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ANIMAL PRODUCTION |
* CSIRO Livestock Industries, Queensland Bioscience Precinct, St Lucia, QLD 4067, Australia; and
and
NSW Agriculture, Elizabeth Macarthur Agricultural Institute, Camden, NSW 2570, Australia.
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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Key Words: Growth Performance • Stress • Swine • Temperature
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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; Wellock et al., 2003). Previous studies have indicated that single stressors have a detrimental effect on pig performance (Nielsen et al., 1996; Gonyou and Stricklin, 1998; Bornett et al., 2000a; Quiniou et al., 2000; de Groot et al., 2001). Hyun et al. (1998a) evaluated the effects of temperature, stocking density, and grouping in a multiple concurrent format and concluded that the effects are additive. Bornett et al. (2000a) investigated the effect of sequential changes in housing arrangement on feeding patterns and social behavior by changing pigs from individual to group and back to individual housing situations. The authors found that feeding behavior was adaptable across these housing changes (i.e., the pigs maintained feed intake). Because a pig reared in a commercial environment can encounter sequences of multiple concurrent stressors, the aim of this study was to investigate the effect of a sequential set of stressors alone and in combination. This was achieved by measuring feed intake and growth performance in pigs in response to sequential changes in housing arrangement from individual to group housing and return to individual penning, with high-ambient-temperature and space-per-pig treatments superimposed on the design. As a result, a dynamic 2 x 2 x 2 factorial design was developed to allow for the examination of a fresh hypothesis on a week-to-week basis, with the overall hypothesis being that these treatments have a detrimental effect on pig performance and that the effects would be reversible. It is envisioned that the results from this study will add to an increased understanding of the effects of stressors on pig performance and will be of value in designing strategies to optimize animal performance.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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illustrates the layout for the pig housing facility. Ninety-six intact male (predominately Large White x Landrace, with some Duroc and Hampshire) pigs weighing 34.5 ± 3.5 kg were sourced from a commercial herd (Westmill, Young, New South Wales, Australia) that had previously irradicated Mycoplasma pneumoniae. The pigs originated from a group of 40 sows farrowed in conventional farrowing crates over a 1-wk period. They had been weaned at 4 wk of age and separated according to sex and transferred to a straw-based shelter and held in groups, and the pigs used in this study were selected according to live weight before leaving the straw-based shelter. All pigs had the same handling, management, and housing experience before commencing the study. The pigs had minimal handling and human contact and had never been housed in individual pens before the study. Once the pigs arrived in the experimental facilities, they were individually housed at 22°C in two adjacent air spaces, with two rooms per air space. One air space (Rooms 1 and 2) was used to increase temperature from 22 to 30°C. The second air space (Rooms 3 and 4) was maintained at 22°C throughout the experiment. Each room initially contained pigs individually housed in 24 pens that allowed the pigs to see, hear, and touch each other through the bars. For each room, the floor area was 2 m2/pig (low density) in 12 pens or 1 m2/pig (high density) in the remaining 12 pens. Lower densities equivalent to commercial conditions were not used to allow the pigs enough space to turn around because the pigs had to spend time in individual pens until approximately 100 kg BW to allow the pigs enough space to move. Also for each room, there were two groups of six pigs at low density and two groups of six pigs at high density. Floor type (concrete slats), feeder space (one per pig), and drinker number (one between each pen; i.e., one half per pig) were similar in each room. Each room was maintained initially at 22°C. Throughout the study, humidity was maintained at 10 g of water/kg of air, air movement at 0.15 m/s, ammonia concentration at <5 ppm (measured at the front of each room each morning), and light on a 12-h light/12-h dark pattern (0600 to 1800). Pigs had ad libitum access to a pelleted, commercial diet (Vella Stockfeeds, Plumpton, Australia) based on wheat and sorghum that was supplemented with meat meal, solvent-extracted canola meal, and solvent-extracted cottonseed meal. Free lysine hydrochloride, DL-methionine, and L-threonine were added to maintain the balance of AA relative to lysine (Baker and Chung, 1992). The diet was calculated to contain (per kilogram) 11.2 g of total lysine and 201.7 g of CP, containing 10 g of available lysine/kg and 13.5 MJ of DE/kg (as-fed basis). The New South Wales Agriculture Animal Ethics Committee approved the experimental protocols.
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) to a dynamic 2 x 2 x 2 factorial design. The experimental design included two stocking densities (six pigs as 1 or 2 m2/pig), two temperatures (22 or 30°C), and two short (from 7 to 21 d) groupings of unfamiliar cohorts (one pig per pen or six pigs per pen). The study was conducted over 8 wk, and weekly measures of live weight gain (WTG) and feed intake (FI) were taken for each pig. During the first week, pigs were housed in individual pens. To group pigs, pen partitions were removed in Rooms 2 and 3 from wk 2 to wk 4, and in Rooms 1 and 4 during wk 7. Pen partitions were replaced in Rooms 2 and 3 at the end of wk 4 and in Rooms 1 and 4 at the end of wk 7 to return pigs to their individual pens. Temperature was increased from 22 to 30°C in Rooms 1 and 2 during wk 4 and 7 and back to 22°C every other week. Each temperature change occurred over 20 min. As noted previously, humidity was maintained at 10 g of water/kg of air using a steam-generated humidifier in each room. Temperature was maintained in each room with a positive-ventilation, ducted air-conditioning system. There was a separate air-conditioning system that supplied cooling to the two air spaces with two rooms per air space. Cooling was provided with a conventional refrigerated gas system and fan-coil unit. Heating was supplied from electrically powered, heat-banks within the duct system to each room. The variation in temperature in each room was ± 1°C. The experimental protocol is outlined in Table 1.
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Data Analyses
The GLM procedure of SAS (SAS Inst., Inc., Cary, NC) was used to assess the sources of variance and to estimate least squares means for WTG and FI. The statistical analyses used were appropriate for the design and sequence of treatment changes. Because there were specific fresh hypotheses under test from week to week, and to fit a model that yielded a complete set of estimable functions while remaining parsimonious (i.e., maximizing error degrees of freedom), data analyses were performed in two stages that accommodated the dynamics of the experimental design (Table 1
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From wk 1 to 5, the following model was used:
 | [1] |
where yijkmp represents the measure of WTG or FI on the pth pig (p = 1 to 96), in the ith stocking density (i = 1 to 2, for 1 or 2 m2/pig), taken at the end of the jth week (j = 1 to 5), from the kth grouping treatment at the second week (k = 1 for one pig per pen in Rooms 1 and 4, and k = 2 for six pigs per pen in Rooms 2 and 3), subjected to the mth temperature treatment at the fourth week (m = 1 for 22°C for pigs in Rooms 3 and 4, and m = 2 for 30°C for pigs in Rooms 1 and 2); µ represents the overall mean; (wg)jk represents the interaction effect of the jth week with the kth grouping treatment; (wt)jm represents the interaction effect of the jth week with the mth temperature treatment; ap[(dgt)ikm] represents the main effect of the pth pig nested within the three-way interaction effect of density, grouping, and temperature; and eijkmp represents the random error associated with yijkmp.
From wk 6 to 8, the following model was used:
 | [2] |
Elements in Model [2] are defined as in Model [1] except that subscript k indicates the kth grouping treatment at the seventh week (i.e., k = 1 for one pig per pen in Rooms 2 and 3, and k = 2 for six pigs per pen in Rooms 1 and 4), and subscript m indicates the mth temperature treatment also at the seventh week (m = 1 for 22°C for pigs in Rooms 3 and 4, and m = 2 for 30°C for pigs in Rooms 1 and 2).
Finally, and to assess the (possible) three-way interaction effect between stocking density, grouping and temperature treatments that was applied in wk 4 and 7, the following model was fitted to the data from both weeks:
 | [3] |
where rk indicates the main effect of the kth room (k = 1 to 4) and remaining elements are defined as before. Note that for Models [1] and [2], the effect of room was obviated because of its confounding with the three-way interaction of density, grouping, and temperature in which pig was nested. Also, for all analyses, the statistical significance of the main effects of grouping, temperature, and week was assessed by estimating the appropriate orthogonal contrast from the interaction where each effect intervened.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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presents least squares means for the main effects of group (individual vs. six pigs per pen) and temperature (22 vs. 30°C) treatments on WTG and FI.
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). However by the end of wk 6, when all pigs had been individually housed for 1 wk and at 22°C for 2 wk, pigs had a similar WTG, and there were no significant effects detected for WTG (or FI) from the previous high-temperature treatments. In the second grouping that occurred at wk 7, decreased (P < 0.001) FI and WTG were observed in pigs housed in groups (14.24 ± 0.41 and 2.99 ± 0.27 kg, respectively) compared with individually housed pigs (17.42 ± 0.46 and 6.70 ± 0.27 kg, respectively). By the end of wk 8, when all pigs had been in individual pens and at 22°C for 1 wk, WTG was increased (P = 0.003) in pigs that had been grouped previously (8.82 ± 0.27 kg) compared with the individually housed pigs (7.69 ± 0.27 kg). These results indicate that the effect of short groupings (from 7 to 21 d) of unfamiliar cohorts was reversible. During the grouping of unfamiliar cohorts, the pigs tended to fight in the first 24 h. There were no clinical signs of disease or injuries noticeable.
The Effect of Increasing Temperature from 22 to 30°C
The first heat treatment (wk 4) resulted in a decrease (P < 0.001) in mean WTG of the pigs housed at 30°C (5.49 ± 0.25 kg) compared with pigs maintained at 22°C (7.71 ± 0.25 kg). However, by the end of wk 5, during which temperature returned to 22°C, this trend was reversed for both FI and WTG (i.e., higher values, P = 0.043, for individuals that suffered the heat stress in the previous week) indicating the effect of overcompensation. By the end of wk 6, after 2 wk at 22°C, no differences (P > 0.10) were detected for either trait. Again, these results indicate that the effect of temperature was reversible.
The second increase in ambient temperature (wk 7) decreased (P < 0.001) mean WTG (5.47 ± 0.27 kg at 22°C compared with 4.22 ± 0.27 kg at 30°C). Also at wk 7, mean FI was decreased (P < 0.001) when pigs were housed at 30°C (14.74 ± 0.42) compared with those maintained at 22°C (16.92 ± 0.45 kg). There were no significant effects on either WTG or FI detected 1 wk after the temperature had returned to 22°C (i.e., wk 8).
The behavioral observations during the high ambient temperature were as follows: the reaction to the increase in temperature from 22 to 30°C was to pant, lie down, spread out, and decrease feed intake. This effect was more noticeable in pigs previously housed in individual pens and then mixed in groups. There were no noticeable clinical signs of disease.
The Combined Effect of the Increase in Temperature and Short Groupings of Unfamiliar Cohorts
During wk 4, grouping arrangements were maintained from wk 3, but ambient temperature was elevated to 30°C in Rooms 1 and 2. The overall mean WTG was lower (P < 0.001) for individually housed pigs (6.25 ± 0.31 kg) than for grouped animals (6.95 ± 0.18 kg). This result was due to the effect of the heat on individually housed pigs. In grouped pigs, WTG decreased (P < 0.001) from 7.49 ± 0.24 kg at 22°C to 6.41 ± 0.24 kg at 30°C. Also, at wk 4, there was a significant temperature x grouping interaction (P < 0.05), by which the effect of heat stress was more notable in individually housed than in grouped pigs. By the end of wk 5, when all the pigs had been individually housed at 22°C for 1 wk, there was no significant effect of the previous grouping or stocking density on FI; however the mean WTG of the previously grouped plus heat-treated animals was increased (7.25 ± 0.25 kg) compared with the individually housed, heat-treated pigs (8.40 ± 0.25 kg; P = 0.002). In addition, pigs that had been grouped and heat-treated had a higher FI (17.97 ± 0.69 kg) than pigs previously maintained in groups at 22°C (15.91 ± 0.72 kg; P = 0.043). Again, these results indicate that pigs had undergone compensatory gain.
By the end of wk 7, the increase in ambient temperature to 30°C for 1 wk decreased (P < 0.001) WTG in the grouped heat-treated pigs (3.00 ± 0.26 kg) compared with heat-treated pigs that remained in individually housed (6.70 ± 0.26 kg). During the grouping of unfamiliar cohorts, the pigs tended to fight in the first 24 h. However, there seemed to be less fighting among the unfamiliar cohorts that had been exposed to heat. There were no clinical signs of disease or injuries evident.
The Effect of Stocking Density
There were only two effects detected for the stocking density treatment (Table 3). At the end of wk 5, when all the pigs had been individually housed at 22°C for 1 wk, pigs maintained at low density had a higher WTG (8.23 ± 0.27 kg) than their high-density counterparts (7.42 ± 0.22 kg; P < 0.02). Within the high-density treatment, pigs maintained at 30°C consumed less (P < 0.01) feed (14.37 ± 0.40 kg) than pigs housed at 22°C (16.26 ± 0.45 kg). Also at the end of wk 5, there was a significant (P < 0.001) stocking density x temperature interaction on FI (P < 0.001; i.e., stocking density had no effect, except when in combination with the heat treatment). Also, 1 wk after the second grouping and increase in temperature treatments (wk 8), pigs held at the 1 m2 had a higher WTG (8.83 ± 0.26 kg) than pigs maintained at 2 m2 (7.69 ± 0.26 kg; P < 0.001).
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Discussion |
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. Bornett et al. (2000a) found that sequential changes of the single factor of housing arrangement from individual to group and back to individual housing in 3-wk phases starting from 22.5 kg had reversible effects on feeding patterns and social behavior. The ability of pigs to undergo compensatory growth following dietary restrictions has been well described (e.g., Fabian et al., 2002) but not in response to a stress challenge associated with decreased feed intake. Results of the current study indicate that growing pigs are able to adapt to the application of a stressor, applied either alone or in combination, by decreasing food intake and hence growth. When the stressor or stressors are removed, compensatory food intake occurs to restore growth to a level equivalent to the unchallenged cohorts.
The current study attempted to investigate the effects of stocking density in a changing housing arrangement format; however, the lower limit of density was restricted to 1 m2/pig in the design of this study to prevent restricting the movement of mature individually housed pigs, as this would have confounded the study with an additional stress (restraint). Our results show that the effect stocking density, although it did not seem to alter the effect of either the grouping or the high-temperature treatments, altered the ability of the pigs to recover from a stress episode such as high temperature. For instance, the pigs housed individually at low density following the application of 30°C during wk 4 had a greater WTG (10.09 kg) in the subsequent week than the pigs maintained at high-density (7.49 kg). This implies that increased space per pig affected the pig’s ability to gain in a compensatory manner because of the effect on feed intake and perhaps on the efficiency of feed utilization. Smith et al. (2004) showed that increasing space allowance (from 0.23 m2 per pig to 0.35 m2 per pig) was associated with increased BW. Conversely, restricted space allowance postweaning reduces early growth rate, but had no effect on final BW (Wolter et al., 2003). Whether the basis of this effect is due to social factors such as group cohesion (Bornett et al., 2000b) or to physiological changes induced by the stress of living in a group (Chapple, 1993) remains to be determined.
Results of the current study indicate that there was no equal additive effect of short groupings of unfamiliar cohorts and heat stress on pig WTG. For instance, during the second application of 30°C in wk 7, grouping with or without heat stress had a more profound effect on pig performance than heat stress alone. Kerr et al. (2003) found that the treatment effects of Actinobacillus pleuropneumoniae challenge and changes in ambient air temperature (15 and 30°C) were not equally additive because the effects of the disease treatment were more profound than the effects of temperature on growth performance. Hyun et al. (1998a) speculated that exposure of pigs to multiple concurrent stressors will result in an additive decrease in growth performance as the demand for nutrients and energy for essential physiological processes increases in an incremental manner. The different conclusions made from the two studies may reflect dissimilarity in the severity of the imposed stressors. Hyun et al. (1998a) applied equally mild concurrent stressors, such as changes in feeder types, decreased space allowance, and grouping, whereas the grouping of unfamiliar cohorts treatment in the current study may have had a more significant effect on WTG than the high-temperature treatments. However, the current study showed a proportionally additive effect on feed intake. For instance, in the present study, even though grouping with or without heat decreased feed intake, the feed intake by pigs exposed to grouping plus heat (12.95 kg) was less than that of the grouped pigs (15.5 kg) maintained at 22°C. The interactions between stress factors on growth performance require further investigation. This may occur through the application of social stressor equations into pig growth simulation models (Wellock et al., 2003).
We speculate that when older, heavy pigs were grouped-housed at 22°C, feed intake increased to compensate for energy expended when the unfamiliar cohorts were grouped. This speculation about adapted feeding behavior in response to grouping is partially supported by some previous studies. For example, group-housed pigs have been shown to eat less frequently but to consume larger meals at a faster rate than individually housed animals (de Haer and de Vries, 1993). In addition, Bornett et al. (2000a) found that when pigs were moved from individual to group housing, feeding frequency decreased and meal duration increased to consume more food per meal. However, results of other studies (Nielsen et al., 1996; Mikesell and Kephart, 1999) indicated that mixing pigs did not increase feeding frequency and that grouped pigs are not very flexible in their feeding patterns. These differing results may be due to other affects such as the type of housing system. For example, another study that compared deep-litter, large group, and conventional systems showed feeding behavior were influenced by access to the feed trough as a function of social interactions around the feeder (Morrison et al., 2003).
This study consisted of two groupings of unfamiliar cohort phases, both of which decreased pig growth performance. The finding that grouping decreases growth performance is in agreement with the results of many other studies (reviewed by Turner et al., 2003; de Haer and de Vries, 1993; Nielsen et al., 1996; Gomez et al., 2000; Hyun and Ellis, 2001); however, this effect can be age-related. For example, very young weanling pigs perform equally well when housed individually or in groups (Bustamante et al., 1996). However, a comparison of the two grouping of unfamiliar cohorts phases indicates that the effect of grouping on growth was greater in the second phase when the pigs were heavier. Thus, live weight may be a factor when determining the effect of grouping on pig performance. This observation is supported by other studies (Heetkamp et al., 1995; Hyun et al., 1998b), where optimal experimental conditions allowed young pigs (20 to 35 kg BW) to be grouped with limited effects on growth; however, Stookey and Gonyou (1994) used heavy pigs (84 kg BW) with BW similar to the ones in the present study and found that grouping unfamiliar animals decreased WTG. The difference in WTG probably is associated with the negative social interactions associated with puberty in heavier pigs. The degree of competition at feeding has been shown to be related to pig size (Georgsson and Svendsen, 2002). Scroggs et al. (2002) found that finisher pigs were the most active (eating, standing, walking, and fighting) in the first 72 h when first mixed (Scroggs et al., 2002). Similarly, Gomez et al. (2000) reported decreased feed intake in older pigs when grouped as they avoided simultaneous eating with peers. Hence, grouping unfamiliar young pigs has less of a negative effect than grouping unfamiliar older pigs.
The second phase grouping of unfamiliar cohorts resulted in a similar decrease in weight gain for both the groupings (i.e., at 30°C or not). Nonetheless, as mentioned earlier, the grouped plus temperature-challenged pigs had lower feed intake compared with the pigs grouped at 22°C. Heat stress has been well documented to decrease feed intake (e.g., Kerr et al., 2003). Pigs grouped at 22°C were less feed efficient than the heat-challenged animals. Group-housed pigs tend to be more active than isolated individuals (Chapple, 1993). Thus, dietary energy was partitioned away from tissue deposition and towards the metabolic process associated with negative social interactions when the pigs were grouped, whereas the pigs housed in groups plus 30°C in the current study were observed to fight less than pigs mixed in groups at 22°C. This observation is supported by the results of another study (Hicks et al., 1998), which reported less aggressive behavior in pigs exposed to hot conditions.
It is apparent from the results of this study that a pig’s response to individual stressors depends on their housing arrangement before application of the stressor. During wk 3 of the study, pigs that had been individually housed had a higher feed intake (15.10 kg) before the imposition of the heat stress during wk 4 compared with the previously group-housed pigs (13.99 kg). However, weight gain at the end of wk 4 in response to the heat stress was lower for the individually housed pigs (6.25 kg) compared with the grouped animals (6.95 kg). Thus, pigs housed previously in individual pens were more affected by high temperature than the animals housed previously in groups. This finding indicates that the effect of individual housing decreases the pigs’ ability to cope with subsequent high ambient temperatures. Another study (Le Bellego et al., 2002) found that low-heat-increment diets (low dietary protein content associated with adequate crystalline AA supplementation) limited the negative effect of a high ambient temperature (29°C) on the growth performance of grower-finisher pigs. Therefore, the response noted in the current study is most likely a function of the pig’s increased feed intake (and hence increased heat production) when housed individually at 22°C that predisposes the animals to increased heat stress following application of 30°C.
It is possible that the effects of the stress factors, especially grouping in this study may have been different if the pigs had been assigned to treatments based on social status. It has been shown that social status is important when studying the effects of stress on pig physiology, and pigs respond to different stressors with different behaviors (Hicks et al., 1998). In the current study, the pigs were not assigned to treatment groups based on social status. Instead, they were allocated based on starting weight and vocalization score. The latter was an attempt to assign temperament equally across treatments; however, even though BW can be related to social status in pigs (Hicks et al., 1998), at this stage, it is unknown whether an association exists between vocalization score and social status. In addition, the results may have differed if the minimal treatment duration had been greater then 1 wk. It was decided that 1 wk was the minimum amount of time required to demonstrate a significant decrease in feed intake and growth rate; this is because the experiment was limited by time factors due to rate of growth, as the pigs would have grown too large for individual pens.
The main conclusions of this study were that housing pigs in groups at 30°C had a negative effect on pig performance. The grouping of unfamiliar heavy intact males was particularly detrimental and should be avoided. Although this study shows that these negative effects on performance are reversible for these two treatments, we did not evaluate the cumulative effect on animal welfare. Maintaining pigs in individual pens or groups, with or without high temperature, had different effects on pig performance that seemed related to the previous treatment. This finding implies that the effect of predictable unavoidable stressors can be managed to lessen the effect. In addition, the stocking densities applied in this study did not seem to alter the effect of either the grouping or the high-temperature treatments; however, it altered the ability of the pigs to recover from a stress episode such as high temperature. Results of this study indicate that the physiological and behavioral interactions of stress factors require further investigation.
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Footnotes |
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3 Current address: School of Sciences, Food, and Horticulture, Hawkesbury Campus, Bldg. K12, Univ. of Western Sydney, Locked Bag 1797, South Penrith Distribution Centre NSW 1797, Australia.
2 Correspondence: 306 Carmody Rd. (phone: +61 7 3214 2326; fax: +61 7 3214 2288; e-mail: Caroline.Kerr{at}csiro.au).
Received for publication July 1, 2004. Accepted for publication January 6, 2005.
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