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J. Anim. Sci. 2004. 82:2548-2557
© 2004 American Society of Animal Science

ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION

Effects of feed restriction on reproductive and metabolic hormones in ewes

Z. Kiyma*, B. M. Alexander*, E. A. Van Kirk*, W. J. Murdoch*, D. M. Hallford{dagger} and G. E. Moss*,1

* Department of Animal Science, University of Wyoming, Laramie 82071; and and {dagger} Department of Animal and Range Sciences, New Mexico State University, Las Cruces 88003


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Literature Cited
 
The goal of this study was to determine the effects of short-term feed withdrawal on reproductive and metabolic hormones during the luteal phase of the estrous cycle in mature ewes. Mature ewes observed in estrus were assigned randomly to control and fasted groups (n = 10 per group Trials 1 and 2). For Trials 1 and 2, control ewes had ad libitum access to feed, whereas fasted ewes were not fed from d 7 through 11 of their estrous cycle; on d 12, all ewes were treated with 10 mg of PGF2{alpha}, and fasted ewes were gvien ad libitum access to feed. For Trial 1, blood samples were collected daily through fasting and at 2-h intervals following PGF2{alpha} for 72 h. Serum concentrations of insulin (P ≤ 0.002) and IGF-I (P ≤ 0.01), but not GH (P ≥ 0.60), were decreased during fasting compared with fed ewes. Serum concentrations of 29 (P = 0.02) and 34 kDa (P = 0.04) IGFBP were greater in fasted ewes at 96 h after initiation of fasting than in control ewes. Two control and four fasted ewes in Trial 1 did not exhibit a preovulatory surge release of LH by 72 h. Therefore, Trial 2 was conducted so that the timing of the LH surge could be predicted following the collection of blood samples at 2-h intervals for 112 h and then at 6-h intervals until 178 h following PGF2{alpha} administration and realimentation. The magnitude of the preovulatory LH surge in Trial 2 was decreased (P = 0.009) and delayed (P = 0.04), and serum concentrations of estradiol were diminished (P ≤ 0.03) 12 h before the LH surge in fasted ewes. Ovulation rates were not influenced (P ≥ 0.32) by fasting in Trials 1 and 2. Serum concentrations of progesterone in both Trials 1 and 2 were, however, greater (P < 0.001) in fasted than in control ewes. A third trial with ovariectomized ewes was conducted to determine whether the increased serum concentrations of progesterone observed in fasted ewes during Trials 1 and 2 were ovarian-derived. Ovariectomized ewes were implanted with progesterone-containing intravaginal implants and allotted to control (n = 5) or fasted (n = 5) treatment groups and fed as described for Trials 1 and 2. Similar to intact ewes, serum concentrations of progesterone were approximately twofold greater (P < 0.001) in fasted than in control implanted ovariectomized ewes. In summary, feed withdrawal for 5 d during the luteal phase of the estrous cycle increased serum concentrations of progesterone and evoked endocrine changes that could perturb the subsequent estrous cycle.

Key Words: Fasting • Ovulation Rates • Reproductive Hormones • Sheep


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Literature Cited
 
Effects of acute dietary restriction on reproduction in cows and ewes are not as clearly defined as those that occur in long-term nutrient-deprived ruminants or short-term nutrient-deprived nonruminants. Restriction of dietary energy to 0.4x maintenance for 13 to 15 d suppressed ovarian follicular development and resulted in anovulation in 60% of beef heifers (Mackey et al., 1999Go). Short-term feed deprivation decreased secretion of estradiol and LH in Syrian hamsters (Morin, 1986Go); LH, testosterone, and glucose in rhesus monkeys (Cameron et al., 1993Go; Cameron, 1994Go); and LH in prepubertal gilts (Foxcroft and Cosgrove, 1994Go) and milk-fed ovariectomized-prepubertal lambs (Foster and Olster, 1985Go; Foster et al., 1989Go). However, a similar effect has not been consistently demonstrated in mature ruminants. Adult sheep and cattle seem resistant to such nutritional restraints, perhaps due to ruminal nutrient reservoirs (Tatman et al., 1991Go). Fasting effects on the hypothalamic-pituitary-ovarian axis may be modulated by metabolic mediators, including glucose, insulin, GH, IGF-I, and IGFBP (Funston et al., 1995bGo). Limited feed resources can decrease reproductive efficiency to an extent dependent on the degree (Mackey et al., 2000Go) and reproductive status (Smith, 1988Go) at the time of feed restriction. Ovulation rate was decreased in protein-restricted (Smith, 1988Go) and fasted ewes (Killeen, 1982Go); an effect more pronounced when ewes were fasted during the luteal phase of the estrous cycle (Killeen, 1982Go). To further evaluate effects of limited feed availability, the current project was conducted to assess endocrine changes associated with fasting during the luteal phase of the estrous cycle preceding ovulation in mature ewes.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Literature Cited
 
Trial 1
Estrous cycles of 39 mature (≥3 yr old) Western White-Faced ewes in moderate body condition (BCS = 5 to 7; Sanson et al., 1993Go) were synchronized with two 10-mg doses of PGF2{alpha} (Lutalyse, Pharmacia & Upjohn Co., Kalamazoo, MI) on d 1 and 10. Estrous behavior was monitored in the presence of two vasectomized rams at 0600 and 1800 for 4 d following the second injection of PGF2{alpha}. Twenty ewes with synchronized estrous cycles were selected and randomly allotted to control (n = 10) or fasted (n = 10) groups. Ewes were housed by treatment in two separate, adjacent pens. Control ewes were given ad libitum access to good-quality grass hay throughout the experiment. Ewes in the fasted group were withheld from feed on d 7 through 11 of their estrous cycle (d 0 = first day of estrus). Ewes in both groups had ad libitum access to water. On d 12, all ewes were treated with 10 mg of PGF2{alpha}, and fasted ewes were returned to ad libitum feed. Ovulation rates were determined laparoscopically by counting CL present 13 d after realimentation and the administration of PGF2{alpha}. Daily blood samples were collected by jugular venipuncture 1 d before and during feed withdrawal. Additional blood samples were obtained at 2-h intervals for 72 h following PGF2{alpha} and realimentation, and then daily at 9, 12, and 14 d following realimentation. Serum concentrations of LH were determined in all samples. Serum concentrations of IGF-I, GH, and insulin were determined in samples collected 1 d before, daily during the 5 d of fasting, and then at 12-h intervals for 72 h and at 9, 12, and 14 d following realimentation. Concentrations of GH were calculated as a percentage of average pretreatment serum concentrations of GH (mean of two samples collected 24 h and just before the initiation of fasting) for each ewe. Relative quantities of IGFBP were determined in serum samples collected 1 d before fasting, at 96 h (d 4) of fasting, and 72 h after realimentation. Samples were analyzed using one-dimensional SDS-PAGE and 125I-IGF-I ligand blotting procedures (Clapper et al., 1998Go). Relative quantities of IGFBP are reported as a percentage of total 125I-IGF-I binding in each sample. Progesterone was monitored in samples collected 1 d before fasting, daily during the 5 d of fasting, and at 2, 4, 6, 8, 24, 48, 72 h and 9, 12, and 14 d after realimentation.

Trial 2
A replicate of Trial 1 was conducted because a proportion of the ewes in the fed and fasted groups did not exhibit a preovulatory surge release of LH by 72 h following administration of PGF2{alpha}. In Trial 2, ewes (n = 10 per group) were treated as in Trial 1, except that daily blood samples were collected 2 d before fasting and then at 2-h intervals until 112 h, at 6-h intervals until 178 h, and on d 10, 13, 16, 18, and 20 after realimentation. Serum concentrations of LH and FSH were assayed in samples collected 1 d before PGF2{alpha} and in all samples collected between 0 and 178 h following realimentation. Progesterone was monitored in samples collected daily from 2 d before and during the 5 d of fasting, at 2, 4, 6, 8, 10, 16, 24, 48, 72, 84, 96, 100 h, then at 6-h intervals until 178 h and at d 10, 13, 16, 18, and 20 following realimentation. Serum samples selected for analysis of estradiol were those samples that spanned the interval from PGF2{alpha} until 24 h after the preovulatory surge release of LH. Cortisol was quantified in morning samples collected 2 d before fasting, through fasting, and 2 d following realimentation and PGF2{alpha}. As in Trial 1, ovulation rates were determined laparoscopically by counting CL 13 d after realimentation and administration of PGF2{alpha}.

Trial 3
A third trial was conducted after it was discovered that serum concentrations of progesterone were increased by fasting in Trials 1 and 2. To determine whether the ovaries were the source of the increased serum progesterone, a single intravaginal progesterone-releasing device (InterAg, Hamilton, NZ) containing 0.3 g of progesterone was placed into each of 10 ovariectomized ewes. Two days after progesterone-releasing device insertion, ewes were equally allotted to control or fasted groups (n = 5 per group) and fed as described for Trials 1 and 2. Blood samples were collected twice daily for 2 d before feed restriction and during the 5 d of fasting. Following progesterone-releasing device removal and realimentation on d 5, blood samples were collected at 0, 30, 60, 90, 120 min, and at 4, 6, 8, 10, 12, 24, 36, 48, and 60 h. Progesterone was assayed in all samples.

Analytical Procedures
All blood samples were allowed to clot overnight at 4°C. Serum was separated by centrifugation at 1500 x g for 20 min. Serum samples were stored at –20°C until analysis. Samples were analyzed for concentrations of LH (Alexander et al., 1994Go), FSH (Bolt, 1981Go; Snyder et al., 1999Go), progesterone (Eggleston et al., 1990Go), estradiol (Field et al., 1990Go), GH (Hoefler and Hallford, 1987Go), IGF-I (Funston et al., 1995aGo), IGFBP (Clapper et al., 1998Go), and insulin (Reimers et al., 1982Go) as described previously. Inter- and intraassay CV, respectively, were 0.7 and 15.4% for progesterone, 4.7 and 5.5% for LH, 2.6 and 4.6% for FSH, and 7.6 and 8.0% for insulin. Samples were analyzed in single assays for GH, IGF-I, estradiol, and IGFBP, which had CV of 15, 9.5, 15, and 12.8%, respectively.

Cortisol was quantified utilizing a commercial RIA kit (Diagnostic Products Corp., Los Angeles, CA). Standards were prepared as doubling dilutions from 12.8 to 0.2 ng of cortisol (Sigma, St. Louis, MO) in 0.01 M PBS containing 0.1% (wt/vol) gelatin. Samples were analyzed in duplicate with 0.1 mL of serum, 0.4 mL of assay buffer, and 1 mL of the tracer solution. Tubes were incubated at room temperature for 3 to 4 h, decanted, and counted for 1 min in a gamma counter. Cross-reactivity reported by the manufacture was 0.03% for aldosterone, 0.94% for corticosterone, 0.98% for cortisone, and 0.02% for progesterone. Assay sensitivity was 0.5 ng/mL at 95% of maximum tracer binding. All samples were quantified in a single assay with an intraassay CV of 2.2% with 96% quantitative recovery of added cortisol.

One animal lacking a functional CL, as indicated by low (<1.0 ng/mL) serum concentrations of progesterone at the initiation of fasting, was removed from Trial 2.

All hormone and IGFBP data were analyzed by GLM procedures of SAS (Ver. 8.0, SAS Inst., Inc., Cary, NC). Effects of treatment were tested as the main effect for serum concentrations of progesterone, insulin, GH, IGF-I, IGFBP, LH, FSH, and estradiol with time and treatment x time interactions tested as subplot effects. Because of the dissimilar nature of the treatments (fed vs. fasted), ewe was considered the experimental unit in all trials. Animal within treatment was used as the error term for treatment effects. For all other effects, Type III sums of squares were used and least squares means and associated standard errors are reported. When significant (P < 0.05) effects were detected, differences between means were separated by PDIFF procedures of SAS. Ovulation rates were analyzed as a one-way ANOVA using GLM procedures of SAS.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Literature Cited
 
Ovulation Rates
Ovulation rates determined 13 d after realimentation and the administration of PGF2{alpha} in Trials 1 (P = 0.71) and 2 (P = 0.32) did not differ between control and fasted ewes (1.8 vs. 1.9 [± 0.2], and 1.9 vs. 1.6 [± 0.2] CL per control and fasted ewe for Trials 1 and 2, respectively).

Progesterone
Fasting increased (P < 0.001) serum concentrations of progesterone in all trials. In Trials 1 and 2, overall mean serum concentrations of progesterone in fasted ewes were 3.6 ± 0.2 and 2.4 ± 0.1 ng/mL, respectively, compared with 2.0 ± 0.2 and 1.6 ± 0.1 ng/mL for control ewes. The treatment x time interaction was significant (P < 0.001) for both studies. In Trial 1, serum concentrations of progesterone were greater (P < 0.001) in fasted than control ewes from 24 h after the initiation of fasting until 24 h after realimentation (P = 0.051; Figure 1AGo). In Trial 2, serum concentrations of progesterone were greater (P ≤ 0.01) in fasted than control ewes from 48 h after the initiation of fasting until 112 h (232 h of the experimental period) following realimentation (Figure 1BGo). In Trial 2, the interval required for serum concentrations of progesterone to decline to ≤0.75 ng/mL following the administration of PGF2{alpha} was longer (P = 0.01) for fasted than control ewes (102.0 ± 10.3 vs. 61.4 ± 9.8 h, respectively).



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  		Figure 1. Serum concentrations of progesterone for Trial 1 (A), Trial 2 (B), and Trial 3 (C). For all trials, concentrations of progesterone were affected (P < 0.001) by a treatment x time interaction. For Trials 1 and 2, ewes (n = 10 per group per trial) were fasted from d 7 to 11 (hour 0 to 120) of the estrous cycle (d 0 = first day of estrus). For Trial 3, intravaginal progesterone releasing devices (CIDR) were placed in ovariectomized ewes (n = 5 per group) and feed was withheld from fasted ewes for 5 d (hour 0 to 120). Note that units for the x-axis differ for Trial 3.

 
Ovariectomized ewes implanted with CIDR in Trial 3 had similar (P = 0.84) serum concentrations of progesterone (1.7 ± 0.1 ng/mL) before initiation of fasting. However, fasting increased (P < 0.001) overall serum concentrations of progesterone compared with control ewes (1.4 vs. 0.8 [± 0.05] ng/mL, respectively) in CIDR-treated ovariectomized ewes. The treatment x time interaction was significant (P < 0.001), and by 36 h after initiation of fasting, serum concentrations of progesterone were greater (P < 0.001) in fasted ewes and remained elevated (P < 0.002) until 36 h following CIDR removal and realimentation (Figure 1CGo).

Luteinizing Hormone
In Trial 1, two control and four fasted ewes did not exhibit a preovulatory surge release of LH by the time blood sample collection ceased at (72 h after PGF2{alpha}. In Trial 2, overall serum concentrations of LH did not differ (P = 0.58) between control and fasted ewes. One ewe from the fasted treatment group in Trial 2 did not have an identifiable surge release of LH. Of those exhibiting a surge release of LH, magnitudes of preovulatory surges of LH were less (P = 0.009) in fasted (35.5 ± 5.4 ng/mL) than in control (56.9 ± 4.8 ng/mL) ewes. In addition, the interval from administration of PGF2{alpha} to the preovulatory LH surge was longer (P = 0.04) in fasted (132.3 ± 14.1 h) than in control (89.4 ± 12.6 h) ewes (Figure 2AGo).



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  		Figure 2. Preovulatory surge concentrations of LH (Panel A) and FSH (Panel B) in control ewes and ewes fasted (n = 10 per group) from d 7 to 11 of the previous estrous cycle (Trial 2). Prostaglandin F2{alpha} was administered on d 12. Values presented are concentrations at specified hour following the administration of PGF2{alpha} and realimentation. Magnitude (P = 0.009; P = 0.007) and timing (P = 0.04; P = 0.04) of the LH and FSH surge, respectively, differed between control and fasted ewes.

 
Follicle-Stimulating Hormone
Similar to LH, overall serum concentrations of FSH in Trial 2 did not differ (P = 0.54), but magnitudes of FSH surges were lower (P = 0.007) in fasted (62.5 ± 4.6 ng/mL) than in control ewes (81.4 ± 4.1 ng/mL). The interval from administration of PGF2{alpha} to the FSH surge was also longer (P = 0.04) in fasted (132.3 ± 14.1 h) than in control (89.4 ± 12.6 h) ewes (Figure 2BGo).

Estradiol 17-ß
Overall serum concentrations of estradiol in Trial 2 did not differ (P = 0.91) in control and fasted ewes, but were influenced (P = 0.01) by a treatment x time interaction (Figure 3Go). When estradiol data were examined based on hours before the preovulatory surge release of LH, mean serum concentrations of estradiol were lower (P ≤ 0.03) during the 12 h immediately preceding the LH surge in fasted than in control ewes.



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  		Figure 3. Serum concentrations of estradiol-17ß preceding the preovulatory surge release of LH in control ewes and ewes fasted (n = 10 per group) from d 7 to 11 of the previous estrous cycle (Trial 2). Prostaglandin F2{alpha} was administered on d 12, and data were realigned based on time of maximal LH release. Concentrations of estradiol differed (P = 0.01) by a treatment x time interaction and were greater (P ≤ 0.03) in control vs. fasted ewes during the 12 h immediately preceding the LH surge, which occurred at 89.4 ± 12.6 or 132.3 ± 14.1 h in control and fasted ewes, respectively.

 
Growth Hormone
Serum concentrations of GH in Trial 1 varied greatly among individual animals; therefore, concentrations were expressed as a percentage of pretreatment values within each animal. Serum concentrations of GH were not influenced by treatment (P = 0.94), but did differ by time (P < 0.001) and treatment x time interaction (P = 0.04). In both groups, overall serum concentrations of GH were greater (P ≤ 0.05) at 60 and 70 h and at d 9 after administration of PGF2{alpha} compared with concentrations before initiation of fasting (131.0, 142.4, and 129.9 ± 8.9%, respectively). Serum concentrations of GH did not differ (P ≥ 0.60) between treatment groups during fasting, but the increase at 60 h following PGF2{alpha} and realimentation was more (P = 0.005) pronounced in fasted than control animals (156.2 vs. 105.8 ± 12.5%, respectively). Concentrations of GH were decreased (P = 0.006) in fasted ewes 12 d following PGF2{alpha} and realimentation compared with control ewes (77.3 vs. 126.6 ± 12.5%, respectively).

Insulin
Serum concentrations of insulin in Trial 1 were influenced (P < 0.001) by a treatment x time interaction (Figure 4AGo). Fasting decreased (P ≤ 0.002) serum concentrations of insulin from 24 h of fasting until realimentation. Following realimentation, concentrations did not differ (P = 0.65) between fasted and fed ewes by 12 h (Figure 4AGo).



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  		Figure 4. Serum concentrations of insulin (Panel A) and IGF-I (Panel B) in control ewes and ewes fasted (n = 10 per group) from d 7 to 11 of the estrous cycle in Trial 1. Concentrations of insulin and IGF-I differed (P < 0.001) by the treatment x time interaction.

 
Insulin-Like Growth Factor-I
Serum concentrations of IGF-I in Trial 1 were influenced (P < 0.001) by a treatment x time interaction. After 48 h of fasting, serum concentrations of IGF-I decreased (P = 0.01) in fasted ewes and remained lower (P ≤ 0.02) than in control animals until 72 h following realimentation (Figure 4BGo).

Insulin-Like Growth Factor Binding Proteins
Relative quantities of IGFBP were determined in Trial 1. All IGFBP, except 28 kDa (IGFBP-4), differed (P ≤ 0.004) by time (data not shown). Binding proteins 1 and 2 (29 and 34 kDa, respectively) were affected by a treatment x time interaction (P ≤ 0.02; Table 1Go). At 96 h of fasting, fasted ewes had increased (P ≤ 0.04) relative quantities of IGFBP-1 and -2 than control ewes. Relative quantities of IGFBP-1 and -2 did not differ (P ≥ 0.08) between fasted and control animals before fasting or following realimentation.


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  		Table 1. Relative abundance of IGFBP in serum of control ewes and ewes fasted (n = 10 per group) from d 7 through 11 of the estrous cycle in Trial 1
 
Cortisol
Serum concentrations of cortisol did not differ (P = 0.17) by treatment (21.8 vs. 18.3 [± 1.7] ng/mL for control and fasted ewes, respectively). There was a trend for a treatment x time interaction (P = 0.06). Serum concentrations (ng/mL) of cortisol in fasted ewes were increased (P = 0.03; 19.0 vs. 7.7 [± 3.6]) at d 2 of fasting, but were decreased (P = 0.02) at d 5 of fasting compared with fed ewes (34.7 vs. 46.7 [± 3.6], respectively; data not shown). Serum concentrations of cortisol did not differ (P > 0.05) between fasted and fed ewes at any other time period.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Literature Cited
 
Ovulation rate in ewes can be influenced by nutrition (Botkin et al., 1988Go; Dunn and Moss, 1992Go). Ewes on a high-protein diet had greater ovulation rates than those on a low-protein diet (Smith, 1988Go). In addition, ewes fasted during the luteal phase of the estrous cycle had reduced ovulation rates (Killeen, 1982Go). In both replicates of the current experiment, however, ovulation rates did not differ between control and fasted ewes. Reasons for the seeming contradiction from the results of Killeen (1982)Go and Smith (1988)Go are not readily evident, but could be due to differences in breed, time of year, age, or nutritional status of the ewes (Botkin et al., 1988Go).

Serum concentrations of progesterone were higher during fasting in Trials 1 and 2 and remained elevated longer following administration of PGF2{alpha} and realimentation in Trial 2 than in fed ewes. Increases in serum concentrations of progesterone were also noted in response to feed restriction in sheep (Williams and Cumming, 1982Go; Parr, 1992Go), pigs (Dyck et al., 1980Go; Miller et al., 1999Go), and cattle (Rabiee et al., 2001Go). Feed restriction may have altered the metabolic clearance of progesterone (Parr et al., 1993bGo; Freetly and Ferrell, 1994Go) because fasting also increased serum concentrations of progesterone in ovariectomized ewes provided with an exogenous source of the hormone (Trial 3). Increased serum concentrations of progesterone were noted in hypophysectomized, ovariectomized ewes treated with exogenous adrenocorticotropin (De Silva et al., 1983Go). However, because treatment differences in serum concentrations of cortisol were not noted in the current study, differences in progesterone are not likely a result of increased adrenal synthesis of progesterone. Hepatic portal blood flow was directly related to the level of feed intake in sheep (Parr et al., 1993aGo). Although the decrease in serum concentrations of progesterone following treatment with PGF2{alpha} and realimentation seemed to be more abrupt in Trial 1 than in Trials 2, the frequency of sample collection in Trial 2 was greater and may more clearly depict progesterone clearance (or alternatively, may indicate prolonged residual CL activity in fasted ewes).

The magnitude of the preovulatory surge release of LH and FSH was diminished by fasting in ewes. Chronic undernourishment of ewes decreased serum and hypophyseal concentrations of LH (Kile et al., 1991Go; Snyder et al., 1999Go) and FSH (Kile et al., 1991Go) due to a suppressed release of GnRH from the hypothalamus (Kile et al., 1991Go; I’anson et al., 2000Go). Feed restriction decreased GnRH pulse frequency, amplitude, and the ability of low-amplitude GnRH pulses to generate a concomitant LH pulse in ovariectomized lambs (I’anson et al., 2000Go). The decreased magnitude of LH and FSH secretion may also be related to decreased serum concentrations of IGF-I and insulin noted in fasted ewes. Basal secretion of LH was enhanced by IGF-I in cultured pig pituitary cells (Barb et al., 2001Go). Also, IGF-I and, to a lesser extent, insulin, stimulated GnRH-induced LH secretion in cultured rat pituitary cells (Soldani et al., 1995Go), an action that was potentiated by estradiol (Xia et al., 2001Go).

The delayed preovulatory surge release of LH and FSH in fasted ewes was associated with a prolonged interval for serum concentrations of progesterone to decline to basal levels after treatment with PGF2{alpha}. This interval was approximately 41 h longer in fasted than in control ewes. Because the preovulatory LH surge also occurred about 43 h later in fasted vs. control ewes, the delayed surge-release of gonadotropins in fasted ewes was probably caused by prolonged negative feedback effects of progesterone on the secretion of GnRH (Turzillo and Nett, 1999Go).

Serum concentrations of estradiol were lower in fasted than in fed ewes during the 12 h immediately preceding the LH surge. Similarly, circulating concentrations of estradiol were decreased following short-term feed deprivation in Syrian hamsters (Morin, 1986Go) and rats (Oukonyong et al., 2000Go). Decreased concentrations of estradiol in serum may result from diminished ovarian follicular development caused by suppressed serum concentrations of gonadotropins (Gougeon, 1996Go). Insulin like growth factor-I, which was suppressed by fasting in the current study, enhanced FSH-stimulated production of estradiol in rat granulosa cells (Duggal et al., 2002Go) and may be important for maintenance of FSH-stimulated production of estradiol.

Feed restriction did not affect overall or serum concentrations of GH during fasting in the current study. However, concentrations of GH in serum increased during the proestrus following administration of PGF2{alpha} in both groups of ewes. Landefeld and Suttie (1989)Go reported that increases in both mRNA and serum concentrations of GH occurred during the follicular phase of the estrous cycle and in response to exogenous estradiol in ewes. The lack of an effect of fasting on GH secretion contrasts with results obtained in chronically feed-restricted ewes (Foster et al., 1989Go; Kile et al., 1991Go), young steers (Breier et al., 1986Go), and chronically and acutely dietary restricted humans (Thissen et al., 1994Go), and may be due to the frequency of sampling in the current study.

Serum concentrations of insulin were lower in fasted than in control ewes from the first day of fasting until 12 h after realimentation. Mean serum concentrations of insulin were likewise decreased in feed restricted heifers (McCann and Hansel, 1986Go; Spicer et al., 1992Go; Amstalden et al., 2000Go) and gilts (Whisnant and Harrell, 2002Go). Acute fasting of dairy heifers between d 8 and 16 of the estrous cycle decreased serum concentrations of insulin from 12 h of fasting until 12 h following refeeding (McCann and Hansel, 1986Go).

Nutritional influences on reproduction may be linked through variations in the IGF-I system (IGF-I and IGFBP) secreted from the liver or present in other reproductive tissues (Roberts et al., 2001Go). Serum concentrations of IGF-I were decreased by fasting and did not return to concentrations comparable to control ewes until 3 d after realimentation. Similar effects were noted in sheep (Oldham et al., 1999Go) and lactating dairy cows (Kobayashi et al., 2002Go). It is generally accepted that IGF-I is produced in response to GH interacting with the GH-receptor in the liver (Etherton and Bauman, 1998Go). In acute feed-restricted growing steers, however, the IGF-I response to bovine GH administration was abolished (Breier et al., 1988Go). Minegishi et al. (2000)Go found that expression of the FSH-receptor was enhanced when IGF-I was added to granulosa cell culture medium along with FSH. Thus, acute nutrient restriction to the point of decreasing IGF-I secretion may affect the ability of developing follicles to respond to FSH through a reduction in FSH-receptor expression.

Serum concentrations, activity, and plasma half-life of IGF-I can be regulated by IGFBP (Thissen et al., 1994Go). Similar to Osborn et al. (1992)Go and Oldham et al. (1999)Go, relative quantities of the 29-kDa IGFBP (presumably IGFBP-1; Snyder et al., 1999Go) and IGFBP-2 were increased in fasted ewes compared with controls at 96 h of fasting. Complexes of IGF-I with IGFBP-1 or –2 can cross the capillary endothelium and may have a role in delivery of IGF-I to tissues (Thissen et al., 1994Go). In ewes fasted for 3 d during late gestation, plasma levels of IGFBP-1 and IGFBP-2 were increased; an effect reversed after 3 d of refeeding and prevented by infusion of glucose during fasting (Osborn et al., 1992Go). In the current study, decreased relative quantities of serum IGFBP-1 and -2 in fasted ewes may be related to presumably lower concentrations of glucose. Funston et al. (1995b)Go also reported a numeric increase in serum 29-kDa IGFBP (presumably IGFBP-1) following treatment with 2-deoxyglucose in ewes.

In conclusion, acute nutrient restriction (i.e., fasting) during the luteal phase of the estrous cycle evoked endocrine changes that influenced timing of the ensuing LH surge and presumably ovulation.

1 Correspondence: Dept. 3684, 1000 E. University Ave. (phone: 307-766-5374; fax 307-766-2355; e-mail: gm{at}uwyo.edu).

Received for publication March 4, 2004. Accepted for publication May 27, 2004.


   Literature Cited
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Literature Cited
 


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