Interrelationships Between Energy Balance and Postpartum
Reproductive Function in Dairy Cattle
ABSTRACT
Genetic improvement of dairy cows
has markedly increased milk yield over
the last three decades. Increased pro-
duction has been associated with reduced
conception rates (66% in 1951 versus 40
to 50% since 1975). Because conception
rate in dairy heifers has remained higher,
the metabolic demands of higher pro-
duction may be related to the decline in
reproductive performance in cows. Dur-
ing early lactation, increasing dietary
intake fails to keep pace with rising milk
production. The resultant negative energy
balance and rate of mobilization of body
reserves appear directly related to the
postpartum interval to first ovulation and
lower conception rate. Delays in the
onset of normal ovarian activity, thus
limiting the number of estrous cycles
before breeding, may account for the ob-
served decrease in fertility. Negative
energy balance probably acts similarly to
undernutrition and may manifest in
delayed ovarian activity by impinging on
pulsatile secretion of LH. Lower avail-
ability of glucose and insulin may also
decrease LH pulsatility or limit ovarian
responsiveness to gonadotropins. Alter-
natively, release of endogenous opioids in
association with increasing feed intake or
other lactational hormone responses may
provide neural or pituitary inhibition of
the pulsatile LH production that is
requisite for ovarian follicular develop-
ment.
INTRODUCTION
In considering the relationships of dietary
energy to reproduction in dairy cattle, the most
Received August 31, 1987.
Accepted December 21, 1987.
1989 J Dairy Sci 72:767-783
W. R. BUTLER and R. D. SMITH
Department of Animal Science
Cornell University
Ithaca, NY 14853
important period is early and peak lactation
when the demand for energy is highest. A cow
producing 35 kg of milk daily requires three
times more energy for production than for
body maintenance. The energy requirements of
a lactating cow are met through a combination
of dietary intake and mobilization of body
reserves. Dairy cattle, having been selected for
high milk production, cannot maintain a
positive dietary energy balance during early
lactation and must mobilize body reserves (9).
Because the shift from negative to positive
energy balance during the course of early
lactation might affect reproductive perform-
ance, a major objective for this paper is an
attempt to relate the energetics or metabolic
demands of milk production to reproductive
function. Second, we address the interaction of
the relative availability and mobilization of
body reserves to subsequent reproductive
performance. Third we propose a working
model for the interaction between negative
energy balance and control of gonadotropin
secretion in dairy cows.
A comprehensive international symposium
was held in 1981 on Factors influencing fer-
tility in the postpartum cow (35). The present
treatise will emphasize and update the recent
literature.
Interactions Between Milk
Production and Reproduction
Research during the past several decades has
yielded conflicting reports on the possible
interactions between milk production and
reproductive performance. Some of the dis-
crepancies are likely due to different measures
of reproductive performance. Nonreturn rates
after AI, postpartum days open, or calving
intervals are not good measures, because the
management decisions of dairy producers are
confounded with biological effects. Alter-
natively, conception rate to artificial insemina-
tion is not subject to the same limitations and
767
768
TABLE 1. Relationship of lactation to conception rate (CR) following artificial insemination.
CR in Cows (%)1 CR in
1 2 n Herifers (%)
66 45,000
50 51 9750
49" 56 212
50 307
51 2820
40 195,000 64
41 48 2426 55
52 +11 400,000 66
52 233,000
1 = First service, 2 = second service.
has been used in the large survey studies sum-
marized in Table 1. The available information
suggests that first service conception rate
declined between 1951 and 1973 but has
remained relatively constant since then. The
studies that include herdmate comparisons have
less confounding effects and overall dem-
onstrate significant negative effects of milk
yield on conception rate.
The decline in conception rate from 66% in
1951 (22) to an average of 50% in 1973 (76)
occurred during a period when the average
annual milk production in the same population
of dairy cows increased by 1500 kg (33%). This
relationship is illustrated in Figure 1. When
milk production was considered, the overall
decline in average conception rate was ex-
plained by the inverse relationship of con-
ception rate to milk yield. Although during the
same period the AI industry shifted from fresh
to frozen semen, fertility (60 to 90 d nonreturn
rates) remained similar until after 1961 (56)
and thus seems to have had little impact on the
reduction in conception rate observed by 1973
(76). A recent survey conducted in 1985
indicates that while herd milk production has
continued to increase, overall conception rate
has declined no further [Figure 1; (75)]. As
indicated in Table 1, conception rates in virgin
dairy heifers have remained as high as those
originally reported for cows in 1951. Because
fertility to AI was equal for heifers and cows in
1954 (32), we conclude that the decline in
conception rates for lactating cows reflects the
Journal of Dairy Science Vol. 72, No. 3, 1989
BUTLER AND SMITH
Herdmate
Milk yield vs. CR comparisons Reference
No (22)
Negative Yes (76)
Negative Yes (71)
Negative Yes (21)
Negative No (78, 79)
Nonsignificant No (33)
No (63)
Nonsignificant No (25)
Yes (20)
Negative No (75)
effects of greater milk production, not genetic
selection for lower fertility.
A final point concerning fertility in lactating
cows is the difference in conception rates
observed for first versus second insemination.
The increased rate at second service observed in
several studies (Table 1) indicates that with
succeeding estrous cycles, increasing days
postpartum or differences in stage of lactation
may have an important bearing on fertility.
Although these factors are obviously con-
founded with time and not easily separated,
they appear associated with another important
relationship regarding fertility: that conception
rate in lactating cows is related to the number
of ovulatory cycles preceding insemination (53,
78, 81, 84, 88). Once initiated, cyclic ovarian
activity in postpartum dairy cows seems to
continue regularly. Hence, the reestablishment
of ovulatory cycles early after parturition
assures multiple estrous cycles prior to the
recommended breeding period and in this
manner influences conception rate.
Linking the effects of lactation on fertility
to the number of preceding luteal phases
suggests important practical advantages to early
reinitiation of ovulatory estrous cycles. This, in
turn, has served to focus research attention on
the postpartum interval to first ovulation and
on questions of possible dietary constraints to
the initiation of ovulatory cyclicity during
rapidly increasing milk production. However,
before attempting to relate the effects of
dietary energy to postpartum reproduction, it
 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION 769

Milk P r o d u c t i o n in New York DHI Herds

8000

7000' R :65%

6000.

~0 CR (%1 b. CR (%1
5000
54 55
z 52 52
9p- 49
J
4000
CI
O
fZ
a.
=,
3000

2000

1000

MILK(kg) < 5398 ~05 7212 > < 6783 7690 8597 >
0 i | i i i i l
1950 1955 1960 1965 1970 1975 1980 1985

YEARS

Figure 1. Annual milk production for cows in New York herds under Dairy Herd Improvement testing
(1950 to 1986). Conception rate (CR = 66%, *) for lactating cows in 1951 (22) is compared to: inset a showing
the inverse effects on CR (mean = 50%) of lactational milk yields (as deviations among herdmates, mean =
6305 kg) in 1973 (76); and inset b showing CR (mean = 51%) by production among herds (not cows) in 1985
(75).

seems appropriate to provide a brief overview
of the key factors or mechanisms that have
been identified as precedent to the initiation of
ovulatory cycles.
Endocrine and Uterine Factors Involved
in the Postpartum Interval to First
Ovulation
Malven (45) defined the problem of the
postpartum period as requiring recovery of
function after pregnancy and parturition of
both the brain-pituitary-ovarian system and the
genital tract. Functional recovery of these
major components of the reproductive system
occurs simultaneously and there are obvious
interactions. The important endocrine and
uterine mechanisms wilt only be summarized
here, since detailed reviews have been published
elsewhere (27, 35, 42, 68).
Prior to the first ovulation and the sub-
sequent reestablishment of normal fertility in
the postpartum period, the brain-pituitary-
ovarian axis undergoes an ordered sequence of
recovery events (45). This sequence includes: 1)
recovery from pregnancy state (exposure to
high concentrations of estrogen, progesterone
and other placental hormones), 2) escape from
suckling (or lactation)-induced inhibition of
gonadotropins, 3) initiation of luteal develop-
ment with or without preceding ovulation, and
4) occurrence of estrus with ovulation and
luteal life span sufficient to foster pregnancy.
As reviewed previously (45, 54, 67, 68), pitui-
tary LH content and responsiveness to gonado-

Journal of Dairy Science Vol. 72, No. 3, 1989

770 BUTLER AND SMITH
tropin-releasing hormone (GnRH) increase
rapidly from their nadir at parturition. Re-
covery seems nearly complete by d 10 in
milked dairy cows as in suckled beef cows (52).
Plasma concentrations of FSH increase within
the first 3 to 5 d postpartum, while recovery of
a normal LH secretion pattern is delayed until d
10 to 20 (42, 43). Basal plasma LH concen-
trations rise as a more frequent episodic pattern
of pulsatile LH release develops. This pulse
pattern appears to be the primary stimulus for
ovarian follicular development leading to first
ovulation, since exogenous GnRH repeatedly
administered at 2-h intervals for 48 h to an-
estrous dairy cows results in pulsatile LH
patterns, a preovulatory type LH surge, ovula-
tion, and normal luteal function (42). The early
establishment of pulsatile GnRH and LH release
requisite for first ovulation is inhibited by
suckling (42) and also is directly related to the
presence of the uterus during the puerperium
(67).
Involution of the uterus following par-
turition affects not only the recovery of LH
secretion but possibly also another important
aspect of ovarian activity, luteal lifespan. An
early sign that gonadotropin secretion has
recovered in postpartum dairy cows is an
increase in progesterone secretion. This initial
luteal progesterone activity often precedes the
first detected estrus and often is short, lasting 4
to 12 d, rather than 13 to 20 d as following
normal ovulation (80). The abbreviated luteal
phase has been suggested to result from ex-
TABLE 2. Effects of milking or suckling during lactation on the postpartum interval (PP1) in days to first
ovulation or estrus in dairy cows.
Days to ovulation (0) or estrus (E)
Milked Suckled
17 (0)
18 (0)
21 (0) 39 (0)
30 (E) 73 (E)
36 (0)
42 (0) 88 (0)
21 (0)
33 (0)
19 (0)
i Positive.
Journal of Dairy Science Vol. 72, No. 3, 1989
aggerated release of prostaglandin F2 a during
uterine involution (38).
Relationship of Milk Production
to Postpartum Interval to Ovulation
The onset of ovulatory estrous cycles occurs
during the first few weeks of lactation. The
postpartum interval to first ovulation ranges
from 17 to 42 d as summarized from a number
of studies (Table 2)~ The interval to first ovula-
tion has been related positively to milk yield in
some studies, but this has not been a consistent
finding. In our own experience, the correlation
between milk yield and days to first ovulation
becomes significant only after the period
(40 d) when most cows have already ovulated
(7). The variation among cows and experi-
mental studies suggests that other factors in
addition to milk yield per se are involved in
determining the interval to first ovulation. As
cited in Table 2, one well-known factor that
delays ovulation and estrus is the suckling
stimulus. However, because dairy cows are
usually milked rather than being suckled the
effects of nursing on first ovulation will not be
considered here.
The metabolic demand of high milk yield in
dairy cows is another factor that should be
considered with regard to its possible effect on
postpartum ovarian activity. During early
lactation the rate of increase in milk production
exceeds that of feed intake. The general re-
lationship between dietary energy intake and
energy utilization is defined as energy balance
PPI related to milk yield Reference
-~. = 4336 kg (69)
Positive (77)
(8)
(72)
X = 7386 kg, Pos.1 (7)
(42)
X = 8260 kg, NS (21)
Est..X = 7618, NS (31)
.X = 4600 kg (13)
 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
A
"10 i | i !
'~" 35
Z "= . -.
0
~_ 30
U 60
0 40
~"
o.
25
20
>
,
-20 ,
-,s ,
-,0 ,
-5 ,
0 I
AVG. ENERGY BALANCE (Mcal/d)
Figure 2. Relationship between average energy
balance and average milk production during the first
20 d of lactation in dairy cows [By permission from
Butler et al. (7)].
and is described by the following equation:
daily energy balance = NE 1 (consumed) - NE 1
(required). Where the NE 1 requirement includes
both maintenance and production components.
Computation of energy balance reflects the
metabolic status of the cow more accurately
than does simply measuring milk yield. During
early lactation the deficiency in dietary energy
intake relative to the energy utilized for milk
production results in negative energy balance,
and this condition may persist for several weeks
(9, 70). Negative energy balance usually reaches
its maximum during wk 1 to 2 of lactation and
recovers at a variable rate. The direct rela-
tionship (r = - . 8 0 ) between milk yield and
energy balance is shown in Figure 2.
Negative energy balance in lactating dairy
cows is similar metabolically to other situations
of undernutrition. Inadequate nutrition ex-
acerbates suckling-induced anestrus in beef
cows (16, 26, 80). In dairy cows, negative
energy balance is directly related to the post-
partum interval to first ovulation (Figure 3).
This relationship became significant by 20 d
postpartum, whereas more recent studies
indicated that the relationship becomes estab-
lished within the first 2 wk of lactation (1, 13).
Recovery or improvement in energy balance
from its most negative state at the onset of
lactation toward a positive state may provide an
important signal for initiation of ovarian
activity. As described in our previous study,
first ovulation occurred, on average, approxi-
771
j i I ! ! |
80 ~- "
~ ~ ~ = .075-2Y35X
S
oe
. .
, " , ", ,
-20 -15 -10 -5 0
AVG. ENERGY BALANCE ( M c a l / d )
Figure 3. Relationship between average energy
balance during the first 20 d of lactation and number
of days to ovulation in dairy cows [By permission
from Butler et al. (7)].
mately 10 d after maximal negative energy
balance and near peak lactation (7). At ovula-
tion, energy balance was still negative, but in all
cases it was returning toward balance. The
significant correlation of days to ovulation with
cumulative or average energy balance, but not
with daily energy balance near ovulation,
suggests that both magnitude of negative energy
balance and recovery rate are important.
Relating negative energy balance to the post-
partum interval to ovulation more directly
quantifies and extends earlier reports that
showed the negative effects of milk yield
(47,88; references in Table 2).
Dairy cows in negative energy balance lose
b o d y weight when b o d y reserves are mobilized
as energy resources to support lactation. Body
weight losses relating to increased days to first
ovulation have approached or reached signifi-
cance in previous studies (31, 70, 77). Because
individual cows respond to negative energy
balance by different combinations of increased
feed intake and mobilization of b o d y reserves,
neither changes in body weight nor milk yield
are as sensitive as energy balance in predicting
the impact on days to ovulation. Examples of
these relationships in two normal Holstein cows
are presented in Figures 4 and 5. Cow 1688
produced 7131 kg in a 305-d lactation. Al-
though increases in feed energy intake lagged
behind the energy demands o f increasing milk
yield, body weight was maintained reflecting
Journal of Dairy Science Vol. 72, No. 3, 1989
772 BUTLER AND SMITH

DAY DAY BRED

22 43 62
50 1000 1O0
110 -
90
40 90- 900 80
70
70. f ~ M l l k Yleld 8OO
i 30
50- ~ D E Intake
"700 i 50
20 30- ~.__ B:l~lY t , 40 w
-600 230 a
m
10- EB
10
- 500
-20
-10- ~
10
-30 I
400 0
0 4 8, , 1~2 16
' 20
Weeks of Lactation

Figure 4. Relationships among milk yield, digestible energy (DE) intake, body weight, and energy balance
(EB) during early lactation for cow 1688. Estrus followed by ovulation occurred on d 22, 43, and 62 as in-
dicated by the arrows and this cow conceived to first insemination (d 62).

DAY DAY
76 96
50 - 1000 I O0
90
900 " 80
40 90-
Milk Yield
70
~i 30 ~" DE 60 ~
"~50.
700 50
.

20 ' 40
,,, ~ Weight -6oo 30
10 EB
10 - 500 20
-10~ ~ f , . ~ . . ~ . ~ ~
10
-30 i I ' I ' I , i
400 0
0 4 8 12 16 20
Weeks of Lactation
Figure 5. Relationships among milk yield, digestible energy (DE) intake, body weight, and energy balance
(EB) during early lactation for cow 26. First ovulation (and estrus) occurred on d 76. Conception did not occur
following inseminations during estrus on d 76 or 96.

Journal of Dairy Science Vol. 72, No. 3, 1989

 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
simultaneous mobilization of body reserves and
increasing gut contents as appetite increased.
Energy balance remained negative for 5 wk of
lactation. First ovulation (and estrus) occurred
on d 22 when the extent of negative energy
balance was diminishing. As another example,
cow 26 (Figure 5) produced more milk (9386
kg/305 d of lactation) and lost 95 kg of b o d y
weight before energy balance neared zero at wk
12 of lactation. The longer duration of negative
energy balance appeared to result from the lack
of sustained increases in feed intake, but no
clinical symptoms of ketosis or other health
problems were observed. Estrus and ovulation
did not occur until d 76 of lactation. As in the
previous example, ovulation occurred when
energy balance was still negative but was ap-
proaching zero.
Collectively, the foregoing information sug-
gests that during the metabolic demands of high
milk yield in early lactation, the consequent
negative energy balance determines the timing
of resumption of ovulatory ovarian cycles.
In turn, the timing of first ovulation determines
and limits the number of estrous cycles which
will occur before the recommended period of
insemination. We suggest that the demonstrable
negative effects of high milk yield on con-
ception rate most likely result through delays
or failure of early resumption of ovulation in
the postpartum period, thereby allowing fewer
ovulatory cycles before insemination and
thus resulting in lower fertility. Support for such
a relationship comes from a study in which
cumulative milk yield during the first 3 wk of
lactation was related to subsequent pregnancy
rates after breeding (14). We conclude that the
negative effects of lactation on fertility are re-
lated to the extent of negative energy balance
and become manifest through timing of first
ovulation.
Relationships of Available Body Reserves
and Condition with Subsequent
Reproductive Performance in
Lactating Cows.
An important component of energy balance
during the puerperium is the mobilization of
b o d y reserves. It seems appropriate to consider
the possible effects of differences in body
condition and reserves at the time of parturi-
tion on a dairy cow's ability to achieve high milk
yield and maintain recommended 1 2 - t o 13-mo
773
calving intervals. In other words, might the
responses to negative energy balance be af-
fected by differences in the body reserves
available in obese versus lean cows?
A serious consequence of overfeeding dairy
cattle is what has become known as the "fat
cow syndrome". This disorder was first de-
scribed in herds where cows were grossly overfed
during late lactation and the dry period and
is characterized by an increased occurrence of
metabolic, infectious, digestive, and repro-
ductive disorders (49, 50). During a 4-mo
period a 600 cow herd fed corn silage and
brewers grains ad lib throughout the lactation
and dry periods experienced a 38% incidence of
ketosis (50). Sixty-two percent of the cows that
calved during this period retained fetal mem-
branes. Metritis, slow uterine involution, and
delayed rebreeding are commonly reported
clinical findings in overtly obese cows (44).
Cows with metabolic disorders commonly
associated with fat cow syndrome (e.g., milk
fever) are at risk to develop subsequent re-
productive disorders (19) which directly and
indirectly result in reduced reproductive
performance (12, 23, 65). The obvious con-
clusion is that obesity at the time of calving
should be avoided (44).
The consequences of fat cow syndrome are
severe, and the grossly obese cow is easily
recognized. Although many producers are
taking precautions to limit intakes of con-
centrates and corn silage during the late lac-
tation and dry periods to prevent classical "fat
cow" problems or to promote b o d y condition
loss, this situation has raised two questions: 1)
Is moderate overconditioning, not resulting in
obese cows and classical fat cow syndrome,
sufficient to cause an increased incidence of
health disorders and impaired reproductive
performance? 2) Will the promotion of dry
period b o d y condition loss affect subsequent
milk production, health, or reproduction?
An experiment designed to answer these
questions has recently been conducted (74).
High producing, mature cows were assigned to
one of three treatment groups at 120 d post-
partum. Controls were fed a hay crop silage
(HCS, 54%) and corn silage (CS, 36%) ration
with an energy density of 1.5 Mcal/kg and a
protein content of 13% during late lactation.
Body condition scores (89) ranging from 1.0
(thin) to 5.8 (obese) were assigned weekly, and
Journal of Dairy Science Vol. 72, No. 3, 1989
774 BUTLER AND SMITH

TABLE 3. T h e incidence of health and reproductive p r o x i m a t e l y 50, 55, and 100% o f N R C re-
disorders in control cows (C), overconditioned cows q u i r e m e n t s for energy, protein, and minerals.
(OC), and overconditioned cows in which body
condition loss was induced by feed restriction during Beginning at 2 w k prior to calving, O C R cows
the dry period (OCR). were fed the dry cow ration previously de-
scribed for C and OC cows. A f t e r calving, all
Group cows were fed ad lib (HCS 25%; CS 44%; 1.6
Disorder C OC OC R Mcal/kg; 16% CP). This p r o t o c o l was repeated
during each of two successive lactations.
No. samples 44 22 30 B o d y c o n d i t i o n scores for C, OC, and O C R
Milk fever 4 4 2 groups averaged 3.9 -+ .06, 4.7 -+ .09 and 4.3 -+
Ketosis 3 3 5 .08. B o d y weights averaged 686 +- 6, 754 + 8
Retained placenta 14 7 11 and 711 -+ 7 kg, respectively, at 1 to 2 wk prior
Metritis 6 7 9 to calving. Scores and weights were higher in
Cystic ovaries 5 6 9
OC than in C and O C R (P<.01). Milk pro-
duction (8000 + 162 kg in experimental lac-
tation 1 and 8063 -+ 228 kg in lactation 2) and
b u t t e r f a t percent (3.7 + .1) did not differ across
feed intakes were adjusted to maintain b o d y t r e a t m e n t groups. The incidence of health and
condition scores in the range 3.8 to 4.2. The reproductive disorders did not differ across
o t h e r two groups were o v e r c o n d i t i o n e d ( b o d y t r e a t m e n t groups (Table 3, P > . 1 0 ) . Likewise,
condition scores in the range 4.5 to 5.2) by reproductive p e r f o r m a n c e (with the e x c e p t i o n
feeding a ration to support 27 kg of milk (HCS, of days to first observed estrus) did not differ
22%; CS, 42%. 1.6 Mcal/kg; 15% CP) during significantly (Table 4).
late lactation. During the entire dry period the These data suggest that overfeeding and
control group (C) and one group of the over- m o d e r a t e overconditioning at calving to the
conditioned cows (OC) were fed a ration to e x t e n t observed in this study ( c o n d i t i o n scores
maintain c o n d i t i o n scores (HCS, 50%; CS; 50%; 4+ to 5 - on the Wildman scale) do not ad-
1.4 Mcal/kg; 9.2% CP; 10 kg DM/d). T h e versely affect reproductive performance. In
second o v e r c o n d i t i o n e d group (OCR) was fed a contrast, others reported that overfeeding
ration to p r o m o t e b o d y c o n d i t i o n toss until during the late lactation, dry periods, or b o t h
2 wk prepartum (HCS, 100%; 1.0 Mcal/kg; 13% increased the incidence of disease (83), retained
CP; 4.1 kg DM/d). This ration provided ap- placenta (17), metritis (17, 88), and cystic

TABLE 4. Reproductive performance ~ in control cows (C), overconditioned cows (OC), and overconditioned
cows in which body condition loss was induced by feed restriction during the dry period (OCR).

Group
Variable C OC OCR

No. samples 43 21 29
Days to first ovulation 2 30 +- 3 32 4 31 4
Days to first observed estrus 49 _+4 a 51 6a 36 5b
Days to first service 71 +- 2 70 3 65 3
First service conception rate, % 56 48 45
Services per conception 2.3 -+ .3 2.2 .4 2.1 .3
Pregnancy rate, % 100 86 93
Days open 103 +- 8 88 -+ 10 94 9

ab' Mean s within

. . rows
. .with different superscripts differ (P<.05).
1Mean -+ SEM.
2 Determined by milk progesterone analysis of samples obtained twice weekly from parturition to confirma-
tion of pregnancy by rectal palpation.

Journal of Dairy Science Vol. 72, No. 3, 1989

 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION 775

ovaries (44) and lengthened the postpartum
intervals to first estrus, ovulation (17, 88), and
conception (51). The reasons for these dif-
ferences remain to be determined, but could
relate to types of rations fed, degree of over-
conditioning at calving, prepartum adjustment
to the lactating cow ration, or postpartum
nutritional status and body condition loss.
Nevertheless, the results of the Cornell,ex-
periments strongly suggest that neither moderate
overconditioning at calving nor energy re-
striction to promote body condition loss in
overconditioned cows during the dry period
adversely affect milk production, health, or
reproductive performance in high producing
cows when rations are carefully monitored and
adjusted as needed to maximize DM intake and
minimize body condition loss during early
lactation.
Relationship of Postpartum Weight
and Body Condition Loss to
Reproductive Performance
The severity of postpartum negative energy
balance and the delay in the initiation of
normal postpartum reproductive cyclicity (7) is
associated with body weight and body condi-
tion loss. One might predict impaired repro-
ductive performance in cows that lose excessive
amounts of body condition during early lac-
tation. The existance of such a relationship
would make body condition scoring a useful
tool for relating suboptimal reproductive
performance to inadequate nutrition in early
lactation.
Cows in the Cornell experiment cited were
regrouped based on body condition loss (BCL)
during the first 5 wk of lactation: minor
(BCL1), <.5 body condition score unit lost;
moderate (BCL2), .5 to 1.0 unit lost; and severe
(BCL3) , >1.0 unit lost. Reproductive per-
formance was impaired in cows exhibiting
severe body condition loss (Table 5). The
incidence of metritis was higher in BCL2 and
BCL 3 (22 and 47%; respectively) than in BCL a
(6%), but this did not account for the dif-
ferences observed in reproductive performance.
Performance in cows treated for metritis
did not differ significantly from that in other
COWS.
Excessive mobilization of body reserves has
been associated with postpartum fatty in-
filtration of the liver and reduced reproductive
performance in high yielding dairy cows. In a
previous study, 69 of 109 cows were classified
as having fatty livers [>20% fat by volume;
(58)] but did not exhibit clinical signs of fat
cow syndrome (59). However, cows with fatty
liver showed significant alterations of liver
function and calved subsequently at intervals
averaging 33 d longer than for cows without
fatty livers. The delay in conception was due to

TABLE 5. The relationship between body condition loss during the first 5 wk postpartum and reproductive
performance. 1

Body condition loss group 2

Variable BCL~ BCL2 BCL3

No. samples 17 64 12
Days to first ovulation 3 27 2a 31 2a 42 5b
Days to first observed estrus 48 6ab 41 3a 62 7b
Days to first service 68 4 a 67 2 a 79 5 b
First service conception rate, % 65 a 53 a 17b
Services per conception 1.8 .4 2.3 .2 2.3 .4
Pregnancy rate, % 94 95 100

a'bMeans within rows with different superscripts differ (P<.05).

1Mean SEM.
2BCL1 = <.5. Body condition score unit loss; BCLa = .5 -1.0 unit loss and BCL3 = >1.0 unit loss.
3Determined by milk progesterone analysis of samples obtained twice weekly from calving to the confirma-
tion of pregnancy by rectal palpation.

Journal of Dairy Science Vol. 72, No. 3, 1989

776 BUTLER
a delay in the onset of estrous cycle activity
after calving and a reduced conception rate.
Studies on the pathogenesis of fatty liver
suggest that it is part of a generalized fat
mobilization syndrome that occurs during early
lactation in high yielding cows. The mobiliza-
tion of these reserves is reflected in a loss of
b o d y condition and body weight. High milk
yield potential and fatness at calving (23, 61,
62) appear to be predisposing factors. Common
features of the syndrome are overfeeding during
the dry period or depression of DM intake and
negative energy balance in early lactation (60,
82).
The mechanism by which fatty infiltration
of the liver affects reproductive performance
remains to be defined. F a t t y liver could simply
be a symptom of the negative energy balance
that has been demonstrated to impair reproduc-
tive performance. The results of the study (74)
presented in the previous paragraph support
this view, since cows in BCL 3 suffered more
severe negative energy balance (P<.05) and
demonstrated higher liver fat contents than the
other groups (35.9 + 2.9 vs. 24.8 + 2.5%,
P<.01).
Mechanisms for Effects of Negative
Energy Balance on Days to
Ovulation
The interactions of the most important
factors affecting ovarian activity in postpartum
cows are summarized in Figure 6 [adopted
from (80)]. As described previously, the
reestablishment of a normal LH pulse pattern is
the key factor responsible for ovarian follicular
development and the initiation of postpartum
ovarian cyclicity. Suckling and related stimuli
or undernutrition have been identified as the
most important negative influences on LH pulse
secretion. Dairy cows in early lactation rep-
resent a situation of undernutrition due to
high milk yields coupled with inadequate feed
intake and the consequent negative energy
balance. In suckled lactating beef cows, un-
dernutrition reduces both FSH and LH con-
centrations for extended periods (80), whereas
in milked dairy cows, only LH seems to be
deficient after 5 to 10 d postpartum (42, 66,
68, 80).
The direct effects of negative energy balance
on LH pulse patterns have been assessed during
Journal of Dairy Science Vol. 72, No. 3, 1989
AND SMITH
periods of energy restriction (34). Heifers were
ovariectomized and fed below requirements
until b o d y weights were reduced 20%. In the
absence of ovarian steroids, energy restriction
resulted in reduced LH pulse frequency but
higher pulse amplitude. The sensitivity to
negative feedback effects of estradiol was
enhanced, but this was secondary to direct ef-
fects on LH pulse secretion.
A number of other studies have provided
information on the relationship of dietary
energy availability to LH secretion. In suckled
beef cows, chronic undernutrition inhibited LH
release in response to calf removal with reduc-
tion in both LH pulse frequency and peak
concentrations (86). The LH response to calf
removal was shown to be blocked by acute
induced hypoglycemia (64). The authors
suggested that the impaired LH response was
due to lower glucose availability. However, LH
patterns remained altered during the entire time
when insulin remained low which extended
beyond the period of hypoglycemia. This
suggests that insulin concentrations rather than
glucose may have directly affected LH secre-
tion. This hypothesis gains support from a
study in nonlactating heifers in which the
suppression of insulin during fasting and abrupt
increases during refeeding were temporally
linked to ongoing LH secretion (48). The
presence of insulin receptors located in the
SUCKLING MILKING
PRL SECRETION p LH PULSATILITY FSH SECRETION
o_ [
ES~IOL
Figure 6. Interactions among external and endo-
crine factors affecting ovarian activity in postpartum
cows [Adapted from Terqui et al. (80)]. --EB =
negative energy balance, PGF2a = prostaglandin
F2a, PRL = Prolactin.
 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
median eminence (85) of the hypothalamus
suggests a regulatory role for insulin in the
metabolism of glucose in this neural tissue,
which could, in turn, modulate hypothalamic
GnRH output. Median eminence and pituitary
tissues from fasted rats preferentially me-
tabolized ketones, rather than glucose (30),
allowing the possibility that a switch from
glucose to ketone utilization during inadequate
energy intake may signal decreased gonado-
tropin activity.
A more likely link than insulin between
negative energy balance and decreased LH
secretion involves activation of neuroendocrine
opioid pathways. One of the most significant
physiological functions of neural opioid pep-
tides is their association with feeding behavior
(3, 10). Activation of opioid pathways stimu-
lates feeding, and blocking opioid receptors
with the antagonist, naloxone, inhibits feed
intake. A direct relationship with negative
energy balance was suggested when Dyer et al.
(15) reported impairment of LH secretion in
fasting ovariectomized rats and that this
could be prevented with naloxone pretreat-
ment. The effect of fasting was a reduction in
LH pulse amplitude. In the same study, fasting
also impaired LH release during neural ex-
citation of the ventral noradrenergic tract in the
brainstem. Here again naloxone prevented the
inhibitory effects of fasting. These important
results and others describing the opioid media-
tion of LH secretion (4, 11, 37, 46) support
and further describe the neural pathways for
opioid inhibition of GnRH release. As reviewed
by Bicknell (5), excitatory noradrenergic
neurons originating in the brainstem synapse on
GnRH producing neurons located in the an-
terior hypothalamus and preoptic area. Pre-
synaptic opioid inhibition of these noradrenergic
neurons arises both from outside the hypo-
thalamus (enkephalin pathway) or from within
the basal hypothalamus near the arcuate
nucleus (3-endorphin pathway). There is
additional evidence suggesting that the /3-
endorphin pathway may also directly impinge
on the GnRH neurons as they terminate near
the pituitary portal vessels in the median
eminence.
Although the evidence suggesting a neural
site of action for inhibitory effects of opioids
on GnRH mediated LH secretion is well-
documented, actions within the anterior
777
pituitary gland must also be considered. Opiate
peptides, acting through specific opiate-binding
sites, exert direct inhibitory effects on anterior
pituitary LH release in vitro (6). The most
prevalent endogenous opioid, 3-endorphin, is
released from the hypothalamus into the
pituitary portal system (39) and could thereby
reach pituitary sites of LH production. Perhaps,
just as importantly, j3-endorphin is produced
within anterior pituitary gland corticotrophs
from pro-opiocortin, the same precursor as for
adrenocorticotropin (18). Incubation of dis-
persed anterior pituitary cells with cortico-
tropin-releasing hormone (CRH) inhibited basal
LH release, an effect that was reversed by
addition of an opiate antagonist (6). The effect
of CRH was presumably through release of
opioid peptides indicating that these may exert
a paracrine inhibitory action on gonadotrophs.
The relevance of these possible direct effects of
opioids to pituitary LH release during negative
energy balance can only be postulated at the
present time. Enhanced t3-endorphin release
from the hypothalamus or anterior pituitary
may be related to the stimulation of appetite
and dietary intake that normally occurs in early
lactation and may, in turn, exert inhibitory
effects on hypothalamic GnRH release, pitui-
tary LH release, or both.
A preliminary model to investigate further
the involvement of opioids on pulsatile LH
secretion during negative energy balance has
been developed (Canfield and gutler, un-
published). Ovariectomized ewes were placed
on an energy restricted diet in October and
within 8 wk had lost 20% of their body weight.
Blood samples were collected through in-
dwelling vascular cannulae for 16 h at 12-min
intervals to characterize LH pulse patterns.
During the last 8 h of frequent sampling, five of
the ewes were infused with naloxone (an opioid
antagonist, 25 mg i.v. at the beginning of each
h) while the other five ewes received saline.
Upon completion of the frequent sampling, all
ewes were injected with GnRH (10 ng/kg), and
blood sampling continued at 30-min intervals for
an additional 4 h. In several ewes naloxone treat-
ment resulted in immediate increments in LH
pulse amplitude without changing pulse frequen-
cy and average basal plasma LH concentrations
increased about 25 to 30% (Figure 7). Pulse
patterns were stable and unchanged during the
same period in control animals. Pituitary LH
Journal of Dairy Science Vol. 72, No. 3, 1989
778 BUTLER AND SMITH

B1075c

"i NALOXONE

70

i-
m

l0

0 I i ! i I i I i I I I I I I I I
0 I~ II O tO 111 14 10

Figure 7. Plasma LH concentrations in an ovariectomized ewe (B1075c) during negative energy balance.
Naloxone was injected hourly (i.v.) beginning at 8 h, which increased LH pulse amplitude and basal LH con-
centrations.

release in response to GnRH was equal in both
naloxone and saline treated groups. These
preliminary results indicate that neural opioid
pathways modulate LH pulse secretion during
negative energy balance. Because LH pulse
amplitude was increased by naloxone, while the
pituitary response to GnRH was unchanged, the
primary effect of opioid inhibition would
appear to be on the magnitude of endogenous
GnRH pulses being produced. The manner or
site of action for such modulation of the GnRH
pulse generating system cannot be determined
from these experiments, but agrees with pre-
vious results in fasting rats (15). Future experi-
ments are planned for early lactating cows to
investigate the role of opioids in the effects of
negative energy balance on patterns of LH
secretion and days to first ovulation. A recent
study has shown that opioids are involved in
suckling-induced anestrous in beef cows (87).
Metabolic and Endocrine Interrelationships
in the Postpartum Cow: A Working Model
The early postpartum period in lactating
dairy cows was characterized in previous
sections as involving many metabolic adjust-
ments and their interplay with complex en-
docrine mechanisms related to normal ovarian
activity. Negative energy balance results from a
temporary imbalance between dietary intake
and the energy demands of increasing milk
production (70). Accommodation to these
metabolic demands is accomplished by com-
binations of increases in dietary intake and
mobilization of body energy reserves, which
differ among individual cows. To understand
the possible negative impacts of lactation on
reproductive performance, it is necessary to
consider the associations among metabolic
factors including increased appetite and marked
increases in glucose utilization, interaction of

Journal of Dairy Science Vol. 72, No. 3, 1989

 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
stimuli responsible for increased milk pro-
duction, and the mechanisms necessary for
ovarian activity that might be subject to in-
hibition. Some of the sequelae to negative
energy balance and increased feeding behavior
relating to metabolites, opioids, and the LH
pulse system are diagrammed in Figure 8. This
simple diagram is intended to emphasize the
metabolic or opioid factors most easily related
to LH pulsatility and does not attempt to
explain the complexities or important mech-
anisms regulating appetite and feeding behavior
in cattle (2, 3).
During negative energy balance in early
lactation, the rapid increases in utilization of
glucose for milk lactose production results in
lower plasma concentrations of both glucose
and insulin as compared with that in later stages
of lactation (29, 73). Although the combined
effects of lower glucose and insulin may play a
minor role in stimulating feeding behavior (2),
the relative lack of insulin would enhance
lipolysis in adipose tissues, thereby further
increasing appetite via increased availability of
free fatty acids for hypothalamic oxidation
(36). The increased feed consumption from
these effects and other additive stimuli in early
lactation would likely be associated with
increased release of /3-endorphin within the
hypothalamo-hypophyseal unit (2, 3, 10).
Elevated /3-endorphin would be expected to
inhibit the GaaRH pulse system (Figure 8). At
NEGATIVEENERGYBALANCE
/
HYPOGLYCEMIA,,-
.'x
=,
_ ~ +KET' (~ES
GNRHPULSATILITY
+
OVARIAN STEROIDS4 IDLHPULSATILITY
Figure 8. Interactions among metabolic and
opioid factors related to negative energy balance,
feeding behavior and the system generating LH pulses.
B-ENDORPHIN = ~-endorphin, GNRH = gonado-
tropin-releasing hormone.
779
the same time, the GnRH system and, hence,
LH pulse patterns may be depressed directly by
low insulin and secondarily by the increased
production and utilization of ketones as a con-
sequence of mobilization of body adipose
reserves (30, 85). Although the relative im-
portance of the various inhibitory inputs
remain to be established, the end result would
be interference with the development of
postpartum LH pulse patterns. In nonlactating
cattle, negative energy balance alters pulsatile
LH release and LH pulses are depressed further
because of enhanced sensitivity to negative
feedback effects of ovarian steroids (34).
Endogenous opioids relate not only to
dietary intake during negative energy balance
but also to the release of several hormones
important to the induction and maintenance of
lactation. Milking induces release of prolactin
(40), adrenocorticotropin [as measured by
glucocorticoids (41)] and oxytocin (24), and
the release of each involves opioids (5, 18, 55).
We suggest that these lactation stimuli, coupled
with increased adrenocorticotropin in response
to hypoglycemia and increased feeding behavior
inspired by the energy deficit, are all super-
imposed during the early lactation period to
yield a situation in which neuroendocrine
opioid mechanisms dominate pulsatile GnRH
and LH secretion. Our speculation on the
linkage between these and other mechanisms in
a model for the postpartum cow is diagrammed
NEGATIVEENERGYBALANCE
HYPOGLYCEMIA
+/ ,\,
FEEDING
~x~.H +~ ACTH+ B-ENDORPHIN I+
,Y,OINSOLINEMIA.... 4--
B-ENDORPHIN
( ~ GNRHPULSATILITY~ NE
I - /
ill+PULSATILITY \+
FSHSECRETION
OVARIANACTIVITY
Figure 9. Model for the relationships of negative
energy balance to gonadotropin secretion in post-
partum lactating cows. ACTH = adrenocorticotropin,
B-ENDORPHIN = ~-endorphin, CRH = corticotropin-
releasing hormone, GNRH = gonadotropin-releasing
hormone, NE = norepinephrine.
Journal of Dairy Science Vol. 72, No. 3, 1989
780 BUTLER AND SMITH
in Figure 9. We suggest that negative energy
balance operating through a n u m b e r o f in-
terrelated pathways involving opioids and
insulin is largely responsible for regulating the
LH pulse patterns that seem crucial for the
onset and timing of p o s t p a r t u m ovarian func-
tion.
A l t h o u g h we hypothesize that the mech-
anisms linking negative energy balance to LH
pulsatility are most i m p o r t a n t for governing
p o s t p a r t u m ovarian activity, an additional
aspect of ovarian regulation has recently been
emerging. Insulin has been shown to exert
actions on ovarian tissues that are very similar
to those of pituitary g o n a d o t r o p i n s (57). These
actions include direct effects on steroidogenic
enzymes, m o d u l a t i o n o f g o n a d o t r o p i n r e c e p t o r
number, synergism with o t h e r gonadotropins,
and nonspecific e n h a n c e m e n t of cell viability.
Based on the diversity of these actions we
postulate that lower insulin availability during
early lactation m a y render ovarian follicles less
responsive to any ongoing g o n a d o t r o p i n stimu-
lation. G o n a d o t r o p i c effects of insulin on
follicular d e v e l o p m e n t have been indicated by
experiments in energy restricted heifers (28,
48).
In summary, p o s t p a r t u m reproductive func-
tion in dairy cattle seems directly d e p e n d e n t on
the availability of nutrient energy relative to its
utilization for lactation. Negative energy
balance primarily appears to interfere with the
ability of the h y p o t h a l a m o - h y p o p h y s e a l axis to
develop the pulsatile LH pattern necessary for
fostering ovarian follicular d e v e l o p m e n t and
ovulation. Secondarily the energy deficit and
low insulin concentrations during this period
m a y limit the responsiveness o f the ovary to
g o n a d o t r o p i n stimulation. T h e interval to first
ovulation in the p o s t p a r t u m period depends
u p o n recovery of the normal f u n c t i o n s of the
brain-pituitary-ovarian axis and the genital
tract. S u b s e q u e n t fertility is c o n v e y e d from an
early onset o f first ovulation and c o m p l e t i o n of
multiple cycles before insemination.
REFERENCES
1 Allrich, R. D., K. A. Berghorn, and C. H. Noller.
1987. Influence of energy balance on ovarian
activity and estrous behavior in postpartum dairy
cows. J. Dairy Sci. 70(Suppl. 1): 184. (Abstr.)
2 Baile, C. A., and M. A. Della-Fera. 1981. Nature of
hunger and satiety control systems in ruminants. J.
Journal of Dairy Science Vol. 72, No. 3, 1989
Dairy Sci. 64:1140.
3 Baile, C. A., C. L. McLaughlin, and M. Della-Fera.
1986. Role of cholecystekinin and opioid peptides
in control of food intake. Physiol. Rev. 66:172.
4 Bhanot, R., and M. Wilkinson. 1984. The in-
hibitory effect of opiates on gonadotrophin
secretion is dependent upon gonadal steroids.
J. Endocrinol. 102:133.
5 Bicknell, R. J. 1985. Endogenous opioid peptides
and hypothalamic neuroendocrine neurones. J.
Endocrinol. 107:437.
6 Blank, M. S., A. Fabbri, K. J. Cart, and M. L.
Dufau. 1986. Inhibition of luteinizing hormone
release by morphine and endogenous opiates in
cultured pituitary cells. Endocrinology 118:2097.
7 Butler, W. R., R. W. Everett, and C. E. Coppock.
1981. The relationships between energy balance,
milk production and ovulation in postpartum
Holstein cows. J. Anim. Sci. 53:742.
8 Carruthers, T. D., and H. D. Hafs. 1980. Suckling
and four-times daily milking: influence on ovula-
tion, estrus and serum luteinizing hormone, glu-
cocorticoids and prolactin in postpartum Holsteins.
J. Anim. Sci. 50:919.
9 Coppock, C. E., C. H. Noller, and S. A. Wolfe.
1974. Effect of forage-concentrate ratio in com-
plete feeds fed ad libitum on energy intake in
relation to requirements by dairy cows. J. Dairy
Sci. 57:1371.
10 Davis, J. M., M. T. Lowy, G.K.W. Yim, D. R.
Lamb, and P. V. Malven. 1983. Relationship
between plasma concentrations of immunoreactive
Beta-endorphin and food intake in rats. Peptides
4:79.
11 Diez-Guerra, F. J., S. Augood, P. C. Emson, and R.
G. Dyer. 1986. Morphine inhibits electrically
stimulated noradrenaline release from slices of rat
medial preoptic area. Neuroendocrinology 43:89.
12 Doohoo, T. R., and S. W. Martin. 1984. Disease,
production and culling in Holstein-Friesian cows.
IV. Effects of disease on production. Prev. Vet.
Med. 2:775.
13 Ducker, M. J., R. A. Haggett, W. J. Fisher, S. V.
Morant, and G. A. Bloomfield. 1985. Nutrition and
reproductive performance of dairy cattle. 1. The
effect of level of feeding in late pregnancy and
around the time of insemination on the repro-
ductive performance of first lactation dairy heifers.
Anita. Prod. 41:1.
14 Ducker, M. J., and S. V. Morant. 1984. Observa-
tions on the relationships between the nutrition,
milk yield, live weight and reproductive perform-
ance of dairy cows. Anim. Prod. 38:9.
15 Dyer, R. G., S. Mansfield, H. Corbet, and A.D.P.
Dean. 1985. Fasting impairs LH secretion in female
rats by activating an inhibitory opioid pathway. J.
Endocriuol. 105:91.
16 Easdon, M. P., J. M. Chesworth, M.B.E. Aboul-ela,
and G. D. Henderson. 1985. The effect of un-
dernutrition of beef cows on blood hormone and
metabolite concentrations postpartum. Reprod.
Nutr. Dev. 25:113.
17 E1-Keraby, F., and E. Schilling. 1976. Effect of
overfeeding of cows during late lactation on
 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
reproductive performance in the early postpartum
period. Page 361 in Proc. 8th AI Int. Congr. Anita.
Reprod. AI.
18 Eipper, B. A., and R. E. Mains. 1980. Structure
and biosynthesis of pro-ACTH/endorphin and
related peptides. Endocr. Rev. 1 : 1.
19 Erb, H. N., R. D. Smith, P. A. Oltenacu, C. L.
Guard, R. B. Hillman, P. A. Powers, M. C. Smith,
and M. E. White. 1985. Path model of reproductive
disorders and performance, milk fever, mastitis,
milk yield and culling in Holstein cows. J. Dairy
Sci. 68:3337.
20 Everett, R. W., and B. Bean. 1986. Semen fer-
t i l i t y - a n evaluation system for artificial insemina-
tion sires, technicians, herds, and systematic fixed
effects. J. Dairy Sci. 69:1630.
21 Fonseca, F. A., J. H. Britt, B. T. McDaniel, J. C.
Wilk, and A. H. Rakes. 1983. Reproductive traits
of Holsteins and Jerseys. Effects of age, milk yield,
and clinical abnormalities on involution of cervix
and uterus, ovulation, estrous cycles, detection of
estrus, conception rate, and days open. J. Dairy
Sci. 66:1128.
22 Foote, R. H. 1978. Reproductive performance and
problems in New York Dairy Herds. Cornell Univ.
Agric. Exp. Sm. Search 8:1.
23 Fronk, T. J., L. H. Schultz, and A. R. Hardie.
1980. Effect of dry period overconditioning on
subsequent metabolic disorders and performance
of dairy cows. J. Dairy Sci. 63:1080.
24 Gorewit, R. C. 1979. Method for determining
oxytocin concentrations in unextracted sera;
characterization in lactating cattle. Proc. Soc. Exp.
Biol. Med. 160:80.
25 Gwazdauskas, F. C., W. D. Whittier, W. E. Vinson,
and R. E. Pearson. 1986. Evaluation o f repro-
ductive efficiency o f dairy cattle with emphasis on
timing o f breeding. J. Dairy Sci. 69:290.
26 Hansen, P. J., and E. R. Hauser. 1983. Genotype
environmental interactions on reproductive traits
o f bovine females. Ill. Seasonal variation in post-
partum reproduction as influenced by genotype,
suckling and dietary regimen. J. Anim. Sci. 56:
1362.
27 Hanzen, C. H. 1986. Endocrine regulation of
postpartum ovarian activity in cattle: a review.
Reprod. Nutr. Dev. 26:1219.
28 Harrison, L. M., and R. D. Randel. 1986. Influence
of insulin and energy intake on ovulation rate,
luteinizing hormone and progesterone in beef
heifers. J. Anita. Sci. 63:1228.
29 Hart, I. C., J. A. Bines, S. V. Morant, and J. L.
Ridley. 1978. Endocrine control of energy me-
tabolism in the cow: Comparison of the levels of
hormones (prolactin, growth hormone, insulin and
thyroxine) and metabolites in the plasma of
high-and low-yielding cattle at various stages of
lactation. J. Endocrinol. 77:333.
30 Hawkins, R. A. and J. F. Biebuyck. 1979. Ketone
bodies are selectively used by individual brain
regions. Science 205 : 325.
31 Henriksen, J., and A. M. Jensen. 1985. Studies on
the endocrine and environmental factors influ-
encing post partum acyclicity in dairy cows based
781
on progesterone profiles (preliminary results).
Ellendorff, F. and F. Eisaesser, ed. Pages 2 2 1 - 2 3 2
in Endocrine causes of seasonal and lactational
anestrus in farm animals. Martinus Nijhoff Publ.,
Boston, MA.
32 Herman H. A. 1956. Age-fertility relationships in
cattle serviced by artificial insemination. Page
56 in Proc. 3rd Int. Congr. Anita. Reprod. AI.
33 Hillers, J. K., P. L. Senger, R. L. Darlington, and
W. N. Fleming. 1984. Effects of production,
season, age of cow, days dry, and days in milk on
conception to first service in large commercial
dairy herds. J. Dairy Sci. 67:861.
34 Imakawa, K., M. L. Day, D. D. Zalesky, A. Clutter,
R. J. Kittok, and J. E. Kinder. 1987. Effects of
17beta-estradiol and diets varying in energy on
secretion of luteinizing hormone in beef heifers. J.
Anita. Sci. 64:805.
35 Karg, H., and E. Schallenberger. 1982. Factors
Influencing Fertility in the Postpartum Cow. Curt.
Topics Vet. Med. Anita. Sci. Vol. 20. Martinus
Nijhoff Publ., Boston, MA.
36 Kasser, T. R., R.B.S. Harris, and R. J. Martin.
1985. Level of satiety: fatty acid and glucose
metabolism in three brain sites associated with
feeding. Am. J. Physiol. 248:R447.
37 Kesner, J. S., J. Kaufman, R. C. wilson, G. Kuroda,
and E. Knobil. 1986. The effect of morphine on
the electrophysiological activity of the hypo-
tbalamic luteinizing hormone-releasing hormone
pulse generator in the Rhesus monkey. Neuro-
endocrinology 43:686.
38 Kindahl, H., L. E. Edquist, K. Larsson, and A.
Malmquist. 1982. Influence of prostaglandins on
ovarian function postpartum. H. Karg and E.
Schallenberger, ed. Factors influencing fertility in
the postpartum cow. Gurr. Topics Vet. Med. Anim.
Sci. 20:173.
39 Koenig, J. I., H. Y. Meltzer, and G. A. Gudelsky.
1986. Morphine or capsaicin administration alters
the secretion of beta-endorphin into the hypo-
physial portal vasculature of the rat. Neuroen-
docrinology 43:611.
40 Koprowski, J. A., and H. A. Tucker. 1973. Serum
prolactin during various physiological states and its
relationship to milk production in the bovine.
Endocrinology 92:1480.
41 Koprowski, J. A., and H. A. Tucker. 1973. Bovine
serum growth hormone, corticoids and insulin
during lactation. Endocrinology 93 : 645.
42 Lamming, G. E., A. R. Peters, G. M. Riley, and M.
W. Fisher. 1982. Endocrine regulation of post-
partum function. H. Karg and E. Schallenberger,
ed. Factors influencing fertility in the post-
partum cow. Curt. Topics Vet. Med. Anita. Sci.
20:148.
43 Lamming, G. E., D. C. Watbes, and A. R. Peters.
1981. Endocrine patterns o f the post-partum cow.
J. Reprod. Fertil (Suppl.) 30:155.
44 MacCormack, J. 1987. Fat cow syndrome and its
complications. Vet. Med. Small Anita. Clin. 73:
1057.
45 Malven, P. V. 1984. Pathophysiology of the puer-
perium: definition o f the problem. Page 1 in Proc.
Journal of Dairy Science Vol. 72, No. 3, 1989
782 BUTLER AND SMITH
10th Int. Congr. Anim. Reprod. AI.
46 Malven, P. V., D.F.B. Bossut, and M. A. Dickman.
1984. Naloxone antagonism o f an opioid mech-
anism inhibitory to LH release in luteal phase ewes.
Page 27 in Proc. 10th Int. C o n g . Anim. Reprod.
AI.
47 Marion, G. G., and H. T. Gier. 1968. Factors
affecting bovine ovarian activity after parturition.
J. Anita. Sci. 27:1621.
48 McCann, J. P., and W. Hansel. 1986. Relationships
between insulin and glucose metabolism and
pituitary-ovarian functions in fasted heifers. Biol.
Reprod. 34:630.
49 Morrow, D. A. 1976. The fat cow syndrome. J.
Dairy Sci. 59:1625.
50 Morrow, D. A., D. Hillman, A. W. Dade, and H.
Kitchen. 1979. Clinical investigation of a dairy
herd with fat cow syndrome. J. Am. Vet. Med.
Assoc. 174:161.
51 Morrow, D. A., H. F. Tyrrell, and G. W. Trim-
berger. 1969. Effects o f liberal concentrate feeding
on reproduction in dairy cattle. J. Am. Vet. Med.
Assoc. 55:1946.
52 Moss, G. E., J. R. Parfet, C. A. Marvin, R. D.
Allrich, and M. A. Diekman. 1985. Pituitary
concentrations of gonadotropins and receptors for
GnRH in suckled beef cows at various intervals
after calving. J. Anita. Sci. 60:285.
53 Nash, J. G., L. Ball, and J. D. Olsen. 1980. Effects
on reproductive performance of administration of
GnRH to early postpartum dairy cows. J. Anita.
Sci. 50:1017.
54 Peters, A. R., and G. E. Lamming. 1984. Endocrine
changes in the postpartum period. Page 17 in
Proc. lOth Int Congr. Anim. Reprod. AI.
55 Pfeiffer, A., and A. Herz. 1984. Endocine actions
of opioids. Horm. Metab. Res. 16:386.
56 Pickett, B. W., R. C. Martig, and W. A. Cowan.
1961. Preservation of bovine spermatozoa at - 7 9
and - 1 9 6 C . J. Dairy Sci. 44:2089.
57 Poretsky, L., and M. F. Kalin, 1987. The gonado-
trophic function o f insulin. Endocr. Rev. 8:132.
58 Reid, I. M. 1980. Incidence and severity of fatty
livers in dairy cows. Vet. Ree. 107:281.
59 Reid, I. M., and R. A. Collins. 1980. The pathology
of postparturient fatty liver in high-yielding dairy
cows. Invest. Clln. Pathol. 3:231.
60 Reid, I. M., and C. J. Roberts. 1983. Subclinical
fatty liver in dairy cows - current research and
future prospects. Ir. Vet. J. 37:104.
61 Reid, I. M., C. J. Roberts, and R. Monston. 1979.
Reduced fertility associated with fatty liver in high
yielding dairy cows. Vet. Sci. Commun. 3:231.
62 Roberts, C. J., I. M. Reid, G. J. Rowlands, and A.
Patterson. 1981. A fat mobilization syndrome in
dairy cows in early lactation. Vet. Rec. 108:7.
63 Ron, M., R. Bar-Anan, and G. R. Wiggans. 1984.
Factors affecting conception rate of Israeli Hol-
stein cattle. J. Dairy Sci. 67:854.
64 Rutter, L. M., and J. G. Manns. 1987. Hypo-
glycemia alters pulsatile luteinizing hormone
secretion in the postpartum beef cow. J. Anita. Sci.
64:479.
65 Sandals, W.C.D., R. A. Cutis, J. F. Cote, and S. W.
Journal of Dairy Science Vol. 72, No. 3, 1989
Martin. 1979. The effect of retained placenta and
metritis complex on reproductive performance in
dairy cattle - a case control study. Can. Vet. J.
20:131.
66 Schallenberger, E. 1985. Gonadotrophins and
ovarian steriods in cattle. III. Pulsatile changes of
gonadotrophin concentrations in the jugular vein
post partum. Acta Endocrinol. 109: 37.
67 Schallenberger, E., D. L. Waiters, S. K. Oschmann,
and H.H.D. Meyer. 1984. Endocrine changes
during the early postpartum period in dairy cattle.
Proc. 10th Int. Congr. Anita. Repro& AI, III:9.
68 Schatlenberger, E. and D. L. Waiters. 1985.
Endocrine mechanisms contributing to postpartum
anoestrus in dairy and beef cattle. Pages 2 0 6 - 2 2 0
in Endocrine causes of seasonal farm animals. F.
Ellendorf and F. Elsaesser, ed. Martinus Nijhoff
Publ., Boston, MA.
69 Schams, D., E. Schallenberger, Ch. Menzer, J.
Stangl, K. Zottmeir, B. Hoffmann, and H. Karg.
1978. Profiles of LH, FSH and progesterone in
postpartum dairy cows and their relationship to
the commencement of cyclic functions. Therio-
genology 10:453.
70 Sejrsen, K., and A. Neimann-Sorensen. 1982.
Nutritional physiology and feeding of the cow
around parturition. Factors influencing fertility in
the postpartum cow. H. Karg and E. Schatlen-
berger, ed. Curt. Topics Vet. Med. Anim. Sci.
20:325.
71 Smidt, D., and E. Farries. 1982. The impact of
lactational performance on post-partum fertility in
dairy cows. Factors influencing fertility in the
postpartum cow. H. Karg and E. Schallenberger,
ed. Curr. Topics Vet. Med. Anirn. Sci. 20:358.
72 Smith, J. F., E. Payne, H. R. Tewit, L. T. Mc-
Gowan, R. Fairclough, R. Kilgour, and P. G.
Goold. 1981. The effect of suckling upon the
endocrine changes associated with anoestrous in
identical twin dairy cows. J. Reprod. Fertil.
(Suppl.)30: 241.
73 Smith, R. D., W. Hansel, and C. E. Coppock. 1976.
Plasma growth hormone and insulin during early
lactation in cows fed silage based diets. J. Dairy
Sci. 59:248.
74 Smith, R. D., B. L. Perkins, C. J. Sniffen, and E. G.
Pearson. 1983. Body condition and fatty liver in
dairy cows - Is there a relationship with repro-
ductive performance? Page 20 in Proc. Cornell
Nutr. Conf., Cornell Univ., Ithaca, NY.
75 Smith T. R. Dairy Herd Profile Summary and
Analysis. 1986. Cornell Univ. Anita. Sci. Mimeo
Ser. 90:27.
76 Spalding, R. W., R. W. Everett, and R. H. Foote.
1975. Fertility in New York artificially insemi-
nated Holstein herds in dairy herd improvement. J.
Dairy Sci. 58:718.
77 Stevenson, J. S., and J. H. Britt. 1979. Relation-
ships among luteinizing hormone, estradiol, pro-
gesterone, glucocorticoids, milk yield, body weight
and postpartum ovarian activity in Holstein cows.
J. Anim. Sci. 48:570.
78 Stevenson, J. S., and E. P. Call. 1983. Influence o f
early estrus, ovulation, and insemination on
 SYMPOSIUM: INTERACTIONS OF NUTRITION AND REPRODUCTION
fertility in postpartum Holstein cows. Therio-
genology 19:367.
79 Stevenson, J. S., M. K. Schmidt, and E. P. CaU.
1983. Factors affecting reproductive performance
of dairy cows first inseminated after five weeks
postpartum. J. Dairy Sci. 66:1148.
80 Terqui, M., D. Chupin, D. Gauthier, N. perez, J.
Pelot, and P. Mauleon. 1982. Influence of man-
agement and nutrition on postpartum endocrine
function and ovarian activity in cows. Factors
influencing fertility in the postpartum cow. H.
Karg and E. Schallenberger, ed. Curr. Topics Vet.
Med. Anim. Sci. 20:384.
81 Thatcher, W. W., and C. J. Wilcox. 1973. Post-
partum estrus as indicator of reproductive status in
the dairy cow. J. Dairy Sci. 56:608.
82 Treacher, R. J., I. M. Reid, and C. J. Roberts.
1981. The effect of body condition at calving on
the development of fatty liver and metabolic
disease. Anita. Prod. 32:363.
83 Treacher, R. J., I. M. Reid, and C. J. Roberts.
1986. Effect o f body condition at calving on the
health and performance o f dairy cows. Anim. Prod.
43:1.
783
84 Trimberger, G. W. 1954. Conception rates in dairy
cattle from services at various intervals after
parturition. J. Dairy Sci. 37:1042.
85 van Houten, M., B. I. Posner, B. M. Kopriwa, and J.
R. Brawer. 1979. Insulin-binding sites in the rat
brain: in vivo localization to the circumventricuiar
organs by quantitative radiography. Endocrinology
105:666.
86 Whisnant, C. S., T. E. Kiser, F. N. Thompson, and
J. B. Hall. 1985. Effect of nutrition on the LH
response to calf removal and GnRH. Theriogenology
24:565.
87 Whisnant, C. S., T. E. Kiser, F. N. Thompson, and
C. R. Barb. 1986. Naloxone infusion increases
pulsatile iuteinizing hormone release in postpartum
beef cows. Domest. Anita. Endocrinol. 3:49.
88 Whitmore, H. L., W. J. Tyler, and L. E. Casida.
1974. Effects of early postpartum breeding in
dairy cattle. J. Anim. Sci. 38:339.
89 Wildman, E. E., G. M. Jones, P. E. Wagner, R. L.
Boman, H. F. Troutt, Jr., and T. N. Lesch. 1982. A
dairy cow condition scoring system and its re-
lationship to selected production characteristics. J.
Dairy Sci. 65:495.
Journal of Dairy Science Vol. 72, No. 3, 1989