BIOLOGY OF REPRODUCTION 23, 1061-1068 (1980)

Photoperiodic Control of Seasonal Breeding in Ewes:

Modulation of the Negative Feedback Action of Estradiol1’2

S. J. LEGAN3 and F. J. KARSCH4

Reproductive Endocrinology Program,

Departments of Physiology and Pathology,
The University of Michigan,
Ann Arbor, Michigan 48109

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ABSTRACT

In ewes, a pivotal neuroendocnine event regulating seasonal breeding is a change in response of

the hypothalaino-pituitary axis to the negative feedback action of estradiol. Further, the major
environmental parameter regulating seasonal breeding is photopeniod. This study was performed to
examine whether changes in photoperiod regulate breeding seasons by modulating response to
steroid feedback. Six intact ewes, five estradiol-treated ovariectomized ewes, and one vasectomized
ram were housed under artificial short-day (8L: 16D) and long-day (16 L:8D) photoperiods which
were alternated every 90 days. Under these conditions, the intact ewes underwent two breeding
and anestrous seasons in 1 year. Further, the transitions between breeding seasons coincided with
striking fluctuations in serum LH (between <0.3 and 10 nglml) and FSH (50-170 ng/ml) in the
estradiol-treated ovaniectomized ewes, long days causing anestrus and an increased response to
estradiol (low LH and FSH), short days resulting in breeding season and a decreased response to
estradiol (high LH and FSH). Similar results were obtained in identical groups of ewes, which were
subjected to 120-day alternations between long and short days, except that there were only three
seasonal transitions and FSH was not measured. These results provide strong support for the
hypothesis that in ewes the mechanism whereby photopeniod regulates seasonal breeding includes
modulation of response to the negative feedback action of estradiol on gonadotropin secretion.

INTRODUCTION was performed to determine whether the

striking seasonal variations in response to
Under natural environmental conditions,
estradiol, postulated to control seasonal breed-
there is a dramatic seasonal variation in the
ing, are dictated by environmental photoperiod,
negative feedback action of estradiol on LU
the major environmental factor controlling the
secretion in the ewe (Legan et al., 1977).
annual reproductive cycle of ewes (Yeates,
During anestrus, estradiol is a potent inhibitor
of LH secretion, whereas in the breeding season 1949, Hafez, 1952; Maul#{233}on and Rougeot,

it is much less effective in this regard. These 1962; Thwaites, 1965; Ducker and Bowman,
1970; Ducker et al., 1970; Newton and Betts,
fluctuations in response to estradiol coincide
1972).
with transitions between breeding and anes-
trous seasons, and they appear to be a pivotal
MATERIALS AND METHODS
neuroendocrine event governing seasonal breed-
ing (Legan et al., 1977; Legan and Karsch, Six intact six ovariectomized
ewes, ewes treated
with s.c. implants containing estradiol- 17(3, and one
1979; Goodman and Karsch, 1980). This study
vasectomized ram were housed in each of two adjacent
photoperiod-controlled rooms (as described below)
beginning on November 21, 1976. The animals, which
were predominantly Suffolk breed, were fed once
Accepted September 24, 1980. daily (0-3 h after lights on) with hay supplemented
Received June 25, 1980. with grain; water was supplied ad libitum. In addition,
‘Portions of these data have appeared in Fed. Proc. a group of 14 intact, untreated ewes was maintained
37, 297 (1978) and BioL Reprod. 20, 74-85. (1979). outdoors in natural conditions of photoperiod and
2This work was supported by NIH Grant HD-083 33 temperature.
and HD-12450. Light was provided by four 40-W fluorescent bulbs,
3Present address: Department of Physiology and and the intensity, measured within 15 cm of the floor,
Biophysics, University of Kentucky, Lexington, KY ranged from 88 lx in the corners to 350 lx under the
40536. lights in each room. Temperature was controlled but
4Send reprint requests to Dr. F. J. Karsch, Depart- not kept constant. The daily average ranged from
ment of Pathology, The University of Michigan, Ann 9340 C and fluctuated according to the natural
Arbor, MI 48109. seasonal pattern. Temperature was recorded continu-

1061
1062 LEGAN AND KARSCH

ously in each room with an Esterline-Angus Minigraph (May 24), whereas those subjected to 120-day alterna-
Recorder, which also monitored time of daily onset of tions were sheared in short days (June 15).
light and dark. In addition, to monitor the occurrence To monitor occurrence of breeding and anestrous
and duration of power failures, the power supply for seasons, the brisket of each vasectomized ram was
each room was connected to a separate clock. The covered with a mixture of paint pigment and motor
rooms also had separate air intake and exhaust ducts oil, and the intact ewes were observed once daily for
which were baffled to prevent light leaks. The rooms signs of estrous behavior (paint mark on center of
were checked every 90 days for light leaks, which rump). In addition, the presence or absence of ovula-
were sealed to ensure total darkness when lights were tion was verified by measurement of serum progester-
out. one in jugular venous samples obtained twice weekly.
The animals were exposed to either long-day The progesterone assay (Foster et al., 1975) had a

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photopeniods (16L:8D) or short-day photopeniods limit of detection, defined as 2 SDs from the buffer
(8L:16D); lights always came on at 0600 h. Beginning control, averaging 0.05 ng/ml, and an intenassay
with long days in both rooms, the photoperiod was coefficient of variation (CV) averaging 8%. Anestrus
alternated abruptly at 120-day intervals in one room, was defined as the interval between last and first
and 90-day intervals in the other room. The animals ovulation.
subjected to 90-day changes in photopeniod were To assess response to the negative feedback action
sheared on the day of a shift to long-day photoperiods of estradiol, LH was measured in sera obtained from

, I I

NATURAL PHOTOPERIOD_______________
:0 : I - I I nI4

z
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0
(I)
____ ARTIFICIAL PHOTOPERIOD

1J 1L
Ui
Ui

2’
I
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Li
U,

I DAY SHIFT1JJSL INTACT

NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN FEB
1977 1978
FIG. 1. Timing of breeding seasons in intact ewes and changes in LH in estradiol-treated ovariectomized ewes
(OVX + E). Upper panel: Occurrence of estrous cycles in 14 intact ewes exposed to natural environmental
photopeniod. Middle panel: Occurrence of estrous cycles in 6 intact ewes housed under abrupt 90-day alterna-
tions of long-day (16L:8D) and short-day (8L:16D) artificial photoperiods. Lower panel: Mean + SEM serum LH
concentrations in 5 OVX + E ewes subjected to the same regimen of artificial photoperiods. The open and closed
portions of the bars subtending each panel represent the relative number of hours of light and dark, respectively,
per day. Onset of breeding season in individual ewes defined as first ovulation: onset of anestrus defined as
last ovulation.
 PHOTOPERIODIC CONTROL OF SEASONAL BREEDING IN EWES 1063

the estradiol-treated ovariectomized ewes three times steroid length) as described by Karsch et al. (1973).
weekly. We employed an LH radioimmunoassay Such implants were determined in an earlier study to
(Niswender et aL, 1969) modified as described pre- maintain physiologic serum estradiol levels of 3-5
viously (Hauger et al., 1977), with a limit of detection pg/mi for at least 1 year (Legan em al., 1977). The
which averaged 0.28 ng/ml for 200 zl serum and an implants were exchanged for new ones after 1 year.
interassay CV of 10%. LH is expressed in terms of
nanograms NIH-LH-S12 per milliliter. In addition, RESULTS
serum FSH concentrations were measured in selected
samples using a modification (Goodman em al., 1981) Under natural photoperiods, the breeding
of a radioimmunoassay described by L’Hermite em al. season began in late August and ended in late
(1972). The limit of detection averaged 3 ng/ml for January, on the average (Fig. 1, upper panel).

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200 M1 serum and the interassay CV was 10%. FSH is
However, when intact ewes were exposed to 90-
expressed in terms of nanograms NIH-FSII-S8 per
day alternations of artificial long-day (16L:8D)
milliliter. In addition to measuring FSH in ewes
housed in the rooms, FSH was monitored throughout and short-day (8 L: 1 6D) photoperiods, the trans-
the year in both untreated and estradiol-treated itions between breeding and anestrous seasons
ovaniectomized ewes maintained outdoors. These ewes became entrained to 90-day intervals, resulting
had been used in a previous study, and their LH
in two breeding and two anestrous seasons in 1
concentrations are described by Legan et al. (1977).
The estradiol implants were constructed of Silastic year (Fig. 1, middle panel). Thus each exposure
tubing (3.35 mm id., 4.65 mm o.d., 37 mm packed to a long-day photoperiod caused a shift to

z
-J

0
U)
Li

Iii

0’
C

I
-J

Li
(I)

NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN FEB
1977 1978
FIG. 2. Timing of breeding seasons and response to estradiol negative feedback under natural environmental
photoperiod and under artificial photoperiods which were alternated between long and short days every 120
days. See legend to Fig. 1 for details. The broken line in the lower panel represents serum LH concentrations in
one ewe, which responded 1 month earlier than the others. Onset of breeding season in individual ewes defined
as first ovulation; onset of anestrus defined as last ovulation.
1064 LEGAN AND KARSCII

anestrus whereas short-day photoperiods elicit- ovariectomized ewes housed in a separate room
ed onset of the breeding season, regardless of and exposed to 120-day alternations between
whether a given change in photoperiod oc- long and short days (Fig. 2). At the end of 1
curred during the natural breeding or anestrous year, therefore, the ewes in the two rooms were
season. out of phase with each other, those in one
Such photoperiodic entrainment of breeding room undergoing a transition to breeding
seasons was mirrored by coincident changes in season and high serum LII levels, the sheep in
circulating LII in the estradiol-treated ovariec- the other room switching to anestrus and low
tomized ewes housed in the same room (Fig. 1, serum LII concentrations.

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lower panel). Each transition to anestrus Patterns of serum FSI-I in estradiol-treated
induced by long days was accompanied by a ovariectomized ewes paralleled those of LII.
simultaneous decrease in LII in ovariectomized Under natural photoperiods, transitions to
ewes. Each short-day-induced onset of breeding breeding season or anestrus in intact ewes were
season coincided with an increase in LII. accompanied by marked increases or decreases,
Similar results were obtained in an addi- respectively, in serum FSII levels in estradiol-
tional group of intact and estradiol-treated treated ovariectomized ewes (Fig. 3). In con-

-I-

0
z 100
-J
C-)
>-
0
C/)
LU
50
LU

500

E 200 OVX+E2 (6)

FSH

I 100 I0
(.1)
Li
5 E
50
D

LU I
U) I -J

05
LU
(J)
I I I I I - I I I I I

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT
1976
FIG. 3. Annual variation in breeding seasons in 14 intact ewes (histogram, upper panel) and in serum FSH
concentrations (mean + SEM, n = 6/group) in ovariectomized (OVX) ewes treated with empty implants or
implants containing estradiol (E2 ). Mean serum LH concentrations, measured in the same samples from the OVX +
E2 ewes, are shown for reference by the thin solid line (redrawn from Legan em al., 1977). The open and closed
areas of the bar subtending the lower portion of the figure represent relative hours of light and dark per day.
 PHOTOPERIODIC CONTROL OF SEASONAL BREEDING IN EWES 1065

trast, there was no comparable seasonal varia- annual reproductive cycle in ewes maintained
tion in FSH in ovariectomized ewes treated outdoors (r = -.056, P<0.05). Onset of anestrus
with empty implants. Further, the natural occurred sooner when photoperiod was switched
annual pattern of response of FSH to estradiol to long days in the high ambient temperatures
was shortened to a period of 180 days by prevailing during the normal anestrus season.
exposing estradiol-treated ovariectomized ewes Thus, last ovulation was 17 days, on the aver-
to abrupt, 90-day alternations between artificial age, after onset of long days in the warmer
long-day and short-day photoperiods (Fig. 4). temperatures of the anestrous season (May),
Thus, exposure to short days resulted in an whereas the latent period for this transition

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increase in serum FSH; long-day photoperiods averaged 41 days in the colder temperatures of
caused a decrease in FSH. the natural breeding season (November).
The latent period of photoperiod-induced
transitions to breeding season, defined as the
interval from the beginning of short days to first DISCUSSION

ovulation, was relatively constant throughout The foregoing observations reinforce previ-
the experiment. Regardless of the ambient ous conclusions that photoperiod is the major
temperature, the period of the entraining environmental “Zeitgeber” for entrainment of
rhythm in photoperiod, or the stage of the seasonal reproductive function in the ewe
seasonal cycle of ewes maintained outdoors, (Yeates, 1949; ilafez, 1952), as is the case in
onset of the breeding season occurred on the the ram (Lincoln, 1977) and in many other
average 55 days after the onset of short days species (Follett, 1978; Turek and Campbell,
(Fig. 5; elevated mean in May due to one ewe 1979). These results further demonstrate a
with extremely long latent period of 90 days). photoperiodic control of the marked seasonal
There was no significant correlation (Snedecor shift in the capacity of a fixed level of estradiol
and Cochran, 1967) between temperature and to inhibit gonadotropin secretion, reflected by
latent period for the transition to breeding the waxing and waning of serum gonadotropins
season (r = 0.01, P>0.05). On the other hand, in ovariectomized ewes treated with estradiol.
the latent period for onset of anestrus (interval Long days, which cause anestrus, heighten
from beginning of long days to last ovulation) responsiveness to the negative feedback of
varied in relation to temperature or stage of the estradiol; short days, which lead to the breeding

I -
z 100
-J INTACT

Li

Li
0 1___

300
0’
C

I
U,
U-

Li
U,

NOV DEC JAN FEB MAR APR MAY JUN JUL AUC SEP OCT NOV DEC JAN FEB
l977 1978

FIG. 4. Photoperiodic entrainment of breeding seasons in intact ewes (upper panel) and response to FSH to
estradiol negative feedback in ovariectomized ewes (lower panel). Serum FSH concentrations (mean + SEM) are
from the same ewes for which LH is illustrated in the lower panel of Fig. 1. See legend to Fig. 1 for details.
1066 LEGAN AND KARSCH

Bush, 1955). In our study, however, a signifi-

0 cant correlation between temperature (and/or
0
season) and latent period was observed only in
Lu
response to inhibitory photoperiods, i.e., during
the transition to anestrus. A similar modulation

I-.-- of inhibitory but not stimulatory photoperiods

4
-J by temperature was observed in male hamsters
(Desjardins and Lopez, 1980). The absence of
an effect of temperature on the photoperiod-

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induced onset of the breeding season in our
U C,
0 z study may be due to the period of the artificial
-J
C.) rhythm of seasonal breeding which has already
Lu >-
I- U maximally accelerated this transition. Alterna-
tively, the attenuated, gradual changes in
temperature in our study may not constitute a
FIG. 5. Annual variation in temperature (lower sufficient signal to advance the breeding season.
panel) and in latent period to onset of breeding season In this regard it is interesting that with respect
(BS) or anestrus (upper panel). The latent period is to photoperiodic entrainment, the shortest
defined as the interval from onset of artificial long or
latent periods are achieved by the largest, most
short days to last or first ovulation, respectively, in
the intact ewes maintained under 90- or 120-day shifts abrupt changes (Ducker and Bowman, 1970;
in artificial photoperiod. Each point represents the Docker et al., 1970; Newton and Betts, 1972).
mean ( SEM) of 6 ewes. In the lower panel, the Finally, the seasonal change in responsive-
points represent monthly means of an average of the
ness to estradiol negative feedback in the ewe is
daily maxima and minima of temperature for both
exerted not only on LII, as described by Legan
rooms. A histogram of the annual pattern of seasonal
breeding in 14 intact ewes housed in natural photo- et al. (1977), but also on FSII secretion.
periodic conditions is redrawn from Figs. 1 and 2 for Considerable evidence suggests that the change
comparison. in feedback control of LII is a pivotal neuro-
endocrine event regulating the seasonal onset
and cessation of estrous cycles in the ewe
(Legan and Karsch, 1979; Goodman and
season, decrease the effect of estradiol. Such Karsch, 1980). Although it remains to be
photoperiodic entrainment of changes in determined what physiologic role, if any,
steroid negative feedback has also been ob- seasonal changes in FSII play in this regard, it
served in rams (Pelletier and Ortavant, 1975) appears that FSII levels in intact ewes are not
and in golden hamsters in which short days are lowered in anestrus (Walton et al., 1977), and
inhibitory and long days stimulatory to gonadal the follicles appear to be competent to respond
function (Tamarkin et al., 1976; Turek, 1977). to LII at this time (Scaramuzzi and Baird,
Although photoperiod is the major “Zeit- 1977; Goodman and Karsch, 1980; McNeilly et
geber,” it is possible that other factors can al., 1980). Nevertheless, recent evidence sug-
modify its effect. Such modulation is suggested gests that the follicular response to LII may
by the variation in latent periods for the decline during the transition to anestrus (Legan
photoperiodically-induced transition to an- et al., 1980). Whatever the role of FSH may be,
estrus. The onset of anestrus was hastened the present observations provide further sup-
during the natural anestrous season, at times port for the hypothesis that the endocrine basis
when ambient temperature was relatively high. of the natural process of reversible fertility has,
This observation suggests that seasonal breeding at its core, a photoperiodically controlled
in the ewe might be influenced by environ- modulation of the brain and/or pituitary to
mental temperature and/or an endogenous gonadal steroid feedback (Hoffmann, 1973).
circannual rhythm. Concerning the former, it is
of interest that although fluctuations in tem-
ACKNOWLEDGMENTS
perature cannot in themselves drive seasonal
We are indebted to Dr. Douglas L Foster for his
reproductive function in the face of constant
assistance in designing this study. We would like to
photopeniod (Wodzicka-Tomaszewska et al.,
thank Ms. Marjorie Hepburn and Ms. Barbara Glover
1967), temperature can modulate the timing of for their expertise in conducting the radioimmuno-
the transition to breeding season (Dutt and assays, and Dna. G. D. Niswender and L E. Reichert,
 PHOTOPERIODIC CONTROL OF SEASONAL BREEDING IN EWES 1067

Jr., for providing reagents used in the radioimmuno- ing hormone secretion in the Rhesus monkey.
assays. We also thank Mr. Douglas Doop for designing, Endocrinology 92, 799-804.
constructing, and maintaining the photoperiod-con- Legan, S. J., Goodman, R. L, Ryan, K. D., Foster, D.
trolled rooms, and for his invaluable assistance in all C. and Karsch, F. J. (1980). Transition into
aspects of the animal experimentation. seasonal anestrus in the ewe: Decreased tonic
LH secretion or decreased ovarian response to
LII? In: Physiologic Cessation of Ovarian Func-
REFERENCES tion. Proceedings of the Dynamics of Ovarian
Desjardins, C. and Lopez, M. J. (1980). Sensory and Function 1980 Workshop, Ann Arbor, MI,
nonsensory modulation of testis function. In: August 9-11, 1980. (N. B. Schwartz and M.
Testicular Development, Structure, and Func- I-Iunzicker-Dunn, eds.). Raven Press, New York.

Downloaded from https://academic.oup.com/biolreprod/article/23/5/1061/2766974 by guest on 22 September 2020

tion. (A. Steinberger and E. Steinberger, eds.). In Press.
Raven Press, New York. pp. 381-388. Legan, S. J. and Karsch, F. J. (1979). Neuroendocrine
Ducker, M. J. and Bowman, J. C. (1970). Photo- regulation of the estrous cycle and seasonal
periodism in the ewe. 3. The effects of various breeding in the ewe. Biol. Reprod. 20, 74-85.
patterns of increasing daylength on the onset of Legan, S. J., Karsch, F. J. and Foster, D. L. (1977).
anoestrus in Clun Forest ewes. Anim. Prod. 12, The endocrine control of seasonal reproductive
46 5-471. function in the ewe: A marked change in re-
Ducker, J. J., Thwaites, C. J. and Bowman, J. C. sponse to the negative feedback action of estra-
(1970). Photoperiodism in the ewe. 2. The diol on luteinizing hormone secretion. Endocrin-
effects of various patterns of decreasing day- ology 101, 818-824.
length on the onset of oestrus in Clun Forest L’Hermitc, M., Niswender, G. D., Reichert, C. E., Jr.
ewes. Anim. Prod. 12, 115-123. and Midgley, A. R, Jr. (1972). Serum follicle
Dutt, R. II. and Bush, L. F. (1955). The effect of low stimulating hormone in sheep as measured
environmental temperature on initiation of the by radioimmunoassay. Biol. Reprod. 6, 325-
breeding season and fertility in sheep. J. Anim. 332.
Sci. 14, 885-896. Lincoln, G. A., Peet, M. J. and Cunningham, R. A.
Follett, B. K. (1978). Photoperiodism and seasonal (1977). Seasonal and circadian changes in the
breeding in birds and mammals. In: Control of episoiic release of follicle-stimulating hormone,
Ovulation. (D. B. Crighton, G. R. Foxcroft, lutcinizing hormone and testosterone in rams
N. B. llaynes and G. E. Lamming, eds.). Butter- exposed to artificial photoperiods. J. Endocrinol.
worths, London. pp. 267-293. 72, 33 7-349.
Foster, D. L, Lemons, J. A., Jaffe, R. B. and Nis- Maukon, P. and Rougeot, J. (1962). Rgulation des
wender, G. D. (1975). Sequential patterns of saisons sexuelles chez des brebis de races differ-
circulating luteinizing hormone and follicle-stim- entes au moyen de divers rythmes lumineux.
ulating hormone in female sheep from early Ann. Biol. Anim. Biochim. Biophys. 2, 209-222.
postnatal life through the first estrous cycles. McNeilly, A. S., O’Connell, M. and Baird, D. T.
Endocrinology 97, 985-994. (1980). Induction of ovulation by pulsatile
Goodman, R. L and Kansch, F. J. (1980). Control of injection of LII in anoestrous ewes. Biol. Reprod.
seasonal breeding in the ewe: Importance of 22 (Suppl. 1), 48A, Abstr. 55.
changes in response to sex-steroid feedback Newton, J. E. and Betts, J. E. (1972). A comparison
In: Progress in Reproductive Biology. Vol. 5 (R. between the effects of various photopeniods on
J. Reiter and B. K. Follett, eds.). S. Karger, Basel. the reproductive performance of Scottish half-
pp. 134-154. bred ewes. J. Agric. Sci. 78, 425-43 3.
Goodman, R. L., Pickover, S. M. and Karsch, F. J. Niswender, G. D., Reichert, C. E., Jr., Midgley, A. R.,
(1981). Ovarian feedback control of follicle- Jr. and Nalbandov, A.V. (1969). Radioimmuno-
stimulating hormone in the ewe: Evidence for assay for bovine and ovine luteinizing hormone.
selective suppression. Endocrinology. In Press. Endocrinology 84, 1166-1173.
Hafez, E.S.E. (1952). Studies on the breeding season Pelletier, J. and Ortavant, R. (1975). Photoperiodic
and reproduction of the ewe. J. Agnic. Sci. 42, control of LII release in the ram II. Light-andro-
189-265. gens interaction. Acta Endocrinol. 78, 442-450.
Hauger, R L, Karsch, F. J. and Foster, D. L. (1977). Scaramuzzi, It. J. and Baird, D. T. (1977). Pulsatile
A new concept for control of the estrous cycle of release of luteinizing hormone and the secretion
the ewe based on temporal relationships between of ovarian steroids in sheep during anestrus.
luteinizing hormone, estradiol and progesterone Endocrinology 101, 1801-1806.
in peripheral serum and evidence that proges- Snedecor, G. W. and Cochran, W. G. (1967). Statistical
terone inhibits tonic LII secretion. Endocrin- Methods. 6th Ed. Iowa State University Press,
ology 101, 807-817. Ames.
Hoffmann, J. C. (1973). Light and feedback control of Tamarkin, C., hlutchison, J. S. and Goldman, B. D.
gonadotropin secretion. In: Proceedings of the (1976). Regulation of serum gonadotropins by
IVth International Congress of Endocrinology, photoperiod and testicular hormone in the
Washington, D. C., June 18-24, 1972. (R. 0. Syrian hamster. Endocrinology 99, 1528-1 533.
Scow, ed). Excerpts Med. Int. Congr. Sen. 273. Thwaites, C. J. (1965). Photoperiodic control of
Elsevier, New York pp. 886 -890. breeding activity in the Southdown ewe with
Karsch, F. J., Dierschke, D.J., Weick, R. F., Yamaji, T., particular reference to the effects of an equator-
Hotchkiss, J. and Knobil, E. (1973). Positive and ial light regime. J. Agric. Sci. 65, 57-64.
negative feedback control by estrogen of luteiniz- Turek, F. W. (1977). The interaction of photoperiod
1068 LEGAN AND KARSCH

and testosterone in regulating serum gonado- oestrus to breeding activity. J. Endocrinol. 75,
tropin levels in castrated male hamsters. Endo- 127-1 36.
crinology 101, 1210-1215. Wodzicka-Tomaszewska, 1st., Hutchinson, J.CD. and
Turek, F. W. and Campbell, C. S. (1979). Photo- Bennett, J. W. (1967). Control of the annual
periodic regulation of neuroendocrine-gonadal rhythm of breeding in ewes: Effect of an equa-
activity. Biol. Reprod. 20, 32-50. torial daylength with reversed thermal seasons. J.
Walton, J. S., McNeilIy, J. R., McNeilly, A. S. and Agnic. Sci. 68, 61-67.
Cunningham, F. J. (1977). Changes in concen- Yeates N.T.M. (1949). The breeding season of the
trations of follicle-stimulating hormone, lutein- sheep with particular reference to its modifica-
izing hormone, prolactin and progesterone in the tion by artificial means using light. J. Agnic.
plasma of ewes during the transition from an- Sci. 39, 1-43.

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