Effect of high temperature and feeding level on energy utilization in

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predefined feeding level close to ad libitum (23AL pigs), one was ... seemed to be due to a greater utilization of feed energy ..... Metabolizable energy (ME).
Effect of high temperature and feeding level on energy utilization in piglets A. Collin, J. van Milgen, S. Dubois and J. Noblet J ANIM SCI 2001, 79:1849-1857.

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Effect of high temperature and feeding level on energy utilization in piglets1 A. Collin, J. van Milgen2, S. Dubois, and J. Noblet Unite´ Mixte de Recherches sur le Veau et le Porc, Institut National de la Recherche Agronomique, 35590 Saint-Gilles, France

ABSTRACT: The effect of temperature (23 or 33°C) and feeding level on components of energy balance was studied in seven groups of individually reared Pie´train × (Landrace × Large White) littermate piglets. Within each litter, one pig was reared at 23°C and given a predefined feeding level close to ad libitum (23AL pigs), one was reared at 33°C and also fed close to ad libitum (33AL), and one was reared at 23°C and pair-fed to the 33AL pig (23PF). Piglets of one litter were acclimated during 2 to 4 wk to their experimental temperature in temperature-controlled rooms before being transferred (one per week) to a respiration chamber for measurement of nitrogen and energy balances. The average initial BW was 22.4 kg. The data on O2 consumption, CO2 production, and physical activity were collected over seven consecutive days and used to calculate total heat production (HPtot) and its components: fasting heat production (FHP), heat production due to physical activity (HPact), and thermic effect of feed (TEF). A preliminary trial was conducted in which heat production was measured in three piglets according to a Latin square design at 23, 25, and 27°C. Total heat production was, but activity-free heat production was not, affected by tem-

perature, and no firm conclusions could be drawn as to whether 23°C was within the thermoneutral zone of fed piglets. In Trial 2, the combination of increased temperature and reduced feed intake resulted in a 20% lesser heat production in 33AL than in 23AL pigs. This was due to a reduction in both TEF (−39%) and FHP (0.642 vs 0.808 MJⴢd−1ⴢkg BW−0.60). Despite the shorter duration of standing activity, HPact was slightly higher at 33°C, probably due to hyperventilation at this temperature. With similar feeding levels (23PF vs 33AL), HPtot and activity-free heat production were less at 33°C and energy retention as protein (+6%) and fat (+31%) was increased. Because HPact was similar for both treatments, the greater energy retention for 33AL seemed to be due to a greater utilization of feed energy or to a reduced maintenance requirement (i.e., reduced FHP). However, the type of stress imposed on 23PF and 33AL pigs was different and may have affected energy metabolism. The results suggest that the reduction in heat production of piglets at high ambient temperatures is caused by a reduction in voluntary feed intake and differences in energetic efficiency. The mechanisms for the lesser efficiency at 23°C compared to 33°C (at the same level of feed intake) remain unclear.

Key Words: Energy Metabolism, Environmental Temperature, Feed Intake, Heat Production, Physical Activity, Piglets 2001 American Society of Animal Science. All rights reserved.

Introduction Under warm conditions, the maintenance of body temperature between narrow limits is achieved by increasing heat loss and(or) reducing heat production (HP). In fact, sensible heat loss decreases with the rise in temperature because the skin-ambient temperature gradient decreases (Curtis, 1983). The increase in

1 The authors thank J. Le Dividich for helpful discussions and suggestions and A. Roger, H. Renoult, J. Gauthier, F. Thomas, M. T. Gauthier, S. Hillion, and P. Bodinier for technical assistance. 2 Correspondence: phone: (33) (0) 223 48 56 44; fax: (33) (0) 223 48 50 80; E-mail: [email protected]. Received November 7, 2000. Accepted April 6, 2001.

J. Anim. Sci. 2001. 79:1849–1857

evaporative heat loss at high temperature is also limited because sudoriparous glands of pigs are not functional (Ingram, 1965). Consequently, homeothermy is maintained mostly by reduction of HP at high temperature in connection with reduced feed intake and physical activity (Nienaber and Hahn, 1982; Nienaber et al., 1987; Quiniou et al., 2001). A previous study conducted with piglets given ad libitum access to feed and housed in groups (Collin et al., 2001a) indicated a 22% reduction in HP when ambient temperature was increased from 23 to 33°C. This change was related both to a reduction in feed intake and the associated thermic effect of feed (TEF) and to a decreased fasting heat production (FHP). The HP associated with physical activity was similar at both temperatures. Apart from the effects of reduced feed intake, a direct effect of

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Table 1. Ingredients and chemical composition of the diet (as-fed basis) Item Ingredient, g/kg Corn Soybean meal Wheat Barley Fish meal Dicalcium phosphate Calcium carbonate Minerals and vitamins mixturea Salt LysineⴢHCl Fungicide

280.5 255.0 232.5 145.0 50.0 18.0 9.0 5.0 4.0 0.5 0.5

Dry matter, %

88.3

Composition in DM Ash, % Crude protein, % Crude fiber, % Ether extract, % Gross energy, MJ/kg

6.9 24.5 3.4 3.2 18.31

a The minerals and vitamins mixture provided per kilogram of diet: Fe, 101 mg; Cu, 20 mg; Mn, 40 mg; Zn, 102 mg; Co, 1.05 mg; I, 0.62 mg; Se, 0.30 mg; vitamin A, 10,000 IU; vitamin D3, 2,000 IU; tocopherol acetate, 20 mg; menadione, 2 mg; thiamine, 2 mg; riboflavin, 5 mg; niacin, 20 mg; D-Ca-pantothenate, 10 mg; pyridoxine, 5 mg; biotin, 0.2 mg; folic acid, 1 mg; vitamin B12, 0.03 mg, choline, 602 mg, and ascorbic acid, 40 mg using calcium carbonate as carrier.

high temperature on components of HP may also be involved. The aim of the present study was to determine whether the extent to which the reduction in HP and its components in young pigs exposed to high temperature was due to a direct effect of high temperature itself, independent of feed intake (Trial 2). A preliminary trial (Trial 1) was carried out to verify that 23°C was within the thermoneutral zone for pigs fed at a reduced feed intake level.

Materials and Methods Respiration Chamber Equipment In both the preliminary and the main trials (Trials 1 and 2, respectively), an open circuit respiration chamber (1.7 m3) was used. Temperature and relative humidity were maintained constant (70% relative humidity) during the trials and gas was extracted at a rate of 3.3 m3/h. In the chamber, the pig was kept in a metabolic cage, which was equipped with a metal slatted floor (1.10 × 0.71 m) and a screen mesh for separate collections of feces and urine plus water spillage. The size of the cage allowed the piglet to move freely. In the respiration chamber, the feed (Table 1) was dispensed automatically in six meals at 0900, 1200, 1500, 1800, 2100, and 0300, and a 12-h photoperiod was used (0800 to 2000). The feed trough was placed on a load cell. Physical activity was determined using force sensors (Type 9104A, Kistler Instrumente

AG, Winterthur, Switzerland), on which the metabolic cage was mounted. These sensors produced an electrical signal proportional to vertical forces exerted on the cage. In order to distinguish different types of physical activity, the distribution of signal intensity relative to the cumulative recorded signal was determined. Infrared cells were also used to determine standing or lying position of the pig. Gas (CO2 and O2) contents of incoming and outgoing air, ventilation rate, weight of the feed trough, and physical activity of the pig were continuously and simultaneously recorded over 10-s intervals. The HP was calculated from gas exchanges according to the formula of Brouwer (1965). The model of van Milgen et al. (1997) was used to partition total heat production (HPtot) into resting heat production (RHP), heat production due to physical activity (HPact), and the short-term thermic effect of feed (TEFst). In brief, the model relates observed changes in O2 and CO2 concentrations in the respiration chamber to both physical aspects of gas exchanges and the O2 consumption and CO2 production by animals in connection with pigs’ feeding patterns and physical activity. In Trial 2, the additional measurement of heat production in fasting animals allowed the separation of RHP into FHP and long-term thermic effect of feeding (TEFlt). Parameter estimates for the components of HPtot were obtained using ACSL/Optimize (Version 2.4, AEgis Technologies Group, Huntsville, AL) for both trials.

Trial 1 A preliminary study was performed to ensure that pigs reared at 23°C and restricted to the feeding level of those kept at 33°C were within the thermoneutral zone. It consisted of exposure of three 25-kg piglets at 23, 25, and 27°C according to a Latin square design. Pigs were placed individually in the respiration chamber. The animals were adapted for 1 d to the respiration chamber at 25°C, and thereafter at one of the three temperatures was maintained over three successive 2d periods. The feeding level was similar to that of pigs used in Trial 2 that were reared at 33°C and given nearly ad libitum access to feed (i.e., 0.14 kg/kg BW0.60); the composition of feed is described in Table 1. The 1st d at a given temperature was considered as an adaptation day and calculation of HP was based only on data from the 2nd d.

Trial 2 Experimental Design. After weaning at 28 d of age, (Large White × Landrace) × Pie´train castrated male pigs were reared in groups of 12 animals in a conventional nursery room and offered ad libitum access to a starter diet providing 21.3% crude protein, 14.0 g/ kg of lysine, and 13.6 MJ/kg of ME. Two weeks after weaning, four or five littermates were placed in two temperature-controlled rooms for acclimation. Tem-

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perature was initially set at 25°C and was progressively decreased or increased within 2 d to either 23 (two or three pigs) or 33°C (two pigs). During the first acclimation week, all pigs were allowed ad libitum access to the same experimental feed as in Trial 1 (Table 1). During the 2nd wk, one or two pigs exposed to 23°C (23AL) were fed at 95% of the estimated ad libitum intake (i.e., 0.18 kg of feed/kg BW0.60). The ad libitum intake at this temperature was determined in two previous experiments (Collin et al., 2001a,b). Two littermates were exposed to 33°C (33AL) and were also given close to ad libitum access to feed at this temperature (0.14 kg/kg BW0.60; Collin et al., 2001a,b). The remaining littermates (23PF) were exposed to 23°C and pair-fed to the 33AL group. The choice of the three littermates used in the study was based on BW and condition of the pigs. For these animals, BW and age at the beginning of the acclimation period were 14.0 ± 3.4 (SD) kg and 42 ± 1 d, respectively. Feed intakes equivalent to 95% of the assumed ad libitum intake ensured that no refusals were left in the feed trough and that the feed was consumed in a limited number of meals. The week after acclimation, the 33AL and 23PF pigs remained in the temperaturecontrolled rooms, whereas the 23AL pig was placed in a metabolic crate and transferred to the respiration chamber for a 7-d measurement. The following week, alternately, the 23PF or the 33AL pig was transferred to the respiration chamber. Measurements on the remaining pig were performed in the 3rd wk. Because only one respiration chamber was available, the transfer of piglets was planned so that the HP was measured in piglets of approximately equal BW for all treatments. A total of seven blocks of three littermates was used in the trial. Measurements of Nitrogen and Energy Balances. The experiment consisted of measuring gas exchanges (O2 and CO2) and collecting urine and feces over six consecutive days in the respiration chamber. Urine was collected daily, whereas feces and samples of outgoing air (for nitrogen analysis) were collected at the end of the 6th d. Feed was withheld from pigs on the 7th d in order to measure the FHP. The animals were weighed in the morning on d 1, 7, and 8. Feces from the first 6 d were weighed, freeze-dried, and sampled; urine plus water spillage was collected daily, pooled, and sampled for analysis at the end of the period. Urinary nitrogen was measured in fresh material, whereas energy content was obtained after freeze-drying approximately 50 mL in a polyethylene bag. Nitrogen and energy contents in feces were measured in freeze-dried material. Retained nitrogen was calculated as the difference between nitrogen intake and excreted nitrogen (fecal, urinary, and evaporated). The DE corresponded to the difference between gross energy intake and energy lost in feces. The ME content corresponded to the difference between DE and energy lost in urine (CH4 production was not measured). Retained energy (RE) was calculated as the difference

between ME intake and total HP. Energy retained as protein (REP, kJ) was calculated as N retention (g) × 6.25 × 23.8, and energy retained as lipid (REL) was calculated as the difference between RE and REP.

Statistics Data of Trial 1 were analyzed with the GLM procedure of SAS (SAS Inst. Inc., Cary, NC) with temperature (T: 23, 25, or 27°C), animal (A: 1, 2, or 3) and period (P: 1, 2, or 3) as main effects. Data of Trial 2 were also analyzed with the GLM procedure of SAS with treatment (Tr: 23AL, 23PF, or 33AL) and litter (L: 1, . . ., 7) as main effects. Results are reported as least squares means.

Results Trial 1 Results (Table 2) indicate that a decrease in total HP tended to occur (P < 0.10) with increasing temperature; the difference was significant between 23°C and 27°C (−7%). However, this difference was due to differences in levels of physical activity between temperatures (21 and 29% less at 25 and 27°C, respectively, than at 23°C), so activity-free HP (HP0) was similar at the three temperatures.

Trial 2 Of the 21 pigs used in the trial, data for only 19 pigs were used in the data analysis. Due to technical malfunction, data for one 23AL and one 33AL pig had to be discarded and standing activity was measured for only three groups of littermates. Performance. As intended in the experimental design, pigs of groups 23PF and 33AL consumed 25% less feed than their 23AL littermates (Table 3). Body weight gain was less (P < 0.01) in 23PF and 33AL pigs than in 23AL pigs; BW gain in 23PF pigs was numerically lower than that in 33AL pigs. The litter effect on BW and feed intake was due to differences in average BW of litters at the start of the trial. The feed:gain ratio was equal in 23AL and 23PF pigs and tended to be less (P < 0.10) in 33AL pigs. Digestibility and Nitrogen Balance. Digestibility coefficients of dry matter, nitrogen, and energy were less (P < 0.01) in 23AL pigs than in 23PF and 33AL pigs. The DE and ME values of feed were 1.8 and 1.3% less in 23AL pigs than in the two other groups (Table 4). The ME:DE ratio was not affected (P = 0.27) by temperature or feeding level and averaged 96.5%. Nitrogen retention tended to be less in 23PF than in 33AL pigs (P < 0.07), both of which were less (P < 0.05) than in the 23AL pigs (Table 3). Energy Balance. Heat production and energy balance data during the experimental period, expressed per kilogram of metabolic weight (BW0.60), are presented in

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Table 2. Effect of ambient temperature on heat production of weaned piglets (Trial 1) Temperature, °C Item

23

Number of animals Average body weight, kg Feed intake, kg/dc

3 24.5 0.951

Heat production, MJⴢd−1ⴢkg BW−0.60 Total As physical activity Free from physical activity

27

RSDa

Statistical analysisb

3 24.7 0.951

— 0.1 0.007

— A**, P** A**, P**

0.031 0.016 0.015

T† T* A*

25 3 24.7 0.953

1.374d 0.233d 1.141

1.309de 0.183e 1.125

1.273e 0.165e 1.108

a

Residual standard deviation. Analysis of variance with temperature (T), animal (A) and period (P) as main effects (Latin square design). Levels of significance: †P < 0.10; *P < 0.05; **P < 0.01. Data of the first day of exposure at each temperature were not included. c Pigs were fed 0.14 kg/kg of their assumed metabolic weight (BW0.60). d,e Within a row, means without a common superscript letter differ (P < 0.05). b

Table 4. The significant effect of litter on FHP, varying between 0.604 and 0.809 MJⴢd−1ⴢkg BW−0.60, was due to the low FHP for piglets of one litter. The 23PF piglets had 13% less HPtot than 23AL pigs, resulting from a reduction in TEF (−40%) and FHP. The increased HPact in the feed-restricted piglets attenuated the difference in HP. In addition, the TEF expressed as a fraction of ME was also less (P < 0.05) in 23PF (13%) than in 23 AL (17%). At an identical feeding level, HPtot was greater (P < 0.05) at 23°C than at 33°C. This difference was not

due to a change in TEF or HPact, which were similar in 23PF and 33AL pigs, but to a 15% reduction in FHP in 33AL pigs. Similarly to what was observed in 23PF pigs (13% of ME), the TEF in 33AL (14% of ME) was less (P < 0.05) than in 23AL (17% of ME) pigs. As a result of the cumulative effects of temperature and feeding level, heat production was 20% less in 33AL pigs than in 23AL pigs. The TEFlt, expressed per kilojoule of ME, represented about 30% of the total TEF for the three treatments and it was unchanged by temperature or feeding level, whereas TEFst declined (P

Table 3. Effect of temperature and feeding level on performance, digestibility coefficients, and nitrogen balance of weaned piglets (Trial 2) Treatmenta Item Number of animals Average body weight, kgd Feed intake, g DM/d Body weight gain, g/d Feed:gain ratio Digestibility coefficients, % Dry matter Nitrogen Energy Nitrogen balance, g/d Intake Excretion Feces Urine Evaporated Total Retention ME, % DE

23AL

23PF

33AL

RSDb

Statistical analysisc

6 25.6 1,117e 914e 1.39

7 24.6 837f 682f 1.40

6 24.8 837f 751f 1.27

— 2.0 38 91 0.12

— L* Tr**, L* Tr** Tr†

88.1f 86.4f 88.6f

89.4e 89.1e 90.1e

89.7e 90.3e 90.3e

1.0 1.4 1.0

Tr* Tr** Tr*

43.7e

32.7f

32.7f

1.5

Tr**, L*

6.0e 11.3e 0.3e 17.6e 26.1e

3.6f 10.0f 0.2f 13.7f 19.0f

3.1f 9.1f 0.3e 12.6g 20.1f

0.5 0.8 0.1 0.7 1.0

Tr**, L* Tr** Tr** Tr**, L* Tr**, L**

96.7

96.4

96.5

0.2

a 23AL: piglets reared at 23°C with nearly ad libitum access to feed (0.18 kg/kg BW0.60); 33AL: piglets reared at 33°C with nearly ad libitum access to feed (0.14 kg/kg BW0.60); 23PF: piglets reared at 23°C and pair-fed to the level of 33AL pigs (0.14 kg/kg BW0.60). b Residual standard deviation. c Analysis of variance with treatment (Tr) and litter origin (L) as main effects. Levels of significance: †P < 0.10, *P < 0.05, **P < 0.01. d Average body weight on 6 d of collection of urine and feces. e,f,g Within a row, means without a common superscript letter differ (P < 0.05).

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Table 4. Effect of temperature and feeding level on energy balance of weaned piglets (Trial 2) Treatmenta Item

23AL

Number of animals Average body weight, kgd

6 26.1

23PF 7 24.9

33AL 6 25.2

RSDb — 2.1

Statistical analysisc —

Energy balance, MJⴢd−1ⴢkg BW−0.60 Digestible energy (DE) Metabolizable energy (ME) Heat production (HP) As fasting heat production (FHP)e As physical activity (HPact) As thermic effect of feed (TEF) Total (HPtot) Resting heat production (RHP) Activity-free heat production (HP0) Retained energy (RE) As protein (REP) As fat (REF) Total RE

2.564f 2.524f

2.005g 1.949g

1.999g 1.948g

0.020 0.018

Tr**, L* Tr**, L*

0.808f 0.214 0.431f 1.454f 0.932f 1.240f

0.755f 0.258 0.259g 1.272g 0.842g 1.014g

0.642g 0.262 0.263g 1.167h 0.736h 0.905h

0.046 0.037 0.030 0.055 0.058 0.044

Tr**, L*

0.561f 0.509f 1.070f

0.414h 0.263h 0.677h

0.437g 0.344g 0.781g

0.012 0.064 0.061

Tr** Tr** Tr**

Respiratory quotient

1.06f

1.02g

1.04fg

0.02

Tr*

TEF, kJ/kJ ME intake As short-term As long-term Total

0.12f 0.05 0.17f

0.09g 0.04 0.13g

0.09g 0.05 0.14g

0.01 0.02 0.01

Tr**, L* — Tr**

0.2 0.2

Tr* Tr*

Energy values, MJ/kg DM Digestible energy (DE) Metabolizable energy (ME)

16.2f 15.7g

16.5g 15.9f

16.5g 15.9f

Tr** Tr** Tr**, L* Tr**, L*

a 23AL: piglets reared at 23°C with nearly ad libitum access to feed (0.18 kg/kg BW0.60); 33A: piglets reared at 33°C with nearly ad libitum access to feed (0.14 kg/kg BW0.60); 23PF: piglets reared at 23°C and pairfed to the level of 33AL pigs (0.14 kg/kg BW0.60). b Residual standard deviation. c Analysis of variance with treatment (Tr) and litter (L) as main effects. Levels of significance: *P < 0.05, **P < 0.01. d Average body weight between d 2 and 6 of heat production measurements (d 1 was not included). e Estimated from FHP on d 7. f,g,h Within a row, means without a common superscript letter differ (P < 0.05).

< 0.05) for the lower feeding levels. The respiratory quotient was lowest in 23PF, intermediate in 33AL, and highest in 23AL pigs. As indicated in Table 4, total RE and its components of energy retained as protein and lipid were affected (P < 0.05) by treatments. As anticipated, pigs on the low feeding levels (23PF and 33AL) retained less energy (−25% on average) than 23AL pigs. However, at a similar level of feeding, pigs kept at 23°C retained 13% less energy than those kept at 33°C. Retained energy as protein was 26% lower in 23PF than in 23AL pigs. In all groups, retained energy as protein was greater than retained energy as lipid. Reduction of feed intake resulted in a lower protein retention. The reduction in 23PF pigs was greater (P < 0.05) than that in 33AL pigs. Lipid retention was affected much more than protein retention by the decrease in feed intake and temperature. At the same feeding level, 23PF pigs gained less (P < 0.05) lipid than 33AL pigs. Physical Activity. Heat production associated with physical activity did not differ (P = 0.10) among treatments (Table 4). At a similar feeding level, pigs had similar HPact, but physical activity in 33AL pigs was

less (P < 0.05) intense (Figure 1), which agrees with the shorter duration of standing (Table 5). However, moderate intensity was more pronounced, probably due to hyperventilation. Consequently, duration of standing accounts for a smaller proportion of HPact at 33°C than at 23°C. At 23°C, duration of standing and HPact at the two feeding levels differed; the greater value in 23PF than in 23AL reflected the effect of energy restriction on behavior of pigs (Table 5).

Discussion Nitrogen Balance, Energy Balance, and Digestibility Coefficients The effect of high temperature and low feeding level on performance and nitrogen and energy balance was studied in young growing pigs. As expected, the 25% decrease in feeding level at 23°C (23PF vs 23AL) resulted in an equivalent decrease in BW gain. However, the reduction of total retained energy was greater (−37%). This discrepancy can be explained by a smaller relative change in protein deposition than in lipid de-

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duction of feeding level increased nitrogen and energy digestibility. The greater digestibility in heat-stressed piglets is mainly related to the lower feed intake. The feed intake data (Table 3), the formulated lysine content, and a presumed standardized ileal digestibility (0.88) allowed calculation of the digestible lysine supply (10.9 g/d for 23AL and 8.2 g/d for 23PF and 33AL). Given the protein deposition (Table 4) and assuming 7% lysine in deposited protein, lysine did not seem to be a limiting factor for protein deposition.

Total and Activity-Free Heat Production

Figure 1. Effect of temperature and feeding level on partitioning of physical activity for piglets maintained at 33°C and allowed nearly ad libitum access to feed (33AL, open bars), piglets maintained at 23°C and allowed nearly ad libitum access to feed (23AL, solid bars) or piglets pair-fed (23PF, shaded bars) to the level of 33AL pigs (Trial 2). The units are arbitrary and relate to the electrical signal of the force sensors. Within groups of three bars, means without a common superscript letter differ (P < 0.05). NS = no treatment effect (P ≥ 0.10). position when dietary energy is reduced (Table 4) and the direct dependency of BW gain on protein gain (Quiniou and Noblet, 1995). Similar phenomena had also been observed in heavier growing pigs (Quiniou et al., 2001). Digestibility coefficients for DM, N, and energy were reduced in 23AL compared to 33AL and 23PF pigs. This result agrees with that of Fuller and Boyne (1971), who reported an increase in feed intake and a decrease in nitrogen digestibility with decreasing temperature (from 23 to 5°C); however, there was no effect of temperature on digestibility when data were adjusted for equal feed intakes. Roth and Kirchgessner (1984) and Noblet et al. (1993b) also showed that re-

The present experiment indicated a marked reduction in total HP when young, growing pigs were exposed to 33°C and fed liberally. This agrees with studies of Stombaugh and Grifo (1977), Nienaber et al. (1987), and Quiniou et al. (2001) in growing-finishing pigs and Collin et al. (2001a) in piglets. However, at a similar feeding level, HP was less at 33°C than at 23°C, which is consistent with the slightly greater BW gain in 33AL than in 23PF pigs. Similarly, in Trial 1 with a smaller range of temperatures, HP was less at 27 than at 23°C for similar energy intakes. These results conflict with those of Gray and McCracken (1974, 1980) and Rinaldo and Le Dividich (1991), who reported similar values for HP at 22 and 29°C or at 25 and 31.5°C, respectively, in piglets given similar amounts of feed. The most striking result of Trial 2 is that, at similar feeding levels and BW, activity-free HP (HP0) was less at 33°C than at 23°C. Possible reasons for this difference are an additional heat production in 23PF pigs for thermoregulatory purposes and(or) a reduced metabolic efficiency. According to Close and Mount (1978), 23°C corresponds to the lower critical temperature (LCT) in 21- to 38-kg pigs fed at maintenance. In the present experiment, 23PF pigs received 2.6 times this maintenance requirement (460 kJ ME/kg BW0.75), suggesting that 23°C was above LCT for 23PF pigs (as well as for 23AL pigs). In Trial 1, total HP decreased with increasing temperature, mainly due to a change

Table 5. Effect of temperature and feeding level on the duration of standing or lying position in weaned piglets (three animals per treatment; Trial 2) Treatmenta Item

23AL

23PF

33AL

RSDb

Duration of standing, h/d Night Day Total

1.1e 2.6e 3.7e

1.5d 3.4d 4.9d

0.5f 1.7f 2.1f

0.1 0.2 0.1

HPact, MJ/d

1.525

1.770

1.832

0.292

a

Statistical analysisc Tr** Tr** Tr**, L*

23AL: piglets reared at 23°C with nearly ad libitum access to feed (0.18 kg/kg BW0.60); 33A: piglets reared at 33°C with nearly ad libitum access to feed (0.14 kg/kg BW0.60); 23PF: piglets reared at 23°C and pairfed to the level of 33AL pigs (0.14 kg/kg BW0.60). b Residual standard deviation. c Analysis of variance with treatment (Tr) and litter (L) as main effects. Levels of significance: *P < 0.05, **P < 0.01. Within a row, means without a common superscript letter differ (P < 0.05). d,e,f Within a row, means without a common superscript letter differ (P < 0.05).

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High temperature and energy balance

in physical activity. Although this may be interpreted to indicate that 23°C is below the thermoneutral zone, it may also bring into question the existence of a thermoneutral zone per se. Nevertheless, it cannot be excluded that 23PF pigs used energy for thermoregulatory processes. Alternatively, it can be hypothesized that 23PF pigs are metabolically less efficient than 33AL pigs. It is, at least theoretically, possible that 33AL animals reduce heat production by improving the efficiency of synthetic processes by, for example, reduction of protein turnover or improved coupling of ATP synthesis. However, the type of stress imposed on 23PF and 33AL pigs is also different. The quantity of feed offered to 33AL pigs was similar to the voluntary feed consumption at this temperature. The main stressor for these pigs was therefore temperature. Compared to their voluntary feed consumption, 23PF pigs were restricted by more than 20%. This resulted in somewhat restless animals (Table 5), which, perhaps through hormonal control, may have altered energy metabolism. If the latter hypothesis were proven to be true, the technique of pair-feeding to specifically address the effect of temperature on energy metabolism is questionable. The question arises whether the reduced metabolic efficiency for PF pigs is due to an increase of the fasting heat production (as an indicator for maintenance) or to the thermic effect of feed (TEF). In agreement with results of Collin et al. (2000a) in group-housed piglets given ad libitum access to feed, the TEF was similar in 23PF and 33AL and pigs less than in 23AL pigs, which suggested that heat exposure did not affect the thermic effect of feed. However, the TEF (more specifically, its long-term component) is calculated by difference between the resting heat production and the FHP. If the FHP had been overestimated (due to a thermoregulatory demand during fasting), the TEF would have been underestimated. Close and Mount (1975) obtained a LCT of 25°C in unfed pigs weighing 25 to 40 kg. Consequently, the FHP measured in 23PF pigs might include some thermoregulatory HP with a subsequent reduction of TEF due to heat stress. In summary, the energetic efficiency of fed pigs seems to be smaller at 23°C than at 33°C. It remains unclear whether this reduction is due to a lower maintenance requirement (through a reduction in FHP), an additional thermoregulatory energy demand at 23°C, or differences in stress affecting energy metabolism. The value of FHP at thermoneutrality in pigs previously allowed nearly ad libitum access to feed (0.808 MJⴢd−1ⴢkg BW−0.60) is close to values obtained in heavier pigs (Le Bellego et al., 2001), which indicates that 0.60 is an appropriate exponent for expressing the metabolic BW in growing pigs (van Milgen et al. 1998; Noblet et al., 1999). The tendency of a difference (P < 0.07) in FHP between 23AL and 23PF pigs supports the hypothesis that the decrease in FHP at high temperature may also be, in part, due to the reduced feeding level, which affects the visceral mass (Rinaldo and

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Le Dividich, 1991) and its associated HP (Koong et al., 1983; van Milgen et al. 1998).

Activity Heat Production The cost of physical activity (8.5% of ME intake), calculated in young growing pigs in the present study, is consistent with the 9.3% and the 6.7% obtained in group-housed piglets at 23°C (Collin et al., 2001a) and growing pigs at 22°C (Quiniou et al., 2001), respectively. However, these values are much lower than what is observed in pregnant sows (approximately 20% of ME intake; Ramonet et al., 2000), which is due to a difference in energy intake. These results agree with the conclusions of Noblet et al. (1993a), who reported that physical activity represents an important factor of variation of energy requirements in pig production. In Trial 2, HPact was numerically greater in 23PF than in 23AL pigs. Apparently, feed restriction can increase activity considerably because pigs are anticipating feed. This was confirmed by analysis of standing behavior, which indicated that 23PF pigs were standing longer than 23AL pigs. The observation that heat production due to activity was similar between 23PF and 33AL seems to contradict the results of Trial 1, in which HPact decreased with increasing temperature, and results of the measurements of standing position (Trial 2). However, Quiniou et al. (2001) reported that the effects of temperature on HPact are not linear. Compared to that at the thermoneutral zone, physical activity was greater at lower (shivering) and at higher temperatures (hyperventilation). This hypothesis agrees with the profiles of partitioning of physical activity in six (arbitrary) levels of activity at 33°C (Figure 1), which show reduced movements of high intensity (and high energy cost) but increased activity of medium intensity, probably in relation to respiratory hyperventilation. Our previous study with group-housed piglets (Collin et al., 2001a) indicated similar results. It can therefore be concluded that the benefit of hyperventilation for increased water evaporation outweighs the associated cost of heat production.

Effect of Temperature on Retained Energy Present results indicate that young, growing pigs retained more protein than lipid, as observed by Noblet and Le Dividich (1982) and Ga¨decken et al. (1985) in piglets. In pigs allowed ad libitum access to feed, protein and fat deposition were affected by temperature and(or) feeding level, and fat deposition was affected more than protein deposition. Indeed, lipid retention was reduced by 31% and protein retention by 23% when temperature increased from 23°C to 33°C in pigs allowed neaarly ad libitum access to feed. The decrease in carcass fatness observed in 33AL pigs is consistent with results of Campbell and Taverner (1988), Giles et al. (1988), and Rinaldo and Le Dividich (1991), who suggested that the decreased fatness at high ambient

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Collin et al.

temperature was related to the reduced availability of energy for fat deposition, compared to thermoneutral or cold temperatures. The reduction in protein deposition at high temperature in pigs given ad libitum access to feed has been reported previously by Fuller (1965) and Rinaldo and Le Dividich (1991). In the present study, at similar levels of feeding, energy retained as protein and fat at 33°C was greater than that retained at 23°C. This agrees with Noblet and Le Dividich (1982), who found higher protein and lipid depositions in early-weaned piglets reared at 32 to 26°C than in those housed at 24 to 18°C and pairfed. These results conflict with results of Rinaldo and Le Dividich (1991), who found no change in protein and lipid retention between 25 and 31.5°C with similar ME intakes. In addition, Close (1983) and Le Dividich et al. (1985) did not find any difference in carcass composition at thermoneutral or high temperatures for pair-fed pigs. Nevertheless, the greater lipid deposition in 33AL pigs than in 23PF pigs was consistent with their slightly greater respiratory quotient, suggesting an increased fatty acid synthesis in 33AL pigs. In the present study, protein deposition was higher in 33AL than in 23PF pigs, indicating that, at similar levels of feed intake, high temperature had no detrimental effect on N retention. Gray and McCracken (1974) also reported in a pair-feeding trial that protein deposition was similar at 22°C and 29°C in piglets. The higher protein deposition at high temperature seems to be unique to piglets; lactating sows reduce milk production (Messias de Braganc¸a et al., 1998) and heavier pigs reduce growth and nitrogen retention (Holmes, 1973; unpublished results from our laboratory) with increasing temperature at constant feed intake.

Implications The present study indicates that the reduction of heat production in heat-stressed piglets is caused by a decrease in the activity-free heat production. No firm conclusions could be drawn as to whether this reduction is due to a reduced maintenance requirement (or fasting heat production) or a more efficient utilization of feed energy, but effects of high temperature and low feeding level (which may cause stress) are both probably involved. Moreover, additional heat production at 23°C in restrictively-fed pigs cannot be excluded. The study also indicates that in piglets, unlike in growing pigs or lactating sows, the effect of high temperature on nitrogen retention is due to a reduced feed intake and that there is no direct detrimental effect of high temperature. Nutritional adjustments such as reducing the fiber or protein content of the feed or selection of animals with low fasting heat production or physical activity may be effective in limiting the negative effects of hot climatic conditions.

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