Ecol Res (2007) 22: 507–514
DOI 10.1007/s11284-006-0044-6
O R I GI N A L A R T IC L E
Zhongkui Luo Æ Osbert J. Sun Æ Quansheng Ge
Wenting Xu Æ Jingyun Zheng
Phenological responses of plants to climate change in an urban
environment
Received: 23 March 2006 / Accepted: 10 August 2006 / Published online: 27 September 2006

The Ecological Society of Japan 2006
Abstract Global climate change is likely to alter the
phenological patterns of plants due to the controlling
effects of climate on plant ontogeny, especially in an
urbanized environment. We studied relationships be-
tween various phenophases (i.e., seasonal biological
events) and interannual variations of air temperature in
three woody plant species (Prunus davidiana, Hibiscus
syriacus, and Cercis chinensis) in the Beijing Metropolis,
China, based on phenological data for the period 1962–
2004 and meteorological data for the period 1951–2004.
Analysis of phenology and climate data indicated sig-
nificant changes in spring and autumn phenophases and
temperatures. Changes in phenophases were observed
for all the three species, consistent with patterns of rising
air temperatures in the Beijing Metropolis. The changing
phenology in the three plant species was reflected mainly
as advances of the spring phenophases and delays in the
autumn phenophases, but with strong variations among
species and phenophases in response to different tem-
perature indices. Most phenophases (both spring and
autumn phenophases) had significant relationships with
temperatures of the preceding months. There existed
large inter- and intra-specific variations, however, in the
responses of phenology to climate change. It is clear that
the urban heat island effect from 1978 onwards is a
dominant cause of the observed phenological changes.
Differences in phenological responses to climate change
Z. Luo Æ O. J. Sun (&) Æ W. Xu
Laboratory of Quantitative Vegetation Ecology,
Institute of Botany, The Chinese Academy of Sciences,
Beijing 100093, China
E-mail: osbertsun@ibcas.ac.cn
Q. Ge Æ J. Zheng
Institute of Geographical Sciences & Natural Resources Research,
The Chinese Academy of Sciences, Beijing 100101, China
Z. Luo
Graduate School of The Chinese Academy of Sciences,
Beijing 100049, China
may cause uncertain ecological consequences, with impli-
cations for ecosystem stability and function in urban
environments.
Keywords Beijing Metropolis Æ Climate change Æ
Phenology Æ Temperature indices Æ Urbanization
Introduction
Over the last century, the global temperature has in-
creased by an average of 0.5–1.0C (IPCC 2001) as a
direct consequence of increasing anthropogenic carbon
emission into the atmosphere. The warming has oc-
curred over two distinct periods: the first from 1910s to
1940s and the second from 1976 onwards (Walther et al.
2002). The second period of warming approximately
doubled the temperature increase of the first one, and
occurred at a magnitude unprecedented during the last
1,000 years (IPCC 2001). These recent climatic changes
have caused notable consequences at all levels of eco-
logical organizations and scales (e.g., Henry and Molau
1997; Corlett and Lafrankie 1998; Parmesan and Yohe
2003; Phoenix and Lee 2004; Edwards and Richardson
2004), creating uncertainties in functional stability, and
potential shifts in the food and energy balances of many
terrestrial ecosystems.
There is widespread evidence indicating changed
phenophases (i.e., seasonal biological events) of animals
and plants in the latest decades (Bradley et al. 1999;
Menzel et al. 2001; Peñuelas et al. 2001; Ahas et al. 2002;
Primack et al. 2004) along with the global climate
change. In Britain, for example, the first flowering date
has on average advanced 4.5 days for 385 plant species
during the past decade in comparison with the previous
four decades (Fitter and Fitter 2002). Distinct surface air
temperature increase has been considered a major cause
of these phenological changes (Chmielewski et al. 2004;
Primack et al. 2004).
In urban areas, the urban heat island (UHI) effect
caused by land-use change from urbanization and
508
industrialization exacerbate the warming in climate,
signifying the impact of climate change (Hansen et al.
1996; Camilloni and Barros 1997; Arnfield 2003; Hinkel
et al. 2003). Although the UHI can be strongly influ-
enced by the physical conditions of the urban sur-
roundings (i.e., topography, hydrology, and amount and
type of vertical obstructions) and climate (i.e., wind
speed and cloudiness), almost all cities show the same
urban–rural temperature differentiation pattern. The
urban environment is generally characterized by lower
interannual variability of temperature (e.g., Camilloni
and Barros 1997) and warmer winters (e.g., Hinkel et al.
2003) when compared with rural areas. It was reported
in a recent study that several mega-cities in Asia have
experienced intense surface UHIs which raised the urban
air temperature by 4–12C during dry seasons (Hung
et al. 2006). In the center of Tokyo, Japan, the air
temperature was recorded reaching a level that was as
much as 8.1C higher than nearby suburbs during a
single night in winter (Saitoh et al. 1996). Many studies
indicated that the UHI intensity is greater in fall and/or
winter than in summer seasons (Figuerola and Mazzeo
1998; Kim and Baik 2002). In China, there has also been
cogent evidence showing a significant urbanization effect
on climate (Zhou et al. 2004). The UHI effect can induce
peculiar ecological changes and affect phenology pat-
terns in urban areas differently from rural areas (Gallo
et al. 1993; Figuerola and Mazzeo 1998; Cleugh and
Grimmond 2001; White et al. 2002; Zhang et al. 2004). A
recent review by Neil and Wu (2006) suggests that there
is a general trend of earlier spring-time flowering in ur-
ban areas than the surrounding rural areas, mainly due
to raised temperatures, and that the effects of urbani-
zation on flowering phenology vary with plant types.
The urbanization-induced warming can be considered
a preview of longer-term global climate change for the
broader terrestrial ecosystems. In urban areas, changes
in phenophases may be amplified because the rate of
urban warming is much greater than the global average
warming. From 1880 to 1985, for example, global
warming would be reduced by 0.1C if cities with pop-
ulation more than 100,000 were excluded (Hansen and
Lebedeff 1987). The urbanization is estimated to con-
tribute 0.1–0.2C to the global rise in temperature
(Hansen and Lebedeff 1987).
The Beijing Metropolis, one of the most ancient as
well as one of the most modernized cities in China, has
experienced marked expansion in population and rapid
increases in the use of electrical facilities and motor
vehicles, all of which contribute to the occurrence of
UHI. Anecdotal observations suggest that winters are
shorter and spring and fall are warmer in recent decades
(Yu et al. 2005; Zhang et al. 2005), leading to notably
extended growing seasons. The phenomenal changes of
climate and plant phenology in the Beijing Metropolis
create a unique opportunity for examining the pheno-
logical responses of plants to accelerated climate
warming in an urbanized environment, using this natu-
ral ‘‘controlled climate facility’’. The availability of long-
term data on major phenological events for some of the
ornamental plant species in Beijing further facilitated the
execution of such experimentation. In this study, we
analyzed a 43-year phenological data set for three dif-
ferent species of woody plants growing in the Summer
Palace, located in the Beijing Metropolis, and the cor-
responding temperature data, and examined changes in
phenophases with time and underlying controlling
mechanism.
Materials and methods
Case study site and plants
Phenological data used in this study were from obser-
vations made at the Summer Palace (latitude 4001¢N,
longitude 11620¢E, and altitude 50 m). The Summer
Palace occupies an area of 290 ha, with three quarters
covered by water. It is located in the northwestern cor-
ner of the Beijing Metropolis, within the city enclosure,
14.0 km from the city center. The Summer Palace was
originally built as a royal garden in the mid-18th century
during the Qing Dynasty, and today is open to the
public as a scenery garden. The weather conditions in-
side the Summer Palace are consistent with the general
weather patterns of the Beijing Metropolis.
We analyzed the phenological data set for three
woody plant species, including Prunus davidiana (Carr.)
Franch, Hibiscus syriacus L., and Cercis chinensis Bun-
ge, which are all common ornamental plants in the
Beijing Metropolis. All three species are broadleaved
and winter deciduous. P. davidiana and C. chinensis are
both small trees that blossom in spring, whilst H. syr-
iacus is an ornamental shrub that blossoms most of the
summer. Table 1 lists the average date of occurrence for
various phenophases, and the number of years that the
observations were made for each phenophase type.
Data sources
Phenological data from 1962 to 1992 were obtained
from the Plant and Animal Phenology Observation
Annals in China Series No.1–No.11 (Institute of Geo-
graphical Sciences and Natural Resources Research, The
Chinese Academy of Sciences 1965–1992). Data for the
period 1993–2004 were made available by the Pheno-
logical Research Group of the Institute of Geographical
Sciences and Natural Resources Research of the Chinese
Academy of Sciences. Site and plant selections, pheno-
phase classification, and observation times were based
on the standard procedures described in the Method for
Phenology Observation in China (Wan and Liu 1979).
Phenological data were collected daily in the month(s) of
occurrence for specific phenophases. The starting date
for a given phenophase was observed from a perma-
nently marked individual selected from a group of more
than 10 individuals for P. davidiana and H. syriacus, and
more than 20 individuals for C. chinensis. Each of the
 509

Table 1 Slopes and correlation coefficients (R2) for linear regression of phenophases as function of time (years) for three woody plant
species in the Beijing Metropolis for the period 1962–1977, 1978–2004, and the period 1962–2004

Species Phenophase Years of observations Average date 1962–1977 1978–2004 1962–2004

Slope R2 Slope R2 Slope R2

Prunus davidiana Bud burst 33 (11, 22) 8 Mar 0.085 0.050 0.243 0.091 0.044 0.008
First flowers open 36 (13, 23) 25 Mar 0.170 0.046 0.669** 0.422 0.274** 0.224
Coloring of leaves 34 (12, 22) 16 Oct 1.487** 0.598 0.308 0.144 0.539** 0.481
End of leaf-falling 32 (13, 19) 14 Nov 0.582* 0.387 0.140 0.031 0.012 0.001
Hibiscus syriacus Bud burst 27 (13, 14) 12 Apr 0.109 0.006 0.612 0.123 0.186 0.050
First flowers open 24 (12, 12) 9 July 0.089 0.002 0.247 0.023 0.263 0.062
Coloring of leaves 27 (13, 14) 10 Oct 0.438 0.138 0.280 0.072 0.474** 0.418
End of leaf-falling 26 (12, 14) 8 Nov 0.266 0.087 0.060 0.006 0.151 0.098
Cercis chinensis Bud burst 32 (11, 21) 29 Mar 0.269 0.028 0.653* 0.266 0.261 0.117
First flowers open 35 (12, 23) 17 Apr 0.337 0.093 0.645** 0.374 0.173 0.084
Coloring of leaves 34 (12, 22) 2 Oct 0.963 0.234 0.123 0.018 0.049 0.005
End of leaf-falling 33 (11, 22) 8 Nov 0.723* 0.413 0.287 0.075 0.096 0.024

The values outside the parentheses for the ‘‘Years of observations’’ column are the years of observations recorded for corresponding
phenopases for the period 1962–2004, and those in the parentheses are for the period 1962–1977 and 1978–2004, respectively
*P<0.05; **P<0.01

individuals used as standard for phenological observa-
tions was selected based on the criteria that it was
healthy, and had blossomed and borne fruits for more
than 3 years. All phenological data were collected from
the standard individuals unless any of them died from
disease or physical injury— in which case it would be
replaced by another individual that fits with the crite-
ria—or if the occurrence of a given phenophase signifi-
cantly deviated from the average value of the
neighboring individuals. The sites and plants that were
used for phenological observations were not subject to
any management scheme such as pruning, irrigation,
and fertilization, etc.
Monthly temperature data, including monthly mean
temperature (Tmean), monthly minimum temperature
(Tmin) and monthly maximum temperature (Tmax), for
Beijing from 1951 to 2004 were from the long-term re-
cords at a standard weather station (latitude 3993¢N,
longitude 11628¢E, and altitude 54 m) of the Beijing
Meteorological Bureau, located in the southeastern
corner of the Beijing Metropolis, 27.0 km from the
Summer Palace across the city center. This is the only
weather station in Beijing that has weather records that
cover the entire period of our phenological data set.
Data analysis
The most noticeable climate warming started in 1976
globally (IPCC 2001; Walther et al. 2004). In China,
significant change in the national climate was found to
coincide with commencement of rapid economic growth
since 1978 (Zhou et al. 2004). Accordingly, we divided
our 54-year temperature data set into two distinct peri-
ods: 1951–1977 and 1978–2004 (Fig. 1). The whole
period of 1951–2004 and each of the two sub-divided
periods were used in the analyses for the relationships of
spring and autumn phenophases with time.
For the phenological data, all occurrence dates were
transformed to day of the year (DOY) for convenience
of data analysis. Comparisons were made of the differ-
ences in inter- and intraspecific responses to interannual
variations of temperatures. In order to determine the
effects of different temperature regimes on the occur-
rence of specific phenophases, we calculated the mean,
minimum, and maximum temperatures based on the
following time periods: the preceding 1 (T1m), 3 (T3m), 6
(T6m), 9 (T9m), and 12 months (T12m) as relative to the
month of occurrence for a specific phenophase, autumn
(September–November; TA), and the whole period of the
previous calendar year (January–December; TY). For
the spring phenophases, regression analysis was made
with T1m, T3m, T6m, TA, and TY; and for the autumn
phenophases, regression analysis was made with T1m,
T3m, T6m, T9m, T12m. To determine the variability of
specific phenophases, we estimated the relative change
(expressed in days) in the date of occurrence for each
phenophase by calculating the difference between the
actual date of occurrence each year and the earliest
occurrence date recorded during the study period, and
then averaged over the entire study period (results
shown in Table 4).
All descriptive statistics, correlation, regression, and
analysis of variance (ANOVA) were performed using the
SPSS 12.0 statistical program. Means of main effects
were compared using Tukey’s (for data with equal
variances) or Tamhane’s (for data with unequal vari-
ances) multi-range test at P<0.05.
Results
Trends of air temperatures from 1951 to 2004
The air temperatures in the Beijing Metropolis displayed
two distinct patterns of changes with time (Fig. 1). From
510
20
18
16
Temperature (°C)
14
12
10
8 Tmin
Tmean
6 periods. H. syriacus displayed a pattern of advance in
Tmax
4
1950 1960 1970 1980 1990 2000 2010
Years
Fig. 1 Long-term trend of air temperature changes in the Beijing
Metropolis from 1951 to 2004. Note: Tmin, annual minimum air
temperature (C); Tmean, annual mean air temperature (C); Tmax,
annual maximum air temperature (C)
1951 to 1977, Tmean, Tmin, and Tmax all fluctuated with
time without apparent trends. From 1978 to 2004, the
above three temperature indices significantly increased
at rates of 0.057C (R2=0.40, P<0.05), 0.074C
(R2=0.57, P<0.05), and 0.040C (R2=0.27, P<0.05)
per annum, corresponding to total changes of 1.5, 2.0,
and 1.0C for the period.
Changes in spring and autumn phenophases
Large changes occurred from 1962 to 2004 in nearly all
the phenophases, with a rate of change which differed
with specific phenophases and species (Table 1). The
most notable changes were an advance in the opening of
the first flowers and a delay in the coloring of leaves in P.
davidiana, and a delay in the occurrence of coloring of
leaves in H. syriacus; in C. chinensis, the bud-burst and
opening of the first flowers both significantly (P<0.01)
advanced from 1978–2004, but no change was detected
for the period 1962–1977.
For the spring phenophases, the change was negligi-
ble from 1962 to 1977 except in C. chinensis, but the
occurrence of bud-burst markedly advanced from 1978
to 2004; the occurrence of the opening of the first flowers
Table 2 Date shifts for the occurrence of two spring phenophases for three woody plant species in the Beijing Metropolis for the period
1962–1977 and 1978–2004
Species Bud-burst
1962–1977
Prunus davidiana 1.4±6.3
Hibiscus syriacusa 1.7±6.6
Cercis chinensis 4.3±8.4
Values shown are means ± standard errors; negative values indicate the advance in the occurrence, and positive values indicate delay.
Sample sizes (years of observations) are as shown in Table 1
a
The opening of the first flowers occurs in summer
advanced in P. davidiana and C. chinensis, and delayed
in H. syriacus from 1978 to 2004 (Table 2). Changes in
the occurrence of autumn phenophases differed with
plant species and between the two sub-divided time
periods (Table 3). In both P. davidiana and C. chinensis,
the occurrence of the coloring of leaves delayed with
time; the occurrence of the end of leaf-falling delayed
from 1962 to 1977, but advanced from 1978 to 2004. The
changes in the coloring of leaves and the end of leaf-
falling in H. syriacus were much less than in the other
two species, and did not differ between the two time
the occurrence of the end of leaf-falling for the entire
period of 1962–2004 (Table 3).
The variation with time differed significantly
(P<0.05) among the different phenophases within spe-
cies and among species within the same phenophases
except the end of leaf-falling (Table 4). In P. davidiana,
the opening of the first flowers and the coloring of leaves
varied with time more than the bud-burst and the end of
leaf-falling; in H. syriacus, the coloring of leaves varied
the most; whereas in C. chinensis, the bud-burst was the
most variable phenophase. Among the three plant spe-
cies, C. chinensis changed the most with time in the bud-
burst, P. davidiana in the opening of the first flowers,
and H. syriacus in the coloring of leaves (Table 4).
Relationships between interannual variation
of temperatures and occurrence of specific phenophases
Regression and correlation analyses indicated that the
temperature indices that were best related with specific
phenophases differed with plant species and phenopha-
ses (Table 5). For the spring phenophases, both bud-
burst and the opening of the first flowers were best
correlated with T3m_max in P. davidiana and C. chinensis;
whereas in H. syriacus, the two phenophases were best
correlated with T3m_mean and TA_min respectively. Au-
tumn phenophases showed more diverse relationships
with temperature indices than the spring phenophases
(Table 5).
Occurrence of the opening of the first flowers was
significantly (P<0.05) and negatively related with
T3m_min and T3m_max in P. davidiana and C. chinensis,
but not in H. syriacus (Fig. 2). Extending the result from
Opening of first flowers
1978–2004 1962–1977 1978–2004
6.6±4.6 2.7±3.7 18.1±4.6
16.5±12.7 1.4±4.6 6.7±13.6
17.6±6.7 5.4±5.3 17.4±4.9
 511

Table 3 Date shifts for the occurrence of two fall phenophases for three woody plant species in the Beijing Metropolis for the period
1962–1977 and 1978–2004

Species Coloring of leaves End of leaf-falling

1962–1977 1978–2004 1962–1977 1978–2004

Prunus davidiana 23.8±5.9 8.3±4.7 9.3±3.7 3.8±5.0

Hibiscus syriacus 7.0±5.3 7.6±7.8 4.3±4.4 1.6±6.5
Cercis chinensis 15.4±8.8 3.3±5.5 11.6±4.6 7.8±6.1

Values shown are means ± standard errors; negative values indicate the advance in the occurrence, and positive values indicate delay.
Sample sizes (years of observations) are as shown in Table 1

Fig. 2, a 1C increase in T3m_max would bring forward
the occurrence of the opening of the first flowers by
4.5 days in P. davidiana and by 3.8 days in C. chinensis.
Discussion
Analysis of long-term phenological records can provide
an effective means for examination of phenological
trends with time (Bradley et al. 1999), and assist with
gaining insight into the responses of species to climate
change (Walther et al. 2002). Using a 43-year pheno-
logical data set for three common ornamental plant
species in the Beijing Metropolis, we depicted impacts of
climate change on plant phenology in an urban envi-
ronment at a relatively smaller temporal scale. Our re-
sults indicated that over the past 4 decades or so, there
had been marked changes in plant phenology in the
Beijing Metropolis, and that the phenological changes
were apparently related with the rising temperature of
the period, especially during the period 1978–2004. The
changing phenology in the three plant species—i.e., P.
davidiana, H. syriacus, and C. chinensis—was reflected
mainly as an advance of the spring phenophases and a
delay in the autumn phenophases, but with strong
variations among species and phenophases in response
to different temperature indices.
In this study, most phenophases (both spring and
autumn) had significant relationships with the temper-
atures of the preceding months. Our findings were con-
sistent with those by remote sensing imagery analysis.
Using the advanced very high resolution radiometer
(AVHRR)/normalized difference vegetation index
(NDVI), Piao et al. (2006) showed that the onsets of
phenological events of temperate vegetation were most
significantly related with the mean temperatures of the
proceeding 2–3 months in China. In the eastern United
States, urbanization-induced warming caused the
growing season to start 5.7 days earlier and to end
2.2 days later than the rural areas (White et al. 2002).
Experiments using artificial heating treatment showed
the significant effects of air warming on changes in
phenology (Suzuki and Kudo 1997; Dunne et al. 2003).
Here we found that changes in the occurrence of the
opening of the first flowers in P. davidiana were almost
at the same pace as changes in the mean maximum
temperature of the preceding 3 months, strongly sug-
gesting that the opening of the first flowers in P. davi-
diana could be a good indicator for global climate
warming (Zhang et al. 2004, 2005).
Different species or different phenophases within the
same species responded differently to temperature
changes. The differential responses of species and phe-
nophases to changing temperatures may be attributed to
other non-temperate-related ecological factors (McCar-
ty 2001), such as photoperiod, plant functional type,
genetic regulatory systems, demography and/or adapt-
ability, etc.
An ecosystem is a dynamic and complex whole.
Phenological changes of vegetation can result in shifts or
changes in other ecological processes within an ecosys-
tem. The three plant species we studied responded to
climate change at different rates. These asynchronisms in
interspecific phenophases may cause uncertain ecologi-
cal consequences by affecting trophic structures in arti-
ficial urban ecosystems where the three species are made

Table 4 Variation in the date of occurrence (days) with time for four phenophases in three woody plant species in the Beijing Metropolis
for the period 1962–2004

Phenophases Prunus davidiana Hibiscus syriacus Cercis chinensis F P

Bud burst 11.5±1.1 a/a 16.9±1.6 a/b 24.7±1.7 a/c 22.10 <0.01
Opening of first flowers 19.0±1.2 b/a 14.92±2.0 a/a 16.8±1.2 b/a 1.92 0.15
Coloring of leaves 21.0±1.6 b/ab 25.9±1.3 b/a 17.8±1.4 b/b 5.78 <0.01
End of leaf-falling 11.6±1.0 a/a 9.0±0.9 c/a 11.2±1.2 c/a 1.38 0.26
F 16.15 5.05 14.88 – –
P <0.01 <0.01 <0.01 – –

Values shown are mean ± standard errors. The letters on the right of the back slash indicate separation of means between the three
species for corresponding phenophases, and those on the left indicate separation of means between the four different phenophases within
species
512

Table 5 Temperature indices that best describe the relationship with given phenophases and corresponding values of correlation coeffi-
cients (R2) and levels of significance (P) for three plant species in the Beijing Metropolis for the period 1962–2004

Phenophase Prunus davidiana Hibiscus syriacus Cercis chinensis

Bud burst T3m_max T3m_mean T3m_max

R2=0.41 R2=0.28 R2=0.38
P=0.001 P=0.012 P=0.001
First flowers open T3m_max TA_min T3m_max
R2=0.83 R2=0.34 R2=0.58
P=0.001 P=0.014 P=0.001
Coloring of leaves T6m_min T9m_min T12m_mean
R2=0.26 R2=0.44 R2=0.12
P=0.018 P=0.004 P=0.290
End of leaf-falling T3m_min T3m_max T1m_max
R2=0.09 R2=0.31 R2=0.13
P=0.399 P=0.030 P=0.056

T1m_max, the maximum temperature for the proceeding month; T3m_mean, T3m_max, and T3m_min, the mean, maximum, and minimum
temperatures for the proceeding 3 months; T6m_min, the minimum temperature for the proceeding 6 months; T9m_min, the minimum
temperature for the proceeding 9 months; T12m_mean, the mean temperature for the proceeding 12 months; TA_min, the minimum tem-
perature for the autumn months (Sep–Nov)

to co-exist. Research by others has shown that earlier which may be further intensified by phenological shifts.
bud-burst could affect associated insects (Dixon 2003), All the three species we studied are entomophilous
and that flowering phenology could affect the genetic plants (i.e., bee-pollinated); the phenological change in
structure of the plant species (Yamagishi et al. 2005), flowering events may break the equilibrium rhythm of
plant–insect interactions, thus causing shifts in the
dynamics of pollinating insects and associated trophic
Prunus davidiana
communities (Nei and Wu 2006). Kudo et al. (2004)
100 found that the 7–17 days’ advance of the opening of the
a b
first flowers in 1 year caused the seed-sets of some bee-
90
pollinated ephemerals to decrease by more than half the
80 usual level in northern Japan.
y = 112.3 - 4.50x y = 79.3 - 2.93x China has experienced significant urbanization since
70 R2 = 0.43 1978, and the trend continues. For the Beijing Metrop-
R2 = 0.83
P < 0.001 P < 0.001
60 olis, the population increased by 1.2 million in the period
2 4 6 8 10 -5 -4 -3 -2 -1 0 1 2 1962–1977, and by 5.8 million in the period 1978–2004;
whilst the city zone expanded from 340 km2 in 1978 to
Hibiscus syriacus 750 km2 in 2004. Nationwide, the total population in
Time of occurrence (DOY)

220
c y = 242.7 - 1.80x d y = 179.1 + 0.62x
China increased from just over 0.96 billion in 1978 to
210 R2 = 0.04 R2 < 0.01
P = 0.324 P = 0.831 nearly 1.31 billion by the end of 2005 (http://www.cpirc.
200 org.cn/). Changes in socio-economic structures in recent
190 decades have caused a marked shift of population from
rural to urban areas, along with rapid population
180
expansion. Statistics showed that the proportion of urban
170 population increased from 17.9% in 1978 to 43% in 2005
26 27 28 29 30 31 16 17 18 19 20 21
in China (http://www.cpirc.org.cn/).
Cercis chinensis A previous study by Zhou et al. (2004) has shown
130 significant effect of urbanization on climate in China
e f y = 108.4 - 2.23x
120 R2 = 0.24 since 1978 because of the rapid economic growth. Our
P = 0.014
110 study showed that climate warming (1.5C) in the
Beijing Metropolis mainly occurred in the latest 20–
100
y = 153.2 - 3.78x 30 years, and was greater than the global average (0.5–
90 R2 = 0.58
P = 0.001
1.0C). Because of the impact of UHI, the increases in
80 air temperature with climate warming are often much
8 10 12 14 -2 -1 0 1 2 3 4 5 greater in urban areas than in rural areas (Arnfield
T3m_max(°C) T3m_min(°C) 2003). Therefore, phenological responses are expected to
be more intense in urban areas, and moderate or even
Fig. 2 Occurrence of the opening of the first flower for three plant not-detectable in rural areas. White et al. (2002) found
species as functions of the mean minimum (T3m_min) and maximum
(T3m_max) temperatures of the preceding three months in the Beijing that, in the eastern United States, the deciduous
Metropolis during the period 1962–2004 broadleaf forests in urban areas displayed greater

changes in spring and autumn phenophases with time
than those in rural areas. Different responses of plant
phenology between urban and rural areas could induce
profound influence among the rural–urban meta-popu-
lation and meta-communities. The different flowering
phenology shifts can block or limit gene flow among
meta-population and meta-community in rural–urban
transect, and speed species polarization (Neil and Wu
2006).
Our studies, using three woody ornamental plants in
the Beijing Metropolis as examples, indicated that phe-
nological events in urban environment have experienced
pronounced change with time in response to climate
change, and the change apparently differed with plant
species and phenophases. It is clear that the UHI effect
from 1978 onwards in the Beijing Metropolis is
responsible for the observed phenological changes. Dif-
ferent phenological responses among species are likely
explained by genetically controlled factors that are
inherent to different species. Such differences may cause
uncertain ecological consequences with implication to
ecosystem stability and function in urban environments.
Acknowledgments This research was financially supported by a
‘‘Talent Recruitment’’ fund of the Institute of Botany, the Chinese
Academy of Sciences, to O. J. Sun. We thank Dr. Jian Ni of the
Institute of Botany, the Chinese Academy of Sciences for providing
the climate dataset.
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