ANIMAL

REPRODUCTION
SCIENCE
ELSEVIER Animal ReproductionScience 40 (1995) 229-238

Dietary protein or energy restriction influences age

and weight at puberty in ewe lambs
B. Boulanouar 1, M. Ahmed 2, T. Klopfenstein, D. Brink,
J. Kinder *
Department of Animal Science, University of Nebraska, Lincoln, ArE 68583-0908, USA

Accepted 16 June 1995

Abstract

The working hypothesis was that restricted protein content in diets of prepubertal ewe lambs
would delay time of onset of puberty to a greater extent than restricted energy content. Restriction
of dietary protein (metabolizable protein, MP) or energy (ME) intake on age and weight at puberty
was studied in ewe lambs in two experiments. In Experiment 1, 85 crossbred ewe lambs were
assigned by weight to one of five dietary treatment groups: control (CTL; 18 mg ME day-~ and
173 g MP day-l); energy restricted (ER; 10.2 mg ME day -1 and 96 g MP day-l); protein
restricted (PR; 11 mg ME day-i and 66 g MP day- I); ER for 9 weeks "then switched to CTL
(ER/CTL); PR for 9 weeks then switched to CTL (PR/CTL). Ewe lambs were weighed
biweekly, bled weekly, and serum was assayed for progesterone to determine time of puberty.
Average age at puberty differed among lambs fed the various diets (P < 0.01). Ewe lambs in the
CTL group were younger and weighed more at puberty. Lambs fed diets restricted in protein or
energy content were similar in age at puberty. Dietary switching, ER/CTL and PR/CTL, affected
body weight and gain (P < 0.05), but did not result in changed age at puberty compared with
lambs fed ER or PR diets. In Experiment 2, two breed types (maternal type and meat type) were
used to compare responses of dietary protein restriction to dietary energy restriction. In Experi-
ment 2, lambs (n = 60) were assigned to either the CTL, PR or ER diets. Lambs in the CTL group
gained more weight than lambs fed the PR diet and lambs fed the PR diet gained more weight
than lambs fed the ER diet (P < 0.05). Diet affected age (P < 0.001), but not weight at puberty
(P = 0.13). Dietary energy and protein restriction influenced age at puberty in ewe lambs with
energy restriction having a greater influence on delaying onset of puberty than protein restriction.
Realimentation did not overcome effects of previous feed restriction by inducing an earlier age at

* Correspondingauthor: Tel(402) 472-6438: Fax (402) 472-6362.

Present address: INRA B.P. 290 Settat, Morocco.
2 Present address: Faculty of Agriculture, Minia University,Egypt.

0378-4320/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved

SSD1 0378-43 20(95)01420-9
230 B. Boulanouar et al./Animal Reproduction Science 40 (1995) 229-238

puberty than ewe lambs fed the ER or PR diet throughout the experimental period. Body weight
gain prepuberty is more important than type of dietary restriction (protein or energy) with regard
to impacting age at puberty. We, therefore, reject the working hypothesis that dietary protein
restriction prepuberty would have a greater impact in delaying onset of puberty than dietary
energy restriction,

Keywords: Sheep; Dietaryrestriction;Protein;Energy;Puberty

1. Introduction

One way of enhancing reproductive performance of female sheep is through extend-

ing lifetime productivity. Age at puberty and age at first lambing are important traits
concerning overall reproductive performance. While the endpoint used to define puberty
is a discrete point in time, the process of sexual maturation occurs gradually during the
pre-, peri- and postpubertal periods. Studies of physiological processes relating to
puberty in a number of species have provided evidence regarding the influence of
dietary intake on sexual maturation. Hafez (1952) suggested that a minimum body
weight was critical for first ovulation to occur in ewe lambs. Lambs reared on a high
plane of nutrition have increased uterine and pituitary weight and more marked thyroid
development (Allen and Lamming, 1961); however, there is no clear effect of a single
nutritionally related blood metabolite on processes of sexual maturation (Schillo, 1992).
Different factors (body fat, insulin, non-esterified fatty acids, amino acids, and availabil-
ity of metabolic fuel such as glucose) may interact to regulate secretion of hormones that
modulate age at puberty (Schillo, 1992).
In previous studies where the influence of restriction of dietary content of protein and
energy on reproductive processes have been compared, protein status has been defined
in terms of crude or digestible protein. Protein deficiencies in ruminants are frequently
accompanied by altered ruminal energy metabolism. Restriction of protein intake should,
therefore, be established in terms of metabolizable protein and not crude or digestible
protein to avoid complications of energy and protein interactions (Drouillard et al.,
1991). The working hypothesis in the present study was that restricted protein content in
diets of prepubertal ewe lambs would delay time of onset of puberty to a greater extent
than restricted energy content. In the present study, therefore, two experiments were
conducted to evaluate effects of metabolizable protein or energy restrictions and
realimentation on body weight gain, age at puberty, and weight at puberty.

2. Materials and methods

2.1. Animals and dietary content

The purpose of Experiment 1 was to evaluate effects of restriction of dietary energy

or metabolizable protein on age and weight at puberty. Ewe lambs ( 1 / 2 Finnish
Landrace 1 / 4 Dorset 1 / 4 Rambouillet; n = 85) were stratified by weight and randomly
 B. Boulanouar et a l . / Animal Reproduction Science 40 (1995) 229-238 231

allotted to one of five treatment groups: control (CTL), low energy (ER), or low protein
(PR). Ewe lambs in the two other groups were fed the PR or ER diet for 9 weeks and
were subsequently switched to the CTL diet ( P R / C T L and E R / C T L , respectively) for
the rest of the experiment. Experiment 1 was initiated in early September 1989 and
terminated in August 1990. Ewe lambs were born during the last week of May and
weaned in early July. Lambs weighed 22.1 + 1.9 kg and were 106 + 1.3 days of age at
the start of Experiment 1.
To broaden the comparison of influence of dietary protein and energy restrictions
during prepuberty on age when puberty is attained, ewe lambs of two breed types
(maternal type and meat type) were utilized in Experiment 2. Prepubertal ewe lambs
(n = 60) were stratified by weight and breed type and randomly assigned to the three
groups (CTL, PR or ER). Lambs were of 1 / 2 Suffolk or Hampshire, 1 / 4 Finnish
Landrace, 1 / 8 Dorset, 1 / 8 Rambouillet, (maternal type, n = 18) or Suffolk or Hamp-
shire (meat type, n = 42) breeding. Lambs weighed 35.5 _+ 0.6 kg and were 131 + 1.5
days of age at initiation of the experiment (June 1991). As ewe lambs attained puberty,
they were removed from the experiment and feed allowance adjusted for the remaining
animals.

2.2. Dietary formulations

Dietary formulations were the same in both experiments. Pelleted diets (Table 1)
were fed to groups of lambs in indoor pens once daily to achieve a daily gain two times
greater in the control group compared with restricted groups. The groups had adequate
bunk space for all ewe lambs to consume feed at the same time.
Basal portions of diets deficient in energy and protein were comprised of corn cobs,
which were low in both energy and protein (2.8% crude protein and 48% total digestible
nutrients). It was, therefore, possible to prepare diets first-limiting in one primary
nutrient (protein or energy) by supplementing the opposite nutrient. The energy re-
stricted diet contained a mixture of feather meal and blood meal (62% and 80.6% escape
protein, respectively; Wilkerson et al., 1993) to ensure that energy, rather than metabo-
lizable protein was limiting. Blood meal and feather meal were mixed with small
amounts of molasses to enhance palatability. Molasses was added to the protein
restricted diet as a source of supplemental energy. Urea was also included in quantities
sufficient to allow for adequate microbial protein synthesis and body weight gain from
energy present in the diet. As a result, metabolizable protein content of the diet restricted
in protein was limited to that provided by the basal portion of the diet plus that of
microbial origin.

2.3. Blood sampling

Experimental protocols used in the two experiments were approved by the Institu-
tional Animal Care and Use Committee. Prior to feeding, lambs were bled weekly via
the jugular vein by repeat venipuncture and weighed bi-weekly during the 344 day
(Experiment 1), and 177 day feeding period (Experiment 2). Blood samples were
allowed to clot on ice and stored for 24 h at 4°C. Serum was harvested from these
232 B. Boulanouar et al. / Animal Reproduction Science 40 (1995) 229-238

Table 1
Composition of diets, percent total digestible nutrients (% TDN), percent crude protein (% CP) and percent
metabolizableprotein (%MP) on a dry matter (DM) basis
Ingredients Control Low energy Low protein
Alfalfa 46.6 - -
Soybean hulls - 33.7 55.9
Corn grain, rolled 49.4 - -
Corncobs - 52.4 34.9
Feather meal 0.3 2.4 -
Blood meal 0.3 2.4 -
Urea 0.2 1.0 1.0
NaC1 0.26 0.27 0.27
Dicalciumphosphate 0.13 0.85 0.82
Trace mineral a 0.04 0.04 0.04
Se premix b 0.01 0.01 0.01
Molasses 2.6 6.9 6.9
DM intake,kg c 1.59/1.69 1.12/1.17 1.12/1.17
% TDN 75 60 65
% CP 15.0 13.5 11.4
% MP d 10.9 8.6 5.9
MP intake, g d-1 c 173/184 96/110 66/79
ME intake, MJ d -1 c 18.0/19.1 10.2/12.0 11.0/12.9
a 10% Mg, 6% Zn, 4.5% Fe, 2% Mn, 0.5% Cu and 0.3% I.
b 0.06% Se.
c Indicates an adjustment in intake on 8 October 1993. Starting that same day, the restricted ewe lambs
received an additional0.11 kg per lamb day-l of soybeanhulls (85% IVDMD and 5% CP).
d Calculated(Burroughs et al., 1975).

samples after centrifugation at 10 000 × g for 20 min and stored at - 20°C until assayed
for progesterone. Concentrations of progesterone in serum samples were determined by
radioimmunoassay (Roberson et al., 1989). Sample volumes of 200 /zl were extracted
with benzene:hexane with 90% recovery of sample during extraction and values reported
were corrected for extraction losses.
In Experiment 1, intra-assay coefficient of variation was 3.9%. Sensitivity of the
progesterone assay averaged 35 pg m1-1 . In Experiment 2, the intra-assay coefficient of
variation was 3.2%. Concentration of progesterone in aliquots from two serum pools
were determined in each assay. Mean concentration of progesterone for these pools were
1.27 and 3.93 ng ml -~. The intra-assay coefficient of variation for these pools was
11.1%. Sensitivity of the assays averaged 2.88 pg per tube. Day when increased
progesterone was detected indicating initiation of corpus luteum function subsequent to
the pubertal ovulation was used as the indicator of attainment of puberty and was
determined based upon concentrations of progesterone _> 1 ng ml-1 of serum for two
consecutive sampling dates. In Experiment 2, five ewe lambs from the restricted groups
did not attain puberty by termination of the experiment. The date of termination of the
experiment was recorded as the puberty date for these five animals. Some lambs (one in
CTL, five ER and four in PR groups which left 50 lambs to be included for experimental
 B. Boulanouaret al./ Animal Reproduction Science 40 (1995) 229-238 233

analyses) were removed from the experiment for health reasons, before they attained
puberty. Their data were discarded from the analyses.

2.4. Statistical analyses

Data from Experiment 1 were analyzed to evaluate effect of dietary treatment on rate
o f weight gain, body weight at puberty and age at puberty. Data from Experiment 2
were analyzed to test the main effect of diet and breed type and their interaction on body
weight gain, age at puberty and weight at puberty. All statistical analyses were done
using G L M procedures (Steel and Torrie, 1980; Statistical Analysis Systems Institute
Inc,, 1985). Differences between means were determined by Fishers Least Significance
test (Steel and Torrie, 1980). Chi square analysis was used to evaluate when differences
existed in number of lambs that had attained puberty among treatment groups (Steel and
Torrie, 1980).

3. Results

3.1. Experiment 1

Average age and weight were similar across groups at initiation of the experiment
( P > 0.05). All lambs attained puberty by the end of the experiment. Lambs fed the
control diet gained weight at a greater rate and were 4 kg heavier at puberty than lambs
fed either PR or ER diets (Table 2). Control lambs attained puberty 17 days earlier than
those fed the E R diet. There was no difference in age at puberty between ewe lambs in
the control and protein restricted groups ( P > 0.10; Table 2). Switching from the
restricted to control diets resulted in a change in rate of gain ( P < 0.05) but did not
result in a changed age at puberty compared with lambs fed ER or PR diets throughout
the entire experimental period.

Table 2
Initial age, initial body weight, body weight gain, weight at puberty and age at puberty of lambs fed the five
diets (Experiment 1)
Variables Diets a SEM b
CTL ER PR ER/CTL PR/CTL
Number of lambs 17 17 17 17 17 17
Initial age (days) 105 106 104 106 108 1.3
Initial weight (kg) 22.0 21.8 22.3 22.4 22.2 1.9
Body weight gain (g gaily) 186 c 107 d 104 d 155 ~ 177 ccd 6.0
Age at puberty (days) 169 c 186 d 178 cd 181 179 5.2
Weight at puberty (kg) 35.3 e 30.6 ~ 31.5 c 32.6 ~d 33.6 de 1.0
a CTL, fed control diet; ER, energy restricted diet; PR, protein restricted diet; ERfCTL, energy restricted diet
then switched to control diet; PR/CTL, protein restricted diet then switched to control diet.
b Pooled standard error of the mean.
c,d,e Means within the same row with unlike superscript differ P < 0.05.
234 B. Boulanouar et al./Animal Reproduction Science 40 (1995) 229-238

Table 3
Initial age, initial body weight, body weight gain, weight at puberty and age at puberty in lambs of two breed
types (Experiment 2)
Variable Maternal type a Meat type a SEM b
Number of lambs 18 32
Initial age (days) 129 c 134 d 1.5
Initial BW (kg) 33.7 36.0 0.6
Body weight gain (g daily) 112 ¢ 121 d 8
Weight at puberty (kg e) 43.1 ¢ 46.9 d 1.2
Age at puberty (days e) 224 c 246 d 4

a Maternal type: 1 / 2 Suffolk or Hampshire 1 / 4 Finnish Landrace 1 / 8 Dorset 1 / 8 Rambouillet; meat type:
Suffolk or Hampshire.
b Pooled standard error of the mean.
c,d Means within the same row with unlike superscript differ P < 0.05.

3.2. Experiment 2

There was no interaction between diet and breed type on age and weight at puberty.
Differences in live weight among lambs fed the CTL diet and lambs fed diets restricted
in protein or energy were greater as the experimental period progressed. Body weight
gain of ewe lambs fed the CTL diet was greater than that of ewe lambs fed restricted
diets ( P < 0.05; 3.1 and 2.4 times greater than that of ewes from the ER and PR groups,
respectively).
At the start of Experiment 2, lambs of the two breed types had similar weights
( P > 0.10) but meat type ewe lambs gained faster than maternal type ewe lambs during
the experiment. Breed type had an effect on both age ( P < 0.001) and weight ( P < 0.05)
at puberty. Even though ewe lambs of the maternal breed type had a slower rate of gain,
they attained puberty 22 days earlier and at a 3.8 kg lighter weight than ewe Iambs of
the meat type (Table 3). The influence of dietary protein or energy restriction was the
same for both breed types with age at puberty being delayed compared with lambs in the
CTL group with both breed types. Diet affected age but not weight at puberty in
Experiment 2. Ewe lambs in the CTL group reached puberty 54 and 37 days earlier

Table 4
Initial age, initial body weight, body weight gain, weight at puberty and age at puberty of lambs fed the three
diets (Experiment 2)
Variable CTL ER PR SEM a
Number of lambs 19 15 16
Initial age (days) 132 130 133 1.9
Initial body weight (kg) 35.0 35.5 35.5 0.7
Body weight gain (g daily) 197 b 62 c 81 d 10
Weight at puberty (kg) 46.8 44.1 44.3 1.4
Age at puberty (days) 205 b 259 ¢ 242 d 5

a Pooled standard error of the mean.

b,c,d Means within the same row with unlike superscript differ P < 0.05.
 B. Boulanouar et a l . / Animal Reproduction Science 40 (1995) 229-238 235

Table 5
Cumulative number and percentage of ewe Iambs attaining puberty over time of lambs fed three diets
(Experiment 2)
Week Control Low energy Low protein p a
Number % Number % Number %
7 0 0 0 0 0 0 0.011
8 1 5.3 0 0 0 0 0.001
9 2 10.6 0 0 0 0 0.001
10 2 10.6 0 0 0 0 0.001
11 4 21.1 0 0 1 6.3 0.001
12 10 52.7 0 0 2 12.6 0.001
13 16 84.3 0 0 2 12.6 0.001
14 16 84.3 0 0 2 12.6 0.01
15 17 89.6 3 20 4 25.1 0.01
16 18 94.9 3 20 7 43.8 0.71
17 19 100 3 20 11 68.8 0.24
18 - - 5 33.3 11 68.8 0.01
19 - - 5 33.3 11 68.8 0.01
20 - - 6 40 11 68.8 0.001
21 - - 11 73.4 14 87.5 0.001
22 - - 13 86.7 14 87.5 0.001
23 - - 14 93.4 15 93.7 0.001
24 - - 15 100 16 100 0.38

Total 19 100 15 100 16 100

a Chi-square P value.

(P < 0.001) than the lambs fed the ER and PR diets, respectively. Likewise, lambs fed
t h e P R d i e t a t t a i n e d p u b e r t y e a r l i e r t h a n l a m b s f e d t h e E R d i e t ( P < 0 . 0 5 ; T a b l e 4).
Cumulative numbers and proportions of ewe lambs that attained puberty are reported
in T a b l e 5 a n d F i g . 1. D a t a f r o m t h e C h i - s q u a r e t e s t f o r d i f f e r e n c e s i n p r o p o r t i o n o f e w e

C vs ER and PR (P<.05)
10o ER vs PR (P<.05) Control

Ill 80 ~ • /'"
"" , ...............:" ..-'" Low energy
OG"t': 60 ~ i "*'~
19
11.

~" 20 ""

7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

Weeks
Fig. 1. Cumulative percentage of ewe lambs attaining puberty when fed three different diets (Experiment 2).
236 B. Boulanouar et al./ Animal Reproduction Science 40 (1995) 229-238

lambs attaining puberty are also included in Table 5. Dietary effects on age at puberty
were first detected 7 weeks after the start of the experiment, when control lambs started
to attain puberty. Lambs in the PR group started to attain puberty 4 weeks after CTL
lambs. Ewe lambs in the ER group started to attain puberty 4 weeks after those in the
PR group. Ewe lambs from the CTL group attained puberty at an average age of 205
days (7 weeks and 5 weeks earlier than lambs in the ER and PR groups, respectively).
When data from ten ewe lambs in the ER and PR groups with similar weight gains were
analyzed with the same statistical model, the analysis indicated that neither age
( P = 0.51) nor weight ( P = 0.62) at puberty were affected by type of dietary restriction.

4. Discussion

Rapidly growing animals (CTL) achieved puberty earlier and at heavier weights than
animals growing at a slower rate (lambs fed PR or ER diets) in Experiment 1. This is
consistent with previous findings (Allen and Lamming, 1961; Burfening et al., 1971;
Keane, 1975; Quirke, 1979). These results are not consistent with the 'minimum body
weight' concept which was previously suggested for ewe lambs (Hafez, 1952; Dyr-
mundsson, 1981). Unlike what occurred in Experiment 1, diet had an effect on age but
not weight at puberty in Experiment 2, which suggests that weight was critical to onset
of puberty in ewe lambs in this experiment. Data analysis for ewe lambs of similar
growth rate indicated that effect of dietary restriction may depend on growth rates
achieved rather than type of dietary restriction (energy vs. metabolizable protein).
Lambs used in Experiment 2 were older and heavier at initiation of the experiment
than those used in Experiment 1. Weight gain in control lambs was 1.8 and 1.8 times in
Experiment 1 and 3.2 and 2.4 times greater than lambs in the ER and PR groups,
respectively, in Experiment 2. These differences may explain why dietary restriction
affected weight at puberty in Experiment 1 but not in Experiment 2. One could
hypothesize that there is a minimum weight a n d / o r body weight gain (Experiment 2)
above which dietary restriction would not affect weight at puberty.
Differences in age at puberty between control lambs and lambs fed restricted diets
were smaller in Experiment 1 than in Experiment 2. This paralleled differences in body
weight gains between the two experiments. There was no difference in response of breed
type to dietary protein and energy restriction because there was no interaction of breed
type with dietary treatment in Experiment 2. Protein and energy restriction prepuberty,
therefore, delays onset of puberty to the same extent in ewe lambs of two diverse breed
types.
There was no response to realimentation of lambs on age at puberty in Experiment 1,
compared with lambs fed restricted diets throughout the study. In contrast with our
findings, Foster and Olster (1985) found that ad libitum feeding of lambs after restriction
resulted in rapid compensatory gain and onset of reproductive cycles, while continuous
feed restriction in lambs of another group resulted in lambs remaining prepuberty.
It is recognized that the effect of nuta-ition on attainment of puberty is mediated
through diminished luteinizing hormone (LH) release (Swanson et al., 1972; Schams et
al., 1981; Day et al., 1984; Foster et al., 1986; Kinder et al., 1987). Low dietary energy
 B. Boulanouar et a l . / Animal Reproduction Science 40 (1995) 229-238 237

intake prepuberty prolonged the negative effects of estradiol on release of LH, and
response to negative feedback regulation of LH release declined after initiation of
feeding a high energy diet (Foster et al., 1986). Inadequate nutrition inhibits reproduc-
tion by actions exerted on hypothalamic neurons responsible for release of LHRH
(Ebling et al., 1990; I'Anson et al., 1990). Schillo (1992) concluded, that there is no
clear effect of a single metabolite on release of LH from the pituitary gland.
Ewe lambs in the ER and PR groups of Experiment 1 had similar gains, but lambs in
the ER group tended to be older when they attained puberty. This may indicate that
intake of dietary energy may have a more important role than dietary protein in
reproductive development of ewe lambs. Data from Experiment 2 are consistent with
those from Experiment 1 with regard to the relative importance of dietary protein and
energy on age at puberty in ewe lambs.
Dietary protein, therefore, may be less important in modulating time of onset of
puberty in ewe lambs than amount of dietary energy consumed. Lambs fed a PR diet
may have maintained a body composition more nearly like lambs fed the control diet.
Lambs fed energy restricted diets may have used body fat stores to deposit lean tissue
(Drouillard et al., 1991) and thus development of fat stores to allow for attainment of
puberty might not have occurred until later in life.

5. C o n c l u s i o n

The relative importance of protein or energy deficiencies can not be clearly con-
cluded from this study. Prepubertal body weight gain is good indicator of age and
weight at puberty. This leads to speculation that the law of the 'first limiting nutrient'
not only applies to weight gain but also impacts on reproductive development in e w e
lambs. If either deficient amounts of protein or energy in diets results in decreased rate
of body weight gain, onset of puberty may be delayed. We, therefore, reject our working
hypothesis that dietary protein restriction prepuberty would have a greater influence in
delaying age at puberty in ewe lambs than restriction of dietary energy intake.

Acknowledgments

We thank Frederick Kojima and Don McClure for their assistance in collecting blood
samples. This research was supported by appropriated funds from the State of Nebraska
and I N R A / M I A C - U S A I D (Project No. 608-0136). This paper is published as Paper
Number 10732, Journal Series, Nebraska Agricultural Research Division.

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