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Photoperiodic control of
reproductive behavior and
physiology of the male
Japanese Quail
Article in Hormones and Behavior July 1969
DOI: 10.1016/0018-506X(69)90002-6

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Hormones and Behavior 1, 7-24 (1969)

Photoperiodic Control of Reproductive Behavior and Physiology

of the Male Japanese Quail (Coturnix coturnix juponica)
BENJAMIN D. SACHS
Department of Psychology, University of California, Berkeley California 94720

The effects of changes in day length on the reproductive condition of

the male Japanese quail (Coturrzix coturnix ~uponicu) were investigated in an
experiment in which several measures of sexual behavior, size of cloacal protrusion, and amount of cloacal foam were the dependent variables. Thirtysix laboratory-raised male cotumix, 6 or 12 months old, were tested on
alternate days throughout the experiments three phases, during which the
experimental groups received different combinations and sequences of long
days (16 hr light: 8 hr dark) or short days (8L:16D), testosterone propionate (TP) or no hormone, castration or sham castration.
The several measures of reproductive condition were highly correlated,
reflecting the same trends. Short days brought males out of breeding condition (in 10-20 days) if they had been maintained in long days. Long days
sustained peak reproductive condition, or returned males to breeding condition (in 10-15 days) if they had been maintained in short days. The breeding condition of the lZmonth-old
males was, relative to that of the
6-month-old males, more readily stimulated by long days and less readily
inhibited by short days. A long-light cycle of only 3 days duration exerted a
stimulatory effect on reproductive condition for several days afterward. The
breeding condition of the males was never insensitive to long days, suggesting that adult male coturnix are nonphotorefractory.
TP prevented the effects that transfer from long to short days had on
sexual behavior and the cloacal protrusion, but TP caused regression of the
testes. Similarly, TP given to males maintained in short photoperiods yielded
the same effects as did transfer to long days, except that it was effective
Sooner (l-5 days) and also caused testicular regression. TP-induced regression
of the testes was reversible by withdrawing the hormone and shifting the
males to long photoperiods.

The crucial role of light in the regulation of reproductive

cycles in animals has been the subject of experimental
study for over 40 years. Still most
of our knowledge
on photoperiodic
control of reproduction
in birds comes
from research on temperate zone passerines. This limitation
has restricted our
understanding
of the nature of photoperiodic
control of breeding cycles in
Present address: Department
Connecticut 06268.

of Psychology, University of Connecticut,

7
Copyright @ 1969 by Academic Press, Inc.

Storrs,

SACHS

non-passerine birds. For example, Farner (1959), in one of his reviews of

work on photoperiodic control of avian gonadal cycles, avoided consideration
of egg production in domestic fowl because . . . the mechanism of photoperiodicity in a domestic species of essentially tropical origin may be only
superficially similar to that of a Temperature Zone wild species. These differences among the species may stem from differences in domesticity, climatological origin, or biological make-up. Cotumiv cotumti, as a gallinaceous bird
of nontropical origin, may be a useful species to help sort out these potential
sources of differences.
The experiment to be reported here had two main objectives:
(I) To test the photosensitivity

of the reproductive

condition

of male

cotumix.

It has been shown previously (Wilson, Abplanalp, and Arrington, 1962;

Tanaka, Mather, Wilson, and McFarland, 1965; Follett and Farner, 1966) that
the rate of sexual maturation of juvenile quail is approximately proportional
to the number of continuous hours of light each day under which they are
reared. However, apart from work on a diurnal variation in gonadotropin secretion (Tanaka, Wilson, Mather, and McFarland, 1966; Konishi and Kato,
1967; Follett and Farner, 1966) little other experimental evidence is available
on the response of adult male coturnix to changes in photoperiod.
(2) To relate this photosensitivity to the changes in the reproductive condition
of cotumix that follow castration and androgen replacement.
The copulatory behavior of coturnix males is abolished by castration
and restored by testosterone replacement (Beach and Inman, 1965). Do appropriate changes in photoperiod have effects similar to those of castration
and androgen replacement and, conversely, does appropriate hormone treatment simulate the effects of changes in photoperiod? How do changes in the
coturnix males copulatory behavior covary with changes in its cloacal gland
and other more common measures of avian reproductive condition?

METHOD
Experiment

Subjects
Thirty-six male Japanese quail (Cotumix cotumix japonica), preselected
as active copulators, served as experimental subjects (Ss). Half were obtained
from Strain 908 of the colony maintained by the Department of Poultry
Husbandry, University of California, Davis. These males were 40-55 days old
when obtained from Davis and transferred to a laboratory at the Field Station

PHOTOPERIOD

AND

REPRODUCTION

for Research on Animal Behavior at Berkeley. Prior to the start of this experiment they had been maintained in the Berkeley laboratory for 10 months where
they had experienced light schedules varying from 7 hr light, 17 hr dark (7L:17D)
to 16L:8D. They were about 12 months old when the experiment started, and
they shall be referred to as the Davis males.
The other half of the Ss were bred from the Davis males and from females of the same strain previously obtained from the Davis colony, and they
were incubated, brooded, and raised at the Field Station. They had experienced only long photoperiods, primarily a 16L:8D cycle. These males were
about 6 months old at the start of the study, and they shaI1 be referred to as
Berkeley males.
Most of the stimulus females used came from the same group of eggs
that yielded the Berkeley males.
Maintenance

The birds were housed individually in galvanized iron cages, 25.5 X 16.5
X 18 cm, with mesh floors and fronts. The Ss could not see or touch each
other. No attempt was made to control auditory or other sources of stimulation. Tap water and Purina Game Bird Layena were always available in dispensers at the front of each cage.
The males were housed and tested in two light-tight rooms separated by
a wooden partition. Illumination
was supplied by two 200-W bulbs in each
room. Since there were no sources of heat other than the birds and the bulbs,
room temperature was close to outside temperature, varying between 5 and
18 during the course of testing.
Testing Apparatus

The cage in which the sexual behavior tests were conducted has been
previously described by Beach and Inman (1965). It consisted of wire mesh,
.63 cm on the floor and 1.27 cm on the sides and top, on a 1.3 X 1.3 X
0.6-meter frame. The cage was painted flat black, and illumination was supplied by a fluorescent light across the roof of the cage.
In two diagonally opposite corners of the cage were clear plastic bottomless holding boxes, mounted on vertical rods and suspended from pulleys.
Counterweights permitted the raising and lowering of these holding boxes
from outside the cage.
Testing Procedure

One of the stimulus females, preselected for receptivity to copulation,

was put in a holding box.

10

SACHS

Measuring the cloaca1protrusion. Before the male was placed in his

holding box his cloacal protrusion was measured(1) from the middle of the
posterior lip of the cloaca to the posterior edge of the protrusion, and (2)
acrossthe protrusion at its widest point. These measuresgave cloaca1protrusion length and width, respectively, and their product yielded Cloaca1Protrusion Area (CPA). At the start of the experiment the feathers in the cloacal
region were plucked to facilitate measurement,and the region was kept clear
of feathers for the remainder of the experiment by occasionalplucking.
Description of sexual behavior. Either the male or the female may make
the initial approach. The malesapproach is often accompaniedby a struthe walks stiff-legged and up on his toes, neck well extended horizontally, head
slightly cocked, and feathers erected. Approach may be followed by crouching
by the female. The male next grabs the females feathers or skin in his beak.
Generally he grabs at the back of the head or neck, but he often seizesthe
wing or tail feathers. The male accompaniesor follows his grabbing motions
by mounting the female. When standing on the females back the male maintains his beak hold and rapidly treads her back with a pumping motion of
his legs. The actions of the male are accompanied or followed by the
femalesincreasedcrouch and a lifting and diverting of her tail feathers. The
male depresseshis tail, and if his actions and position are coordinated with
the females, their cloacas are approximated and contact can occur. Following
cloacal contact, the male releaseshis hold on the female and dismounts. Dismounting is often followed by feather erection and shaking(fluffing, Farris,
1964) on the part of the male and, lessfrequently, the female. The male may
also strut after dismounting.
Measures of sexual behavior. Approach Latency (AL): The male was
placed in his holding box and releasedIO-30 set later, at a time when he was
oriented toward the females corner. The female was releasedafter the male
(1) approached, (2) pecked at the femalesholding box, and (3) stayed within
15 cm of the holding box for 5 sec. The time from the malesreleaseto the
time of his first peck at the femalesholding box is the AL.
If the male failed to approach and peck within 60 set after his release,
then the female was releasedand, to facilitate statistical treatment, the males
AL was defined as 60 sec.
Grab Latency (GL) and Mount Latency (ML): The time from the femalesreleaseto the males initial grab of her feathers or skin is the GL, and
the time from the females releaseto the males first mount is the ML. GL
and ML were scored regardlessof which end of the female the male grabbed
or mounted.
The test continued for 120 set after the malesfirst grab, or for 120 set
after the females release if the mate failed to grab. If the male neither
grabbednor mounted, then his GL and ML were defined as 120 sec.

PHOTOPERIOD

AND REPRODUCTION

11

Cloaca1Contact (CC): A count was taken of the number of times during the test that the male appearedto achieve CC with the female. To score a
CC, the male had to mount, show tail depression,approximate his cloacal region with the females,and show feather fluffing after dismounting.
Foam. After the behavior test the males cloacal protrusion was
squeezedand the amount of foam expressedwas rated on a three-point scale.
A rating of 0 indicated no foam. A rating of 1 meant that a small amount of
rather watery foam was seen.A rating of 2 wasused for all larger amounts of
foam. This test for foam was carried out after the behavior test in order to
avoid possibleeffects that squeezingout the foam might have on behavior.
Experimental Treatment Conditions
Phase 1. This phase served as the standardization period. All the males
were maintained on the 16L:8D schedulewhich they had been on for at least
1 month prior to the start of the experiment (lights on from 0500 to 2100,
Pacific Standard Time). Half the maleswere tested for sexual performance on
alternate days, and after all the maleshad been tested five times they were
assignedto experimental groups. The groups were matched for cloaca1protrusion area, and an equal number of Davis and Berkeley maleswas assignedto
each group.
Phase2. Two days after the end of Phase1, the experimental treatments
of Phase2 began.
Group SL il was transferred to a short light schedule,8L: 16D (lights on
from 0900 to 1700). At the sametime they were implanted subcutaneouslyin
the mid-back with pellets of crystalline testosterone propionatez (TP) compressedinto cylinders approximately 2 mm wide and 1 mm high, and weighing 100 mg f 9 mg.
Group SLNH was also transferred to short light, but no hormone was
implanted. A sham implantation, including everything but the insertion of the
pellet, was carried out.
Group LLNH was maintained under long light (16L:8D) with no hormone implant, but the shamimplantation was carried out.
During Phase2 all maleswere tested 13 times, once every other day.
Phase3. At the end of Phase2 the treatment conditions were changed
as follows:
Group SLNH-four maleswere maintained on short light and TP was implanted (Group SLTP-3); four males were switched to long light and sham
2Testosterone
propionategenerouslysuppliedby Dr. Preston L. Perlman of the
BiologicalResearch
Department,ScheringCorporation,Bloomfield, N. J.

SACHS

12

implanted (Group LLNHa-3); four males were maintained on short light

and sham implanted (Group SLNH3).
Group LLNH-four

males were castrated bilaterally and maintained in long

light (Group LLTX3); five males were sham castrated and switched to
short light (Group SLSX3); three males were sham castrated and maintamed in long light (Group LLSX3).

Group &!,V-four

males were switched to long light and the TP was removed

(Group LLTPX3); four males were maintained on short light and the
TP was removed (Group SLTPX3);
four males in which no pellet remained were switched to long light (Group LLNHb-3).

Pellet implantation was carried out as reported for Phase 2. To remove

the previously implanted pellets, the dorsal feathers were plucked, an incision
was made, the pellet was removed, and the incision was sewn shut. When no
pellet could be found, sham removal was performed.
Castration and sham castration were performed in two stages, unilateral
operations occurring 4 days apart. The technique is described in Sachs (1966).
(For an improved castration technique, see Selinger and Bermant, 1967.) The
males in the castrate group (LLTX3) were subjected to post-mortem laparotomy at the end of Phase 3 to check for the completeness of castration.
Eight days elapsed between the last test of Phase 2 and the first test of
Phase 3. The initial behavior test of Phase 3 occurred 2 days after the completion of castration, implantation, pellet removal, or change in the light
schedule. With few exceptions testing continued on alternate days until the
members of each group had again reached an asymptote of sexual performance.
Despite all precautions there was an accidental interference with the
planned light schedule. From Day 4 to Day 6 of Phase 3 the schedule was

incorrect for the males that should have been on short light. On Day 4 the
lights went off at 2100 instead of at 1700. On Day 5 the lights were on from
0500 to 2100, and on Day 6 the lights were on from 0500 to 1700. Then
starting again on Day 7 the lights were on from 0900 to 1700. Thus shortly
after the start of Phase 3, the males in the short light groups that should have
had 8 hr light were exposed to 2 days with 12 m light and 1 day with ] 6
hours light.
Table 1 summarizes the treatment conditions and chronology for all the
subjects.
The data from Phases 1 and 2 were treated by an analysis of variance
(Edwards, 1960, p. 233) in which Experimental Group, Test Days, and Population (Davis or Berkeley males) were the factors. In some cases analysis of
variance was followed by multiple t tests.

PHOTOPERIOD

13

AND REPRODUCTION
TABLE I

Treatment Conditions and Chronology throughout the Experiment

The group, for example, that received long light and castration in Phase 3 (LLTX-3) had
received long light and no hormone in Phases 1 and 2. For additional details, see text.
Phase 3

Phase 2

Phase 1
(Days 1 - 10)

Day 12

(Days 15 - 42)

Day 48

(Day 50 - end)

LLTX-3
SLSX-3
LLSX-3

LLNHo
LLNH
LLNH

LLNH

LLNH

LLNH
LLNH
LLNH

SLNH
SLNH
SLNH

SLNH-3

LLNH
LLNH
LLNH

SLTP
SLTP
SLTP

LLTPX-3
SLTPX-3
LLNHb-3

LLNH

LLNHa-3
SLTP-3

LL = long light; SL = short light; NH = no hormone; TP = testosterone propionate pellet; TPX = TP removed; TX = testes removed; SX = sham testis removal.

RESULTS
Phase1

The data in Table 2 show the parameters of the variables when the
males were in peak reproductive condition. The very short latency measures
indicate the speed with which copulation ensued after the male was released.
Since the male had generally mounted within 6 set after his release (ALtCLt
ML4.8 set) there was little time for elaborate courtship ritual. As expected,
TABLE

Means and Standard Deviations for All Variables on Last Day of Phase 10
Variables

Mean

SD

Approach latency (set)

Grab latency (secl
Mount latency (set)
Cloaca1 contacts
Cloacal protrusion width (mm)
Cloacal protrusion length (mm)
Cloacal protrusion area (mm21
Foam rating

2.1
1.1
2.6
2.3
20.0
11.0
220.4
2.0

2.5
0.5
2.1
1.1
1.2
1.1
31.9
0.0

For meaning of variables, see Method section.

14

SACHS

the mean foam rating was 2, with no variance, since the males were preselected for the presence of foam, and the conditions of Phase 1 were such as to
maintain foam.
Beach and Inman (1965) have previously demonstrated the reliability of
the latency measures, but the reliability of measurement of the cloaca1 protrusion was determined for this study by having two observers, experienced in
handling quail, independently measure the cloaca1 protrusions of 20 males in
various stages of reproductive condition. The interobserver rank-order correlations were t.89 for length, t.91 for width, and t.93 for area, with p < .05 for
all correlations.
Analyses of variance of the data from Phase 1 indicated no significant
differences among experimental groups, showing that they were well matched.
The absence of significant differences among test days indicated that the variables were reasonably stable during Phase 1.
However, there were sign&ant
differences between the two populations. The Davis males had longer cloacal protrusions (Fz6.17; df-1,30;
p < .02) and more cloaca1 contacts (F = 6.30; p < .02). They also had shorter
Grab Latencies at the beginning of Phase 1, but this difference disappeared by
the end of the Phase as the Berkeley males became faster.
Phase 2
To obtain a measure of the relation among the variables, productmoment correlation coefficients were obtained for the data from Group SLNH
on Day 10 of Phase 2, a period of high intragroup variability. The correlations
among the latencies and among the protrusion measures were high and positive (t.74 to t.99) and the correlations between the latencies and protrusion
size were high and negative (-.79 to -.90). However, correlation analyses applied to the data of Phase 1, when there was less variability among the birds,
showed that one cannot predict from among a group of males with developed
cloacal protrusions which of them will have the shortest latencies or the most
cloacal contacts.
To reduce the amount of data to be compared, one behavioral measure,
Approach Latnecy (AL), and one morphological measure, Cloacal Protrusion
Area (CPA), have been selected to represent the data in many of the analyses
that follow. AL is a highly reliable measure, well correlated (t.74 to +.87)
with other measures and with the actual occurrence of copulation. It is the
behavioral variable that is most independent of the behavior of the female.
CPA is the most reliable morphological measure and is also highly correlated
with the behavioral variables (t.85 to t.97).
The mean values for the representative variables for the three groups
during Phase 2 are presented in Table 3. (The other variables reflected the

PHOTOPERIOD

15

AND RBPRODUCTION
TABLE 3

Means (and Standard Deviations) of Approach Latency and Cloacal

Protrusion Area for Each Group at Beginning (Day l),
Middle (Day 15), and End (Day 29) of Phase 2a
Phase 2
Group
Approach latency (set)
LLNH
SLTP
SLNH
Cloacal protrusion area (mm2)
LLNH
SLTP
SLNH

Day 1

Day 15

Day 29

1.6 (0.7)
2.4 (1.6)
1.6 (0.8)

1.5 (0.5)
1.9 (1.3)
36.9 (28.7)

1.7 (0.8)
7.3 (16.8)
55.3 (16.3)

220.9 (33.7)
220.8 (35.4)
214.9 (19.6)

222.8 (32.4)
222.3 (43.7)
130.0 (36.8)

227.2 (40.6)
226.5 (46.2)
93.1 (20.5)

aAl differences between Group SLNH and the other two groups on Days 15 and 29 are
significant @ < .05). No other differences among groups or days are significant. For meanings of variables and group abbreviations, see Method section.

sametrend.) Group LLNH was maintained by long light at the level of reproductive condition displayed in Phase 1. Group SLNH dropped out of reproductive condition rapidly, and by Day 29 had reached a low asymptote of
sexual performance and cloacal protrusion size. Group SLTP followed the
samecourse as Group LLNH, showing no decline in reproductive condition
during Phase2. (The relatively high approach latency for Group SLTP on Day
29 resulted from the deviant scoresof only one male in this group.) Statistical
tests confirmed that there were no significant differences between Groups
LLNH and SLTP for any variable on any day. In contrast, the differences between Group SLNH and the other two groups were highly significant
(p < .OOl), starting on Day 3 for CPA and on Day 5 for AL, and increasing
thereafter. Clearly, transfer to short light acted to depressthe reproductive
condition of Group SLNH, and the testosterone pellets in Group SLTP served
to counteract the effects of transfer to short light.
There were no significant differences between Berkeley and Davis males
in Groups LLNH and SLTP. However, in Group SLNH there were significant
differences 03 < .Ol) between the two populations. As shown in Figs. 1 and 2,
the Berkeley males started down from high asymptote sooner than the Davis
malesand reached low asymptote sooner. (The slightly higher low asymptote
of the Davis males is attributable to one male that was still copulating at the
end of Phase2 and showed little reduction in CPA. The reason for his idiosyncratic performance is not known.) Further analysis of the behavioral data
in terms of percentage Ss copulating and latencies of copulating Ss reflected
the same trends as those shown in Fig. 1, and confirmed that the two

16

SACHS

Days

after

tranrfor

to 81:

160

80 c
II

10

12

I5

17

19

Days

after

transfer

to

22 24 26

29

81:16D

Figs. I and 2. Changes in approach latency (AL) and cloacal protrusion area
(CPA) during Phase 2 for Davis (0) and Berkeley (0) males in Group SLNH. N=6 in
both groups. These males were maintained in 16L:8D prior to Phase 2 and in 8L:16D
during Phase 2. In Fig. 1, AL scale has been condensed at AL > 10 sec. and inverted. At
each point is the number of males still copulating (AL < 60 set).

PHOTOPERIOD

populations responded
short days.

AND REPRODUCTION

at very different

17

rates to the transfer from long days to

Phase 3
Ma&s from Gmup SLNH in Phase 2. Four of the males that had been in
SLNH in Phase 2 were switched to a long photoperiod
in Phase 3
(Group
LLNHa-3), and another four males had TP pellets implanted in them
(Group
SLTP-3). In order to have a control for the possibility of spontaneous
return to reproductive
condition
by these two groups, another four males
were to have been maintained on the short-light schedule (Group SLNH3). It
was noted before that there was an accidental modification in that schedule.
The effects of the treatments on these groups is shown iti Figs. 3 and 4.
Groups LLNHa-3 and SLTP3: Ten days after their transfer to long
photoperiod, three of the four males in Group LLNHa-3 were copulating, and
7 days after that at1 four males had ALs at their Phase 1 levels. It was about
15 days before the CPAs of the males in this group reached their Phase 1
levels. Both Davis males in Group LLNHa-3 responded to the change in treatment sooner than the Berkeley males did, reaching asymptote 5 days earlier.
In contrast to Group LLNHa-3, Group SLTP-3 returned to reproductive
condition almost immediately. Within 3 days after the hormone was implanted
three of the four males were copulating, and the fourth copulated 2 days
later, As early as 2 days after the pellet was implanted, the CPA of all the
males in this group had nearly doubled. Eight to ten days after TP implantation, the CfAs of these males were back to their Phase 1 levels.
Group SLNH-3: During the first 3 days of Phase 3 these males were
maintained on the short photoperiod, and in contrast to the increase in reproductive condition in the other two groups, these males maintained their low
asymptotes. However, during the period from Day 4 to Day 6 of Phase 3
these males were accidentally
exposed to long photoperiods
(12-l 6 hr of
light). On Day 8 there was an increase in CPA for three of the four males,
and 2 days later the Davis males in the group were copulating. The CPAs of
the Davis males reached their Phase 1 levels by Day 15 of Phase 3. Somewhat
later, on Day 19, one of the Berkeley males started to copulate, while the
other stayed at low asymptote. At the end of Phase 3, 21 days after the last
of the long photoperiod days, these three males were still in reproductive condition. Though it cannot be established with certainty that these males did
not return to breeding condition spontaneously,
evidence from other groups,
to be presented below, lends support to the hypothesis that the 3 long-light
days were responsible. (In some colony cages in the same room as this group,
most of the males and a quarter of the females returned to reproductive condition at about the same time, as indicated by the crowing of the males and
the foam on their droppings,
and by the resumption of egg laying by the
females.)
Group

18

SACHS
0
2*

,..o...o ..._ .. ..._.o...

p....

X6
2

5
s

0
30

i,

,:.
50

:
:

10

S//J
c
ff

23

10

12

a. P.

15

Day

of

17

Phase

19

22

24

27

2%

0
-E
.E
L
U
c

2oc

1x

1oc

n
0

-(Y
f
f
?

23

10

12

Day

of

15

Phase

17

19

22

24

27

Figs. 3 and 4. Approach latency (AL) and cloacal protrusion area (CPA) at end of
Phase 1, end of Phase 2, and during Phase 3 for Groups LLNHa-3 (o), SLTP-3 (W) and
SLNH-3 (o), which had been in 16L:8D in Phase 1 and in 8L:l6D in Phase 2. Treatments during Phase 3 were as follows. Group LLNHa-3: returned to 16L:8D with no
hormone; Group SLTP-3: maintained in 8L:16D and implanted with testosterone propionate pellet; Group SLNH-3: maintained in 8L:16D with no hormone. From Day 4 to
Day 7 of Phase 3, Groups SLTP-3 and SLNH-3 were accidentally exposed to 12-16 hr of
light. N=4 in all groups. AL scale has been condensed at AL > 10 set, and inverted.

PHOTOPERIOD

AND

REPRODUCTION

19

Effect of exogenous testosterone on the testes of cotmix. The m&s in

Group SLTP3 were laparotomized after Phase 3, having had TP Mets in
them for 29 days. The mean weight of both testes was 24 mg. The comparable average for males at the peak of reproductive condition is 2700 mg. All of
the testes in the SLTP-3 males were smaller than any found in males that had
been on short-light cycles for 28 days (Sachs, 1967). Since the cloacaf protrusion of these males was at maximum size at autopsy, it is apparent that TP
stimulated the cloaca1 gland and inhibited the testes of the quail.
Males from Group LLNH in Phase 2. In order to compare the rate of
decline in breeding condition following transfer to short photoperiod with the
decline after surgical castration, some males from Group LLNH were castrated
and maintained in long light (Group LLTX3), some were sham castrated and
maintained in long light (Group LLSX3), and some were sham castrated and
shifted to short light (Group SLSX-3).
Groups LLSX-3 and SLSX3: Except for a small drop in CPA 2 days
after sham castration, Group LLSX3 showed no effects of the operation.
They maintained their high asymptote. The decline in breeding condition of
Group SLSX3 may, therefore, be attributed to the transfer to short photoperiod rather than to the sham castration. Indeed, the operation did not even
accelerate the regression of Group SLSX-3. The four males in this group (one
male had died during the operation) evidenced no reduction in reproductive
condition until about Day 15 or 17, and one of them, a Davis male, delayed
until Day 21 or 23. In contrast, the reproductive condition of Group SLNH in
Phase 2 had declined a week or more sooner after transfer to short photoperiod. The delay in Group SLSX-3 may be attributable to the 3 days of long
photoperiod to which this group was exposed from Day 4 to Day 6.
Group LLTX3:
Four males were operated upon to remove both testes.
Of these birds one died in surgery and one, on autopsy, revealed functioning
testicular tissue. Since only two of the males were completely castrated, the
data are of doubtful reliability and will not be presented here.
Males from Group SLTP in Phase 2. The TP pellets were removed from
eight of the males in which they had been implanted during Phase 2. Of these
males, four were continued under short photoperiod (Group SLTPX3) and
four were transferred to a long photoperiod (Group LLTPX-3).
Another
four
males whose pellets had been resorbed were also transferred to a long-fight
cycle (Group LLNHb-3).
Group SLTPX3: AS expected the SLTPX3 males declined rapidly in reproductive condition in the days following pellet removal-much more rapidly
than had Group SLNH in Phase 2. By Day 8 of Phase 3, these males had
stopped copulating and had CPAs less than half their Phase 2 size. However,
on Day 10 the only Davis male in this group began copulating again and

20

SACHS

showed an increase in CPA. After Day 19 his AL and CPA returned to low
asymptote. It is suggested that this males temporary return to reproductive
condition is again attributable to the 3 days of long light which this group
experienced starting Day 4, and it should be noted that it was again a Davis
male which showed this responsiveness.
Group LLTPX-3: Initially the reproductive condition of the males in
this group declined after the removal of the TP pellet, and this decline seemed
to occur at about the same rate as that of the males in Group SLTPX-3. But
the median ALs and CPAs indicate a reversal of the decline after 5 days, presumably resulting from an increase in endogenous androgen following stimulation by long photoperiods. Within 22 days after Phase 3 began, all these males
had reached their Phase 1 levels of AL and CPA. Hence, the suppression of
the testes induced by TP was readily reversible by exposing the male to long
photoperiods.
Group LLNHb-3: It was noted before that by the end of Phase 2 one
male in Group SLTP showed signs of reduction of reproductive condition. A
week elapsed between the last test of Phase 2 and the time that a search was
made for the pellet in the SLTP males. During this interval three additional
birds in this group showed considerable reduction in cloacal protrusion size,
and their foam rating had fallen from 2 to 0. No trace of the pellet could be
found in these four males; apparently the pellet had been totally absorbed.
These males in Group LLNHb-3 were also transferred from short light to
long light. It took 9-21 days for three of these males to return to peak reproductive condition. The other male in the group gave no evidence of shorter
AL or larger CPA even after 27 days exposure to long photoperiod. There was
no apparent relation between the time the males stopped showing a response
to the pellet and the males rate of return to reproductive condition.
DISCUSSION
The reproductive condition of male cotumix was depressed by shifting
them from long to short photoperiods. Exposure of the males to long photoperiods maintained their breeding condition, or returned the males to breeding
condition if it had been depressed by short photoperiods. These results sup
port other fmdings on the effect of photoperiod on the testis weight (Follett
and Famer, 1966) and the cloacal gland (Sachs, 1965, 1967) of cotumix, and
they indicate that the reproductive condition of adult male coturnix depends
on the duration of the daily period of light.
Although the duration of light each day is clearly important in regulating the reproductive condition of male cotumix, other factors are also in
volved, as there is no simple correspondence between number of hours of
daily light and any measure of reproductive condition. For example, the temporal spacing of the light must be considered. Eight hours of continuous light

PHOTOPERIOD

AND REPRODUCTION

21

each day result in a regressed reproductive condition, but the same amount of
light on an intermittent schedule (lL:2D) is h.ighIy StimUlatOryfor c0turni.x
(Wilson, Abplanalp, and Arrmgton, 1962).
In addition to the light schedule each day, the duration of the daily
regimen must be considered. During Phase 3 of the experiment, three days of
long light stimulated the reproductive condition of many birds for several days
after the change back to short light. A similar effect following a few days of
long light has also been observed in coturnix by Konishi, Ishiguro, and Kate
(1965). This means that light cycles of only a few days duration can exert an
effect for several days afterward, perhaps by triggering a physiological
process or by entraining a circadian rhythm (Hamner, 1965; Wolfson, 1966).
Another variable involved in the effect of light on the animal is the
birds age. The Berkeley males lost their reproductive condition more rapidly
than the Davis males after being switched from long to short photoperiod, and
they regained their breeding condition more slowly upon being shifted from
short to long photoperiods. The Davis males were about 12 months old and
the Berkeley males were about 6 months old. There have been reports
(Selander, 1965; Selander and Hauser, 1965; Farner and Wilson, 1957) of
other species showing similar differences in the rate at which the reproductive
systems of first-year and older males respond to natural or artificial changes in
daylength. In the present study, the older males had experienced both short
and long light cycles, but the younger males had been brooded and raised
only under long light cycles. It may be that experience with various photoperiods, and not just maturation per se, contributed to the difference in
photosensitivity between the older and younger males. That is, the birds exposure to different right cycles during development may act on his neuroendocrine system in such a way as to make his reproductive condition either
less sensitive to environmental light conditions that inhibit breeding or more
sensitive to conditions that facilitate breeding.
Following their annual breeding period many species of birds enter an
extended period of photorefractoriness, when conditions of illumination that
formerly stimulated gonadal activity are no longer effective. The onset of this
refractory period is marked by a spontaneous regression of the gonads
(Wolfson, 1960)-spontaneous because the onset is thought to be controlled
by internal mechanisms rather than by changing environmental conditions.
Kirkpatrick (1959) has shown that female bobwhite do not require an
interval of short-light days after laying a clutch of eggs before they can again
be induced to lay by long-light days. These data are commonly interpreted as
indicating that there is no refractory period in bobwhite, a member with
coturmx of the Phasianidae family. On the basis of similar evidence it would
appear that cotunk
do not have an annual refractory period either. Woodard,
Abplanalp, and Wilson (1965) have reported that coturnix hens lay almost an

22

SACHS

egg a day throughout the year under appropriate lighting conditions. In an

earlier study (Sachs, 1965) and in the present one, no intact male was ever
insensitive to long photoperiods.3 Whenever the photoperiod was adjusted at
16L:8D the males system responded positively, regardlessof whether the
male was already in peak reproductive condition, was in declining reproductive
condition, or was in a nonreproductive state. In addition, no males ever
showed evidence of a spontaneousgonadal regression,though some of them
had been maintained in 16L:8D for more than 5 months. These facts, taken
together with the evidence of Farner and Follett (1966) that juvenile quail are
not photorefractory, suggestthat coturnix of both sexes are nonphotorefractory asjuveniles and asadults.
Treatment of intact coturnix males with testosterone propionate (TP)
simulatedmany of the effects of long photoperiods: Sexual behavior was stimulated, as were the cloaca1gland and cloaca1foam, and molting was inhibited.
However, unlike the action of long photoperiods, TP causedregressionof the
testes. Since testicular regressionis usually symptomatic of low gonadotropin
levels, we may conclude that TP inhibited gonadotropin secretion, and that
gonadotropins are not essentialto those elementsof reproductive behavior and
physiology that are maintained by exogenousandrogen.
Suppressionof testis activity, whether by reduction in photoperiod or
treatment with TP, was readily reversible by withdrawing TP and shifting the
males to long light. Following photoperiodically-induced gonadal regression,
the administration of exogenousandrogen(Group SLTP3) returned the males
to breeding condition sooner than did placing the birds in a long photoperiod
(Group LLNHa-3). Although some of this difference in rate may be attributable to differences in the source and amount of testosterone, the relative lag
of Group LLNHa-3 may also have stemmedfrom a delay between exposure to
light and releaseof gonadotropins, and from a delay between gonadotropin
reIeaseand effective androgen secretion. Presumably, with Group SLTP-3 the
TP could act directly on the target organs.
We may assumethat light exerts its effect on the reproductive condition
of male coturnix by controlling gonadotropin secretion, which in turn controls
gonadal growth and androgen secretion. Androgen then stimulatesthe growth
and secretion of the cloaca1gland, acts on the neural tissuesto stimulate mating behavior, and feeds back onto the hypothalamo-hypophysial system to
regulate gonadotropin secretion.
ACKNOWLEDGMENTS
This paper is based on part of a doctoral dissertation submitted in August, 1966 to
the University of California, Berkeley. The work was supported by NIMH fellowship
3The sole exception was a male in Group LLNHb-3
16L:8D after having been treated with TP in Phase 2.

that failed to respond to

PHOTOPERIOD

AND REPRODUCTION

23

21,586 to the author and by NIMH grant MH-04000 to Frank A. Beach. Part of the
work was done at the Berkeley Field Station for Research on Animal Behavior. The
manuscript was prepared at the Institute of Animal Behavior, Rutgers-The State University, Newark, NJ. during the authors tenure as a NICHHD postdoctoral fellow. I thank
R.J. Barfield for valuable criticisms of the manuscript.
REFERENCES
Beach, F. A., and Inman, N.G. (1965). Effects of castration and androgen replacement on
mating in male quail. Proc. Natl. Acad. Sci. 54, 1426-1431.
Edwards, A. L. Experimental
design in psychological
research.
New York: Holt, Rinehart
and Winston, 1960.
Farner, D. S. (1959). Photoperiodic control of annual gonadal cycles in birds. In R. B.
Withsow
(Ed.), Photopenodism
and related
phenomena
in plants
and animals.
AAAS, Washington, D.C. Pp. 717-750.
Famer, D. S. and FoIlett, B. K. (1966). Light and other environmental factors affecting
avian reproduction. J. Animai Sci. 25 (suppl.), 90-115.
Famer, D. S. and Wilson, A. C. (1957). A quantitative examination of testicular growth
in the white-crowned sparrow. Bioi. Btdl.. 113, 254-267.
Farris, H. E. (1964). Behavioral development, social organization, and conditioning of
courting behavior in the Japanese quail, Cotumix
cotumix
japonica.
Unpublished
doctoral dissertation, Michigan State University.
FolIett, B. K. and Farmer, D. S. (1966). The effects of daily photoperiod on gonadal
growth, neurohypophysial hormone content, and neurosecretion in the hypothalamo-hypophysial system of the Japanese quail (Cotumix
coturnix
japonica).
Gen. Comp. Endocrinol.
7, 111-124.
Hamner, W. M. (1965). Photoperiodic refractoriness: reevaluation and interpretation.
Am. Zool. 5, 681-682.
Kirkpatrick, C. M. (1959). Interrupted dark period: tests for refractoriness in bobwhite
quail hens. In R. B. Withrow (Ed.), Photoperiodism
and related phenomena
in
plants and animals.
AAAS, Washington, D.C. Pp. 751-758.
Konishi, T., Ishiguro, T., and Kato, M. (1965). Zool. IbfQg. 74, 54. In Japanese. Cited in
Konishi, T. and Kato, M. (1967).
Konishi, T. and Kato, M. (1967). Light-induced rhythmic changes in the hypothalamic
neurosecretory activity in Japanese quail, Coturnix
coturnix
japonica.
Endocrinologia

Japonica

14, 239-245.

Sachs, B. D. (1965). Social influences on the reproductive condition of male Japanese

quail Paper read at meeting of Western Psychological Association, Honolulu,
Hawaii.
Sachs, B. D. (1966). Photoperiodic control of sexual behavior and physiology of male
quail (C~t~mix
coturnix
japonica).
Unpublished doctoral dissertation, University of
California, Berkeley.
Sachs, B. D. (1967). Photoperiodic control of the cloacaI gland of the Japanese quail.
Science 157, 201-203.
Selander, R. K. (1965). On mating systems and natural selection. Am. Natural.
99, 129141.
Selander, R. K., and Hauser, R. J. (1965). Gonadal and behavioral cycles in the greattailed grackle. Condor 67, 157-182.
Selinger, H. E., and Bermant, G. (1967). Hormonal control of aggressive behavior in
Japanese quail (Coturnix
cotumix
japonica).
Behaviour
28, 255-268.

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SACHS

Tanaka, K., Mather, F. B., Wilson, W. O., and McFarland, L. Z. (1965). Effect of photoperiods on early growth of gonads and on potency of gonadotropins of the anteriOI pituitary in Coturnix. Poult. Sci. 44, 662-665.
Tanaka, K., Wilson, W. O., Mather, F. B., and McFarland, L. Z. (1966). Diurnal variation
in gonadotropic potency of the adenohypophysis of Japanese quail (Coturnix
cotumix japonica). Gen. Comp. Endocrinol. 6, l-4.
Wilson, W. O., Abplanalp, H., and Arrington, L. (1962). Sexual development of Cotumix
as affected by changes in photoperiod. Poult. Sci. 41, 17-22.
Wolfson, A. (1960). Regulation of annual periodicity in the migration and reproduction of
birds. Cold Spring Harbor Symp. Qua&. Biol. 25, 507-514.
Wolfson, A. (1966). Environmental and neuroendocrine regulation of annual gonadal
cycles and migratory behavior in birds. Recent Bog. Hormone Res. 22, 177-244.
Woodard, A. E., Abplanalp, H., and Wilson, W. 0. (1965). Japanese quail husbandry in
the laboratory. Bound manuscript, Department of Poultry Husbandry, University
of California, Davis.