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Climate change and bird phenology: a long-term study in
the Iberian Peninsula
OSCAR GORDO
*
wand J U A N J O S E
´SANZw
*
Departament de Biologia Animal (Vertebrats), Universitat de Barcelona, Av. Diagonal 645, E-08028 Barcelona,
Spain, wDepartamento de Ecologı
´a Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), C/Jose
´Gutie
´rrez Abascal 2,
E-28006 Madrid, Spain
Abstract
Many studies in recent years have demonstrated long-term temporal trends in biological
parameters that can only be explained by climate change. Bird phenology has received
great attention, as it studies one of the most conspicuous, popular, and easily observable
phenomena in nature. There are many studies of long-term changes in spring arrival
dates, most of which concur with earlier records from the last few decades. However, few
data are available for autumn departures or length of stays. Furthermore, existing data
offer an equivocal picture. In this study, we analysed a huge database of about 44 000
records for five trans-Saharan bird species (Ciconia ciconia,Cuculus canorus,Apus apus,
Hirundo rustica and Luscinia megarhynchos). Data were collected from over 1300 sites
around Spain during the period 1944–2004. Common spring arrival patterns were found
in all species. Spring arrival dates have tended to advance since the mid-1970s. Current
dates are similar to those from the 1940s (except for C. ciconia). Thus, the advance of
spring migration over the last three decades could be seen as a return to the initial timing
of arrival dates, after abnormally delayed arrivals during the 1970s. A strong negative
relationship with temperature in Spain at arrival time was observed in all species.
A negative relationship with the Sahel Index (a measurement of precipitation in the
African Sahel area during the rainy season) for the previous year was also found in
C. canorus,A. apus and H. rustica. Regarding autumn departures, all species showed
common interdecadal fluctuations, but only H. rustica is leaving earlier Spain at present.
All species departed earlier in years that had higher temperatures during their repro-
ductive period. However, only for H. rustica the relation between Spanish temperatures
at departure time and the last sightings of individuals was significant. A heterogeneous
temporal response for the length of stay was also found: C. ciconia increased, A. apus did
not change and H. rustica decreased its stay. This is the first study, based on an extensive
bird phenology observational network covering a large region, that shows the most
complete and thorough analysis available for the Mediterranean region.
Keywords: arrival, bird migration, departure, length of stay, Sahel Index, Spain, temperature, temporal
trend, trans-Saharan birds
Received 25 July 2005; revised version received 1 December 2005 and accepted 9 March 2006
Introduction
Long-term phenological changes have been used as
irrefutable evidence that most plant and animal species
are currently reacting to climate change (Parmesan &
Yohe, 2003; Root et al., 2003). In most cases, these
responses are correlated with changes in ambient tem-
perature (IPCC, 2001; Root et al., 2005).
Many biological features of birds, such as: migratory
behaviour (Sparks, 1999); breeding performance (Crick
et al., 1997); fitness components (Sanz et al., 2003);
population dynamics (Sæther et al., 2000); or geographi-
cal distribution (Thomas & Lennon, 1999) have been
significantly linked to climate change. Most published
studies look at migratory behaviour. They examine
temporal changes in the arrival of migrants to their
breeding grounds. Such studies indicate that the arrival
time is advancing (Sanz, 2002; Crick, 2004; Lehikoinen
et al., 2004). This supports the hypothesis that an earlier
Correspondence: Juan Jose
´Sanz, fax 134 915645078,
e-mail: sanz@mncn.csic.es
Global Change Biology (2006) 12, 1993–2004, doi: 10.1111/j.1365-2486.2006.01178.x
r2006 The Authors
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arrival is advantageous for individuals, as spring begins
earlier in their breeding grounds (e.g., Menzel et al.,
2001). However, few studies have analysed temporal
changes in the autumn departure of migrants and no
clear patterns have been found. This suggests that there
is probably a highly specific component in species’
responses, due to the different selective pressures acting
on them (Gatter, 1992; Jenni & Ke
´ry, 2003).
Most bird phenological studies have relied on records
from local field stations or from historical data sets
collected systematically (Whitfield, 2001). Therefore,
most have used data from only one site. The observed
results could not be extrapolated for a whole region.
Most of the results reported to date come from central
and northern Europe (Sanz, 2002; Crick, 2004). Only
long-term time series have been analysed from two
Mediterranean localities (Pen
˜uelas et al., 2002; Gordo
& Sanz, 2005; Gordo et al., 2005). Most western Eur-
opean migrants arrive at breeding grounds throughout
the Iberian Peninsula. Huin and Sparks (1998, 2000)
showed that barn swallows (Hirundo rustica), nightin-
gales (Luscinia megarhynchos) and spotted flycatchers
(Muscicapa striata) arrive in Britain early after warmer
Marches and Aprils in the Iberian Peninsula. There-
fore, it is important to obtain conclusive results about
the impact of climate on bird migration in this region.
This study presents some data to fill this gap. We
analysed a huge database of bird migratory behaviour,
covering hundreds of Spanish sites over the last 60
years. This study examined whether some migratory
birds show long-term changes in their migratory beha-
viour in the Spanish part of the Iberian Peninsula, and
whether these changes can be attributed to climate
change.
Material and methods
Bird phenological database
In 1942, the Instituto Nacional de Meteorologı
´a(INM)
created a monitoring network to study phenology in
Spain. The aim was to better understand the timing of
the seasons and to improve agricultural practices, like
in other European countries (Germany, Menzel et al.,
2001; UK, Huin & Sparks, 1998). This phenological
network is still in operation. It is probably one of the
most successful long-term volunteer monitoring pro-
grams in Europe. Since 1943, hundreds of volunteer
observers have been recording phenological plant and
animal events, using standard observation rules and a
list of common, popular and easily identifiable species
(Anonymous, 1943). These individual observers simply
pay attention to plants and animals in streets, parks,
gardens, fields or forests in or around their home cities
and towns. They record all observable phenological
events throughout the year, with no special emphasis
on a particular season or species. Such observations are
simple and easy, as INM proposed species which have
favourable characteristics for a volunteer phenological
monitoring programme: (i) species are widespread
throughout Spain (everyone in the country is a potential
observer); (ii) they are abundant (observation of pheno-
logical events is not constrained by the number of
individuals and no special effort is required to observe
them); (iii) they have an unmistakable morphology
and/or behaviour (everybody knows them, which
makes data highly reliable). Therefore, this methodol-
ogy ensures that data are highly homogeneous, en-
abling all collected records from different observers to
be compared.
The migratory behaviour of five trans-Saharan bird
species (white stork Ciconia ciconia; cuckoo Cuculus
canorus; swift Apus apus; barn swallow and nightingale)
was selected and proposed by the INM as a potential
bioindicator of the timing of seasons. The species mon-
itored are some of the most common and abundant
migrants in the Iberian Peninsula (Martı
´& Del Moral,
2003). These species’ spring phenology was measured
by the date the first individuals were detected in the
study sites each year. For the white stork, swift and barn
swallow, detection was defined as the first sighting of
an individual member of the local population. For less
conspicuous species (cuckoo and nightingale) it was
defined as the first singing male heard. The autumn
phenology of the white stork, swift and barn swallow
was monitored by means of the last individual sighted
in the study sites. A third phenological variable could
also be defined for these three species: the length of the
stay. This new variable was calculated as the number of
days between the first and the last sighting of indivi-
duals, when both records were available for the same
site and the same phenological year.
We collected and computerized all available records
of these five species’ spring and autumn phenology.
Data were checked to eliminate incorrectly recorded
single values, which could have resulted from human
error in recording dates or in the computerization
process. A database of about 44 000 records remained
after this data quality check. Data came from sites all
around Spain (1384 sites) and was collected from 1944
to 2004. Each date was transformed into a Julian day
(1 51 January), taking into account leap years. In leap
years, 1 day was added after February 28.
Information about UTM coordinates (longitude and
latitude) and altitude (m a.s.l.) from each observer ’s
site was also available. We used them to account for
the observed variability in arrival dates, caused by the
broad geographical range of used sites and thus to
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prevent spatial gradients (Legendre, 1993). For this
purpose, we constructed a multiple regression model
with these variables as predictors and recorded dates
for each species and phenophase as dependent variable.
Quadratic terms were also included to identify non-
linear patterns only in those cases in which they were
significant. The interaction between latitude and long-
itude was also included. Hence, arrival dates were
corrected for their spatial position, giving fully compar-
able values of a species’ early or late arrivals from
different sites since within year variability were re-
moved. For each species and phenophase, the residuals
were averaged by year to obtain a unique annual
phenological value for Spain. Years with less than 20
observations were not included. These time series were
used hereinafter for statistical analyses.
Climate data
To evaluate the impact of climate on spring arrivals, we
took into account climate data from both breeding and
wintering grounds. Spain’s climate in the spring was
measured as the average of the mean monthly tempera-
ture for the best adjusted 2 months to the arrival date of
each species. Therefore, the average of temperatures for
January and February was used for the white stork and
the average of March and April temperatures was used
for the other species.
The effect of the African wintering grounds’ climate
was evaluated by means of rainfall in the Sahel. Pre-
vious studies have pointed out the importance of win-
tering conditions for trans-Saharan species. Such
conditions affect subsequent life cycle traits (e.g. spring
arrivals, Gordo et al., 2005; reproductive success, Saino
et al., 2004; or sexual selection, Mller, 2004). Interann-
ual variability in Western African rainfall was seen to be
the main driver of changes in spring phenology for
some species analysed in a previous study of one
Spanish site (Gordo et al., 2005). We wanted to test
whether these results could be generalized to most
Iberian populations of these species. Therefore, we used
the Sahel Index, a synthetic measure of precipitation
anomalies in the Sahel. Such anomalies have already
been quantified by some authors (Nicholson, 1979;
Tarhule & Lamb, 2003; Dai et al., 2004) and are available
at http://tao.atmos.washington.edu/data_sets/sahel/
for the years 1898–2004. This index is derived from
the average deviation from monthly rainfall at 14 me-
teorological stations located in the western part of this
region (101N–171N and 181W–61E). The average of
monthly Sahel Index values was calculated for the rainy
season (i.e. June–October; Dai et al., 2004).
The influence of climate on autumn departures was
evaluated by examining monthly temperatures during
two phases of the bird’s stay in Spain. The hypothetical
delaying effect of climate on departures was tested
using the mean temperature for Spain during breeding
months (April–June). Better climatic conditions during
hatching and/or when raising juveniles may accelerate
this phase, which in turn could advance subsequent
stages of the vital cycle (e.g. second clutches) until
departure time (Lack, 1958; Ellegren, 1990). In addition,
we controlled for the potential prompt and direct effect
of climate on departures, including temperatures dur-
ing the month birds leave Iberia. The best-adjusted
month, according to the mean value for the whole
departure of each species, was selected to examine the
direct effect of climate on departure. Therefore, August
was selected for the white stork and the swift, and
September for the barn swallow.
Statistical analyses
The analyses can be divided into two parts. Firstly, the
existence of temporal trends were tested in all three
phenological phases (arrivals, departures and stays) by
means of a multiple regression model for each species
including only year and its quadratic term (when it was
significant) as predictors. Secondly, we examined the
effect of climatic variables on temporal trends in arrival
and departure dates by means of another multiple
regression model for each species including only those
selected climatic variables. All analyses were conducted
with Statistica (StatSoft, 2001).
Results
Temporal trends
With exception of the nightingale, spring arrival dates
for all species showed significant temporal trends dur-
ing the last six decades (Table 1). The white stork had
the best model. Its arrival dates showed the most
pronounced changes with advancement about 40 days
over the study period. This advance occurred over the
last 20 years in particular (Fig. 1). In the rest of species,
arrival dates at present are similar to those ones re-
ported during the 1940s–1950s (Fig. 1). However, for the
swift and the barn swallow a notable delay in their
arrivals was noticed during the early 1970s, with a clear
trend towards the advance since that time (approxi-
mately 6 days for the swift and 13 days for the barn
swallow). Singing dates for the cuckoo and nightingale
were always fitted to a narrow band in the first and
second weeks, respectively, of April. The maximum
interannual difference recorded in the last six decades
has been about 12 days (Fig. 1).
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Table 1 Results of the multiple regression models for temporal trends in phenological data
Species
Annual
records Mean year PSquared year Pr
2
Fdf P
Arrivals
White Stork 88 29.4 57.85 o0.001 0.015 o0.001 0.754 86.04 2, 56 o0.001
Cuckoo 104 95.6 11.66 0.039 0.003 0.040 0.132 3.94 2, 52 0.025
Swift 94 109.6 16.41 0.013 0.004 0.014 0.140 4.55 2, 56 0.015
Barn Swallow 182 82.1 38.14 o0.001 0.010 o0.001 0.387 17.96 2, 57 o0.001
Nightingale 53 107.1 0.020 0.353 0.016 0.88 1, 55 0.353
Departures
White Stork 45 226.4 0.04 0.187 0.030 1.78 1, 57 0.187
Swift 69 239.2 0.05 0.080 0.052 3.17 1, 58 0.080
Barn Swallow 110 264.4 0.06 o0.001 0.201 14.33 1, 57 o0.001
Stays
White Stork 41 197.7 47.80 o0.001 0.012 o0.001 0.838 131.67 2, 51 o0.001
Swift 57 127.5 0.05 0.291 0.020 1.14 1, 56 0.291
Barn Swallow 93 181.3 22.11 0.012 0.006 0.012 0.318 13.31 2, 57 o0.001
The mean number of records per year employed, the mean (arrivals and departures in Julian day, stays number of days), the values
of the slope and its significance in the linear and quadratic term of the year, and the final model explanatory capacity (r
2
), F-test (F),
degrees of freedom (df) and its significance are indicated in each case.
1944 1954 1964 1974 1984 1994 2004 1944 1954 1964 1974 1984 1994 200
4
Year Year
Residual of first sighted individual
–35
–30
–25
–20
–15
–10
-5
0
5
10
15
White Stork
–10
–8
–6
–4
–2
0
2
4
6
8
10
12 Barn Swallow
–10
–8
–6
–4
–2
0
2
4
6
8
10
12
Swift
Residual of first singing male
–10
–8
–6
–4
–2
0
2
4
6
8
10
12
Cuckoo
–10
–8
–6
–4
–2
0
2
4
6
8
10
12
Nightingale
Fig. 1 Temporal trends for the residuals once the geographical variability was removed of the first individuals of the white stork,
cuckoo, swift, barn swallow and nightingale to be detected. Black dots are the mean residual for each year and bars are standard error.
A distance-weighted smoothed line (least squares method; Statsoft, 2001) has been superimposed to emphasize the underlying trend
(solid line). x-axis units 5days.
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Only departure dates of the barn swallow showed a
significant temporal trend (Table 1) in spite of the clear
interannual fluctuations observed in all three species
(Fig. 2). In all species, an advancement of departures
was recorded until mid-1960s. During the next 20 years
a certain trend to leave later the breeding grounds was
observed (Fig. 2). Since mid-1980s individuals are de-
parting earlier, being this especially patent in the swift
and barn swallow (Fig. 2).
The picture offered by the length of the stay was quite
different for the white stork, the swift and the barn
swallow (Fig. 3) due to the peculiar interannual fluctua-
tions in each species’ arrivals and departures. The
length of the stay in the white stork showed really the
best explicative temporal model (Table 1). Since the
1970s it has increased more than 1 month. In the case
of the barn swallow, despite of the same sign in the
parameters of the model, a clear break point appears in
the early 1970s which reduced about 15 days the length
of the stay. Since then, a slight trend towards the
increase of this period has been recorded. The swift
did not show significant temporal trends (Fig. 3).
Relationships with climate
Spring arrival dates of all species showed highly sig-
nificant models with climatic variables accounting up to
56% of variability. In all cases, temperatures in Spain
Year
Residual of last detected individuals
1945 1955 1965 1975 1985 1995 2005
–16
–12
–8
–4
0
4
8
12
16
20
White Stork
–16
–12
–8
–4
0
4
8
12
16
Swift
–16
–12
–8
–4
0
4
8
12
16
Barn Swallow
Fig. 2 Temporal trends for the residuals once the geographical
variability was removed of the last detected individuals of the
white stork, swift and barn swallow. Black dots are the mean
residual for each year and bars are standard error. A distance-
weighted smoothed line (least squares method; Statsoft, 2001)
has been superimposed to emphasize the underlying trend (solid
line). x-axis units 5days.
–20
–15
–10
–5
0
5
10
15
20
25
30 Barn Swallow
Residual of the duration of stay
1945 1955 1965 1975 1985 1995 2005
Year
–20
–15
–10
–5
0
5
10
15
20
25
30
35
White Stork
–20
–15
–10
–5
0
5
10
15
20
25
30 Swift
Fig. 3 Temporal trends for the residuals once the geographical
variability was removed of the length of the stay of the white
stork, swift and barn swallow. Black dots are the mean residual
for each year and bars are standard error. A distance-weighted
smoothed line (least squares method; Statsoft, 2001) has been
superimposed to emphasize the underlying trend (solid line).
x-axis units 5number of days.
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during arrival month were included. The negative sign
of the relationships means that individuals arrived ear-
lier in warmer years. The effect of climate in wintering
ground was also significant in the cuckoo, the swift and
the barn swallow. In these three cases, the effect was
also negative. Therefore, wet years in the Sahel region
were linked to earlier detections of individuals.
Climatic effects on departures were much less strong
than climatic effects on arrivals. A trend towards earlier
departures after warmer springs was found in all three
species studied (Table 2), although in the case of swift
this relationship was non-significant. The prompt and
direct effect of temperatures during the month of de-
partures was only significant in the case of barn swal-
low. This species trends to depart later in years with
warmer Septembers.
Discussion
General remarks
This is the first study assessing the impacts of climate
change on temporal trends in the migratory behaviour
of a large number of populations in the Mediterranean
region. Furthermore, no study on bird migration has
used such an extensive number of records and sites (but
see Sparks & Braslavska
´, 2001; Forchhammer et al., 2002;
Ptaszyk et al., 2003). Recently, some authors have at-
tempted to compare data covering part of Europe
(Sparks et al., 2005). This study used high-quality re-
cords, but too few sites were considered for such a wide
range of geographical, environmental and climatic con-
ditions. Despite the coherent patterns of advances in
spring migration reported in most of the studies and for
most species (Sokolov et al., 1998; Sparks, 1999; Tryja-
nowski et al., 2002; Hu
¨ppop & Hu
¨ppop, 2003; Lehikoi-
nen et al., 2004; Zalakevicius et al., 2006), more caution is
required when extrapolating conclusions. Only studies
that involve a large number of time series and represent
a wide range of conditions would be conclusive (For-
chhammer et al., 2002).
Two aspects of our database could be criticized: (1)
records belong to a broad range of geographical (from
9.051E to 3.221W, from 36.021S to 43.681N, from 3 to
1730 m a.s.l.) and environmental conditions (from the
most arid Mediterranean to wet Euro Siberian); (2) data
were provided by hundreds of amateur observers.
However, results indicate that these facts do not seem
to be problematic. In spite of the enormous heteroge-
neity of the data, changes in the year-to-year timing of
migration of the species studied are large enough to be
detected. This heterogeneity could include opposite
responses in different regions (Gordo & Sanz, 2005;
Gordo et al., 2005), which can make it difficult to detect
global effects. Additionally, the first arrival date (or last
departure date) may in itself be another source of bias,
as indicated in many studies (Sparks et al., 2001; Tryja-
nowski & Sparks, 2001; Lehikoinen et al., 2004). How-
ever, the drift effect that may be induced by recording
the first individual in a single site does not occur in our
Table 2 Results of the multiple regression models for climatic effects in phenological data
Species
Arrival temperature Sahel Index Multiple regression model
bPbPr
2
Fdf P
Arrivals
White Stork 3.453 0.015 0.035 0.136 0.150 4.93 2,56 0.011
Cuckoo 1.758 o0.001 0.014 0.005 0.511 27.17 2,52 o0.001
Swift 1.671 o0.001 0.016 0.023 0.308 12.48 2,56 o0.001
Barn Swallow 2.041 o0.001 0.052 o0.001 0.564 36.85 2,57 o0.001
Nightingale 1.505 o0.001 0.006 0.301 0.272 10.07 2,54 o0.001
Reproduction
temperature
Departure
temperature Multiple regression model
bPbPr
2
Fdf P
Departures
White Stork 1.837 0.005 0.299 0.599 0.131 4.21 2,56 0.020
Swift 1.165 0.074 0.411 0.476 0.075 2.32 2,57 0.108
Barn Swallow 0.675 0.047 0.487 0.016 0.155 5.13 2,56 0.009
The values of the slope (b) and its significance (P) for climatic variables and the final model explanatory capacity (r
2
), F-test (F),
degrees of freedom (df) and its significance are indicated in each case.
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study. Our study is not subject to the aberrant or
anomalous, nonrepresentative migratory behaviour of
one individual as we worked with many records per
year (in some cases over 400). Therefore, interannual
changes in the first arrival date for the whole of Spain
are not subject to the bias effect of data on the first
individual. They reflect a real trend of earlier or later
arrivals of these first individuals in many Spanish
populations in a certain year. Thus, results offer a real
picture of the timing of migration each year. The errors
or vagueness in some records (an unavoidable problem
when working with large databases) are absorbed by
the vast sample size employed.
Most of the previous studies assessing temporal
trends in migratory behaviour and the relation of such
trends to climatic changes have the advantage of ana-
lysing a large number of species. This is due to the great
monitoring effort undertaken by specialists at a single
site (e.g. 81 species in Va
¨ha
¨talo et al., 2004; 65 in Jenni &
Ke
´ry, 2003; 60 in Loxton et al., 1998; 46 in Gatter, 1992; 40
in Zalakevicius et al., 2006; 39 in Sparks & Mason, 2001).
Our study showed trends in only five species. These
species are common, popular and widespread enough
throughout Spain to be recorded by anybody, with no
search effort and no specific abilities. However, in our
opinion, these species are heterogeneous enough (in size,
timing of migration, food supplies, habitat preferences or
reproductive performance) to indicate a common tem-
poral signal in the majority of trans-Saharan migrants.
Spring arrivals
Spring migration did not advance steadily; there were
decadal fluctuations (i.e. polynomial patterns). Current
arrival dates are similar or even seem to be a bit later
(see the cuckoo, swift and nightingale in Fig. 1) to those
occurring at the beginning of the study period (except
for the white stork). Therefore, caution is required when
interpreting results, to avoid drawing erroneous con-
clusions about changes in the migratory behaviour of
bird species. In this study, the advance in arrival date
recorded over the last few decades should be better
interpreted as a trend towards re-establishing the tim-
ing of migration after an anomalous period of delayed
arrivals during the 1970s–1980s.
Despite of our purely correlational analyses, spring
temperatures in Spain (Fig. 4) seem to be an important
driver of the observed interannual fluctuations in arri-
vals for all species. This result is in agreement with most
of the previous studies (Loxton et al., 1998; Sokolov
et al., 1998; Sparks, 1999; Sparks & Mason, 2001; Tryja-
nowski et al., 2002; Zalakevicius et al., 2006). The earlier
arrivals related to higher temperatures should be due to
the advancement of the spring course in the Iberian
Peninsula and consequently the presence of ecological
suitable conditions for an early colonization of first bree-
ders. In basis to the found relationship, we thus may
hypothesize that predicted future warming (IPCC, 2001;
de Castro et al., 2005) will favour earlier arrival dates.
African climate was also significantly related to some
species’ arrivals. The negative relation indicates that
dry years in the Sahel were associated with later arrivals
of Spanish populations. In arid environments such as
the Sahel, water availability is a restrictive factor (Win-
stanley et al., 1974; Svensson, 1985; Mullie
´et al., 1995;
Shine, 2003; Gordo et al., 2005). Wet years enhance
ecological conditions in the region, due to higher plant
productivity (Nicholson et al., 1990; Herrmann et al.,
2005). This leads to a greater abundance of insects,
which are food resources for insectivorous birds (such
as our studied species; Winstanley et al., 1974). In the
case of the white stork, the amount of rainfall also
directly affects the availability and extension of wet-
lands. Wetlands are a key ecosystem for the stork’s
1945 1955 1965 1975 1985 1995
Year
–120
–80
–40
0
40
80
120
Sahel Index
2005 1945 1955 1965 1975 1985 1995
Year
9
10
11
12
13
March-April Spain temperature (°C)
2005
Fig. 4 Annual values of the Sahel Index during the rainy season (June–October) and the average temperature of Spain for March
and April.
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survival (Mullie
´et al., 1995; Brouwer et al., 2003; Shine,
2003). Increased food supplies can benefit species in two
ways: (i) they increase winter survival rates; (ii) they
enhance the winter moult and the chances of obtaining
the necessary fat reserves before the beginning of the
spring migration and/or during the journey. Both of
these factors, either individually or together, would
result in advanced arrival dates. If winter survival rates
increased, there would be more individuals, which
would increase the chance of early observations. In
the second case, birds would complete their journey
in less time, as they would have improved feathers and
body condition and/or enhanced environmental condi-
tions en route, which in turn may reduce stopover
times. Furthermore, the northern limit reached by the
monsoons in dry years is at lower latitudes, moving
transitional regions between desert and savannah some
hundreds of kilometres southward. This notably in-
creases spring migration distances over the Sahara
(Winstanley et al., 1974; Svensson, 1985). Therefore,
recent earlier arrivals for some species are induced by
a combination of climate warming in Spain and im-
proved ecological conditions in the Sahel region of
Africa, as a result of the end of a drought period.
One of the most notable results in our data was the
great delay in arrival dates of the swift and barn
swallow during the years 1970–1972 (see Fig. 1). An
examination of the climatic variables shows that the
Sahel Index was very low between 1969 and 1971 (see
Fig. 4). In parallel, the subsequent springs in Spain for
those years (i.e. 1970–1972) were three consecutive and
extremely cold seasons (see Fig. 4). The mean tempera-
ture for March and April (the mean arrival months of
these species) of this three years was only 9.1 1C. The
mean temperature at this time in the rest of the study
years was 10.5 1C(t
57
52.59; P50.012). We suggest that
the pronounced delay in arrivals from 1970–1972 was
due to the synergistic effect of extremely unfavourable
conditions both in wintering and breeding areas. In the
case of the barn swallow, the effect of these three
successive bad years seems to have been especially long
lasting, as it has only arrived on similar dates to those
previous to 1970 in recent years.
Autumn departures
The last sighting of a migratory species is more difficult
to interpret than the first sighting. It is probably affected
by the same sources of bias as the first arrival date (it is
the tail of a population size-dependent distribution).
Hence, it could be argued that it is not representative of
the real autumn migratory behaviour of the whole
population. Furthermore, intrinsically, it is a less precise
measure than first arrival date. The behaviour of in-
dividuals before departure is generally more cryptic
than during spring arrivals (e.g. there is an absence of
singing activity; although barn swallows make large
roosts before migrating in flocks) and it, therefore,
requires more attention. Despite these difficulties, there
were strong interdecadal oscillations in all species (see
Fig. 2) although only in the barn swallow these had a
significant temporal trend.
There is a lack of data for the last sighting of indivi-
duals, as indicated in previous studies. Bird departures
attract less attention than arrivals, as they are a less
conspicuous phenomenon. Few time-series to date have
analysed the phenology of autumn migration (Harmata,
1980; Gatter, 1992; Bezzel & Jetz, 1995; Sokolov et al.,
1999; Bairlein & Winkel, 2001; Sparks & Braslavska
´,
2001; Sparks & Mason, 2001; Gilyazov & Sparks, 2002;
Cotton, 2003; Jenni & Ke
´ry, 2003; Witt, 2004; Gordo &
Sanz, 2005), and evidence of delays or advances are
equivocal. Although our broad study was only carried
out with three species, similar temporal patterns were
found for all of them during certain decades (see Fig. 3).
Since the beginning of 1980s, the common trend has
been towards an advance in departure dates (which
agrees with long-distance migrant results of Jenni &
Ke
´ry, 2003). This advance in autumn departures is
probably indirectly affected by phenological changes
in arrivals (but see Kosicki et al., 2004) through inter-
mediate phases of the life cycle. Individuals arrive
earlier, reproduce earlier (Crick et al., 1997; Sokolov &
Payevsky, 1998; Both & Visser, 2001), and due to the
nexus between reproduction and autumn departure
(Lack, 1958; Ellegren, 1990; Sokolov, 2000; Bojarinova
et al., 2002) then depart earlier, to take advantage of the
benign environmental conditions in the Sahel at the end
of the rainy season in October (Morel, 1973; Gatter, 1992;
Jenni & Ke
´ry, 2003). This hypothesis may explain the
negative relations found between reproductive period
temperatures and departure dates (see Table 2). But it is
difficult to understand how climate change can be
related to temporal trends in autumn phenology, if
weak direct (temperature at departure time) and indir-
ect (temperature affecting the timing of reproduction)
relations exist.
Length of stay
The consequences of long-term changes in the time
between arrivals and departures has been assessed in
very few studies (Bairlein & Winkel, 2001; Sparks &
Braslavska
´, 2001; Sparks & Mason, 2001; Gilyazov &
Sparks, 2002; Cotton, 2003; Gordo & Sanz, 2005), despite
the biological implications that fluctuations in this
measure should have on the species’ life cycle. An
increase in length of stay should be advantageous to
2000 O.GORDO&J.J.SANZ
r2006 The Authors
Journal compilation r2006 Blackwell Publishing Ltd, Global Change Biology,12, 1993–2004
reproduction, as it increases fledgling survival and
chances of second or third broods. A reduction should
be disadvantageous for the opposite reasons (unfortu-
nately, no data about reproductive success of the species
studied are available to test this hypothesis). However,
species can also maintain this part of their life cycle
constant, regardless of changes in migratory behaviour.
We studied few species, but the variation in their
responses seems to disagree with the general trend
towards increased stays reported previously (Bairlein
& Winkel, 2001; Sparks & Mason, 2001; Gilyazov &
Sparks, 2002). If we look at the results for the swift
and barn swallow in such studies, variation between
sites is also observed. It is, therefore, quite difficult to
draw conclusions, as each species showed a different
pattern over the last 60 years. Thus, there is an inter-
esting, but complex, picture of possible heterogeneous
responses of stay length to climate change.
The special case of the white stork
This species showed the greatest rates of advance in
their spring arrivals, inducing the greatest changes in
the length of stay. These results concur with an study of
this species in Poland (Ptaszyk et al., 2003; but see
Czy(owicz & Konieczny, 2001; Zalakevicius et al.,
2006), even though this was clearly a different popula-
tion with different migratory pathways and wintering
areas (Bernis, 1959; Fiedler, 2001).
The presence of wintering individuals in Iberia has
been repeatedly reported since many decades ago
(Duclo
´s, 1956; Cruz-Valero, 1964). The occurrence of
wintering individuals in other places in the Mediterra-
nean basin is also well known (Van den Bosche, 2002).
Therefore, there have always been some individuals
both in western and eastern European populations that
do not overwinter in Africa. This nonmigratory beha-
viour seems to be spreading. Over the last decade,
increasing numbers of individuals have been recorded
in Iberia during the winter (Tortosa, 1992; Ma
´n
˜ez et al.,
1994; Tortosa et al., 1995; Anonymous, 1996). Wintering
has also been reported in other western Mediterranean
areas (Archaux et al., 2004, in France; Samraoui &
Houhamdi, 2002, in Algeria). Human-induced environ-
mental changes (e.g. increases in the numbers of rub-
bish dumps) have been proposed as the origin of this
apparent trend towards settlement of the white stork
(Ma
´n
˜ez et al., 1994; Tortosa et al., 1995, 2002; Peris, 2003;
Archaux et al., 2004). However, recent climate change
may also favour this settlement, due to milder winters
(Mata et al., 2001). The notable advance in spring
arrivals, recorded since the 1980s, could be due to
individuals that remained in the Iberian Peninsula or
North Africa during the winter (Ma
´n
˜ez et al., 1994;
Tortosa et al., 1995), thus reducing strongly their migra-
tory journeys (Fiedler, 2001). This hypothesis has been
proposed as an explanation for earlier spring arrivals in
migratory birds (Coppack & Both, 2003; Coppack et al.,
2003). Therefore, we suggest that the major changes in
spring phenology reported in the populations studied
since the 1980s reflect changes in migratory behaviour.
Changes in migratory behaviour may be due to selec-
tive pressures acting on the white stork. Individuals
that migrate to Afrotropics are faced with many ha-
zards, which have a negative effect on their survival
and probably on their reproductive success. Bad ecolo-
gical conditions in the Sahel, resulting from hard
droughts until the mid-1980s (see Fig. 4; Dai et al.,
2004; Herrmann et al., 2005), improved human hunting
activity in sub-Saharan countries (Thauront & Duquet,
1991); the degradation of wetlands used for resting and
thermoregulation (Mullie
´et al., 1995; Brouwer et al.,
2003; Shine, 2003); and expenditure of time and energy
on a longer journey, due to the southward expansion of
the Sahara desert (Tucker et al., 1991; Mullie
´et al., 1995;
Nicholson, 2001), are some examples of the migration
costs for this species. Individuals that remained in
Iberia or North Africa, benefit from: mild winters;
guaranteed food supplies from rubbish dumps; an
increase in populations of the invasive red swamp
crayfish Procambarus clarkii (Ma
´n
˜ez et al., 1994; Tortosa
et al., 1995, 2002; Peris, 2003); and better opportunities to
adjust their spring arrivals to the spring course in the
breeding grounds. Thus, nonmigrant white storks ben-
efit from many factors. It is, therefore, likely that the
absence of migratory behaviour is increasing in Spanish
populations. Consequently, earlier arrivals are detected.
Acknowledgements
This work is dedicated to all observers of the Spanish phenolo-
gical network which have made possible this study with their
volunteer task. We thank to the INM for the access to pheno-
logical data. We are very grateful two anonymous reviewers
for their constructive comments on the manuscript. O. G. ack-
nowledges Xavier Ferrer, Lluı
´s Brotons and the MEC for the
financial support of a Doctoral Fellowship of the FPU pro-
gramme (ref. AP2002-1439). J. J. S. was supported by the Spanish
MEC (project REN-2001-0611/GLO).
References
Anonymous (1943) Atlas de plantas para las observaciones fenolo
´gi-
cas. Servicio Meteorolo
´gico Nacional–Seccio
´n de Climatologı
´a,
Madrid.
Anonymous (1996) I censo invernal de Cigu
¨en
˜a Blanca en
Espan
˜a. La Garcilla,96, 42–43.
Archaux F, Balanc¸a G, Henry PY et al. (2004) Wintering of white
storks in Mediterranean France. Waterbirds,27, 441–445.
BIRD PHENOLOGY AND CLIMATE CHANGE 2001
r2006 The Authors
Journal compilation r2006 Blackwell Publishing Ltd, Global Change Biology,12, 1993–2004
Bairlein F, Winkel W (2001) Birds and climate change. In: Climate
of the 21st Century: Changes and Risks (eds Lozan JL, GralH,
Hupfer P), pp. 278–282. Scientific Facts, GEO, Hamburg.
Bernis F (1959) La migracion de la cigu
¨en
˜as espan
˜olas y de las
otras cigu
¨en
˜as ‘occidentales’. Ardeola,5, 9–80.
Bezzel E, Jetz W (1995) Verschiebung der Wegzugperiode bei
der Monchsgrasmucke (Sylvia atricapilla) 1966–1993 – Reaktion
auf die Klimaerwarmung. Journal fu
¨r Ornitologie,136,
83–87.
Bojarinova JG, Rymkevich TA, Smirnov OP (2002) Timing of
autumn migration of early and late-hatched Great Tits Parus
major in NW Russia. Ardea,90, 401–409.
Both C, Visser ME (2001) Adjustment to climate change is
constrained by arrival date in a long-distance migrant bird.
Nature,411, 296–298.
Brouwer J, Mullie
´WC, Scholte P (2003) White Storks Ciconia
ciconia wintering in Chad, northern Cameroon and Niger: a
comment on Berthold et al. (2001). Ibis,145, 499–501.
Coppack T, Both C (2003) Predicting life-cycle adaptation of
migratory birds to global climate change. Ardea,90, 369–377.
Coppack T, Pulido F, Czisch M et al. (2003) Photoperiodic
response may facilitate adaptation to climate change in long-
distance migratory birds. Proceedings of the Royal Society of
London, Series B,270, 43–45.
Cotton PA (2003) Avian migration phenology and global climate
change. Proceedings of the National Academy of Sciences USA,
100, 12219–12222.
Crick HQP (2004) The impact of climate change on birds. Ibis,
146, 48–56.
Crick HQP, Dudley C, Glue DE et al. (1997) UK birds are laying
eggs earlier. Nature,388, 527–527.
Cruz-Valero A (1964) Primeras observaciones de Cigu
¨en
˜as en
1962 y 1963 en Badajoz. Ardeola,9, 137.
Czy(owicz W, Konieczny K (2001) Terminy przyloto
´w i odloto
´w
wybranych gatunko
´w ptako
´w w okolicach wsi Brzo
´zka
(powiat Wolo
´w) w latach 1947–1985. Ptaki Slaska,13, 126–129.
Dai A, Lamb PJ, Trenberth KE et al. (2004) The recent Sahel drought
is real. International Journal of Climatology,24, 1323–1331.
de Castro M, Martı
´n-Vide J, Alonso S (2005) El clima de Espan
˜a:
pasado, presente y escenarios de clima para el siglo XXI. In:
Evaluacio
´n preliminar de los impactos en Espan
˜a por efecto del
cambio clima
´tico (ed. Moreno Rodrı
´guez JM), pp. 1–65. Minis-
terio de Medio Ambiente, Madrid.
Duclo
´s C (1956) Permanencia de Ciconia ciconia en nuestra
penı
´nsula. Ardeola,3, 304.
Ellegren H (1990) Timing of autumn migration in bluethroats
Luscinia svecica svecica depends on timing of breeding. Ornis
Fennica,67, 13–17.
Fiedler W (2001) Large-scale ringing recovery analysis of
European White Storks (Ciconia ciconia). Ring,23, 73–79.
Forchhammer MC, Post E, Stenseth NC (2002) North Atlantic
Oscillation timing of long- and short-distance migration.
Journal of Animal Ecology,71, 1002–1014.
Gatter W (1992) Zugzeiten und Zugmuster im Herbst: Einflu
des Tribhauseffekts auf den Vogelzug? Journal fu
¨r Ornitologie,
133, 427–436.
Gilyazov A, Sparks TH (2002) Change in the timing of migration
of common birds at the Lapland Nature Reserve (Kola Penin-
sula, Russia) during 1931–1999. Avian Ecology and Behaviour,8,
35–47.
Gordo O, Brotons L, Ferrer X et al. (2005) Do changes in climate
patterns in wintering areas affect the timing of the spring
arrival of trans-Saharan migrant birds? Global Change Biology,
11, 12–21.
Gordo O, Sanz JJ (2005) Phenology and climate change: a long-
term study in a Mediterranean locality. Oecologia,146, 484–495.
Harmata W (1980) Phenological dynamics of arrivals and de-
partures on migratory birds in Cracov, Poland, and the envir-
onments in the 19th and 20th century. International Journal of
Biometeorology,24, 137–140.
Herrmann SM, Anyamba A, Tucker CJ (2005) Recent trends
in vegetation dynamics in the African Sahel and their relation-
ship to climate. Global Environmental Change,15, 394–404.
Huin N, Sparks TH (1998) Arrival and progression of the swallow
Hirundo rustica through Britain. Bird Study,45, 361–370.
Huin N, Sparks TH (2000) Spring arrival patterns of the Cuckoo
Cuculus canorus, Nightingale Luscinia megarhynchos and
Spotted Flycatcher Muscicapa striata in Britain. Bird Study,47,
22–31.
Hu
¨ppop O, Hu
¨ppop K (2003) North Atlantic Oscillation and
timing of spring migration in birds. Proceedings of the Royal
Society of London, Series B,270, 233–240.
IPCC (2001) Climate change 2001: impacts, adaptation, and
vulnerability. In: Contribution of Working Group II to the Third
Assessment Report of the Intergovernmental Panel on Climate
Change (eds McCarthy JJ, Canziani OF, Leary NA, Dokken
DJ, White KS), Cambridge University Press, Cambridge.
Jenni L, Ke
´ry M (2003) Timing of autumn bird migration under
climate change: advances in long-distance migrants, delays in
short-distance migrants. Proceedings of the Royal Society of
London, Series B,270, 1467–1471.
Kosicki J, Sparks TH, Tryjanowski P (2004) Does arrival date
influence autumn departure of the White Stork Ciconia ciconia?
Ornis Fennica,81, 91–95.
Lack D (1958) The return and departure of swifts Apus apus at
Oxford. Ibis,100, 477–502.
Legendre P (1993) Spatial autocorrelation: trouble or new para-
digm? Ecology,74, 1659–1673.
Lehikoinen A, Sparks TH, Zalakevicius M (2004) Arrival and
departure dates. Advances in Ecological Research,35, 1–31.
Loxton RG, Sparks TH, Newnham JA (1998) Spring arrivals
dates of migrants in Sussex and Leicestershire (1966–1996).
The Sussex Bird Report,50, 181–196.
Ma
´n
˜ez M, Tortosa FS, Barcell M et al. (1994) La invernada de
la ciguena blanca en el suroeste de Espana. Quercus,105,
10–12.
Martı
´R, Del Moral JC (2003) Atlas de las aves reproductoras de
Espan
˜a. Direccio
´n General de Conservacio
´n de la Naturaleza-
Sociedad Espan
˜ola de Ornitologı
´a, Madrid.
Mata AJ, Caloin M, Michard-Picamelot D et al. (2001) Are non-
migrant white storks (Ciconia ciconia) able to survive a cold-
induced fast? Comparative Biochemistry and Physiology A –
Molecular and Integrative Physiology,130, 93–104.
Menzel A, Estrella N, Fabian P (2001) Spatial and temporal
variability of the phenological seasons in Germany from
1951 to 1996. Global Change Biology,7, 657–666.
2002 O.GORDO&J.J.SANZ
r2006 The Authors
Journal compilation r2006 Blackwell Publishing Ltd, Global Change Biology,12, 1993–2004
Mller AP (2004) Protandry, sexual selection and climate change.
Global Change Biology,10, 2028–2035.
Morel GJ (1973) The Sahel zone as an environment for Palaeartic
migrants. Ibis,115, 413–417.
Mullie
´WC, Brouwer J, Scholte P (1995) Numbers, distribution
and habitat of wintering White Storks in the eastcentral Sahel
in relation to rainfall, food and anthropogenic influences. In:
Proceedings of the International Symposium on the White Stork
(Western Population), Basel Switzerland, 7–10 April 1994 (eds
Biber O, Enggist P, Marti C, Salathe
´T), pp. 219–240. Schwei-
zerische Vogelwarte Sempach, Switzerland.
Nicholson SE (1979) Revised rainfall series for the West African
subtropics. Monthly Weather Review,107, 620–623.
Nicholson SE (2001) Climatic and environmental change in
Africa during the last two centuries. Climate Research,17,
123–144.
Nicholson SE, Davenport ML, Malo AR (1990) A comparison of
the vegetation response to rainfall in the Sahel and east Africa,
using normalized difference vegetation index from NOAA
AVHRR. Climatic Change,17, 209–241.
Parmesan C, Yohe G (2003) A globally coherent fingerprint of
climate change impacts across natural systems. Nature,421,
37–42.
Pen
˜uelas J, Filella I, Comas P (2002) Changed plant and animal
life cycles from 1952 to 2000 in the Mediterranean region.
Global Change Biology,8, 531–544.
Peris S (2003) Feeding in urban refuse dumps: ingestion of plastic
objects by the White Stork (Ciconia ciconia). Ardeola,50, 81–84.
Ptaszyk J, Kosicki J, Sparks TH et al. (2003) Changes in the timing
and pattern of arrival of the white stork (Ciconia ciconia)in
western Poland. Journal fu
¨r Ornitologie,144, 323–329.
Root TL, MacMynowski DP, Mastrandrea MD et al. (2005) Hu-
man-modified temperatures induce species changes: joint
attribution. Proceedings of the National Academy of Sciences
USA,102, 7465–7469.
Root TL, Price JT, Hall KR et al. (2003) Fingerprints of global
warming on wild animals and plants. Nature,421, 57–60.
Sæther BE, Tufto J, Engen S et al. (2000) Population dynamical
consequences of climate change for a small temperate song-
bird. Science,287, 855–856.
Saino N, Sze
´p T, Ambrosini R et al. (2004) Ecological conditions
during winter affect sexual selection and breeding in a mi-
gratory bird. Proceedings of the Royal Society of London, Series B,
271, 681–686.
Samraoui B, Houhamdi M (2002) L’hivernage de la cigogne
blanche Ciconia ciconia en Algerie. Alauda,70, 221–223.
Sanz JJ (2002) Climate change and birds: have their ecological
consequences already been detected in the Mediterranean
region? Ardeola,49, 109–120.
Sanz JJ, Potti J, Moreno J et al. (2003) Climate change and fitness
components of a migratory bird breeding in the Mediterra-
nean region. Global Change Biology,9, 461–472.
Shine T (2003) The conservation status of eastern Mauritania’s
ephemeral wetlands and their role in the migration and
wintering of black storks (Ciconia nigra). Aves,40, 228–240.
Sokolov LV (2000) Spring ambient temperature as an important
factor controlling timing of arrival, breeding, post-fledging
dispersal and breeding success of Pied Flycatchers Ficedula
hypoleuca in Eastern Baltic. Avian Ecology and Behaviour,5,
79–104.
Sokolov LV, Markovets MY, Morozov YG (1999) Long-term
dynamics of the mean date of autumn migration in passerines
on the Courish Spit of the Baltic Sea. Avian Ecology and
Behaviour,2, 1–18.
Sokolov LV, Markovets MY, Shapoval AP et al. (1998) Long-term
trends in the timing of spring migration of passerines on
the Courish Spit of the Baltic Sea. Avian Ecology and Behaviour,
1, 1–21.
Sokolov LV, Payevsky VA (1998) Spring temperatures influence
year-to-year variations in the breeding phenology of passer-
ines on the Courish Spit, eastern Baltic. Avian Ecology and
Behaviour,1, 22–36.
Sparks TH (1999) Phenology and the changing pattern of bird
migration in Britain. International Journal of Biometeorology,42,
134–138.
Sparks TH, Bairlein F, Bojarinova JG et al. (2005) Examining the
total arrival distribution of migratory birds. Global Change
Biology,11, 22–30.
Sparks TH, Braslavska
´O (2001) The effects of temperature,
altitude and latitude on the arrival and departure of the
swallow Hirundo rustica in the Slovak Republic. International
Journal of Biometeorology,45, 212–216.
Sparks TH, Mason CF (2001) Dates of arrivals and departures of
spring migrants taken from Essex Bird Reports 1950–1998.
Essex Bird Report,1999, 154–164.
Sparks TH, Roberts DR, Crick HQP (2001) What is the value of
first arrival dates of spring migrants in phenology? Avian
Ecology and Behaviour,7, 75–85.
StatSoft Inc. (2001) Statistica (data analysis software system),
version 6. www.statsoft.com.
Svensson SE (1985) Effects of changes in tropical environments
on the north European avifauna. Ornis Fennica,62, 56–63.
Tarhule A, Lamb PJ (2003) Climate research and seasonal fore-
casting for West Africans: perceptions, dissemination, and
use? Bulletin of the American Meteorological Society,84, 1741–
1759.
Thauront M, Duquet M (1991) Distribution et conditions d’hi-
vernage de la cigogne blanche Ciconia ciconia au Mali. Alauda,
59, 101–110.
Thomas CD, Lennon JJ (1999) Birds extend their ranges north-
wards. Nature,399, 213–213.
Tortosa FS (1992) Censo invernal de ciguena blanca Ciconia
ciconia en la provincia de Cordoba durante 1989 y 1990.
Oxyura,6, 95–96.
Tortosa FS, Caballero JM, Reyes-Lo
´pez J (2002) Effect of rubbish
dumps on breeding success in the White Stork in southern
Spain. Waterbirds,25, 39–43.
Tortosa FS, Ma
´n
˜ez M, Barcell M (1995) Wintering white storks
(Ciconia ciconia) in South West Spain in the years 1991 and
1992. Die Vogelwarte,38, 41–45.
Tryjanowski P, Ku$niak S, Sparks TH (2002) Earlier arrival of
some farmland migrants in western Poland. Ibis,144, 62–68.
Tryjanowski P, Sparks TH (2001) Is the detection of the first
arrival date of migrating birds influenced by population size?
A case study of the red-backed shrike Lanius collurio.Interna-
tional Journal of Biometeorology,45, 217–219.
BIRD PHENOLOGY AND CLIMATE CHANGE 2003
r2006 The Authors
Journal compilation r2006 Blackwell Publishing Ltd, Global Change Biology,12, 1993–2004
Tucker CJ, Dregne HE, Newcome WW (1991) Expansion and
contraction of the Sahara desert from 1980 to 1990. Science,253,
299–301.
Va
¨ha
¨talo AV, Rainio K, Lehikoinen A et al. (2004) Spring arrival
of birds depends on the North Atlantic Oscillation. Journal of
Avian Biology,35, 210–216.
Van den Bosche W (2002) Eastern European White Stork popula-
tions: migration studies and elaboration of conservation measures.
Bundesamt fu
¨r Naturschutz (BfN)/German Federal Agency
for Nature Conservation, Bonn.
Whitfield J (2001) The budding amateurs. Nature,414, 578–579.
Winstanley D, Spencer R, Williamson K (1974) Where have all
the Whitethroats gone? Bird Study,21, 1–14.
Witt K (2004) Erst-und Letztbeobachtungen des Mauerseglers
(Apus apus) in Berlin. Berliner Ornithologischer Bericht,14,
186–192.
Zalakevicius M, Bartkeviciene G, Raudonikis L et al. (2006)
Spring arrival response to climate change in birds: a case
study from eastern Europe. Journal of Ornithology,147,
326–343.
2004 O.GORDO&J.J.SANZ
r2006 The Authors
Journal compilation r2006 Blackwell Publishing Ltd, Global Change Biology,12, 1993–2004
