A tropical bird can use the equatorial change in sunrise and sunset times to synchronize its circannual clock.

Abstract

At higher latitudes, most organisms use the periodic changes in day length to time their annual life cycle. At the equator, changes in day length are minimal, and it is unknown which cues organisms use to synchronize their underlying circannual rhythms to environmental conditions. Here, we demonstrate that the African stonechat (Saxicola torquatus axillaris)-an equatorial songbird-can use subtle solar cues for the annual timing of postnuptial moult, a reliable marker of the circannual cycle. We compared four groups that were kept over more than 3 years: (i) a control group maintained under constant equatorial day length, (ii) a 12-month solar time group maintained under equatorial day length, but including a simulation of the annual periodic change in sunrise and sunset times (solar time), (iii) a 14-month solar time group similar to the previous group but with an extended solar time cycle and (iv) a group maintained under a European temperate photoperiod. Within all 3 years, 12-month solar time birds were significantly more synchronized than controls and 14-month solar time birds. Furthermore, the moult of 12-month solar time birds occurred during the same time of the year as that of free-living Kenyan conspecifics. Thus, our data indicate that stonechats may use the subtle periodic pattern of sunrise and sunset at the equator to synchronize their circannual clock.

Full text

Page 1

A tropical bird can use the equatorial
change in sunrise and sunset times to
synchronize its circannual clock
Wolfgang Goymann1,*, Barbara Helm2,3, Willi Jensen1,
Ingrid Schwabl1and Ignacio T. Moore4
1Max-Planck-Institut fu ¨r Ornithologie, Abteilung fu ¨r Verhaltensneurobiologie,
Eberhard-Gwinner-Straße 6A, 82319 Seewiesen, Germany
2Fachbereich Biologie, Universita ¨t Konstanz, Postfach 616, 78457 Konstanz, Germany
3Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow,
Graham Kerr Building, Glasgow G12 8QQ, UK
4Department of Biological Sciences, Virginia Tech, 2119 Derring Hall, Blacksburg, VA 24060, USA
At higher latitudes, most organisms use the periodic changes in day length to time their annual life cycle.
At the equator, changes in day length are minimal, and it is unknown which cues organisms use to syn-
chronize their underlying circannual rhythms to environmental conditions. Here, we demonstrate that the
African stonechat (Saxicola torquatus axillaris)—an equatorial songbird—can use subtle solar cues for the
annual timing of postnuptial moult, a reliable marker of the circannual cycle. We compared four groups
that were kept over more than 3 years: (i) a control group maintained under constant equatorial day
length, (ii) a 12-month solar time group maintained under equatorial day length, but including a simu-
lation of the annual periodic change in sunrise and sunset times (solar time), (iii) a 14-month solar time
group similar to the previous group but with an extended solar time cycle and (iv) a group maintained
under a European temperate photoperiod. Within all 3 years, 12-month solar time birds were significantly
more synchronized than controls and 14-month solar time birds. Furthermore, the moult of 12-month
solar time birds occurred during the same time of the year as that of free-living Kenyan conspecifics.
Thus, our data indicate that stonechats may use the subtle periodic pattern of sunrise and sunset at
the equator to synchronize their circannual clock.
Keywords: circannual rhythm; equation of time; photoperiod; moult Zeitgeber; life cycle
1. INTRODUCTION
For seasonal organisms, the annual change in day length
(photoperiod) represents the most reliable predictive cue
for the timing of life-cycle stages. For example, many
birds at temperate and high latitudes show circannual
rhythms that are synchronized by photoperiodic infor-
mation as the main Zeitgeber (a synchronizing external
cue; [1]). This synchronization is crucial for the proper
timing of life-history stages and activities such as
migration, breeding and moult (the annual loss and repla-
cement of feathers that is an essential part of the life cycle
of birds) [2–5]. The strength of photoperiod as a Zeitgeber
is demonstrated by the fact that some species can entrain
to photoperiodic cycles that differ greatly from the
12-month period they are naturally exposed to. For
example, sika deer (Cervus nippon) can entrain antler
growth to photoperiodic cycles of only four-month dur-
ation [6] and European starlings (Sturnus vulgaris) are
capable of adjusting their annual life cycle to photo-
periods with a duration of just 2.4 months [3,7].
Further, organisms can be very sensitive to even subtle
photoperiodic cues: some tropical plants and birds have
been shown to respond to slight and gradual changes in
day length with an amplitude of just 15–17 min [8,9].
However, close to the equator, photoperiod is practically
constant (figure 1) and yet, many local organisms show
strictly annual cycles in breeding and other activities
such as moult [10–13]. It is unknown which environ-
mental cues they use to time and synchronize their life
cycle. Gwinner & Scheuerlein [14] addressed this topic
in a tropical songbird, the African stonechat (Saxicola tor-
quatus axillaris). Stonechats show robust endogenous
circannual rhythms [15], but in nature, their life-cycle
stages occur annually. In Kenya, breeding is limited to
the rains around March to June and is followed by post-
nuptial moult that starts at the end of June and
continues until mid-November [16] (see also phenology
data in figure 1). Gwinner & Scheuerlein [14] demon-
strated experimentally that changes in day light intensity
(i.e. mimicking the annual pattern in cloud cover during
the rainy and dry seasons) may provide synchronizing
cues. However, cloud cover is very variable within and
between years and hence may not be precise. There is,
however, an alternative photic cue that is more predictive
and could be used as Zeitgeber: while day length is con-
stant at the equator, the times of sunrise and sunset
fluctuate in parallel by about 30 min over the year with
two recurring annual maxima and minima (referred to
in astronomy as the ‘equation of time’; figure 1 and sup-
plementary discussion 1 in Borchert et al. [12]). This
annual fluctuation is caused by the elliptic shape of the
* Author for correspondence (goymann@orn.mpg.de).
Proc. R. Soc. B (2012) 279, 3527–3534
doi:10.1098/rspb.2012.0743
Published online 30 May 2012
Received 3 April 2012
Accepted 3 May 2012
3527
This journal is q 2012 The Royal Society

Page 2

Earth’s orbit around the sun and the tilt of the Earth’s
axis relative to its orbit and corresponds to the difference
between apparent solar time and the mean time. As a
slight but reliable environmental cue, it is consistent
from year to year and independent of climate, but so far
it is unknown whether animals can use this cue to time
their life cycle. It has been suggested that—close to the
equator—tropical trees synchronize flowering according
to the annual change in the time of sunrise and sunset
or associated changes in insolation [12,17]. In view of
the sensitivity of birds to subtle photic cues [9,18], we
hypothesized that they may be able to entrain to the
annual pattern of sunrise and sunset times at the equator
(hereafter called ‘solar time’).
To test this hypothesis, we examined synchronicity in
fourexperimental groupsof African stonechats of equator-
ial origin that were kept under different photic conditions.
We exposed one group to a constant equatorial photo-
period (constant day length) and simulated the annual
variation in sunrise and sunset time at the equator (12-
month solar time group; upper graph in figure 2b). As a
control to assess the birds’ behaviour in the absence of
any Zeitgeber, a second group was kept under the same
constant equatorial photoperiod but without simulat-
ing the annual change in sunrise and sunset times
(constant time group; upper graph in figure 2a). To
further investigate the ability of stonechats to synchronize
to solar time, we exposed a third group to this poten-
tial Zeitgeber but weakened its strength by extending
the Zeitgeber period to 14 months (14-month solar time
group; upper graph in figure 2c). Because postnuptial
moult was previously found to be a reliable marker
for the annual cycle of stonechats [19–21], we used
individual timing patterns of moult as a measure of syn-
chronization. We further compared the synchronicity of
postnuptial moult of these three groups with that of a
fourth group, consisting of African stonechats studied ear-
lier by our team under a naturally changing European
photoperiod (upper graph in figure 3). The published
studies had shown that this photoperiodic condition acts
as strong Zeitgeber [20,22,23] and are therefore used
here as a positive reference for tight synchronization (via
extraction of information on synchronicity from the
original data).
We predicted that whether variation in sunrise and
sunset functioned as a Zeitgeber, moult of birds in the
12-month solar time group should cycle with the Zeitgeber
period length of 12 months and should be synchronous
between individuals as measured by a synchronicity
index (defined as the per cent overlap in the timing of
moult between individuals). Moult in this group should
occur at a similar time relative to the Zeitgeber as it does
in free-living Kenyan conspecifics (i.e. show a similar
phase-angle difference (c) relative to the periodic change
in sunrise and sunset times as in free-living conspecifics
[16] (see also figure 1). In contrast, birds in the constant
time group should free run with respect to each other
and to external time, i.e. there should be little synchroni-
city among birds and no synchronicity to external time.
The 14-month solar time group was used to further exam-
ine possible Zeitgeber characteristics of solar time. If birds
are able to entrain to this extended and weaker cycle (with
smaller changes in solar time per unit of time when com-
pared with the 12-month solar time group), then they
should synchronize to each other and to a 14-month
cycle, or else, show individual free-running rhythms.
Differences between the three solar time groups should
develop over time, as free-running birds would follow their
individual schedules, so that the last recorded cycles
should yield the clearest contrasts. Furthermore, moult
in birds can proceed independently for body plumage
and flight feathers [24]. In the absence of a Zeitgeber, the
two processes may dissociate, and flight feather moult in
particular can be omitted [14,25,26]. We therefore use
dissociation of the two moult processes as further evidence
of weak or absent entrainment.
2. METHODS
(a) Study animals
Originally, we used 24 African stonechats, all of which were
descendantsofaresident
Nakuru, Kenya (08140S, 36800E; 2500 m a.s.l.) in 1999.
Six birds hatched in 1999 were collected as nestlings in
Kenya, the other birds were bred and raised in captivity in
2001 (n ¼ 1), 2002 (n ¼ 3), 2003 (n ¼ 7), 2004 (n ¼ 1)
and 2005 (n ¼ 6). Before the experiment, all birds were
maintained and synchronized under the local photoperiod
of Erling-Andechs, Germany (47.58 N). On 5 August
2005, during postnuptial moult, the birds were moved to
three identical indoor rooms. Birds of different sex and age
classes and siblings were equally distributed among rooms
so that these factors would not bias results. Three additional
stonechats entered the experiment in October and Decem-
ber 2005 and in March 2006 (hatched in 1999 and 2004)
to replace birds that had died. The birds received our stan-
dard diet [27] and were kept in individual cages (60 ?
35 ? 45 cm) where they could hear but not see each other
until January 2009. In addition, we used data from 13
African stonechats collected in Kenya that were maintained
under a European photoperiod in the same temperature-
controlled indoor rooms from 1982 to 1984. These African
stonechats were studied from fledging until the completion
of their second adult moult. We include data from five
females and eight males (for details on these birds see earlier
studies [20,22]).
populationimportedfrom
(b) Experimental rooms and treatment
Birds were kept in three adjacent sound-proof and tempera-
ture-controlled rooms connected to the same ventilation
system [18]. Each room was equipped with two halogen
lamps with dimmable 150 W Osram Haloline 646 959
bulbs (colour rendering index 100, colour temperature
3000 K). The lamps were mounted in line with the cages,
so that the birds received light only indirectly from a white
reflecting wall opposite the light source, i.e. birds could not
get any ‘celestial cues’ from the two light sources. Light inten-
sity was approximately 400 lux at the front of each cage.
During the night, several small light bulbs ensured indirect
‘moonlight’ illumination of 0.01 lux. Room temperature in
all rooms ranged between 188C and 208C during the night
and from 22 to 258C during the day. The photoperiod in all
three rooms was 12.07 h of light plus two 25 min periods of
dawn and dusk during which light intensity gradually
increased or decreased from 0.01 (night level) to 400 lux
(day level). These conditions simulated the natural day
length including dusk and dawn (based on civil twilight) at
an elevation of 2500 m a.s.l. at the equator, corresponding
3528W. Goymann et al.
Solar time synchronizes circannual clock
Proc. R. Soc. B (2012)

Page 3

to the altitude at Nakuru, Kenya. The first room housed the
constant time group. Here, the timing of sunrise and sunset
was kept constant throughout the year with dawn starting at
06.05 (full daylight at 06.30) and dusk starting at 18.37
(full night at 18.02; figure 2a). Day length and sunrise
times were calculated with Astronomy Lab 2 (Personal
MicroCosms, Greenwood Village, CO 80112, USA). The
second room housed the 12-month solar time group. This
group received a simulation of the annual variation in sunrise
and sunset time at the equator: the onset of dawn started
between 05.51 and 06.22 (full day light between 06.16 and
06.47) and onset of dusk between 18.23 and 18.54 (night
between 18.48–19.19; figure 2b). In the third room, birds
received a simulation of the annual variation in sunrise/
sunset time, but the natural cycle of 12 months was length-
ened to 14 months (14-month solar time group; figure 2c).
The changes in sunrise and sunset times were implemented
in weekly intervals in steps ranging from 0 to 3 min depend-
ing on the steepness of the cycle (figures 1 and 2). In
addition, we compared the data from these three groups
with a fourth group of 13 African stonechats that had been
maintained under the photoperiodic conditions of migratory
European stonechats at 47.58 N during summer and 408 N
during winter in a previous study (see earlier studies
[20,22,23]). In these birds, day length was adjusted weekly
assuming that they reach 458 on 4 October 42.58 on 11 Octo-
ber and 408 on 18 October (figure 3). In spring, birds were
assumed to reach 42.58 on 28 February, 458 on 7 March
and 47.58 on 14 March. In these birds, there was no simu-
lation of dawn and dusk, but light intensity was similar to
the other three groups with 0.01 lux at night and 400 lux
during the day.
To examine entrainment to the change in sunrise and
sunset time, we quantified the phase-angle difference (c) of
moult onset to the putative Zeitgeber cycle as follows.
As reference phase, we chose the date on which sunrise
and sunset were timed the latest (Julian date 41, i.e. 10
February; figure 1). Based on published field data from
free-living Kenyan stonechats, moult started on 30 June (cal-
culated as the mean date between captures of free-living
stonechats that did not yet moult and the first captures that
showed substantial moult (see our fig. 1 and fig. 4d,e in
Dittami & Gwinner [16])). This yielded a phase-delayed
and, hence negative, phase-angle difference c of 2141 days.
(c) Moult parameters and statistical analysis
For the duration of the study, every two to three weeks we
recorded—for each bird—the state of moult for body and
flight feathers separately. We assessed the state of body
moult by noting feather growth in any of the 19 different
feather tracts on the bird’s body [28]. We defined the onset
of body moult as the mean date between the last recording
without moult and the first day on which moult was detected
in at least four of the 19 feather tracts. End of moult was
defined as the mean date between the last recording with
moult finished in at least 15 of the 19 feather tracts and the
first day without moult. Flight feather moult was scored fol-
lowing [29]. All 10 primaries and all nine secondary wing
feathers were scored on a scale from 0 (old) to 5 (fully
grown new). Scores were averaged over the two wings result-
ing in values ranging from 0 (all feathers old) to 95 (all
feathers new). Onset of flight feather moult was defined as
the mean date between the last recording without flight
feather moult and the first day on which at least one primary
or secondary moulted, and completion was defined as the
mean date between the last recording with moult and the
first recording without moult. For each year and within each
group, we then measured the proportion of overlap in moult
of each individual with each other individual. An example
illustrates how the proportion of overlap in moult was calcu-
lated: let us assume we have two individuals A and B. A
moults from day 50 to 100, and B moults from day 75 to
150. This means that the moult of individual A overlaps
during 50 per cent of its total duration (days 75–100) with
the moult of individual B. However, the moult of individual
B overlaps only 33.3 per cent of its total duration (days 75–
100) with that of individual A. From these individual
values, we then calculated the mean for each individual,
which gives the moult synchronicity index of each individual
within its group (figure 4). This moult synchronicity index
was then compared between groups using a non-parametric
Kruskal–Wallis test and Conover post hoc tests [30]. Non-
parametric testswereused because theyaremoreconservative
and with small sample sizes normality tests are not very
reliable. However,parametric
mixed model) rendered similar results. For the calculation,
we used data only for individuals that had entered the exper-
iment at the latest in April 2006 and that had completed all
cycles from the beginning of the experiment until the period
of analysis (first, second and third year). The sample sizes
for the first, second and third year were 7, 7 and 6 for the con-
stant time group, 7, 7 and 5 for the 12-month solar time
group, and 5, 5 and 4 for the 14-month solar time group
(see also table 1). We also created mean body and flight
feather moult curves of individuals within each treatment
group by taking the mean score of a 20-day period. Smooth-
ing was performed by calculating a moving average over five
adjacent 20-day periods. A regular sinusoidal curve with
tests (generalized-linear
Table 1. Per cent of synchronicity in body moult and flight feather (wing) moult during three consecutive years. Values are
means+95% CIs; values printed in bold are significantly different from the constant time and/or the 14-month solar time
group (for details, see text and figure 4). Asterisk represents not included, as during juvenile moult flight feathers show no
regular moult pattern.
yearmoultConstant 12-month solar time14-month solar timeEuropean photoperiod
first body
wing
22.0+12.0; n ¼ 7
7.7+7.6; n ¼ 7
15.0+12.3; n ¼ 6
17.5+14.6; n ¼ 6
18.0+8.4; n ¼ 5
14.4+9.9; n ¼ 5
31.9+11.3; n ¼ 7
43.1+13.7; n ¼ 7
22.2+19.4; n ¼ 5
38.8+19.4; n ¼ 5
50.4+12.7; n ¼ 5
53.6+24.7; n ¼ 5
15.5+11.6; n ¼ 8
6.6+6.4; n ¼ 5
25.8+29.1; n ¼ 4
10.2+19.6; n ¼ 4
19.5+23.6; n ¼ 4
18.5+16.5; n ¼ 4
88.9+3.6; n ¼ 13
*
86.5+2.9; n ¼ 13
85.2+4.2; n ¼ 13
84.0+5.0; n ¼ 10
86.5+4.7; n ¼ 10
secondbody
wing
thirdbody
Wing
Solar time synchronizes circannual clock
W. Goymann et al.3529
Proc. R. Soc. B (2012)

Page 4

one peak per year indicates synchronization to an external cue
with the magnitude of the amplitude reflecting the degree of
synchronization among birds within a group: a high ampli-
tude indicates that the birds of one group are synchronous
to each other whereas a low amplitude indicates low synchro-
nicity among birds. In contrast, an irregular curve with
various peaks per year indicates free-running rhythms, i.e.
each bird follows its own endogenous schedule without syn-
chronization to an external Zeitgeber cue.
To calculate the period length t of moult cycles between
the second and third year, we used body moult only, because
several birds of the constant time and 14-month solar time
group showed irregular patterns or skipped flight feather
moult. Period length t for each bird was measured by calcu-
lating the difference between moult completion date in the
third year and moult completion date in the second year.
Statistical comparisons were conducted with SYSTAT 13 at
an a-level of 0.05 (two-tailed). To minimize the loss of
birds along the experiment, we did not measure gonad size
that requires invasive surgery, nor puncture the birds’ veins
for repeated blood sampling.
3. RESULTS
We found that during the first cycle, for which we had pre-
dicted weak differences between treatments, the groups
differed significantly in synchronicity of body moult
(Kruskal–Wallis test Hbody moult¼ 25.80, p , 0.0001).
The body moult was significantly more synchronous
between birds exposed to a European photoperiod
than between birds of all other groups (post hoc Conover
tests: all ps , 0.0001). Birds of the 12-month solar time
group were significantly more synchronous to each other
than birds of the 14-month solar time group (p ¼ 0.01)
and tended to be more synchronous than birds in the con-
stant control group (p ¼ 0.08; table 1, figures 2 and 3).
Flight feather moult also differed significantly in synchro-
nicity between groups (H ¼ 13.03, p , 0.002), being
significantly higher in the 12-month solar time group
than in the control (p , 0.001) and the 14-month solar
time group (p , 0.001; table 1, figures 2 and 3). Birds
maintained under a European photoperiod were not
included in this comparison because their first cycle,
post-juvenile moult, did not involve replacement of flight
feathers (figure 3).
During the second cycle, synchronicity of body and
flight feather moult also differed significantly between
the groups (Hbody moult¼ 10.55, p ¼ 0.0001; Hflight feather
moult¼ 22.20, p , 0.0001; figures 2 and 3). Body and
flight feather moult of birds under a European photo-
period was more synchronous than those of birds in all
other groups (all ps , 0.0001). Furthermore, synchroni-
city of flight feather moult was significantly higher in
birds of the 12-month solar treatment than in birds of
the constant control group (p ¼ 0.02) and the 14-month
solar time group (p ¼ 0.007; table 1, figures 2 and 3).
In the third and last year, the synchronicity of both
body and flight feather moult differed significantly
between treatments (Hbody
Hflight feather moult¼ 19.59, p ¼ 0.0002): body and flight
feather moults of birds in the 12-month solar time group
were significantly moresynchronous than thoseof the con-
stant time and the 14-month solar time group (figures
2–4, table 1), but less so than in the group of African
moult¼ 20.45, p , 0.0002,
stonechats entrained to the European photoperiod
(figures 3 and 4, table 1).
Furthermore, in contrast to birds of the constant time
and the 14-month solar time group, birds of the 12-
month solar time group showed coupled patterns of
body and flight feather moult in all years (figure 2), indi-
cating a common Zeitgeber for the different kinds of
moult. Another indicator of a common Zeitgeber were
the smoothed averages of body and flight feather moult
in the 12-month solar time group (blue and orange
curves in figure 2b): similar to the European photoperiod
group (figure 3), the 12-month solar time group showed a
regular pattern with one clear sinusoidal moulting peak
per year (figure 2b), indicating synchronization among
birds and within each year. The sinus amplitude of the
European photoperiod group was higher than the ampli-
tude of the 12-month solar time group, demonstrating
that photoperiod is a stronger Zeitgeber than solar time.
In contrast to these two groups, the constant control
group and the 14-month solar time group showed irregu-
lar smoothed average curves without a clear annual peak
in combination with low amplitudes (figure 2a,c), thus
indicating low synchronicity among birds, suggesting
that each bird followed its own free-running rhythm.
Period length of the body moult cycle between the
second and third year was closest to the expected 365
days in birds maintained under a European photoperiod
and in the 12-month solar time group (figure5). The coef-
ficient of variation (CV) in period length was lowest in the
group maintained under a European photoperiod (CV ¼
0.05), intermediate for the 12-month solar time group
(CV ¼ 0.16) and highest for the groups maintained
under 14-month solar time (CV ¼ 0.34) and constant
time conditions (CV ¼ 0.33). For flight feather moult,
we could not calculate the period length between
06.49
06.44
06.39
time of sunrise
day length (h)
06.34
06.29
06.24
06.190
60 120
Julian date (days)
180240 300 360
sunrise and day length
y = –141 days
12.11
12.09
12.07
12.05
12.03
Figure 1. The annual change in the time of sunrise (solid red
line) and subsequent sunset (not shown) in combination with
a constant photoperiod (horizontal dotted black line) at
Nakuru, Kenya (08000N, 368000E). This annual change in
sunrise and sunset is referred to as the ‘equation of time’ in
astronomy and is caused by the elliptic shape of the Earth’s
orbit around the sun and the tilt of the Earth’s axis relative
to its orbit. The horizontal bars indicate the period during
which free-living African stonechats at Nakuru, Kenya,
breed (black bar) and moult their body- (blue bar) and
flight feathers (orange bar) [16]. The arrow between the
two vertical dashed lines indicates the phase-angle difference
(c) between the day on which sunrise is latest (Julian day 41)
and the mean date with the first occasion of moult (Julian day
182) in free-living African stonechats.
3530W. Goymann et al.
Solar time synchronizes circannual clock
Proc. R. Soc. B (2012)

Page 5

the second and third year for the constant time and the
14-month solar time group, because some birds showed
irregular moult patterns. By contrast, all birds of the
12-month solar time group showed a consistent pattern
of flight feather moult with a period close to one year
(mean period +95% CI: 360.8+60.3 days, CV ¼ 0.13).
06.36
06.51
06.43
06.35
06.27
06.19
f 372
f 334
m 367
m 389
f 365
f 391
m 358
06.51
06.43
06.35
06.27
06.19
m 395
f 347
f 392
f 393
f 360
m 355
m 323
m 327
sunrise
individual
sunrise
individual
sunrise
individual
first year second yearthird year
first year second yearthird year
first cyclesecond cyclethird cycle
(a)
(b)
(c)
06.30
06.24
m 329
m 375
m 390
f 364
m 366
f 388
f 362
25
20
15
mean moult score
10
5
0
25
20
15
mean moult score
10
5
0
25
20
15
mean moult score
10
5
0
200400600800
time (days)
100012001400
Figure 2. Body moult (blue bars) and flight feather moult (orange bars) of African stonechats maintained under an equatorial
photoperiod for almost 31
2years. The thin (brown) lines indicate the total time each individual bird stayed in the experiment.
The time axis represents consecutive days (1 denotes 1 January 2005). The experiment started in August 2005 (day 215) and
ended in January 2009 (day 1500). Depicted are three groups of birds which either received (a) no change in the timing of
sunrise and sunset (constant time conditions; upper graph in (a), (b) a simulation of the natural, 12-month cycle in the
change of sunrise and sunset times at the equator (12-month solar time conditions, upper graph in (b); only change in sunrise
shown, but sunset changes accordingly) and (c) a simulation of the annual pattern in sunrise and sunset times at the equator
stretched to 14 months (14-month solar time conditions; upper graph in c; only sunrise shown). The blue and orange curves
represent smoothed averages of body moult and flight feather moult scores of all individuals within one group (represented on
the right y-axis scale; see methods for the details of how the smoothed averages were calculated), respectively. A sinusoidal
curve with one peak per year indicates synchronization to an external annual Zeitgeber with the magnitude of the amplitude
reflecting synchronicity among birds within one group. A curve with several peaks per year indicates the absence of synchro-
nization to an external Zeitgeber. Please note that owing to differences in scoring method the amplitude of body moult (blue) is
naturally smaller than the amplitude of flight feather moult (orange). The dashed vertical lines indicate the external years in
(a,b) and the prolonged 14 month ‘year’ in (c). (b) Black vertical arrows in the upper graphs indicate the onset of moult in
free-living stonechats at Nakuru, Kenya. (c) Vertical arrows indicate the expected onset of moult in case the birds would
have synchronized to a 14-month solar time period. Both the vertical dashed lines and the arrows serve as orientation how
rhythms should be arranged if they were entrained. Note that all birds were initially synchronized to a European photoperiod
before they entered the experiment (with most birds still moulting when entering the experiment around day 215). Bird IDs
starting with ‘f’ represent females, those starting with ‘m’ represent males.
Solar time synchronizes circannual clock
W. Goymann et al.3531
Proc. R. Soc. B (2012)

Page 6

Together,these results indicatethat birdsmaintained under
the 12-month solar time condition were more closely syn-
chronized to the 365 day cycle than the birds of the
constant and 14-month solar time period, but less so than
birds maintained under a European photoperiod.
Onset of moult in birds of the 12-month solar time
group was timed similarly as in free-living conspecifics.
For free-living Kenyan stonechats, flight feather and
body moult was observed to start 141 days after the
chosen reference phase (i.e. the day with the latest sunrise
and sunset; figure 1). This negative phase-angle difference
was closely matched by the timing of flight feather moult
in the 12-month solar time group (mean c+95%
CI ¼ 2141+28 days in the first year, c ¼ 2144+57
days in the second year and c ¼ 2138+64 days in the
third year). Onset of body moult occurred slightly earlier
with c ¼ 2129+63 days in the first year, c ¼ 2142+
63 days in the second year and c ¼ 2109+43 days
in the third year. The smoothed averages (figure 2b)
indicate that both types of moult were highly synchronized
in birds of the 12-month solar time group. These data
strongly suggest that the photic cues of the 12-month
solar time simulation acted as a Zeitgeber to which the
birds could synchronize.
4. DISCUSSION
Our findings support the hypothesis that the annual
change in the timing of sunrise and sunset is a potential
Zeitgeber for circannual rhythms of equatorial birds. In
the absence of any change in day length, stonechats in
the 12-month solar time group entrained to the subtle
shift of the solar day and assumed a phase relationship
to the Zeitgeber that was similar to the situation observed
in free-living birds [16]. Compared with the photoperi-
odic cues of a northern temperate photoperiod this
Zeitgeber was relatively weak, potentially allowing other
environmental cues (e.g. cloud cover [14] or slight
changes in the duration of dawn and dusk [18,31]) to
further modify the circannual rhythm. When this subtle
Zeitgeber was further reduced in strength by changing its
period length from a natural 12-month solar time cycle
to a 14-month solar time cycle (and consequently attenu-
ated changes in sunrise and sunset times), entrainment
was absent. Because the stonechats’ endogenous circann-
ual rhythm is usually 9–10 months [15] and entrainment
gets weaker the further the Zeitgeber period differs from
the endogenous period [7] birds in the 14-month solar
18
16
14
12
10
day length
(h)
individual
m gr79
f gr76
m gr75
f gr72
f gr70
m gr69
m gr66
m gr62
m gr60
f gr59
f gr56
m gr52
m gr50
0 200 400
time (days)
6008001000
50
40
30
mean moult score
20
10
0
first yearsecond year third year
Figure 3. Body moult (blue bar) and flight feather moult
(orange bar) of African stonechats maintained under a Euro-
pean photoperiod (upper graph with the red line indicating
the length of the daily period with lights-on) from hatching
(approx. day 115) until the end of their third year of life.
The time axis represents consecutive days (1 denotes 1 Jan-
uary 1982). The thin brown line indicates the total time
each individual bird stayed in the experiment. The blue
and orange curves represent smoothed averages of body
moult and flight feather moult scores (represented on the
right y-axis scale; see methods for the details of how the
smoothed averages were calculated), respectively. A sinusoi-
dal curve with one peak per year indicates synchronization
to an external annual Zeitgeber with the magnitude of the
amplitude reflecting synchronicity among birds. A curve
with several peaks per year indicates the absence of synchro-
nization to an external Zeitgeber. Please note that owing to
differences in scoring method the amplitude of body moult
(blue) is naturally smaller than the amplitude of flight feather
moult (orange). Bird IDs starting with ‘f’ represent females,
those starting with ‘m’ represent males.
(a)
(b)
100
p = 0.0005
p = 0.012
p < 0.002
p < 0.0001
p< 0.002
constant
time
12-month
solar time
14-month
solar time
European
photoperiod
p = 0.004
80
60
% overlap in moult
40
20
0
100
80
60
% overlap in moult
40
20
0
Figure 4. (a) Synchronicity of flight feather and (b) body
moult of equatorial stonechats during the third year of the
experiment (median and interquartile range). Birds main-
tained under a simulation of the natural 12-month change
in sunrise and sunset times at the equator (12-month solar
time group) showed an intermediate pattern of moult syn-
chronicity. They were significantly more synchronous than
birds kept under equatorial conditions with a constant time
of sunrise and sunset (constant time group), and birds main-
tained under a simulation of the change in sunrise and sunset
times extended to a 14-month period (14-month solar time
group). At the same time, they were less synchronous than
equatorial stonechats maintained under a northern temper-
ate European photoperiod (Kruskal–Wallis test with post
hoc comparisons following Conover [30]).
3532W. Goymann et al.
Solar time synchronizes circannual clock
Proc. R. Soc. B (2012)

Page 7

time group may not have been able to adjust their clocks
to this particular Zeitgeber. In fact, the 14-month cycle
even seemed to disrupt the circannual rhythm as the indi-
vidual moult patterns of birds appeared to be less regular
in the 14-month solar time group compared with the con-
stant time group (figure 2). This is intriguing, as it has
been demonstrated before that a circannual cycle can
develop only under permissive conditions, i.e. African
stonechats showed circannual cycles under a constant
photoperiod with 12.25 hrs of light, but 70 per cent of
them ceased to cycle with a constant photoperiod of
12.8 hrs of light without simulated dawn and dusk [25].
Similar to many other longer-lived tropical organisms,
African stonechats at the equator express a highly seasonal
annual life cycle with reproduction during the rainy season
and subsequent moult when the young become indepen-
dent [16,32]. In captivity, African stonechats show
strong and robust endogenous circannual cycles under
permissive conditions [19,21,25], but how these cycles
are synchronized in nature had remained unclear although
changes in day light intensity owing to annual cycles of
cloud cover may play a role [14]. Our data suggest that
the annual pattern of sunrise and sunset time at the
equator may be a sufficient environmental cue to function
as a Zeitgeber. We are aware of only one other experimental
study that examined entrainment to an annual cycle of
sunrise and sunset times. The study species, Anoura geof-
froyi, a tropical bat, failed to synchronize its circannual
rhythm to a nine-month cycle, or in fact to any kind of
photoperiodic simulation [33].
It is highly unlikely that the higher synchronicity of the
12-month solar time group was caused by an external
stimulus other than the change in the timing of sunrise
and sunset. All three experimental rooms were adjacent
to each other, were connected to the same ventilation,
electrical and light-control systems, sex and age classes
were similar between the rooms, and all birds were fed
and cages cleaned at the same time of the day. Thus, any
disturbance would have affected all three rooms equally.
Furthermore, any synchronization owing to vocal inter-
actions (the birds could not see each other!) should have
been similar in all experimental rooms. Before the exper-
iment, all birds were maintained under a European
photoperiod, which represents a very strong Zeitgeber
cue, potentially explaining why it took the 12-month
solar time birds three cycles to fully synchronize to the
weaker Zeitgeber.
The mechanistic details of circannual rhythms and
their entrainment to Zeitgeber are still poorly understood.
However, in a number of organisms from beetles to mam-
mals [34–36], it has become clear that circannual clocks
respond to photic cues in a phase-dependent way. This
may explain how African stonechats could breed annually
despite the biannual changes in sunrise and sunset times.
Stonechats are highly responsive to slight differences in
photic cues during specific times of year [37], while
during other periods of the year their reproductive
system shows little or no response to stimulatory light
conditions [14]. If accommodated to equatorial light con-
ditions, then circannual phase responses could function
as a filter that enables the birds to respond to only one
annual recurrence of inductive light conditions. Such
putative filter effects of circannual rhythms would fit
well with current thinking of their adaptive significance
[38,39]. Recent research, most visibly in the context of
rapid global change, has documented the fitness costs of
mismatches between seasonal behaviours and environ-
mental cycles. The ability of organisms to avoid such
mismatches hinges on their ability to correctly predict
and anticipate environmental seasonality, not only at
high latitudes but also in seasonal tropical habitats such
as those used by African stonechats [15,16]. On their
Kenyan breeding grounds, the occurrence of rainy and
dry seasons is predictable over a range of several years,
and timely preparation for breeding may give birds a valu-
able head start for maximizing reproductive output
during the short time of high insect availability. Com-
pared with photoperiodically predictable high-latitude
habitats, it is more difficult at the equator to anticipate
the time of highest likelihood of rains and to buffer against
breeding after spurious, short rains. Being able to use
subtle solar cues to predict correctly upcoming seasons
could therefore provide survival and reproductive value,
and thus enhance fitness [39]. As a consequence, selec-
tion should favour animals that are able to predict
periods of favourable conditions to time life cycles such
as reproduction or moult [38].
To our knowledge, this is the first experimental
study demonstrating that a tropical organism can use
the subtle celestial cue of the timing in sunrise and
sunset to set its circannual clock. Because the annual
variation in sunrise and sunset at the equator has pre-
viously been suggested to time the synchronicity in
flowering and bud-breaking in tropical plants [12, 17],
we suggest that the use of solar time may be widespread
among taxonomic groups with strong seasonality within
the tropics.
We thank Andrea Peter and Sonja Bauer for bird care and
assistance with the measurements, and Monika Trappschuh
for assistance with data entry. Furthermore, we thank
NicoleGeberzahn,Michaela
Scheuerlein for discussions and comments. This study was
funded by the Max-Planck Gesellschaft, B.H. is supported
by the European Social Fund in Baden-Wu ¨rttemberg.
I.T.M. acknowledges support from NSF grant no. IOS-
0545735. This paper is dedicated to the memory of the late
Ebo Gwinner, who encouraged this kind of experiment in
1985 [31], and the famous chronobiology institute in
Erling-Andechs.
Hauand Alexander
800
period of body moult (days)
700
600
500
400
300
200
100
365days
constant
time
12-month
solar time
14-month
solar time
European
photoperiod
0
Figure 5. Mean period length t (+95% CI) of body moult
between the second and the third year of the experiment.
The variance around the mean was significantly lower in
the 12-month solar time group than those maintained
under constant time conditions (for details, see text).
Solar time synchronizes circannual clock
W. Goymann et al. 3533
Proc. R. Soc. B (2012)

Page 8

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