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ANIMAL NUTRITION |
Department of Animal and Ranges Sciences, North Dakota State University, Fargo 58105
Abstract
Our objectives were to evaluate maternal body changes in response to dietary restriction or the increased nutrient requirement of fetal growth. In Exp. 1, 28 mature crossbred ewes (61.6 ± 1.8 kg initial BW) were fed a pelleted forage-based diet to evaluate effects of pregnancy and nutrient restriction on visceral organ mass. Treatments were arranged in 2 x 3 factorially, with dietary restriction (60% restriction vs. 100% maintenance) and reproductive status (nonpregnant [NP], d 90 or d 130 of gestation) as main effects. Dietary treatments were begun at d 50 of gestation, and restricted ewes remained at 60% of maintenance throughout the experiment. Nonpregnant and d-90 ewes were fed dietary treatments for 40 d and slaughtered. The d-130 ewes were fed dietary treatments for 80 d and then slaughtered. In Exp. 2, four Romanov ewes were naturally mated (Romanov fetus and Romanov dam; R/R), and two Romanov embryos were transferred to each of four Columbia recipients (Romanov embryos and Columbia recipient; R/C). Three Columbia ewes were naturally mated (Columbia fetus and Columbia recipient; C/C). In both experiments, maternal organ weights were reported as fresh weight (grams), scaled to empty body weight (EBW; grams per kilogram) and maternal body weight (MBW; grams per kilogram). In Exp. 1, ewe EBW and fetal mass were decreased (P < 0.02) with restriction compared with maintenance. Dietary restriction decreased liver mass (16.7 vs. 14.5 g/kg EBW or 18.8 vs. 16.4 g/kg MBW; P < 0.01), but dietary restriction did not affect total digestive tract mass. In Exp. 2, ewe BW was less for the R/R compared with R/C and C/C (44.8 vs. 110.4 and 98.1 ± 7.9 kg, respectively; P < 0.01). Fetal weight at d 130 was less for the R/R than for R/C and C/C (2.2 vs. 3.3 and 4.7 ± 0.3 kg, respectively; P < 0.01) when measured as individual fetuses; however, when measured as total fetal mass carried in each ewe, there was no effect of ewe type. These data suggest that the gastrointestinal tract, along with other maternal organs, responds to both level of dietary intake and nutrient requirements for gestation, and that fetal weight is decreased as a result of a 40% decrease in nutrients offered.
Key Words: Dietary Restriction • Gastrointestinal Tract • Pregnancy • Sheep
Introduction
The initial two-thirds of gestation is an anabolic physiological state (Vernon et al., 1985
), whereas the last third is catabolic in regards to maternal metabolism (Symonds and Clarke, 1996). Increased nutrient demand of fetal growth requires the maternal system to shuttle nutrients to the gravid uterus. Maternal system responses to dietary restriction coupled with the demand of pregnancy are not well understood.
A decrease in gastrointestinal (GI) tract mass owing to dietary restriction was demonstrated previously in nonpregnant animals (Wester et al., 1995; Burrin et al., 1990). The biological priority of reproduction (i.e., gestation, fetal growth, and mammary development) may compete more successfully for nutrients and impact the GI tract mass differently than simple nutrient restriction (Bell, 1993). Factors that alter gut mass alter the relationship between BW and energy expenditure (Reeds et al., 1999). Battaglia (1992) reported that during a 5-d maternal fast, amino acid uptake across the umbilicus was unchanged, illustrating the priority of nutrient delivery to the gravid uterus.
The ability of the maternal system to deliver a normal fetus is dependent on the capacity of the maternal system to meet uterine nutrient demands. Gluckman and Liggins (1984) suggested that fetal genetic growth potential is rarely completely expressed because it is constrained by maternal factors influencing the fetal environment. McNeill et al. (1997) used lean or fat ewes slaughtered in late gestation to analyze maternal body components and demonstrated that fetal and placental weights were not different owing to ewe body condition, although fetal lipid contents were less in thin ewes. Limited data are currently available on how the GI tract and other visceral tissues respond to the nutrient demands of gestation. Our objectives were to evaluate effects of dietary restriction and nutrient demand of pregnancy on fetal and maternal weight and visceral organ mass in ewes.
Materials and Methods
Experiment 1
Animals.
Twenty-eight mature crossbred ewes were used to evaluate effects of dietary restriction and pregnancy on mobilization of maternal nutrient stores. Experimental protocols were approved by the North Dakota State University Institutional Animal Care and Use Committee. All ewes were qualified as reproductively sound by the exhibition of standing estrus during the estrous cycle prior to exposure to rams. Pregnant ewes were randomly assigned to either d-90 or d-130 pregnancy status, and ewes in the nonpregnant (NP) reproductive status were not bred.
Ewes were shorn and moved into an indoor facility with a maintained ambient temperature of 18 ± 3°C. Individually penned ewes were adjusted to a 12:12 (light:dark) cycle for 5 to 7 d. During the adaptation period, ewes were individually fed maintenance diets. Dietary treatments (Table 1) were imposed at d 50 of gestation for the d-90 (mid-gestation) and d-130 (late-gestation) reproductive status; the NP reproductive status group was on treatment for 40 d. Dietary restriction was 60% of the maintenance level for NP, d-90, and d-130 animals. The decrease in dietary intake was imposed as a total diet reduction by offering less feed to restricted animals. The maintenance treatment was fed at 100% of the maintenance level for each reproductive status. The formulation of feedstuffs was adjusted at d 100 of gestation for the d-130 reproductive status in accordance with the NRC (1985) recommendation.
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Slaughter Procedure and Tissue Collection.
Ewes were assigned randomly to a slaughter date which resulted in their assignment to reproductive status. Two ewes were transported to the abattoir at 0730 on the appropriate day of sample collection. One ewe was stunned and exsanguinated at 0800, and the second at 1300. Reproductive tracts were immediately removed and dissected from the vagina at the cervix and weighed, and fetal variables measured. Individual fetal and total fetal masses as well as crown rump lengths were measured. Uterine mass of the nonpregnant ewes was calculated to be 28.4 g from the data of Johnson et al. (1997). The ewe was then eviscerated and organ weights recorded. The stomach complex was divided from the esophagus at the cardia and from the intestine at the pyloric valve. Contents were removed, and the tissue weighed. The omentum was separated from the stomach complex and weighed.
Intestinal tissues were located, and the demarcations of duodenum, jejunum, ileum, cecum, and colon were made. Duodenal tissue was determined to be the region from the pyloric valve distally to the point adjacent to the branch of the gastrosplenic vein and the anterior mesenteric vein. Jejunal tissue was considered to lie from the distal end of the duodenum to a point 10 cm distal from the junction of the mesenteric vein and the ileocecal vein. Ileal tissue was defined as the remaining portion of the small intestine. The large intestine was divided into the cecum and colon at the ileocecal junction.
After specific regions were identified, the mesentery was dissected away from the tissue; digesta were gently stripped, and the segment weighed. The liver was dissected out of the visceral tissues and weighed. The gall bladder was drained and then weighed. The lungs, heart, kidneys, and spleen were also weighed. The weight of the carcass, including hide and head, was defined as the eviscerated BW.
Calculations and Statistics.
Tissue masses are reported as fresh weight as previous data has suggested little difference in fresh and dry weights (Jin et al., 1994; Swanson, 1996; Swanson et al., 2000). Empty BW (EBW) was the summed weight of the carcass (including head, hide, feet, and mammary gland), lungs, spleen, heart, kidneys, stomach complex, intestinal tissue, omentum, mesentery, and gravid uterus. Empty BW is often used to evaluate the contribution of organ mass to metabolism of animals of different body sizes (Sainz and Bently, 1997; Koong et al., 1985; NRC, 1996). Empty BW is intended to be a measure of metabolically active tissue and is ideally defined as BW less gut fill. However, when considering nutrient delivery by pregnant animals, the uterine compartment should be considered metabolically active tissue and was, therefore, included in EBW. Maternal BW (MBW) was calculated as EBW with the exclusion of gravid uterine weight (Rattray et al., 1974; Robinson et al., 1978). Expression of data on EBW and MBW bases should allow comparisons with other data sets (Burrin et al., 1990). Small intestinal mass was the summation of individual weights of the duodenum, jejunum, and ileum, and large intestinal mass was the summation of the colon and cecum (Seal and Reynolds, 1993). The digestive tract was the summation of the intestines and the stomach complex. Total internal organ mass was the summation of the lungs, spleen, heart, liver, kidneys, stomach complex, intestinal tissue, omentum, mesentery, and gravid uterus.
Data were analyzed using with the General Linear Model of SAS (SAS Inst. Inc., Cary, NC) as a 2 x 3 factorial treatment arrangement. The statistical model included dietary treatment and reproductive status, and the interaction of dietary treatment and reproductive status. Planned comparisons of NP vs. d 90 and d 130 to determine the effect of pregnancy and d 90 vs. d 130 were used to evaluate the affect of advancing gestation.
Experiment 2
Estrus was synchronized in Romanov and Columbia ewes using a Norgestomet implant (Sychromate-B; Merial Ltd., Athens, GA). At the detection of estrus (d 0), recipients were identified, and donor ewes were bred by a Columbia or Romanov ram, respectively. On d 2 of the estrous cycle, 2- to 4-cell Romanov embryos (two) were collected and were transferred to the oviduct of four Columbia recipients, resulting in the Romanov embryo-Columbia ewe treatment (R/C; n = 4). The Romanov/Romanov (R/R) treatment consisted of Romanov ewes (four) naturally mated to Romanov rams. Similarly, Columbia ewes (n = 3) were naturally mated to Columbia rams (C/C). Pregnant ewes were housed outdoors with an open-faced barn for shelter. Animals had ad-libitum access to grass hay, mineralized salt blocks, and fresh water. Tissue collections in Exp. 2 were identical to those in Exp. 1.
Calculations and Statistics.
Calculations of EBW and MBW were performed similarly to those in Exp. 1. Differences between treatments were analyzed using analysis of variance with the General Linear Models of SAS (SAS Inst. Inc.). Treatment means were separated using the method of least significant difference and were protected with a significant F-test for treatment (P < 0.10).
Results
Experiment 1
Initial BW of ewes did not differ among dietary treatment or reproductive status (Table 2). Ewe BW was decreased by dietary restriction (P < 0.01) and was increased by reproductive status (P < 0.01). Carcass mass was decreased (P < 0.01) by dietary treatment (P < 0.01) although reproductive status did not alter carcass mass. Empty BW was decreased by restriction (P 
0.01) and increased by reproductive status (P 0.01). Maternal BW was decreased by restriction (P 0.01) and unchanged by reproductive status. Daily weight change of maintenance ewes was a 174.8 g/d gain, whereas restricted ewes lost 11.6 g/d (P 0.01).
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). Gravid uterine mass was not affected by dietary treatment; however, mass of individual fetuses was decreased (P < 0.01) and crown rump length (CRL) unaffected by treatment. The interaction (Table 3; treatment x reproductive status) observed for individual fetal weights and CRL resulted from fetal weights and CRL of maintenance ewes being numerically less at d 90 and a significant reduction of individual fetal weight and CRL at d 130 owing to restriction (data not shown).
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) owing to decreasing BW. Lung mass was not affected by dietary treatment. Of these variables, only liver mass decreased (P 0.01) when organ weights were scaled to (divided by) either EBW or MBW.
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0.01) from NP to d 130. Spleen weight was also decreased owing to reproductive status and remained smaller (P < 0.01) whether scaled to EBW or MBW. Heart mass was decreased (P < 0.04) owing to dietary restriction. Heart weight scaled to EBW was also decreased (P < 0.01) because of reproductive status (7.8, 6.3, 6.1 ± 0.4 g/kg EBW for NP, d 90, and d 130, respectively). Liver mass was decreased (P 0.01) as a result of dietary restriction and increased owing to pregnancy. When scaled to EBW or MBW, liver weight increased (P 0.01) in pregnant relative to NP ewes, but d 90 and d 130 were similar. Kidney mass (grams) was decreased (P < 0.07) in response to dietary restriction. The mass of the kidney decreased (P < 0.09) owing to reproductive status when scaled to EBW and was unchanged when scaled to MBW (Table 4
).
Empty stomach complex weight was decreased (P < 0.04) in response to dietary restriction (Table 5) and increased (P < 0.02) in its ratio to MBW owing to reproductive status. The omentum was also decreased (P 0.09) because of reproductive status when scaled to EBW and MBW. Duodenum weight was not affected by restriction or reproductive status. Jejunal and ileal masses (grams) were decreased (P 0.03) by restriction and increased by reproductive status, and were increased (P 0.07) in response to reproductive status when scaled to MBW. Likewise, when scaled to MBW, the increased mass of the jejunum and ileum caused by reproductive status contributed to a similar response (P 0.01) in the total small intestinal mass. The large intestine was unaffected by restriction or reproductive status. Dietary restriction was effective in reducing total digestive tract mass. Total internal organ mass was increased (P < 0.01) owing to reproductive status.
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). The Romanov ewes weighed 44.8 kg at d 130 of gestation, whereas Columbia ewes averaged 104 kg (P < 0.01). Carcass mass, EBW, and MBW were less (P < 0.01) in the R/R ewes compared with either of the Columbia groups.
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. Total mass of the gravid uterus did not differ by type of fetus or ewe; however, when scaled to EBW, gravid uterus was larger (P < 0.01) for the R/R (220 g/kg EBW) compared with the R/C or C/C (101 vs. 139 g/kg EBW, respectively). When scaled to MBW, the R/R again had a greater (P 0.01) proportion of gravid uterus to MBW when compared with other treatments.
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). Weight of individual fetuses was affected (P = 0.01) by ewe type. The R/R had the smallest fetal mass at 2.16 kg compared with the R/C and C/C fetuses, which weighed 3.33 kg and 4.71 kg, respectively. This difference resulting from ewe type was alleviated when total fetal mass was calculated. The CRL was least for the R/R group, with a fetal length of 41.7 cm, and increased in the R/C group (46.7 cm) and increased further in the C/C ewes (54.3 cm).
The overall masses (grams) of the lung, spleen, heart, liver, and kidneys were less (P < 0.01) in R/R ewes compared with R/C and C/C ewes (Table 8). When scaled ratios (EBW or MBW) of the lungs were analyzed, they did not differ between the treatments. Spleen mass (grams per kilogram MBW) was less (P 0.03) for R/R compared with R/C or C/C. Heart mass, scaled to EBW or MBW, did not differ owing to ewe type. The ratio of liver mass to EBW or MBW did not differ with ewe type. The response of the kidneys was similar to that of the liver, except that R/R ewes had a greater kidney-to-MBW ratio compared with the R/C or C/C ewes at 3.7 vs. 3.1 and 3.1 g/kg MBW, respectively (P < 0.01).
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). Also, the stomach complex was lowest in R/R, intermediate in C/C, and highest in R/C ewes (P < 0.10). The omentum was not different between any of the groups when scaled to MBW.
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0.02) duodenum and jejunum to EBW and MBW ratio than either the R/C or C/C ewes. The ratio of the ileum to MBW was also greater (P < 0.09) in the R/R ewes compared with the R/C and C/C groups. When the three sections of the small intestine were summed, the R/R ewes had the greatest small intestinal mass and ratio to EBW and MBW (P < 0.03). The intestinal mesenteric mass was smallest (P < 0.02) in the R/R group.
The cecum and colon masses responded similarly between the ewe types; R/R had less (P < 0.01) cecal and colonic mass when compared with the other ewe types (Table 9). When considered as a ratio to EBW, no differences that were due to ewe type were observed, although the R/R ewes had a greater (P 0.05) ratio of cecal and colonic tissue per unit of MBW. A similar pattern of response was observed when these tissues were compiled and analyzed together as the large intestine.
The total digestive tract weight (grams) was less (P < 0.01) in the R/R ewes. When scaled to EBW, the difference in ewe type did not result in an overall response; however, the R/R and R/C ewes had a greater (P < 0.07) ratio of digestive tract tissue per unit of EBW compared with the C/C ewes. When scaled to MBW, R/R had the greatest (P < 0.05) proportion of digestive tract tissue per unit of MBW.
For total mass of internal organs, the R/R group had less (P < 0.08) total mass. Conversely, when scaled to either EBW or MBW, the R/R group had a greater (P < 0.01) ratio of internal organ mass.
Discussion
Body Weight
We investigated the hypothesis that individual maternal visceral organ weights are responsive to dietary restriction and reproductive status in sheep. Previous reports have evaluated the response of total visceral organ mass resulting from nutrient restriction during pregnancy (McNeill et al., 1997). Alternatively, the gastrointestinal tract as a whole and the liver have been the focus of experiments (Robinson et al., 1978). The level of dietary restriction imposed on d 50 of gestation in the present trial is similar to the design of Faichney and White (1987). Their level of restriction resulted in BW losses by d 135 of gestation. In the present description of the maternal system, BW was decreased at d 90 and 130 as a result of dietary restriction. Carcass weight was also decreased at d 90 and 130, whereas EBW was decreased only at d 130. Nonpregnant ewes also lost weight, 56.1 g/d, whereas the d 90 ewes gained 131.7 g/d, and the d 130 ewes gained 169.1 g/d. Weight gains by the d-90 and d-130 ewes were primarily due to the development of the conceptus because carcass weight and MBW were not different between d 90 and 130.
Body weight parameters were intended to be different in Exp. 2, in which the R/R were less than one-half the BW at d 130 of gestation than R/C and C/C animals. This difference was consistent for ewe BW, carcass weight, EBW, and MBW. In a similar experiment with cows, large discrepancies in mature maternal BW had a dramatic impact on uterine blood flow and function of the uteroplacental compartment (Ferrell, 1991b).
Uterine Variables
Gravid uterine mass was unaffected by treatment in Exp. 1. Data of Exp. 1 are similar to data reported by Faichney and White (1987), which showed that dietary restriction from d 50 to 135 of gestation did not change gravid uterine weight. No changes were observed when gravid uterine weights were scaled to BW, EBW, or MBW in the present study. In contrast, a reciprocal embryo transfer experiment done in Brahman and Charolais, Ferrell (1991a) described an increase in gravid uterine mass with Charolais fetuses regardless of maternal breed. In the present report, gravid uterine mass was greater in R/R ewes when scaled to EBW and the difference was increased when scaled against MBW. Data reported by Ferrell (1991a) indicated that Brahman cows carrying Charolais fetuses had a gravid uterine weight of 83.9 g/kg of MBW compared with 55.7 g/kg MBW for the Brahman cows carrying Brahman fetuses. At d 232 of gestation, the Charolais cows carrying Brahman fetuses had a uterine weight of 45.4 g/kg, and Charolais fetuses were 68.4 g/kg of MBW. The proportion of gravid uterine mass to BW was greater when a large-growth-potential breed fetus was carried by a small-mature-body-size breed. Similarly, in our study the R/C ewes had the lowest gravid uterine mass (74 g/kg of MBW), whereas the gravid uterus mass was 156 g/kg for the R/R ewes and 111 g/kg BW for the C/C ewes. These data suggest that metabolic demand of pregnancy was the most intense in the R/R ewes, intermediate for the C/C ewes, and least in the R/C ewes. It appears that fetal growth potential impacts maternal physiology and possibly increases mobilization of maternal body stores to meet fetal development nutrient demands. This response in fetal growth rate when embryos have been transferred to a divergent breed has also been reported in sows (Biensen et al., 1999) and cows (Ferrell, 1991a,b).
The level of dietary restriction imposed at d 50 of gestation did not impact the number of fetuses carried to d 130. Fetuses carried by restricted ewes were smaller than fetuses of the maintenance ewes, which is supported by McNeill et al. (1997), who observed a reduction in fetal lipid deposition owing to decreased maternal nutrient intake. When total fetal mass per ewe was analyzed, restriction had no effect.
Crown rump length was not different as a result of restriction, and it followed a similar pattern of individual fetal weight in Exp. 2, with the R/R group being the least, intermediate in R/C, and largest in C/C. A similar intermediate mass and CRL of the smaller growth-potential fetus in the larger BW maternal system was also observed when Charolais fetuses were carried by Brahman cows or Brahman fetuses carried by Charolais cows (Ferrell, 1991a). The intermediate fetal mass between prolific breeds and large-mature-body-size breeds has also been shown in pigs, with which Chinese Meishan embryos were implanted into Yorkshire uteri and Yorkshire embryos were implanted into Meishan uteri (Biensen et al., 1999). Mass and development response in these reports has been attributed to the placental mass, uterine blood flow, and nutrient exchange between the maternal and fetal compartments required for fetal growth. The mass of the late gestation fetus is determined by the type of fetus; however, the ability of that fetus to reach its full growth potential is limited to the ability of the maternal system to deliver essential substrates. Level of dietary restriction previously shown by Symonds et al. (1998) decreased placental weight but did not alter fetal weight. In an experiment described in a companion article, placental weight was decreased owing to dietary restriction (Arnold et al., 2001), whereas fetal weight was not different owing to restriction at d 90, but was less at d 130.
Lungs, Spleen, Heart, Liver, and Kidneys
The mass of the lungs in pregnant ewes was not different as a result of dietary restriction but decreased with advancing reproductive status. When scaled to EBW, the lungs contributed a smaller proportion to BW at d 90 and d 130 of reproductive status compared with nonpregnant. This difference was not different when expressed per unit of MBW. In Exp. 2, ewe type resulted in a difference in lung mass; however, when scaled to EBW or MBW, all treatments were similar. These observations indicate the necessity of the maternal tissues to maintain a threshold of functional mass to support the increased metabolic needs of conceptus development.
Spleen mass was decreased owing to restriction, and the nonpregnant ewes had larger spleens when compared with d 90 or 130. The spleen has been shown to decline in mass as a consequence of advancing gestation with no change in blood flow (Rosenfeld, 1977). In Exp. 2, the spleen was smaller owing to ewe type on a total mass basis and when expressed per unit of EBW or MBW. Johnson et al. (1985) demonstrated an increase in rabbit maternal BW without an impact on spleen mass. A similar lack of response in the spleen was also observed in a comparative serial slaughter trial in sows (Heap and Lodge, 1967).
As maternal metabolism adapts in response to pregnancy, maternal blood volume, cardiac output, stroke volume, and heart rate increase in order to deliver the nutrients and take away the waste products resulting from fetal development (Stock and Metcalfe, 1994; Magness, 1998). Heart mass was decreased by dietary restriction and was greater in nonpregnant ewes compared with d 90 or 130. When heart mass was scaled to EBW, nonpregnant was greater compared with d 90 or 130; however, when considered as a proportion to MBW, no difference owing to reproductive status was observed. An unexpected observation in this data set was that there seems to be a required level of functional cardiac tissue of 0.5 to 0.7% of BW when comparing the heart mass in ewes of such divergent body sizes in both experiments. It should be noted that going from 0.5 to 0.7% of BW is a large change (40%); however, this ratio of heart mass to EBW can also be calculated from other data sets, resulting in similar values (Robinson et al., 1978; Scheaffer et al., 2001).
The liver plays a pivotal role during adaptation of maternal metabolism to pregnancy, which is reflected through changes in mass and function. Freetly and Ferrell (1998a) have shown that hepatic oxygen consumption increases owing to ewes’ litter size. When ewes were fed a restricted diet (Robinson et al., 1978) of an energy concentration similar to that in the present study, liver mass was maintained late in pregnancy in comparison to the early gestation values. During pregnancy, liver sensitivity to dietary nutrient intake may be altered owing to nutrient demand of the gravid uterus. When dietary restriction was imposed in Exp. 1, results showed a decrease in liver mass in response to restriction (911.9 vs. 717.8 g), although when evaluated over pregnancy, liver mass increased. A similar response was present when liver mass was scaled to EBW and MBW. The difference of liver mass between the nonpregnant, d-90, and d-130 reproductive status was significant as a proportion of MBW. Experiment 2 also revealed that liver mass, when scaled to MBW, was greater in the R/R compared with R/C and C/C ewes. These data show that increased functional metabolic requirement and clearing of metabolic waste owing to pregnancy in the ewe results in an increase in hepatic tissue in proportion of MBW. This increase in hepatic tissue in proportion of MBW demonstrates that in ewes, metabolic demand (pregnancy) is reflected by adjustments in functional tissue mass whether that is a reduction in mass (lung, spleen, and omentum) to potentially conserve metabolic fuel or to increase level of functional tissue (liver or small intestine) to meet the metabolic priorities. These data seem to contradict an earlier report (Scheaffer et al., 2003) that indicated heifers had decreased energy use by small intestinal tissues in pregnant compared with nonpregnant. Additional research is needed to further define intestinal and total visceral responses to the metabolic demands of pregnancy.
Gastrointestinal Tract
The GI tract (Tables 5 and 9 for Exp. 1 and 2, respectively) and liver are responsible for a disproportionately high fraction of whole-body energy utilization (McBride and Kelly, 1990). When dietary intake is restricted to the level of limiting increases in body mass, the small intestine decreases in mass, which results in an overall decrease in energy use by the animal (Koong et al., 1985). In spite of this adjustment by the GI tract in the nonpregnant animal, the level of amino acid uptake by the gravid uterus remains similar to the pre-fast level during a 5-d fasting period (Battaglia, 1992). In the current data, an apparent required threshold of maternal organ mass is maintained in order to deliver the required nutrients to the gravid uterus.
The stomach complex was decreased owing to restriction and was less in nonpregnant compared with d-90 and d-130 ewes when scaled to MBW. In Exp. 2, R/R ewes had a greater stomach complex when expressed as g/kg of MBW. The stomach complex mass has been shown to be responsive to type of diet (Fluharty et al., 1999) and level of diet (Fluharty and McClure, 1997). This information validated the effectiveness of our dietary restriction treatment. Results of Exp. 2 demonstrate that the stomach complex is decreased, owing to decreased overall body mass, but the pattern when the stomach complex is scaled to MBW is reversed. This response of the stomach complex is another point, which demonstrates the apparent requirement of a threshold of functional tissue needed for successful metabolism during pregnancy to deliver a viable neonate. This interpretation of the stomach complex data results from the ewes of Exp. 2 having been fed the same diet; thus, when the mass of the stomach complex was scaled to MBW, R/R was greater when compared with R/C and C/C.
The omentum is a body cavity fat depot that lies over the rumen. It is a readily mobilized deposit of internal body stores in the pregnant ewe (Guesnet et al., 1991) and it was shown in the study that, from d 120 of gestation through early lactation, the omental fat depot was less lipogenic than during early pregnancy. In the present study, the decrease in mass was significant when d 130 was compared with d 90.
The contribution of the GI tract to whole-body metabolism is dramatic. According to Reeds et al. (1999), the fractional rate of protein turnover in intestinal tissues exceeds that of peripheral tissues in adults by as much as 30-fold. In a previous experiment in our laboratory (Scheaffer et al., 2001), responses of intestinal tissues to pregnancy in beef heifers were inconsistent and appeared dependent on stage of gestation and segment of the GI tract examined. In the present study, mass of the duodenum was not different as a result of dietary restriction, reproductive status, or ewe type when scaled to EBW or MBW. Duodenal mass scaled to EBW was greater in Romanov compared with the Columbia ewes. This difference was also observed in relation to MBW. Jejunum mass was decreased owing to restriction and increased with advancing reproductive status. Jejunal mass (grams per kilogram MBW) increased with advancing reproductive status. This increase was also observed in the R/R ewes compared with either the R/C or C/C ewes. The effect of ewe type resulted in a twofold increase in jejunal mass in proportion to MBW in Romanov compared with Columbia ewes. The jejunum adapts to increased fiber content of the diet by increasing epithelial cell turnover (Jin et al., 1994). The jejunum has also been shown to decrease in mass owing to a limited level of dietary intake (Burrin et al., 1990). The ileum displayed a response similar to that of the jejunum in Exp. 1 and was not affected by ewe type in Exp. 2. Patterns of response observed in the jejunum were similar to the results of the total small intestinal tissue. The intestinal mesentery was largely unaffected in the present experiments. The mesentery was less at d 130 compared with d 90 (grams per kilogram EBW); however, when analyzed as grams per kilogram MBW, the decrease was determined to be a result of the increased BW owing to the contribution of the gravid uterus.
The portal-drained viscera have been a focus of considerable research, and many experiments have focused on the absorption and metabolism of nutrients (Seal and Reynolds, 1993; MacRae et al., 1997; Freetly and Ferrell, 1998b). Current experiments indicate that digestive tract tissues increase in mass, proportional to MBW, owing to the metabolic requirement of ewes when dietary nutrients are not optimal. We are aware of only a few other reports that demonstrate an increase in mass ratio to BW as a result of dietary restriction. The literature contains evidence that portal-drained viscera or digestive tract mass decreases in metabolic rate (Huntington et al., 1988; Krehbiel et al., 1998) and proportion to BW (Ferrell and Koong, 1986) owing to decreasing levels of dietary intake. In contrast with these reports, Robinson et al. (1978) has shown a numerical increase in intestinal mass due to advancing gestation in ewes fed a restricted level of intake. However, in a majority of these cases, the overall body mass requiring nutrients is also less, responding to decreasing levels of intake. In contrast, the present experiments show that BW increases primarily because of the dramatic increase of the reproductive tract owing to expansion of the conceptus.
Large intestinal mass was not altered by dietary restriction. As seen in other tissues, the mass of the large intestine scaled to MBW was greater in the R/R ewes compared with the R/C and C/C. The mass of the metabolic machinery—total internal organ mass—was increased in response to reproductive status. In Exp. 2, the Romanov ewes had greater proportions of internal organ mass to EBW or MBW (Table 9).
Reeds et al. (1999) stated that the portal-drained viscera contributes 3 to 6% of BW, and the present experiments are within that range. In Exp. 2, the R/R ewes had a portal-drained viscera mass of 6.2%, whereas the C/C ewes had 3.6% expressed on a MBW basis. In Exp. 1, the range was 4.1 to 4.9% of MBW, increasing with advancing reproductive status. Accounting for the energetics of gestation has been an elusive task. Ferrell (1988) suggested that the energetic expenditures that were unaccounted for due to pregnancy could be explained by the requirement of maternal metabolism to increase service functions, the functions of metabolism that deliver the needed substrates for conceptus development. Kleiber (1975) suggested that metabolic rate of pregnancy in rats increased with gestation, but the increase was not completely explained by the metabolic rate of fetal or uterine tissue. This discrepancy may be explained by fetal mass proportional to MBW, which has been shown to be 23.1% in the rat (Battaglia and Hay, 1984). The ratio of gravid uterine mass to maternal mass in the rat is similar to the gravid uterine to maternal mass ratio observed in Exp. 2 of 28.2% (Table 7) and helps to clarify the basis for the wide range of responses in the maternal system of large animals. This observation may help explain why it has been difficult to quantify specific adjustments within maternal body in response to the gravid uterine development.
The conclusions from these data are that dietary restriction to 60% of maintenance imposed at d 50 of gestation is effective in decreasing fetal weight near term in the pregnant sheep. Restricted ewes lose BW; however, as reproductive status advances, the proportion of visceral organ mass and liver to EBW or MBW increases. The response of the R/R ewes was similar to the restricted ewes of Exp. 1, showing that the proportion of visceral organ mass to EBW or MBW is greater than in the R/C or C/C ewes. These results provide an indication that the discrepancy of the heat increment of gestation compared with that of the nonpregnant system (Brody, 1938) may be partially but not fully explained by service functions associated with splanchnic tissues (Ferrell, 1988).
Implications
Proportions of visceral organs increase with advancing reproductive status in pregnant ewes fed restricted or maintenance diets. These increases are indicative of the preservation of a functional tissue mass to support development of the conceptus. The comparison of dietary restriction vs. maintenance feeding and of small-framed prolific Romanov ewes vs. large-framed Columbia ewes resulted in a similar total fetal mass developing within each ewe type. Additional stresses placed on maternal metabolism to provide adequate substrates for optimal fetal growth may result in similar responses throughout the splanchnic tissues of the maternal system.
Footnotes
1 Gratitude is expressed to the NDSU Sheep Unit and the Animal and Range Sciences Physiology and Nutrition Laboratories for their valuable assistance with the project. 
2 Correspondence—phone: 701-231-7653; fax: 701-231-7590; e-mail: joel.caton{at}ndsu.nodak.edu.
Received for publication February 20, 2003. Accepted for publication February 11, 2004.
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