Pied Flycatchers Ficedula hypoleuca travelling from Africa to breed in Europe: differential effects of winter and migration conditions on breeding date

Abstract

2006. Pied Flycatchers Ficedula hypoleuca travelling from Africa to breed in Europe: differential effects of winter and migration condi-tions on breeding date. Ardea 94(3): 511–525. In most bird species there is only a short time window available for opti-mal breeding due to variation in ecological conditions in a seasonal environment. Long-distance migrants must travel before they start breeding, and conditions at the wintering grounds and during migration may affect travelling speed and hence arrival and breeding dates. These effects are to a large extent determined by climate variables such as rainfall and temperature, and need to be identified to predict how well species can adapt to climate change. In this paper we analyse effects of vegetation growth on the wintering grounds and sites en route on the annual timing of breeding of 17 populations of Pied Flycatchers Ficedula hypoleuca studied between 1982–2000. Timing of breeding was largely correlated with local spring temperatures, supplemented by striking effects of African vegetation and NAO. Populations differed in the effects of vegetation growth on the wintering grounds, and on their northern African staging grounds, as well as ecological conditions in Europe as measured by the winter NAO. In general, early breeding populations (low altitude, western European populations) bred earlier in years with more vegetation in the Northern Sahel zone, as well as in Northern Africa. In contrast, late breeding populations (high altitude and north-ern and eastern populations) advanced their breeding dates when cir-cumstances in Europe were more advanced (high NAO). Thus, timing of breeding in most Pied Flycatcher populations not only depends upon local circumstances, but also on conditions encountered during travel-ling, and these effects differ across populations dependent on the timing of travelling and breeding.

Full text

Pied Flycatchers Ficedula hypoleuca travelling from Africa
to breed in Europe: differential effects of winter and
migration conditions on breeding date
Both C., Sanz J.J., Artemyev A.A., Blaauw B., Cowie R.J., Dekhuijzen
A.J., Enemar A., Järvinen A., Nyholm N.E.I., Potti J., Ravussin P.-A.,
Silverin B., Slater F.M., Sokolov L.V., Visser M.E., Winkel W., Wright J. &
Zang H. 2006. Pied Flycatchers Ficedula hypoleuca travelling from Africa
to breed in Europe: differential effects of winter and migration condi-
tions on breeding date. Ardea 94(3): 511–525.
In most bird species there is only a short time window available for opti-
mal breeding due to variation in ecological conditions in a seasonal
environment. Long-distance migrants must travel before they start
breeding, and conditions at the wintering grounds and during migration
may affect travelling speed and hence arrival and breeding dates. These
effects are to a large extent determined by climate variables such as
rainfall and temperature, and need to be identified to predict how well
species can adapt to climate change. In this paper we analyse effects of
vegetation growth on the wintering grounds and sites en route on the
annual timing of breeding of 17 populations of Pied Flycatchers Ficedula
hypoleuca studied between 1982–2000. Timing of breeding was largely
correlated with local spring temperatures, supplemented by striking
effects of African vegetation and NAO. Populations differed in the effects
of vegetation growth on the wintering grounds, and on their northern
African staging grounds, as well as ecological conditions in Europe as
measured by the winter NAO. In general, early breeding populations
(low altitude, western European populations) bred earlier in years with
more vegetation in the Northern Sahel zone, as well as in Northern
Africa. In contrast, late breeding populations (high altitude and north-
ern and eastern populations) advanced their breeding dates when cir-
cumstances in Europe were more advanced (high NAO). Thus, timing of
breeding in most Pied Flycatcher populations not only depends upon
local circumstances, but also on conditions encountered during travel-
ling, and these effects differ across populations dependent on the timing
of travelling and breeding.
Key words: Ficedula hypoleuca, laying date, migration, climate
1
Netherlands Institute of Ecology, P.O. Box 40, 6666 ZG Heteren, The
Netherlands and Dept. of Animal Ecology, Centre for Ecological and Evo-
lutionary Studies, University of Groningen, P.O. Box 14, 9750 AA Haren,
The Netherlands;
Christiaan Both1,*, Juan José Sanz2, Aleksandr V. Artemyev3, Bert Blaauw4,
Richard J. Cowie5, Aarnoud J. Dekhuizen6, Anders Enemar7, Antero Järvinen8,
N. Erik I. Nyholm9, Jaime Potti10, Pierre-Alain Ravussin11, Bengt Silverin7, Fred
M. Slater12, Leonid V. Sokolov13, Marcel E. Visser14, Wolfgang Winkel15,
Jonathan Wright16 & Herwig Zang17

INTRODUCTION
Long-distance migrant birds may be particularly
vulnerable to climate change, because prior to
departure from their wintering grounds they may
lack information regarding circumstances at their
breeding grounds and hence the optimal time for
breeding. They may therefore have limited ability
to adjust to changes in the timing of optimal
breeding conditions (Both & Visser 2001, Coppack
& Both 2002, Strode 2003, Both et al. 2006). Such
species have typically evolved mechanisms to time
their migration according to cues related to calen-
dar date (Gwinner 1996, Gwinner & Helm 2003),
allowing them to arrive on average at the right
time on their breeding grounds. However such
cues are unaltered by climate change (unlike food
phenology on the breeding grounds), so that birds
can arrive too late on their breeding grounds. This
is especially so if they breed in habitats charac-
terised by a short and abundant food supply when
the response of the birds to such cues becomes
ultimately maladaptive. The primary example of
such a maladaptive response comes from a study
on Pied Flycatchers Ficedula hypoleuca, where
despite an advance of laying dates, selection for
early laying has continued to strengthen, but the
spring arrival dates of birds have not advanced
(Both & Visser 2001, Hüppop & Winkel 2006).
These flycatchers have advanced laying dates by
reducing the interval between arrival and the start
of egg-laying, but the extent of this adjustment is
ultimately constrained by the date of arrival.
Contrary to the argument that long-distance
migrants are absolutely constrained in their arrival
time to adjust to climate change, several European
species show clear advances in spring arrival in
recent decades (Hüppop & Hüppop 2003, Cotton
2003, Sokolov & Kosarev 2003, Sokolov L.V. 2000,
Huin & Sparks 1998, Huin & Sparks 2000,
Lehikoinen et al. 2004, Sparks 1999, Jonzen et al.
2006) and North America (Marra et al. 2005,
Butler 2003, Bradley et al. 1999). Spring arrival of
long-distance migrants appears more flexible than
expected, showing correlation with factors during
migration (Huin & Sparks 1998, Huin & Sparks
2000, Hüppop & Hüppop 2003, Sokolov 2000,
Marra et al. 2005, Hüppop & Winkel 2006, Both et
al. 2005) or on the wintering grounds (Saino et al.
2004, Cotton 2003, Sokolov & Kosarev 2003),
512
ARDEA 94(3), 2006
2
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias
Naturales (CSIC), José Gutiérrez Abascal 2, 28006 Madrid ;
3
Institute of Biology, Karelian Research Centre, Russ. Acad. Sci.,
Pushkinskaya str. 11, 185610 Petrozavodsk, Russia;
4
Prins Clauslaan 68,
7957 EB De Wijk, The Netherlands;
5
Cardiff School of Biosciences,
Llysdinam Field Centre, Newbridge-on-Wye, Llandrindod Wells, Powys
LD1 6ND Wales, UK;
6
Kuypersweg 3, 6871 EC Renkum, The Netherlands;
7
University of Gothenburg, Box 463, SE 405 30 Gothenburg, Sweden;
8
Kilpisjärvi Biological Station, P.O. Box 17, FIN-University of Helsinki,
Finland;
9
Dept. Ecology and Environmental Science, Umeå University,
S-901 87 Sweden;
10
Estación Biológica de Doñana - CSIC, Pabellón del
Perú, Av. Mª Luisa s/n, 41013 Sevilla, Spain;
11
Rue du Theu, CH-1446
Baulmes, Switserland;
12
Cardiff School of Biosciences, Cardiff University,
Cardiff CF10 1XL, Wales, UK;
13
Biological station Rybachy, Zoological
Instutute of Russ. Acad. Sci., Rybachy 238535, Kaliningrad Region,
Russia;
14
Netherlands Institute of Ecology, P.O. Box 40, 6666 ZG Heteren,
The Netherlands;
15
Institute of Avian Research ‘Vogelwarte Helgoland’,
Working Group Population Ecology, Bauernstr. 14, D-38162 Cremlingen,
Germany;
16
Institute of Biology, Norwegian University for Science and
Technology (NTNU), N-7491 Trondheim, Norway;
17
Oberer Triftweg
31A, D-38640 Goslar, Germany;
*corresponding author (c.both@rug.nl)

opening up the possibility that birds can adjust
timing of migration to climate change. In addition,
for Pied Flycatchers there is now evidence that
spring arrival has advanced at some sites (Hüppop
& Hüppop 2003, Sokolov 2000) but not in others
(Hüppop & Winkel 2006), and that it is correlated
with environmental circumstances during migra-
tion (Hüppop & Hüppop 2003, Ahola et al. 2004,
Both et al. 2005). The observed correlation be-
tween arrival and environmental circumstances
encountered en route has been used to challenge
the idea that inflexible migration schedules con-
strain any adaptive adjustment to climate change
(Marra et al. 2005, Jonzen et al. 2006). It is this
notion that we want to address in this paper.
If spring arrival constrains breeding date, we
might expect individual breeding dates to correlate
with arrival dates as found in Pied Flycatchers
(Alatalo et al. 1984, Potti & Montalvo 1991) and
other species (Smith & Moore 2005, Bensch &
Hasselquist 1992, Cristol 1995). More indirectly,
we also expect a correlation between environmen-
tal circumstances en route and breeding date, be-
cause these circumstances probably affect speed of
migration and hence arrival date, which in turn
determines breeding date (Both et al. 2005,
Hüppop & Winkel 2006). It may be that environ-
mental circumstances at the wintering grounds
also have an effect, because these may allow birds
to initiate their migration earlier. The effects on
breeding dates of environmental conditions at the
wintering grounds and during migration may thus
be key to understanding how severely long-dis-
tance migrants are constrained by their migration
in adjusting to climate change.
In this paper, we address the following ques-
tions: (1) Are environmental circumstances at the
wintering grounds or during migration correlated
with the advance of spring at the breeding areas,
and are birds on the wintering grounds therefore
able to predict when they should arrive at the
breeding grounds? (2) Are there effects of environ-
mental circumstances at the wintering grounds, or
during migration, on the timing of laying in differ-
ent populations of Pied Flycatchers across Europe?
For these purposes we used data on annual laying
dates from 17 long-term populations of Pied
Flycatchers for which some have advanced as a
result of climate change, while others have not
(Both et al. 2004). The extent of advance was cor-
related with the extent of spring warming at each
locality, and here we investigate whether on top of
these local temperature effects, laying dates were
correlated with environmental circumstances dur-
ing wintering and migration.
METHODS
We used 17 long-term population studies of nest
box breeding Pied Flycatchers in the period
1982–2000 when vegetation indices (NDVI, see
below) were available (Both et al. 2004). Popu-
lations with less than 16 years of data were
excluded, as were Collared Flycatcher Ficedula
albicollis populations because of their different
winter distribution. At study sites nest boxes were
checked weekly in most instances, and the laying
date of each nest was calculated assuming that
one egg was laid every day. Where laying date
could not be determined this way, but hatch date
was known, we assumed 13 days for incubation
(beginning on the last egg) and that one egg was
laid per day. For each year and study site combina-
tion, we calculated the median laying date. Only
first broods were included, which excluded broods
of females that were previously known to have
started a brood in that year, as well as broods that
were started later than 30 days after the very first
brood in that year for each study site. The first
year of nest box provisioning at each study site
was excluded from the analyses, because newly
established populations contain a high proportion
of young birds that tend to lay later in the season
(Lundberg & Alatalo 1992).
Study sites covered most of the species’ breed-
ing range, from Spain in the south to Northern
Finland in the north, and from Wales in the west
to Moscow in the east. Study sites were not spread
evenly over Europe because we used existing
datasets collected for other purposes. Daily mean
temperatures were obtained from meteorological
Both et al.: PIED FLYCATCHERS BREEDING DATE
513

stations close to the study sites. Populations at dif-
ferent latitudes commencing breeding on different
dates, and are therefore expected to respond to
temperatures at different times in the year. To
assign a time window to calculate site specific
temperatures we calculated the mean of the
annual median laying dates of the first five years
for each study area (1982–1986 for all areas
except La Hiruela, which was 1985–1989). Mean
daily temperatures from the 30 day period before
this date were taken as the local temperature
effect (see Both et al. 2004 for rationale). Average
laying date for each population was calculated for
1985–1989. This restricted period was used
because laying date advanced strongly in some
populations in response to local increases in spring
temperature since 1980, while others did not
(Both et al. 2004).
Environmental variables
Timing of migration and consequently timing of
breeding may be affected by conditions the birds
encounter on the wintering grounds and during
migration. Pied Flycatchers winter in west-Africa,
mainly in the Sahel area (Lundberg & Alatalo
1992), and have to cross the Sahara en route to
the European breeding areas. For some areas in
Africa (Fig. 1), the Normalized Difference Vege-
tation Index (NDVI) based on satellite images was
calculated. This index is calculated as the normal-
ized difference in reflectance between red
(0.55–0.68 µm) and infrared (0.73–1.1 µm) chan-
nels of the Advanced Very High Resolution
Radiometer (AVHRR) sensor of National Oceanic
and Atmospheric Administration (NOAA) satellites
and processed by the National Aeronautics and
Space Administration (NASA, Prince & Justice
1991a). NDVI provides a measure of the amount
and vigour of vegetation at the land surface
related to the level of photosynthetic activity
(Prince & Justice 1991b, Myneni et al. 1997). This
index is strongly correlated with the fraction of
photosynthetically active radiation absorbed by
vegetation, which depends on local rainfall condi-
tions (Asrar et al. 1984, Myneni et al. 1995). Since
Pied Flycatchers are insectivorous and the insect
abundance in turn depends on plant productivity,
the NDVI is likely to reflect the relative seasonal
abundance of insect supplies in the wintering
areas (Szép & Møller 2005, Wolda 1988, Dean &
Milton 2001). NDVI data corrected for surface
topography, land-cover type, presence of clouds
and solar zenith angle were provided by Clark
Labs in IDRISI format as world monthly images at
spatial resolutions of 0.1 degree from a 0 to 255
scale values between August 1981 and December
2000 (excepting September-December 1994).
Using a Geographic Information System (Clark
Labs 2001), we obtained mean NDVI values for
those selected areas in Africa (see Fig. 1) from
December to April.
A second environmental variable analysed was
the North Atlantic Oscillation (NAO). NAO is a
natural large scale atmospheric fluctuation
514
ARDEA 94(3), 2006
1
4
2
3
5-7
9
810
11
1213
14
17
16
15
wintering area
N. SAHEL
S. SAHEL
N. AFRICA
Figure 1. Map indicating areas used for NDVI data
extraction and sites of population studies of Pied
Flycatchers in Europe.

between the subtropical (centred on the Azores)
and the subpolar (centred on Iceland) North
Atlantic region (Lamb & Peppler 1987). This phe-
nomenon is particularly important in winter, when
it exerts a strong control on the climate of Europe
and when it exhibits the strongest interdecadal
variability (Hurrell 1995). The NAO-index is quan-
tified from December to March as the difference of
normalized sea level surface pressures between
Lisbon, Portugal and Stykkisholmur/ Reykjavik,
Iceland from 1864 through 1998 (Hurrell &
VanLoon 1997). This winter NAO-index is cur-
rently updated at the website: http://
www.cgd.ucar.edu/~jhurrell/nao.html. The winter
NAO-index can be either positive or negative, and
major climate variations occur when it remains for
long periods in one mode or in the other (Hurrell
1995). A positive NAO-index results from intensi-
fying high pressure over the subtropical Atlantic
and deepening low pressure over the subpolar
Atlantic, and is associated with stronger, more
southerly tracking of westerly winds and higher
temperatures in western Europe. A negative NAO
occurs when the subtropical Atlantic high pressure
is weak and the subpolar Atlantic low pressure
moves south, associated with cold drier winter in
northern Europe and wetter winters in southern
Europe.
RESULTS
Temporal trends in environmental variables
Temporal trends in local temperatures in the dif-
ferent breeding areas have been described before,
and these differ geographically, with strong
increases in western and central Europe and only
mild or no increases in southern, northern and
eastern Europe (see Both et al. 2004 for details).
Among the NDVI data from Africa we found an
increase over the years in the northern Sahel zone
(r=0.60, n=19, P=0.007, Fig. 2), and no sig-
Both et al.: PIED FLYCATCHERS BREEDING DATE
515
D
B
A
135
137
139
141
NDVI northern Africa
1980
C
1985 1990 1995 2000
0
1
2
3
4
5
North Atlantic oscilation
1980 1985 1990 1995 2000
160
NDVI southern Sahel
146
NDVI northern Sahel
148
150
152
154
165
170
175
180
185
Figure 2. Annual values of NDVI in the different areas in Africa as used in the analysis and winter NAO (Dec–Mar).

516
ARDEA 94(3), 2006
Correlation between local temp Maximal possible effect sizes
LD and on laying date of
1985– Local S Sah N Sah N Afr
No. Area Latitude Longitude First Last 1989 S Sah N Sah N Afr NAO temp NDVI NDVI NDVI NAO
1La Hiruela 41°04'N 03°27'W 1985 2000 23 May –0.36 0.09 0.11 0.42 –8.37 –6.42 5.15 2.91 –4.52
2Llanwrthwl, Powys 52°13'N 03°27’W 1982 2000 13 May –0.13 0.16 –0.11 0.24 –4.70 –8.16 3.19 0.44 –9.25
3Abergwyngregyn 53°13'N 04°00’W 1982 2000 12 May –0.28 0.02 0.04 0.18 –3.55 8.57 –9.74 –1.57 –1.10
4Baulmes 46°47'N 06°31'E 1982 2000 18 May –0.25 0.06 –0.04 0.15 –8.94 9.19 –8.89 6.04 0.38
5Hoge Veluwe 52°02'N 05°51’E 1982 2000 13 May –0.21 0.06 –0.18 0.17 –7.91 13.23 –9.30 –1.72 5.34
6Warnsborn 52°00'N 05°51’E 1982 2000 13 May –0.12 0.14 –0.15 0.23 –6.65 9.23 –7.01 –4.75 2.45
7Deelerwoud 52°05'N 05°55’E 1982 2000 12 May –0.12 0.14 –0.15 0.23 –6.65 12.02 –6.75 –0.01 3.40
8Staphorst 52°37'N 06°17’E 1982 2000 11 May –0.13 0.12 –0.18 0.20 –6.65 11.87 –7.43 –2.58 7.10
9Lingen/Emsland 52°27'N 07°15'E 1982 2000 14 May –0.32 –0.04 –0.24 0.21 –9.74 8.44 –6.91 –2.89 7.50
10 Harz 51°53'N 10°37'E 1982 2000 16 May –0.33 0.02 –0.27 0.26 –11.69 –2.17 1.65 –0.14 –4.46
11 Gunnebo 57°40'N 12°05'E 1982 1998 25 May –0.51 –0.43 0.03 0.35 –6.88 16.11 –11.26 8.17 –1.85
12 Goteborg 57°43'N 11°58'E 1982 2000 26 May –0.29 –0.05 0.00 0.38 –6.42 –3.18 0.81 –1.17 –4.81
13 Borlange 60°23'N 15°30'E 1982 1999 27 May –0.40 –0.30 0.15 0.49 –6.53 15.22 –9.67 8.66 1.91
14 Ammarnäs 65°58'N 16°13'E 1982 2000 8 Jun –0.59 –0.49 –0.17 0.32 –6.65 6.01 1.39 7.53 –1.73
15 Kilpisjärvi 69°03'N 20°50'E 1982 2000 10 Jun –0.46 –0.44 –0.21 0.24 –6.76 –1.11 8.72 5.09 –7.72
16 Rybachy 55°05'N 20°44'E 1982 2000 28 May –0.48 –0.57 –0.34 0.04 –4.13 10.51 –5.83 2.74 –4.10
17 Karelia 60°46'N 32°48'E 1982 2000 30 May –0.31 –0.30 0.07 0.24 –7.11 1.36 2.20 3.80 –8.27
Table 1. Details of the population studies of Pied Flycatchers, the correlation between local spring temperature and NDVI index in different parts of Africa
and NAO, and the possible maximal effect sizes of the different environmental variables on laying date (LD) for these populations. Significant correlations
are in bold. Population identifiers in first column refer to Fig. 1.

nificant changes in the southern Sahel zone (r=
0.37, n=19, P=0.110), nor in northern Africa
(r=0.28, n=19, P=0.250). However, these
temporal trends were not significantly different
across areas, and the non-significant effects are to
a large extent determined by the extreme last year
(see Fig. 2). Excluding this year yields significant
correlations between NDVI and year for all three
areas (northern Sahel r=0.61, P< 0.001, south-
ern Sahel: r=0.50, P=0.040, northern Africa:
P=0.68, P=0.002, n=18). NAO was not corre-
lated with year for this period of time (r=–0.022,
n=19, P=0.99).
Correlations between environmental variables
Across areas there was a strong correlation
between NDVI in the southern and northern Sahel
(r=0.78, n=19, P<0.001), but not between
the Sahel and northern Africa nor with NAO (all
r< 0.21, all P>0.390). It therefore seems that
the vegetation experienced by the flycatchers
south of the Sahara does not provide them with
information regarding what they can expect later
in their journey in northern Africa or in Europe in
general (as exemplified by NAO).
If correlations exist between environmental
conditions at the wintering grounds and in the
local breeding area, birds may have evolved to use
such cues to start spring migration. Therefore, we
examined correlations between vegetation in
Africa and NAO and the spring temperatures at the
17 breeding localities (Table 1). Only in a few
cases were significant correlations found between
NDVI in the Sahel zone or NAO and spring tem-
peratures in Europe, and these few correlations
could be due to chance effects. However, we
examined whether there were any patterns in the
correlation coefficients between European spring
temperatures and African NDVI across breeding
localities, and we found that areas which have a
late laying date showed a stronger correlation
between NDVI in the Sahel and local spring tem-
perature. We found no such correlation in areas
with an early laying date. In the late laying areas,
more vegetation in the Sahel coincided with low
temperatures in the breeding areas (Fig. 3).
Flycatchers from more northern and eastern popu-
lations may thus use the lack of rainfall related
vegetation on the wintering grounds to advance
their migration, because in those years it is more
likely that spring starts earlier.
Breeding date and environmental conditions
The annual median laying date advanced clearly
with rising local temperatures, and did not differ
across populations (Table 2). Additionally, laying
Both et al.: PIED FLYCATCHERS BREEDING DATE
517
B
10
2
4
6
8
spring temperature (°C)
160
NDVI southern Sahel
A
12
14
16
165 170 175 180 185
–0.2
–0.6
–0.5
–0.4
–0.3
cor. local temp. – NDVI southern Sahel
40
laying date (1985–1989) since March 30 (days)
–0.1
0.0
45 50 55 60 65 70
Hoge Veluwe
Ammarnäs
Figure 3. Correlations between vegetation in the sou-
thern Sahel and local spring temperatures at different
breeding localities in Europe. (A) Two examples of areas
of how these variables are correlated. (B) Per area the
correlation coefficient and its relation to the average lay-
ing date in each area (correlation: r= 0.82, n= 17, P<
0.001).

date advanced by three days, and again this was
not different across populations. In contrast, the
effects of NDVI in both the southern and northern
Sahel, and northern Africa, as well as NAO, dif-
fered significantly between populations (Table 2).
Some examples of the effects of all four environ-
mental factors are given in Fig. 4, showing differ-
ent relationships between laying dates of Pied
Flycatchers in different populations and NDVI in
different parts of Africa and NAO.
The different effects of environmental circum-
stances at the wintering grounds or during migra-
tion are not random, but depend on the average
laying date of each population (Fig. 5). MANOVA
on the slopes of southern Sahel NDVI, northern
Sahel NDVI, northern African NDVI and NAO
against breeding date (see model in Table 2)
showed a significant effect of average laying date
(Wilks’ lambda = 0.173, P<0.001). More specifi-
cally, in populations with an early laying date,
more vegetation in both the northern Sahel and
northern Africa was associated with an advance in
laying date (simultaneously taking local tempera-
ture into account, Fig. 5B,C), whereas in late breed-
ing populations the vegetation in northern Africa
was associated with a delayed effect on laying date
(Fig. 5C). The opposite was the case for the associ-
ations with NAO: in years with a relatively mild
and wet winter (high values of NAO) the flycatch-
ers delayed laying in areas with a early laying date,
whereas in areas with an late laying date these con-
ditions advanced the laying date (Fig. 5D). The
effects of northern African NDVI and NAO were on
average smaller for these early breeding popula-
tions, and stronger for late breeding populations.
What do these different environmental effects
mean quantitatively for laying date in different
areas? For this purpose, we calculated the magni-
tude of the effects for all variables using the study
area specific slopes for the different environmental
effects from the model in Table 2. Next we calcu-
lated how laying date changed from the minimal
518
ARDEA 94(3), 2006
Dependent variable df F P Slope (SE)
Intercept 1,225 23.72 < 0.0005
Breeding area 16,225 3.10 n.a.
Local temperature 1,225 95.08 < 0.0005 –1.180 (0.120)
Year 1,225 14.35 < 0.0005 –0.156 (0.043)
NDVI southern Sahel 1,225 21.38 n.a.
NDVI southern Sahel 1,225 9.42 n.a.
NDVI northern Africa 1,225 6.18 n.a.
NAO 1,225 1.59 n.a.
Breeding area xNDVI southern Sahel 16,225 2.27 0.004
Breeding area xNDVI northern Sahel 16,225 2.68 0.001
Breeding area xNDVI northern Africa 16,225 2.19 0.006
Breeding Area xNAO 16,225 2.30 0.004
Non-significant terms
Breeding area xLocal temperature 16,209 1.13 0.33
Breeding area xYear 16,193 1.57 0.08
Table 2. Results of ANCOVA on annual median breeding date of 17 populations of Pied Flycatchers in relation to local
temperatures and environmental conditions on the wintering grounds and during migration. Slopes are given for main
effects.

to maximal value for each environmental factor
(Table 1, assuming that all of these were indepen-
dent). The maximal magnitudes of each environ-
mental factor on laying date depended thus on the
variation in the factor, as well as on the study area
specific slope of the factor on laying date. Because
areas did not differ in the effect of local spring
temperature, it is not surprising that increases in
spring temperature always advanced laying date.
The effects of vegetation in the two Sahel areas
were more complicated, because annual NDVI val-
ues are highly correlated across the southern and
northern Sahel, and so for each population the
effect of northern Sahel NDVI tends to be opposite
Both et al.: PIED FLYCATCHERS BREEDING DATE
519
–8
–4
0
4
8
res laying date
160
NDVI southern Sahel
170 180 146
NDVI northern Sahel
148 150 135
NDVI northern Africa
137 139 –4
NAO
–2 0152 154 141 2 4
Karelia
–6
–4
–2
0
4
Ammarnäs
–6
–4
–2
0
4
Hoge Veluwe
–6
–3
0
3
9
Aber
2
2
6
Figure 4. Effects of the vegetation index (NDVI) in three parts of Africa and NAO on the laying dates of four Pied
Flycatcher populations. On the y-axis the residual laying date is given from a model including only local spring tempe-
rature. The rows are different populations: from top to bottom: Abergwyngregyn (Wales), Hoge Veluwe (Netherlands),
Ammernäs (Sweden), Karelia (Russia). The different columns are for effects of different environmental variables: NDVI
southern Sahel, NDVI northern Sahel, NDVI northern Africa, NAO.

to the effect of southern Sahel NDVI (correlation
between slopes of laying date to either southern or
northern Sahel NDVI: r=–0.88, n=17, P<
0.001). Thus, on average, an increase in vegeta-
tion in the southern Sahel had a delaying effect on
laying date in most populations, but this is mostly
balanced by the advancing effect of vegetation in
the northern Sahel. This does not mean that these
effects of Sahel vegetation are therefore non-exis-
tent. For example, in the Hoge Veluwe area we
depicted the effects of the variation in the two
NDVI-indices, and this example shows that with
the same vegetation in the southern Sahel there is
a potential variation of eight-days in laying date,
whereas a variation of nine days is possible for the
same value in the northern Sahel NDVI (Fig. 6).
DISCUSSION
Predicting breeding conditions at wintering
or migration sites
If there is a correlation between climatic condi-
tions at the wintering site and the breeding site,
birds may use the information at the wintering site
to adjust the timing of migration in order to arrive
at the right time at the breeding grounds. We
found no correlations between the rainfall related
vegetation development in the Sahel zone and the
spring temperature at the breeding grounds in
populations breeding early, but for late breeding
populations we found that dry years in the south-
ern Sahel coincided with warm springs at the
breeding grounds. Flycatchers in these populations
520
ARDEA 94(3), 2006
slope of northern African NDVI (d)
–1
0
1
2
40 50 60 70
laying date (1985–1989)
slope of NAO (d)
–1
0
1
40 50 60 70
slope of southern Sahel NDVI (d)
–1
0
1
slope of northern Sahel NDVI (d)
–1
0
1
2
–2
Figure 5. The strength of the effect of different environmental variables on laying date in different populations of Pied
Flycatchers in relation to the average laying date of these populations. Each data point represents one study area and is
the area specific slope of laying date and the environmental variable. For NDVI positive values mean that more vegeta-
tion delays laying date. For NAO positive values mean that laying date advances after a relatively mild winter. The uni-
variate effects are: southern Sahel: F
1,15
= 0.54, P= 0.470, northern Sahel: F
1,15
= 5.54, P= 0.030, northern Africa:
F
1,15
= 15.63, P= 0.001, NAO: F
1,15
= 5.87, P= 0.030.

would therefore benefit from starting earlier
migration in dry years in order to arrive favou-
rably early at the breeding grounds.
In addition, environmental circumstances dur-
ing migration may provide birds with information
regarding the advance of the spring at their breed-
ing grounds. However, we found few correlations
between either northern Africa NDVI or NAO and
spring temperatures at the breeding grounds. Not
surprisingly, correlations with NAO were all posi-
tive (although only one was significant), reflecting
the effect of the prevailing winds on temperatures
in large parts of Europe. Birds can of course not
measure NAO directly, but since its effect probably
leads to an advance of spring in large parts of
Europe, its effects may give some information on
the advance at each breeding locality, even given
the low correlation coefficients involved.
Conditions at the wintering grounds
and breeding date
We have found that populations differed in the
effect of vegetation in sub-Saharan Africa on lay-
ing dates. These effects of vegetation development
in the wintering areas on laying date are difficult
to interpret from our correlations. In breeding pop-
ulations with a positive effect from the northern
Sahel on laying date we found a negative effect
from the southern Sahel and vice versa. Moreover,
the annual NDVIs in both areas were highly corre-
lated, and the positive effect from one area on lay-
ing date was on average counterbalanced by the
negative effect from the other area. This does not
mean that the effects may be trivial, and in Fig. 6
we illustrate that with the variation that exists
across the northern and southern Sahel NDVI the
laying date may be either advanced or delayed
considerably. It is difficult to understand why with-
in some populations the southern Sahel vegetation
tends to advance laying, and northern Sahel vege-
tation tends to delay it, whilst in others these
effects are completely reversed, but this may result
from breeding populations wintering at different
sites. If so, we might have expected clearer results
showing geographically close breeding populations
with similar pattern, or a correlation of this effect
with the average laying date of populations, but
neither were found. Since it is difficult to give a
biological explanation to the correlations between
sub-Saharan vegetation and laying dates, we can-
not conclude whether there is any real effect of
environmental circumstances in the wintering
grounds on the breeding dates in Europe.
Recently, some studies have reported correla-
tions between arrival date at the breeding grounds
and environmental conditions at the wintering
grounds (Saino et al. 2004, Cotton 2003, Sokolov
& Kosarev 2003), suggesting that birds not only
time their migration to internal or day-length
related clocks (Gwinner 1996, Gwinner & Helm
2003), but also to environmental conditions.
These internal clocks induce physiological changes
in the birds, preparing them for the start of migra-
tion, and constraining how early birds can mi-
grate. The environmental conditions at the time
the birds start their internal migratory program
may therefore modulate the actual timing of
migration. Under favourable environmental condi-
tions, the interval between the internally based
Both et al.: PIED FLYCATCHERS BREEDING DATE
521
148
NDVI northern Sahel
162
NDVI southern Sahel
150
146
152
166 170 174 178 182
154
9.5 days delay
8.1 days advance
Figure 6. The correlation between the vegetation index
in the southern and northern Sahel across different years,
and as example we depict here the effect variation in
vegetation in both areas can have on variation in laying
date in the Hoge Veluwe area. Along the regression slope
the effect of variation in both vegetation indices is only
small (i.e. a four-day delay from the bottom-left to the
top-right corner).

start of the migration program and the actual start
of migration may be small, while in adverse circum-
stances this interval may become larger. In such a
model, the start of migration is constrained by an
internal clock, only if circumstances at the wintering
sites are favourable. Whether environmental condi-
tions at the wintering grounds influence arrival and
breeding dates therefore depends upon how often
environmental conditions constrain the actual start
of migration, and whether the speed of migration is
related to environmental conditions en route, and
this may make it difficult to detect these type of
effects on the breeding grounds.
Conditions during migration and breeding date
We have shown that Pied Flycatchers breed earlier
when it was warmer at their breeding locality, and
that environmental circumstances en route have an
additional effect, but this effect differed between
populations. Early breeding populations advanced
their laying date with more vegetation in Northern
Africa (probably wet conditions). In late breeding
populations the effects were more pronounced, with
an advance in laying date with low vegetation index
in Northern Africa (probably dry circumstances)
and a relatively mild winter (high NAO) in Europe.
In the discussion below we assume that annual vari-
ation in NDVI in Africa is to a large extent related to
variation in rainfall (Schmidt & Karnieli 2000), and
insect availability relies on vegetation growth
(Wolda 1988, Dean & Milton 2001).
In general one would expect that more (rain-
fall related) vegetation in Northern Africa would
make circumstances for migration easier and
hence advance arrival and breeding (Møller &
Merilä 2004), but this was only found amongst
early breeding populations while late breeding
populations advanced breeding with dry condi-
tions. The timing of passage through northern
Africa of late breeding populations is probably
later than earlier breeding populations (Bell
1996), so the degree to which rainfall may create
favourable circumstances may change during the
season. Thus, early in the migration season rainfall
may improve circumstances for breeders because
they profit from the explosion in insect emergence
following the rain. However, in such years the
insects may be gone by the time the late popula-
tions pass by, and therefore late populations may
in fact profit from dry circumstances when at least
some limited amount of food is available. The
profitability of particular environmental circum-
stances may thus depend to a large extent on time
and place, and populations of the same species of
different geographical origin may be affected dif-
ferently by the same environmental factors.
The North Atlantic Oscillation affects the
nature of the weather in large parts of Europe, and
can therefore be considered as a good indicator of
the environmental conditions encountered during
the second part of migration. The effect of NAO
again showed differences across populations: in
early breeding populations there was, on average,
little effect of NAO on the timing of breeding,
while late populations advanced when winters and
spring were mild (high values of NAO). This lack
of an effect in early populations may be because
they migrate generally shorter distances through
Europe, and may therefore be less affected by envi-
ronmental circumstances. That late breeding popu-
lations can advance as a result of high NAO values
has been shown before: the timing of passage on
Helgoland of migrants heading for Scandinavia
has been shown to advance in years with high
NAO values (Hüppop & Hüppop 2003). Under
these circumstances birds can probably speed up
their migration, because of more favourable cir-
cumstances en route to refuel (Jenni & Schaub
2003, Schaub & Jenni 2001). In an earlier study
on breeding dates of Pied Flycatchers across
Europe, it was also found that NAO had a stronger
effect on more northern populations (Sanz 2003),
even without taking local spring temperatures into
account. We suggest that the NAO effects reported
here are not so much an effect of local breeding
circumstances, but rather are an effect of circum-
stances encountered during migration.
Travelling to breed: are breeding dates
constrained by arrival?
In this study we have looked at patterns of envi-
ronmental conditions on the wintering grounds
522
ARDEA 94(3), 2006

and during migration on breeding dates in 17 pop-
ulations of Pied Flycatchers. The effects of winter-
ing conditions were difficult to interpret, but we
found clear effects of circumstances during migra-
tion on breeding dates, although these differed
across populations. There are two non-exclusive
hypotheses why birds breed earlier if circum-
stances en route are more favourable: (1) they
migrate at higher speeds because they can refuel
more quickly and therefore arrive earlier, or (2)
they arrive in better condition and therefore they
can reduce the time between arrival and the start
of breeding. Pied Flycatchers show reverse migra-
tion under adverse spring circumstances (Walther
& Bingman 1984), and refuelling rates have been
found to be higher under more favourable condi-
tions (Bairlein & Hüppop 2004, Jenni & Schaub
2003, Schaub & Jenni 2001), thereby supporting
the first hypothesis. Additionally, there are several
studies showing that within years the early arriv-
ing birds also lay early, supporting the idea that
arrival date indeed constrains laying (Smith &
Moore 2005, Cristol 1995), and that across years
late arrival leads to reduced pre-laying intervals
(Potti 1999). There is some evidence against the
second hypothesis, because within years there is
no relationship between the interval between
arrival and breeding and female condition (Potti
1999, Smith & Moore 2005), and Pied Flycatchers
on average arrive with low body reserves at their
breeding grounds (Silverin 1980). Conditions dur-
ing migration therefore most likely affect arrival
date, which in turn affects breeding dates.
The finding that arrival date is to a certain
extent determined by environmental circum-
stances en route, has been used to question the
hypothesis that relatively inflexible migration
schedules constrain species in their adjustment to
climate change (Marra et al. 2005). The reasoning
is that if arrival date is advanced under favourable
climatic conditions, arrival cannot be such a con-
straint in advancing breeding date under climate
change. Although arrival is not as inflexible as we
may have suggested earlier (Both & Visser 2001),
it may still be the case that the ‘optimal breeding
time’ is advancing faster than the birds’ arrival
time, and hence the average breeding date.
Furthermore, our data showing that breeding
dates do simultaneously correlate with local spring
temperatures, as well as with vegetation in North
Africa, suggests that breeding dates are to a cer-
tain extent constrained by arrival time and/or con-
dition at arrival (either of which may depend on
circumstances en route). As the start of the migra-
tory process is likely to depend to some extent
upon day-length or internal clocks (Gwinner 1996,
Gwinner & Helm 2003), even an improvement in
conditions on the wintering grounds is likely to be
constrained in its effects on the start of migration.
Because birds apparently lay earlier when they
arrive earlier, and since advancing arrival must be
constrained by internal programs determining the
start of the migration program, it is most likely
that adjusting laying date to climate change must
be constrained by such a migration program. This
is despite the fact that, as we have shown here,
environmental variation in conditions at both the
wintering grounds and during migration speed up
migration.
Both et al.: PIED FLYCATCHERS BREEDING DATE
523
ACKNOWLEDGEMENTS
Many people were involved in collecting the data, and we
especially want to acknowledge C.M. Askew, J.H. van
Balen, Duncan Brown, Countryside Council for Wales
(CCW), H.M. Dekhuijzen, Oscar Frías, A. Kerimov, M.
Kern, J. Moreno, S. Merino, and D. Winkel. Temperature
data were kindly provided by the British Atmospheric
Data Centre, the Deutscher Wetterdienst Offenbach,
Dutch Royal Meteorological Service, the Finnish
Meteorological Insitute, Instituto Nacional de Mete-
reología, MeteoSwiss, Swedish Meteorological and
Hydrological Institute, the UK Meteorological Office.
J.J.S. was supported by the Spanish MEC (project REN-
2001-0611/GLO).
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SAMENVATTING
Veel vogelsoorten hebben een korte periode beschikbaar
om te broeden, omdat de omstandigheden in hun leefom-
geving door seizoensinvloeden sterk veranderen. Wanneer
vogels broeden, hangt onder meer af van het moment van
aankomst in het broedgebied, die – zeker bij langeaf-
standstrekkers – bepaald wordt door de treksnelheid. De
treksnelheid is afhankelijk van de omstandigheden in het
overwinteringsgebied en gedurende de trek; factoren als
temperatuur en de hoeveelheid regen kunnen hierbij
belangrijk zijn. Kennis omtrent deze cruciale factoren zou
het mogelijk kunnen maken te voorspellen hoe goed soor-
ten zich aanpassen aan klimaatsveranderingen. Dit artikel
geeft een analyse van effecten van vegetatiegroei in het
overwinteringsgebied en langs de trekroute op het tijdstip
van broeden van 17 populaties Bonte Vliegenvanger
Ficedula hypoleuca in de periode 1982–2000. Het tijdstip
van broeden was niet alleen nauw gecorreleerd met de
voorjaarstemperatuur in het broedgebied, maar ook met
de vegetatiegroei in Afrika en met de NAO (North Atlantic
Oscillation, een maat voor variatie in luchtdruk over de
Atlantische Oceaan en grote delen van Europa). De effec-
ten van vegetatiegroei in het overwinteringsgebied en
langs de trekroute verschilden tussen populaties.
Datzelfde gold voor de omstandigheden in Europa zoals
gemeten door middel van de winter NAO. In het alge-
meen broedden de vroege populaties van het laagland en
in West-Europa eerder in jaren met meer vegetatiegroei in
de Noordelijke Sahel en Noord-Afrika. Daarentegen kwa-
men late populaties uit het hooggebergte en uit Noord- en
Oost-Europa eerder tot broeden in jaren met een vroege
zomer (samenvallend met een hoge NAO). De effecten
verschillen dus tussen populaties afhankelijk van wanneer
precies de vliegenvangers trekken en broeden.
Received 12 April 2005; accepted 12 December 2006

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name of Nederlandse Ornithologische Unie, Ir. van Stuivenbergweg 4, 6644 AB
Ewijk, The Netherlands (BIC: PSTBNL21 IBAN: NL65 PSTB 0000 125347).
Correspondence concerning membership: J.J. de Vries, Oosterend 10 b, 8897
HZ Oosterend, The Netherlands (jacobird@xs4all.nl).
Internet – www.nou.nu