J. Anim Sci. 2006. 84:2072-2082. doi:10.2527/jas.2005-597
© 2006 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Photoperiod influences the immune status of multiparous pregnant sows and their piglets1
S. R. Niekamp,
M. A. Sutherland,
G. E. Dahl and
J. L. Salak-Johnson2
Department of Animal Sciences, University of Illinois, Urbana 61801
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Abstract
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Manipulation of photoperiod may provide a noninvasive, easily implemented, effective method to improve immune status and enhance the efficiency of production. The objective of this study was to evaluate the impact of manipulation of photoperiod on endocrine and immune responses of pregnant sows and their offspring. At d 83 of gestation, sows were moved to gestation stalls and kept on a photoperiod of 12 h of light:12 h of dark until d 90, when sows were assigned to a long day (LD; 16 h of light/d) or a short day (SD; 8 h of light/d) treatment. During farrowing and lactation, one-half of the sows remained on their initial photoperiod (LD:LD or SD:SD), whereas one-half were switched to the opposite treatment (LD:SD or SD:LD). Blood samples were collected from sows at d 0, 7, 14, and 21 posttreatment, 24-h postfarrowing, and the end of lactation (~d 21 postfarrowing). Piglets were bled at 7 and 21 d of age for immune measures. Relative to sows on LD, sows on SD had greater concanavalin A- (P = 0.003) and lipopolysaccharide- (P = 0.02) induced proliferative responses at d 7 but reduced responses at d 14. Compared with SD, sows on LD had a greater (P < 0.05) percentage of neutrophils and fewer (P < 0.05) lymphocytes at d 7, resulting in a greater (P = 0.05) neutrophil:lymphocyte ratio. Neutrophil phagocytosis was greater at d 21 in sows kept on LD. Cortisol concentrations tended to be greatest (P = 0.10) in sows on SD:SD at 24-h postfarrowing and throughout lactation. At 7 d of age, piglets on LD:SD had greater (P = 0.001) total white blood cells (WBC) and plasma cortisol (P = 0.001) relative to those on the other photoperiod treatments. Plasma immunoglobulin G was less (P = 0.001) in piglets from sows kept on SD:LD compared with the other photoperiod treatments. Piglets from sows kept on LD:LD tended to have lower total WBC (P = 0.08) at 21 d of age. Piglets from sows kept on SD:SD had greater concanavalin A- (P < 0.001) and lipopolysaccharide-induced (P 
0.10) proliferation responses and cortisol (P = 0.05). Phagocytosis was greater (P < 0.003) in piglets from sows that were kept on LD:LD. Cortisol (P = 0.02), WBC (P = 0.003), and immunoglobulin G (P = 0.001) were all influenced by gestational photoperiod treatment. These data indicate that photoperiod influences the immune status and endocrine response of piglets from dams that have been kept on a defined photoperiod. We conclude that photoperiod effects on piglets may be programmed in utero and can last throughout lactation.
Key Words: endocrine • immune • photoperiod • piglet • sow
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INTRODUCTION
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Manipulation of photoperiod has been shown to be a noninvasive and easily implemented method to enhance the efficiency of production and potentially change immune status of animals. In dairy cattle, 8 h of light (short day; SD) during the dry period increased milk yield in the succeeding lactation (Miller et al., 2000
). The immune system can be stimulated by a SD photoperiod, as evidenced by mitogen-induced proliferation in hamsters (Zhou et al., 2002) and neutrophil chemotaxis in cattle (Auchtung et al., 2004). However, in hamsters, there were no photoperiod effects on innate immune responses (Zhou et al., 2002). Also in hamsters, glucocorticoid concentrations and total number of leukocytes increased under 9 h of light compared with hamsters kept on 15 h of light (Bilbo et al., 2002). Despite these findings, few reports exist about the photoperiod effects on performance, immune, and endocrine responses in swine.
To date, studies conducted in swine have shown that long day photoperiod (LD; 16 h light/d) can influence productivity. Milking frequency and total milk solid content were greater in sows kept on LD, which also had heavier piglets and weaned more pigs per litter relative to sows on SD photoperiod (Mabry et al., 1983). Stevenson et al. (1983) also found that piglets from sows kept on LD had greater weaning BW compared with those kept on 1 h of light, whereas McGlone et al. (1988) found no effects of 1 h or 23 h of light on piglet BW. Thus, information regarding photoperiod effects on piglet performance is conflicting. Moreover, there is limited information regarding the impact of manipulation of photoperiod on immune status of sows during gestation and lactation and on their offspring. The objectives of this study were to determine the impact of manipulation of photoperiod on sow performance and health during late gestation and throughout the lactation period and the effect of these photoperiod treatments on immune status and performance of their piglets.
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MATERIALS AND METHODS
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Animals, Housing, and Experimental Design
The University of Illinois Institutional Animal Care and Use Committee approved all experimental procedures. Multiparous, white, crossbred sows (n = 24) from the University of Illinois Research Farm were used for these experiments. The experiment was conducted between February and September. Sows were similar in parity and BW. Before the study, sows had not experienced a defined photoperiod.
Eight sows were kept in standard gestation stalls within 2 environmentally controlled rooms (4 sows/room). Each stall was equipped with a feeding trough and nipple waterer. The gestation rooms were constructed of solid concrete floors with mechanical ventilation. Ventilation fans were fitted with light-baffling boxes to eliminate the effects of the natural outdoor photoperiod. Farrowing rooms were constructed similarly to the gestation rooms. Sows were kept in standard farrowing stalls with woven-wire floors. Room temperature was at 23 ± 2°C. Heat mats were used postfarrowing to provide supplemental heat to the neonatal pigs.
Pregnant and lactating sows were individually fed their respective diets formulated to meet or exceed established nutrient allowances (NRC, 1998). During gestation, each sow was fed 2.5 kg of a corn-soy-based diet/d with a calculated composition (as-fed) of 12.5% CP and 3,300 kcal of ME/kg. Lactating sows were fed ad libitum a corn-soy-based diet with a calculated composition (as-fed) of 16.7% CP and 3,426 kcal of ME/kg. Cleaning, feeding, and other housekeeping chores were on the same fixed schedule in all rooms.
At d 83 of gestation, all sows were exposed to a photoperiod of 12 h of light:12 h of dark for 1 wk. After this adjustment period, sows were randomly assigned to a LD (16 h of light/d; lights on at 0700 h and off at 2300 h) or a SD (8 h of light/d; lights on at 0700 h and off at 1500 h). The experiment was replicated 3 times, and photoperiod treatments were randomized between rooms. Supplemental light was provided with fluorescent tubes to achieve an intensity of 250 lux at the eye level of the sow.
Sows remained on their initial light treatment until they were moved to farrowing, when one-half were switched to the opposite treatment (LD:SD or SD:LD) and the other sows remained on their original treatment (LD:LD or SD:SD). Sows remained on their postpartum photoperiod treatments until the end of lactation (21 d postfarrowing). Crossfostering did not occur among litters, but litter size was adjusted based on teat number; extra piglets were removed from the study within 24 h postpartum. Litter processing procedures, including ear notching, teeth clipping, tail docking, castration, and an iron-dextrose injection, were all completed within 24 h of birth.
Blood and Tissue Collection
Sows were nose-snared, and 15 mL of blood was collected via jugular venipuncture with syringes containing sodium heparin (the procedure lasted <2 min) at d 0 (d 90 of gestation), 7, 14, and 21 of the experimental period, 24-h postfarrowing, and at the end of lactation. All piglets (115 barrows and 90 gilts) were bled at 7 d of age, and 4 piglets per litter (40 barrows and 40 gilts) were bled at 21 d (weaning) of age. Piglets were held in a supine position, and samples were collected via jugular venipuncture (the procedure lasted ~1 min).
Plasma Analysis
Immunoglobulin G (IgG) was measured using an ELISA, as previously described by Morrow-Tesch et al. (1994), with minor modifications. Porcine plasma samples were diluted 1:3,000 in 0.05% Tween-PBS. In duplicate, 120 µL of diluted sample or standard was added to 96-well microtiter plates coated with porcine IgG (Jackson Immunoresearch, West Grove, PA). Rabbit anti-pig IgG (120 µL; Sigma, St. Louis, MO) was added, and plates were incubated for 2 h at 25°C and then washed 3 times with 0.05% Tween-PBS. Enzyme-linked anti-rabbit IgG (200 µL; Jackson Immunoresearch) was added at a dilution of 1:7,500.
The plates were incubated for 1 h, decanted, and then washed 3 times. Substrate solution (200 µL; 1 mg/mL of p-nitrophenyl phosphate; Sigma) was added, and after a 30-min incubation, the reaction was stopped with 100 µL of 2 M NaOH. The plates were read using a microplate reader (BioTek Instruments, Winooski, VT) at a wavelength 405 nm. A standard curve (0, 0.1, 0.5, 1, 5, 10, 20, and 40 µg of IgG/mL) was used to estimate total plasma IgG.
Insulin-like growth factor-I was also measured using a commercially available ELISA assay kit following the manufacturer’s protocol (R & D Systems, Minneapolis, MN). Plasma samples were pretreated with pretreatment solutions provided in the kit to release IGF-I from binding proteins. In duplicate, 50 µL of treated sample or standard was added to 150 µL of assay diluent. The samples were added to precoated 96-well microtiter plates provided in the kit. The plates were incubated for 2 h at 2°C and washed 4 times with wash buffer. Enzyme-conjugated IGF-I solution (200 µL) was added, and the plates were incubated for 1 h, decanted, and then washed 4 times. Substrate solution (200 µL) was added, and after a 30-min incubation, the reaction was stopped with 50 µL of stop solution. The plates were read using a microplate reader at a wavelength 405 nm. A standard curve (0, 0.094, 0.188, 0.375, 0.75, 1.5, 3, 6, and 60 ng of IGF-I/mL) was used to estimate the total plasma IGF-I. The assay was validated for porcine plasma by parallelism, such that porcine serum depressed binding in parallel to the standard curve in the IGF-I assay. For IGF-I, the intra- and interassay CV were 4.3 and 8.3%, respectively; the minimal detectable concentration was 0.026 ng/mL.
Plasma cortisol was measured using a commercially available RIA kit (Coat-A-Count; Diagnostic Products, Los Angeles, CA). Intra- and interassay CV were 7.0 and 16.5%, respectively, and the minimal detectable concentration was 2 ng/mL.
Prolactin was also measured by RIA using a specific antiporcine prolactin antibody, in a modification of the assay previously described by Miller et al. (1999). The primary antibody (pPRL AFP-0842255Rb, NHPP and NIDDK, Torrance, CA) was diluted to a 1:50,000 working solution and a final tube dilution of 1:200,000. Porcine serum depressed binding in parallel to the standard curve. Mean intra-and interassay CV were 8.5 and 16.4%, respectively, and the assay sensitivity averaged 0.54 ng/mL.
Cell Count and Isolation
Whole blood (10 µL) was added to Isoflow (10 mL; Beckman Coulter, Miami, FL), and red blood cells were lysed. Total white blood cell (WBC) counts were measured electronically using a Coulter Z1 Particle Counter (Beckman Coulter). To determine the percentage of differential white blood cell populations, differential smears were made and manually counted using a light microscope. Whole blood was diluted with Roswell Park Memorial Institute (RPMI; Gibco, Carlsbad, CA) medium, layered over Histopaque-1077 (density = 1.077 g/mL; Sigma) and -1119 (density = 1.119 g/mL; Sigma), and centrifuged at 700 x g for 30 min at 25°C. Lymphocytes were removed from the top of the second layer and neutrophils from the top of the third layer. Red blood cells were lysed from the neutrophil fraction, which was then washed in RPMI and counted. Cell concentrations were adjusted with RPMI based on the immune assay requirements.
Immune Assays
The mitogen-induced lymphocyte proliferation assay was performed using a CellTiter 96 nonradioactive cell proliferation assay (Promega, Madison, WI), following the manufacturer’s protocol with minor modification. Briefly, porcine lymphocytes were used at a concentration of 5 million cells/mL; concanavalin A (ConA; Sigma) and lipopolysaccharide (LPS; Sigma) were used as mitogens (0, 25, and 50 µg/mL) to stimulate T and B cells, respectively.
Neutrophil chemotaxis was measured using an assay previously described by Salak et al. (1993). Neutrophils were used at a concentration of 3 million cells/mL to evaluate the ability of cells to migrate toward assay medium (control; random migration) or recombinant human complement-5a (10–7 M; Sigma) and recombinant human IL-8 (100 µg/mL; Sigma) (chemotaxis-directed migration).
Neutrophil phagocytosis was measured using a flow cytometry-based assay as previously described by Jolie et al. (1997), with a minor modification. Fluorescent beads were preincubated for 30 min with nonheat-inactivated porcine serum before adding beads to the samples at a 10:1 (beads:neutrophils) ratio. Cells and beads were incubated together for 45 min. The percentage of engulfment of beads by cells was evaluated using a flow cytometer.
Deuterium Oxide Dilution Procedure
Milk consumption of piglets at 14 to 17 d of age was estimated using a modified version of the deuterium oxide (D2O) isotope procedure previously described by Pluske et al. (1997). Immediately after a suckling bout, piglets were separated from their dams and weighed to the nearest 0.01 g. After a 45-min fasting period (to standardize gut fill), piglets were injected i.m. with 500 mg of D2O (99.9%; Sigma) per kg of BW. The D2O was allowed to equilibrate with body water for 60 min, and then a blood sample was taken. Piglets were returned to their dam, and the same maternal separation and blood collection procedures after a suckling bout were repeated for 3 consecutive days. Blood samples were allowed to clot for 1 h at room temperature and then centrifuged at 900 x g for 20 min. Samples were read using a mass spectrometer (model IR200 spectrometer, ThermoNicolet Corp., Madison, WI), and D2O concentrations were expressed as parts per million. Estimated milk intake was calculated using a serum D2O disappearance curve for each piglet, as described in Auchtung et al. (2002). Final milk intake volumes were calculated using established conversion factors (Prawirodigdo et al., 1990; Pluske et al., 1997).
Statistical Analysis
Statistical analyses were performed using SAS version 8 (SAS Inst. Inc., Cary, NC). All traits were tested for departure from a normal distribution. Natural logarithmic transformation was applied to WBC, neutrophil:lymphocyte ratio (N:L), cortisol, IgG, prolactin, and lymphocyte proliferation for sows and piglets. Additionally, data were transformed for lymphocyte and neutrophil counts for the piglets. Minimum values for percentage of monocytes and eosinophils were zero; thus, a value smaller than the lowest nonzero number was added to all the observations to allow for logarithmic transformation. For all traits that were subjected to logarithmic transformation, means presented in tables and graphs are nontransformed means.
A linear, mixed effects model was used to analyze sow variables. Main fixed effects were treatment and day. Random effects were pig and block. The model had a repeated structure on day, allowing the incorporation of heterogeneity of variance across days. A GLM was used to analyze piglet variables. The main fixed effects included treatment and sex; variance among litters was used as the error term. Contrasts were conducted to evaluate the influence of the maternal lighting treatment on the piglets. Sow immune measures were correlated with piglet immune measures to identify potential relationships. Significance was set at P 0.05, and trends were discussed at P 0.10.
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RESULTS
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Immune and Endocrine Measures
Sows.
Pregnant sows kept on LD for 7 d tended to have greater (P = 0.098) percentages of neutrophils and fewer (P = 0.10) lymphocytes compared with those kept on SD, thus resulting in an increased N:L ratio in sows on LD (P = 0.05; Table 1). Total neutrophil numbers tended to be greater (P = 0.07) in those same sows at d 21 posttreatment (Table 1). There was a treatment x day interaction (P < 0.05) found for total WBC counts in lactation (Figure 1). Sows kept on LD during gestation, then switched to SD for the duration of the farrowing-lactation period (LD:SD), had greater (P < 0.05) total WBC 24 h postfarrowing compared with all other treatment groups (Figure 1).
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Table 1. Total white blood cell (WBC), lymphocyte, and neutrophil counts for sows kept on long day (LD; 16 h light/d) or short day (SD; 8 h light/d) photoperiod during late gestation1
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Sows on SD had greater ConA- (P = 0.003; Figure 2A) and LPS-induced (P = 0.02; Figure 2B) lymphocyte proliferation responses d 7 posttreatment, whereas sows kept on LD had greater responses at d 14. At the end of lactation, ConA-induced proliferation was greater (P = 0.05) in sows kept on LD for the entire duration of the study (LD:LD). Also, there was a tendency for sows kept on LD:SD to have less (P = 0.08) LPS-induced proliferation at the end of lactation.
Sows kept on LD during gestation had a tendency for greater (P = 0.095) phagocytosis; d 21 posttreatment than those sows kept on SD (Figure 3). However, relative to sows kept on LD, sows kept on SD for the duration of the study (SD:SD) tended to have greater (P = 0.10) plasma cortisol 24 h postfarrowing and at the end of lactation (Table 2). However, prolactin concentrations did not differ among photoperiod treatments (P > 0.20; Table 2). In addition, there was no treatment x day interaction for chemotaxis-directed migration, IgG, or IGF-I during late gestation or through lactation (Table 2).
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Table 2. Plasma hormone concentrations for sows kept on long day (LD; 16 h light/d) or short day (SD; 8 h light/d) photoperiod during late gestation and throughout lactation (LD:LD, LD:SD, SD:LD, or SD:SD)1
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Piglets.
Compared across treatments, piglets from those sows on LD:SD had greater (P = 0.001) total WBC at 7 d of age, whereas piglets from sows on LD:LD tended to have lower (P = 0.08) counts at weaning (Table 3). Piglets from sows on LD:SD had greater percentage of monocytes at weaning (P = 0.009). There was a treatment x sex interaction at 7 and 21 d of age (Table 2
). Barrows from sows that were kept on SD:LD had a greater (P = 0.024) percentage of lymphocytes but fewer (P = 0.05) neutrophils; these changes resulted in a reduced (P = 0.05) N:L ratio in these pigs relative to the barrows from other treatments. At weaning, barrows from those sows kept on SD throughout late gestation and lactation had lower (P = 0.042) percentage of monocytes. There was also an effect of gestational photoperiod treatment on total WBC (P = 0.003) of piglets at 7 d of age.
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Table 3. Total numbers and percentages of different leukocyte populations for piglets of different sexes from sows kept on long days (LD; 16 h light/d) or short days (SD; 8 h light/d) during late gestation and throughout lactation (SD:SD or LD:LD) or from sows that had switched photoperiod at farrowing (LD:SD or SD:LD)1
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At 7 d of age, piglets from sows kept on SD during gestation, then switched to LD (SD:LD), had lower (P = 0.01) total plasma IgG than all other treatment groups (Table 4). Also at 7 d of age, plasma cortisol was greater (P = 0.001) in LD:SD piglets, whereas those from sows on SD:SD had greater (P = 0.05) cortisol at weaning compared with other treatments (Table 4). More specifically, gestational lighting treatment on the sow influenced her piglets’ total IgG (P = 0.001) and plasma cortisol (P = 0.02) concentration at 7 d of age.
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Table 4. Plasma hormone concentrations at 7 and 21 d of age for piglets from sows kept on long days (LD; 16 h light/d) or short days (SD; 8 h light/d) during late gestation and throughout lactation (SD:SD or LD:LD) or from sows that had switched photoperiod at farrowing (LD:SD or SD:LD)1
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At weaning, piglets from sows that were on SD:SD had greater (P < 0.001) ConA and tended to have greater (P = 0.10) LPS-induced lymphocyte proliferative responses (Figure 4). In contrast, piglets from those sows on LD:LD had greater (P = 0.003; Figure 5) neutrophil phagocytosis, which was apparently influenced by the sow’s gestational lighting treatment (P = 0.005). Light treatment experienced by the sow during gestation also influenced the ConA-induced proliferative response (P < 0.001) of her piglets. In piglets, there was no treatment effect on prolactin concentrations or milk consumption.
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Figure 4. Photoperiod effects on concanavalin A-(ConA; Panel A) and lipopolysaccharide- (LPS; Panel B) induced proliferation responses for piglets at 21 d of age. Piglets from sows kept on a short day (SD) photoperiod had the greatest lymphocyte proliferation responses to ConA (P < 0.001) and LPS (P < 0.001). a,bLeast squares means denoted by different letters differ, and means denoted by  differ by contrast (P < 0.05). Photoperiod treatments of the piglet’s sows were LD (16 h light/d) or short days (SD; 8 h light/d) during gestation followed by lactation: LD:LD, LD:SD, SD:LD, and SD:SD.
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Figure 5. Photoperiod effects on percent engulfment of fluorescent beads by porcine neutrophils as a measure of phagocytosis for piglets at 21 d of age. Piglets from sows kept on a long day (LD) photoperiod had the greatest percentage (P = 0.003) of engulfment of beads. Gestational photoperiod treatment also influenced phagocytosis (P = 0.005). a,bLeast squares means denoted by different letters differ, and means denoted by differ by contrast (P < 0.05). Photoperiod treatments of the piglet’s sows were LD (16 h light/d) or short days (SD; 8 h light/d) during gestation followed by lactation: LD:LD, LD:SD, SD:LD, and SD:SD.
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Body Weight and Litter Data
Weights and litter data are presented in Table 5. Sow BW was not different between sows exposed to LD or SD at the beginning of the study. Sows kept on SD during gestation tended to have more (P = 0.07) piglets born alive and had greater (P = 0.03) number of female piglets than those sows on LD photoperiod (Table 5). Conversely, piglets from sows kept on LD photoperiod were heavier (P = 0.002) at birth than those from sows on SD. Regardless of treatment, barrows were heavier (P = 0.008) at birth than gilts. There was no lighting effect on number of piglets weaned, piglet weaning BW, or sow weaning BW.
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Table 5. Weights and litter data for 24 sows that were kept on either long days (LD; 16 h light/d) or short days (SD; 8 h light/d) during late gestation and throughout lactation (SD:SD or LD:LD) or from sows that had switched photoperiod at farrowing (LD:SD or SD:LD)1
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Correlation Analysis
Piglet cortisol concentration was moderately correlated with the immune response of their dams during gestation. Specifically, as total WBC counts (r = 0.33, P < 0.001), percentage of neutrophils (r = 0.35, P < 0.001), and N:L ratio (r = 0.33, P < 0.001) increased in sows at 14 d posttreatment, their piglets’ plasma cortisol concentrations increased at 7 d of age. There were also positive relationships between 7- and 21-d cortisol (r = 0.32, P = 0.007) and IgG (r = 0.39, P < 0.001) concentrations in piglets.
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DISCUSSION
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These data indicate that a distinct photoperiod during the late-gestational and lactational periods may temporarily influence sow health and performance and also influence the physiological responses of her progeny. During gestation, immune effects were apparent within the first 7 d after implementation (i.e., d 97 of gestation) of a LD or SD, but these effects were less evident by 21 d postpartum. This rapid adjustment to photoperiod may be attributed to the ability of the pig to alter melatonin secretion within 1 wk after a prompt change in photoperiod (Tast et al., 2001). The mitogen-induced lymphocyte proliferation responses were affected in this study, with T and B cell responses being stimulated within the first 7 d after exposure to SD photoperiodic treatment. A similar response has been reported in dry cows (Auchtung et al., 2002) and hamsters (Bilbo et al., 2002; Zhou et al., 2002). Physiological changes associated with the change in seasons, which are primarily cued by day length, may partially explain this increase in mitogen-induced lymphocyte proliferation responses. An enhancement in immune function is a common response in anticipation of seasonal stressors. However, in the current study, the effect of photoperiod on lymphocyte proliferation response was only observed at d 7 in the sows on SD and d 14 in the sows on LD, suggesting that the effect of photoperiod observed in these animals might have been influenced by previous photoperiodic experience. Even though all the sows in this study were kept on a 12L:12D photoperiod for 1 wk before being put on a LD or SD photoperiod, the direction of change is critical to photoperiodic responses. Thus, the decline in light exposure in sows that were switched from 12L:12D to SD may have accelerated the proliferative response compared with sows that moved to LD. However, by 21 d after initiation of photoperiodic treatment, there was no difference between sows on SD and those on LD, implying that the changes in photoperiodic exposure caused transient shifts in immune response rather than reprogramming the long-term immune response of the sow.
Despite the transient effect found on lymphocyte proliferation, the time that the sows were on photoperiod treatment during gestation was observed to be enough to influence litter size and performance as well as endocrine responses in lactation in the current study. Sows kept on SD during late gestation had more piglets born alive and tended to wean more piglets than those sows kept on LD. Even though these findings are similar to those of Prunier et al. (1994), who reported that sows kept on SD had more piglets born alive and more piglets weaned, we view our findings with caution due to small sample size and limited photoperiodic treatment exposure before farrowing. In contrast to our findings and those of Prunier et al. (1994), Mabry et al. (1983) reported that 8 h of light had no effect on the number of piglets born alive, but sows on 16 h of light during the lactation period weaned more piglets. The unknown previous photoperiod experiences of the sows as well as no gestational photoperiod treatment in the Mabry et al. (1983) study may account for the contradictions among studies. Moreover, sows kept on SD during gestation had more female piglets than those sows on LD. It is possible that the number of piglets born alive and the sex difference observed herein are not directly due to the photoperiodic treatment but rather to some random effect.
The photoperiod that an animal experiences during gestation may alter the magnitude and duration of the cortisol spike at the time of parturition. For example, Kraeling et al. (1983) reported no effects of photoperiod on cortisol concentrations during lactation in Yorkshire x Landrace sows, but Yorkshire sows kept on 8 h of light beginning at d 102 of gestation had less cortisol than sows on 16 h of light. Contrary to these findings, we found that sows kept on SD throughout the entire study (SD:SD) had elevated cortisol postfarrowing and throughout lactation. One difference between the current study and that of Kraeling et al. (1983) is the length of exposure to photoperiod during gestation. Typically, cortisol increases within a 24- to 48-h period surrounding parturition and tends to return to basal concentrations during lactation (Ash and Heap, 1975; Martin et al., 1978; Osterlundh et al., 1998). The elevated cortisol concentrations in sows kept on SD through lactation could be attributed not only to the reprogramming that occurred during gestation but also to an increase in the frequencies of nursing bouts by the piglets. Teat stimulation during lactation has been shown to increase cortisol (Varley and Foxcroft, 1990); therefore, it is possible that SD may increase the frequency of nursing bouts by the piglets, which was not evaluated in this study. However, the D2O data in the current study do not support this concept; there was no difference in milk consumption among the different treatment groups. In view of this, photoperiod may have increased the frequency of nursing attempts by piglets, but not the amount of milk produced by the sow. Another possibility is the sows on SD photoperiod actually had more piglets suckling, which may have contributed to teat stimulation. Overall, it appears that photoperiod affects cortisol concentrations in sows at farrowing and through lactation but does not affect milk consumption by the piglets.
Although photoperiod effects during late gestation on sow immune function were transient, photoperiod did influence the physiological responses of the piglets. Similarly, in the ewe, photoperiodic manipulation during gestation has a direct impact on the lamb. Lambs born to ewes kept on 16 h of light for 100 to 122 d before parturition had greater prolactin concentrations than lambs from ewes kept on 8 h of light (Ebling et al., 1989; Helliwell et al., 1997). A potential mechanism to explain the maternal influence is the pattern of melatonin secretion of the sow. Maternal melatonin crosses the placental barrier to relay photoperiodic information to the fetus (Horton and Stetson, 1990; Davis, 1997; Goldman, 2003). Similar to prolactin in lambs, we found that piglets from sows kept on LD (d 90 of gestation to farrowing) had greater plasma cortisol at 7 d of age. It is also of interest that piglets from sows kept on SD through lactation had the greatest cortisol concentrations at 21 d of age. Perhaps the increased cortisol concentrations found in the sows at 24 h postpartum had an influence on the fetal development of the hypothalamic-pituitary-adrenal (HPA) axis, therefore resulting in greater baseline cortisol concentrations in their piglets at 21 d of age.
Exposing sows to SD from d 90 of gestation until farrowing also influenced IgG concentrations in their offspring at 7 d of age. Less total IgG may be indicative of impaired passive-immunity due to decreased immunoglobulin secretions by the dam or decreased immunoglobulin absorption by the digestive tract of a neonatal piglet. Thus, those piglets from sows kept on SD during late gestation may be more vulnerable to antigens in the environment due to this decrease in plasma IgG. However, the B-cell-induced proliferation response at weaning was greater in piglets whose dams were kept on a SD throughout the study. Perhaps this greater antibody producing B-cell response at weaning is a compensatory response to the reduced IgG concentrations seen at 7 d of age. Moreover, it is possible that an increase in the number of B cells does not necessarily coincide with greater antibody production because these cells may be naive lymphocytes that have not differentiated into plasma cells capable of producing antibodies. In addition to gestational photoperiod, the direction of change in day length experienced by the sows just before parturition may have also influenced the differences in immune function in piglets observed in the current study.
In addition to the maternal influences on piglet responses, we found that the immunological responses to photoperiod are influenced by pig sex. Most often the differences were evident in the barrows; often they had stimulated immunological responses compared with the gilts. Typically, there have been no differences reported between barrows and gilts in basal and stress-induced HPA-axis activity (Ekkel et al., 1996; de Jong et al., 1998; Tuchscherer et al., 1998); therefore it is possible that the stimulated responses observed in the current study may be indicative of an enhanced response to castration stress due to sex and lighting treatment. At 7 d of age, barrows from sows on SD:LD had greater percentage of lymphocytes and reduced percentage of neutrophils, resulting in a decreased N:L ratio. Thus, these piglets may be less sensitive to a stressor, such as castration. Prunier et al. (2005) reported an increase in ACTH and cortisol immediately after castration, indicating that castration activated the HPA axis. In addition to activation, castration could also cause the HPA axis to become sensitized to stressors that occur later in life (McGlone et al., 1993; Raeside et al., 1997; de Groot et al., 2001). It is likely that the HPA axis was activated in response to castration of the barrows at 1 d of age in the current study. It is also possible that piglet HPA development was influenced by prenatal programming of photoperiod, consistent with the altered cortisol concentrations observed under SD. Therefore, barrows that were on SD:LD were better able to cope with the stress of castration and return to homeostasis quicker than barrows on other photoperiod treatments.
In summary, the late-gestational photoperiod treatment applied to sows in this study might have been insufficient to completely alter immune function during gestation but sufficient to influence endocrine (i.e., cortisol) and performance (i.e., litter size) measures at farrowing and throughout lactation. However, additional research is warranted to determine the influence of previous photoperiod experience on these responses and to determine the optimal period during gestation that photoperiod exposure should begin that will influence these responses long-term. Despite these short-term alterations on the immune status of the sow, photoperiod did influence cortisol concentrations. Interestingly, cortisol concentrations of sows at parturition, as evident by elevated residual concentrations 24 h postpartum, may have influenced piglet cortisol by affecting the final development of the HPA axis prenatally, resulting in greater baseline function. More importantly, the effect of manipulation of photoperiod on a sow during gestation may ultimately influence the immune status of her piglets, thus enhancing the ability of piglets to resist infection until weaning. Furthermore, the direction of change in day length experienced by the sows just before parturition may have also influenced the differences in piglet immune function among the photoperiod treatments. It is possible that these immunological changes could benefit pigs throughout the nursery phase. It seems plausible that the photoperiod perceived in utero may also influence the response of the HPA axis to postnatal stressors. For example, in response to castration, barrow stress responses and HPA activation were affected or altered by photoperiod. Based on these data, we believe that manipulation of photoperiod might be useful for altering sow productivity and piglet immune function as well as their stress responsiveness.
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Footnotes
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1 This research was supported by the National Pork Board and the Illinois Agricultural Experiment Station. The authors thank Sandra Rodriguez-Zas for advice and statistical assistance and Jennifer Dauderman, Debra Evans, and Jim Pettigrew for technical assistance. 
2 Corresponding author: johnso17{at}uiuc.edu
Received for publication October 18, 2005.
Accepted for publication March 15, 2006.
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Abstract
INTRODUCTION
) or SD (8 h light/d; •) during gestation followed by lactation: LD:LD (
), SD:LD (
), or SD:SD (•).
