TE gonadal responses of several species of birds exposed to stimula-
tory daily photoperiods of constant duration conform in that an initial
rectilinear relationship exists between the logarithm of testicular weight
and time on long days. They conform further in that the rate of photo-
induced testicular growth, as determined from the rectilinear relation-
ship, is a function of daylength. These and other observations support
the thesis that increased daylength plays an indispensable role in initiating
vernal testicular growth and determining its rate in many species. The
current consensus is, however, that long days are gonadostimulatory not
because they exceed a critical length, but because they illunfinate a
photoinducible phase of a circadian oscillation in photosensitivity. (For
reviews see Farner, 1959, 1961, 1964a, 1964b, 1970; Hamner, 1966;
Lofts et al., 1970.)
Quantification of photoperiodic gonadal responses has been limited
essentially to males. To our knowledge, only four definitive studies--
one on White-crowned Sparrows (Farner et al., 1966) and three on Japa-
nese Quail (Follett and Farner, 1966; Sayler and Wolfson, 1967; Follett
and Sharp, 1969)--describe the temporal course and/or rate of ovarian
growth induced by constant daylengths, and only one suggests that rate
of ovarian growth varies with daylength (Follett and Sharp, 1969).
Moreover, although a circadian oscillation in photosensitivity apparently
is involved in the control of ovarian growth in Japanese Quail (Follett
and Sharp, 1969), there is no evidence for or against involvement of a
similar oscillation in the control of photoperiodic ovarian growth in
species that breed seasonally. In this report, we describe the temporal
course and rate of ovarian growth in Tree Sparrows (Spizella arborea)
exposed to daylengths of 8, 11, 15, or 20 hours and examine rate of
photoinduced ovarian growth as a function of daylength. In addition,
we report results of a preliminary experiment that suggest a circadian
oscillation operates in the photoperiodic ovarian response of the Tree
Sparrow. The pineal body is exanfined as the possible seat of the
circadian oscillator.
M^TRrLS ^NI MTROIS
In the first of three experiments, 53 female Tree Sparrows captured between
Contribution No. 1113, Division of Biology, Agricultural Experiment Station,
Kansas State University, Manhattan 66502.
146 The Auk, 89: 146-155. January 1972
: 2.0-
o,
2.0-
Z tõ-
o 1.0-
o,
2.0-
0.5'
0-20L 4D
o-SL 16D
Begin ø
20L 4D
ß -15L 9D
o-SL 16D
DAYS
Begin
15L 9D
DAYS
ß -11L 13D
o- 8L 16D
Begin
11L 13D
Figure 1.
DAYS
Relationships between ovarian weight and time in Tree Sparrows after
daily photoperiods were changed from 8 to 20 (upper), 8 to 15 (middle), and 8 to
11 (lower) hours. Regression lines were obtained by the method of least squares.
14 January and 10 February 1967 were held on 8-hour daily pho.toperiods (08:30-
16:30 CST) until 21 June 1967 when they were divided into groups designated
PSL-20 and PSL-15 and caged in adjacent rooms on 20~ (08:30-04:30 CST) and
15-hour (08:30-23:30 CST) daily photoperiods, respectively. Six birds sacrificed
on 21 June permitted us to estimate ovaria.n weight at the beginning of the
long-day treatmen, ts, and eight birds (group PSS-42) continued on 8-hour daily
photoperiods (8L) for 42 days served as terminal short-day controls. Thirty-three
other females (group PSL-11) captured between 19 December 1969 and 21 February
1970 were transferred from 8- (08:30-16:30 CST) to 11-hour (08:30-19:30 CST)
daily photoperiods on 30 April 1970. Eight birds killed on that day served as
initial controls, and five birds (group PSS-56) killed after 56 additional days on
8L, as terminal controls. Birds of groups PSL-20, -15, and -11 were sacrificed at
selected intervals during 5, 6, and 8 weeks of photostimulation, respectively. Minimum
intensity was 400 lux.
In the second experiment, Tree Sparrows captured between 17 February and
11 March 1967 were held on 20-hour daily photoperiods (08:30-04:30 CST) until
5 July 1967 when the photoperiod was reduced 1 hour per day to 8 hours (08:30-
16:30 CST). Beginning 17 July, 24 females were sacrificed over a 12-month
period during which the photoperiod remained at 8 hours.
In the third experiment, female Tree Sparrows captured between 11 November
1967 and 31 January 1968 were held on 8L (08:30-16:30 CST) until mid-July
1968 when they were subjected to pinealectomy or to sham pinealectomy (for
procedures see Donham, 1968) or sacrificed as initial controls (N : 8). Pinealec-
tomized birds were divided into groups designated PC (N = 9) and PD (N : 12)
and continued on 8L (08:30-16:30 CST and 08:30-14:30, then 01:30-03:30 CST,
respectively). Sham-pinealectomized birds were divided into similar groups desig-
nated SPC (N = 11) and SPD (N : 14). All birds were sacrificed during the
next 100 days.
Tree Sparrows used in these experiments were captured with mist nets from
wintering populations near Manhattan, Kansas, and held, four or five per cage,
in small cages (51 X 27 X 27 cm or 23 X 25 X 41 cm). Illumination was
by overhead fluorescent lamps, sometimes in combination with incandescent lamps;
extraneous light was excluded. Food (a vitamin- and mineral-enriched chick-
starter crumble supplemented with commercially prepared parakeet foods) and
water were freely available. Temperature varied within a few degrees of 21øC.
Sex was determined by laparotomy under Nembutal anesthesia (Donovan, 1958)
prior to each experiment. Immediately after sacrifice by decapitation, ovaries were
removed and placed in an aqueous solution of acetic acid, formalin, and ethanol
(AFA); 5 days thereafter they were transferred to 70 percent ethanol. Ten days
after sacrifice, ovaries were freed of extraneous tissue and weighed to the nearest
0.01 mg on a torsion balance. Logarithmic ovarian growth-rate constants and their
95 percent confidence intervals were estimated using formulae described by Simpson
et al. (1960).
RESULTS AND DISCUSSION
A rectilinear relationship exists between the logarithm of ovarian
weight and time (in days) when photosensitive Tree Sparrows, held on
8L since capture, are exposed to constant daily photoperiods of 20, 15, or
11 hours (20L, 15L, or IlL) for at least 35, 42, or 56 days, respectively
(Figure 1). That relationship, which depicts the approximate temporal
course of photoinduced ovarian growth and defines its rate, may be
expressed algebraically as
log Wt = kt + log Wo (I)
where Wt is ovarian weight in mg after t days on 20L, 15L, or IlL; Wo
is ovarian weight at day 0; and k is the logarithmic ovarian growth-rate
TABLE 1
RATE OF OVARIA GROWTIt: (k) AS A FU'l'CTIO OF D.a. YLEf;TI{
149
Daylength,
Group hours k , days log Wo
PSL-20 20 0.025 _+ 0.004 (34) 0.567 --+ 0.048 (34)
PSL-15 15 0.022 '+- 0.004 (31) 0.597 _+ 0.053 (31)
PSL-11 11 0.005 _--+- 0.002 (41) 0.615 _--+- 0.035 (41)
PSS-42 8 0.002 _--+- 0.005 (14) 0.560 _--+- 0.098 (14)
PSS-56 8 0.001 _+ 0.003 (13) 0.617 _+ 0.076 (13)
Logarithmic ovarian growth-rate constant q- 95 percent confidence interval. For groups PSL-20,
-15, and -11, k is estimated for days 0-35, 042, and 0 56, respectively. For groups PSS-42 and
-56, k is estimated for days 042 and 0-56, respectively. Number of birds in each sample is
indicated in parentheses.
2 Ordinate-intercept (equation 1) q- 95 percent confidence interval. Number of b!rds in each
sample is indicated in parentheses.
constant (= coefficient o.f regression; see Figure 1) in days 4. On
the other hand, when photosensitive Tree Sparrows are continued on 8L
in short-term experiments, ovarian weight is ostensibly independent of
time (Table 1; Figure 1).
Rate of photoinduced ovarian growth (k) in Tree Sparrows is examined
as a function of daylength (p) in Figure 2. Although it is apparent
that k depends on p, at least over part of the range, the real relationship
between k and p remains somewhat uncertain for several reasons: (1)
Relatively small changes in ovarian weight with respect to natural
variability make estimation of k difficult in short-term experiments when
p is short; (2) an approximately fourfold increase in k over the interval
p = 11-15 hours, coupled with a lack of data for intermediate values of p,
makes charting the rate of change in k difficult; and (3) k may be
slightly underestimated when p = 11 hours if, as in some male passerines
(Farnet, 1962), photosensitivity increases with retention on 8L. (Be-
cause of inadequate numbers of Tree Sparrows in one year and scheduling
problems in another, it was necessary to determine k for PSL-11 birds
some 6-7 weeks earlier on a calendar basis than for PSL-15 and -20
birds.) For these reasons, the curve in Figure 2, fitted to the points
by eye, should be regarded as approximate, especially over the intervals
p = 8-11 hours and p = 11-15 hours. In birds of equal photosensitivity,
the rate of ovarian growth induced by 15L is not significantly different
from that induced by 20L.
For males of most photoperiodic species, there is a complete daily
photoperiod below which testicular growth is not induced as well as
one that induces testicular growth maximally. Between those limits,
0.025 -
0.020 -
0.015 -
0.010 -
0.005-
0 22h
' ' ' '
8 10 14 16
HOURS
Figure 2. Rate of ovarian growth (K) as a function of daylength (hours).
Vertical lines represent 95 percent confidence intervals. The estimate at 8 hours
is based on group PSS-56 (Table 1).
rate of testicular growth (k) varies with daylength (p), and k is some-
times directly proportional to p. These principles have emerged from
quantitative examinations of photoperiodic testicular responses of several
avian species (see Lofts et al., 1970); our data on female Tree Sparrows
raise the possibility that similar principles may apply to photoperiodic
ovarian responses and, further, that differences between photoperiodic
testicular and ovarian responses may be primarily quantitative, at least
initially. The latter possibility seemingly has been confirmed, for when
photosensitive male and female Tree Sparrows (Table 1; cf. Wilson and
Hands, 1968), White-crowned Sparrows (Farner et al., 1966), or Japanese
Quail (Follett and Farner, 1966; Follett and Sharp, 1969) are exposed
to 20L at approximately the same time of year, gonadal growth initially
follows a log-linear function of time, but k for testicular growth is two
to four times greater than k for ovarian growth, which for Tree (Table
1) and White-crowned (Farner et al., 1966) Sparrows is 0.025 and 0.027
days , respectively, when p = 20 hours. The rate of ovarian growth in
1.5-
1.0.
0.5-
o-
MONTHS
Figure 3. Relationship between ovarian weight and time in initially photore-
fractory Tree Sparrows held 0-12 months on 8-hour daily photoperiods. The re-
gression line was obtained by the method of least squares.
Japanese Quail exposed to similar photoperiodic conditions (Follett and
Farner, 1966; Follett and Sharp, 1969) is two to three times more rapid.
Logarithmic growth continues in White-crowned Sparrows (Farner et al.,
1966) and Japanese Quail (Follett and Sharp, 1969) until ovarian
weights of about 50 and 100 mg, respectively, are achieved. Although
equation (1) is valid for Tree Sparrows until ovarian weight reaches
approximately 45 mg (Figure 1), its validity beyond 45 mg has not
been established.
As noted, ovarian weight did not increase significantly when photo-
sensitive Tree Sparrows were continued on 8L in short-term (42- or 56-
day) experiments (Table 1; Figure 1). However, when initially photo-
refractory Tree Sparows were transferred from 20L to 8L and sacrificed
over the course of a year, it became apparent that ovarian growth did
occur during retention on 8L (Figure 3). Such growth showed good
conformance with equation (1), but its rate (k = 0.00095 -+ 0.00026
days x) was very slow; an increase from 4 to 45 mg, as might occur
within 5 weeks after transferring photosensitive birds to 20L, would re~
quire approximately 3 years. It should be emphasized that ovarian
growth in birds on 8L was similar, except for rate, to that in birds on
IlL, 15L, or 20L (cf. Figures 1 and 3), even though birds on 8L (unlike
those on IlL, 15L, or 20L) were initially photorefractory (see Materials
and Methods). As photosensitivity doubtlessly gradually increased from
zero (photorefractoriness) during the year (see Farner, 1964a), ovarian
growth occurred apparently independently of physiological state. Non-
photoperiodic ovarian growth--i.e. that which is independent of physio-
logical (photorefractory vs. photosensitive) state or daylength--also has
been noted in White-crowned Sparrows (Farner et al., 1966). In first-
TABLE 2
RTE OP OVARraN GROWTa (k)
IN PINEALECTO1VHZED AND 8ItA1V-P1NEALECTO1VIZED TREE SPARROWS
EXPOSED TO 8 HOURS OF CONTIlgUOUS OR DISCONTINUOUS LIGtlT PER DAY
Light (L) - dark (D)
Group schedule, hours k e, days - Days
PC 8L-16D 0.002 ñ 0.003 (11) 76
SPC 8L-16D 0.000 ñ 0.001 (13) 100
PD 6L4-11D-2LS-SD 0.012 __+ 0.006 (8) 49
SPD 6L4-11D-2LS-5D 0.008 ñ 0.003 (11) 790
Prefixes P and SP refer to pinealectomy and sham pinealectomy, respectively.
oLogarithmic ovarian growth-rate constant q- 95 percent confidence interval. Number of birds
in each sample is indicated in parentheses.
a 08:30-16:30 CST.
4 08:30-14:30 CST.
5 01:304)3:30 CST.
6Ovarian growth approximated a logarithmic function of time for number of days indicated
(see Figures 4 and 5).
year birds, and to a lesser extent in adults, ovarian growth, which began
in midsummer during photorefractoriness, continued at a slow rate through
early winter and, then, after transfer to 8L. The contribution of non-
photoperiodic ovarian growth to overall ovarian development in both
Tree and White-crowned Sparrows is minimal, especially in highly photo-
sensitive birds exposed to long daily photoperiods. However, its occur-
rence emphasizes the necessity of determining ovarian weight at the
beginning of the interval over which k is to be estimated, for to assume
that ovarian weight is maintained at some "resting" value during re-
tention on short days is clearly invalid.
Differences in rate of ovarian growth when p = 8, 11, or 15 (or 20)
hours indicate that photosensitive females can measure, within limits,
the duration of the daily photoperiod. Time measurement in avian
photoperiodic gonadal responses is presumed to be effected through an
endogenous circadian oscillation in photosensitivity. According to that
idea, which derives support from the investigations of Hamner (1963,
1964, 1966) and others on male passerines and from the study of Fol-
lett and Sharp (1969) on male and female Japanese Quail, a long day
is gonadostimulatory not because it exceeds a critical length, but because
a portion of it illuminates a photoinducible phase of a circadian rhythm
in photosensitivity. By the same token, a short day is nonstimulatory
because light and photoinducible phase are not coincident. We found
in a preliminary test that, although 8 hours of continuous light in a
24-hour cycle (6L-2L-16D) failed to induce ovarian growth in either
_o o.5
2.0-
jo 1.0-
8 L 16 D Pineaectornized
:- :
6L-11D-2L-5D Pinealectomized
2'o 4b o o 6o
DAYS
Figure 4. Relationship between ovarian weight and time in pinealectomized Tree
Sparrows exposed to 8 hours of continuous or discontinuous light per day. Re-
gression lines were obtained by the method of least squares.
pinealectomized or sham-pinealectomized Tree Sparrows (Figures 4 and
5), 8 hours of discontinuous light in a 24-hour cycle (6L-11D-2L-5D)
stimulated ovarian growth at a slow rate for 49 days in pinealectomized
birds and for 79 days in sham-pinealectomized birds (Figures 4 and 5;
Table 2). These observations are consistent with the notion that an
endogenous periodicity in photosensitivity is entrained to a 24-hour cycle
with coincidence between light and photoinducible phase after termina-
tion of the main (6-hour) photoperiod (or after termination of the 2-
hour photoperiod if "phase-jumping" occurred) and suggest that the
circadian oscillator does not operate through the pineal body. In ad-
dition, the decline in ovarian weights of both pinealectomized and sham-
pinealectomized birds at 100 days to or near initial values suggests that
long-term exposure to 6L-11D-2L-5D, as to conventional long days, may
cause ovarian regression.
ACKIOWLEDG1VfEITS
This investigation was supported in part by the Undergraduate Research Par-
tic/pation Program (GY-2932) of the National Science Foundation. We are grateful '
to French's Pet Bird Laboratory, Rochester, New York, for donating the parakeet
foods: to Richard S. Donham for performing the pineaIectomies, and to Edward
K. Cusick for assisting with laparotomies and field operations. Illustrations were
prepared by the art staff of Extension Information, Kansas State University.
o.s
2.0-
rs-
8 L 16 D Sham-Pinealectomized
6 L - 11 D - 2 L - 5 D Sham-Pinealectomized
6 o 4'0 o 8'0 o'o
DAYS
Figure 5. Relationship between ovarian weight and time in sham-pinealectomized
Tree Sparrows exposed to 8 hours of continuous or discontinous light per day.
Regression lines were obtained by the method of least squares.
SUMMARY
Ovarian growth in photosensitive Tree Sparrows exposed to 20-, 15-, or 11-hour daily photoperiods, after being held on 8-hour daily photoperiods for several months, approximated a logarithmic function of time for at least 35, 42, or 56 days, respectively; photosensitive Tree Sparrows continued simultaneously on 8-hour daily photoperiods for 42 or 56 days failed to show detectable ovarian growth. Rate of photoinduced ovarian growth varied with daylength and was four to five times slower in birds exposed to 11-hour daily photoperiods than in birds exposed to 15- or 20-hour daily photoperiods. Though the rate at 15 hours was exceeded by that at 20, the difference was not statistically significant. An endogenous circadian oscillation in photosensitivity of the response mechanism was suggested by a slow rate of ovarian growth in both pinealectomized and sham-pinealectomized Tree Sparrows exposed to 6-hour daily photoperiods with an additional 2-hour light period beginning 11 hours after onset of darkness. Nonphotoperiodic ovarian growth, of minor importance quantitatively and of no apparent functional significance, was detected in initially photorefractory Tree Sparrows held up to 12 months on 8-hour daily photoperiods.
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Division of Biology, Kansas State University, Manhattan, Kansas
66502. Accepted 30 March 1971.