)  RT752 (n = 7)  RT1503 (n = 7)  SEM  P-value  Heart rate  39.0a  20.1b  19.3b  4.5  0.024  Respiratory rate  38.2a  18.3b  17.8b  3.4  <0.001  Temperature  112.1a  89.3b  82.6b  7.7  0.021  Posture  89.9a  70.9b  71.5b  5.1  0.038    Treatment    Item  RT351 (n = 7)  RT752 (n = 7)  RT1503 (n = 7)  SEM  P-value  Heart rate  39.0a  20.1b  19.3b  4.5  0.024  Respiratory rate  38.2a  18.3b  17.8b  3.4  <0.001  Temperature  112.1a  89.3b  82.6b  7.7  0.021  Posture  89.9a  70.9b  71.5b  5.1  0.038  a,bMeans within a row with different superscripts differ (P < 0.05). 1RT35: pigs given 35 min rest. 2RT75: pigs given 75 min rest. 3RT150: pigs given 150 min rest. View Large Table 3. Comparison of the latencies (min) for heart and respiratory rates, temperature, and posture to return to baseline values during the full Rest Period 2 (150 min) among the 3 treatments   Treatment    Item  RT351 (n = 7)  RT752 (n = 7)  RT1503 (n = 7)  SEM  P-value  Heart rate  39.0a  20.1b  19.3b  4.5  0.024  Respiratory rate  38.2a  18.3b  17.8b  3.4  <0.001  Temperature  112.1a  89.3b  82.6b  7.7  0.021  Posture  89.9a  70.9b  71.5b  5.1  0.038    Treatment    Item  RT351 (n = 7)  RT752 (n = 7)  RT1503 (n = 7)  SEM  P-value  Heart rate  39.0a  20.1b  19.3b  4.5  0.024  Respiratory rate  38.2a  18.3b  17.8b  3.4  <0.001  Temperature  112.1a  89.3b  82.6b  7.7  0.021  Posture  89.9a  70.9b  71.5b  5.1  0.038  a,bMeans within a row with different superscripts differ (P < 0.05). 1RT35: pigs given 35 min rest. 2RT75: pigs given 75 min rest. 3RT150: pigs given 150 min rest. View Large Skin Temperature The ST measured during the baseline period was lower (P < 0.001) than the ST during the other periods for RT35 (Fig. 4a) and RT75 (Fig. 4b) pigs, whereas it was not different from the ST in RP1 and RP2 for RT150 pigs (P > 0.05; Fig. 4c). For RT35 pigs, ST recorded during Ex1 and RP1 were not different from each other (P > 0.05; Fig. 4a), but both were significantly lower (P < 0.001) than ST recorded during Ex2 and RP2, which did not differ from each other (P > 0.05). For RT75 pigs, ST recorded during Ex1, RP1, and RP2 did not differ (P > 0.05) from each other, whereas ST during Ex1 was lower (P = 0.006) than temperature during Ex2 (Fig. 4b). However, ST recorded during RP1, Ex2, and RP2 were not significantly different (P > 0.05). For RT150 pigs, the ST recorded during Ex1 did not differ from ST recorded during Ex2 (P > 0.05; Fig. 4c) but was greater than the ST recorded during RP1 and RP2 (P = 0.028 and P = 0.035, respectively), which did not differ from each other (P > 0.05). Skin temperature recorded during Ex2 did not differ from RP2 (P > 0.05) but was greater (P = 0.039) than the ST recorded during RP1. The effect of the number of rest periods on ST tended to be linear for RT35 and RT150 pigs (P = 0.064 and P = 0.078, respectively; Table 2), whereas it was not linear for RP75 pigs (P > 0.05). The effect of the number of exercise bouts on ST was linear for RT35 and RT75 pigs (P = 0.003 and P = 0.038, respectively; Table 2), whereas it was not linear for RT150 pigs (P > 0.05). It took more time for the ST of RT35 pigs to return to baseline compared to RT75 and RT150 pigs (P = 0.021; Table 3). Figure 4. View largeDownload slide Comparison of the skin temperature response throughout the experiment of (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; < 0.001), and c) RT150 (n = 7; P = 0.012) pigs. RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a–cWithin each treatment, means with different superscripts differ (P < 0.05). Figure 4. View largeDownload slide Comparison of the skin temperature response throughout the experiment of (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; < 0.001), and c) RT150 (n = 7; P = 0.012) pigs. RP1, Rest Period 1; RP2, Rest Period 2; Ex1, exercise 1; Ex2, exercise 2; RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a–cWithin each treatment, means with different superscripts differ (P < 0.05). Respiratory Rate The RR of RT35 pigs was greater (P < 0.001) during RP2 compared to the baseline and RP1, which did not differ from one another (Fig. 5a). There were no differences (P > 0.05) in RR between the baseline, RP1, and RP2 for pigs given either RT75 or RT150 (Fig. 5b and 5c). The effect of the number of exercise bouts on RR was not linear (P > 0.05; Table 2) for RT35 and RT75 pigs, whereas it tended to be linear (P = 0.061) for RT150 pigs. The latencies of the RR and posture to return to baseline were greater for RT35 pigs compared to RT75 and RT150 pigs (P < 0.001 and P = 0.038, respectively; Table 3). Figure 5. View largeDownload slide Comparison of the respiratory response of pigs for (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; P = 0.331), and (c) RT150 (n = 7; P = 0.225) pigs during rest periods 1 (RP1) and 2 (RP2). RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a,bWithin each treatment, means with different superscripts differ (P < 0.05); RP1: Rest Period 1; RP2: Rest Period 2. Figure 5. View largeDownload slide Comparison of the respiratory response of pigs for (a) RT35 (n = 7; P < 0.001), (b) RT75 (n = 7; P = 0.331), and (c) RT150 (n = 7; P = 0.225) pigs during rest periods 1 (RP1) and 2 (RP2). RT35, RT75, and RT150, treatments consisting of rest times of 35, 75, and 150 min, respectively. a,bWithin each treatment, means with different superscripts differ (P < 0.05); RP1: Rest Period 1; RP2: Rest Period 2. Handling Time Pigs given half of the FRT (RT35) required more time to complete the handling course during Ex2 compared to Ex1 (20.4 ± 1.8 and 16.6 ± 0.6 min, respectively; P = 0.039; data not shown), and RT150 pigs took more time to complete Ex1 compared to Ex2 (17.5 ± 1.3 vs. 14.4 ± 0.9 min; respectively; P = 0.036; data not shown). No differences in handling time between Ex1 and Ex2 were observed for RT75 pigs (16.4 ± 1.3 vs. 15.8 ± 0.7 min; respectively; P > 0.05; data not shown). Ambient Temperature The ambient temperatures recorded during Ex1 and Ex2 (21.2°C and 22.1°C, respectively) were greater (P = 0.006) than those recorded during RP0 and RP1 (18.6°C and 18.9°C, respectively), whereas the temperature measured during RP2 (20.8°C) was not different (P > 0.05; data not shown) from the temperatures recorded during the other periods. DISCUSSION The aim of this study was to determine the extent to which the duration of the rest time given to near-market-weight pigs after an initial exposure to exercise affected their recovery from subsequent exercise. The results show that when pigs are given the appropriate duration of rest allowing a full recovery (RT75 treatment), there is no detrimental effect of a second exposure to exercise on cardiac and respiratory responses or on handling time. Exposure to exercise resulted in similar increases in heart rate to those found during loading under commercial conditions in other studies (Geverink et al., 1998; Correa et al., 2010, 2013). Both heart and respiratory rates returned to their respective baseline levels during RP1. This result was expected because the duration of RP1 was greater than the heart rate and respiratory recovery times (18 and 15 min, respectively) measured during the aforementioned preliminary study. The baseline values obtained in the present study were similar to the resting cardiac values found by Correa et al. (2013; approximately 100 beats/min) in commercial farms or the average resting respiratory rate reported by the (American Veterinary Medical Association 2012); 25–30 breaths/min), demonstrating that the animals were indeed at rest before the first exercise. A return to baseline was also found for these same variables in RP2. Different from cardiac and respiratory responses, skin temperature, after an initial rise during handling, most likely associated with physical stress (Betley and Bayley, 1988), did not return to baseline by the end of RP1 for RT35 and RT75. This result is surprising on the basis of the results of the preliminary study showing that 75 min were necessary for thermal recovery. The fact that pigs' skin temperature returned to baseline levels after 82 min suggests that the 75-min rest period used was not sufficient for pigs to achieve full thermal recovery. This may lead us to reconsider the validity of the recovery time of ST and consequently FRT, which was supposed to give pigs enough time to recover with regard to all variables. The inability to achieve thermal recovery after 75 min could not be explained by differences in ambient temperature between the pilot and the present study because the experimental temperatures were within the range of the pilot temperatures. However, it may be attributed to differences in reactivity to exercise between groups of pigs. In the present study, there was an additive increase in skin temperature during the second exercise period compared to the first one, suggesting that the second exposure to exercise was more challenging than the first one. Similar results and conclusions were found by Brown et al. (2005), who recorded a greater skin temperature during unloading compared to loading. The increase in skin temperature during Ex2 is most likely because RT75 pigs did not recover with regard to the thermal response during RP1. Indeed, the combination of the remaining body heat from Ex1, which was not dissipated, and the heat produced during the second exercise must have contributed to the greater temperature in Ex2 compared to Ex1. The second exposure to exercise did not have a detrimental effect on the recovery of the animals, as shown by the absence of difference in skin temperature during RP1 and RP2. The fact that the temperature during these 2 rest periods was greater than the baseline confirms that the heat could not be dissipated within the rest time given to the animals. Contrary to RT75 pigs, RT150 pigs had time to fully recover from both exposures to exercise. Doubling the rest period did not provide any more benefits with regard to the respiratory and cardiac responses during exercise and recovery periods compared to RT75 pigs, as shown by the similar latencies to recover for these 2 variables. However, RT150 pigs had similar skin temperature during each exercise and required less time to complete the handling course during the second exercise. Although pigs in all treatments may have become more familiar with the standard handling course during the second exercise, the novelty reduction effect was only shown for RT150 pigs. These pigs were likely in a similar physiological state during both exercise periods, whereas for the other pigs, fatigue may have overcome the positive effect of familiarization. Our results are consistent with the literature showing that if pigs are kept in lairage for a long time (>4 h), they have time to physiologically recover (Marchant-Forde and Marchant-Forde, 2009). Most of the studies on this subject also show that pigs may begin to fight with pen mates once they recover from unloading stress (Nanni Costa et al., 2002; Warriss, 2003; Guàrdia et al., 2009). However, in the present study, pigs were individually penned to preclude this confounding factor. Finally, the results of this study show that a lack of rest after an initial exposure to exercise makes pigs more susceptible to stress during the second exercise and rest periods. Although the cardiac and respiratory responses of RT35 pigs returned to the baselines during RP1, skin temperature did not. As expected, the animals were not in a physiological state of recovery, which may explain the increase observed in all variables during Ex2 and RP2 compared to Ex1 and RP1, respectively. These observations suggest that the second exercise was more challenging for pigs not given enough time to recover from the exercise. This is confirmed by the fact that those pigs completed the handling course more slowly the second time. Because pigs were more familiar with the handling course the second time around, the challenge was likely more physical than psychological. Chevillon (2001) reported that the lack of rest between exiting the finishing pen and loading contributed to a more physically challenging handling and demonstrated that holding pigs in resting areas before loading could decrease heart rate compared to immediate loading (110 vs. 170 beats/min, respectively) onto the truck. It is unlikely that the ambient temperature played a role in the greater responses observed during Ex2 and RP2 because there were no differences in this variable between the exercise and rest periods. The measure of additional variables, such as indicators of muscle fatigue (i.e., lactate), could have helped explain the potential mechanism(s) underlying the greater response observed for RT35. The greater physiological responses observed after exposure to the second exercise confirm the detrimental effect of a lack of rest found by studies looking at the time needed by pigs in lairage to recover from transport stress. It has been reported that short lairage times (<1 to 2 h) do not give pigs sufficient time to recover from the stressors experienced during transport. Pigs may then become harder to handle (Milligan et al., 1998) and have increased levels of cortisol, creatine phosphokinase (CPK), and lactate (Warriss et al., 1998a,b; Pérez et al., 2002; Hambrecht et al., 2005), indicating fatigue and stress. The effect of the number of exposures to exercise on heart rate was additive, whereas the effect of the number of rest periods on the same variable tended to be additive. These results agree with other studies reporting additive effects of exposures to concurrent stressors on production and health variables (McFarlane et al. 1989a,b; Hyun et al., 1998) or metabolic stress responses (Ritter et al., 2009a). In the present study, RT35 pigs did not recover from the second exposure to exercise when given the same rest duration as after the first exercise. However, when given more than 35 min to rest, they eventually recovered. Their latencies of recovery were all significantly greater than those obtained for RT75 or RT150 pigs. Indeed, the latencies of the cardiac and respiratory responses doubled compared to the 2 other groups of pigs, whereas for skin temperature and posture, the latencies were approximately 25% and 36% and 27% and 26% longer compared to RT75 and RT150 pigs, respectively. These observations support studies suggesting that fatigued pigs, when given more time to rest, may physiologically recover from this condition and return to normal appearance and mobility (Benjamin, 2005; Ritter et al., 2009b). Conclusion The results of this study show the importance of the length of the rest period and highlight that if pigs are not initially given enough rest to recover from the exposure to exercise, there will be a detrimental effect on the recovery from subsequent exposure to the same exercise. Thus, giving pigs an appropriate time to recover during transport or lairage will help them cope with further exposures to stressors and will ultimately improve animal welfare. More research needs to be conducted on factors contributing to the quality of rest, with a particular focus on conditions that do not allow a proper rest on the truck or in lairage (high and low stocking density, short journey, mixing, noise, vibration). LITERATURE CITED American Veterinary Medical Association 2012. Recommendations for risk management at swine exhibitions and for show pigs. http://ce.ingham.org/Portals/CE/4HDocs/Tabs/Member%20Resources/Projects/Animals/Swine/Recommendations%20for%20Risk%20Management%20at%20Swine%20Exhibitions%20and%20for%20Show%20Pigs%20-%2008%2015%2012.pdf. (Accessed 29 November 2012.) Betley M. P. Bayley H. S. 1988. Exercise and postexercise energy expenditure in growing pigs. Can. J. Physiol. Pharmacol.  66: 721– 730. Google Scholar CrossRef Search ADS PubMed  Benjamin M 2005. Pig trucking and handling—Stress and fatigued pig. Adv. Pork Prod.  16: 57– 66. Brown J. A. Dewey C. Delange C. F. M. Mandell I. B. Purslow P. P. Robinson J. A. Squires E. J. Widowski T. M. 2009. Reliability of temperament tests on finishing pigs in group housing and comparison to social tests. Appl. Anim. Behav. Sci.  118: 28– 35. Google Scholar CrossRef Search ADS   Brown S. N. Knowles T. G. Wilkins L. J. Chadd S. A. Warriss P. D. 2005. The response of pigs to being loaded or unloaded onto commercial animal transporters using three systems. Vet. J.  170: 91– 100. Google Scholar CrossRef Search ADS PubMed  Canadian Council on Animal Care 2009. Guidelines on the care and use of farm animals in research, teaching and testing. Can. Counc. Anim. Care, Ottawa. Chevillon P 2001. Pig welfare during pre-slaughter and stunning. In: Proc. 1st Int. Virtual Conf. on Pork Quality,  Concordia, Brazil. p. 145– 158. Correa J. A. Gonyou H. W. Torrey S. Widowski T.M. Crowe T. G. Laforest J. -P. Faucitano L. 2013. Welfare and carcass and meat quality of pigs being transported for 2 hours using two vehicle types during two seasons of the year. Can. J. Anim. Sci.  93( 1). 43– 55. Google Scholar CrossRef Search ADS   Correa J. A. Torrey S. Devillers N. Laforest J. P. Gonyou H. W. Faucitano L. 2010. Effects of different moving devices at loading on stress response and meat quality in pigs. J. Anim. Sci.  88: 4086– 4093. Google Scholar CrossRef Search ADS PubMed  Geverink N. A. Buhnemann A. Van de Burgwal J. A. Lambooij E. Blokhuis H. J. Wiegant V. M. 1998. Responses of slaughter pigs to transport and lairage sounds. Physiol. Behav.  63: 667– 673. Google Scholar CrossRef Search ADS PubMed  Grandin T 1997. Assessment of stress during handling and transport. J. Anim. Sci.  75: 249– 257. Google Scholar CrossRef Search ADS PubMed  Guàrdia M. D. Estany J. Balasch S. Oliver M. A. Gispert M. Diestre A. 2009. Risk assessment of skin damage due to pre-slaughter conditions and RYRI gene in pigs. Meat Sci.  81: 745– 751. Google Scholar CrossRef Search ADS PubMed  Hambrecht E. Eissen J. J. Newman D. J. Smits C. H. M. Den Hartog L. A. Verstegen M. W. A. 2005. Negative effects of stress immediately before slaughter on pork quality are aggravated by suboptimal transport and lairage conditions. J. Anim. Sci.  83: 440– 448. Google Scholar CrossRef Search ADS PubMed  Hyun Y. Ellis M. Riskowski G. Johnson R. W. 1998. Growth performance of pigs subjected to multiple concurrent environmental stressors. J. Anim. Sci.  76: 721– 727. Google Scholar CrossRef Search ADS PubMed  Marchant-Forde J. N. Marchant-Forde R. M. 2009. Welfare of pigs during transport and slaughter. In: Marchant-Forde J. N. editor, The welfare of pigs.  Springer, Dordrecht, Netherlands. p. 301– 330. Google Scholar CrossRef Search ADS   McFarlane J. M. Curtis S. E. Shanks R. D. Carmer S. G. 1989a. Multiple concurrent stressors in chicks. 1. Effect on weight gain, feed intake, and behavior. Poult. Sci.  68: 501– 509. Google Scholar CrossRef Search ADS   McFarlane J. M. Curtis S. E. Shanks R. D. Carmer S. G. 1989b. Multiple concurrent stressors in chicks. 3. Effect on plasma corticosterone and heterophil:lymphocyte ratio. Poult. Sci.  68: 522– 527. Google Scholar CrossRef Search ADS   Milligan S. D. Ramsey C. B. Miller M. F. Kaster C. S. Thompson L. D. 1998. Resting pigs and hot fat trimming and accelerated chilling of carcasses to improve pork quality. J. Anim. Sci.  76: 74– 86. Google Scholar CrossRef Search ADS PubMed  Nanni Costa L. Lo Fiego D. P. Dallolio S. Davoli R. Russo V. 2002. Combined effects of pre-slaughter treatments and lairage time on carcass and meat quality in pigs of different halothane genotype. Meat Sci.  61: 41– 47. Google Scholar CrossRef Search ADS PubMed  Peeters E. Deprez K. Beckers F. de Baerdemaeker J. Aubert A. E. Geers R. 2008. Effect of driver and driving style on the stress responses of pigs during a short journey by trailer. Anim. Welf.  17: 189– 196. Pérez M. P. Palacio J. Santolaria M. P. Acena M. C. Chacon G. Gascon M. Calvo J. H. Zaragoza P. Beltran J. A. Garcia-Belenguer S. 2002. Effect of transport time on welfare and meat quality in pigs. Meat Sci.  61: 425– 433. Google Scholar CrossRef Search ADS PubMed  Perremans S. Randall J. M. Rombouts G. Decuypere E. Geers R. 2001. Effect of whole body vibration in the vertical axis on cortisol and adevenocorti hormone levels in piglets. J. Anim. Sci.  79: 975– 981. Google Scholar CrossRef Search ADS PubMed  Pilcher C. M. Ellis M. Rojo-Gómez A. Curtis S. E. Wolter B. F. Peterson C. M. Peterson B. A. Ritter M. J. Brinkmann J. 2011. Effects of floor space during transport and journey time on indicators of stress and transport losses of market-weight pigs. J. Anim. Sci.  89: 3809– 3818. Google Scholar CrossRef Search ADS PubMed  Ritter M. J. Ellis M. Anderson D. B. Curtis S. E. Keffaber K. K. Killefer J. McKeith F. K. Murphy C. M. Peterson B. A. 2009a. Effects of multiple concurrent stressors on rectal temperature, blood acid-base status, and longissimus muscle glycolytic potential in market-weight pigs. J. Anim. Sci.  87: 351– 362. Google Scholar CrossRef Search ADS   Ritter M. J. Ellis M. Berry N. L. Curtis S. E. Anil L. Berg E. Benjamin M. Butler D. Dewey C. Driessen B. DuBois P. Hill J. D. Marchant-Forde J. N. Matzat P. McGlone J. Mormede P. Moyer T. Pfalzgraf K. Salak-Johnson J. Siemens M. Sterle J. Stull C. Whiting T. Wolter B. Niekamp S. R. Johnson A. K. 2009b. Transport losses in market weight pigs: A review of definitions, incidence, and economic impact. Prof. Anim. Sci.  25: 404– 414. Torrey S. Bergeron R. Widowski T. Lewis N. Crowe T. Correa J. A. Brown J. Gonyou H. W. Faucitano L. 2013. Transportation of market-weight pigs: I. Effect of season, truck type, and location within truck on behavior with a two-hour transport. J. Anim. Sci.  91: 2863– 2871. Google Scholar CrossRef Search ADS PubMed  Warriss P. D 1998. Choosing appropriate space allowances for slaughter pigs transported by road: A review. Vet. Rec.  142: 449– 454. Google Scholar CrossRef Search ADS PubMed  Warriss P. D 2003. Optimal lairage times and conditions for slaughter pigs: A review. Vet. Rec.  153: 170– 176. Google Scholar CrossRef Search ADS PubMed  Warriss P. D. Brown S. N. Edwards J. E. Knowles T. G. 1998a. Effect of lairage time on levels of stress and meat quality in pigs. Anim. Sci.  66: 255– 261. Google Scholar CrossRef Search ADS   Warriss P. D. Brown S. N. Knowles T. G. Edwards J. E. Kettlewell P. J. Guise H. J. 1998b. The effect of stocking density in transit on the carcass quality and welfare of slaughter pigs. 2. Results from the analysis of blood and meat samples. Meat Sci.  50: 447– 456. Google Scholar CrossRef Search ADS   American Society of Animal Science TI - Effect of rest duration on recovery from repeated exercise in near-market-weight pigs JF - Journal of Animal Science DO - 10.2527/jas.2012-6184 DA - 2013-12-01 UR - https://www.deepdyve.com/lp/oxford-university-press/effect-of-rest-duration-on-recovery-from-repeated-exercise-in-near-VeGUE0Vx7P SP - 5859 EP - 5867 VL - 91 IS - 12 DP - DeepDyve ER -