BIOLOGY OF REPRODUCTION 49, 555-560 (1993)

Sustained Hormonal Responses of Siberian Hamsters (Phodopus sungorus) to a Single

Longer Day at Weaning'
CAROL S. WHALING,2 4' KIMBERLY K. KELLY, 5 CYNTHIA M. FINLEY,5 NORAH SPEARS, 3' 5 PAUL LICHT,4' 6
and IRVING ZUCKER4'5
Group in Endocrinology,4 Department of Psychology,5 and Department of Integrative Biology6
University of California, Berkeley, California, 94720
ABSTRACT
Siberian hamsters undergo gonadal development for several weeks after exposure to a single longer day at weaning. To
characterize changes in gonadotropin secretion after a single acute light stimulus, hamsters housed in a long photoperiod (16L:8D)
were given a single longer day (20L:4D) or maintained in the 16L:8D photoperiod at 19 days of age and transferred to a short
photoperiod (8L:16D) on Day 20. Elevated plasma FSH concentrations were detected in male hamsters at 5, 7, and 12 but not
at 17 days after the single longer day.
Melatonin treatment during light exposure and on two succeeding nights blocked the stimulatory effect of light on the reproductive axis; melatonin injections limited to one night were marginally effective. Pinealectomy during the dark phase of the
photocycle and the resultant truncation of the melatonin signal for one night did not stimulate a greater degree of gonadal
development than pinealectomy during the light phase. We conclude that the single extra 4-h light pulse at weaning alters
hypothalamic-pituitary function for approximately 2 wk. Trophic effects of the light pulse appear to be mediated by suppression
of melatonin secretion for several days; one truncated melatonin signal is not sufficient to simulate the effects of a single long
day on the reproductive axis.

INTRODUCTION
Day length is an important proximal cue used for phasing the seasonal reproductive rhythms of mammals. The
pineal gland transduces the effects of day length on the
neuroendocrine axis; variation in duration of nighttime
melatonin secretion controls photoperiodic responses in
several mammalian species [1]. Daily infusion of melatonin
to pinealectomized Siberian hamsters over the course of
several weeks simulates effects of different day lengths and
induces gonadal regression or development, depending on
the duration of the daily melatonin signal [2-6].
A single exposure to a 4-h light pulse at weaning has
long-term effects on testicular and somatic development in
Siberian hamsters [7]. The protracted effects of acute light
treatment suggest that photic cues induce long-term circadian [8] and neuroendocrine responses that outlast the
initiating light stimulus (cf. [7]). Thus, lengthening photoperiods around the time of weaning may initiate increased
gonadotropin secretion that can persist for several days even
if animals subsequently are not exposed to stimulatory long
photoperiods. The present study provides a test of this hypothesis.
The discovery that acute light exposure stimulates the
gonadal axis for several weeks allows further examination
Accepted April 3, 1993.
Received May 22, 1992.
'This research was supported by NIH grant HD-02982 and NSF grant DCB 904040576.
2
Correspondence: Dr. Carol Whaling, Department of Animal Physiology, University of California, Davis, CA 95616. FAX: (916) 752-6049.
3
Current address: Department of Physiology, Edinburgh University Medical School,
Teviot Place, Edinburgh EH8 9AG, Scotland, UK

555

of the neuroendocrine basis of photoperiodism. Exposure

to a single long day previously has been used to examine
photoperiodic control of gonadotropin secretion in Japanese quail (Coturnix coturnixjaponica) and Syrian hamsters (Mesocricetus auratus). Japanese quail housed in short
day lengths responded to a single long day (20L:4D) with
increased LH secretion. The LH response to light was amplified if birds were castrated to remove negative feedback
exerted by gonadal steroids. In castrated quail, plasma LH
concentrations increased within 30 h after the stimulatory
light signal and remained elevated for at least 10 days [9].
In castrated Syrian hamsters, a change in FSH was detected
3 days after exposure to a long photoperiod [10, 11]. In castrated Siberian hamsters, differences in plasma FSH concentration also were measurable after 3 days of repeated
exposure to a 14L:10D photoperiod but not after a single
long-day treatment [12]. In experiment 1, the goal was to
establish the temporal course of changes in gonadotropin
secretion in hamsters given an acute light stimulus. Accordingly, we measured FSH concentrations in intact Siberian hamsters after exposure to a single longer day.
Plasma and pineal melatonin concentrations of Siberian
hamsters are elevated during the dark phase of the light:dark
cycle [13]; even brief light exposure during the dark phase
acutely depresses melatonin synthesis and secretion [14].
Because shorter durations of melatonin secretion in Siberian hamsters are associated with gonadal growth [2, 3], we
speculated that the effect of the 4-h light pulse on the gonadal axis may be due to a depression in melatonin secretion that endures for several days [8,15]. This hypothesis
was tested in two different but complementary ways. In experiment 2a, we administered melatonin during the ex-

556

WVHALING ET AL.

tended light treatment and on the two succeeding nights.

If the pronounced effect of acute light exposure on the gonadal axis is contingent on sustained inhibition of melatonin secretion, then exogenous melatonin should counteract the effects of the extra 4-h light signal. Melatonin was
administered on three successive nights because suppression of melatonin synthesis appears to be sustained for a
least 36 h in light-interruption studies with rats [15]. To delimit this phenomenon, in experiment 2b, the experiment
was repeated with melatonin treatment restricted to only
one night.
In experiment 3, hamsters were pinealectomized during
the dark or light phases of the photocycle to determine
whether shortening of the melatonin signal on one night
can affect the gonadal axis. Pinealectomy during the dark
portion of the light:dark cycle truncates nocturnal melatonin secretion for one night and eliminates subsequent melatonin secretion. This permits a test of the hypothesis that
a single shorter melatonin signal is sufficient to stimulate
gonadal growth. This experiment also is relevant to the hypothesis that the long-term absence of a melatonin signal
achieved by pinealectomy is less stimulatory to gonadal
growth than the short melatonin signal effected when Siberian hamsters are transferred from short to long days (cf.
[16]).
MATERIALS AND METHODS
Siberian hamsters (Phodopus sungorus) were gestated
and maintained in a 16L:8D photoperiod until the day of
weaning (exact age reported below), at which time they
were housed singly in polypropylene cages (27 x 16 x 13
cm high), experimental interventions were performed, and
animals were transferred to a short photoperiod (8L:16D)
for the remainder of the experiment. Hamsters had ad libitum access to food (Mouse Chow #5015, Purina Mills, St.
Louis, MO) and water.
Experiment 1: FSH Secretion after a Single Light Pulse
Male hamsters were gestated and maintained in a 16L:8D
photoperiod, lights-on 0800-2400 h, PST. At 19 days of age,
some hamsters (n = 60) were exposed to 20L:4D by extending the normal 16-h light phase by 4 h, while others
(n = 57) remained in the 16L:8D photoperiod. On Day 20,
all animals were transferred to an 8L:16D photoperiod (lightson 0900-1700 h), where they remained until the experiment was completed. At 1130 h, 5, 7, 12, or 17 days after
exposure to the 20L:4D photocycle, animals were decapitated, and blood samples were collected in heparinized tubes
and centrifuged to separate plasma from red blood cells;
plasma was stored at -30 0C until assayed. Blood samples
12 and 17 days after the light treatment were collected from
anesthetized hamsters (sodium pentobarbital, 20 mg/animal 2-5 min prior to decapitation). FSH RIAs were performed with use of the NIAMDD rat FSH kit previously val-

idated for use in the Siberian hamster [17]. Samples were

run in two assays. Those collected 5 and 7 days after the
light treatment were assayed using FSH standard RP-2 with
an intraassay coefficient of variation of 15.4%. Samples collected 12 and 17 days later were assayed using FSH RP-1
(intraassay coefficient of variation of 23.7%). FSH values obtained with RP-2 were multiplied by 45 to correct for differences in potency according to NIAMMD specifications.
Data from the two assays were analyzed separately by means
of two-way ANOVA followed by two-tailed t-tests.
Experiment 2: Administration of Melatonin during Light
Treatment
a) Male hamsters were gestated and maintained postnatally in a 16L:8D photoperiod (lights-on 0500-2100 h)
until weaning (Days 18-20 of age). On the day of weaning,
animals were given a 4-h light extension (20L:4D; lights-on
0500-0100 h) on one day only. The day after the light treatment, animals were transferred to an 8L:16D photoperiod
(lights-on 0900-1700 h). They were autopsied 17 days later,
at which time they were between 35 and 37 days old.
On three consecutive nights, beginning the night of the
light pulse, hamsters received three nightly injections of
melatonin (Sigma Chemical Co., St. Louis, MO) or vehicle
(n = 10 and n = 9, respectively). Injections were performed at 1900, 2300, and 0300 h under dim red illumination. Melatonin was dissolved in ethanol and diluted with
saline to a final concentration of 10 [pg/0.1 ml ethanolic
saline per injection. Control hamsters received 0.1 ml of
the vehicle on the same schedule. Three injections were
given in an attempt to ensure that melatonin concentrations
would be elevated during the light pulse; injection times
bracketed the extended light pulse beginning 2 h before
and ending 2 h after the 4-h light extension. Because the
endogenous pattern of melatonin secretion after the light
treatment is not known, the interval for melatonin injection
was extended past the light treatment to prevent a decline
in plasma melatonin concentration before the onset of endogenous melatonin secretion.
A third group of hamsters (n = 9) that did not receive
a 4-h light pulse was transferred from the 16L:8D to an 8L:16D
photoperiod at the same time as the other two groups. These
hamsters were not treated with melatonin or saline. Animals in the three groups were equated for age at time of
transfer to the 8L:16D photoperiod (range 19.7-20.1 days).
b) A second experiment assessed the efficacy of one night
of melatonin treatment in blocking stimulatory effects of
light. The design was identical to that of experiment 2a. On
the night of the extended light pulse (20L:4D), hamsters
received three injections of melatonin or saline at 2-h intervals beginning 2 h before and ending 2 h after the 4-h
light extension. This experiment differed from experiment
2a in that melatonin injections were restricted to one night
whereas previously animals were treated for three consecutive nights.

SUSTAINED HORMONAL RESPONSE TO A SINGLE LONGER DAY

557

g
U)

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v,
Ca

0
.o

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(,

tL-

(D
{1}

a,

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co

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Wd
EL

Days after Light Treatment

FIG. 1. FSH concentrations (mean + SE) of male hamsters at varying
times after receiving a 4-h extension of the 16-h light phase (experimental)
or the usual 16-h light treatment (control) at 19 days of age. Hamsters were
maintained in 8L:16D after experimental treatments. *Indicates significant
difference between experimental and control groups.

The four groups tested consisted of male hamsters 1)

given the extended light treatment and melatonin injections (n = 13; two aberrant animals were eliminated from
the experiment); 2) given the extended light treatment and
saline injections, (n = 16); 3) given the extended light
treatment and no injections (n = 18); or 4) given no extended light treatment (16L:8D) on Day 18 and no injections (controls, n = 16).
Paired testes and body weights were recorded at autopsy. Data were analyzed with one-way ANOVA (experiment 2a) or two-way ANOVA (experiment 2b) followed by
planned comparisons using two-tailed t-tests.

FIG. 2. Testes and body weights at 36 days of age of hamsters that

received injections of melatonin or saline on 3 consecutive nights after a
4-h light pulse at 19 days of age. Control hamsters did not receive the light
pulse and were not injected. Before 19 days of age, all animals were kept
in a 16L:8D photoperiod. Beginning on the day after the extended light
treatment, all hamsters were kept in an 8L:16D photoperiod. *, **Indicate
significant differences from corresponding values of the saline group.

cedure. Anesthesia consisted of sodium pentobarbital (90

mg/kg i.p.), supplemented as necessary with methoxyflurane vapors. On Day 20, all hamsters were moved to an 8L:16D
photoperiod (lights-on 0400-1200 h). Testes and body
weights were obtained at 35 days of age.
Short-day photoperiod. Hamsters were gestated in a
16L:8D photoperiod (lights-on 2400-1600 h). Beginning on
the day of birth, dams and pups were housed in an 8L:16D
photoperiod (lights-on 0400-1200 h). On Day 19, males were
pinx or sham-pinx during the light phase (1000 h; n = 29)
or in the middle of the dark phase (2000 h; n = 23), 8 h
after onset of darkness. Other procedures were as described above. Autopsies were performed at 35 days of age.
Data were analyzed with one-way ANOVA and t-tests.
RESULTS

Experiment 3: Pinealectomy during the Light or Dark

Phase of the Photocycle
Long-day photoperiod. Hamsters were gestated in a
16L:8D photoperiod (lights-on 0100-1700 h). On Day 19,
animals were weaned, and males were assigned to treatment groups as follows: 1) pinealectomy (pinx) during the
dark period on Day 19, 4 h after lights-off (2100 h; n = 10);
2) sham-pinx at the same time (n = 6); or 3) pinx during
the light phase of the succeeding day (1100 h; n = 14).
Pinealectomies were performed by the method of Carter
and Goldman [2]. Sham-operated and pinx hamsters were
treated similarly except that the skull flap was not detached
during the sham procedure to prevent unintentional denervation of the pineal gland. To preclude photostimulation during the nighttime surgeries, hamsters were anesthetized under dim red light and their eye sockets occluded
with opaque black tape for the duration of the surgical pro-

Experiment I
There was a significant overall effect of the light pulse
on plasma FSH concentrations in hamsters kept in a long
photoperiod until weaning (F = 9.98; p < 0.005). Compared to untreated animals, male hamsters pulsed with light
at weaning had significantly elevated plasma FSH concentrations at 5 (p < 0.03), 7 (p < 0.02), and 12 (p < 0.05),
but not 17 (p > 0.05), days after light treatment (Fig. 1).
Experiment 2
a) The single 4-h photophase extension and melatonin
treatment each exerted significant effects on subsequent
testicular growth (F = 4.62;p < 0.05; Fig. 2). Animals given
the light pulse (saline group) had heavier gonads than unstimulated controls at 35 days of age (p < 0.05). More importantly, the testes of the melatonin-treated hamsters were

558

WHALING ET AL.

TABLE 1. Testes and body weights (means SEMI a 35 days of age.

Treatment*

N+

20L:4D
20L:4D
20L:4D
16L:8D

13
16
18
16

+ Mel
+ Sal
+ NI
+ NI

Testes weights (mg)

60
93
178
53

+ 10
+ 28
+ 50a
+ 58

Body weights (g)

22.3
23.4
24.3
23.9

+ 1.0
0.7
0.4
- 0.5

*At 18 days of age, hamsters were givin a 4-h light extension (20L:4D) or
kept in the 16L:8D photoperiod. Beginning 2 h before and ending 2 h after
the light extension, hamsters were injected three times with melatonin
(Mel) or saline (Sal), or were not injected (NI).
tN = Number of animales per group.
'Means with the same superscript are significantly different (p = 0.02).

0
0

0,

.0

(D
v
ns

FD

significantly lighter than those of saline-treated hamsters (p

< 0.05).
Body weights differed significantly among the three
treatment groups (Fig. 2; F = 3.64; p < 0.05). Melatonintreated hamsters weighed significantly less than their saline-treated counterparts (p < 0.05) and the untreated controls (p < 0.05) at 35 days of age. The differences in body
weights were much smaller than those in testes weights (9%
vs. 70%) in melatonin- compared with saline-treated hamsters.
b) The 4-h photophase extension had a marginal main
effect on testicular growth in short days (F = 2.52, p =
0.11); the main effect of injections was not significant (p >
0.40), but there were significant interaction effects of light
and injections (F = 3.60 and 8.28,p = 0.03 andp < 0.007).
Hamsters given the light pulse (20L:4D and no injection)
had heavier gonads than unstimulated controls (16L:8D and
no injection; p = 0.02, Table 1). Testes weights of hamsters
treated with melatonin were lower than those of vehicletreated controls, but the difference was not significant (p
= 0.28; Table 1). Photostimulated animals given vehicle had

E
CD
0

'ID

FIG. 3. Testes and body weights at 35 days of age of long-day hamsters pinealectomized or sham-operated during the dark (night pinx and
night sham) or light (day pinx) phase. Until 19 days of age, hamsters were
housed in a 16L:BD photoperiod. Beginning on Day 20, they were maintained in 8L:16D. *, **Indicate significant differences from corresponding
values of night sham group.

FIG. 4. Testes and body weights at 35 days of age of short-day hamsters pinealectomized or sham-operated during the dark or light phase.
Hamsters were kept in an 8L:16D photoperiod throughout the experiment.
Other conventions and symbols as in Figure 3.

lighter testes than similarly treated uninjected hamsters, but

this difference also was not significant (p = 0.15).
Experiment 3
Long-day photoperiod. There was a significant overall
effect on testes weights (F = 21.3;p < 0.005; Fig. 3). At 35
days of age, testes of hamsters sham-pinx on Days 19-20
were significantly lighter than those of pinx hamsters (p <
0.005). Testes weights of night- and day-pinx hamster were
not significantly different (p > 0.2) and were comparable
to those of animals given a single 4-h light pulse on Day
19 (553 + 68 [7]).
There was a significant overall effect on body weight (F
= 7.4; p < 0.003; Fig. 3). Body and testes weights followed
the same trend: they were indistinguishable for the two pinx
groups (p > 0.2) and higher in pinx than in sham-operated
animals (p < 0.01).
Short-day photoperiod. There was a significant treatment effect on testes weights (F = 36.9;p < 0.005; Fig. 4).
Testes weights of day- and night-pinx hamsters were indistinguishable (p > 0.5) and significantly heavier than those
of corresponding sham-pinx hamsters (p < 0.001 for each
comparison). Hamsters sham-pinx at the two time points
had similar testes weights (p > 0.2). As in long days, the
mean testes weights at 35 days of age of day- and nightpinx hamsters were similar to those of animals exposed to
32 h of continuous light at weaning [18].
There was a significant treatment effect on body weight
(F = 13.3;p < 0.005; Fig. 4). Body weights were similar in
animals pinx during the day and night (p > 0.5). Males
pinx at night weighed more than their sham-pinx counterparts (p < 0.005) as did day-pinx hamsters, but the latter
difference fell short of significance (p = 0.07).

SUSTAINED HORMONAL RESPONSE TO A SINGLE LONGER DAY

DISCUSSION
Exposure on one day only to an extra 4-h light pulse
was sufficient to elevate plasma FSH concentrations in young
male Siberian hamsters transferred to a short photoperiod.
Hypothalamic-pituitary function was altered for approximately two weeks by the 4-h light pulse. Plasma FSH concentrations were elevated 12 days later but were indistinguishable from control values after 17 days (at 35 days of
age). The FSH response is reflected in testis weight: a single
4-h light pulse at weaning stimulated testicular growth that
was measurable 17 days later (testis data for these subjects
reported in Fig. 3 (p. 639) of Spears et al. [7]). The decline
in FSH concentrations by 35 days of age in both control
and experimental animals parallels FSH profiles of hamsters reared in long days (16L:8D) from birth. FSH concentrations increase to a peak at approximately 25 days of age
and then decline to baseline by 50 days of age [17].
The stimulatory effects of light were blocked by administration of melatonin during the 4-h light pulse and on two
subsequent nights; testes weights of light-treated hamsters
injected with melatonin were indistinguishable from those
of control animals not given the extended light treatment.
Although the comparison was not planned, hamsters given
the 4-h light pulse but no injections had heavier gonads
than similarly treated animals that received melatonin injections on one night only (p = 0.03). The planned comparisons indicated a nonsignificant attenuation of the briefer
melatonin treatment on testes weights. Overall, these results suggest that briefer melatonin treatment (1 day) is at
best marginally effective in blocking the effects of the light
pulse on the gonads. We suggest that the 4-h light pulse
stimulates FSH secretion and subsequent gonadal growth
by decreasing melatonin secretion for several days. One
truncated melatonin signal, induced by nighttime pineal extirpation, likewise did not differentially increase gonadal
growth. The duration of the melatonin signal may have to
change for several days to influence gonadal development:
e.g., in Siberian hamsters, two or more long duration melatonin signals on consecutive nights were required to inhibit testicular development [19], and melatonin administration to pregnant Siberian hamsters on two consecutive
nights but not on one night during the latter phase of gestation affected postnatal testicular development in the offspring [20]. These data all point to the conclusion that two
or more nights of altered melatonin secretion are necessary
and sufficient to induce changes in the male reproductive
system (cf. [21]).
Pinealectomy was in every instance associated with increased gonadal weights; this was expected because in the
absence of nightly long-duration melatonin signals, testes
of Siberian hamsters undergo gradual development [2, 3].
Long-day hamsters pinealectomized on Day 19 had substantially heavier testes at 35 days than their similarly treated
short-day counterparts. Responsiveness to day length de-

559

velops around 15 days of age [22-24]. Presumably the exposure to long days during the few days immediately preceding pinealectomy had initiated the process of gonadal
growth, which was then maintained in the absence of further influence of pineal secretions.
Short-day hamsters pinealectomized at 19 days of age
(present experiment) underwent substantially more testicular growth by Day 35 (150 mg) than did similar animals
pinealectomized on Day 23 (48 mg;) [3]. Because the interval between pinealectomy and autopsy differed, the discrepancy may be more apparent than real. Several findings
([3, 25], Kelly and Zucker, unpublished observations) indicate, however, that pinealectomy has far more pronounced
effects on testicular growth of younger than older Siberian
hamsters. The basis for this age-related effect remains to be
elaborated; it could reflect the animals' photoperiodic history at the time of pinealectomy rather than age per se.
ACKNOWLEDGMENTS
We thank Sushama Pavgi, Chris Tuthill, Kim Pelz, Rick Lauraya, and Cecile Gunn
for excellent technical assistance.

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