Botanical Studies (2006) 47: 153-161.
*
Corresponding author: E-mail: yuq@igsnrr.ac.cn; Fax:
86-10-64851844; Tel: 86-10-64856515.
Effects of changes in spring temperature on flowering
dates of woody plants across China
Pei-Ling LU
1
, Qiang YU
2,
*, Jian-Dong LIU
3
, and Qing-Tang HE
1
1
College of Resource and Environment, Beijing Forestry University, Beijing 100083, P.R. China
2
Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, No. 11A Datun
Road, Beijing 100101, P.R. China
3
Institute of Ecology and Agrometeorology, Chinese Academy of Meteorological Sciences, Beijing 100081, P.R. China
(Received March 4, 2005; Accepted November 8, 2005)
ABSTRACT.
In China, changes in the timing of plant phenological phases are influenced greatly by mon-
soonal climate fluctuations, and also vary with species and region. Observations of phenological phases of
trees were conducted in the Phenological Observation Network of China from 1963 to 1988. Records of flow-
ering dates of four species (Syringa oblata Lindl., Cercis chinensis Bunge, Robinia pseudoacacia L., Albizzia
julibrissin Durazz) at ten sites, together with corresponding climate data, were used to investigate phenophase
responses to variation in temperature. The ten sites extend over a wide area, with latitudes ranging from
25oN to 46XN, and altitudes ranging from 17 to 1,922 m a.s.l. Spring temperature was significantly related to
flowering date of the trees under the monsoonal climate in the eastern Eurasian Continent. The period during
which temperature influences flowering time varies from 60 to 90 days for Robinia pseudoacacia in the south
to 30 to 40 days in the north, due to the shorter warm period before flowering in the north. The three other
species showed similar trends of changes with latitude in the length of the period of temperature influence.
The flowering season for Cercis chinensis in response to a temperature increase 30-60 days prior to flowering
advanced from 2.7 to 5.9 days/XC in the low plain, and in response to a temperature increase 60-90 days prior
to flowering, advanced from 7.1 to 14.8 days/XC in the Yunnan-Guizhou Plateau. The flowering for Syringa
oblata, Robinia pseudoacacia and Albizzia julibrissin, in response to a temperature increase advanced in the
range 2.7-4.9, 2.5-6.5, and 2.4-6.0 days/XC in the low plain, respectively. Flowering advanced by 4.7-12.4
days/XC for Robinia pseudoacacia and 13.1 days/XC for Albizzia julibrissin in the plateau.
Keywords: China; Flowering date; Phenology; Temperature.
INTRODUCTION
Phenology has emerged recently as an important focus
for ecological research (Schwartz, 1999, 2003). Because
phenological phenomena are visible and responses
are closely related to climate, increasing attention is
being paid to the analysis of phenological variation and
growth length in the context of climatic change. Most
phenological events are significantly related to climatic
variables and change through time (Walther et al.,
2002; Parmesan and Yohe, 2003). A good example of
this is the Marsham phenological record from 1736 to
1947 in England (Sparks and Carey, 1995). In general,
higher temperatures in the late winter and early spring
promote earlier leafing and flowering of plants. There are
numerous observations and investigations on the shifting
of phenological events in response to climate change in
different regions (Walther et al., 2001). In Europe, the
lengthening of growing season has been described by
Menzel and Fabian (1999). It has also been documented
that spring events, such as leaf unfolding or needle flush,
are particularly sensitive to temperature (Walkovszky,
1998; Beaubien and Freeland, 2000; Sparks et al., 2000;
Rotzer et al., 2000; Defila and Clot, 2001; Ahas et al.,
2002; Van Vliet et al., 2002; Sparks and Menzel, 2002). In
addition, a number of papers have looked at the effects of
temperature on the phenological timings of plants at single
study sites (e.g. Fitter et al., 1995; Sparks et al., 1997).
In the British Isles, Sparks et al. (2000) reported that the
timing of spring and summer species gets progressively
earlier as the climate warms, and 25 phenological events
studied were significantly related to temperature. Fitter
et al. (1995) reported that warmer spring temperatures
advanced flowering dates by about 4 days/XC increase in
the mean monthly temperatures. Warmer than average
winter and spring temperatures have been noted over the
PHYSIOLOGY
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154
Botanical Studies, Vol. 47, 2006
last century in Western Canada (Beaubien and Freeland,
2000). First-bloom dates for Edmonton (Alberta)
were extracted from four historical data sets, and a
spring flowering index showed progressively earlier
development.
Using data from the International Phenological Gardens
for the period 1969-1998 across Europe, Chmielewski and
Rotzer (2001) noted that a warming in the early spring
(February-April) by 1XC induced the growing season to
begin 7 days earlier. The observed extension of the grow-
ing season was mainly the result of an earlier onset of
spring. An increase in mean annual air temperature by 1
XC led to an extension of 5 days. Using the phenologi-
cal data from ten central European regions, Rotzer et al.
(2000) analyzed and quantified the influence of large-
scale climate change and urban climate effects on four
spring phenophases for the years 1951-1995. The trends
for the period from 1980-1995 were much stronger: the
pre-spring phenophases on average became earlier by 13.9
days/decade in the urban areas and 15.3 days/decade in the
rural areas. In Estonia, Ahas (1999) analyzed a long-term
phenological time series for the impact assessment of cli-
mate changes. The study showed that Estonian springs had
advanced 8 days on average over the last 80-year period,
rates of change being faster in the last 40 years. Kramer
et al. (2000) noted that the phenology of the boreal and
temperate zone forests is mainly driven by temperature,
affecting the timing of the start of the growing season and
its duration.
China is located in the eastern edge of the Eurasian
Continent. The climate in the eastern part is influenced
predominantly by monsoons. The maximum monthly
mean temperature of the region is 26 to 30XC in July.
The minimum monthly mean temperature decreases
greatly from south to north, which occurs in January, and
ranges from 7 to -12XC. As the climate in eastern China is
controlled by interactions between oceanic and continental
air masses, variations in temperature, precipitation and
solar radiation are much greater than at the same latitude
on the American continent or west Eurasian Continent
(Domros and Peng, 1988). Therefore, there are potentially
pronounced inter-annual variations within this region,
causing significant variations in phenology.
The objectives of this study are (1) to investigate
relationships between plant development and temperature
in eastern and central China, based on observations from
1963 to 1988; and (2) to identify climatic factors causing
inter-annual variations in phenology in monsoonal
climate. This study tries to answer how the phenology of
flowering responds to temperature change and attempts to
identify periods within a year when plant phenophases are
significantly affected by temperature.
MATERIALS AND METHODS
The Phenological Observation Network of China was
initiated in the early 1960s, but was interrupted after 1988,
except for Beijing. There are about 35 stations across Chi-
na, mainly concentrated in the east. The methodology of
the Phenological Observation Network of China has been
described in detail by Wan and Liu (1979) and Lu et al.
(2006). The observation guidelines state that plant species
were chosen for their dominance in regional vegetation
and for the existence of records about their growth in an-
cient times and/or in other countries for comparison. The
plants were local varieties older than four years, and five
individual plants per species were observed at each site.
Some stations have continuous records during 1963-1988.
Phenological records from 1963-1988 were available in
the form of annual reports (Institute of Geography, Chi-
nese Academy of Sciences, 1989). Four species, Syringa
oblata, Cercis chinensis, Robinia pseudoacacia and Albiz-
zia julibrissin, which have a wide distribution, were se-
lected. We used the observations from ten sites distributed
all over China, which had continuous observation records.
The distribution of the sites and their latitude, longitude,
and altitude are shown in Figure 1 and Table 1. The sites
are located over a wide range of geographic regions. In
general, altitude in mainland China increases from the
coast in the east to the Tibetan Plateau. Consequently, the
topography can be divided into three tablelands. The se-
lected sites are on the low plains in the east, the first table-
land, including northeast China (Harbin and Shenyang),
the North China Plain (Taian and Beijing) and the lower
and middle reach of Yangtze River (Hangzhou and Wu-
han), and on the second tableland, i.e. Inner Mongolia
Plateau in north China (Huhehaote), the Loess Plateau in
central China (Xian) and Yunnan-Guizhou Plateau in the
southwest (Kunming and Guiyang). There are no records
from the Tibetan Plateau, the third table land with an aver-
age height of over 4,000 m above sea level, inland desert
in the west and the plain in southeast.
Daily average temperature data during the 1963-1988
period were provided by the Meteorological Bureau of
China. The meteorological stations are located in places
representative of regional climate. They are within 5 km
of phenological observational sites, and their height dif-
ferences are lower than 20 m in the low plain and 70 m
on the plateaus. The temperature influence was assumed
to start when the daily temperature rose over 0oC from
winter to spring and to end on the day of blooming. This
period was divided into several sub-periods, and the aver-
age temperature within each sub-period was calculated.
Temperatures in these sub-periods were considered as in-
dependent variables with variable lengths, i.e. 20, 30 and
40 days. Ten days were taken as a basic unit. For example,
the period from March 1 to April 10 was divided into ten
sub-periods of different lengths, i.e., March 1-10, March
11-20, March 21-31, April 1-10 for 10 days (or 11 days),
and March 1-20, March 11-31, March 21-April 10 for 20
days (or 21 days), and March 1-31 and March 11-April
10 for 30 days (or 31 days), and March 1-April 10 for 40
days (or 41 days).
To determine the significant period of temperature
pg_0003
LU et al. X Temperature effect on flowering dates in China
155
influence on flowering date, linear regression analysis
was applied. Since the period of temperature influence on
flowering dates can start when the temperature rises above
0oC, statistical analysis ranged from the day temperature
rose above 0oC in winter to the day of flowering although
this period changes annually. Based on the time series of
average temperatures in each year during the 1963-1988
period, significant periods of temperature influence are
obtained in accordance with the highest correlation coef-
ficient, after linear regression between flowering dates and
average temperature in the specific period is conducted
(Xu et al., 2005).
RESULTS
There were large differences in climate between the
stations due to the large differences in geographic position
and altitude. Climate in the east is dominated by mon-
soons. Rainfall is concentrated in summer and decreases
from southeast to northwest. There is abundant sunshine
in winter and spring. The spatial difference in temperature
is highest in winter and lowest in summer. Therefore, sea-
sonal variation of temperature in the south is much lower
than in the north (Figure 2) according to the variation pat-
tern of solar radiation. In the spring, temperature rises rap-
Figure 1. Distribution of the 10 observational sites in eastern China (latitude, longitude, and altitude of each station are listed in Table
1).
Table 1. Distribution of the phenological observation sites.
Site
Latitude Longitude Altitude (m) Average temperature
(oC)
Average rainfall
(mm)
Observation period
Kunming
25X0 103X0
1922
14.6
993
1963-1988
Guiyang
26X42 107X0
1050
15.3
1120
1963-1988
Hangzhou 30X5 120X4
17
16.2
1317
1963-1988
Wuhan
31X0 114X0
33
16.3
1169
1963-1988
Xian
34X4 109X4
437
13.4
563
1963-1988
Taian
36X2 116X55
137
12.7
683
1963-1988
Beijing
39X55 116X18
50
11.7
578
1963-1988
Huhehaote 41X12 111X43
1063
6.1
391
1963-1988
Shenyang
41X59 123X11
44
8.2
681
1963-1988
Harbin
46X43 126X42
149
3.7
523
1963-1988
pg_0004
156
Botanical Studies, Vol. 47, 2006
idly in northern China. The growth period is short in the
north, but extends to almost the whole year in the south.
For example, the annual amplitude in mean monthly tem-
perature is 35.7oC in Shenyang (northeast), with mean
monthly maximum and minimum of 24.7oC and -11.0oC,
respectively, and 18.7oC in Guiyang (Yunnan-Guizhou
Plateau) with a maximum temperature of 24.6oC and a
minimum of 5.9oC. Variation in altitude also results in site
differences in temperature regimes, particularly in winter.
In the south, Guiyang is substantially the warmest among
the study sites in winter, with an average daily temperature
of 5-7oC (Figure 2) because it is less influenced by cold
air masses from the north due to its high elevation. These
seasonal characteristics in temperature and annual ranges
may determine patterns of flowering.
There are three sites (Kunming, Guiyang, Huhehaote)
over 1,000 m, and all of them are located in western re-
gions, far away from the sea (Figure 1 and Table 1). Nev-
ertheless, the temperatures in the winter and early spring
in the Yunnan-Guizhou Plateau (Kunming, and Guiyang),
southwest China, are not as low as at other sites at the
same latitude. The low plain in eastern China is indeed
very cold due to advection of winter monsoons from the
north and inner Eurasian Continent. Guiyang is the warm-
est site in winter (Figure 2). Kunming, at 1,922 m a.s.l. in
the Yunnan-Guizhou Plateau (Table 1), is known as the
"Spring City," with warm winters and moderate summers.
On the other hand, Huhehaote, at 1,063 m a.s.l. in north
China, is 12oC colder than Guiyang (1,050 m) in winter, as
cold air masses from the north of the Eurasian Continent
pass through it. This effect of altitude and longitude on
temperature enhanced the trend of flowering dates along
with latitude. As there are only three sites on plateaus, the
general trend displays the influence of latitude.
Average flowering dates were delayed linearly with
increasing latitude (Figure 3). Flowering of Syringa oblata
Lindl., Cercis chinensis Bunge, Robinia pseudoacacia
L., and Albizzia julibrissin Durazz were delayed with an
increase in latitude, at rates of 3.3, 2.9, 2.3 and 2.2 days/
o
N, respectively (Figure 3). Cercis chinensis is widely
distributed in China, and its delayed rate of flowering was
similar to Albizzia julibrissin, Robinia pseudoacacia and
Syringa oblata. The four species bloom successively from
early spring to summer. Syringa oblata blooms slightly
before Cercis chinensis at a low latitude, but flowering
date was delayed rapidly at high latitudes, where there
is no Cercis chinensis (Figure 3). Flowering dates may
be also influenced by altitude and longitude, but latitude
dominantly determines phenophases distribution in this
region (Zheng et al., 2002).
Standard deviation (_) of flowering dates of the four
trees was calculated for each site separately. Figure 4
illustrates changes in _ with latitude. It is shown that _
decreases with latitude, which means flowering dates
fluctuated more in southern China than in northern China.
The line of 34oN divides eastern China into subtropical
and temperate zones, or the south and the north. The
decrease rate of _ with latitude was 3.2 days per
10-degree, i.e. about 6-10 days in the north and 2-6 days
in the south. The significant decrease in _ with latitude
demonstrated that inter-annual changes in flowering dates
increase gradually from the north to the south. However,
the deviation from the regression line may be explained
by altitude or longitude (Figure 4). Latitude apparently
has greater influence on flowering dates than altitude and
longitude in eastern China (Zheng et al., 2002).
As indicated in Materials and Methods, average
temperatures over different non-freezing periods were
used to calculate the correlation of temperature with
Figure 2. Variation in average daily temperatures between 1963
and 1988 at observation sites, demonstrating the influence of
latitude and altitude.
Figure 3. Changes in average flowering dates with latitude for
the four woody plants, Cercis chinensis, Albizzia julibrissin, Sy-
ringa oblata and Robinia pseudoacacia. Average flowering dates
show a significant trend with latitude although the influence of
altitude and longitude was not excluded, which may induce the
dates to fluctuate along with the latitude trend.
pg_0005
LU et al. X Temperature effect on flowering dates in China
157
sensitive period is generally shorter in the north. Syringa
oblata and Cercis chinensis are widely distributed in
China, and they bloom approximately at the same time.
Although the sensitive periods for the two species differ
somewhat, their durations are usually similar (Figure 5).
For each species, flowering dates were significantly
related to the average temperature of the specific period
prior to flowering (Figures 7-10). The degree of sensitivity
of Syringa oblatas flowering to temperature ranged from
2.7 to 4.9 days/oC in the eastern low plain, including
Harbin, Shenyang, Beijing, Xian, and Taian (Figure 7).
Figure 4. Variations in standard deviations for Cercis chinensis,
Albizzia julibrissin, Syringa oblata and Robinia pseudoacacia
with latitude.
Figure 5. Periods of s ignificant
temperature influence on flowering
date at different sites for the four
woody plant s pecies. Points indi -
cate average flowering dates.
flowering dates. It was assumed that the temperature
period that influenced flowering the most corresponded to
the highest correlation coefficient. The significant periods
of temperature influence were illustrated in Figures 5 and
6. The period when temperature had a significant influence
on the flowering time was mainly from 30 to 50 days in
northern China and 50 to 80 days in the south (Figure 5),
where the growing season is longer (Figure 6), especially
in the Yunnan-Guizhou Plateau (Kunming and Guiyang).
The time when temperature could affect the date of
flowering started later and ended sooner; therefore, the
Figure 6. L en gt h of g row in g s ea s o n at t h e di ffe r en t
obs ervational s ites. The vertical axis is day of year; the bar
repres ents growing length from 0o C in winter to the day of
flowering, and
is the length of the bar, i.e. the growing length.
pg_0006
158
Botanical Studies, Vol. 47, 2006
The rate of advance of Cercis chinensis was from 2.7 to
5.9 days/oC in the low plain and from 7.1 to 14.8 days/oC
in the plateau (Kunming and Guiyang) (Figure 8). The rate
of Robinia pseudoacacia was from 2.5 to 6.5 days/oC in
the low plain and 4.7-12.4 days/oC in the plateau (Figure
9). For Hungary, Walkovszky (1998) reported that a rise
in the average spring temperature from March 15 to May
15
by 1oC caused the flowering of Robinia pseudoacacia
to advance by 6.8 days. This rate is higher than that of the
low plain and lower than on the plateau in China. The rate
of Albizzia julibrissin was from 2.4 to 6.0 days/oC and
13.1 days/oC in the low plain and the plateau, respectively
(Figure 10). Flowering dates for Cercis chinensis varied
from 30 to 50 days with a temperature variation of 2-6oC,
in Kunming and Guiyang in the Yunnan-Guiyang Planteau
while it was 15-25 days, with temperature variation of
3-5oC, in the low plain (Figure 8). Robinia pseudoacacia
(Figure 9) and Albizzia julibrissin (Figure 10) yielded
similar results. The sensitivity of flowering to temperature
is thus higher in the south than in the north.
DISCUSSION AND CONCLUSION
Plant development is determined by both temperature
and day length on the basis of sensitivity to thermal
conditions and photoperiod (Thomas and Vince-Prue,
1997). The change in flowering dates of the species with
latitude may be partially attributable to the effect of
day length. In a monsoonal climate, temperature is the
dominant factor controlling the timing of phenological
events in the spring (Zhang, 1995). Using the phenological
data of Europe for the 1951-1996 periods, Menzel (2000)
reported that spring events, such as leaf unfolding, have
advanced, on average, by 6.3 days while autumn events,
such as leaf coloring, have been delayed, on average, by
4.5 days. Thus, the average annual growing season has
lengthened, on average, by 10.8 days. Chmielewski and
Rotzer (2001) reported that a nearly Europe-wide warming
in the early spring over the last 30 years (1969-1998)
led to an earlier beginning of the growing season by 8
days. They found good correlations between the average
temperature of February to April (about 90 days) and the
beginning of the growing season in European regions.
In this study, we found significant correlations within
regions between flowering and average temperature over
the period of 60-90 days prior to flowering for Robinia
pseudoacacia in the south and 30-40 days in the north.
However, there were some differences in varieties of each
species among the different regions. Genetic differences
Figu re 7. Relationship between flowering date and average
temperature in significantly sensitive periods (indicated in Fig-
ure 5) at different sites for Syringa oblata during 1963-1988 (
**
and
*
stand for significance levels of 0.01 and 0.05, respective-
ly).
Figu re 8. Relationship between flowering date and average
temperature in significantly sensitive periods (indicated in Fig-
ure 5) at different sites for Cercis chinensis during 1963-1988
(
**
and
*
stand for significance levels of 0.01 and 0.05, respec-
tively).
pg_0007
LU et al. X Temperature effect on flowering dates in China
159
among varieties probably generated differences in the
flowering response to temperature increase (Rotzer and
Chmielewski, 2001). Day length, rainfall, and sunshine
hours may also have influenced flowering and need to be
considered in future analysis (Zhang, 1995).
Flowering dates fluctuate from year to year as
a consequence of multiple interactions between
physiological processes and physical constraints imposed
by the environment. Temperature is an important factor
influencing phenophases under the monsoonal climate in
China (Zhang, 1995), as well as in most parts of the world
where soil water is not a dominant factor in growth, e.g.
Europe and North America. The growth of plants
may
be stimulated when the temperature is higher than 0XC
in the spring, and sap flow can be observed in the stem
(Wan and Liu, 1979). Therefore, the significant period of
temperature influence increases from north to south due to
longer growing seasons in the south, in both low plain and
plateau. The results of this study show that temperature
influences flowering 30 to 80 days prior, depending on
the species and region. The temperature over shorter or
longer periods, such as 10 or 90 days, was less related to
flowering time, probably because shorter periods do not
represent climatic characteristics well in a growth stage,
and longer time scales smooth out climate fluctuations.
The geographical elementsXaltitude, latitude, and
longitudeXmay influence distribution of temperature,
rainfall as well as day length, so that further multiple
regression analysis should be applied to determine their
influence on flowering. The work of Zheng et al. (2002)
indicated phenophases change most significantly with
latitude in the range of eastern China. The present work
focuses on the periods when temperature might have a
significant influence on plant flowering.
It can be concluded that (1) interannual variation of
flowering dates increases from north to south, and (2)
sensitive period of flowering dates to temperature is
longer in the south than in the north. The advance rate of
flowering dates in response to temperature increase ranges
from 2-7 days/oC in the low plain to 5-15 days/oC on the
plateau. Due to low daily temperature during growing
seasons on the plateau, the advance of flowering dates is
more sensitive to temperature increase than that in the low
plain.
Figure 9. Relationship between flowering date and average
temperature in s ignificantly sensitive periods (indicated in
Figure 5) at different s ites for Robinia pseudoacacia during
1963-1988 (
**
and
*
stand for significance levels of 0.01 and 0.05,
respectively).
Figure 10. Relationship between flowering date and average
temperature in s ignificantly sensitive periods (indicated in
F igure 5) at different site s for Al bizz ia juli br is si n duri ng
1963-1988 (** and * stand for significance levels of 0.01 and
0.05, respectively).
pg_0008
160
Botanical Studies, Vol. 47, 2006
Acknowledgements. The authors dedicate this paper
to the memory of Professor Kezhen Zhu (1890-1974),
formerly the vice president of the Chinese Academy
of Sciences, for his leadership and organization of the
phenological network in China. The observers of the
Institute of Geography, now the IGSNRR, Chinese
Academy of Sciences, are gratefully acknowledged. We
thank Professor Tian-Duo Wang at the Shanghai Institute
of Plant Physiology and Ecology and Drs. T. Green and
G. N. Flerchinger at USDA-ARS for their review of
the manuscript before submission. The two anonymous
reviewers are gratefully acknowledged for their valuable
suggestions and comments.
LITERATURE CITED
Ahas, R. 1999. Long-term phyto-, ornitho- and ichthyopheno-
logical time-series analyses in Estonia. Int. J. Biometeorol.
44: 119-123.
Ahas, R., A. Aasa, A. Menzel, V.G. Fedotova, and H. Scheifin-
ger. 2002. Changes in European spring phenology. Int. J.
Climatol. 22: 1727-1738.
Beaubien, E.G. and H.J. Freeland. 2000. Spring phenology
trends in Alberta, Canada: links to ocean temperature. Int. J.
Biometeorol. 44: 53-59.
Chmielewski, F.M. and T. Rotzer. 2001. Response of tree phe-
nology to climate change across Europe. Agri. For. Meteo-
rol. 108(2): 101-112.
Defila, C. and B. Clot. 2001. Phytophenological trends in Swit-
zerland. Int. J. Biometeorol. 45: 203-207.
Domros, M. and G. Peng. 1988. The Climate of China. Springer-
Verlag, New York, 361 pp.
Fitter, A.H., R.S.R. Fitter, I.T.B. Harris, and M.H. Williamson.
1995. Relationships between first flowering date and tem -
perature in the flora of a locality in central England, Funct.
Ecology 9: 55-60.
Institute of Geography, Chines e Academy of Sciences . 1989.
Annual Report of Animal and Plant Phenology in China.
(serial reports with number from 1-11, 1963-1988, Science
Press, Beijing.)
Kramer, K., I. Leinonen, and D. Loustau. 2000. The importance
of phenology for the evaluation of impact of climate change
on growth of boreal, temperate and Mediterranean forests
ecosystems: an overview. Int. J. Biometeorol. 44: 67-75.
Lu, P.L., Q. Yu, J.D. Liu, and X.H. Lee. 2006. Advance of tree-
flowering dates in response to urban climate change. Agric.
For. Meteorol. (in press).
Menzel, A. and P. F abian. 1999. Growing season extended in
Europe. Nature 397: 659.
Menzel, A. 2000. Trends in phenological phases in Europe be-
tween 1951 and 1996. Int. J. Biometeorol. 44: 76-81.
Parmesan, C. and G. Yohe. 2003. A globally coherent fingerprint
of climate change impacts across natural systems. Nature
421: 37-42.
Rotzer, T., M. Wittenzeller, H. Haeckel, and J. Nekovar. 2000.
Phenology in central Europe differences a nd trends of
spring phenophases in urban and rural areas. Int. J. Biome-
teorol. 44: 60-66.
Rotzer, T. and F.M. Chmielewski. 2001. Phenological maps of
Europe. Climate Res. 18: 49-257.
Schwartz, M.D. 1999. Advancing to full bloom: planning phe-
nological research for the 21st century. Int. J. Biometeorol.
42: 113-118.
Schwartz, M.D. 2003. Phenology: An Integrative Environmental
Science. Kluwer Academic Publishers, Dordrecht.
Sparks, T.H. and P.D. Carey. 1995. The responses of species
to climate over two centuries: an analysis of the Marsham
phenological record, 1736-1947. Ecology 83: 321-329.
Sparks, T.H., P.D. Carey, and J . Combes. 1997. F irst leafing
dates of trees in Surrey between 1947 and 1996. Lond. Nat.
76: 15-20.
Sparks, T.H., E.P. Jeffree, and C.E. Jeffree. 2000. An examina-
tion of the relationship between flowering times and tem -
perature at the national scale using long-term phenological
records from the UK. Int. J. Biometeorol. 44: 82-87.
Sparks, T.H. and A. Menzel. 2002. Observed changes in seasons:
an overview. Int. J. Climatol. 22: 1715-1725.
Thomas, B. and D. Vince-Prue. 1997. Photoperiodism in Plants.
Academic Press. San Diego, pp. 22-34.
Van Vliet, A.J.H., A. Overeem, R.S. De Groot, A.F.G. Jacobs,
and F.T.M. Spieksma. 2002. The influence of temperature
and climate change on the timing of pollen release in the
Netherlands. Int. J. Climatol. 22: 1757-1768.
Walkovszky, A. 1998. Changes in phenology of the locust tree
Robinia pseudoacacia in Hungary. Int. J. Biometeorol. 41:
155-160.
Walther, G.R., C.A. Burga, and P.J. Edwards. 2001. Fingerprints
of Climate Change-Adapted Behaviour and Shifting Spe-
cies Ranges. New York and London, Kluwer Academic/Ple-
num Publishers.
Walther, G.R., E. Post, P. Convey, A. Menzel, C. Parmesan,
T.J.C. Beebee, J.M. Fromentin, O. Hoegh-Guldberg, and
F. Bairlein. 2002. Ecological responses to recent climate
change. Nature 416: 389-395.
Wan, M.W. and X.Z. Liu. 1979. Method of Phenology Observa-
tion of China. Science Press, Beijing, pp. 1-22 [in Chinese].
Xu, Y.Q., P.L. Lu, and Q. Yu. 2005. Response of tree phenology
to climate change for recent 50 years in Beijing. Geographi-
cal Res. 24: 412-420 [in Chinese with English abstract].
Zhang, F.C. 1995. Effects of global warming on plant pheno-
logical events in China. Acta Geographica Sin. 50: 403-408
[in Chinese with English abstract].
Zheng, J.Y., Q.S. Ge, and Z.X. Hao. 2002. Impacts of climate
warming on plant phenophases in China for the las t 40
years. Chinese Science Bulletin. 47: 1826-1831.
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LU et al. X Temperature effect on flowering dates in China
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