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The effects of season, sex, age and weather on
population-level variation in the timing of activity in
Eurasian Blue Tits Cyanistes caeruleus
LOTTE SCHLICHT*& BART KEMPENAERS
Max Planck Institute for Ornithology, Eberhard-Gwinner-Str. 7, 82369, Seewiesen, Germany
All birds sleep and many do so in a specific location, the roost. Thus, every day each
individual needs to decide when to go to (enter) and leave the roosting place. This deter-
mines the timing of activity, a trait shaped by both natural and sexual selection. Despite
its importance in a variety of contexts, including foraging, predation, mating success and
parental care, variation in the timing of activity has rarely been studied. Here, we
describe this variation in a population of Eurasian Blue Tits Cyanistes caeruleus roosting
in nestboxes using data collected over 7 years. We investigate seasonal changes in the
start and end of activity and assess to what extent these parameters are sex- and age-
specific and affected by weather. We show that the start of activity is relatively constant
in relation to sunrise during winter but undergoes drastic changes during the breeding
season. The end of activity is markedly later relative to sunset in mid-winter and is also
strongly influenced by breeding behaviour. Females generally start their activity later and
end it earlier than males. The duration of daily activity is shorter during periods of rain
and longer when temperatures are relatively high for the time of year.
Keywords: breeding, daily rhythm, diurnal behaviour, long-term dataset, non-breeding, passerine.
All birds, and indeed most animals, sleep (Miya-
zaki et al. 2017), but the timing of activity and
rest may vary dramatically both between and
within species (Campbell & Tobler 1984, Randler
2014). Generally, individuals show specific rest–ac-
tivity cycles, depending on their circadian rhythm
(e.g. diurnality, nocturnality) or feeding routines
(e.g. crepuscular hunting in owls or tide-depen-
dent feeding in shorebirds; reviewed in Campbell
& Tobler 1984). In arctic regions, under periods of
constant light or darkness, individuals may also
become arrhythmic (e.g. Peiponen 1962, Steiger
et al. 2013). At the within-species level, individu-
als may differ in their level and timing of activity
depending on a variety of individual-specific (e.g.
condition), environmental (e.g. weather) and social
factors (e.g. activity of the partner).
Activity patterns are shaped by both natural
and sexual selection. An example of the latter
stems from a study on activity in the Pectoral
Sandpiper Calidris melanotos (Lesku et al. 2012).
In this polygynous shorebird that breeds in the
high arctic under continuous daylight, males were
active on average 90% of the total time during the
period when fertile females were present, and the
most active males sired the most offspring. A few
weeks later, when fertile females were no longer
available, activity levels dropped substantially (to
about 70%; Lesku et al. 2012). The timing and
amount of activity will also be under natural selec-
tion, for example to optimize foraging opportuni-
ties, to respond to the needs of the offspring (e.g.
incubation, Kluijver 1950) or to avoid predation.
Many terrestrial, diurnal birds breed in cavities.
They typically also spend the night in a roosting
cavity, although some individuals may roost on
branches hidden in the foliage (reviewed by Main-
waring 2011). During most of the period they
spend inside their roost they sleep, although they
may also engage in activities such as resting, preen-
ing or nest maintenance (Steinmeyer et al. 2010).
The amount of time spent sleeping may especially
*Corresponding author.
Email: lschlicht@orn.mpg.de
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
Ibis (2020) doi: 10.1111/ibi.12818
be reduced when individuals are disturbed, for
instance by the presence of nestlings or artificial
light (Raap et al. 2016, but see Sun et al. 2017).
The roost may also serve as a refuge, protecting
the individual against predators and adverse
weather conditions. Being tied to a roost, however,
prohibits other behaviours such as foraging, mate
attraction, territory defence, mate guarding and
nestling provisioning. It is therefore likely that
individuals face fitness-relevant trade-offs about
when to enter their roosting place in the evening
and when to leave it in the morning (Mainwaring
2011). Despite the importance of the timing and
amount of activity, studies that describe the start
and end of activity in detail, span a larger period
and monitor more than a few individuals remain
rare.
The few existing studies are mostly about solitar-
ily roosting, cavity-nesting songbirds, specifically
Eurasian Blue Tits Cyanistes careuleus (hereafter,
‘Blue Tit’) and Great Tits Parus major (Kluijver
1950, Hinde 1952, Steinmeyer et al. 2010, Schlicht
et al. 2014, Stuber et al. 2015). The first two studies
present data on only one (Hinde 1952) or a few
(Kluijver 1950) individuals during breeding, with
many data points per individual (>50), whereas the
last three investigated many individuals, but with
relatively few data points per individual across the
year. Several other studies have investigated the
start and/or end of activity, but instead of providing
detailed information on timing, they focus on the
relationship with other variables (see below). Fur-
thermore, many studies do not investigate the start
and end of activity itself, but rather related beha-
viour, usually the start of dawn song (e.g. Cuthill &
McDonald 1990, Poesel et al. 2004, Da Silva &
Kempenaers 2017).
Several predictors of the timing of activity have
been investigated. First, the main determinant of
the start and end of daily activity is day length
(Kluijver 1950, Hinde 1952, Amlaner & Ball
1983). Songbirds are generally day-active and
vision-dependent, so a link with ambient light
levels is inevitable. Nonetheless, small-scale varia-
tion in light levels at the roost did not influence an
individual’s timing of entering or leaving the roost
in one study of Blue Tits (Steinmeyer et al. 2010).
In accordance with the importance of light levels,
rainfall or cloudiness delayed the start of morning
activity and hastened the time when individuals
retired in the evening across several species (Klui-
jver 1950, Hinde 1952, Bruni et al. 2014, Da Silva
et al. 2016). However, the effect of rain may also
be driven by reduced foraging success, reduced
predator recognition and hampering of flight.
Finally, several studies showed that exposure to
artificial night lighting influences activity patterns
and sleep (e.g. Kempenaers et al. 2010, Dominoni
et al. 2013, 2014, Russ et al. 2015, Raap et al.
2016, Da Silva et al. 2017, Sun et al. 2017; but
see Raap et al. 2018).
Second, the timing of activity seems to be tem-
perature-dependent, although findings vary. For
example, Bruni et al. (2014) found that individuals
of several songbird species started to sing earlier
when it was warmer, but Da Silva et al. (2016)
found no such effect for several other songbird
species. In further contrast, Hinde (1952) reported
that Great Tits emerged later when temperatures
were higher. Lower temperatures may be linked to
reduced foraging success or increased need for
energy saving (explaining later emergence and ear-
lier start of roosting), but the higher need for
energy and reduced foraging efficiency may also
force individuals to be active for longer. It is there-
fore likely that the effects of relative temperature
vary, for example with the season, with latitude
and with individual traits such as body size or
dominance.
Third, the start and end of daily activity are
known to change abruptly during the breeding sea-
son (Kluijver 1950, Hinde 1952, Amlaner & Ball
1983, Steinmeyer et al. 2010). For example, male
Blue Tits became active earlier relative to females
at the start of the breeding season (Steinmeyer
et al. 2010), and Great Tit females showed a much
shorter active period during incubation (Kluijver
1950). Similarly, female Blue Tits emerged earliest
around the time when they lay their first egg (Sch-
licht et al. 2014), and the same pattern has been
reported in several species for the start of male
dawn singing (e.g. Cuthill & McDonald 1990,
Halfwerk et al. 2011). In females, an advance in
emergence times could be driven by energetic
needs prior to laying, allowing increased foraging
time. Alternatively, hormonal changes may influ-
ence activity patterns. For instance, the daily and
seasonal timing of female reproduction may be
linked to differences in the timing of the photosen-
sitive period (Graham et al. 2017). Males may also
advance their emergence times as a result of ener-
getic demands or changes in hormone levels, or
they may follow female emergence patterns to
ensure paternity. Testosterone levels peak with
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
2L. Schlicht &B. Kempenaers
singing activity in temperate-zone songbirds, and
testosterone may therefore have an impact on the
start or end of activity. However, a study of Blue
Tits did not find a relationship between experi-
mentally elevated testosterone levels and the tim-
ing of the dawn chorus (Kunc et al. 2006).
Fourth, several individual-specific traits are
known to influence the timing of activity. For
example, females typically enter their roosting
place earlier in the evening and leave later in the
morning than males (e.g. Kluijver 1950, Hinde
1952, Steinmeyer et al. 2010, Stuber et al. 2015),
and younger birds may be less active than older
ones (e.g. roosting in fledgling Great Tits com-
pared with adults, Kluijver 1950; start of dawn
singing in yearling vs. adult male Blue Tits; Poesel
et al. 2004). The timing of activity also varies with
hormone levels (Greives et al. 2015) and food
availability (Kluijver 1950, Cuthill & McDonald
1990; but see Saggese et al. 2011), suggesting a
potential influence of condition.
Fifth, the start and the end of activity may be
individual-specific. Although a study of Great Tits
reported no repeatability of both start and end of
activity (Stuber et al. 2015), these traits were
moderately and significantly repeatable in Blue Tits
(r0.3–0.4, Steinmeyer et al. 2010, Schlicht
et al. 2014) and in Common Blackbirds Turdus
merula (r0.5, Dominoni et al. 2013). Similarly,
Mace (1986) and Kluijver (1950) reported that
two individual Great Tits (of fewer than 10 stud-
ied) emerged from their respective roosts more
than 1 h apart on the same date and during nest-
ling provisioning, when activity (foraging) should
be under strong selection. Interestingly, the start of
morning activity appears to be less variable than
the time an individual retires to roost (Hinde
1952, Amlaner & Ball 1983, Slagsvold 1996, see
also Da Silva et al. 2017). This could indicate that
selection on the timing of morning behaviour is
stronger than selection on evening behaviour. Such
an effect could be linked to a strongly pronounced
dawn chorus compared with the dusk chorus
(Catchpole & Slater 2008). Alternatively, waking-
up times, which correlate closely with emergence
times (Steinmeyer et al. 2010), may be genetically
or physiologically determined (Steinmeyer et al.
2012, Stuber et al. 2016), for example via light
and melatonin levels (Greives et al. 2015).
Other variables that may influence patterns of
activity are latitude (Amlaner & Ball 1983, Da
Silva & Kempenaers 2017), predation risk
(Amlaner & Ball 1983, Santema et al. 2019), noise
(Arroyo-Sol
ıset al. 2013; but see Da Silva et al.
2017), the lunar phase (York et al. 2018) and the
risk of territorial intrusions (Foote et al. 2011; but
see Amrhein & Erne 2006).
Here, we report on a comprehensive, 7-year
study of the start and end of activity in a population
of Blue Tits. The aim of this study is three-fold:
•To describe within-population variation in
year-round activity patterns (separately for the
non-breeding and the breeding period)
•To assess how activity patterns vary with sex
and age
•To test the effects of season (which includes
variation in day length), temperature and rain-
fall as important mediators of the timing of
activity.
We discuss the general implications of our find-
ings in relation to previous work and with respect
to the ecological and behavioural causes and con-
sequences of variation in activity. We provide the
full dataset to allow other researchers to verify our
results and to extract data as a basis for experi-
ments, own data collection or power analyses.
METHODS
Study species
Blue Tits are small (9–11 g), diurnal, hole-nesting
passerines that are non-migratory in central Europe
(Cramp & Perrins 1993). They readily accept nest-
boxes for breeding and roosting. Blue Tits are typi-
cally socially monogamous, but social polygyny
regularly occurs (Kempenaers 1994, Schlicht &
Kempenaers 2013) and extra-pair paternity is
common (e.g. Schlicht & Kempenaers 2013). Dur-
ing the breeding season, Blue Tits build nests
made of moss with a feather and hair lining. The
female lays on average 10 eggs, usually one each
morning. She then incubates the clutch alone,
while her mate often provides her with food
(Bambini et al. 2018). The eggs hatch about
2 weeks after the start of incubation and the nest-
lings are fed by both parents for about 20 days.
Blue Tits are generally single-brooded; we never
observed a second clutch in our study population,
although replacement breeding attempts after fail-
ure of the first regularly occur.
In winter, nestboxes are used for roosting, espe-
cially by males. Blue Tits often use the same
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 3
nestbox on consecutive nights but may switch to a
new roost or to a previous one after disturbance or
for no apparent reason. Towards the breeding sea-
son, males reduce their use of nestboxes for roost-
ing, whereas females start to use them more
frequently, often roosting in the future nesting
box. In the days before and during egg-laying,
females usually spend the night in the nesting box
and continue to roost there until a few days before
the young fledge (Schlicht et al. 2014). After the
breeding season, individuals rarely sleep in nest-
boxes and we have no record of a Blue Tit roost-
ing inside a nestbox during summer (between 27
June and 1 October; present authors’unpublished
data).
Study area and breeding data
We studied a Blue Tit population in a mixed-de-
ciduous oak forest (Westerholz, 48°08026″N,
10°53029″E) close to Landsberg am Lech, Ger-
many. Since 2007, the 40-ha forest patch has con-
tained 277 small-holed nestboxes. During
breeding, we visited each nestbox weekly and close
to the start of egg-laying and hatching, daily, to
determine the date of the first egg (lay date),
clutch size and hatch date. We caught Blue Tits in
winter, either inside a nestbox or in a mist-net at
feeding stations. We also caught individuals at
their nestbox during nestling provisioning. Up to
the summer of 2014, individuals were generally
caught during provisioning and only a few individ-
uals were caught in winter. Later, we set up mist-
nets almost daily during each winter and caught
most individuals soon after they arrived. As a
result, we have more data on the timing of enter-
ing and leaving the nestbox in winter from the
autumn of 2014 onwards.
After capture, we banded each individual with
a metal ring and one to three colour rings, mea-
sured tarsus and wing (3rd primary) length and
body mass, and visually determined age (yearling
or older; Cramp & Perrins 1993). A 5- to 15-lL
blood sample was taken from the brachial vein for
paternity analysis and sex determination. A PIT-
tag was inserted under the skin on the back
(2010–12: EM4102 ISO animal tag 134.2 kHz
ISO, 8.5 92.12 mm, 0.067 g; 2013–16: BIO-
MARK HPT8 animal tag 134.2 kHz FDXB,
8.4 91.4 mm, 0.03 g, Biomark, ID; 2016–17:
SMARTRAC Glass tag 134 kHz, EM4305,
1.41 98.3 mm, 0.03 g). Sex was determined by
genotyping with the marker P2P8 (Griffiths et al.
1998). For further details on the study area and
the field procedures see Schlicht et al. (2012).
Data on activity patterns
Whenever a PIT-tagged Blue Tit entered or left a
nestbox, a radiofrequency identification
(RFID) reader located around the entrance of the
box recorded the individual’s identity and the date
and time, and two light barriers, one inside and one
outside the box, recorded the direction of the bird’s
movement (for details see Lo€
es et al. 2019). All
RFID readers were active year-round. Because
sometimes individuals entering or exiting the nest-
box were not registered or the direction may have
been mis-assigned, we conservatively used data only
if an individual carrying a transponder was recorded
both when entering the box in the evening and
when leaving it the next morning, and when the
direction of both movements was certain.
In 2012 and 2013, we used morning sound
recordings from inside 33 nestboxes to test the
reliability of the RFID data (given that a bird’s
movements inside the nestbox and when it leaves
are audible). In 214 of 336 recordings, the RFID
data suggested that the bird spent the night inside
the nestbox, and this was confirmed by the sound
recordings. The remaining 122 RFID recordings
suggested that the bird spent the night outside the
nestbox, but this was confirmed in only 12 cases
(10%) by the sound recordings. This implies that
our criteria to use the RFID data are conservative
and that valid data are excluded from the analysis.
In most cases this is because the evening entry
could not unequivocally be confirmed. Erroneously
excluding data only results in a loss of data,
whereas including doubtful cases may result in
erroneous data. We therefore accepted a loss of
data quantity to ensure high data quality. We then
assessed how the timing of the start of activity dif-
fered between RFID and sound recording data in
cases where overnight roosting in the nestbox was
recorded by both (n=214). We excluded four
data points where the exact time of emergence
could not be assessed in the sound data because
females emerged after the end of the recording.
On average, estimates of exit times based on the
sound recordings were 100 s later than estimates
based on the RFID readers (n=210, range =–71
to 35 min); 90% of all estimates from both meth-
ods lay within 12 min of each other.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
4L. Schlicht &B. Kempenaers
For further analyses, we discarded two types of
data. We excluded all data from replacement
clutches and from clutches where the start of
activity was experimentally manipulated (some
clutches in 2012–13, Schlicht et al. (2014) and
some in 2017, Santema et al. (2019)). Second, we
visually inspected whether fitted models fulfilled
the assumptions of homoscedasticity and normal
distribution of residuals. Because these model
assumptions were strongly violated when using the
entire dataset, we removed outliers (2627 of
37 451 data points, 7%) using the definition of a
boxplot (Tukey 1977). This yielded a sufficient fit
of the model assumptions. Note that models that
included these outliers gave qualitatively similar
results. Overall, our dataset included 34 824 roost-
ing events (evening entry plus morning exit) of
769 individuals across 7 years (2011: n=809,
n
ind
=81; 2012: n=2491, n
ind
=159; 2013:
n=2669, n
ind
=134; 2014: n=4008, n
ind
=136;
2015: n=7594, n
ind
=206; 2016: n=8964,
n
ind
=252; 2017: n=8289, n
ind
=266). Thus, we
obtained an average of 45 data points per individ-
ual (range: 1–405), and 36% (n=282) of individ-
uals were recorded in more than one breeding
season (two seasons: 78 males, 97 females; three
seasons: 34 males, 37 females; four seasons: eight
males, 14 females; five seasons: five males, six
females; six seasons: one male, two females).
We defined ‘Start of activity’as the time in min-
utes to sunrise when an individual emerged from the
nestbox in which it roosted. Similarly, we defined
‘End of activity’as the time in minutes to sunset
when an individual entered the nestbox in the eve-
ning. Because an individual was only scored as ‘roost-
ing in the box’if it was recorded both in the evening
and the next morning, the number of recorded eve-
ning entry and morning exit times is identical.
Weather data
We obtained hourly meteorological data from a
nearby weather station (http://www.am.rlp.de, sta-
tion 61: Landsberg, 10 km from the study site).
Temperatures (°C) were measured 2 m above
ground, and rainfall was measured in mm/h. Tem-
peratures recorded during the time of this study
ranged between –15.8 and 26.1 °C. Rainfall ran-
ged between 0.0 and 8.2 mm/h (see Fig. S1 for
seasonal distribution).
Decisions about entering or leaving the roost
may depend on weather conditions around dusk
and dawn, but they may also be influenced by the
conditions during the day or night. Thus, for rain-
fall, we used both average daily values and hourly
values closest to time of nestbox exit or entry in
separate models. Because daily averages resulted in
qualitatively similar, but overall smaller effects, we
present the results using hourly rainfall data. For
temperature, we used daily averages because these
values correlated strongly with the hourly values
around dawn and dusk (r=0.91–0.98).
Statistical analyses
All statistical analyses were performed using gener-
alized additive mixed models (GAMMs) calculated
with the package ‘gamm4’(Wood & Scheipl
2017) in R 3.6.1 (R Core Team 2019). A GAMM
applies a smooth function to an explanatory vari-
able of choice (here Julian date or days to the first
egg) and uses this ‘smoothed’variable in a (gener-
alized) mixed model (package ‘lme4’, Bates et al.
2015). For smoothing we used a thin-plate regres-
sion spline (‘tp’) as a basis with the dimension
k=40 (for details on the choice of k, see
Appendix S1). Smoothing was performed either
within each sex and age class (for models on age)
or within each sex (for all other models).
We performed all analyses for two time peri-
ods: (1) the non-breeding season (1 October–31
March) and (2) the breeding season (3 weeks
before the start of egg-laying until 31 July).
Note that the two periods overlap and that their
definitions are somewhat arbitrary. We chose to
end the non-breeding period on 31 March
because during the years that are part of this
study, egg-laying started after this date. We
chose the start of the breeding season as 3 weeks
before the first egg was laid because 95% of
nests are completed within 2 weeks and we
assumed that territory establishment, pair forma-
tion and nest-site choice take at least 1 week. In
each year, non-breeding individuals (30% of all
individuals) were included only in analyses for
the non-breeding season.
We calculated models using three different
response variables: start of activity (minutes to
sunrise), end of activity (minutes to sunset) and
total time spent active (hours). First, we modelled
each of these three response variables separately
for males and females, and for the non-breeding
and the breeding period (12 models, results in Figs
1–3, where each panel presents two separate
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 5
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Nest Egg Inc. Young Post−Br.
Start of activity
−40
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10
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Date (1 = 1 January)
−40
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Date (1 = 1 January)
ONDJFM
−50 0 50
Days to first eggDays to first egg
−20 0 20 40 60
R = 0.67 R = 0.49
R = 0.46 R = 0.39
Figure 1. Seasonal changes in the start of activity (emergence from the roost) for male (blue) and female (red) Blue Tits. The left
set of panels shows data between October and 31 March (‘non-breeding’, months indicated by letters); the right set shows the data
from 21 days before the focal female's first egg (day 0) until July (‘breeding’). The approximate breeding stage is shown in between
the right set of panels (Nest building, Egg-laying, Incubation, Nestling period, Post-breeding). The upper two panels show the raw
data using modified boxplots, where the filled dots represent the medians, the white space between the whiskers represents the
interquartile range (‘boxes’), the whiskers are 1.5 times the interquartile range, and the open dots are any values outside of the whis-
ker range. The bottom panel displays the smoothed values of the start of activity as calculated by the GAMM (solid line; see Meth-
ods) and the 95% confidence intervals (dashed lines). The corresponding sample sizes are given in Figures S2 and S3. A
repeatability estimate (R) is given in each panel.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
6L. Schlicht &B. Kempenaers
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Nest Egg Inc. Young Post−Br.
End of activity
−60
−40
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0
Date (1 = 1 January)
−60
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ONDJFM
−50 0 50
Days to first egg
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Males
Females
R = 0.79 R = 0.58
R = 0.37 R = 0.29
Figure 2. Seasonal changes in the cessation of activity (roost entry) for male (blue) and female (red) Blue Tits. The left set of panels
shows data between October and 31 March (‘non-breeding’, months indicated by letters); the right set shows the data from 21 days
before the focal female's first egg (day 0) until July (‘breeding’). The approximate breeding stage is shown in between the right set of
panels (Nest building, Egg-laying, Incubation, Nestling period, Post-breeding). The upper two panels show the raw data using modi-
fied boxplots, where the filled dots represent the medians, the white space between the whiskers represents the interquartile range
(‘boxes’), the whiskers are 1.5 times the interquartile range and the open dots are any values outside of the whisker range. The bot-
tom panel displays the smoothed values of the start of activity as calculated by the GAMM (solid line; see Methods) and the 95%
confidence intervals (dashed lines). The corresponding sample sizes are given in Figures S2 and S3. A repeatability estimate (R)is
given in each panel.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 7
models). The explanatory variables in these models
are ‘smoothed’day of the year (non-breeding per-
iod) or ‘smoothed’days to the female’sfirst egg
(breeding period). Time spent active is a compos-
ite variable: it is completely defined by the daily
start and end of activity. Hence, in all further
models, we focus exclusively on the start and end
of activity. Second, we tested whether the start
and end of activity differed between males and
females, and between yearling and adult individu-
als. We ran GAMMs for the non-breeding and the
breeding period separately, with start and end of
activity as the response variable (smoothed, as
explained above, separately for each age–sex-class),
and age (yearling or adult) and sex (male or
female) and their interaction as explanatory vari-
ables (four models; results are presented in Fig. 4
and Table S1). Finally, we investigated whether
weather variables (rainfall and temperature)
explained activity patterns. We used the same
GAMMs as described above, but added either
rainfall or temperature as an explanatory variable,
including a three-way interaction with sex and age.
We did not include rainfall and temperature
together in the same model because these two
variables are strongly correlated, making the inter-
pretation of the effects in a joint model difficult.
Results of the four models are described in Figure 5
and Table S2. Interactions between age and rainfall
or temperature were not significant, except in one
model (age 9rainfall during the breeding season).
The main effects of age have already been pre-
sented in the previous analyses. We therefore also
ran the models excluding age. This yielded qualita-
tively similar results. Thus, to simplify the descrip-
tion of the results, we present the models without
age as an explanatory variable and discuss the sta-
tistically significant interaction separately.
We modelled both scaled (standardized and
centred) variables to allow assessment of the rela-
tive importance of the effect sizes (Figs 4 and 5),
and unscaled variables to allow biologically mean-
ingful interpretation in terms of units (Tables S1
and S2).
Finally, to calculate individual repeatabilities,
we fitted GAMMs similarly to those described
above. As the response variable we used the tim-
ing of either the start or the end of activity. We
calculated repeatability separately for each sex and
each period (non-breeding and breeding season).
Thus, we ran eight different models and present
the respective repeatability estimates in the panels
of Figures 1 and 2. As explanatory variables, we
included the smoothed day of year or the number
of days to the first egg (for the non-breeding and
breeding season, respectively), average daily tem-
perature and rainfall at dawn (for the start of
activity) or dusk (for the end of activity). We then
extracted the adjusted repeatabilities from the
LME-part of the GAMM by dividing the variance
8
10
12
14
16
8
10
12
14
16
Date (1 = 1 January)
Hours of activity
–100 –50 0 50
ONDJFM
Days to first egg
–20 0 20 40 60
Nest Egg Inc. Young Post−Br.
Figure 3. Seasonal changes in the total active period (time between emergence from the roost and entering the roost again) for
male (blue) and female (red) Blue Tits. The left panel shows data between October and 31 March (‘non-breeding’, months indicated
by letters); the right panel shows the data from 21 days before the focal female's first egg (day 0) until July (‘breeding’). Shown are
smoothed values as calculated by the GAMM (solid line; see Methods) and the 95% confidence intervals (dashed lines). The black
solid line shows day length (i.e. the time between sunrise and sunset). The right panel shows the data from 21 days before the focal
female's first egg (day 0) until July. The approximate breeding stage is shown above the right panel (Nest building, Egg-laying, Incu-
bation, Nestling period, Post-breeding).
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
8L. Schlicht &B. Kempenaers
explained by the random intercept ‘individual ID’
by the sum of the variance explained by ‘ID’and
the residual variance. We do not present
confidence intervals for these repeatability esti-
mates here, because these are not straightforward
to compute in a GAMM. Note that the estimate
–22 –20 –18 –16 –14
●
●
adult females
yearling females
adult males
yearling males
(a)
–15 –10 –5 0 5
(b)
–
14 –12 –10 –8 –6 –4
(c)
–36 –34 –32 –30 –28 –26
(d)
Non−breeding Breeding
Start of activity (estimate±CI)
End of activity (estimate±CI)
Figure 4. Effects of sex and age on the start and cessation of activity in Blue Tits. Shown are estimates based on a GAMM (see
Methods) and the 95% confidence intervals (CI). For this figure, age class and sex were included in the model as a four-level factor
instead of an interaction (Table S1). (a, b) Start of activity, i.e. timing of emergence from the nestbox; (c, d) cessation of activity, i.e.
timing of entering the nestbox to roost. (a, c) Winter and early breeding season (October–31 March); (b, d) breeding season (period
from 21 days before the first egg until July).
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 9
of repeatability we use here will capture
both short-term temporal autocorrelation and
individual-specific preferences.
RESULTS
Seasonal variation in activity patterns
Start of activity
Start of activity is shown in Figure 1. Overall, both
males and females usually left their roost before sun-
rise, with no distinct seasonal changes outside the
breeding season. Males on average became active
somewhat earlier as the season progressed, whereas
females emerged later. About 2 weeks before the
female laid her first egg, both pair members
emerged progressively earlier until shortly before
laying. Females then suddenly changed their beha-
viour. On the day before and on the day of laying,
they emerged approximately 10 min later than
previously. During laying and incubation, females
progressively delayed emergence until the young
hatched, when the pattern reversed and females
emerged earlier again. In contrast, males emerged
progressively later from the end of the laying period
onwards. The repeatability of the start of activity
was high (0.39–0.67) in both sexes and both outside
and during the breeding season.
End of activity
End of activity is shown in Figure 2. Overall, in
both sexes, individuals usually entered the roost
before sunset, except during mid-winter when the
days are shortest. In winter, individuals were
therefore active for a much shorter period than in
summer (Fig. 3). During the breeding season, indi-
viduals changed their timing around the start of
laying: both sexes entered the nestbox progres-
sively earlier in the evening, but the pattern was
most pronounced in females during the incubation
–0.1 0.0 0.1 0.2
Start of activity (estimate ± CI)
Rainfall
Temperature
Non−breeding female
Breeding female
Non−breeding male
Breeding male
–0.1 0.0 0.1 0.2
End of activity (estimate ± CI)
Rainfall
Temperature
(a)
(b)
Figure 5. Relationship between rainfall and temperature (relative to time of year) and timing of activity in male and female Blue Tits.
(a) Start of activity, i.e. timing of emergence from the nestbox. (b) Cessation of activity, i.e. timing of entering the nestbox to roost.
Shown are standardized (scaled) effect sizes to allow comparison between the variables. Original units are given in Table S2.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
10 L. Schlicht &B. Kempenaers
period. Individuals returned to pre-breeding times
of roost entry during the nestling period. The
repeatability of the end of activity was moderate
to high (0.29–0.79) in both sexes and both outside
and during the breeding season.
Effects of sex and age on activity patterns
Across most of the year, and particularly during the
early breeding season, males emerged significantly
earlier and entered the roost significantly later than
females (Figs 1, 2 and 4; Table S1). In the non-
breeding season, males emerged on average >5 min
earlier and entered the roost >5 min later than
females (Fig. 4a,c). During the breeding season,
males emerged >15 min earlier and went to roost
5 min later (Fig. 4b,d). The difference between
males and females was especially pronounced dur-
ing the egg-laying and incubation period.
Activity patterns are also age-dependent, but
these effects are much smaller than the effects of
sex (Fig. 4; Table S1). In winter, adult males
started and stopped activity earlier than yearlings,
whereas during breeding they started to be active
earlier and stopped activity later than yearling
males. Adult and yearling females were more simi-
lar in the timing of their behaviour, except that
during the breeding season adult females entered
their roost about 2 min later compared with year-
ling females.
Effects of rainfall and temperature on activity patterns
Overall, an additional 1 mm of rainfall delayed the
start 4–6 min and advanced the end of activity by
4 min for both sexes across all periods (Fig. 5;
Table S2). The start, but not the end, of activity
was more delayed for males than for females. At
dawn, during the breeding period, older individu-
als responded more strongly to increased rainfall
than yearlings (slope of rainfall on the start of
activity for yearlings: 0.10 0.01, interaction with
male age: 0.01 0.01, t=2.03, P=0.04; esti-
mated after removal of the non-significant three-
way interaction between rainfall, age and sex).
An increase in temperature (given the time of
year) by 1 °C was associated with an advance in
the start by 6 s and a delay in the end of activ-
ity by 41–55 s for both sexes across all periods
(Fig. 5; Table S2). The start of activity was influ-
enced similarly for males and females. However,
when temperatures were higher, females delayed
going to the roost more than males in winter and
early breeding, but not during the breeding season.
DISCUSSION
This study shows that Blue Tit activity patterns
are strongly shaped by seasonal changes in day
length and by breeding activities. During the non-
breeding season, the start of activity changes little
relative to sunrise, but the birds go to roost later
relative to sunset in mid-winter. Blue Tits had
slightly shorter active days during periods of rain-
fall and longer days when temperatures were
higher.
Seasonal patterns
Confirming previous studies (Hinde 1952, Amla-
ner & Ball 1983, Slagsvold 1996), we found that
the start of activity in the morning closely follows
sunrise and thus overall light levels (Fig. 1).
Indeed, despite extreme changes in the environ-
ment from warm and long summer days with
abundant food to cold and short winter days with
little food, individuals varied surprisingly little in
their start of activity in relation to sunrise. This
means that the period during which individuals
were active ranged from about 9 h in winter to
about 14 h in summer. However, individuals used
a higher proportion of the available daylight when
days were short by ending their activity later in
the evening (Figs 2 and 3). This suggests that they
may be constrained in winter by the time required
to find sufficient food. In line with previous find-
ings, our results suggest that the start of activity is
relatively fixed, whereas the end of activity is more
flexible (Hinde 1952, Amlaner & Ball 1983, Slags-
vold 1996, Da Silva et al. 2017). When foraging
success is unpredictable, individuals may face
strong selection to start their activity as early in
the day as possible to ensure that they have
enough time to acquire resources to survive the
coming night. In contrast, in the evening, when
some individuals have fed well but others have
not, selection may favour flexibility, with individu-
als adjusting their behaviour to their current state.
Our results clearly show sex differences in activ-
ity patterns (Figs 1–4; Table S1). Across the year,
females emerged from roost later in the morning
and entered it earlier in the evening compared
with males (see also Kluijver 1950, Hinde 1952,
Steinmeyer et al. 2010, Stuber et al. 2015). Out-
side the breeding season, sex differences cannot be
attributed to different tasks the sexes have to per-
form. Males are generally somewhat larger than
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 11
females and dominate over them (e.g. Hegner
1985, Hogstad 1989). Because subdominant indi-
viduals seem to have limited access to the pre-
ferred food sources (see Hogstad 1989 and
references therein), females may have reduced
access to food and hence may need more time for
foraging or use alternative foraging strategies. If
this is the case, females might have to use a larger
proportion of the day for foraging, but our results
do not show this. The difference in activity seems
more pronounced later in winter and during early
spring, when males start to defend territories, and
may thus be linked to sexual selection.
During the breeding season, activity patterns
show drastic changes. Towards the start of egg-lay-
ing, both males and females advanced their emer-
gence times substantially, whereas the end of
activity remained relatively constant. The former
may be related to the energetic demands the breed-
ing season makes on the individuals, as it allows
more time for foraging. Alternatively, the daily and
seasonal timing could be correlated. Many animals
possess a photosensitive period during which light
exposure triggers reproductive behaviour. In Japa-
nese Quail Coturnix japonica, this photosensitive
period occurs 10–16 h after the lights turn on (i.e.
sunrise, Nicholls et al. 1983). Graham et al. (2017)
propose that females that emerge earlier in the
morning may be sensitive to photic stimulation ear-
lier in the evening. As days grow longer, these
females would be the first to experience sunlight in
their photosensitive period. They would therefore
be early in developing reproductive behaviour and
would start to lay relatively early. The advance in
emergence time before egg-laying may therefore be
a by-product of the effect that early emergence trig-
gers egg-laying. The delay in emergence times as
well as the gradual advance of the end of activity
once egg-laying starts (Figs 1 and 2) could then sim-
ply result from the time it takes to lay the egg and
later to incubate the clutch. Why females had
already emerged substantially later one day before
they started laying remains unclear. Males generally
followed similar patterns and were overall active
longer than females. This suggests a role of sexual
selection. For example, males may benefit from
being active to defend their territory or to guard
their fertile partner. Males that started singing ear-
lier also sired more extra-pair offspring (Poesel et al.
2004, Kempenaers et al. 2010). Later during the
breeding season, differences in activity levels
between males and females seem related to sex-
specific roles (e.g. only females lay eggs and incubate
them). Interestingly, the male activity pattern par-
tially follows that of females (Figs 1–3). This is
expected during the fertile period (e.g. because of
mate guarding), but also occurs during incubation.
Despite other (extra-pair) females being available,
males generally did not continue to emerge early,
suggesting that extra-pair mating opportunities do
not strongly influence male activity patterns at that
time. It has been reported that males accompany
their mate to the roost in the evening and from it in
the morning (Hinde 1952, Poesel et al. 2004).
Although these are anecdotes, such behaviour may
be important for the social pair bond and may
explain the match between male and female timing.
Adult males (but not females) emerged on
average 2.6–2.8 min earlier than yearling males
both during the non-breeding and during the
breeding season (Fig. 4; Table S1). A previous
study investigating Blue Tit sleep in the same
study area reported that yearlings (across sexes)
emerged on average 4 min later than older indi-
viduals (Steinmeyer et al. 2010). Similarly, Poesel
et al. (2004) reported that yearling males started
to sing later than older males. In contrast to Stein-
meyer et al. (2010), we found that older males
also entered the roost later in the evening during
breeding, but it remains unknown whether this
also influences reproductive success. During the
non-breeding season, however, older males
entered the roost earlier than younger males. Sev-
eral studies reported that older males have an
advantage over younger males in terms of food
acquisition because of experience and social domi-
nance (Hogstad 1989 and references therein, Lahti
et al. 1996, Edler & Friedl 2010), but other stud-
ies did not find an age effect (Hegner 1985, Koi-
vula et al. 1993, Zanette & Ratcliffe 1994). If
older males are dominant, they may be able to
obtain resources faster in winter, whereas sub-
dominant, yearling individuals may need to stay
active for longer to feed. Interestingly, we again
found that the start of activity is less flexible than
the end of activity. The age-related differences in
males are unlikely to be driven by testosterone
levels because these are age-independent in male
Blue Tits (Peters et al. 2006). Melatonin levels
appear to decrease with increasing age in birds,
but only later in life (senescence; Tarlow et al.
2003 and references therein). It seems unlikely
that our classification of ‘yearlings’and ‘older’
individuals captures this process.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
12 L. Schlicht &B. Kempenaers
Effects of rainfall and temperature on
activity patterns
As in previous studies (e.g. Kluijver 1950, Hinde
1952, Bruni et al. 2014, Da Silva et al. 2016), we
found that rainfall caused Blue Tits to leave their
roost later in the morning, and enter it earlier in
the evening, independent of time of year (Fig. 5,
Figs S8 and S9). Rainfall implies cloud cover and
lower light levels, which in turn may affect activ-
ity. However, a previous study of Blue Tits in the
same study area found no relationship between
local light levels and activity patterns (Steinmeyer
et al. 2010). Thus, the effect of rain on activity
may also be related to the reduced benefits of
being active, for example because of reduced for-
aging efficiency or because the noise associated
with rain impedes acoustic communication. Dur-
ing the breeding season, older individuals delayed
their emergence times more compared with year-
lings during periods of rain. Older individuals gen-
erally emerged earlier than yearlings during the
breeding season (Table S1) and may have a greater
potential to delay their emergence.
In accordance with Bruni et al. (2014, but see
Hinde 1952, Da Silva et al. 2016) we found that
higher temperatures –given the time of the year –
were linked to earlier morning emergence and later
evening entry in both sexes (Fig. 5; Table S2); that
is, on a relatively warm day, individuals were
active longer than on a cold day. Higher tempera-
tures may increase foraging success and reduce the
need for individuals to save energy. We investi-
gated how the relationship between temperature
and activity changes across the year based on
monthly estimates (Figs S6 and S7). The relation-
ship between temperature and the start and the
end of activity was weak or absent in the winter
months, especially around the time when days are
shortest (November–January; winter solstice: 21
December). Effect sizes increased towards the
breeding season. In winter, individuals may be less
flexible and responsive to variation in temperature
because they may need all available time during
the short days.
CONCLUSIONS
The timing of the start and end of activity is likely
to be shaped by two mechanisms: (1) a ‘fixed’
genetic predisposition, modulated for example by
hormonal changes in response to increased
daylength (Graham et al. 2017) or hormonal dif-
ferences between the sexes (Dawson et al. 2001,
see also Yu et al. 2018), and (2) a ‘flexible’trade-
off between costs and benefits of being inside or
outside the roost (reviewed by Mainwaring 2011).
Benefits of being inside the roost may be avoid-
ance of avian predators (e.g. Eurasian Spar-
rowhawks Accipiter nisus), energy conservation,
sleep and essential behaviour related to breeding
such as egg-laying, incubation and nest mainte-
nance. Benefits of being outside the roost are the
ability to feed, to avoid parasites and predators
that enter cavities (e.g. mustelids or snakes), and
to engage in breeding behaviours such as territory
establishment and defence, mate acquisition, mate
guarding and (extra-pair) copulation.
The close match of the start and end of activity
to sunrise and sunset, respectively, shows that
overall patterns are primarily determined by light
levels, presumably through the light-regulated hor-
mone melatonin (e.g. El Halawani et al. 2009,
Greives et al. 2015). Our results show that indi-
viduals can fine-tune their behaviour in response
to environmental factors (rain and temperature)
and in relation to breeding activities.
Blue Tits show the greatest flexibility in emer-
gence times during the breeding season: both sexes
advance their start of activity before laying and
delay it afterwards. The advance in the start of
activity before laying may be related to nest-build-
ing and acquiring resources for egg production (for
females) and to mate-guarding and advertising for
extra-pair copulations (for males). The delay in
emergence times during laying and afterwards
seems to be driven mostly by the constraints of
egg-laying and incubation.
In winter, when survival during short and cold
days is key, individuals need to budget their energy
income and expenditure. In small songbirds,
energy reserves are limited. For example, in Eura-
sian Tree Sparrows Passer montanus, energy
reserves are sufficient for at most 24 h (Pinowski
et al. 2006). In winter it may therefore be key to
be active for as long as possible. Indeed, Blue Tits
went to their roost later in the evening in winter
(in relation to sunset) and were thereby active for
a longer proportion of the total day (period when
light was available). Also, individuals adjusted the
timing of their activity to temperatures only out-
side of the winter months (Figs S6 and S7). Poten-
tially, the flexibility in the timing of activity in
winter is limited.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 13
In winter, when the need to save energy is high,
an alternative strategy to adjusting activity patterns
could be to use nestboxes more frequently (re-
viewed by Mainwaring 2011). Indeed, Vel’ky
(2006) reports that Great Tits roosted most fre-
quently in nestboxes when temperatures were
lowest. Our data do not support this, as sample
sizes (equivalent to occupancy rates) are –if any-
thing –lower in mid-winter (Fig. S1).
Although we present population-wide patterns,
individuals may vary substantially in their activity
patterns on a day-to-day basis (examples in Figs S4
and S5). Despite this variation, we found high or
moderately high repeatabilities in both the start and
the end of activity for both males and females, and
both outside and during the breeding season (all
repeatability estimates between 0.29 and 0.79, Figs
1 and 2). However, it is likely that much of this
repeatability can be explained by temporal autocor-
relation in data recorded within a relatively short
period (e.g. within a few days or weeks). It remains
unclear how much can be attributed to the individ-
ual per se, in other words its ‘chronotype’. Note that
this is also the case for repeatability estimates
reported previously (Steinmeyer et al. 2010, Domi-
noni et al. 2013, Schlicht et al. 2014, Stuber et al.
2015). A more refined analysis controlling for tem-
poral autocorrelation is beyond the scope of this
paper. Some individuals emerged unusually late,
more than 1 h after sunrise. Although we cannot
exclude that some of these cases are RFID data
errors, we confirmed four of these cases during early
breeding by sound recordings inside the nestbox.
This also confirms anecdotes described by Kluijver
(1950), who studied breeding Great Tits and men-
tioned ‘two inexplicable cases in which she (the
Great Tit female) became active very late’.Why
some individuals sometimes leave their nestbox so
late remains unexplained but might be associated
with the presence of a predator nearby (Santema
et al. 2019).
We could only assess activity patterns of a sub-
set of all Blue Tits present in the population,
namely those that roost in a nestbox. Decisions to
roost in a box may depend on the local availability
of natural cavities or other roosting sites, weather
conditions, and the presence of parasites and
predators (Vel’ky et al. 2010, Mainwaring 2011).
All nestboxes in our study area are cleaned once a
year after the young have fledged, which presum-
ably reduces parasite infestation. Thus, as with
other studies using nestboxes, results may differ
for populations without nestboxes or where nests
are not removed.
This study presents detailed information about
the start and end of daily activity in Blue Tits. We
show clear seasonal patterns, with drastic beha-
vioural changes towards the breeding season. We
also show that rain consistently shortens the over-
all time spent active, but the effects of variation in
temperature are less clear. The general patterns
described here can be used as the foundation for
other (experimental) studies of activity patterns in
Blue Tits and similar species. Our results lead to
several questions that need to be addressed at the
between- and within-individual level. For example,
how far does the start and end of activity in males
during the breeding season track that of their
mate? Do individuals change their activity patterns
through life (e.g. from yearling to adult)? We also
need to understand the fitness consequences of
individual variation in activity patterns. For exam-
ple, do females that emerge earlier in the early
breeding season or that are active for longer (rela-
tive to day length) also lay eggs earlier (Graham
et al. 2017)? Does variation in the timing of emer-
gence or in overall male activity affect reproduc-
tive success? Which components of reproductive
success are affected (e.g. paternity gain or loss)?
Finally, we do not yet understand why most
females seem to emerge earliest 2 days before they
lay their first egg.
We thank all members of the Blue Tit group and two
anonymous reviewers for constructive feedback. We are
especially grateful to everyone who collected data in the
field, in particular Agnes T€
urk, Andrea Wittenzellner
and Carol Gilsenan, to Peter Lo€
es and Peter Skripsky for
designing and maintaining the automated nestbox sys-
tem, and to Mihai Valcu for establishing and maintain-
ing the database.
DATA AVAILABILITY STATEMENT
All code and data (.RData and.csv) are supplied in
the R package ‘BTemergence’(Schlicht 2019).
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Received 16 August 2019;
revision accepted 15 January 2020.
Associate Editor: Stuart Sharp
SUPPORTING INFORMATION
Additional supporting information may be found
online in the Supporting Information section at
the end of the article.
Appendix S1. The choice of K in the GAMMs.
Figure S1. (A) Temperature and (B) rainfall at
dawn and (C) at dusk across the year.
Figure S2. Sample sizes in relation to date.
Figure S3. Sample sizes in relation to progress
of the breeding season.
Figure S4. Examples of the start of activity of a
yearling and adult male and female Blue Tit.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
16 L. Schlicht &B. Kempenaers
Figure S5. Examples of the cessation of activity
of a yearling and adult male and female Blue Tit.
Figure S6. Estimates of the effect of average
daily temperature on the start of activity.
Figure S7. Estimates of the effect of average
daily temperature on the cessation of activity.
Figure S8. Estimates of the effect of average
rainfall at dawn on the start of activity.
Figure S9. Estimates of the effect of average
rainfall at dusk on the cessation of activity.
Table S1. Start and cessation of activity for
male and female and for yearling and adult Blue
Tits.
Table S2. Effects of rainfall and temperature on
the start and the cessation of activity.
© 2020 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists' Union.
Timing of activity in Blue Tits 17