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A prolonged photoperiod improves feed intake and energy metabolism of weanling pigs

E. M. A. M. Bruininx^,2, M. J. W. Heetkamp^*, D. van den Bogaart^*, C. M. C. van der Peet-Schwering, A. C. Beynen, H. Everts, L. A. den Hartog and J. W. Schrama^*

Research Institute for Animal Husbandry, 8203 AD Lelystad, The Netherlands; and ^* Wageningen University, Department of Animal Science, 6700 AH Wageningen, The Netherlands; and Nutreco Agriculture R&D,5830 AE Boxmeer, The Netherlands; and and Utrecht University, Faculty of Veterinary Medicine, Department of Nutrition, 3508 TD Utrecht, The Netherlands

² Correspondence:
P.O. Box 2176 (phone: 0031 320293211; fax: 0031 320241548; E-mail:
e.m.a.m.bruininx{at}pv.agro.nl).

	Abstract

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In a 2-wk experiment, the effect of photoperiod on performance and energy metabolism of newly weaned pigs was studied. Forty 4-wk-old crossbred weanling barrows weighing 8.0 kg (SE = 0.13) were assigned to one of eight groups (five pigs per group) based on BW and litter. Groups were allotted to one of two lighting schedules: 8 h light:16 h darkness or 23 h light:1 h darkness. Each group was housed in a climate respiration chamber. Piglets had ad libitum access to feed and water. Energy and nitrogen balances, heat production, ADFI, and ADG were measured weekly. Heat production, energy metabolism, and performance were unaffected (P > 0.10) by photoperiod during wk 1. However, in the 2nd wk ADFI (418 vs 302 g/d) and ADG (381 vs 240 g/d) were higher (P < 0.05 and P = 0.05, respectively) for pigs on the 23:1 h lighting schedule than for those on the 8:16 h schedule. Furthermore, heat production (P < 0.10), total energy retention, and energy retained as protein and as fat were higher (P < 0.05) during wk 2 in pigs on the 23:1 h lighting schedule (8, 125, 41, and 350%, respectively) than in those on the 8:16 h schedule. Moreover, metabolizability of energy tended to be higher (P < 0.10) and energy requirements for maintenance were lower (P < 0.05) during wk 2 for pigs on the 23:1 h schedule compared with those on the 8:16 h schedule (P < 0.10). In conclusion, exposing pigs to a longer period of light after weaning stimulated ADFI and ADG. In addition to the feed intake, the high ADG is due to an improved metabolizability of energy and a reduced energy requirement for maintenance. This study suggests that lighting schedule can be used as a tool to stimulate feed intake after weaning.

Key Words: Feed Intake • Heat Production • Lighting • Pigs • Weaning

	Introduction

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Feed intake is an important determinant of performance and may also reflect the health status of weanling pigs (Makkink, 1993; McCracken et al., 1995). After weaning, piglets are exposed to a period of underfeeding (Le Dividich and Herpin, 1994). This period is associated with villous atrophy in the small intestine of piglets (McCracken, et al., 1995; Pluske et al., 1996). Villous atrophy is considered a predisposing factor for postweaning health problems (e.g., diarrhea and mortality). Apart from the reduced feed intake, the 1st wk after weaning is also characterized by increased energy requirements for maintenance (Gentry et al., 1997; Moon et al., 1997; Sijben et al., 1998), being associated with weaning stress. Both the reduced energy intake immediately after weaning and this reallocation of nutrients toward maintenance processes may conflict with the allocation required to maintain good health and performance (Schrama et al., 1997).

Recently it was demonstrated that the majority of weanling pigs did not start eating during the dark periods of the day (Bruininx et al., 2001a). Based on this observation we hypothesized that a prolonged photoperiod within the nursery room may stimulate an early start and development of feed intake in pigs during the first days after weaning. A minimal period without feed intake postweaning is considered essential to maintain the structure and function of the small intestine (Pluske et al., 1996). Therefore, this experiment assessed the effects of lighting schedule on feed intake and energy metabolism after weaning as a reflection of the pigs’ health.

	Materials and Methods

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Animals.

Forty (eight groups of five pigs) crossbred weanling barrows, weighing an average of 8.0 ± 0.13 kg, were used during four successive trials. During nursing all pigs had free access to water, but creep feed was not provided. In the farrowing room, artificial lights were on from 0800 to 1600. Farrowing rooms had one window that allowed natural lighting. The experiment was conducted during the winter and therefore the farrowing rooms were completely dark when lights were off. Immediately after weaning (at 1200), barrows were transported to the metabolism laboratory (approximately 30 km). The experiment was approved by the Animal Experiments Committee of Wageningen University, The Netherlands.

Experimental Design.

In each trial, five pairs of two barrows were selected from five litters at weaning. Littermates were randomly allotted to one of two lighting schedules: 8 h light:16 h darkness (8L:16D) or 23 h light:1 h darkness (23L:1D). Pigs in the 8L:16D and 23L:1D group were exposed to light, respectively, from 0800 to 1600 and from 1700 to 1600. When lights were on and off, the light intensity was, respectively, 44 lx and < 1 lx. The experiment started exactly at 1600 (approximately 4 h after weaning). Consequently, both experimental groups started in complete darkness. The experimental period consisted of two consecutive metabolism periods of 5.7 d (from Thursday 1600 to Wednesday 0800; wk 1) and 7 d (from Wednesday 0800 to Wednesday 0800; wk 2). The beginning of a day was set at 0800. Therefore, d 1 was not complete. Energy and protein metabolism were measured by indirect calorimetry using two open-circuit climatic respiration chambers (Verstegen et al., 1987).

Housing and Feeding.

The respiration chambers measured 1.5 x 1.6 x 1.8 m (length x width x height). The temperature was kept within the thermoneutral zone (28°C on d 0 to 3; 27°C on d 3 to 6; 26°C on d 6 to 10; 25°C on d 10 to 13). Relative humidity was maintained at approximately 67.5% and air velocity was below 0.2 m/s. All pigs were allowed ad libitum access to water and to a commercial weaner diet (Cehave Landbuwbelang Voeders B.V., Veghel, The Netherlands) without antibiotics, organic acids, and pharmacological levels of copper and zinc (Table 1). In both respiration chambers feed was available from a dry feeder. In order to monitor the feed intake pattern per pen, each feeder was placed on a balance (Mettler, KA32S, Mettler Toledo B.V., Tiel, The Netherlands). The feeders and balances were surrounded by a wooden casing (0.36 x 0.46 x 1.13 m) that protected them from being disturbed by other pigs. Pigs could access the feed through a hole (0.14 x 0.36 m) in the casing, approximately 10 cm above the floor. The balances provided a continuous recording of the feeder weight. Additionally, during the first 48 h of the experiment pigs were filmed by time-lapse video recording (6 frames per second, Panasonic, Den Haag, The Netherlands). Infrared light facilitated filming during the dark periods. Each pig was individually identifiable by a black mark on the back.

Individual BW was measured at the start of the experimental period (d 1) and on the last day of both balance/metabolism periods (d 7 and 13). Each day at 0800 the feeder weight of both chambers was recorded. The feeder was designed to minimize feed spillage. Therefore, daily feed intake was calculated by subtracting subsequent feeder weights from the initial feeder weights. Observers who reviewed the videos collected behavioral data. The time at the beginning and end of each visit to the feeder (defined as the time the pig’s head was completely covered by the wooden casing) that lasted 3 s or more was recorded in a database. Based on elapsed time, this database on feeder visits was matched with the data on feeder weight. The resulting database was used to calculate the time (h) between the start of the experiment and the first visit to the feeder for each individual pig. Additionally, the time between the start of the experiment and the first visit to the feeder during which there was a change of at least 1 g in feeder weight (latency time; Bruininx et al., 2001a) was calculated for each individual pig.

Together with the collection of feed samples, feces with urine (manure) were collected quantitatively per group and sampled for energy and nitrogen analysis on d 7 and 13. Gross energy content of feed and manure were determined with adiabatic bomb calorimetry after freeze drying, and N contents were measured with the Kjeldahl method. Metabolizable energy intake per group was derived from the energy contents of feed, manure, and methane production. Total heat production for each group was determined every 9 min from the measurements of oxygen consumption, carbon dioxide, and methane gas production as described by Verstegen et al. (1987), using the method of Brouwer (1965). Heat production was measured throughout the experiment, excluding d 1 and d 7. Total energy retention was calculated by subtracting total heat production from metabolizable energy intake. The retention of N was calculated by subtracting N in feces plus urine, in aerial NH₃, and in NH₄⁺ of water that condensed on the heat exchanger from N intake. Energy retention as protein was calculated from the N retention, and the energy retention as fat was calculated by subtracting energy retention as protein from total energy retention, as described by Henken et al. (1991). The ME requirements for maintenance (ME_m) were calculated as follows:

[1]

where 0.54 and 0.74 were used as the efficiency of utilization of ME for protein and fat retention, respectively (ARC, 1981).

Statistics.

Apart from the time between the start of the experiment and first feed intake (latency time) all data were analyzed with group as the experimental unit. Preliminary analysis showed that for most parameters the variation was different between wk 1 and 2. Therefore, all performance and metabolism traits were statistically analyzed separately per week. Furthermore, the average values for wk 1 and 2 combined (total period) were analyzed for the effect of lighting schedule with the same model using the GLM procedures of SAS (SAS Inst. Inc., Cary, NC):

[2]

where Y_ijk = response of a specific trait in wk 1, wk 2, or the total period; µ = overall mean; trial_i = fixed effect of trial_i (i = 1,2,3,4); lighting schedule_j = fixed effect of lighting schedule j (j = 1, 2); and e_ijk = error term, which represents the random effect between groups.

To study the development of the average daily feed intake in time, the model was extended with fixed effects of day number and two-factor interactions between day number and lighting schedule. An additional random error term for differences between days within a group was added also. To study the within-day variation in feed intake and total heat production model 2 was extended with fixed effects of hour and two-factor interactions between hour and lighting schedule. An additional random error term for differences between hours within a group was added also. Again these analyses were performed separately for wk 1 and 2. In both analyses the main effect of lightning schedule was tested against the random effect between groups.

Preliminary analysis showed that the time to the first visit to the feeder and latency time did not follow a normal distribution. Therefore, survival-like, Kaplan-Meier curves were constructed for both variables as affected by lighting schedule as described by Bruininx et al. (2001a). Because 14 pigs did not eat and 1 pig did not visit the feeders within the 48 h in which feeding behavior was videotaped, both variables were censored (Kalbfleisch and Prentice, 1980).

	Results

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During Trial 1, on d 6 and d 8 one pig (littermates) was removed respectively, from, the 23L:1D and 8L:16D group because of health problems.

Performance.

Averaged over the total experimental period, ADFI of the 23L:1D pigs was 71 g/d higher than for the 8L:16D pigs (P < 0.05; Table 2). For the 23L:1D treatment, ADFI was higher during both wk 1 (15.7%) and wk 2 (38.4%) after weaning. However, this difference was only significant (P < 0.05) for wk 2.

View larger version (14K): [in this window] [in a new window]   Figure 1. Percentage of weanling pigs that had not visited the feeder for at least 3 s as a function of postweaning interval as affected by lighting schedule. Curves are given for pigs exposed to 23 h of light and 1 h of darkness (23L:1D, solid line) or 8 h of light and 16 h of darkness (8L:16D, dotted line).

View larger version (14K): [in this window] [in a new window]   Figure 2. Percentage of weanling pigs that had not eaten at least 1 g during one visit as a function of postweaning interval as affected by lighting schedule. Curves are given for pigs exposed to 23 h of light and 1 h of darkness (23L:1D, solid line) or 8 h of light and 16 h of darkness (8L:16D, dotted line).

View larger version (29K): [in this window] [in a new window]   Figure 3. Daily feed intake (panel a) and daily heat production (panel b) from d 2 to d 6 and from d 8 to d 13 of weanling pigs, exposed to 23 h of light and 1 h of darkness (23L:1D, ) or 8 h of light and 16 h of darkness (8L:16D, ).

Energy Intake and Metabolizability.

The differences in energy intake (GE and ME; Table 3) between both lighting schedules were similar to the differences in ADFI. Averaged over the total experimental period and during wk 1 the energy metabolizability (ME/GE) was unaffected (P > 0.10) by lighting schedule (Table 3). During wk 2, however, the metabolizability of energy for the 23L:1D pigs was 3.2% higher (P = 0.06) than for the 8L:16D pigs (Table 3).

Despite the 163 kJ•kg^-0.75•d^-1 (39.0 kcal•kg^-0.75•d^-1) higher ME intake by the 23L:1D group during the total experiment, total heat production for this group only tended to be higher (P = 0.07; Table 4). This difference developed totally during wk 2. As with ADFI, daily total heat production increased within wk 1 and 2 (P < 0.001; Figure 3b). However, an effect of lighting schedule on the time-related change in the total heat production was only significant during wk 2 (P < 0.001). From d 11 to 13 the total heat production of the 8L:16D pigs was lower than of the 23L:1D pigs, whereas from d 8 to 10 total heat production of the 8L:16D pigs was higher (Figure 3b).

Although not significant (P > 0.10), when averaged over the total experimental period, the ME_m of the 8L:16D pigs was 7.7% higher than for the 23L:1D pigs. This numerical difference was due to a tendency (P = 0.06) toward a higher ME_m for the 8L:16D pigs during wk 2 (Table 4).

Within-Day Variation in Feed Intake and Total Heat Production.

The average hourly pattern of feed intake averaged over days during wk 1 (Figure 4a) was not affected by lighting schedule (P > 0.10), whereas during wk 2 (Figure 4b) the hourly pattern differed between both lighting schedules (P < 0.05). In general, during the second week hourly feed intake of the 23L:1D pigs was continuously higher than that of the 8L:16D pigs.

View larger version (32K): [in this window] [in a new window]   Figure 4. Hourly means of feed intake during wk 1 (panel a; SEM = 1.43) and wk 2 (panel b; SEM = 2.10) of weanling pigs, exposed to 23 h of light and 1 h of darkness (23L:1D, ) or 8 h of light and 16 h of darkness (8L:16D, ).

View larger version (33K): [in this window] [in a new window]   Figure 5. Hourly means of total heat production during wk 1 (panel a; SEM = 2.7) and wk 2 (panel b; SEM = 3.0) of weanling pigs, exposed to 23 h of light and 1 h of darkness (23L:1D, ) or 8 h of light and 16 h of darkness (8L:16D, ).

	Discussion

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During wk 1, ADFI did not differ between lighting schedules. Although an indication of a higher feed intake was already present during the first week after weaning, the results of the present study show that a prolonged photoperiod (23 h of illumination vs 8 h of illumination within a day) enhances ADFI, especially during the second week after weaning. Moreover, a prolonged photoperiod resulted in an increase in ADG and gain to feed ratios. Again, these differences were most pronounced during wk 2.

In addition to the depression in feed intake, the first days after weaning can also be characterized by a reallocation of nutrients toward maintenance processes, which is indicative of impaired health (Schrama et al., 1997). In the present study a prolonged photoperiod resulted in an increase in heat production and energy retention for pigs during the first 14 d after weaning. However, as with feed intake, these differences were most pronounced during wk 2. Because some indications toward these differences already existed during wk 1, the observed effects of lighting schedule during wk 2 on energy parameters possibly result from carry-over effects during wk 1. This trend toward a lower feed intake of the 8L:16D pigs may have resulted in a decrease of the digestive and absorptive capacity due to an increasing degree in villous atrophy in the small intestine during wk 1 (McCracken et al., 1995; Pluske et al., 1996). Additionally, weaning anorexia is also associated with local inflammation in the small intestine (McCracken et al., 1999). This damage to the morphology and function of the small intestinal wall due to the hampered feed intake may explain the increase of energy losses in feces and urine (decrease of the metabolizability of GE) and the increase in the energy requirements for maintenance of the 8L:16D pigs during wk 2 after weaning. A direct effect of lighting schedule on performance and energy metabolism during wk 2 is, however, also possible. During wk 2 the base levels of feed intake and heat production within a day by the 23L:1D pigs were higher than that of 8L:16D pigs (Figures 4b and 5b). Additionally the deviations from these base levels in feed intake and heat production within a day were higher for the 8L:16D pigs than for the 23L:1D pigs. These findings suggest a more continuous feeding activity and therefore a more continuous supply of nutrients for the 23L:1D pigs, which is considered to be beneficial for an efficient digestion (Makkink, 1993). The absence of this effect on feed intake during wk 1 (Figure 4a) may be explained by the time pigs need to develop a circadian/diurnal rhythm, as suggested by Gentry et al. (1997). On the other hand, during wk 1 there already was a difference in heat production within a day (Figure 5b) between the two lighting schedules, suggesting the existence of a rhythm in heat production, and therefore activity, during wk 1. However, by excluding the first hour during which lights were on (from 0800 to 0859) for the 8L:16D pigs, differences in heat production within a day were no longer present during wk1 (P > 0.1).

Furthermore, during wk 2 the 23L:1D pigs spent less energy on maintenance processes than the 8L:16D pigs. This may be the result of less energy that is needed for the recovery of the gut wall (as discussed above). Theoretically, it may also have been caused by a decrease in physical activity of the 23L:1D pigs. The latter is not very likely, because Apeldoorn et al. (1998) showed that continuous lighting increases energy expenditure for physical activity in broiler chickens. As a consequence of the increase in feed intake and metabolizability of GE and the decrease in ME_m during wk 2, the retention of energy both as protein and fat is strongly affected by lighting schedule, being highest for the 23L:1D pigs. Although effects were not observed during wk 1 after weaning, the present study clearly shows that performance of weanling pigs is strongly enhanced by a prolonged photoperiod. These effects are the result of an increase in feed intake and metabolizability of energy and a decrease in the energy requirements for maintenance. Moreover, considering performance and energy metabolism as a reflection of health of the weanling pig, the present study provides clues for the use of lighting schedules within nursery rooms to optimize postweaning health.

	Implications

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This study showed that performance of weanling pigs is strongly affected by the lighting schedule that is used in the nursery room. A prolonged photoperiod (23 h vs 8 h within a 24-h period) resulted in an increase in feed intake and metabolizability of energy and a decrease in the energy requirements for maintenance. These effects were most pronounced during the 2nd wk after weaning. Consequently, energy retention as protein and fat of the pigs that were exposed to a prolonged photoperiod was higher. Considering performance and energy metabolism as a reflection of the health of the weanling pig, the present study provides clues for the use of lighting schedules within nursery rooms to optimize postweaning health. However, the mechanism by which performance and energy metabolism are mediated by lighting schedule is not clear.

	Footnotes

 
¹ The authors thank T. Zandstra, J. M. van der Linden, and P. Vos for their biotechnical assistance and W. Gerrits for critically reviewing the manuscript.

Received for publication October 18, 2001. Accepted for publication January 25, 2002.

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