CLIMATE RESEARCH
Clim Res
Vol. 54: 95-112, 2012
doi: 10.3354/cr01099
Published online September 12
Drivers of population variability in phenological
responses to climate change in Japanese birds
Osear Gordo!, Hideyuki Doi 2 ,3,'
lDepartment oi Zoology and Physical Anthropology, Complutense University oi Madrid, José Antonio Novais 2,
28040 Madrid, Spain
2Institute ior Chemistry and Biology oi the Marine Environment, Carl von Ossietzky University Oldenburg, Schleusenstrasse 1,
26382 Wilhelmshaven, Germany
3Presenl address: Institute ior Sustainable Sciences and Development, Hiroshima University, 1-3-1 Kagamiyama,
Higashi-Hiroshima, 739-8530 Japan
ABSTRACT: The impact of climate change on the bird communities of Asia is poorly understood.
Sinee lhe 19505, lhe Japanese Meleorology Ageney has recorded !irsl arrival (Le. !irsl sighting)
and first singing for a selection of resident ,:A1auda arvensis, Cettia diphone, and Lanius
bucephalus) and migratory species (Hirundo rustica and Cuculus canorus) in more than 300 bird
populations. Firsl records (Le. !irsl sighting or singing) showa delay 015.4 d sinee lhe end 01 lhe
1 Q70s. Nevertheless, there is él mélrkeo heterogeneity in the temporél 1 trenos élmong populéltions in
each species. Most populations of A. arvensis, C. diphone and H. rustica show a negative relationship with local temperature (Le. first records were earlier in warmer years) and this sensitivity to
temperatures has increased in recent decades. Exploration of the possible causes of variability in
phenological trends among populations demonstrated that greater delays were observed in those
populations subjected to smaHer increases in local temperature and a greater increase in human
population (a surrogate for the conservation status of bird populations). Therefore, declining bird
populations are the most probable cause of the observed delay in the phenology of first individuals. Migratory species were affected by clima te in theirwintering and passage areas. Overall,
first sightings of H. rustica were earlier, while the onset of singing by C. canorus was delayed in
response to warmer temperatures in southeastern Asia. However, there was a noteworthy variability among populations, with no discernable regionalization or spatial organization. This
suggests that there is no clear connectivity between breeding and wintering populations.
KEY WORDS: Arrival dale· Heal island effeel . Long-lerm sludy . Migralory birds . Phenology .
Singing onset . Temperature . Warming
- - - - - - - - - - - R e s a l e or republication not permitted viÍthout lNTitten consent 01 the pubJisher - - - - - - - - - - -
It is widely aeeepled lhal global clima le is ehanging,
and organisms are responding to this change in a variely 01 ways (Parmesan 2006). Mosl 01 lhe evidenee
has be en provided by long-term studies, which usuaHy focus on single or a few populations of one or a
few species. Consequently, there are just one or a few
replica tes for many studies addressing the potential
effect of climate change on organisms. Phenological
studies are an exception. Phenological data are plentiful, and thousands of time series have be en studied
lo dale (Lehikoinen el al. 2004, Menzel el al. 2006,
Rubolini el al. 2007). These sludies demonslrale a
common signal in the life cycles of many organisms
in response to recent changes in climate, especially
temperature increase (Root et al. 2005, Menzel et
al. 2006). Nevertheless, responses to climate change
have an important species-specific component, and
physiology, ecology, or phylogeny may conslrain lhe
*Corresponding author. Email: doih@hiroshima-u.ac.jp
© Inter-Research 2012 . www.int-res.com
1. INTRODUCTION
96
Clim Res 54: 95-112, 2012
observed responses. For instance, Willis et al. (2008)
demonstrated that evolutionary history is essential for
an understanding of flowering time responses of
species in plant communities. Similarly, Gordo &
Sanz (2009, 2010) lound that pollination system is an
important characteristic that influences phenological
trends of flowering dates in Mediterranean ecosystems. Among migratory birds, migratory distance
affects phenological response both in arrival (Tryjanowski et al. 2005, Lehikoinen et al. 2004, T0ttrup et
al. 2006a, Hubálek & Capek 2008, but see Hüppop &
Hüppop 2003) and departure dates (Jenni & Kéry
2003, T0ttrup et al. 2006b, Van Buskirk et al. 2009).
Other traits, such as size, diet, moult or the number of
broods per season, have also been linked to the extent of bird responses to climate change (Jenni & Kéry
2003, Végvári et al. 2010). Buller (2003) also lound
that the advance in arrival dates over the last 100 yr
was related to the habitat used by each species. For
instance, the arrivals of grassland birds were more advanced than those of forest birds, probably beca use of
the uneven effects of clima te change on the trophic
level on which birds 01 each habitat depend (plants
and insects, respectively). Such species-specific phenological responses are more than a mere difference
in the number of days that each species shifts its phenology. Different rates of advance are the most plausible underlying cause for the uneven trends in population numbers observed among migratory bird species
during recent decades (M011er et al. 2008). Those species that are less responsive, such as long-distance
migrants breeding in strongly seasonal habitats, suffer the greatest declines due to increased mismatch
with their environment (Both et al. 2006a, 2010).
While there is now sorne understanding of why
species differ in their responses to climate change,
and of the biological consequences of these differences, almost nothing is known at the population
level (what are the reasons for different responses of
populations belonging to the same species?) or at the
individual level (why are sorne individuals able to
adjust to the new conditions while others are not?).
Studies at intra-specific levels are probably limited
by the scarcity of long-term monitoring data that are
compatible for different populations of the same species. The few that exist include sorne studies of laying
dates of species such as tits Parus spp. (Visser et al.
2003), pied flycatcher Ficedula hypoleuca (Both et al.
2004, 2006b, Both & te Marvelde 2007), and tree
swallow Tachycineta bicolor (Dunn & Winkler 1999).
These studies demonstrated that those populations
subjected to larger increases in local temperatures
show greater advances in their laying phenology.
In the case 01 migratory phenology, the differences
in the passage periods and areas for each population
have been suggested as the origin for the observed
differences in the temporal trends of mean passage
time of birds among ringing stations (Sparks et al.
2005a, Hüppop & Winkel 2006, Jonzén et al. 2006,
T0ttrup et al. 2008). While the number 01 sites with
long-term ringing schemes is extremely reduced,
other measures of migratory phenology, such as the
first arrival date, are plentiful and would allow a
more detailed exploration of variability patterns with
a higher resolution and over larger areas. However,
there are very few studies explaining how and why
arrivals at the breeding grounds by populations of
the same species are advancing at different rates (but
see Forchhammer et al. 2002, Ahas & Aasa 2006).
The heterogeneous nature of monitoring schemes
from each region or country, as well as differences in
the study periods, make comparisons difficult (Gordo
2007a, Miller-Rushing et al. 2008c, but see Rubolini
et al. 2007). Nonetheless, it is 01 paramount importance to disentangle the causes of the observed variability in phenological trends, to understand the extent to which it is due to spatial variability of changes
in climate, to the different abilities of populations to
respond to these changes, or to other factors also
operating in the long-term at local scales and affecting the responses of each particular population.
We propose 3 possible explanations for differences
in phenological trends among populations:
(1) Differences in the magnitude 01 climate change
experienced. The larger the change in clima te over
time, the larger the phenological response expected
(e.g. Both et al. 2004).
(2) Differences in the sensitivity or responsiveness
to climate. Populations more sensitive to clima te
show larger responses in their phenology (e.g. Gordo
& Sanz 2010).
(3) Differences in the population status. Changes
in population abundance affect our ability to detect
the earliest individuals, and consequently long-term
changes in population size may confound trends in
first annual records of any phenologcial event (Tryjanowski & Sparks 2001, Tryjanowski et al. 2005,
Miller-Rushing et al. 2008a,b).
To examine these hypotheses, we studied an exceptional dataset with phenological information on
more than 300 bird populations across Japan. Japan
provides a broad latitudinal range. Bird populations
of widely distributed species in Japan occur from
subtropical clima tes in the south (25 0 N) to hemiboreal ones in the north (45° N). Thus, we can compare
phenological responses to the same event of a certain
Gordo & Doi: Climate change and bird phenology
species across a wide range of environmental conditions (Doi & Takahashi 2008).
Our study also aimed to provide evidence about
phenological responses of birds to clima te change in
the far eastern part of the Asian continent, an area in
which lhis issue has been barely explored (Koike &
Higuchi 2002, Gordo 2007b, Walanuki 2011, Kobori
el al. 2012). In a rece nI sludy 01 planl and animal
phenology in Korea and Japan, Primack el al. (2009b)
explored how phenological matching between trophic
levels may be disrupled by geographical and species-specific variation of phenological responses to
climate. However, the community-Ievel approach
carried out in that study does not allow a comprehensive scrutiny of the phenological responses of the 3
bird species studied. Moreover, as the authors recognized, lhe sludy period (November lo March) was
prabably nol lhe mosl suitable lor lesting lhe effecl 01
temperatures on the phenology of animal species
(Primack el al. 2009b). Periods 01 climale sensitivity
are species-specitic (Doi el al. 2008), consequently,
Primack el al. (2009b) may have underestimaled lhe
aclual effecl 01 lemperalure on lhe phenology 01
birds from Japan and Korea.
Finally, long-distance bird migrants from Japan
provide an opportunity to study the effects of climate
change in a migratory system that has rarely been
studied, the eastern Palearctic. Because western and
eastern populations of Palearctic bird species do not
share passage and wintering areas, they are subjected to different environmental pressures, and it is
important to ascertain the extent to which these promote different phenological responses.
2. DATA AND METHODS
2.1. Phenological dala
The Japanese Meleorological Agency (JMA) monitored the phenology of 5 common bird species belween 1953 and 2005 al 102 sites spread lhraughoul
Japan (Iatilude: 24.33 lo 45.41 'N, longitude: 123.01
lo 145.59' E, altilude: O lo 610 m). Observations 01
plant and animal phenology were carried out daily
by prolessional slaff al each 01 lhe JMA meleorological stations according to standardized protocols
(JMA 1985), which assure high reliabilily and comparability of records among observers. Furthermore,
any change in the monitoring effort, which may
affect species detectability, was improbable, because
sampling prolocols did nol change during lhe sludy
periodo
97
The 'first singing day' for each species was defined
as the first date of the year when the species was
heard singing around the respective JMA station.
This date was examined for the Japanese skylark
Alauda arvensis (subsp. japonica Temminck &
Schlegel, 1848), lhe Japanese bush warbler Cettia
diphone (subsp. cantans Temminck & Schlegel,
1847), the common cuckoo Cuculus canorus (subsp.
subtelephonus Zarudny, 1914), and lhe bul!-headed
shrike Lanius bucephalus (subsp. bucephalus Temminck & Schlegel, 1845). In lhe case 01 lhe tirsl
singing day refers to the higher-tone song used to
defend wintering territories in autumn. The date
when the first barn swallow Hirundo rustica (subsp.
gutturalis Scopoli, 1786) was seen (tirsl arrival dale)
was also recorded. A. arvensis, C. diphone, and
L. bucephalus are resident birds, while H. rustica
and C. canorus are long-distance migrants. Japanese
populations of H. rustica and C. canorus overwinter
in Indochina, Philippines, the Indonesian Archipelago, New Guinea, and even in locations as distant
as Auslralia (Brazil 1991, Fig. Si in lhe supplemenl
al www.inl-res.comlarticles/suppl/c054p095.pdl).Al!
species are common and familiar enough to avoid
misidentification. Dates were transformed into a day
ofyear (DOY) scale (1 = 1 January). In leap years, one
day was added alter February 28.
The validity 01 dala on lhe phenology 01 tirsl individuals has be en strongly criticized due to a number
of potential biases that may be present in these
records (Sparks el al. 2001, Tryjanowski & Sparks
2001, Tryjanowski el al. 2005, Miller-Rushing el al.
2008b). The main drawback 01 recording tirsl individuals is that they may show migratory behaviour
that is unrepresentative of the whole population.
However, each species studied had records for
many Japanese sites per year¡ thus errors or vagueness in sorne records (an unavoidable problem
when working with large dala bases) are offsel by
the large number of samples covering an extensive
geographical area (Gordo & Sanz 2006, Barretl
2011). Ralher lhan a single arrival dale per year, lhe
data shows the distribution of first arrival dates
for each species from southern to northern Japan
each year.
2.2. Climale dala
JMA provided monthly average temperatures
lor each sludy site lor lhe period 1953 lo 2005. We
also gathered monthly temperatures for this period
lram lhe Global Hislorical Climalological Nel-
Clim Res 54: 95-112, 2012
98
work (GHCN) databas e Version 2 (Peterson & Vose
1997, Peterson et al. 1995) lor lOS weather stations
in southeastern Asia (latitude: 10 to 31 e N, longitude:
92 to 125°E), the main wintering and passage area
for the Japanese populations of migratory birds (see
Fig. Si).
2.3. Temporallrends
We divided the study period into 2 sub-periods:
1953-1979 and 1979-2005. We adopted this proeedure beca use temperature did not change steadily
throughout the entire period (Fig. 1). Between 1953
and 1979, temperature did not show any significant
trend, while during the period 1979 to 2005, temperatufe increased markedly, in accordance with global
warming (IPCC 2007). We established the break
point for the phenological time series in 1979 to
obtain 2 equallength sub-periods 0127 yr.
To study the temporal trends 01 bird phenology we
carried out 10 multiple regression models (5 species
x 2 periods). Each model included site as a categorical factor and year as a discrete explanatory variable.
The model was:
Yij = a +ai x Sitei+ セ@ x Yearj+ セゥ@
x Sitei xYearj+ Eij (1)
where Yij is the phenological date of a species recorded in Site i during Year j, ai is the intercept for
r-----------------------------------,28
-0-
Spring
27
-----.- Summer
26
セ@
25
::J
"E
ID
Q.
セ@
E
16
9
24
o
.:'\0
15
o
14
O:,
O
13
1950
1960
1970
1980
1990
2000
2010
Fig. 1. Temporal trends oí spring and summer temperatures
in Japan during 1953 to 2005. Spring: average between February and April¡ summer: average oí August and September.
These were the most important pericx:ls íor the phenology oí
the bird species. Lines: fitted linear regression in each subpericx:l (solid: p < 0.05, dotted: non-significant). Temperature
increased at a similar rate in both seasons during 1979 to
2005 (spring +0.049°C yr- 1, summer +0.045°C yr-l)
Site i, セ@ is the overall slope with Year, セᄀ@ is the slope 01
the fitted Hne to each Site i, and 8ij is the error for
eaeh observed phenologieal date. Therelore, the セ@
parameter determines whether phenological dates
show a significant or non-significant temporal trend
(Le. slope) lor ea eh sub-period and species, while
the interaction between Site and Year determines
whether or not trends differ significantly among populations. We only analyzed time series with records
for at least 20 years during each sub-period, to
reduce potential bias es caused by differences in the
length of the time series. It is important to note that
the average number of records per time series was
25.0 (±2.0 SD) in both sub-periods, Le. most 01 the
time series are complete since 1953.
2.4. Ellecls 01 local lemperalures
To determine the effect of temperature at the study
sites on bird phenology, we built 10 new multiple
regression models including local temperature as a
continuous explanatory variable. Models were:
Yij = a + ai x Sitei + セ@ x Yearj + セゥ@ x Sitei x Yearj +
y x Tempij + Yi x Sitei x Tempij + 8ij
(2)
where the y parameter estima tes the overall effect of
temperature in bird phenology, and the Yi parameters
estimate the particular sensitivity of each population
to temperature. Therefore, the interaction term between Site and Temperature tests for differences in
sensitivity to local temperatures among populations
(Le. heterogeneity 01 the slopes y¡). We included Year
as a covariate in this model to account for its potential
confounding effect on the true relationship between
climate and phenology. Phenology 01 !irst individuals
may show long-term shifts unrelated to climate, e.g.
due to ehanges in population size (Sparks et al. 2001,
Tryjanowski & Sparks 2001, Tryjanowski et al. 2005,
Miller-Rushing et al. 200Sb). Henee, this may give
rise to spurious relationships with climate due to
temporal collinearity.
Temperature values were calculated as the average during the month when a phenological event
occurred and the preceding month at the same JMA
site. We used average temperature values calculated
for a 2 mo period beca use the average standard deviation of phenological dates was 10.1 d, and consequently 95 % of all phenological records of a certain
time series were included in an average range of 40 d
(Le. ±2 SD). Once again, only those time series with
at least 20 records during each sub-period were used
for these models.
Gordo & Doi: Climate change and bird phenology
2.5. Variabilily among populalions
Causes of variability in temporal trends among
populations during 1979-2005 were studied according to the 3 hypotheses proposed in the lntroduction.
We focused on this period, as most of the climate
warming recorded in Japan occurred during this
time (see Fig. 1). Differences in the magnitude of climate change experienced at a local scale were quantified as the increase in temperatures (slope against
year) from 1979-2005 during the 2 mo period adjusted to each population phenology. Differences in
the sensitivity to climate were quantified by the parameterYi (Eq. 2). To quantify the status of bird populations, we used the percentage increase in the number
of inhabitants between the 19S0 and 2005 censuses.
This information was provided by the Statistical
Bureau of the Japanese Ministry of Internal Affairs
and Communications (www.stat.go.jp/index.htm) in
the form of indo km- 2 for each Japanese municipality
(average area of the 102 municipalities covered
by this study = 412 km 2 , range = 2S to 21S7 km 2 ).
Observed changes in the number of people in Japanese municipalities accurately minor landscape transformations at a small scale of a few km 2 in urban ce nters and their peripheries. One may assume that the
environment suffers the greatest impacts in those
areas with the highest numbers of humans (McKinney 2002). Therefore, one expects scarcer availability
and poorer quality of natural habitats at those more
populated sites and consequently smaller populations of wild organisms, including birds (Beissinger &
Osborne 19S2, Mason 2006, Shaw et al. 200S). The
land areas of Japanese cities and towns showed
extraordinary growth during the second half of the
20th century as urban populations increased (Hanis
19S2, Yamada & Tukuoka 1996). Urban sprawl has
caused the deterioration and even disappearance of
natural and traditional Japanese landscapes, dominated by agriculturalland use, in the areas surrounding many cities and towns (Nakamura & Short 2001).
These areas are the main habitats for local populations of birds and where the JMA monitors bird
phenology. In spite of the fact that sorne bird species
tolera te human presence (e.g. Hirundo rustica). We
expect those JMA sites with a grea ter increase in
human population and urban sprawl since 1980
to have a more impacted environment. Therefore,
human population increase can be used as a proxy
for environmental degradation and consequently for
long-term declines in local bird populations.
We carried out a multiple regression model for
each species with phenological trends (values of セゥ@
99
from Eq. 1) as a dependent variable and temporal
trends of local temperatures from 1979 to 2005
(regression slopes of temperatures from each study
site against year), sensitivity to temperature (values
of Yi from Eq. 2), and human population change
between 19S0 and 2005 as explanatory variables.
Residuals from these models were used as response
variables in new multiple regression models, which
included latitude, longitude, and altitude of the study
sites as predictors. The aim of the latter models was
to explore any remaining spatial structure in the residuals of the temporal trends observed in bird phenology (Fig. S2 and Table Si). Quadratic terms of latitude, longitude, and altitude were also included to
account for potential nonlinear spatial gradients
(Legendre & Legendre 1995). We also included the
interaction between latitude and longitude. All spatial predictors were standardized (mean = O, SD = 1)
to avoid scale measurement effects on matrix calculations. The best model was selected according to
Mallow's Cp. Similar to other information criteria,
Mallow's Cp chooses the best subset of predictors
that optimizes the balance between model fit and the
number of variables.
2.6. Migratory species
In the case of Hirundo rustica and Cuculus canorus, we also as ses sed the potential effect of clima te
in wintering and passage areas, because the departure date from wintering grounds and progression
rate through passage areas is affected by weather
and ecological conditions there (Gordo 2007b, Gordo
& Sanz 200S).
All phenological time series with at least 20 records
during 1953-2005 for Hirundo rustica and Cuculus
canorus (S6 and 25 JMA-sites, respectively) were
regressed against the temperature time series of all
the weather stations from southeastern Asia selected
from the GHCN (lOS sites). We used temperature
records for February and March for H. rustica, and
data for March and April for C. canorus. Time series
of both bird phenology and temperatures were detrended prior to implementing the regressions. We
removed temporal trends (Le. year effect was set to O)
to avoid potential spurious relationships due to temporal collinearity between phenological and climatic
time series. For this purpose, all the time series were
regressed against the year and the resulting residuals from these regressions were used in the analyses.
Regression slopes between climate and phenology
were organized in 2 matrices (one for each species),
100
Clim Res 54: 95-112, 2012
where columns were the Japanese populations of
Hirundo rustica or Cuculus canorus and rows the 108
weather stations trom southeastern Asia. Therefore,
each colunm was the sensitivity pattern of one population to the spring temperatures in southeastern
Asia. A Principal Componenl Analysis (PCA) was
applied to each one of the matrices with the Japanese
bird populations (Le. columns) as dependent variables. The aim of these peAs was to summarize aH
sensitivity patterns into a few principal components
(PCs), which could help in idenlifying common palterns of sensitivity among the Japanese populations
of H. rustica and C. canorus. We selected only those
pes with an eigenvalue higher than 5. pe scores
were mapped and visually inspected to detect the
most influential areas in southeastern Asia for bird
phenology. PC loadings provided lhe relalionship 01
each Japanese populalion 10 lhe pallerns depicled by
those PC scores. Therefore, loadings allowed us to
define groups of populations with similar sensitivity
pa tterns to tempera tures in wintering and passage
areas. We modelled the spatial structure of these PC
loadings across Japan using multiple regression
models wilh lalilude, longilude, and allilude 01 phenological sites as predictors and following the same
procedure as previously described. The best model
was selected using Mallow's Cp. The aim of these
models was to determine more reliably whether
Japanese populations with similar sensitivity to temperature in southeastern Asia have a regional distribution pattern in Japan or whether they are randomly distributed across the country.
All statistical analyses were carried out with STATISTICA soflware ISlalSofl, Inc. (2004), version 7.
(www.slalsofl.com)l·
3. RESULTS
3.1. Temporallrends
All species showed different trends between periods
(Fig. 2). During lhe sub-period 1953-1979, !irsl records
of singing males of Alauda arvensis and Cettia diphone were markedly delayed, while !irsl sighlings 01
Hirundo rustica were advanced. The onset of singing
by Cuculus canorus and Lanius bucephalus tended to
advance, but not significantly. With the exception of
C. canorus, all species showed significant differences
in temporal trends among populations (Site x Year
inleraclion: p < 0.00001 in al! cases, Fig. 3).
During lhe more recenl sub-period 1979-2005, al!
species showed a positive relationship with Year, Le.
lhere was an overal! delay in lhe phenology 01 lhe
!irsl individuals (Fig. 2). Neverlheless, lhis delay was
only significant for Hirundo rustica, Cuculus canorus
and Lanius bucephalus. We found strongly significant
differences among populations in all species (Site x
year inleraclion: p < 0.00001 in al! cases, Fig. 3).
In the case of Alauda arvensis and Cettia diphone,
this heterogeneity among populations was especially
marked, Le. there were both significant delays and
advances (Fig. 3), which counlerbalanced each olher
and precluded any statistically significant temporal
lrend lor lhe whole sel 01 popula lions (Fig. 2).
3.2. Ellecl 01 local lemperalures
First individuals of Alauda arvensis, Cettia diphone
and Hirundo rustica were detected earlier in response to warmer springs, while Cuculus canorus
and Lanius bucephalus did not show any relationship
wilh locallemperalures (Table 1). The effecl 01 lemperalure was slronger during 1979-2005 lhan during
1953-1979 in lhose species lhal responded significantly to local temperature, (repeated mea sures
ANOVA: Fl,146 = 6.491, P = 0.012, Fig. 4).
There were significant differences in the sensitivity
to temperatures among populations in sorne species
and sub-periods (Fig. 4). Alauda arvensis, Cettia
diphone and Hirundo rustica showed differences
among populations (Site x Temperature interaction:
p < 0.01 in al! cases) during 1953-1979, whereas
during 1979-2005 only C. diphone slill showed
such heterogeneity (Site x Temperature interaction:
F6s.154s = 1.523, P = 0.004). Differences among populations were due to differences in the steepness of
slopes, Le. the phenology of first individuals was
more advanced in sorne populations than in others in
response to a given temperature increase. Cuculus
canorus and Lanius bucephalus did not show significant differences among populations (Site x Temperature interaction: p > 0.42 in all cases). Therefore, in
these species, the absence of an overall temperature
effect was real and not a result of countervailing patterns among populations.
3.3. Variabilily among populalions
Overall, there were few statistically significant
effects among the selected explanatory variables,
and the explanatory capacity of models was low
(Table 2). Neverlheless, lhe resul1s supporl our predictions. With the exception of Alauda arvensis, tem-
101
Gordo & Doi: Climate change and bird phenology
84
Alauda arvensis
1
セ@
80
76
= 0.208
¡
I
1
11' 1I 11 11
i! 11 1¡
1[[' ¡,III,I' Nャᄀiセ M イhョェヲAᄀ{
M
,¡ 111[111 1 [I¡j¡l¡ 1 I¡ ¡ 1
n = 48 I
72
68
64
I
1
I
60
88
1
セ@
1 = 0032
n = 53
Cettia diphone
84
セ@
al
セ@
80
<D
-E
76
O
セ@
O
72
68
n = 44
64
276
1953
Lanius bucephalus
1969
1985
Year
2001
272
268
264
260
256
1953
1969
1985
2001
Fig. 2. Day oí year (1 = 1 January) oí bird phenology during 1953-2005. Error bars show the standard error oí annual means. The estimate íor the year effect írom the multiple regression models (13 in Eq. 1) and the number oí
time series used (n) during each sub-period are shown. A
solid (p < 0.05) or dotted (non-signiíicant) line represents
fue estimated 13
Year
paral trends in local temperature during 1979-2005
had a negative effect. This variable was non-significant in A. arvensis, while in the other species p-values were low (Table 2). Therelare, the larger the
recorded warming during 1979-2005, the larger the
advance in population phenology. Sensitivity to temperature did not show any significant effect. This
result is not surprising if one takes into account that
there were no differences in Yi among populations
except in the case of Cettia diphone. In agreement
with our hypothesis, those bird populations from sites
with the largest increases in human population
showed the greatest delays in their first singing or
arrival dates. Changes in human population numbers
that oeeurred sinee 1980 at the study siles had a significant positive effect on the phenology of A. arvensis and C. diphone (Table 2). This variable also had a
marginal positive effect in Hirundo rustica.
The amount of variability in temporal trends
accounted for in significant models ranged from 13 to
22 % (Table 2). Those species wilh the weakest models (Hirundo rusticaa, Cuculus canorus and Lanius
bucephalus) showed significant spatial gradients in
their residuals (see Fig. S2 and Table Si in the supplement). This suggests that part 01 the variability
among populations is due to the location of the study
site. For instance, delays in first arrival dates were
especially marked in southern populations of H.
rustica, while trends in singing onset dates of L.
bucephaluswere increasingly delayed along a southwestern to northeastern axis (see Fig. 3). In the case
of C. canorus, a second order polynomial of longitude
accounted for more than 60 % of variability in the
residuals of first singing dates. Populations located in
the eastern and western extremes of the distribution
in Japan showed the largest delays in the singing
Clim Res 54: 95-112,2012
102
A. arvensis
C. diphone
C. canorus
H. rustica
L. bucephalus
•
,
4'
4'
)
;j
··
®
N
セ@
.,
..
4'
··
4'
)
)
•
•
セ@
.
.,
4'
セ@
)
セ@
..
"
Trend
(d yr- 1)
'.
'. 4'
·,
'.
'.
'. 4'
.
.,
' 4'
·
·
.,
)
)
,
,
..
,
•
.
'. 4'
'{
..
セ@
セ@
"
•
セ@
<-1.00
•
•
- 0.75
- 0.50
- 0.25
0.00
0.25
0.50
0.75
>1.00
j •·
)
•
.
セ@
•••
•
Fig. 3. Temporal !rends 01 bird phenology during 1953-1979 and 1979-2005. Each do! is a site. FuI! species na mes in Fig. 2
Gordo & Doi: Climate change and bird phenology
A. arvensis
c.
diphone
103
C. canorus
H. rustica
L. bucephalus
•
•
,·
}·
®
N
.,1
,
,
.··
,
.-
··
}
Nセ@
}
セ@
.,1
•
.-·
,-.
}
·
.,1
.,1
•
Sensitivity
(d °C-1)
.\
,
.-.
.·
N セ@
...-·
'.
'.
.,1
...-·
'.
[セ@
}
.,1
,
セ@
•セ@
•
.". 0
,
'.
'.
•
.
.-.
·
,
.
'. 4'
)
}
J
.,1
•
<- 7.6
•
•
- 5.7
- 3.8
-1 .9
0.0
1.9
3.8
5.7
>7.6
•
•••
•
Fig. 4. Sensitivity 01 bird phenology to local temperatures during 1953-1979 and 1979-2005. Each dot is a site. FuI! species
names in Fig. 2
Clim Res 54: 95-112, 2012
104
Table 1. Results for multiple regression models oí fue phenology oí 5 cornmonly occurring migrant and resident bird species
in Japan, with local temperature and year as continuous explanatory variables and the Japan Meteorological Agency
(JMA) site as a categorical factor (see Eq. 2 in 'Data and methods'). Parameter estimates for temperature (r) and year (13)
Species
Temperature
r
p
1953-1919
Alauda arvensis
-2.317 <0.001
-2.856 <0.001
Cettia diphone
-1.964 <0.001
Hirundo rustica
-0.138
Cuculus canOHlS
0.692
Lanius bucephalus 0.373
0.383
1919-2005
Alauda arvensis
-2.756 <0.001
-3.906 <0.001
-2.193 <0.001
Hirundo rustica
Cuculus canOHlS
0.228
0.319
Lanius bucephalus 0.511
0.134
Cettia diphone
Table 3. Hirundo rustica and Cuculus canorus. Results oí the
principal component analysis (PCA) oí the sensitivity oí
populations to spring temperatures in southeastern Asia.
Eigenvalue (Eigenv.) and cumulative percentage oí variance
accollllted íor (Cum %) shown íor selected principal components (PC)
pe
Year
セ@
p
0.174
0.143
-0.116
-0.014
-0.071
0.013
0.038
0.001
0.701
0.219
0.175
0.023
0.244 <0.001
0.298 <0.001
0.136
0.005
0.190
0.012
0.854
0.735
0.668
0.399
0.559
0.847
0.843
0.715
0.473
0.502
onset date. However, note the small sample size for
this species and the weak temporal trends in its populalions (Figs. 3 & S2, Table Si). In sharl, lhose spedes weakly affected by variables sueh as local
ehanges in tempera ture, sensitivity to tempera ture,
and human population ehange showed sorne geographical regionalization in the temporal trends in
lhe phenology 01 lheir !irsl individuals.
3.4. Migratory species
We lound 5 PCs wilh an eigenvalue > 5 in lhe PCA
for Hirundo rustica. The first 5 PCs aeeounted for
almost 66 % of variability in patterns of sensitivity to
temperatures in southeastern Asia both in February
and March (Table 3). PCi depicls 2 areas wilh opposite effeets of temperature on H. rustica arrival dates.
Temperatures on the eoast of China had negative
seores, while in the remaining areas from Thailand to
Indonesia and the Philippines, temperatures had
positive seores. This pattern was important for many
1
2
3
4
5
Hirundo rustica
Eigenv.
Cum%
19.82
14.24
8.69
7.61
6.23
Cuculus canorus
Eigenv.
Cum%
8.20
32.81
23.04
39.60
49.70
58.55
65.79
populalions, as lhe large magnilude 01 lhe loadings
demonslraled (Fig. 5). However, loadings lar populations breeding in eastern prefeetures of Honshu
(Japan's largesl island) were mainly negalive, while
in western prefeetures loadings were positive. In
eastern populations (negative loadings), H. rustica
advaneed its arrival in response to high tempera tures
in the area from Thailand to Indonesia and the
Philippines, while warmer temperatures in China
delayed arrivals. However, Japanese populations of
H. rustica breeding in western regions oí the country
(posilive loadings) had lhe opposile response 10 climatie eonditions in southeastern Asia. Their arrival
was advaneed in response to high temperatures in
China during February and March, bul delayed in
response to warm springs in the rest of southeastern
Asia. This was con!irmed by a spalial model (Table 4).
Its explanatory eapacity was low, but it had a markedly significant negative gradient from the southwest to the northeast of Japan. Loadings were more
negative in northeastern populations.
PC2 in Hirundo rustica showed a marked effeet of
climate in the Philippines, northern Borneo, eastern
Java and Timor. Other regions of southeastern Asia
also showed notable seores, but there were no obvious spatial patterns. The overwhelming majority of
Japanese populalions had negalive loadings, al1hough
Table 2. Results oí multiple regression models oí inter-site variability oí temporal trends in bird phenology in Japan¡ p: significance of the model
Species
Alauda anrensis
Cettia diphone
Hirundo rustica
Cuculus canorus
Lanius bucephalus
Temperature trend
p
セ@
0.260
-1.024
-0.444
-0.613
-0.975
0.472
0.009
0.026
0.111
0.092
Sensitivity to temperature
p
セ@
-0.052
-0.016
0.041
0.016
0.054
0.112
0.491
0.080
0.799
0.189
Change in human population
p
セ@
0.0146
Om05
0.0039
-0.0013
0.0031
0.002
0.004
0.085
0.767
0.615
R2
p
0.223
0.212
0.128
0.185
0.091
0.007
0.003
0.029
0.398
0.301
Gordo & Doi: Climate change and bird phenology
PC 1
105
PC4
•
:(
.,
.)
®
®
N
N
PC 5
,
'. f
•
.,
•
Nセ@
.•
セ@
Scores <-2 .0
- 1.0
0.0
1.0
>2.0
Loadings <-0.7
-0.35
0.0
0.35
>0.7
•••••••••• •••••••
'f
.'
•
•
Fig. 5. Hirundo rustica. Principal Component Analysis (PCA)
of sensitivity (d OC- 1 ) of migratory phenology to temperatures in southeastern Asia during February-March. PC
scores for the 108 weather stations from the Global Historical Climatological Network (GHCN) used in the present
study are represented by dots on the maps of southeastern
Asia. PC loadings for the Japanese bird populations are
shown by dots on the maps of Japan
Clim Res 54: 95-112, 2012
106
Table 4. Hirundo rustica and Cuculus canorus. Results of spatial models for principal component (PC) loadings. Parameter
estimates (b) and their significan ce (p) are shown only for those variables included in the best model selected according to the
lowest value of the Mallow's Cp. In the lower part of the table, the explanatory capacity (R 2 ), F-statistic (F), degrees of freedom
(df) and significan ce (p) of the model are shown
Variable
PCl
b
Latitude
Longitude
Latitude 2
Longitude 2
Lat x Long
Altitude
Altitude 2
R2
F
df
P
1.298
-1.320
0.135
6.481
2, 83
0.002
PC2
P
b
P
H. rustica
PC3
b
P
C. canorus
PC4
b
PC5
P
b
PCl
P
0.001
0.001
1.391
0.596
-1.946
-0.149
0.189
0.186
3.644
5, 80
0.005
0.004
0.001
0.002
0.118
0.045
-0.152
0.204
0.071
0.016
-0.09
-0.045
0.079
3.570
2, 83
0.033
they were of great magnitude only in sorne populations from central regions of Honshu. This PC
accounted for only 14 % of variance. Therefore,
this PC summarized correlation patterns for few
J apanese populations. These populations were characterized by delayed arrivals under warmer temperatures in the Philippines, Java or Timor, and advanced
arrivals under warmer temperatures in Borneo or
northern China. Loadings for this PC showed several
significant spatial gradients (Table 4). Significant
quadratic latitudinal and longitudinal gradients suggested that largest loadings occur at mid-Iatitudes
and mid-Iongitudes (Le. in central Japan). Similar
to PC1, there was also a marked negative gradient
from southwest to northeast. Altitude was of minor
importance.
PCs 3, 4 and 5 together accounted for just 26 % of
variance (Table 3). Each of these PCs summarized
sensitivity patterns representative for a few populations (se e small magnitude of loadings in Fig. 5). In all
cases, climate in China had very low importance (low
scores), while climate in other areas in southeastern
Asia was the most important factor. Nevertheless, the
effect of climate in these areas was variable. In PC3,
there were markedly negative scores in the Malay
Peninsula. In PC4, the Philippines and northern stations in Myanmar had positive scores, while most
of the other stations had negative values. Finally, in
PC5, regions from the Malay Peninsula to northern
Laos and Myanmar had again positive scores, while
the Philippines showed negative score. Spatial modeIs for PC loadings were weak or even nonexistent
(Table 4). This fact can be interpreted as further proof
that the sensitivity patterns depicted by these PCs are
only representative of a few Japanese populations.
0.002
b
P
8.045
0.072
1.658
-9.541
0.109
0.077
0.165
0.023
1.958
1, 84
0.165
0.110
10.43
1, 84
0.002
0.237
2.170
3,21
0.122
PCA for Cuculus canorus provided only one PC
with an eigenvalue >5. However, this PC accounted
for almost 33 % of variance (Table 3). Scores showed
2 regions in southeastern Asia with an opposite influence on the onset of singing dates of C. canorus
(Fig. 6). The northern coast of China (near Shanghai)
and the Philippines had positive scores, while the
®
N
セ@
Scores
<-2 .0
®
N
-1 .0 0.0 1.0 >2.0
•••••••• •••••••••
Loadings <-0.7 -0.350 .0 0.35 >0.7
Fig. 6. Cuculus canorus. Principal Component Analysis
(PCA) of sensitivity (d OC- 1) of migratory phenology to temperatures in southeastern Asia during March-April. PC
scores for the 108 weather stations from the Global Historical Climatological Network (GHCN) used in the present
study are represented by dots on the map of southeastern
Asia. PC loadings for the Japanese bird populations are
shown by dots on the map of Japan
Gordo & Doi: Climate change and bird phenology
region from the Malay Peninsula to Timor had negative scores. Loadings were negative and high in all
populalions. Thus, al! populalions had similar palterns of sensitivity to climate in southeastern Asia.
Taking the negative sign of loadings into account, we
found that warm springs in the Philippines and China
are related to earlier singing onset of C. canorus in
Japan, while warm springs in the Malay Peninsula
and equatorial regions of Indonesia were related to
a delay in lhe onsel 01 singing. Loadings lor lhe C.
canorus did not show any statisticaHy significant
spalial slruclure (Table 4).
In summary, temperature from southeastern Asia
had effects on Hirundo rustica and Cuculus canorus
phenology, bul such e!fecls varied regional!y. Palterns of sensitivity were much more diverse in H. rustica than in C. canorus, as the larger number of relevant PCs and heterogeneity of loading signs among
populations demonstrated.
4. DISCUSSION
4.1. Trends in bird phenology
Recorded dates of the first singing and arrival of
migrant individuals during the spring in Japanese
bird populations have not shown an advance in
recent decades. This suggests that other factors operating on a long-term temporal scale are controlling
phenological responses. For instance, Alauda arvensis, Cettia diphone and Hirundo rustica had earlier
records in warm years, but none of these species
showed a consistent tendency of advanced arrivals
in recent decades, in spite of the notable increase in
lemperalures in Japan (see Fig. 1). This result is
interesting, as the spring phenology of populations
of A. arvensis and H. rustica from the western Palearctic is indeed advancing in response to similar
increases in temperatures (Tryjanowski et al. 2002,
Buller 2003, Collon 2003, Peinlinger & Schusler
2005, Ahas & Aasa 2006, Croxlon el al. 2006, Gordo
& Sanz 2006, Zalakevicius el al. 2006, Askeyev el al.
2009, Barrell 2011, Eddowes 2011, Sepp el al. 2011).
One may obtain evidence for a hidden driver of
bird phenology by comparing lhe year e!fecl HセI@
in
models with (Eq. 2) and withoul (Eq. 1) lemperalure.
AH species showed marked and significant delays
(see セ@ in Table 1) when lhe e!fecl 01 lemperalure was
isolated. First records of Alauda arvensis, Cettia
diphone and Hirundo rustica are actually advancing
in response to warmer local temperatures: the difference belween lhe observed (see Fig. 2) and lhe lalenl
107
lemporal lrend (see Table 1) was -0.143, -0.191, and
-0.109 d yc 1, respectively. However, such an advance
promoted by warmer temperatures in Japan was not
enough lo lul!y counlerbalance lhe lalenl delay and,
as a result, A. arvensis and C. diphone did not show
any temporal trend and first arrivals of H. rustica
were even delayed. In the case of Cuculus canorus
and Lanius bucephalus, observed and expected (Le.
lalenl) changes in phenology were lhe same. These
species were not affected by local temperature and
consequently, this did not counterbalance their latent
delay. Neverlheless, L. bucephalus phenology was
studied during autumn, and its singing activity during this sea son cannot be interpreted in the same
way as the the onset of singing in spring. L. bucephaJus phenology was posilively (bul non -significanlly)
related to temperatures during August and September; therefore a delay in the onset of its singing is
expected as a response to warmer temperatures.
Moreover, L. bucephalus is a double-brooded species (Lelranc & Worlolk 1997) and consequenlly its
breeding sea son finishes at the end of the summer.
The beginning of the defence of winter territories is
probably driven by lhe end 01 lhe breeding sea son,
which is in turn affected by weather conditions in
la te summer.
Whal is lhis hidden driver lhal is able lo modily lhe
expected advance of first singing and arrival dates in
response to warmer temperatures in Japan? Extreme
dates of any phenological distribution are sensitive
lo changes in populalion size (Miller-Rushing el al.
2008). For instance, earliest migrants arrive later in
cases 01 bird populalion decline (Sparks el al. 2001,
Tryjanowski & Sparks 2001, 2005, Miller-Rushing el
al. 2008b, Eddowes 2011). We did nol have sufficienl
information regarding population dynamics of the
bird species at our study sites to determine how population changes have affected the detection of first
individuals. However, we had indirect evidence that
population declines were the most plausible origin
lor lhe lalenl delay 01 phenology. In lhe case 01
Alauda arvensis, Cettia diphone and Hirundo rustica, greater delays were detected in those bird populations from sites that have experienced a greater
increase in the number of human inhabitants; A.
arvensis and C. diphone, the species most affected by
changes in human populalion, had lhe grealesl delay
belween lhe observed and lhe lalenl phenology. Furthermore, both species are resident and as a consequence they must endure anthropogenic habitat
degradation resulting year round. Therefore, it is
possible that those bird populations located at more
heavily human-populated sites have also suffered
108
Clim Res 54: 95-112, 2012
lhe grealesl declines in lheir numbers (Doi 2008).
Our hypothesis agrees with empirical evidence of
declines in bird communities, especially in long-distance migrants, reported for sorne regions of Japan
(Brazil 1991, Hirano 1996, Higuchi & Morishila 1999,
Ozaki el al. 2002, Tamada 2006). In Korea, H. rustica
has also shown marked delays in the arrival of their
first individuals and there is indirect evidence of a
severe decline in their populations in recent decades
(Lee el al. 2011).
4.2. Variabilily among populalion
Temporal lrends differed markedly among populations during recent decades. Good examples of this
are Alauda arvensis and Cettia diphone, which did
not show any temporal trend in their phenology over
lhe period since 1979 as a whole (see Fig. 2). However, many of their populations are indeed shifting
lheir phenology, bul in opposile direclions (see
Fig. 3). Spalial differences in lhe phenological responses of the Japanese populations of plants and
animals have aIready be en demonstrated (Matsumolo el al. 2003, Doi 2008, Doi & Takahashi 2008,
Primack et al. 200gb, Ibáñez et al. 2010), but the environmental/biological causes for such variability
among sites remains poorly understood (but see Doi
el al. 2010). We praposed 3 polenlial causes lor lhe
observed heterogeneity among populations: climate
change at a local scale, sensitivity to clima te, and
population size trends (see Introduction). Sensitivity
to clima te was the only hypothesis with no empirical
suppor1. In lacl, populalions did nol differ significantly in their sensitivity to local temperatures in
most cases. Nevertheless, we detected an increase in
sensitivity during recent decades in populations of A.
arvensis, C. diphone and Hirundo rustica, Le. the
phenology of these species shows greater sensitivity
in response to a given increase in temperature than it
did several decades ago. This phenomenon has also
been reported in a few other populations of birds
(Sparks & Tryjanowski 2007, Askeyev el al. 2009)
and planls (Sparks el al. 2009) and may help species
to deal with climate change challenges by reacting
more strongly to increases in temperature.
In agreement with our prediction, those populations subjected to the greatest increase in local temperatures showed the greatest advance in phenology. Temperature increased faster at those sites with
a grealer human popula!ion (see Fig. SS) due 10 lhe
urban he al island effecl (Karl el al. 1988, Hua el al.
2008). Therelore, lhe lemporal lrends 01 lempera-
tures in Japan shown in Fig. 1 are probably overestimated, as we used a sample ofweather stations from
the JMA tha t are loca ted only in towns and cities,
where the heat island effect is more pronounced
(Primack el al. 2009a). Neverlheless, lemperalure
has markedly increased on a local scale at our study
sites, whatever the cause, and the local scale is the
most relevant one for bird biology. Therefore, bird
populalions may be doubly jeopardized by development of human society in Japan. Gn the one
hand, human population growth and urban sprawl
are reducing the quality and availability of natural
habilals (Nakamura & Shorl 2001, Noda & Yamaguchi 2008), and as a consequence bird communities
are declining (Sugimura el al. 2003, Tamada 2006).
As we showed, latent delays observed in all species
are probably evidence of declining bird populations
acrass lhe counlry (Doi 2008, Lee el al. 2011). On lhe
other hand, urban sprawl is enhancing temperature
increases at a local scale via the heat island effect,
and birds are facing especially large increases in
temperatures. These are causing steep advances in
spring phenology at lower trophic levels, such as in
plants or insects, at the same localities (Matsumoto et
al. 2003, Doi 2007, MilIer-Rushing el al. 2007, Doi &
Kalano 2008, Doi el al. 2008, Primack el al. 2009a,b).
Therefore, if the observed shifts in first singing or
arrival dates are representative of the entire popula!ion phenology, Japanese bird populalions may be
suffering from an increasing phenological mismatch
with their environment during the breeding period
(Primack el al. 2009b). In lhe parlicular case 01 Cuculus canorus, such phenological mismatching could
be especially hazardous beca use it could affect interactions with host species.
The magnitude of temperature and population size
effects was small and accounted for only a small part
of the variability among populations. Japan provides
an enormous geographical range from south to north,
bul il may sliII be insufficienllo delecl marked differences among populations. For instance, the warming
rate detected in our study sites during the period
1979 10 2005 ranged lram +0.01 10 +0.07 ce ye !
(Fig. S3), while in a sludy 01 laying phenology in
Eurapean populalions 01 lhe pied fIycalcher during a
similar period temperature shifts ranged between
-0.11 and +0.17 ce ye ! (Bolh el al. 2004). Similarly,
changes in human population abundance and their
expected consequences for bird populations may
only have deleclable effecls beyond sorne lhreshold
01 severily (Lee el al. 2011). Abundanl and 10 sorne
extent human-tolerant populations, such as the species studied here, may buffer small and modera te
Gordo & Doi: Climate change and bird phenology
population declines without showing an appreciable
e!fecl on lheir phenology. Finally, one may argue lhal
observable variability among sites is simply random
noise as a result of the inaccurate nature of phenological mea sures, such as first arrivals or the onset of
singing. However, the latter hypothesis is not supported by our results. Residuals showed notable spatial gradients, especially in those species without a
significant model (Le. Cuculus canorus and Lanius
bucephalus, see Fig. S2 and Table Si). Therelore, in
sorne regions of Japan, the phenology of populations
advanced (or delayed) more lhan would be expecled
by chanceo
Another important difference between the species
was the effect of clima te itself. While arrivals of many
populations of Hirundo rustica were advanced in
response to warmer temperatures in southeastern
Asia, arrivals of Cuculus canorus tended to be
delayed. The response of H. rustica concurs with
the advancement of arrivals observed in Western
Palearctic populations under warmer temperatures
en TOute (Huin & Sparks 1998, Zalakevicius el al.
2006, Sparks & Tryjanowski 2007, Gordo & Sanz
2008) and suggesls lhal clima le a!fecls populations in
both migratory systems of H. rustica in a similar way.
H. rustica is an airborne feeder, and warm years are
probably related to improved foraging conditions
during migration. However, despite a temperature
increase of about 0.5°C across southeastern Asia
since lhe 19705 (IPCC 2007), !irsl individuals arrived
later in Japan. Hence, the hypothesis of a decline in
population size is also supported by these results.
Such a decline has be en reported for sorne longdistance migrants, probably also as a result of degradation 01 lhe winlering habitals (Higuchi & Morishita
1999, Lee el al. 2011). For inslance, C. canorus has
recently disappeared in sorne areas of Japan
(Tamada 2006). In Britain, sorne populations 01 lhis
species also show delayed phenology, and population declines have been suggested as the most probable cause (Sparks el al. 2005b, Croxlon el al. 2006).
However, lhe phenology 01 Japanese populations 01
C. canorus was positively related to temperatures in
sorne areas of southeastern Asia; thus the arrival of
this species could be delayed in response to warmer
temperatures in its wintering area.
4.3. Asian populalions 01 migratory birds
Hirundo rustica and Cuculus canorus offered a
unique opportunity to examine bird phenology responses to climate in wintering and passage areas in
the Asian migratory system. In agreement with previous studies from the western Palearctic (Cotton
2003, Gordo el al. 2005, Rodriguez-Teijeiro el al.
2005, Hüppop & Winkel 2006, Jonzén el al. 2006,
Gordo & Sanz 2006, Zalakevicius el al. 2006, Saino
et al. 2007), climate in wintering and passage areas
affected arrival dates. Passage areas on the coast of
China showed generally smaller effects than the rest
01 lhe regions in soulheaslern Asia (Figs. 5 & 6). This
suggests lesser sensitivity to climate en route than to
climate from departure areas in Indonesia, Malaysia
or lhe Philippines. An alternative hypolhesis is lhal
Japanese populations make a direct flight from wintering areas to Japan over the sea, since recoveries
on the Chinese coast are uncommon (see Fig. S1).
Furthermore, the Pacific Ocean is covered by many
islands and archipelagos from Australia to Japan and
thus, migratory species have ample opportunity to
land and stop-over.
Cuculus canorus showed a much more homogeneous response to climate in southeastern Asia
among populations than Hirundo rusticaa. We suggesl 2 hypolheses. (1) Di!ferences could be jusI a
matter of sample size. The number of populations
for H. rustica was larger than for C. canorus (86 vs.
25 sites) and lhus, lhere was more variability. (2)
Differences between species indica te 2 different
strategies during the winter. In the case of H. rustica, individuals would spread throughout all of
southeastern Asia, while Japanese populations of C.
canorus would concentra te on the Malay Peninsula.
Our results do not unambiguously support one or
lhe olher.
109
Acknowledgements. We fuank fue Japan Meteorological
Agency for collecting phenological and climate data over so
many decades and 4 anonymous reviewers for fueir comments. O.G. received a Juan de la Cierva grant (JCI-2oo905274). H.D. thanks the Aquatic Restoration Research Center, Japan, for helping him while writing fue paper. Fllllding
was provided by fue Japan Society for fue Promotion of Science to H.D.
LITERATURE CITED
)o-
)o-
)o-
Ahas R, Aasa A (2006) The effects of climate change on the
phenology of selected Estonian plant, bird and fish populations. Int J BiometeoroI51:17-26
Askeyev OV, Sparks TH, Askeyev IV (2009) Earliest recorded Tatarstan skylark in 2008: non-linear response
to temperature suggests advances in arrival dates may
accelerate. Clim Res 38:189-192
Barrett RT (2011) Recent response to climate change among
migrant birds in northern Norway. Ring Migr 26:83-93
Beissinger SR, Osborne DR (1982) Effects of urbanization
on avian cornmurrity organization. Condor 84:75-83
110
Clim Res 54: 95-112, 2012
>- Both C, te Marvelde L (2007) Spatial and temporal variatian >- Gordo O,
>>-
>-
>>-
>>>>>>>-
>-
in climate change and their effects on timing oí avian
breeding and migratian throughout Europe. Clim Res 35:
93-105
Both C, Artemyev AA, Blaauw B, Cowie RJ, and others
(2004) Large-scale geographical variatian confirms that
climate change causes birds to lay earlier. Proc Biol Sci
27U657-1662
Both C, Bouwhuis Sr Lessells CM, Visser ME (2006a) Climate change and population declines in a long-distance
migratory bird. Nature 441:81-83
Both C, Sanz JJ, Artemyev AA, Blaauw B, and others
(2006b) Pied Flycatchers Ficedula hypoleuca travelling
from Africa to breed in Europe: differential effects oí
winter and migratian conditions on breeding date. Ardea
94,511-525
Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van
Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for longdistance migrants in seasonal habitats. Proc Biol Sci 277:
1259-1266
Brazil MA (1991) The birds of Japan. Christopher Helm,
London
Butler CJ (2003) The disproportionate effect of global warming on fue arrival dates of short-distance migratory birds
in Norfu America. Ibis 145:484-495
CoUon PA (2003) Avian migration phenology and global climate change. Proc Natl Acad Sci USA 100:12219-12222
Croxton PJ, Sparks TH, Cade M, Loxton RG (2006) Trends
and temperature effects in the arrival of spring migrants
in Portland (United Kingdom) 1959-2005. Acta Ornifuol
4U03-111
Doi H (2007) Winter flowering phenology of Japanese apricot Prunus mume reflects climate change across Japan.
Clim Res 34:99-104
Doi H (2008) Delayed phenological timing of dragonfly
emergence in Japan over five decades. Biol LeU 4:
388-391
Doi H, Katano I (2008) Phenological timings of leaf budburst
wifu climate change in Japan. Agric For Meteorol 148:
512-516
Doi H, Takahashi M (2008) Latitudinal patterns in the phenological responses of leaf colouring and leaf fall to climate change in Japan. Glob Ecol Biogeogr 17:556-561
Doi H, Gordo O, Katano 1 (2008) Heterogeneous intraammal climatic changes drive different phenological responses at two trophic levels. Clim Res 36: 181-190
Doi H, Takahashi M, Katano I (2010) Genetic diversity increases regional variation in phenological dates in response to climate change. Glob Change Biol 16:373-379
Dwm PO, Winkler DW (1999) Climate change has affected
fue breeding date of tree swallows throughout North
America. Proc Biol Sci 266:2487-2490
Eddowes MJ (2011) Longer term trends in arrival timing of
long distance migrants: the influence of ablllldance and
population change. Ring Migr 26:56-63
Forchhammer MC, Post E, Stenseth NC (2002) NorfuAtlantic
Oscillation timing of long- and short-distance migration.
J Anim Eco17U002-1014
Gordo O (2oo7a) Does climate change affect cornmon swift
Apus apus migratory phenology? APUSlist 3237. www.
cornmonswift.org/3237Gordo.htrnl
Gordo O (2007b) Why are bird migration dates shifting? A
review of weather and climate effects on avian migratory
phenology. Clim Res 35:37-58
>>>>>-
>-
>>>-
>-
>>-
Sanz JJ (2006) Climate change and bird phenology: a long-term study in the Iberian Peninsula. Glob
Change BioI12:1993-2004
Gordo O, Sanz JJ (2008) The relative importance of conditions in wintering and passage areas on spring arrival
dates: fue case of long-distance Iberian migrants.
J OrnithoI149,199-210
Gordo O, Sanz JJ (2009) Long-term temporal changes of
plant phenology in fue Western Mediterranean. Glob
Change BioI15:1930-1948
Gordo O, Sanz JJ (2010) Impact of climate change on plant
phenology in Mediterranean ecosystems. Glob Change
BioI16,1082-1106
Gordo O, Brotons L, Ferrer X, Comas P (2005) Do changes in
climate paUerns in wintering areas affect the timing of
the spring arrival of trans-Saharan migrant birds? Glob
Change Biol11:12-21
Harris CD (1982) The urban and industrial transformation of
Japan. Geogr Rev 72:50-89
Higuchi H, Morishita E (1999) Population declines of tropical migratory birds in Japan. Actinia 12:51-59
Hirano T (1996) Changes in breeding avifalllla during the
past 25 years at Tomatsuriyama in Utsllllomiya City,
central Japan. Strix 14:25-31 [in Japanese 1
Hua LJ, Ma ZG, Guo WD (2008) The impact of urbanization
on air temperature across China. Theor Appl Climatol
93,179-194
Hubálek Z, Capek M (2008) Migration distance and the
effect of North Atlantic Oscillation on the spring arrival
of birds in central Europe. Folia Zool (Brno) 57:212-220
Huin N, Sparks TH (1998) Arrival and progression of the
swallow Hirundo rustica through Britain. Bird Study 45:
361-370
Hüppop O, Hüppop K (2003) Norfu Atlantic Oscillation and
timing of spring migration in birds. Proc Biol Sci 270:
233-240
Hüppop O, Winkel W (2006) Climate change and timing of
spring migration in the long-distance migrant Ficedula
hypoleuca in central Europe: fue role of spatially different
temperature changes along migration routes. J Ornifuol
147,344-353
Kobori H, Kamamoto T, Nomura H, Oka K. Primack RB
(2012) The effects of climate change on the phenology of
winter birds in Yokohama, Japan. Ecol Res 27:173-180
Ibánez 1, Primack RB, Miller-Rushing AJ, Ellwooo E and others (2010) Forecasting phenology llllder global warming.
Phil Trans R Soc B 365:3247-3260
IPCC (Intergovernmental Panel on Climate Change ) (2007)
Climate Change 2007: fue Physical Science Basis. Contribution of Working Group I to the Fourth Assessment
Report of fue Intergovernmental Panel on Climate Change.
Cambridge University Press, Cambridge
Jenni L, Kéry M (2003) Timing of autumn bird migration
llllder climate change: advancesinlong-distance migrants,
delays in short-distance migrants. Proc R Soc Lond B 270:
1467-1471
JMA (Japan Meteorological Agency) (1985) Guidelines for
the observation of phenology, 3rd edn. Japan Meteorological Agency, Tokyo [in Japanese 1
Jonzén N, lindén A, Ergon T, Knudsen E, and others (2006)
Rapid advance of spring arrival dates in long-distance
migratory birds. Science 312: 1959-1961
Karl TR, Diaz HF, Kukla G (1988) Urbanization: its detection
and effect in the United States climate record. J Clim
UQ99-1123
Gordo & Doi: Climate change and bird phenology
>- Koike
>-
>>>>>>>>>>>-
>-
>>-
S, Higuchi H (2002) Long-term trends in the egg
laying date and clutch size of red-cheeked starlings Sturma plillippensis. Ibis 144: 150-152
Lee SD, Ellwood ER, Park SY, Primack RB (2011) Latearriving barn swallows linked to population declines.
Biol Conserv 144:2182-2187
Lefranc N, Worfolk T (1997) Shrikes. A guide to the shrikes
of the world. Pica Press, Robertsbridge, UK
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn.
EIsevier, Amsterdam
Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and
departure dates. Adv Ecol Res 35:1-31
Mason CF (2006) Avian species richness and numbers in the
built environment: can new housing developments be
good for birds? Biol Conserv 15:2365-2378
Matsumoto K. Ohta T, Irasawa M, Nakamura T (2003) Climate change and extension of the Ginkgo biloba L.
growing season in Japan. Glob Change Biol 9: 1634-1642
McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883-890
Menzel A, Sparks TH, Estrella N, Koch E, and others (2006)
European phenological response to climate change
matches the warming pattern. Glob Change Biol 12:
1969-1976
Miller-Rushing AJ, Katsuki T, Primack RB, Ishii Y, Lee SD,
Higuchi H (2007) Impact of global warming on a group of
related species and their hybrids: cherry tree (Rosaceae)
flowering at Mi. Takao, Japan. AmJ Bot 94:1470-1478
Miller-Rushing AJ, Inouye DW, Primack RB (2oo8a) How
well do first flowering dates measure plant responses to
climate change? The effects of population size and sampling frequency. J Ecol 96: 1289-1296
Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger
p (2008b) Bird migration times, climate change, and
changing population sizes. Glob Change Biol 14:
1959-1972
Miller-Rushing AJ, Primack RB, Stymeist R (2008c) Interpreting variation in bird migration times as observed by
vohmteers. Auk 125:565-573
Moller AP, Rubolini D, Lehikoinen E (2008) Populations of
migratory bird species that did not show a phenological
response to climate change are declining. Proc Natl Acad
Sei USA 105,16195-16200
Nakamura T, Short K (2001) Land-use planning and distribution of threatened wildlife in a city of Japan. Landsc
Urban Plan 53:1-15
Noda A, Yamaguchi Y (2008) Characterizing urban sprawl
using remote sensing and a simple spatial metric for
a medium-sized city in Japan. Int J Geoinformatics 4:
43-50
Ozaki K. Baba T, Komeda S, Kinjyo M, Toguchi Y, Harato T
(2002) The declining distribution of the Okinawa Rail
Gallira11us okinawae. J Yamashina Inst Ornithol 34:
136-144 (in Japanese)
Parmesan C (2006) Ecological and evolutionary responses to
recent climate change. Annu Rev Ecol Evol Syst 37:
637-669
Peintinger M, Schuster S (2005) Changes in first arrival
dates of cornmon migratory bird species in southwestern
Germany. Vogelwarte 43:161-169
Peterson TC, Vose RS (1997) An overview of the Global
Historical Climatology Network temperature database.
Bull Am Meteorol Soc 78:2837-2849
Peterson TC, Vose RS, Schmoyer R, Razuvaev V (1998)
Global Historical Climatology Network (GHCN) quality
>>-
>>>-
>>-
>>>-
>-
111
control of monthly temperature data. Int J Climatol 18:
1169-1179
Primack RB, Higuchi H, Miller-Rushing AJ (2009a) The
impact of climate change on cherry trees and other
species in Japan. Biol Conserv 142:1943-1949
Primack RB, Ibánez 1, Higuchi H, Lee SD, Miller-Rushing
AJ, Wilson AM, Silander JA (2009b) Spatial and interspecific variability in phenological responses to warming
temperatures. Biol Conserv 142:2569-2577
Rooríguez- Teijeiro JD, Gordo O, Puigcerver M, Gallego S,
Vinyoles D, Ferrer X (2005) African climate warming
advances spring arrival of the cornmon quail Coturmx
coturmx. Ardeola 52:159-162
Root TL, MacMynowski DP, Mastrandrea MD, Schneider
SH (2005) Human-modified temperatures induce species
changes: joint attribution. Proc Natl Acad Sci USA 102:
7465-7469
Rubolini D, Moller AP, Rainio K. Lehikoinen E (2007)
Intraspecific consistency and geographic variability in
temporal trends of spring migration phenology among
European bird species. Clim Res 35:135-146
Saino N, Rubolini D, Jonzén N, Ergon T, Montemaggiori A,
Stenseth NC, Spina F (2007) Temperature and rainfall
anomalies in Africa predict timing of spring migration in
trans-Saharan migratory birds. Clim Res 35: 123-134
Saino N, Rubolini D, Lehikoinen E, Sokolov LV and others
(2009) Climate change effects on migration phenology
may mismatch brooo parasitic cuckoos and their hosts.
Biol Lett 5:539-541
Sepp M, Palm V, Leito A, Piiiidam K. Truu J (2011) Effect of
atmospheric circulation types on spring arrival of migratory birds and long-term trends in the first arrival dates
in Estonia. Estonian J Ecol 60: 111-131
Shaw LM, Chamberlain D, Evans M (2008) The house sparrow Passer domesticus in urban are as: reviewing a possible link between post-decline distribution and human
socioeconomic status. J Ornithol 149:293-299
Sparks TH, Tryjanowski P (2007) Rapid (but differential)
advance of spring arrival dates in two hinmdines. Clim
Res 35,159-164
Sparks TH, Roberts DR, Crick HQP (2001) What is the value
of first arrival dates of spring migrants in phenology?
Avian Ecol Behav 7:75-85
Sparks TH, Bairlein F, Bojarinova JG, Hüppop O and others
(2005a) Examining the total arrival distribution of migratory birds. Glob Change Biol 11:22-30
Sparks TH, Croxton PJ, Collison N, Taylor PW (2005b)
Examples of phenological change, past and present, in
UK farming. Ann Appl Biol 146:531-537
Sparks TH, Jaroszewicz B, Krawczyk M, Tryjanowski P
(2009) Advancing phenology in Europe's last lowland
primeval forest: non-linear temperature response. Clim
Res 39,221-226
Sugimura K. Yamada F, Miyamoto A (2003) Population trend,
habitat change and conservation of the rnrique wildlife
species on Amami Island, Japan. Glob Env Res 7 :79-89
Tamada K (2006) Population change of grassland birds over
ten years in Nakashibetsu, eastern Hokkaido. Ornitholog
Sei 5,127-131
Tottrup AP, Thorup K. Rahbek C (2oo6a) Patterns of change
in timing of spring migration in North European songbird populations. J Avian BioI37:84-92
Tottrup AP, Thorup K. Rahbek C (2006b) Changes in timing
of autumn migration in North European songbird populations. Ardea 94:527-536
112
Clim Res 54: 95-112, 2012
>- Tottrup
>-
>>-
AP, Thorup K. Rainio K. Yosef R, Lehikoinen E,
Rahbek e (2008) Avian migrants adjust migratian in
response to environmental conditions en raute. Biol Lett
4,685-688
Tryjanowski P, Sparks TH (2001) Is fue detection oí fue first
arrival date oí migrating birds influenced by population
size? A case study oí fue red-backed shrike Lamus collurio. Int J Biometeoro145:217-219
Tryjanowski P, Kuzniak Sr Sparks TH (2002) Earlier arrival
oí sorne farrnland migrants in western Poland. Ibis 144:
62-68
Tryjanowski P, Kuzniak Sr Sparks TH (2005) What affects
fue magnitude oí change in first arrival dates oí migrant
birds? J Ornithol 146:200-205
Van Buskirk J, Mulhivill RS, Leberman Re (2009) Variable
shifts in spring and autumn migratian phenology in
NorthAmericansongbirds associated with climate change.
Glob Change Biol 15:760-'7'71
Végvári Z, Bókony V, Barta Z, Kovács G (2010) Life history
Editorial responsibility: Tim Sparks,
Cambridge, UK
>-
>>>-
predicts advancement of avian spring migration in
response to climate change. Glob Change Biol16:1-11
Visser ME, Adriaensen F, Van Balen JH, Blondel J and
others (2003) Variable responses to large-scale climate
change in European Parus populations. Proc Biol Sci 270:
367-372
Watanuki y (2011) Climate variability and the timing of
breeding and reproduction in seabirds. Mem Fac Fish
Sci Hokkaido Univ 53:19-26 (in Japanese)
Willis CG, Rubiel B, Primack RB, Miller-Rushing AJ, Davis
CC (2008) Phylogenetic patterns of species loss in
Thoreau's wooos are driven by climate change. Proc Natl
Aead Sei USA 105,17029-17033
Yamada H, Tokuoka K (1996) Population and urbanization
trends in post-war Japan. Asian Econ J 10:187-206
Zalakevicius M, Bartkeviciene G, Raudonikis L, Janulaitis J
(2006) Spring arrival response to climate change in birds:
a case study from eastern Europe. J Ornithol 147:
326-343
Subrrritted: September 27, 2010¡ Accepted: Febllla¡y 26,2012
Praofs received fram author(s): July 26,2012